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Avian Histopathology
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 Avian
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Histopathology
4 th Edition

Tahseen Abdul-Aziz
Oscar J. Fletcher
H. John Barnes

With contributions from

H. L. Shivaprasad
David E. Swayne

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The American Association of Avian Pathologists

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Copyright © 2016 by
American Association of Avian Pathologists, Inc.

All Rights Reserved

Prin ted by Omnipress

Madison, WI 53704

Libra1y of Congress Catalog Number 2016932938

International Standard Book Number 978-0-9789 163 -6-7

Copies availab le from

American Association of Avian Pathologists

AAAP, Inc
12627 San Jose Blvd., Su ite 202
Jacksonville, Florida 32223-8638
AAAP@ aaap.info
 PREFACE

This is the 4th edition of Avian Histopathology. Avian pathology is considered a distinct discipline within the field of veterinary pathol-
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ogy as birds have organs not found in mammals, or lack organs that are found in mammals. Many avian organs and tissues have distinct
cellular composition and histological architecture. Normal histology can vary with the species of bird and state of physiologic development
and fimction . The response of avian tissues to injuries, as well as the dynamics and progression oflesions, while having some similarities, can
be fundamentally different from those in mammals. Of course, birds have their own infectious and non-infectious diseases. Thus, training in
avian histopathology is necessary for optimal evaluation of the microscopic appearance of avian organs and tissues. Histopathologic changes
often can be correlated with gross lesions and clinical signs that may help in understanding the pathogenesis of a disease. We hope that Avian
Histopathology will continue to serve the needs of veterinary pathologists and diagnosticians as an aid for recogni zing and interpreting his-
topathological changes in organs and tissues of birds.
Several chapters in this edition have been revised by incorporating new information and adding new images. As in previous editions,
the book maintains the organization of chapters by organ systems, which provides a systemic approach to avian histopathology. Lesions
associated with specific diseases and conditions in different organs and tissues are described. In each chapter, the format of grouping figures
by etiology is continued. It is worth remembering that lesion development is a dynamic process. For any disease condition, the extent and
severity of the changes in tissues vary from case to case, or even among areas within the same organ. The authors have attempted to use
images that show typical lesions and key histomorphological features of avian diseases. The images, with few exceptions, are from the col-
lections of the authors. Material received from others is acknowledged in the figure legends.
Books are not perfect, and no one should expect them to be. Attempting to write a comprehensive book without missing any errors is
probably impossible and unrealistic, but it is worth the effort. Our goal is to make thi s book an informative and valuable source of informa-
tion for veterinary pathologists and diagnosticians involved with avian cases . We would welcome feedback from those who use the book.
We are grateful to the Board of Directors of the American Association of Av ian Pathologists (AAAP) for allowing us to write the 4th
edition. It is a pleasure and honor to serve the AAAP with a task like this . Our sincere thanks go Drs. H. L. Shivaprasad and David E. Swayne
for their contributions to their respective chapters.

Tahseen Abdul-Aziz
Oscar J. Fletcher
H. John Barnes

Avian Histopathology (4 th Edition) f iii

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AUTHORS

Tahseen Abdul-Aziz
Veterinary Pathologist (Avian)
Rollins Animal Disease Diagnostic Laboratory
North Carolina Department of Agriculture and Consumer Services
Raleigh, North Carolina
USA

H. John Barnes
Professor
Department of Population Health and Pathobiology
College of Veterinary Medicine
North Carolina State University
Raleigh, North Carolina
USA

Oscar J. Fletcher
Professor
Department of Population Health and Pathobiology
College of Veterinary Medicine
North Carolina State University
Raleigh, North Carolina
USA

H. L. Shivaprasad
Professor
California Animal Health and Food Safety Laboratory, Tulare Branch
School of Veterinary Medicine
University of California- Davis
Tulare, California
USA

David E. Swayne
Laboratory Director
South East Poultry Research Laborato1y
Agricultural Research Service
U.S. Department of Agriculture
Athens, Georgia
USA

iv I American Association of Avian Pathologists

 TABLE OF CONTENTS

Chapter 1 . . . . . . . . . . . . . . . . . . . 1
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Hemic System
H. John Barnes, Oscar J. Fletcher

Chapter 2 . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
Lymphoid System
Tahseen Abdul-Aziz, Oscar J. Fletcher

Chapter 3 . . . . . . . . . . . . . . . . . . . . 73
Skeletal System
Oscar J. Fletche1; H. John Barnes, Tahseen Abdul-Aziz

Chapter 4 . . . . . . . . . . . . . . . . . . . . . 107
Muscular System
H. John Barnes, Tahseen Abdul-Aziz, Oscar J. Fletcher

Chapter 5 . . . . . . . . . . . . . . . . . . . . . . 143
Cardiovascular System
Tahseen Abdul-Aziz, Oscar J. Fletcher

Chapter 6 ... .. . .. .. . . . . 195

Respiratory System
Oscar J. Fletche1; Tahseen Abdul-Aziz

Chapter 7 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271
Alimentary System
Oscar J. Fletche,; Tahseen Abdul-Aziz

Chapter 8 . . . . . . . . . . . . . 355
Hepatobiliary System
Tahseen Abdul-Aziz, Oscar J. Fletcher

Chapter 9 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
Urinary System
Tahseen Abdul-Aziz, Oscar J. Fletcher

Chapter 10 . . . . . . . . 469
Nervous System
David E. Swayne, H. John Barnes, Tahseen Abdul-Aziz, Oscar J. Fletcher

Chapter 11 . . . . . . 521
Eye and Ear
H. L. Shivaprasad

Chapter 12 . . . . . . . . . . . . . . . . 545
Endocrine System
Tahseen Abdul-Aziz, Oscar J. Fletcher

Chapter 13 . . . . . . . . . . . . . . . . . . . 581
Reproductive System
H. John Barnes, Oscar Fletche1; Tahseen Abdul-Aziz

Chapter 14 . . . . . . . . . 615
Integumentary System
H. L. Shivaprasad, H. John Barnes

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 641

Avian Histopathology ( 4 111 Edition) Iv

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CHAPTER
Hemic System
H. John Barnes • Oscar J. Fletcher
Introduction
Cells and tissues that arise from pluripotent hematopoietic stem
cells including bone marrow, extramedullaiy hematopoietic foci,
osteoclasts, osteoblasts, macrophages, lymphoreticular tissues, and
blood comprise the hemic system. Lymphoreticular tissues are cov-
ered separately (see Chapter 2). Information on the pathology of
bemic tissues is sparse compared to information on hematology. In
general, hematology reflects the status of hemic tissues and only
wi ll be discussed in the context of pathologic changes in the hemic
sys tem.
Hematopoiesis
Differentiation and maturation of blood cells occurs continuously
throughout the life of the bird and follows precise, highly controlled
pathways regulated primarily by cytokines that act to either inhibit
or accelerate the process. Hematopoiesis is intimately associated
with bone and supporting mesenchymal tissues, which differentiate
from pluripotential mesenchymal stem cells and participate in the
control of blood cell differentiation. Type of cell, percentage of the
cell population, and point in the maturation pathway when cells are
affected, determine the impact of a disease process on blood and
hemic tissues, e.g., chicken anemia virus, which affects hematopoi-
etic stem cells (hemocytoblasts), causes not only anemia, but also
pancytopenia and lymphoid atrophy.
Hematopoiesis normally occurs within the marrow cavities
of skeletal bones and non-skeletal osseous tissues such as tracheal
rings, ossified tendons, ectopic bone that develops within the lungs,
or areas of osseous metaplasia. Distribution of bone marrow in
birds is restricted by air sacs that invade marrow bones and con-
vert them to pneumatic bones . In laying birds, occurrence of bone
marrow coincides with medullary bone . Medullary bone develops
within the marrow cavity but does not eliminate the bone marrow.
Bone marrow of young birds is typically more cellular than that of
older birds. In young birds, there should be abundant hematopoietic
cells that fill the marrow cavity and approximately equal amounts
of myelopoiesis and erythropoiesis. Age related conversion of red
marrow to fatty marrow is a normal process, but the precise time
sequence in birds has not been determined. In the mid-shaft of the
femur of chickens, this conversion stat1s at around 40 days of ag~.
Disease is another cause of red marrow depletion. In these birds,
small islands of active hematopoietic cells are usually found along
cortical bone and metaphyseal areas while the center of the marrow
cavity is filled with fat cells. In starvation, lipid is depleted in fat
I
1
cells and the reticular stroma produces a mucoid substance (serous
atrophy of fat, gelatinous transformation). Marrow depletion result-
ing naturally because of aging or from disease varies among dif-
ferent hematopoietic sites. When assessing bone marrow activity,
it is useful to examine multiple sites. Red marrow sites need to be
examined for evidence of hypoplasia or aplasia, while hyperplasia
is best determined by examination of fatty marrow sites (e.g. , mid-
shaft femur). Bone marrow in the ulna is considered the best site for
determining starvation.
In birds, hematopoiesis within the marrow is compat1mental-
ized; erytlu·opoiesis occurs within medullaty sinuses whereas gran-
ulopoiesis occurs in extravascular spaces between sinusoids. The
amount of etytlu·opoiesis and granulopoiesis are approximately
equal in normal bone marrow. Medullary sinuses are composed of
reticulin cells that lack a basement membrane. Hemocytoblasts in
close contact or adhering to the internal surface of the sinus wall
give rise to a gradient of maturing etytll.l'ocytes that can be followed
to mature e1ythrocytes in the center of the sinuses. Erythropoiesis
in birds is not as easy to evaluate as it is in mammals because of the
normal nucleated red cells in birds. Sinuses anastomose and eventu-
ally drain into the large central vein allowing etythrocytes to enter
the general circulation. In regenerative anemias, immature as well as
mature cells leave the sinuses. Birds do not have megakatyocytes;
tlu·ombocytes arise from stem cells in the same way as erytlu·ocytes.
Granulocytes (heterophils, eosinophils, basophils) develop in the
extravascular spaces from hemocytoblasts in contact with the ex-
ternal sinusoidal membrane. Microscopically, hemocytoblasts that
produce granulocytes are indistinguishable from those that produce
erythrocytes and thrombocytes. Granulocytes eventually enter si-
nuses through gaps in the sinus wall where final maturation occurs.
Variable amounts of fat and lymphoid aggregates or nodules
are also located within the extra-sinusoidal spaces. Lymphoid tissue
within marrow generally increases with age due to repeated anti-
genic stimulation and may be focal or diffuse. It is often admixed
with myeloid cells.
Hematopoiesis in soft tissues outside of the bone marrow is re-
ferred to as extramedullaty (ectopic) hematopoiesis (hemopoiesis).
Extramedullary hematopoiesis may occur in any tissue, but is most
frequent in tissues where hematopoiesis occurred in the embryo
including liver, intestine, spleen, kidney, thymus, gonads, heart,
nerves, Meckel 's diverticulum, and bursa ofFabricius. Extramedul-
lary hematopoiesis frequently occurs in hepatic portal areas where
it may be mixed with lymphocytes . Often hematopoietic foci are
Avian Histopathology (4 11, Edition) I 1
 H. John Barnes • Oscar J, Fletcher
I associated with vessels; it is normal for them to extend tlu-ough the
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vessel wall. The amount of extramedullary hematopoiesis varies
with the age and species of bird and is increased in diseases that af-
fect bone marrow or blood. Enlarged, mottled livers of condemned
chickens often have marked hematopoiesis in portal areas, which
can be confused with cholangitis. Extramedullary hematopoiesis
needs to be distinguished from inflanmrntory lesions and leukoses
involving hematopoietic cells, e.g. , myeloid leukosis. Hematopoi-
etic foci consist of mixed cells in varying proportions representing
different maturational stages of e1ythrocytic and granulocytic cells .
Occasionally only granulopoiesis is seen. Mitotic figures are usu-
ally present, but are not numerous, and surrounding tissues are nor-
mal, except for vacuolated hepatocytes that are occasionally seen
when foci occur in the liver. ln some birds, hematopoietic and fat
tissue form myelolipomatous foci , which may be numerous in the
liver. Granulocyte foci in the intestinal wall of neonatal chicks may
provide innate immunity during the first week of life.
Hemic Cells
In contrast to mammals, all avian blood cells, including erythrocytes
and tlu·ombocytes, are nucleated. Presence of nucleated erytlu·o-
cytes in an unknown tissue indicates the tissue is not mammalian,
but the tissue could have originated from a bird, reptile, amphibian,
or fish as they all have nucleated erythrocytes. Nucleated erythro-
cytes in avian tissues make them appear more cellular, which con-
trasts sharply with sections of similar tissues from mammals.
E1J1t/1 rocytes
Avian erythrocytes are flattened , ellipsoidal cells with bright, red-
orange, eosinophilic cytoplasm and deeply stained basophilic oval
nuclei that are located centrally in the cell. They normally are intra-
vascular and are readily identified in tissue sections.
Autolysis or exposure to hemolytic toxins such as those pro-
duced by C/ostridi11111 spp. causes the cytoplasm of e1ythrocytes to
lyse leaving " ghost cells" or only the intensely stained nuclei. The
latter can be confused with small lymphocytes or thrombocytes.
The relatively large, uniform, dark oval nuclei without cytoplasmic
staining that are usually within vessels helps to identify the cells as
lysed erythrocytes.
Only very inunature erythroid cells are identifiable in tissue
sections. They are larger and more round than mature erythrocytes,
and have basophilic cytoplasm that lacks granules. The nucleus of
immature erythroid cells remains centrally located but is rounder,
becomes less condensed with an identifiable chromatin pattern, and
is typically surrounded by a narrow pale zone in the cytoplasm.
Nucleoli may be seen in erythroblasts. Immature lymphocytes have
less cytoplasm that is pale staining, which helps to distinguish the
two cell types. There are no granules in the cytoplasm of eryth-
roblasts, which is useful in differentiating them from myeloblasts.
However, in some cases, cytoplasmic granules may be difficult to
identify in myeloblasts making it necessary to rely on other morpho-
logic features to distinguish the two cell types. Immature erythroid
cells are intravascular and are uncommon in tissues other than bone
marrow, although they may rarely be found in the sinusoids of the
liver and spleen when erythropoiesis is intense.
2 I American Association of Avian Pathologists
Thrombocytes
Avian thrombocytes function similarly to mammalian platelets.
Their aggregation provides an important physical occlusion to re-
duce hemorrhage from damaged vessels, however, they produce
little thromboplastin and play only a minor role in initiating blood
clotting. Granules contain 5-hydroxytryptamine (serotonin), which
is an early inflammatory mediator. Thrombocytes rapidly clear par-
ticulates in the blood and are considered the primary phagocyte in
the circulation. Morphologically, avian tlu·ombocytes are similar to
erythrocytes but are smaller, have clear cytoplasm, are less elongat-
ed, and have a rounded nucleus. Their cytoplasm stains positively
with periodic acid-Schiff because of its high carbohydrate content.
They rapidly degenerate and lose their oval shape in blood smears
and tissue sections. Thrombocytes are difficult to recognize in tis-
sues unless there is intravascular aggregation from vascular dam-
age. Intravascular clumping of thrombocytes is increased by par-
ticulates in the circulation. Aggregated thrombocytes do not fuse to
form giant cells. Tlu-ombocyte aggregates are most often observed
in the small and intermediate vessels of the lungs. In tissue sections,
their location within intravascular aggregates and small size help
distinguish thrombocytes from nuclei of lysed erytlu·ocytes or small
lymphocytes.
Gmnu/ar leukocytes - heterophils, eosinophils, basophils,
and mast cells
Like mammals, birds have 3 granular leukocytes - heterophils, eo-
sinophils, and basophils - in the circulatory system and mast cells
in tissues. Each avian granulocyte contains more than one type of
granule and there are differences among avian species. Both hetero-
phils and eosinophils have eosinophilic cytoplasmic granules that
are often difficult to distinguish in tissues by conventional stains.
Following prolonged storage in aqueous fixatives, heterophil gran-
ules can degrade and lose their characteristic spindle shape. After
heterophils die, which can occur both ante- or post-mortem, het-
erophil granules become spherical as they degenerate. In addition,
immature heterophils have spherical granules and in some avian
species (e.g., waterfowl), heterophil granules are normally round.
In most tissue sections, heterophil granules generally are spherical
making it difficult to distinguish heterophils from eosinophils. Spe-
cial staining for phospholipids with Sudan black B or peroxidase
can be used to differentiate the two cell types - heterophils are nega-
tive for both stains while eosinophils are positive. In descriptions
of tissue changes, heterophils and eosinophils are often grouped to-
gether and collectively referred to as granulocytes, unless the defin-
ing granules of each cell type can be definitively identified.
Heterophils are the most abundant avian granular leukocytes.
Those of the chicken and turkey are round with a lobulated nucleus,
have numerous, spindle- or rod-shaped, eosinophilic, cytoplasmic
granules, and pale staining cytoplasm. In well-preserved tissues,
mature heterophils in areas of acute inflammation can usually be
identified. Granules often are seen extracellularly where heterophils
are numerous. It is common to find heterophils marginated in pul-
monary vessels, especially venules, of normal lungs. Perhaps this
represents a pool of cells that can be rapidly mobilized. In addition
to being increased in response to acute inflammation, heterophils

also are increased during mild to moderate stress, but decreased if
stress is extreme. The ratio of heterophils to lymphocytes (H/L ra-
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tio) in blood of stressed birds increases (heterophils increase, lym-
phocytes decrease) making it a good method for assessing the onset,
duration, and intensity of stress responses in birds .
Heterophils are functionally equivalent to mammalian neutro-
phils and are the primary cells involved in early acute inflammation.
Although they lack myeloperoxidase, catalase, and alkaline phos-
phatase found in manunalian neutrophils (see Harmon, 1998), avian
heterophils are highly efficient at phagocytosis and bacterial killing
by non-oxidative processes. Oxidative burst, degranulation, and up
regulation of pro-inflammatory cytokine production by heterophils
results from stimulation of Toll-like receptors on the cell surface.
Heterophils contain several cationic P-defensins that are capable of
killing a variety of bacteria both intra-and extracellularly. Differenc-
es in enzyme content also are believed to account for the caseation
of heterophilic exudate that occurs in birds compared to liquefaction
and formation of purulent exudate in mammals. Activated hetero-
phils have increased functional capabilities (adherence, chemotaxis,
phagocytosis, and bacterial killing) compared to non-stimulated het-
erophils. Heterophils show intense chemoattraction to endotoxin
and are the principal cell that responds to Gram-negative bacterial
infections. Evidence indicates that heterophils also may be the main
effector cells in both antibody dependent and natural cytotoxicity.
Morphologic changes in heterophils in response to severe stress
include increased tabulation and fragmentation. Toxic heterophils
characterized by swelling, condensed nucleus, loss of eosinophilic
staining and granules, and vacuolation are seen in blood films from
birds with inflanunatory lesions. In tissues, these changes appear as
degeneration and necrosis of the cells. Eventually heterophils un-
dergo caseous necrosis that results in a mass of inspissated exudate.
Macrophages progressively increase on the surface of the exudate
and fuse to form multi-nucleated giant cells that form a complete
layer covering the central caseated mass. Microscopically, this ap-
pears as a palisade of giant cells and macrophages surrounding an
area of caseated exudate.
Eosinophils of chickens and turkeys appear similar to hetero-
phils, but have densely packed, round , eosinophilic, cytoplasmic
granules, and pale basophilic cytoplasm. The latter may not be
seen because of numerous granules filling the cytoplasm. As noted
above, it is often difficult to distinguish heterophils and eosinophils
from each other in routine stained histologic sections. Experimental
eosinophilia in birds is difficult to produce and there are few repo11s
of naturally occurring eosinophilia. Unless confirmed by special
stains, most reports of significant numbers of eosinophils in avian
lesions are debatable.
Eosinophils are suspected of being involved in the response of
the bird to parasitism and allergies, but confirmation that the cells
are actually eosinophils has been done in only a limited number of
studies. Eosinophils have been shown to be involved in the early
stages of acute inftanunation induced by certain experimental sub-
stances, suggesting they play a modulating role in delayed-type
hypersensitivity reactions. Cells morphologically consistent with
eosinophils frequently are found in the deep lamina propria of the
intestine, but their identity has not been confirmed.
Hemic System
Avian basophils are round cells with an oval nucleus that have
many intensely basophilic, spherical, cytoplasmic granules that con-
I
tain histamine. They appear early in the inflammatory response,
and, like eosinophils, are thought to play a role in modulating the
early events in the inflammatory process. Endotoxin is strongly
chemotactic for basophils. Basophilia with degranulation of cells
often occurs in response to stressful situations. While basophils are
readily identified in blood films , they are not easily recogni zed in
conventionally stained histologic sections.
Mast cells contain several inflammatory mediators, of which
histamine has been best studied, that are released from their cyto-
plasmic granules following stimulation. They are important effector
cells in inflammation, immediate but not delayed hypersensitivity,
anaphylaxis, and play a significant role in intestinal immunity, e.g. ,
coccidiosis. The relationship between basophils in the circulation
and mast cells in tissues remains uncertain, but current evidence
suggests they arise from different cell lineages. Staining methods
can differentiate basophils and mast cells, as well as two types of
mast cells - mucosa! and connective tissue mast cells. Mast cells
are widely distributed in birds. They can be found in tissues of
the alimenta1y tract, lung, ovaiy, oviduct, lymphoid organs, thyroid
glands, peritoneum, brain, nerves, eye, and skin. Distribution and
number of mast cells varies within and among avian species. Typi-
cally they are located in perivascular connective tissue and are espe-
cially numerous in the lamina propria of the digestive and reproduc-
tive tracts. Mast cells respond to parasitic infections in the intestinal
tract and are significantly increased in the duodenum of turkeys that
develop intestinal lesions following infection with hemorrhagic en-
teritis virus. Mast cells in the brain produce gonadotropic hormones
and function in reproduction . Birds with muscular dystrophy have
decreased mast cells in the thymus. Special stains (Giemsa, Tolu-
idine blue, Alcian blue/safranine, Acid-fast) are necessaty to iden-
tify mast cells in tissues; fixation in alcoholic formalin or Carnoy's
fix ative improves preservation of the granules.
No11gra1111lar leukocytes - lymphocytes and 111011ocytes
Nongranular leukocytes in birds - lymphocytes and monocytes
- are similar to those in mammals. Lymphocytes are classified
morphologically as small , medium, or large. Small and medium
lymphocytes are considered most important; large lymphocytes are
considered immature cells. Functionally, lymphocytes are divided
into those cells that differentiate in the thymus (T-cells) and those
that differentiate in the bursa ofFabricius (B-cells). T-cells possess
specific surface antigens (CD3, CD4, CDS) and proliferate follow-
ing exposure to ce11ain lectins (phytohemagglutinin and concana-
valin A), which is referred to as a mitogenic response. Natural killer
cells are small lymphocytes (5-6 µm) with a low cytoplasm:nucleus
ratio and many surface projections. They are CDS+ but lack both
8- and T-cell markers. 8-cells can be identified by the presence of
markers including Fe receptors and surface immunoglobulins.
Lymphocytes within inflammatory lesions are considered to be
responding to antigens or abnormal cells. Responses of these cells
are closely regulated and interwoven with those of the monocyte-de-
rived macrophages through chemicals (cytokines) elaborated by the
cell types; lymphokines produced by lymphocytes and monokines
Avian Histopathology (4 th Edition) I 3
 H. Jolin Barnes • Oscar J. Fletclier
I produced by macrophages. Organized lymphoid nodules mature
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into germina l centers that contain large B-lymphocytes centrally.
Smaller T-cells form a more diffuse infiltrate around the periphery
of the B-cells and within interstitial tissues. Natural killer cells are
important in intestinal mucosa( immunity and destruction of tumor
cells. Under appropriate stimulation, B-lymphocytes differentiate
into plasma cells, which can be identified in tissue sections by their
eccentrically located nucleus, often with a roughly radially arranged
clu·omatin pattern ; thin, pale perinuclear area of cytoplasm; and rich,
basophilic staining of the remaining cytoplasm. Single or multiple
accumulations of globulin may occur in the cytoplasm of plasma
cells that are actively producing antibody. They appear as hyaline,
eosinophilic globules and are termed Russell bodies . Cells contain-
ing Russell bodies are referred to as Mott cells. Lymphocytic or
lymphoplasmacytic inflammation occurs most frequently in viral
infections and tumor diseases.
Monocytes are larger than lymphocytes with more cytoplasm
that is less basophilic and often contains vacuoles. They have an
elongated, indented nucleus surrounding a pale area of cytoplasm
known as the "Hof', which contains well-developed Golgi com-
plexes. Monocytes and large lymphocytes appear similar, especial-
ly in tissues. Extravascular monocytes become activated and morph
into tissue macrophages, which exhibit chemotaxis, are phagocytic,
and participate in antigen processing and immune regulation. Mac-
rophages can develop an epithelioid appearance and fuse to form
multinucleated giant cells. When differentiating into epithelioid
cells they Jose IgG receptors, which may be related to an inabil-
ity to remove necrotic material resulting in the persistent caseous
exudate that characterizes chicken heterophilic granulomas. Initial
macrophages recruited to an area of inflammation are less phago-
cytic compared to later macrophages. Bactericidal activity of mac-
rophages is less than that of heterophils.
Macrophages in tissues can be specifically identified by con-
canavalin A binding. Staining for lysozyme also is usefol for iden-
tifying macrophages, but is less specific. In turkeys, intravascular
macrophages are primarily found in liver sinusoids along with lower
numbers in the spleen and bone marrow, but are not present in the
lung. Viruses can adversely affect macrophage fonction and may
replicate in the cells causing necrosis. Similarly, endotoxin impairs
intracellular bacterial killing by pulmonary macrophages, but does
not affect oxidative burst.
Bone Marrow
Changes in bone marrow include disturbances of growth (atro-
phy, hyperplasia), pigment deposition , inflammation, and neo-
plasia . They result from direct involvement of the marrow, or as
reflections of pathologic processes in other organ systems. Bone
marrow responses are limited to either a decrease or increase in
cells or inflammation. Cellular depletion results in atrophy and is
usually caused by direct damage to marrow cells. Bone marrow
atrophy is manifested in the bird by anemia, leukopenia, throm-
bocytopenia, or pancytopenia depending on which cell type is
affected. Survival and recovery from the cause of bone marrow
atrophy results in regeneration and eventual return to a normal
cell population. Bone marrow hyperplasia occurs during recovery
4 I American Association of Avian Pathologists
from bone marrow atrophy or in response to an external stimulus
to the hemic system. For example, hypoxia stimulates erythroid
hyperplasia, which results in polycythemia, while acute inflam-
mation stimulates granulocytic hyperplasia resulting in leukocyto-
sis. Compared to mammals, bone marrow of birds is substantially
more reactive, and hyperplasia resulting from sepsis, bacterial in-
fections , or exposure to endotoxin can be so pronounced that it is
difficult to distinguish it from myeloid neoplasia. Lack of tissue
effacement or invasion, presence of cells representing all stages
of maturation, and absence of tumors in other tissues are useful
features for identifying hyperplasia. In contrast, expansive nod-
ules composed ofa monomorphic population ofmyeloid cell s, and
destruction or spread into adjacent tissues characterizes neoplas-
tic myeloid lesions. Presence of numerous mitotic figures is not
helpful in differentiating myeloid hyperplasia and neoplasia as cell
proliferation is a feature of both.
Manifestations of bone marrow changes have been associated
with a variety of diseases, but their pathogenesis and the histo-
pathologic appearance of the bone marrow have been studied in-
frequently. This is particularly true of anemia, which can easily
be determined by procedures such as hematocrits. As identification
of decreased numbers of tluombocytes and leukocytes is more dif-
ficult, involvement of other blood cells besides erytluocytes can go
unrecognized if bone marrow is not evaluated. Many "anemias",
especially those that result from either toxic or infectious agents,
are actually pancytopenias. In birds with diseases that manifest a
hematologic disorder, histopathological evaluation of the bone mar-
row should be done.
Anemia
Anemia is characterized by an abnormally low number of erythro-
cytes or hemoglobin concentration within the erythrocytes, which
results in impaired oxygen delivery to tissues. Hypoxia signals
release of e1ytluopoietin, which initiates erytlu·opoiesis. Anemia
results from either loss of erythrocytes in excess of the ability to
produce them or a failure to produce new cells to replace those lost
through attrition. If there is a bone marrow response, the anemia
is classified as regenerative, and there is increased erytluopoiesis
in the marrow and immature red cells in the circulation . If the
bone marrow is unresponsive to an increased demand for oxygen
and erytiu·ocytes, the anemia is classified as non-regenerative. In
non-regenerative anemia, bone marrow is depleted and immature
red cells are not present in the blood. If sufficient residual hema-
topoietic stem cells survive in cases of direct destruction by toxic
substances, infectious agents, or radiation, what begins as a non-
regenerative anemia will transition to a regenerative anemia, as the
erythron is re-established.
Anemia also can be classified according to the basic causative
mechanism as hemorrhagic, hemolytic, aplastic, or myelopathic
(myelophthisic). Hemorrhagic and hemolytic anemias are usually
regenerative while aplastic and myelopathic anemias are usually
non-regenerative. Aplastic anemias are generally only part ofa pan-
cytopenia in which leukocytes and thrombocytes also are decreased
in the circulation. Many causes of anemia have been described in
birds (Table I).
 Hemic System

Hemorrhagic anemia
Hemorrhagic anemia results when blood loss exceeds replacement.
the marrow, and possibly in extramedullary sites (hepatic sinusoids,
spleen), can be seen.
I
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It occurs in conditions characterized by acute or chronic blood loss.

B irds are capable of rapid recovery through intense erythropoiesis
fo llowing an episode of hemorrhage or clll'onic, sub-lethal blood
loss. Identifying the cause of hemorrhagic anemia should pres-
ent little difficulty unless blood loss has resulted from a seemingly
minor lesion. Other than hemorrhage at the site of blood loss and
possible identification of a cause, there are no specific microscopic
les ions. Normal variation in the number of red blood cells within
vesse ls obscures any overall deficit of erythrocytes . One exception
mi ght be diffu se empty capillaries in the lungs; which are normally
filled with blood. If blood loss is chronic, e1ythroid hyperplasia in
Hemolytic anemia
Hemolytic anemia results from erythrocyte destruction exceeding
the ability of the bird to replace the destroyed cells. Red cell de-
struction may occur by cell lysis within the vascular compartment
(intravascular hemolytic anemia) or extravascularly following
phagocytosis by macrophages (extravascular hemolytic anemia).
Hemoglobinuric nephrosis can result if sufficient intravascular he-
molysis occurs, but this has rarely been recognized in birds and has
not been reported from poultty. In hemoglobinuric nephrosis, bright
orange hemoglobin fills Bowman's space of glomeruli and renal tu-
bules and some tubules show acute epithelial necrosis. Splenic hy-

Table 1: Causes of Anemia in Poultry

A.Hemorrhagic Anemia h. Aegyptianellosis (Aegyptian e//a 4. Beak necrosis

I. Blood Loss p11//orn111) 5. Hypothyroidism
a. Trauma 3. Mycotic G. Myelopathic (myelophthisic) Anemia
b. Persecution (Cannibalism) a. Aspergillosis I. Lymphosarcoma
c. Servicing (beak trimming, toe 4. Parasitic 2. Myeloid leukosis
trimming) a. Hemoprotozoa (Plas111odi11111, 3. Erythroid leukosis
2. Disease Hae111oprote11s, Leucocytozoon) 4 . Osteopetrosis
a. Aortic rupture 5. Toxic 5. Spindle-Cell Proliferative Disease
b. Fatty liver syndrome a. Aflatoxin 6. Mycobacteriosis
c. Neoplasia - hemangioma, b. Lead - acute F. Pancytopenia/Aplastic Anemia
hemangiosarcoma c. Copper I. Viral J,?fections
3. Parasites d. Dimethyl disulfide- plants in the a. Chicken infectious anemia virus
a. Black flies (Si11111li11111 spp.) Brassica family b. Infectious bursal disease virus -
b. Ticks (e.g. Argas spp. , hard ticks) e. Phenylhydra zine very virulent forms
c. Mites (e.g. Der111a11yss11s, f. Methylsulfonate c. Newcastle disease virus
Ornithonyssus) g. Paraquat d. Virulent reoviruses
d. Internal helminths (e.g. h. Albendazole/Fenbendazole e. Adenoviruses (usually serogroup
A111idosto11111111, Ornithostrongylus, i. Crude oil 8)
Trichostrongylus, Capi//aria, etc .) j . Green onions f. Avian leukosis viruses-
e. Intestinal and cecal coccidiosis k. Garlic myeloblastosis virus
4 . Roden/icicles- Warfarin, C.Nutritional Anemia g. Marek's disease virus- absence of
Brodifacoum, Diphacinone 1. Minerals maternal immunity
B.Hemolytic Anemia a. Iron deficiency h. Psittacine beak & feather disease
1. Viral infections i. Ochratoxin-induced (Circovirus) (?)
a. Marek 's disease virus? ii. Myeloblastosis virus 2. Toxic
b. Myeloblastosis virus b. Copper deficiency a. Sulfonamides
c. West Nile virus 2. Vitamins b. Lead - clll'onic
2. Bacterial !,?fee/ions a. Pyridoxine- ducklings c. Methyl mercury- high exposure
a. Fowl typhoid (Sal111one//a b. Folic acid- megaloblastic anemia d. Mycotoxins
gallinamm) c. Vitamin K- bone marrow atrophy i. Trichothecene mycotoxins
b. Salmonellosis D.Inherited Anemia ii. Ochratoxin
c. Erysipelas E. Undetermined 111. Citrinin
d. Streptococcosis 1. Rapeseed meal e. Cyclophosphamide
e. Spirochetosis (Borrelia anserina) 2. Duck anemia (reticuloendotheliosis) f. Irradiation
f. Mycobacteriosis virus 3. Nutrition
g. Chlamydiosis 3. Avian leukosis viruses- certain types a. Starvation

Avian Histopathology (4 th Edition) I5

 H. John Bames • Oscar J. Fletcher
I because of a lack of erythroid stem cells, but normal numbers of oth-
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perplasia, e1ythrophagocytosis, and excess hemosiderin (hemosid-
erosis) in hepatic and splenic macrophages, hepatocytes, and, less
frequently, renal tubular epithelium, are characteristic microscopic
changes seen in extravascular hemolytic anemias . Degenerative
changes resulting from hypoxia may be seen in the liver (periacinar
degeneration and necrosis) and myo cardium if the anemia is severe.
Hemoprotozoan infections, bacterial infections, and toxins
cause hemolytic anemias in birds. Hemoprotozoa can be seen in
heavy infections or when parasites are large, e.g. , Leucocytozoon ,
but are best diagnosed from blood smears or tissue impressions
rather than histologic sections. If present, exoerythrocytic stages
of some parasites are usually easier to identify than erythrocytic
stages. Destruction ofparasitized red cells can be mediated through
antibodies or by anti-erythrocytic factors. Autoimmune hemolytic
anemia has rarely been described in birds and has not been reported
in poultry. When bacteria cause hemolytic anemia, they can gen-
erally be identified in lesions in affected tissues although special
stains may be needed. Finding bacteria in the bone marrow is useful
for identifying septicemia. Toxic causes of hemolytic anemia are
more difficult to identify, as tissue changes are often not specific.
However, Heinz body anemias have been produced experimentally
in birds with dimethyl disulfide and phenylhydrazine, acid-fast in-
tranuclear inclusion bodies in liver and kidney can occasionally be
found in cases of lead poisoning, and Mallory's stain may reveal
blue granules in sinusoidal lining cells (Kupffer cells) indicative of
copper accumulation in copper toxicity.
Myelopatltic anemia
Myelopathic (myelophthisic) anemia results from replacement of
marrow by another tissue. The cause is usually neoplasia that prolif-
erates within the bone effacing the marrow. An exception is myco-
bacteriosis in which epithelioid macrophages and giant cells packed
with acid-fast bacilli replace normal bone marrow.
Other types of anemia
Inherited and nutritional anemias are of little significance in poultry.
The former is apparently rare while nutritional anemia is unlikely
to occur in poultry fed commercially formulated rations. However,
iron-deficiency anemia can result from interference with iron up-
take and utilization by ochratoxin, and feeding 10% rapeseed meal
to adult chickens caused a regenerative macrocytic anemia, but the
mechanism responsible for the anemia was not determined.
Significant anemia without tumor formation in young chick-
ens and turkeys has been associated with infection by certain strains
of leukosis/sarcoma viruses. In most instances, the pathogenesis is
unknown. Avian leukosis viruses in subgroups B and D caused the
most severe anemia in experimentally inoculated chickens. Some
chickens that survived the initial anemia, later died from a nonre-
generative anemia following reactivation of virus infection.
Pa11cytopenia
Pancytopenia (aplastic anemia) occurs when pluripotent hematopoi-
etic stem cells are impaired or lost, which also results in leukopenia
and thrombocytopenia in addition to anemia. Pure red cell hypopla-
sia refers to conditions in which there is a nomegenerative anemia
6 I American Association of Avian Pathologists
er blood cells. Until the diseases in birds characterized by extensive
loss of bone marrow cells are better defined, it seems best that they
should be treated together and referred to as pancytopenia . Diseases
that cause pancytopenia are characterized by anemia, which is ini-
tially nonregenerative; thrombocytopenia associated with bleeding
disorders; increased susceptibility to bacterial infections related to
leukopenia, decreased macrophages, and immunosuppression; pale,
atrophied hypocellular bone marrow with increased fat content; and
lymphoid organ atrophy. Viral infections, toxicities, and starvation
are the main causes of pancytopenia in birds (Table l ). Irradiation
also causes pancytopenia, but it is of little practical significance to
the diagnostician.
Pancytopenia is recognized microscopically by marked deple-
tion of the bone marrow leaving only the reticular framework of
the sinusoids and fat cells. In the early stages, necrosis of marrow
cells characterized by pyknosis (karyopyknosis) and karyorrhexis
is seen. Inclusions typical of adenoviruses and chicken infectious
anemia virus may be seen in poultry while those of polyomavirus,
herpesvirus, and psittacine circovirus have been reported from other
avian species . Death due to sepsis is a common cause of mortality
in birds with pancytopenia. In such cases, intravascular bacteria
usually are seen in the marrow. When bone marrow depletion is
severe, it often is still possible to find single or small clusters of
ve1y large hemocytoblasts . These will serve as the source for reple-
tion of the marrow and undergo hyperplasia to regenerate the bone
marrow if the bird survives and the cause of the pancytopenia has
been eliminated. Depletion of lymphocytes from lymphoid organs
typically parallels bone marrow changes in pancytopenia .
Bone Marrow Hyperplasia
In contrast to anemia, polycythemia is an abnormal increase in the
number of red cells in the circulation that is manifested by elevated
packed cell volumes and increased hemoglobin concentrations. He-
moconcentration caused by dehydration results in a relative increase
in red cells that must be differentiated from polycythemia. Abso-
lute increases of red cells are unconunon, but occur in meat-type
chickens in response to hypoxia from altitude, insufficient cardio-
pulmonaiy capacity, pulmonary or skeletal disease, or low ambient
temperatures. Polycythemia increases blood viscosity, which pre-
disposes to pulmonaiy hypertension, right heart failure, and ascites.
Decreased deformability of red cells also contributes to pulmonary
hypertension. Bone marrow changes in polycythemia have not been
reported but e1ythroid hyperplasia would be expected. Increased
white blood cells in the circulation (leukocytosis), which occurs
frequently in many avian infectious diseases and as a response to
stress, would be expected to be associated with myeloid hyperplasia.
However, there appears to be only limited information correlating
the histopathology of the bone marrow with episodes of leukocyto-
sis. Acute viral, bacterial, and fungal infections can cause myeloid
hyperplasia. Hematopoietic stem cell proliferation and hyperplasia
accompanied leukocytosis and selective thrombocytopenia in chick-
ens experimentally infected with virulent influenza (H5N2) virus .
Non-specific myeloid hyperplasia is frequently seen in diagnostic
case material. Myeloid hyperplasia can be marked and needs to be

di stinguished from myeloid leukosis in which clonal populations of
granulocytes at a single maturation stage predominate, there is tis-
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sue destruction or invasion, and tumors are present in other tissues.
Bone Marrow Inflammation
Although bone marrow actively participates in inflammatory pro-
cesses in the body, there is little information on the local response
of bone marrow to injmy. Necrosis of bone marrow occurs in some
acute viral diseases and toxicities, but the response to the injury is
not inflammation, but regenerative hyperplasia. Particulate uptake
by bone marrow approximates that of the spleen, and bone marrow
is recognized as an excellent site for isolating systemic infectious
agents. Listeria monocytogenes causes necrosis, fibrin exudation,
and a mixed cell inflammatory response. Intralesional bacteria are
evident. A Coxiella-like organism causes focal mixed inflammato1y
cell lesions. Cytoplasmic vacuoles that displace the nucleus are a
characteristic of infection with this organism. Guinea fowl infected
with Toxoplasma gondii had multifocal necrosis, fibrin exudation,
marked erytlu-oid hyperplasia, and granulocytic hyperplasia with
intralesional protozoa in the bone marrow.
Infectious agents and viral inclusions may be found in bone
marrow macrophages when diseases are systemic . Meronts of he-
moprotozoa and Sarcocystis develop in endothelial cells of many
organs including bone marrow. In avian mycobacteriosis, granulo-
mas frequently form in bone marrow and can become so extensive
that a myelopathic anemia results. Increasing diffuse and nodular
lymphoid tissue seen in commercial birds as they age suggests bone
marrow pat1icipates in systemic responses to antigens.
Pigments
Hemosiderin can be found in bone marrow, especially in cases of
extravascular hemolytic anemia. Dark brown to black protoporphy-
rin pigment accumulates in bone marrow in addition to the liver and
spleen in birds with protoporphyria, an inherited defect in heme syn-
Table 2. Comparative Terminology for Inflammation in Birds
Mammalian Term(s) Avian Term(s)
Suppurative, Purulent Heterophilic, Granulocytic
Nongranulocytic, Lymphocytic,
Nonsuppurative, Nonpurulent
Lymphoplasmacytic, Histiocytic, etc.
Other compound words containing suppurative or purulent should be similarly modified to describe types of inflammation in avian
species, e.g. fibrinopurulent in mammals would become fibrinoheterophilic or fibrinogranulocytic in birds.
Pyogranulomatous Heterophilic Granuloma
Granulomatous Histiocytic Granuloma
Abscess Fibriscess
Hemic System
thesis. The pigment has a Maltese cross appearance when viewed
with polarized light.
I
Inflammation
Inflammation occurs in response to an irritant. The degree and type
of inflammatory response depends on the tissue that is damaged,
degree to which the irritant can damage tissue, ability of the bird
to respond, and duration and severity of the injury. Necrotic tissue
increases the degree of inflammation and persistence of a lesion;
the dead tissue serves as an additional irritant until it is removed or
can be sequestered by a granulomatous response. In general, the
inflammatory process in birds is similar to that of mammals, except
1) basophils and eosinophils are more involved in modulating the
early phases of inflammation in birds, 2) fibrinous and heterophilic
exudates undergo caseation instead of liquefaction and are slowly
removed by macrophages and giant cells, 3) the role of eosinophils
in allergic reactions and response to metazoan parasites is less well
known in birds, and 4) the stages of inflammation proceed at a rapid
rate. Stages of inflammation requiring days to weeks in mammals
occur within hours to days in birds. Similarities between inflam-
mation in mammals and birds have resulted in terminology used
for mammals being applied to birds. In some instances, (e.g. , ca-
tarrhal, serous, fibrinous, etc.) the application is appropriate, while
with other types of inflammation, use of terms more descriptive for
birds are preferred (Table 2). Liquid to semisolid purulent exudate
that is common in acute mammalian inflammation occurs rarely in
birds making use of the term purulent to describe the solid caseous
exudate in birds inaccurate. The term fibriscess is preferred for fo-
cal inflanunat01y lesions in birds and reptiles in which multiple lay-
ers of fibrin entrap inflammatory cells and causative agents, instead
of the mammalian term abscess, a lesion that forms by a wholly
different process. Inflammation in birds sequesters the causative
agent by trapping and surrounding it with fibrin. Microorganisms
trapped within the fibrin can multiply to form discrete colonies and
Justification
Acute cellular exudate in birds is composed primarily of
heterophils and undergoes caseation, not liquefaction
Same as above; cellular composition of exudate provides best
descriptor if a cell type is predominant
Virtually all inflanrniation of any duration in birds has a
granulomatous component; it is useful to distinguish those
resulting from caseated heterophilic exudate from those caused
by intracellular microorganisms
Term for granulomas resulting from intracellular bacteria e.g.,
Mycobacterium, or fungi in which macrophages rather than
heterophils are the predominant cell type
Localized inflammatory lesions in birds consist of multiple
layers of fibrin that entrap causative agents and inflammat01y
cells, not by necrosis and neutrophilic exudation as in mammals
Avian Histopathology (4 th Edition) I 7
 H. John Bames • Oscar J. Fletcher
I remain vi able for long periods. It has been suggested that the viable
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organisms can be released in response to stress and re-initiate the
inflammatory process. In mammals, irritants are destroyed and re-
moved via pus formation . Sometimes, considerable collateral tissue
damage and destruction results from this process.
Mild irritation of secreto1y membranes stimulates hypersecretion
resulting in catarrhal inflammation of mucous membranes, serositis of
serosal membranes, or synovitis of synovial membranes. In catarrhal
inflammation, goblet cells and mucous gland activity are increased and
excess mucus is present on the mucosal surface and in the lumen of
the affected organ. Increased eosinophilic staining reflects changes in
mucus composition. Often mucociliary clearance in airways is com-
promised in catarrhal inflammation of the respiratory tract, which can
lead to accumulation of mucus on the mucosa! epithelium.
Microscopic changes in mild inflammation of serosal and sy-
novial membranes are more difficult to detect. Membranes may be
thickened and edematous because of the excess fluid , and epithelial
cells are swollen and rounded. Epithelial hyperplasia that progresses
to polypoid proliferations is a feature of chronic lesions of secreto1y
membranes. Lymphoid infiltrates often accompany chronic prolifera-
tive lesions. Fibrin exudation and cellular infiltration are not features
of this stage ofinflanuuation. With intense irritants, the inflammato1y
process proceeds so rapidly that these early changes are often not seen.
Continued or more severe irritation leads to vascular changes
and leakage of proteins causing edema with or without accompany-
ing fibrin (serous, serofibrinous, or fibrinou s inflammation). Early
vascular changes, most likely in response to the release of vasoac-
tive amines from mast cells and basophils, affect the post-capillary
venules. Serous fluids containing protein are homogenous and stain
pink with H&E stains, the intensity of color being proportional to
the protein content. Proteinaceous fluid, often seen around sheathed
capillaries in the spleen of birds with bacterial sepsis, needs to be
distinguished from amyloid because of its similar appearance and
occurrence in that organ. Fibrin forms eosinophilic strands or net-
works that appear more solid as it condenses. Interconnections of
fibrin are marked by a characteristic, small, bead-like consolidation,
which aids in its histologic identification. At this stage, there may
be small , intravascular aggregates oftluombocytes or thrombocytes
adhering to the vasculature intima . Intravascular fibrin thrombi in
the liver, spleen, kidneys , and, less commonly, lungs also may be
present and indicate a systemic process. Disseminated intravascular
coagulation can occur, usually because of bacterial septicemia.
Accompanying leakage of proteins, margination and emi gra-
tion of cells accelerates to become the dominant feature of the in-
flamm atory process. Within 30-60 minutes of exposure of a tissue
to an irritant, there is dilation ofvenules, margination ofheterophils
and monocytes, and emigration of these cells into surrounding tis-
sues in response to locally generated chemoattractants. Heterophils
may predominate, be less than, or approximately equal to the num-
ber of monocytoid cells depending on the nature of the irritant. En-
dotoxin is strongly chemotactic for heterophils. While heterophils
and monocytoid cells continue to increase, variable numbers of ba-
sophils also migrate to the damaged site. This constellation of rapid
mobili zation and emigration of heterophils and monocytes with ba-
sophil participation is considered characteristic of early inflamma-
8 I American Association of Avian Pathologists
tion in the chicken and an essential survival mechanism. Marginated
intravascular reserves and circulating pool of leukocytes provide the
cells for the initial response. Transient heteropenia occurs simulta-
neously with the rapid increase in tissue heterophils. Subsequent
heterophilia likely results from bone marrow activation and hyper-
plasia. As inflanunation develops, monocytes become activated into
macrophages and heterophils undergo degeneration and degranula-
tion releasing toxic substances (defensins) into surrounding tissues.
By approximately 12 hours, basophils are no longer a feature of
the process and heterophils, many of which are degenerating, reach
maximal numbers and begin to decrease. Over the next 12-24 hours,
lymphoid cells and macrophages continue to increase and become
the prominent feahire of the lesion; macrophages fuse to form mul-
ti nucleated giant cells. Presence of giant cells in avian inflammation
should not be interpreted as an indication of chronicity.
Macrophages play a central role in avian inflammation. Con-
troversy exists concerning the relative significance of macrophages
and heterophils as primaiy phagocytic cells in vivo. Both are capable
of phagocytosis and probably pe1form this function although varia-
tions likely exist depending on the specific circumstances involved in
the inflammato1y process. Cytokines, produced primarily by macro-
phages, with activities similar to mammalian IL-I, IL-2, TL-6, TNF,
and granulocyte colony-stimulating factor, orchestrate local and sys-
temic responses. Toll-like receptors on the cell membrane recognize
basic molecular patterns of infectious agents, which stimulate produc-
tion of reactive oxygen products, nitric oxide, and proinflammat01y
cytokines. Macrophages also are responsible for recruiting lympho-
cytes to the area and stimulating their multiplication and differentia-
tion into plasma cells. They also process antigens and deliver them to
lymphocytes initiating an acquired immune response.
Exudate that results from tissue necrosis and massive fibrin and
heterophil accumulation caseates to form a heterophilic fibriscess .
Caseation may not be a static process as repeated episodes of in-
flammation can occur resulting in enlargement of the original mass
and a laminated "onion-skin" appearance grossly and microscopi-
cally. Often intralesional bacterial colonies are located within the
caseous exudate. Although the bacteria are sequestered within the
exudate, they remain viable and can be isolated using appropriate
culh1ral methods. Colonial morphology may provide a presumptive
identification, but isolation and identification should be relied on
to confirm the identity of the organism. Macrophages accumulate
around the core of necrotic fibrinoheterophilic debris; many fuse to
become giant cells. After a few days, a layer of macrophages and
giant cells forms on the surface of the necrotic core isolating it from
adjacent viable tissue, which results in the formation of a hetero-
philic granuloma. Microscopically, a palisade of radially arranged
multinucleated giant cells rims the caseous core. An incomplete
layer of macrophages and giant cells or focal necrosis of the cells
with extension of exudation through this cell layer indicates the pro-
cess is still active and has not been completely controlled. A broader
zone of predominantly macrophages, often mixed with a few het-
erophils and giant cells, surrounds the core rimmed by giant cells.
The heterophilic granuloma later beco mes surrounded by fibrous
tissue that condenses with age and may contain variable numbers
of lymphocytes and plasma cells . Phagocytic cells slowly erode

th e caseous exudate over an extended period. However, variable
numbers of heterophils continue to be present in these lesions sug-
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gesting the exudate itself serves as an irritant provoking a continued
mild inflanunatory reaction. If the caseated central mass is eventu-
all y removed, the damaged site fills with granulation tissue, which
matures to fibrous connective tissue. With the possible exception
of parasitic granulomas, calcification of exudate is not a feature of
either heterophilic or histiocytic granulomas in birds.
Histiocytic granulomas develop by an entirely different pro-
cess. The initial lesion is a collection of foamy macrophages, which
contain the causative organism (e.g. , Mycobacteri11111) . As the lesion
ex pands, centrally located cells undergo degeneration and necrosis,
often provoking a mild heterophilic response. This is accompanied
by marked proliferation of giant cells. The causative agent may be
demonstrable in these cells or free in the necrotic central area. At
certain stages, particularly terminally, histiocytic granulomas can
appear similar to heterophilic granulomas. The primary difference
between heterophilic and histiocytic granulomas is the type of cell
forming the necrotic center of the lesion.
Inflammation in chickens also has been studied by examining
wound repair. In wound healing, inflammato1y and reparative pro-
cesses occur together. Fibroplasia begins at around 18 hours follow-
ing the injmy. By three days, angiogenesis and re-epithelialization are
occurring, healing is essentially complete by day 7, and tissue is nearly
normal by day 10. Beginning on day 5, there is a period when multi-
nucleated cells are present in granulation tissue. Newly formed vessels
within granulation tissue persist and remain patent. This same process
occurs in response to ulceration of the skin or mucous membranes.
Advantages accrue to birds from having caseous rather than
purulent exudate. Caseous exudate is dehydrated and weighs less
than liquid purulent exudate. Caseous exudate does not move
around like purulent exudate; it stays in one place. Both of these are
advantageous for flight. Additionally infectious organisms or other
irritants are rapidly isolated and separated from adjacent viable tis-
sues minimizing spread and damage.
Neoplasia
A variety of mesenchymal and some epithelial neoplasms result
from infection with avian retroviruses (leukosis/sarcoma viruses)
including ones involving cells of the hematopoietic system - lym-
phoid leukosis (see Chap. 2), myeloid leukosis (myeloblastosis,
myelocytomatosis), and erythroblastosis (erythroid leukosis) . The
type of neoplasia that develops depends on the strain and dose of
virus; genotype, age, and sex of the bird; route of inoculation; and
presence or absence of " helper" viruses. In companion birds, lym-
phosarcoma can occur without convincing evidence of retroviral
infection. As noted above hematopoietic neoplasia needs to be
differentiated from bone marrow hyperplasia, extra-medullary he-
matopoiesis, and inflammation. Hematopoietic neoplasia may be
aleukemic or leukemic. Circulating tumor cells are often abundant
and readily identified in hepatic sinusoids or lung capillaries when
leukemia is present. Any hemopoietic neoplasia can efface normal
cells in the bone marrow and cause myelopathic anemia .
Myeloid tumors may be comprised of cells in any stage of dif-
ferentiation from blast cells (myeloblastosis, myeloblastomas) to
Hemic System
nearly mature granulocytes (myelocytomatosis, myelocytomas).
When myeloid leukosis is caused by serogroup J avian leukosis
I
virus (ALV-J), tumors composed of cell populations in different
stages of maturation can be found in the same bird. Collectively
granulocytic tumors are referred to as myeloid leukosis regardless
of the maturational stage of the cell type, which is useful since tu-
mors representing the full gradient of myeloid differentiation have
the same etiology. However, myeloblastomas and myelocytomas
differ in both gross and microscopic pathology.
Myelocytomas are cream-colored, soft, nodular, multiple, tumors
that are conunonly associated with the periosteum and cai1ilaginous
junctions of bones, especially ribs, sternum, ve11ebrae, synsacrum, and
flat bones of the skull. Bone marrow is pale. Visceral organs (liver,
spleen, kidney, gonads, lungs, etc. ) also are affected. Microscopically,
tumors consist of sheets of uniform myelocytes characterized by me-
dium size; large, round to elongated nuclei ; and cytoplasm containing
abundant, intensely eosinophilic round granules. Mitotic figures are
common. Marrow is effaced and tumors extend through bone along
Haversian and Volkmann 's canals into adjacent soft tissues. Initial le-
sions begin in the bone marrow of the epiphysis. Atrophy and perios-
teal proliferation of bone accompanies myeloid lesions. Lesions also
may occur in the dura mater and ossified respirat01y tissues.
Myeloblastomas are characterized by enlargement of liver,
spleen, and kidneys, which are pale, mottled or, on rare occasions,
contain gray nodules. Bone marrow is pale gray to white. Organ
enlargement is due to massive intra- and extravascular accumula-
tions of immature myeloid cells (myeloblasts, promyelocytes). My-
eloblasts tend to be larger than myelocytes but smaller than erythro-
blasts; have a more acidophilic cytoplasm, often with faintly visible,
large, pale granules; and are polygonal or angular shaped compared
to the round to oval shape of e1ytlll'oblasts. Their nucleus is denser
and nucleoli may be visible, but they are not as prominent as those
seen in erythroblasts. Affected birds are usually leukemic and large
numbers of these cells can be seen in blood smears. Extramedullary
bematopoiesis is often prominent, and should not be interpreted as
representing a different type of neoplasm.
Erytlu·oblastosis (erythroid leukosis) is much less common
compared to lymphoid or myeloid leukosis. Two distinct diseases
result from infection with e1ythroblastosis viruses - a proliferative
form and an anemic form. In the proliferative form , there is dif-
fuse hepatic and splenic enlargement. The organs and bone marrow
are bright red. Sinusoids in these organs and the bone marrow are
packed with erythroblasts. Tumors per se do not develop in erythro-
blastosis; lesions remain intravascular. In the anemic form , visceral
organs are normal or atrophic, birds are severely anemic, and bone
marrow is pale, almost acellular, and partly replaced by massive
proliferation of endosteal bone. Erytlll'oblasts have a large round
nucleus with fine chromatin, one or two nucleoli, and abundant ba-
sophilic cytoplasm that is often pale immediately surrounding the
nucleus. They are generally larger than myeloblasts. Presence of
cytoplasmic granules in the cells distinguishes myeloblastosis from
e1ytlll'oblastosis, but granules in myeloblasts can be difficult to iden-
tify. Both myeloblasts and e1ythroblasts may be intravascular, but
erythroblasts are only intra vascular. If necessary, cell markers spe-
cific for each cell type can be identified by immunohistochemistry.
Avian Histopathology (4 th Edition) I 9
 H. John Ba mes • Oscar J. Fletcher
I Campbell, T. W. and C. K. E llis. 2007. Avian and Exotic Animal
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In blood smears, large numbers of erythroblasts and other immature
erythrocytes can be seen in both forms. As with myeloblastosis,
extramedullary hematopoiesis can be extensive in birds with eryth-
roblastosis and should not be confused with neoplasia.
Additionally, mixed erythroblastosis and myeloblastosis cases,
and rare tumors compri sed of hemopoietic stem cells, which must
be differentiated from myeloblasts and erytluob lasts occur. Cells in
he1i1opoietic stem cell tumors are much larger and more basophilic
than either erythrob lasts or myeloblasts. They have a large nucleus
with prominent nucleoli and abundant intense staining cytoplasm
that lacks visible granules.
Infrequently, neoplasia in other tissues metastasizes to the bone
marrow. Examples include malignant melanoma in a pigeon that
spread from the beak to several tissues including bone marrow and a
mast cell tumor with systemic mastocytosis in a lovebird.
Additional Readings
Andreasen, C. B. and K. S. Latimer. 1990. Cytochemical staining
characteristics of chicken heterophils and eos inophils. Vet C/in
Patho/ 19:51-54.
Awadhiya, R . P. , J. L. Vegad, and G. N . Kolte. 1980.
Demonstration of the phagocytic activity of chicken
thrombocytes using colloidal carbon. Res Vet Sci 29 : 120-122.
Awadhiya, R. P. , J. L. Vegad, and G.N. Kolte. 1980. Studies on
acute inflammation in the chicken using mesente1y as a test
system. Res Vet Sci 29: 172-180.
Bar-Shira, E. and A. Friedman. 2006. Development and
adaptations of innate immunity in the gastrointestinal tract of
the newly hatched chick. Dev Comp !11111111110/ 30:930-941 .
Bermudez, A. J. and B . A. Hopkins. 1995 . Hemoglobinuric
nephrosis in a rhea (Rhea americana).Avian Dis 39:661-665 .
Bougiouklis, P., G. Brellou, E . Fragkiadaki, P. Iordanidis, I.
Vlemmas, and I. Georgopoulou. 2005 . Outbreak of avian
mycobacteriosis in a flock of two-year-old domestic pigeons
(Co /11111 ba livia f. do111estica). Avian Dis 49:442-425 .
Botmous, D.l. and N.L. Stedman. 2000. Normal avian hematology:
chicken and turkey. In Scha/m s VeterinalJ' Hematology, 5th
ed., B.F. Feldman, J.G. Zinkl, and N.C. Jain, Eds. Lippincott
Williams & Wilkins, Baltimore, MD. pp. 1147-1154.
Brooks, R . L. Jr., D . I. Bmmous, and C. B. Andreasen. 1996.
Functional comparison of avian heterophils with human and
canine neutrophils. Comp. Haemato/ Int. 6: 153-159.
Burgos-Rodriguez, A . G ., M . Garner, T. K. Ritzman, and C. J.
Orcutt. 2007 . Cutaneous lymphosarcoma in a double yellow-
headed Amazon parrot (Amazona ochrocepha/a oratrix). J
Avian Med Surg 21 :283-289.
Calderon, N. L. , F. Galindo-Muniz, M. Orti z, B. Lonmiczi, T.
Fehervari, and L. H . Paasch. 2005. Thrombocytopenia in
Newcast le disease: haematological evaluation and study of
bone marrow. Acta Vet Hung 53:507-513.
Ca ldwell , D. J. , H . D . Danforth, B. C. Morris, K . A. Ameiss, and A.
P. McElroy.2004 . Participation of the intestinal epithelium and
mast cells in local mucosa! immune responses in commercial
poultry. Pou/t Sci 83:591 -599.
IO J American Association of Avian Pathologists
Hematology and Cytology. Blackwell Publishing Professional ,
Ames, IA . pp. 3-50.
Chiu, H. and D. Lagunoff. ( I 972). Histochemical comparison of
vertebrate mast cells. Histoche111 J 4: 135-144.
C lark, M. W. , R. P. Gildersleeve, J . P. Thaxton, C.R. Parkhurst,
C . R ., and D. I. McRee. 1988.Hematological effects of ethyl
methanesulfonate, paraquat and phenylhydrazine in Japanese
quail.Comp Bioche111 Physiol C 89: 15-30.
Crespo, R. and R. P. Chin. 2004. Effect offeeding green onions
(A!lium asca/onicum) to white Ch inese geese (Threskiornis
spinico!lis). J Vet Diagn Invest 16:321-325.
Dall wig, R. K. , J. K. Whittington, K. Terio, and A. Barger.2012.
Cutaneous mast cell tumor and mastocytosis in a black-masked
lovebird (Agapornis persona/a). J Avian Med Surg 26:29-35.
Gobel, T. W. , B. Kaspers , and M. Stangassinger. 200 I. NK and
T cells constitute two major, functionally distinct intestinal
epithe li al lymphocyte subsets in the chicken. Int /11111111110/
13 :75 7-762.
Harmon, B. G . 1998. Avian heterophils in inflammation and
disease resistance. Poul! Sci 77:972-977.
He, H., K. J. Genovese, D. J . N isbet, and M. H . Kogut. 2006.
Profile of Toll-like receptor expressions and induction of
nitric oxide synthesis by Toll-like receptor agonists in chicken
monocytes. A1o/ /11111111110/ 43:783-789.
Howard, L. L. , R. Papendick, I. H. Stalis, J. L. Allen, M.
Sutherland-Smith, J. R. Zuba, D . L. Ward , and B. A. Rideout.
2002. Fenbendazole and albendazo le toxicity in pigeons and
doves. J Avian Med Surg 16:203-210.
Huchzermeyer, F. W. and J.E. Cooper. 2000. Fibriscess, not
abscess, resulting from a localised inflammatory response to
infection in reptiles and birds. Vet Rec 147:515-517.
Hutchinson, A. E. and R. B . Owen. 1984 . Bone marrow fat in
waterfowl. J Wild/ Manage 48:585-591.
Inoue, M. , A. Fujita, and K. Maeda. 1999. Lysis of myelocytes
in ch ickens infected with infectious bursa] disease virus. Vet
Patho/ 36: 146-151.
Johnston, M. S., T. T. Son, and K. L. Rosenthal. 2007. Immune-
mediated hemolytic anemia in an Eclectus parrot. J Am Vet
Med Assoc 230 : I 028-1031.
Jones , K . H ., F. D. Wilson, S. D . Fitzgera ld, and M . Kiupel. 2012.
A natural outbreak of c lini ca l toxoplasmosis in a backyard
flock of guinea fowl in Mississippi. Avian Dis 56:750-753.
Joyner, P.H., S. Kelly, A. A. Shreve, S. E . Snead, J.M. Sleeman,
and D . A. Pettit. 2006. West Nile virus in raptors from Virginia
during 2003: clinical, diagnostic, and epidemiologic findings . J
Wild/ Dis 42 :335-344.
Kaiser, P. 2007. The avian immune genome - a glass half-full or
half-empty?Cytogenet Genome Res 117:221-230.
Kajigaya, H., K. Konagaya , H. Ejima, Z. Usuda, S. Kodama , and
J. Thone. 2010. Metastatic mel anoma appearing to originate
from the beak ofa racing pigeon (Co/11111ba /ivia). Avian Dis
54:958-960.
Klasing, K. C . 1998. Av ian macrophages: regulators of local and
systemic immune responses. Pou/t. Sci 77: 983-989.

Kogut, M. H. , l. Muhammad, H. He, V. Philbin, P. Kaiser, and A.
Smith. 2005. Expression and function of Toll-like receptors in
VetBooks.ir
chicken heterophils. Develop Comp !11111111110129: 791-807.
K unkle, R. A. and R. B. Rimler. 1996. Pathology of acute
aspergillosis in turkeys. Avian Dis 40: 875-886.
Latimer, K. S., K. N . Tang, M.A. Goodw in, W.L. Steffens, and
J. Brown. 1988. Leukocyte changes associated with acute
inflammation in chickens. Avian Dis 32:760-772.
Lowry, V. K., K. J. Genovese, L.L. Bowen, and M. H . Kogut.
1997. Ontogeny of the phagocytic and bactericidal activities
ofhirkey heterophils and their potentiation by Sal111011ella
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Microbial 19:95- 100.
Maxwell, M. H. 1987. The avian eosinophil - a review. World's
Pou It Sci J 43: l 90-207 .
Maxwell, M. H. 1995. The avian basophilic leukocyte: a review.
World's Po11lt Sci J 51 :307-325
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2007. Foot pad dermatitis in growing hirkeys is associated with
cytokine and cellular changes indicative of an inflammatory
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Monta li , R.J. 1988. Comparative pathology of inflammat ion in
the higher vertebrates (reptiles, birds and mammals). J Comp
Pathol 99: 1-26.
Na ir, M. K. I 973 . The early inflammatory reaction in the fowl. A
light microscopical , ultrastructural and autorad iographic study.
Acta Vet Scand (Suppl) 42: 1-103.
Nakamura, K. , M. Ogiso, K. Tsukamoto, N. Hamazaki, H. Hihara,
and N . Yuasa. 2000. Lesions of bone and bone marrow in
myeloid leukosis occurring naturally in adult broiler breeders.
Avian Dis 44:215-221.
National Research Council. 1994. Nutrient R equirem ents of
PoulhJ', 9th ed. National Academy Press, Washington D.C. pp.
46-57 . htt ://www.na .edu/o enbook. h ?isbn=0309048923
O li as, P. , A. D. Gruber, A. 0. Heydorn, A. Kohls , H. M . Hafez, and
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(Co lumba livia f. domestica) follow ing experimental infection
with Sarcocystis calchasi. Avian Dis 54: I 032-1037.
Osofsky, A ., M . G. Hawkins, 0 . Foreman, M. S. Kent, W. Vernau,
and L .J. Lowenstine. 201 1. T-cell chronic lymphocytic
leukemia in a double yellow-headed Amazon parrot (Amazona
ochrocephala oratrix). J Avian Med Surg 25:286-2894.
Pantin-Jackwood, M. J. , T. P. Brown, and G. R. Huff. 2004.
Proventriculitis in broiler chickens: immunohistochemical
characterization of the lymphocytes infiltrating the
proventricular glands. Vet Pathol 41 :641-648.
Petrone, V. M., C. F. Constantino, and P. Pradal-Roa. 2002.
Identification and quantification of granulocytes in caecal
mucosa and submucosa of chi ckens experimentally infected
with Eimeria tenella and Sal111011ella enteritidis. B r Poult Sci
43 :653-66 I.
Qureshi, M . A. 2003. Avian macrophage and immune response: an
overview. Po11/t Sci 82:69 1-698.
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Schepelmann, K. 1990. Erythropoieti c bone marrow in the pigeon:
development of its distribution and volume during growth and
I
pneumatization of bones. J Mo 1phol 203:2 l-34.
Schoemaker, N. J., G. M. Dorrestein, K. S. Latimer, J. T. Lumeij ,
M. J. Kik, M. H. van der Hage, and R. P. Campagnoli. 2000.
Severe leukopenia and liver necrosis in young African grey
parrots (Psittacus erithac11s erithacus) infected with psittacine
circovirus. Avian Dis 44:470-478.
Shivaprasad, H. L. , R. Kokka , and R. L. Walker. 2007. Listeriosis
in a cocka tiel (Ny111phic11s hollandicus). Avian Dis 51 :800-804.
Shivaprasad, H. L., M. B. Cadenas, S. S. Diab, R. Nordhausen, D.
Bradway, R. Crespo, and E. B. Breitschwerdt. 2008 . Coxie//a-
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432 .
Shivaprasad, H. L., T. Kim, D. Tripathy, P. R. Woolcock, and F.
Uzal. 2009. Unusual pathology of canary poxvirus infection
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Siatskas, C. and R. Boyd. 2000. Regulation of chicken
haemopoiesis by cytokines. Develop Comp !11111111110124 :37-59.
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brain mast cells and behavior. In, Progress in Brain Research ,
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2006. Chicken anaemia virus inoculated by the oral route
causes lymphocyte depletion in the thymus in 3-week-old and
6-week-old chickens. Avian Pathol 35:254-259.
Takami, S. , M. Goryo, T. Masegi, and K. Okada. 2005. Systemic
spind le-ce ll proliferative disease in broiler chickens. J Vet Med
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Ueda, Y. , Y. Aohagi, and S. Nakahara. 2005 . Distribution of
protoporphyrin in female broiler chickens affected with
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Ve gad, J. L. and A. K. Katiyar. 1995. The acute inflammatory
response in the chicken. Vet Bu/165:399-409.
Venugopal, K. 1999. Avian leukosis virus subgroup J: a rapidly
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119.
Wade, L. L. and S. J. Newman. 2004.Hemoglobinuric nephrosis
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sativum). J Avian Med S11rg 18: 155-161.
Weber, M.A. , S. P. Terrell , D. L. Neiffer, M.A. Miller, and B. J.
Mangold. 2002. Bone marrow hypoplasia and intestinal c1ypt
cell necrosis associated with fenbendazole administration in
five painted storks. J Am Vet Med Assoc 221 :417-419.
Zhang, Z., F. Wilson, R. Read , L. Pace, and S. Zhang. 2006.
Detection and characterization of naturally acquired West Nile
virus infection in a female wild hirkey. J Vet Diagn Invest
18:204-208.
Avian Histopathology (4 th Edition) I 11
 H. Jol,11 Rames • Oscar J. Fletcher
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1.1. Bone Marrow, femur, mid-shaft. Normal. 41-day-old
chicken. A. Hematopoiesis is compartmentalized in the bone
marrow of birds. faythropoiesis occurs within sinusoids while
myelopoiesis takes place in the extrasinusoidal spaces. B. Focus
of myelopoiesis composed of granulocytes in different stages of
maturation. C. Lymphoid foci occur frequently in bone marrow
and increase in both size and number with age. D . Myeloid and
lymphoid cells often occur together. (Case courtesy of F. Wilson) .
1.2. Liver. Extramedullary hematopoiesis (EMH). Chronic
right-sided heart failure. 43-week-old broiler breeder.
Hematopoiesis in organs outside of the bone marrow (extramedullary
hematopoiesis [EMH]) is common in both normal and diseased
birds. This hematopoietic focus is primarily myelopoietic because it
is composed of myelocytes in different stages of maturation. EMH
increases in birds when there is greater demand for blood cells.
EMH must be differentiated from inflammatory and neoplastic
lesions.
12 I American Association of Avian Pathologists
1.3. Liver. Extramedullary erythropoiesis. Normal. Adult
violet euphonia (Tmwgra 11iolacea) . Similar to its occurrence
in bone marrow, extramedullary erythropoiesis occurs within
vessels. Large round to oval , intensely basophilic cells, with central
nucleus line the sinusoids in which erythropoiesis is occurring.
Extramedullmy e1ythropoiesis without concurrent myelopoiesis is
unconunon.
1.4. Heart. Extramedullary hematopoiesis (EMH). Normal.
Broiler. Extramedulla1y hematopoiesis (EMH) occurs in the heart
of young birds . Both myelo- and erythropoiesis are evident here.
EMH can be differentiated from inflammatory and neoplastic
lesions by the mix of cells and lack of invasion or adverse effects on
adjacent tissues.
 Hemic System

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1.5. Air Sac. Fowl cholera. 6 hours post experimental infection
with Pasteure/la 11111/tocida. 8-week-old turkey. In well preserved
ac ute inflammatory lesions, heterophils of chickens and turkeys can
be recognized by their spiculate, eosinophilic, cytoplasmic granules.
More commonly, the granules are not as distinct and differentiation
of heterophils from eosinophils requires special staining methods.
Heterophils are aggregating where bacteria have breached the air
sac epithelium, as endotoxin is strongly chemotactic. Protein-rich
fluid also is accumulating in the air sac interstitium.
1.7. Kidney. Hemoglobinuria. Undetermined etiology.
2-year-old guinea fowl. A. Excess hemoglobin resulting from
intravascular hemolysis is filtered by the glomeruli and may
accumulate in renal tubules as hemoglobinuric casts. Casts are
acellular, hyaline, and stain bright orange with H&E stain in contrast
to the more common pink-staining protein casts. Degeneration and
necrosis of tubular epithelium (arrowheads) can occur in severe
cases. 8. Detail showing hemoglobinuric casts. Note lysis of
erythrocytes in vessels.

1- l

1.6. Lung. Intravascular hemolysis. Undetermined etiology.
27-week-old broiler breeder hen. Pulmonary capillaries and small
vessels contain lysed erythrocytes. Phagocytic cells within the
vessels are capturing hemoglobin, which is in the process of being
converted into hemosiderin. Insert. Detail showing early formation
ofhemosiderin (*). The cause of the hemolysis was not determined.
1.8. Bone Marrow. Pancytopenia. Chicken infectious
anemia. 7 and 14 days post experimental infection. SPF
chickens. A. There is mild loss ofhemopoietic cells in bone marrow
at 7 days after infection with chicken infectious anemia virus on day
1. B. By 14 days post-infection, the marrow is virtually devoid of
hemopoietic cells. (Case courtesy of M. Go1J10) .

Avian Histopathology (4 th Edition) I 13

 H. Jol,11 Bames • Oscar J. Fletcher
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1.9. Bone Marrow. Pancytopenia. Chicken infectious
anemia. 7 days post experimental infection. SPF chicken. At
7 days post infection, hemocytoblasts (center) frequently contain
multiple small eosinophilic inclusion bodies (arrows) within their
nuclei. Inclusions are rarely seen after day 12 and are no longer
present by day 16. (Case co11r/e5y of M. Go1J10).
1.10. Bone Marrow, femur, mid-Shaft. Hyperplasia. Type 1
Avian adenovirus infection (inclusion body hepatitis). 3-week-
old chicken. Viruses are not usually considered as causes of
bone marrow hyperplasia, but in this natural infection with Type
1 avian adenovirus, there is marked bone marrow hyperplasia.
A. Basophilic cells along sinusoids, and extrasinusoidal spaces
expanded by confluent granulocytes characterize bone marrow
hyperplasia. B , C. Detail showing hyperplastic changes. D . Several
blast cells. Whether these are myeloblasts, erythroblasts, or even
more primitive hemocytoblasts cannot be determined with certainty.
(Cas e co11r/e5y of F Wilson).
14 I American Association of Avian Pathologists
1.11. Bone Marrow, femur, mid-shaft. Hyperplasia. Aspergillus
sp. infection (aspergillosis). Adult victoria crowned-pigeon
(Go11n1 victoria). In addition to viral and bacterial diseases, fungal
infections can also stimulate bone marrow hyperplasia, especially
of myeloid cells. lntrasinusoidal spaces are markedly expanded by
immature myeloid cells in various stages of development. Note the
mitotic figures and compression of adjacent sinusoids. Presence
of immature myeloid cells in different stages of development
distinguishes hyperplasia from neoplasia in which cell populations
are usually monoclonal.
•
1.12. Air Sac. Airsacculitis. 3 hours post experimental
inoculation. 8-week-old turkey tom. The post-capillary venule
is the site of inflammatory changes. This air sac was exposed to
phorbol myristate acetate, potent initiator of inflammation. Normal
unaffected arteriole (far right) and severely inflamed venule (center
to left) can be seen . Within the venule is thrombus composed of
degenerating thrombocytes that is surrounded by heterophils.
Emigrating heterophils are remaining close to the venule, possibly
because of lack of chemotactic factors to draw them away. Dense
proteinaceous fluid is leaking from the venule indicating severe
damage to the vessel wall (lower left).

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1.13. Liver. Leukocytosis, heterophilia, liver necrosis.
Suspected Clostridium sp. 6-day-old broiler. Dilated sinusoids
co ntaining numerous granulocytes provide histopathologic evidence
ofleukocytosi s and heterophilia. Compare the number ofleukocytes
with the number of erytlu·ocytes in this section. Normally sinusoids
contain mostly erythrocytes w ith fewer leukocytes.
1.14. Liver. Granulomatous hepatitis. Mycobacteriosis.
9-year-old duck. Multiple nodules of pale cells replace much of
the liver parenchyma. Small nodules associated with larger nodules
indicate this is an active process. Large nodule contains central
mass of caseous exudate that is ringed with multinucleated giant
cells. Granulomas are common in birds and come in two types -
heterophilic and histiocytic depending on the cell type making up
the caseous center of the lesion. This is an example of histiocytic
granu loma caused by Afycobacteri11111 sp. Insert. Detail of granuloma
wa ll. Caseous center is in the upper left.
Hemic System
I
1.15. Liver. Myeloid leukosis. Adult broiler breeder, avian
leukosis virus J-erotype positive flock. Focus of tumor cells
has replaced liver tissue to form tumor nodule. Cells comprising
the tumor are uniform population with sparse, but well defined,
eosinophilic granules in the cytoplasm, round, open nucleus with
distinct nucleolus, and often an angu lar shape. These features define
the cells as myeloid cells. Occasional mitotic figures are present.
Observe the expansion of tumor cells along sinusoids, which has
resulted in isolation, compression, and loss of liver cells. Compare
with extramedullary hematopoiesis. Insert. Detail of neop lastic
myeloid cells.
1.16. Liver. Myeloid leukosis. Adult broiler breeder, avian
leukosis virus J-serotype positive flock. Portal area is infiltrated
by neoplastic myeloid cells, which form layer 2 to 3 cells thick
around vessel. On the opposite side (upper right) is an infiltrate
of myeloblasts. Myeloblasts approximate the size of liver cells. It
is common in ALV-J virus infections to have multiple neoplastic
cell types. Insert. Neop lastic myeloid cells (left) compared to
myeloblasts (right).
Avian Histopathology (4 th Edition) I 15
 H. Jol,11 Barnes • Oscar J. Fletcl,er

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1.17. Ovary. Myeloblastosis. Adult broiler breeder, avian

leukosis virus J-serotype positive flock. Expanding mass of
tumor cells fills a space within the ovary. Cells are large, basophilic,
have an eccentric round nucleus with prominent nucleolus, and
the cytoplasm of most cells contains pale pink, hyaline granules.
These features define the cells as myeloblastic. Compare the size
of neoplastic myeloblasts with the normal granulocytes that are in
the ovarian stroma . Insert. Detail of myeloblasts showing their
characteristic features.

1.18. Ovary. Myeloblastosis. Adult broiler breeder, avian

leukosis virus J-serotype positive flock. Expanding mass of
tumor cells fills space within the ovary. Cells are large, basophilic,
have an eccentric round nucleus with prominent nucleolus, and
the cytoplasm of most cells contains pale pink, hyaline granules.
These features define the cells as myeloblastic. Compare the size
of neoplastic myeloblasts with the normal granulocytes that are in
the ovarian stroma. Insert. Detail of myeloblasts showing their
characteristic features.

16 I American Association of Avian Pathologists

VetBooks.ir
CHAPTER
Lymphoid System
Tahseen Abdul-Aziz • Oscar J. Fletcher
Introduction
The lymphoid system is comprised of two primary lymphoid or-
gans, bursa of Fabricius (BF) and thymus), and secondary lym-
phoid tissues in the spleen and most organs and tissues . Bursa-
dependent lymphocytes (B-lymphocytes) are responsible for
immunoglobulin production while T-dependent lymphocytes
(T-lymphocytes) are responsible for cell-mediated immune func-
tions. In addition to B- and T-lymphocytes, the immune system
a lso includes the supporting framework of reticular cells, the his-
tiocytes or macrophages, dendritic cells, and lymphatics. B- and
T-lymphocytes can be tentatively identified based on location and
histologic pattern in the spleen and other organs or tissues, but
definitive identification requires special immunohistochemistry
staining, usually for CD markers on the cell surface. Stem cells of
yolk sac origin are critical for populating the BF and thymus dur-
ing embryonic development.
Secondary Lymphoid Tissues
(!) Spleen (see below).
(2) Gut-associated lymphoid tissues (GALT) that include Peyer's
patches in the small intestine, esophageal tonsil in the esophagus at
the junction with the proventriculus, pyloric tonsil at the junction
of the duodenum with the gizzard (on the duodenum side), cecal
tonsils, Meckel's diverticulum, and lymphoid tissue in the wall of
the cloaca. Ducks have distinct annular bands of lymphoid tissue in
the jejunum and ileum. The GALT frequently has a well-organized
structure where B-lymphocytes form follicles, while T-cells accu-
mulate in the interfollicular spaces.
(3) Bronchus-associated lymphoid tissues (BALT) in the wall of pri-
mary and seconda1y bronchi ;
(4) Head-associated lymphoid tissues that include conjunctiva-asso-
ciated lymphoid tissues
(CALT), Harderian gland, lymphoid tissues in the nasal turbinates
and lateral nasal glands and their ducts, and lymphoid accumula-
tions in the roof of the phary1u.
(5) Lymphoid cell aggregates associated with the walls of deep lym-
phatic vesse ls especially those that course together with the femoral
and deep tibial veins. These lymphoid aggregates are considered
primitive lymph nodes and are named " mural lymph nodes". Paired
cervicothoracic and lumbar lymph nodes are present in some spe-
cies of water, marsh, and shore birds.
The location and architectural structure of secondary lymphoid
tissues allow maximum contact between ant igen, antigen presenting
2
I
cells, and lymphocytes in order to generate quick and robust adap-
tive immune responses.
Well-circumscribed lymphoid nodules or less organized, small
accumulations of lymphoid cells are sometimes seen in different
organs and tissues such as liver, kidney, pancreas, adrenal glands,
gonads, thyroid, and bone marrow. These lymphoid cell nodules
or accumul ations are sometimes referred to as "ectopic or tertiary
lymphoid tissues" . In chickens, ectopic lymphoid tissues begins to
develop after 3 weeks of age and disappears after 3-4 months of age.
A particularly prominent lymphoid accumu lation appears in the pi-
neal gland of chickens after 3 weeks of age, and may constitute 50%
of the pineal gland mass.
Lymphatic vessels are less numerous in birds than in mammals,
and they are closely associated with blood vessels, surrounded by
a sheath of collagen fibers, and relatively difficult to visualize in
histologic sections stained with H&E stain. The absence of well-
defined lymph nodes in most avian species does not mean less need
for a highly functional lymphoreticular system, but rather that birds
have dispersed their lymphoid cells throughout many tissues. The
avian lympho id system has the capacity when stimulated to respond
with the formation of new, widely distributed lymphoid foci, so their
presence in many tissues should not be interpreted as evidence of
lymphoid neoplasia.
Bursa of Fabricius
The wall of the bursa ofFabricius (BF) is composed of an outer thin
serosal layer, a middle smooth muscle layer, and an inner mucosa.
The mucosa has many folds or plicae (about 12-15 major ones) that
fill the lumen and comprises the greatest portion of the thickness
of the wall. The surface of the folds is smooth and covered mostly
by pseudostratified columnar epithelial cells, which produce mucin-
like substance. Often visible is a tuft of specialized low co lumnar
epithelium capable of pinocytosis located at the points of contact of
the follicles with the epithelium. The tuft is referred to as follicular-
associated epithelium (FAE). Each mucosa] fold has several closely
packed polygonal to oval shaped lymphoid follicles separated by
a thin capsule of collagen-rich connective tissue (interfollicular
connective tissue). The lymphoid follicles are the structural and
functional units of the BF. Each follicles has its own blood sup-
ply independent of the adjacent follicles . Each follicle has an outer
cortex and inner medulla, except in ratites where this pattern is re-
versed. Separating the cortex from the medulla is a basal lamina (on
the cortical side) covered by undifferentiated epithelial cells (on the
Avian Histopathology (4th Edition) I 17
 Tahseen Abdul-Aziz • Oscar J. Fletcher
VetBooks.ir
medullary side). The basement lamina and the epithelial cells are
continuous with the surface epithelium. The FAE provides a con-
nection between the bursal lumen and the follicular medulla . Both
I
cortex and medulla possess a supporting network of reticular cells
whose meshes are filled with lymphoid cells. The cortico-medullary
epithelial cells and the cortical and medullary reticular cells become
more visible when there is loss of follicular lymphocytes. On his-
tologic sections, the cortices stain more deeply than cortices as they
contain larger numbers of closely packed small lymphocytes than
the medullas. Macrophages, are present in both cortex and medulla
but they are largely obscured by the lymphocyte population and are
often difficult to identify histologically. Macrophages with phago-
cytized material are easily recognizable in both the cortex and me-
dulla, and they are particularly seen in concert with necrosis and loss
of lymphocytes. Secretory dendritic cells have been described in
the medullae. Mitotic figures and variable numbers of pyknotic nu-
clei ofapoptotic lymphocytes are seen usually in follicles. Ve1y few
plasma cells may be seen, especially in involuting BF. The medulla
is a vascular. A capillary network is present at the cortico-medullary
border and in the cortex . Bursa) follicles do not contain lymphatics,
but lymph vessels are present in the interfollicular connective tissue.
Regeneration frequently occurs in the BF following bursa)
injury and typically is characterized by irregularity of follicle size
and variation in the density of the lymphoid cell population in the
follicles. Some follicles are well populated with lymphoid cells,
while the others shows lymphoid depletion that range in severity
from mild to moderate to severe. The mucosa) epithelium appears
irregular in some areas. Regenerative changes are similar to those
that occur during natural, (age-related) involution. Regeneration of
the BF does not occur after natural involution.
The BF in the chicken grows rapidly after hatching, reaching
maximum size around 12 weeks of age. Natural involution starts
as sexual maturity approaches. Early involution is characterized by
necrosis and loss of lymphocytes in medullae first then in cortices.
As the involution advances, there is reduction in size and number
of follicles, formation of medullary cysts, marked increase in the
interfollicular fibrous connective tissue, and infolding of the epi-
thelium. Heavily involuted bursas may consist of only connective
tissue containing few atrophied lymphoid follicles.
The BF is the primary lymphoid organ where the first stage
of B-lymphocyte differentiation takes place. At least 98% of lym-
phocyte population is B-lymphocytes. B-lymphocytes, which
probably enter the folli c les via cortical capillaries, mature and
differentiate in the follicles . Few, scattered T-cells are present in
the follicles. As B-lymphocytes mature, they leave the BF and
relocate in secondary lymphoid tissues. Stimulation ofB-lympho-
cytes by antigens and subsequent proliferation and differentiation
into memory cells or antibody-producing plasma cells occurs in
secondary lymphoid organs (e.g. spleen). Follicular lymphocytes
migrate from the cortex to the blood via the lymphatics in the in-
terfollicular interstitium.
Thymus
The thymus in birds consists of a string of ovoid or irregularly
shaped, flattened lobes embedded in the subcutaneous tissue on
18 f American Association of Avian Pathologists
both sides of the neck in close association with the jugular vein.
In chickens, there are usually seven lobes on each side of the neck.
The posterior end extends to be in close proximity to the thyroid
gland. Histologically, each lobe of the avian thymus is enclosed by
a connective tissue capsule. Septa from the capsule incompletely
divide the lobe into lobules, each consists of a centrally located
medulla surrounded by cortex. Septa end at the cortico-medullary
interface, leaving the medullae undivided. The cortex consists of
a mesh of epithelial reticular cells that are densely packed and
obscured by large numbers of lymphocytes (also called thymo-
cytes). A moderate numbers of macrophages are also present in
the cortex. The dense lymphocyte population gives the cortex the
deep basophilic staining in histologic sections . Many apoptotic
vacuoles containing condensed (pyknotic) nuclei are seen in the
cortex. The medulla contains epithelial cells, highly variable ep-
ithelial-like cells, and, compared to the cortex, small numbers of
lymphocytes. Large epithelial cells with abundant lightly eosino-
philic cytoplasm ands and large nuclei can be identified among the
lymphoid cells in the medullae. The large numbers of epithelial
cell s and the smaller number of lymphocytes in the medullae result
in less basophilic staining comparted to cortices. Skeletal muscle
cells (also called myoid cells) of uncertain function are a feature
of the thymic medullae. These cells are round or ovoid in shape
and have cytoplasmic striated myofibrils encircling the nucleus.
Macrophages with phagocytized debris are found normally in both
the cortex and medulla. Commonly seen in the medulla are het-
erophils, red blood cells, and small masses of eosinophilic mate-
rial , some of which have a nucleus. These eosinophilic masses
likely represent epithelial cells that are undergoing degeneration
and necrosis. Poorly delineated aggregates of epithelial cells, ei-
ther intact or at various stages of degeneration, occur in the medul-
lae of chicken thymus. These aggregates are considered a form
of Hassall 's corpuscles. The epithelial cells in the aggregates are
large and have abundant eosinophilic cytoplasm. Granulocytic
leukocytes are commonly found free or within vacuolar spaces
among these aggregates. Concentric arrays of squamous cells and
typical rounded , laminated and cornified Hassall 's corpuscles seen
in mammals are found in some avian species but rarely in chicken
thymus.
The thymus is the site ofT-lymphocyte maturation. It reaches
a maximum size in the chicken at 3-4 months of age and start to
regress naturally at the onset of sexual maturity.
Spleen
A capsule of connective tissue and smooth muscle surrounds the
spleen, but true trabeculae do not occur. The splenic artery enters
the spleen and gives rise to numerous branches of arteries, which
ramifies into arterioles and penicilliforrn capillaries. Arterioles
(also called central aiierioles) have a prominent muscular layer and
are surrounded a dense population of primarily T-lymphocytes that
form the periarteriolar lymphoid sheath (PALS). B-lymphocyte fol-
licles (bursa-dependent follicles) are scattered within the PALS and
are located adjacent to arterioles. In chickens, unlike in mammals,
a pale central (mantle) zone and a darker marginal zone are difficult
to distinguish morphologically in the B-lymphocyte lymphoid fol-

Iicles. With respect to handling and reaction to antigens, a compart-
ment that is considered fimctionally equivalent to the mantle and
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marginal zone in mammalian spleen has been described in chickens .
This compartment consists of ellipsoidal sheath of reticular cells,
and the surrounding population of B-lymphocytes with a surround-
ing ring of macrophages.
The penicilliform capillaries have very thick, discontinuous
basement membrane and are recogni zed by having high or plump
endothelial cells, no muscular layer, and by being surrounded by a
sheat h of reticular cells (also called ellipsoidal reticular cells), thus
the name sheathed capillaries. The sheath is known as the ellipsoid
or Schwei gge r-Seidel sheath. A ring of hi ghly phagocytic reticu-
lar cells called ellipsoid-associated cells are found on the surface
of the ellipsoid. The phagocytic cells are surrounded by a ring of
B-lymphocytes (sometimes described as periellipsoid lymphocyte
sheath), which in turn are surrounded by a ring of macrophages.
The PALS, ellipsoids and the sheath of B-lymphocytes and macro-
phages around the ellipsoids form the white pulp region.
The red pulp is the region around the ellipsoids and periellip-
soidal white pulp. The distinction between the white and red pulp
regions is much less evident in the avian spleen as compared to
mammals as these regions intermingle in the avian spleen. The red
pulp consists of connected venous sinuses a fine supporting network
of collagen fibers, lymphoid and nonlymphoid cells, and a network
of capillaries and venules . The sinuses are lined with flat endothe-
lial cells. The cell population of the red pulp comprises erytlu·o-
cytes, numerous T-lymphocytes, many macrophages, some plasma
cells, and scattered granulocytic leukocytes. Unlike the spleen of
mammals, the avian spleen does not have a major blood storage or
reservoir function. A major function of the spleen is the removing of
se nescent erythrocytes from the blood circulation. Recognition of
the pattern of splenic architecture is critical for appreciation of the
changes associated with diseases. Interpretation of changes in the
spleen is aided by experience in examining the organ in a variety of
normal and pathological conditions. For example, the number and
size of lymphoid follicles can vary from few to multiple per I OX
microscope field. Hyperplasia of lymphoid cells is often difficult to
interpret as it could be due to antigenic stimulation following vac-
cination, or to a disease.
Avian spleen has a closed circulatory pathway, which provides
for rapid transit of blood through the red pulp. In this pathway, af-
ferent capillaries are connected with sinuses in the red pulp. The
sinuses are in direct continuity with venules that are drained by col-
lecting veins, which join to form larger veins that leave the spleen.
Lymphoid Hyperplasia
With antigenic stimulation, reactive follicles (also called germinal
centers) are developed in spleens and other secondary lymphoid
tissues. Reactive follicles are almost always found in the second-
ary lymphoid tissues that include cecal tonsils, Meckel's diverticu-
lum, and Peyer 's patches that are in continuous contact with an-
tigenic material. As mentioned earlier, 8-cell follicles associated
with periarteriolar lymphoid sheaths are only occasionally found
in the spleens of birds. Increased numbers of bursa-dependent
follicles is an indication of immunoreactivity (activation of the
Lymphoid System
immune system), and such spleens may be referred to as "reac-
tive sp leens". These reactive follicles are the site of B-cell clonal
expansion and differentiation into plasma cells and memory B
I
cells. Driven by antigen stimulation, na'ive B-lymphocytes under-
go clonal expansion of antigen-specific founder B cells and form
reactive follicles. The B-lymphocytes in these follicles proliferate
extremely rapidly, and many of them undergo apoptosis. Histo-
log ically, reactive follicles typically are surround the by a thin cap-
sule of connective tissue, and the activated B-lymphocytes in them
are large r than nai've B-lymphocytes. In H&E-stained histologic
sections, the reactive follicles in chickens are composed mostly
of large lymphoblast-like cells . Mitotic fi gures and apoptosis are
common in these highly reactive follicles. The light central zo ne
of centerocytes and dark peripheral zone of centroblasts described
in the germinal centers of mammals are difficult to discern in birds.
Activated B-cells exit the germinal centers into the plasma cell or
the memory B-cell fate. Numerous plasma cells may be seen in
reactive spleens . Plasma cells are short-lived in the spleen, but
some plasma cells migrate from the spleen to bone marrow where
the majority enter a long-lived population of plasma cells for long-
lasting antibody production.
Lymphoid Depletion (Atrophy)
Most, if not all diseases, including nutritional deficiencies and tox-
icities, can result in bursa! atrophy and lymphoid depletion, but gen-
erally the atrophy is not as diffuse as that associated with infectious
bursa! disease or Marek's disease. Nutritional and toxic causes of
bursa! atrophy include, but are not limited to: Vitamin A deficiency,
selenium deficiency, vitamin E deficiency, zinc deficiency, aflatox-
ins, citrinin, cyclopiazonic acid, fumoni sin BI , ochratoxin, rubra-
toxin, trichothecenes, and zeara lenone. Vitamin A deficiency can
cause squamous metaplasia of the epithelium of the plicae of the
BF, and this may be accompanied by an accumulation of caseous
material in the bursa! lumen. Non-specific bursa! atrophy and lym-
phoid depletion may be associated with many different infections
and stress conditions.
Amyloidosis
Accumulation of amorphous, fibrillar eosinophilic material that
distorts the splenic architecture is characteristic of amyloidosis.
Amyloid is more common in waterfowl but can occur in cluonic
infectious diseases in any avian species. Deposition of amyloid may
involve primarily the wall of branches of splenic arteries. Amyloid
must be distinguished from fibrin , and the Congo red stain followed
by examination under polarized light is recommended.
Hemosiderin Pigment and Erythrophagocytosis
Accumulation of hemosiderin pigment in the cytoplasm of many
macrophages in the spleen can result from excessive destruction
of erythrocytes from any cause and in hemosiderosis. Erythro-
phagocytosis in the spleen is characterized by the presence of
erythrocytes at various stages of degradation in the cytoplasm of
macrophages in the red pulp. Clumps of pyknotic erythrocytes or,
more commonly, red or reddish brown globules or debris, repre-
senting partially degraded erytluocytes, are seen in the cytoplasm
of numerous macrophages.
Avian Histopathology (4 th Edition) I 19
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
Urate Deposition
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In severe cases of visceral gout, usually secondary to renal failure,
urate crystals are deposited in the spleen, with subsequent injury to
I the splenic tissues. The lesions consists offew or many discrete foci
of severe necrosis, with basophilic material representing remnants
ofurate crystals visible in the center of some necrotic foci.
Infections
Viral infections
The major causes of atrophy of the BF and/or thymus in chickens
is infection with infectious bursa! disease virus (IBDV), chicken
anemia virus (CAY), or Marek's disease virus (MDV). Classical
IBDV causes necrosis ofbursal lymphoid cells with frequent forma-
tion of cystic cavities in the medullae of follicles. Inflammation is
a prominent feature and includes intrafollicular and interfollicular
edema, infiltration of variable numbers of heterophils, and conges-
tion and/or hemorrhage. As the disease progresses, follicles become
atrophied, and fibroplasia and expansion of the interfollicular con-
nective tissue occurs. The mucosa! surface becomes irregular due
to hyperplasia of epithelial cells and info Iding of the epithelial layer.
Variant strains ofIBDV cause lymphoid necrosis and bursa! atrophy
without inflammation and without the more diffuse and acute necro-
sis seen in the classical form ofIBD. Virulent strains of IBDV also
cause hemorrhage in the bone marrow and thymus, in addition to the
necrosis of lymphoid cells.
Chicken anemia virus results in very severe atrophy of the thy-
mus, in addition to lymphoid depletion in the bursa of Fabricius
and marked hypoplasia of hematopoietic tissue in the bone mar-
row. Lymphoid depletion and hyperplasia of ellipsoidal reticular
cells are seen in the spleens of some birds. Chickens frequently die
from secondary infections, especially adenoviral hepatitis, follow-
ing CAY infection. In the thymus, there is a major loss of lymphoid
cells, beginning with the outer cortical thymocytes and proceeding
to involve the cortex and then the medulla. Inflammation is absent.
Thymus lobules become severely atrophied, and there is loss of zon-
al architecture with absence of a distinct demarcation between the
cortex and the medulla. CAY produces a protein (VP3 or apoptin)
that induces apoptosis, and it is this apoptotic mechanism of de-
struction of thymocytes that likely explains the lymphoid depletion
in the absence of significant inflammation . CAY in experimental
infections rarely damages bursa! lymphocytes, so bursa! atrophy in
field cases of CAY is likely due to secondary rather than to direct
CAY effects. CAY produces small eosinophilic intranuclear inclu-
sion bodies, first in infected cells of the outer thymic cortex. Small
eosinophilic intranuclear inclusions may also be found in the bone
marrow, the lymphohistiocytic cells in the lamina propria of the pro-
ventriculus, intestine, and in other organs including kidney, lung,
and heart. These intranuclear inclusions are transitory, being found
during the first 10 days following experimental infection with CAY,
thus have not been relied upon in the diagnosis of field cases of
CAY. These inclusions are found in cells with enlarged nuclei; and
careful examination of the lymphoid cell populations in the lamina
propria of the intestine and in the kidneys and lung, in addition to
the thymus and spleen, is required to find the inclusion bodies. CAY
infects and kills hemocytoblasts in the bone marrow resulting in a
20 I American Association of Avian Pathologists
severe depletion of both erythroid and myeloid cell populations.
Anemia is severe and loss of thrombocytes leads to frequent bleed-
ing (blue wing syndrome).
Marek's disease virus can cause bursa! atrophy resembling that
seen in IBO, but the presence of diffuse inflammatory lesions sup-
ports a diagnosis of infection with classis IBDY. The presence of
histopathological lesions suggestive of MD in other organs will be
very helpful to determine whether the bursa! atrophy is caused by
MDV or variant strains of IBDY.
Bursa! lesions in pigeons infected with circovirus include lym-
pholysis, loss of lymphoid cells, and cystic cavitation of follicles,
with formation of fluid-filled cysts. A diagnostic lesion is the pres-
ence variable numbers of darkly basophilic botryoid inclusion bod-
ies in the cytoplasm of follicular macrophages and epithelial cells at
the cortico-medullary border. In some cases, there is minimal dam-
age to lymphoid follicles with few or several typical intracytoplas-
mic circovirus inclusions in lymphoid follicles. The large circovirus
inclusions may totally obscure the cell outline.
Other viral infections that cause necrosis of bursa! lymphoid
cells and depletion of lymphocytes in the spleen and other organs
include reovirus infection, velogenic viscerotropic Newcastle dis-
ease, avian influenza, and duck virus enteritis that causes intranu-
clear inclusions in bursa! macrophages. Vaccination of chickens
with a virulent laryngotracheitis (LT) virus applied to the vent, an
older method of immunization, can cause necrosis in the BF with
the formation of syncytial cells containing intranuclear inclusions
in the mucosa! epithelium and in medulla (likely in epithelial cells
separating medulla from cortex) of follicles. Pet birds infected with
polyomavirus may have bursa! lesions characterized by widespread
karyopyknosis of lymphoid cell, with some follicles are severely
depleted of lymphoid cells and have several reticular epithelial cells
with typical polyomavirus intranuclear inclusion bodies.
Viral infections may cause generalized depletion of lymphoid
cells with or without necrotic foci or widespread of individual cell
necrosis. Variable numbers of apoptotic lymphoid cells with pyk-
notic nuclei are expected in the BF, thymus, spleen, and dispersed
lymphoid cell collections. Apoptosis may be accelerated or stimu-
lated by some viral infections, CAY being a classic example, so that
loss of lymphoid cells is caused by an indirect mechanism rather
than direct viral injury leading to cell death. In well preserved
splenic tissue, the presence of many necrotic lymphoid cells and/or
necrotic foci should arouse suspicion of an infectious process.
Bacterial infections
Bacterial infections in the BF can result in focal areas of caseous ne-
crosis replacing one or more lymphoid follicles. In severe bacterial
infection, the bursa I lumen can become filled with a core of caseous
necrotic material. In some cases of necrotic enteritis, C/ostridiw11
pe1:fringens colonize the mucosa! surface ofplicae and cause severe
necrosis of the lining epithelium, with extension of the infection to
lymphoid follicles in severe cases, resulting in necrosis of the fol-
licles and disruption of interfollicular tissues by edema and inflam-
matory exudate. Few or several plicae may be affected.
Lesions usually found in the spleens of birds with bacterial sep-
ticemia are multiple discrete or confluent foci of necrosis and/or of

acc umulations of amorphous, fibrin-like material of varying density.
The term "fibrinoid necrosis" is used to refer to the accumulation of
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such material. Fibrinoid necrosis is often found in the ellipsoids of
th e spleen, and its presence suggests damage to blood vessels with
subsequent leakage of protein-rich fluid into the surrounding tissues.
Clumps of bacteria may or may not be seen, but fibrinoid necrosis is
hi ghly suggestive of bacterial septicemia. With certain septicemic
di seases (e.g. some cases E. coli septicemia), carefol examination of
the spleen is necessary to find few small clumps of bacterial in the
parenchyma. Vascular thrombosis and diffuse hemorrhages in the
spleen are other features of bacterial septicemia. The entire spleen
may be necrotic and/or hemorrhagic in some septicemic diseases.
F ibrin may accumulate on the capsule of the spleen (fibrinous splen-
ic serositis) and is a common feature in colibacillosis. Bacterial tox-
ins produced by Clostridi11111 spp., gangrenous dermatitis being an
example, cause lymphoid cell depletion and fibrinoid necrosis in the
ellipsoids. Depletion of lymphoid cells with hyperplasia of reticular
cells of the ellipsoids are lesions found in grossly enlarged spleens
of few-day-old chicks with E. coli septicemia. Splenic granulocy-
tosis (increase in number of granulocytic leukocytes) may be seen
in inflammatory conditions involving other organs and tissues. The
presence of aggregates of macrophages or histiocytes with granu-
lar, faintly eosinophilic cytoplasm should arouse suspicion of my-
cobacteriosis. Acid-fast staining reveals many acid-fast bacteria in
the cytoplasm of macrophages or histiocytes. These macrophage-
histiocyte nodules may be mistaken for neoplasia. Histiocytosis of
the white pulp or diffuse plasmacytosis occurs in the spleens of birds
infected with Chlamydia psittaci. Organisms, usually few, are seen
as basophilic smudges in the cytoplasm of macrophages.
Protozoa/ i11fectio11s
In Leucocy tozoon infections, numerous parasites (megaloschizonts)
may be found in the spleen, and their presence is accompanied by
reticular cell hyperplasia . Intracellular accumulation of hemosid-
erin pigment is prominent due to destruction of erythrocytes. With
systemic toxoplasmosis, tissue cysts may be found in the spleen.
Diffuse increase in number of plasma cells, macrophages, and lym-
phoblasts, with increase in erythrophagocytosis are found in the
spleens of birds infected with Sarcocystis falcatula. Merozoites of
A toxoplasma organisms are seen as groups of tiny, round basophilic
bodies in the cytoplasm of macrophages.
Cryptosporidia and coccidia that infect the lower intestinal
tract, ceca, or cloaca also may be found in the epithelial cells of the
bursa of Fabricius. Occasional stages of cecal coccidia of chick-
ens (Eimeria tenella) and pheasants (Eimeria colchici) develop in
the mucosa! epithelium of the bursa. Cryptosporidia are often nu-
merous, especially if there is concurrent immunosuppression from
infectious bursa! disease or chicken anemia virus infection. Para-
sites appear as 2-5 mm basophilic spherical bodies or clear, round
to slightly ovoid larger "ring shapes" that are closely associated
with the apical surface of mucosa! epithelial cells. Organisms may
appear to protrude or bulge from the cell surface. OJ,plosporidi-
11111 develop within the cell membrane and are intracellular but ex-
tracytoplasmic. Epithelial hyperplasia, hypertrophy, degeneration,
epithelial cell sloughing, heterophil infiltrates, and irregularity of
Lymphoid System
the surface epithelium are seen in cryptosporidiosis. Infrequently,
a core of inflammatory exudate develops within the bursa in heavy
infections. OJ,ptosporidi11111 baileyi is the most frequent cause of
I
bursa! cryptosporidiosis. It infects chickens, turkeys, quail, ducks,
and geese. Parasites consistent with C. meleagridis infect the bursa
of turkeys and quail. Heavy bursa! infections can impair immune
responses to vaccines .
Neoplasia
Neoplasia involving the various cell populations of the lymphoid
system is a major diagnostic challenge. The avian retroviruses
cause a variety of morphologic types of tumors including lymphoid
leukosis, erythroblastosis, myeloblastosis, myelocytomatosis, fibro-
sarcomas, myxomatous sarcomas, and hemangiomas.
Lymphoid leukosis (LL) originates in the BF and is a tumor of
B-lymphocytes. Within involved organs, including the spleen, LL
tumors have a nodular pattern and they grow by expansion. The
tumor nodules are composed of a relatively uniform population of
lymphoid cells. LL tumors in the BF are located within the follicles
(intrafollicular) although, if large, the follicles and interfollicular
tissue are effaced by tumor cells, thus making the bursa! origin of
cells difficult or impossible to discern. Differentiation of lymphoid
leukosis from the lymphoid cell tumors of Marek's disease (MD)
is a continuing challenge at the level of light microscopy. Find-
ings of lymphoid cell infiltrations in peripheral nerves, iris and/or
brain support a diagnosis of MD. Marek's disease is the primary
rule out when histopathologic examination of an enlarged spleen
reveals that the enlargement is caused primarily by expansion of
the periaiteriolar lymphoid sheath region by lymphocytes. Cells in
MD tumors are small to medium lymphocytes, lymphoblasts, and
reticular cells and these neoplastic cells infiltrate tissues rather than
grow by expansion. Neoplastic involvement of the BF in MD is not
always present, but when found has a characteristic interfollicular
infiltration of lymphoid cells. As mentioned earlier, bursa! atrophy
is a common lesion caused by MDV. Myelocytomas are diagnosed
by the presence of eosinophilic granules in the cytoplasm of the tu-
mor cells.
Reticuloendotheliosis virus (REV) causes lymphoid neoplasia
in chickens, turkeys, and other avian species including ducks, quail,
pheasants, geese, peafowl, and prairie chickens. REV can cause
runting and stunting when vaccines contaminated with REV are
given to young chickens. REV also can cause bursa! lymphomas
composed of a uniform population of lymphoblasts that are indis-
tinguishable from LL tumors in chickens. REV also may cause in
chickens nonbursal lymphomas located in the thymus and spleen as
well as in the liver. These nonbursal lymphomas are composed of a
population of immature lymphoreticular cells. They are usually not
uniform so can be confosed with MDV. REV lymphomas in turkeys
are characterized by a relatively uniform population of lymphore-
ticular cells in the neoplastic nodules found in the spleen, liver, in-
testine, and other organs. In the runting and stunting syndrome as
well as some of the lymphomas, peripheral nerve lesions character-
ized by infiltration oflymphocytes and plasma cells may be present.
Lymphoproliferative disease of turkeys is characterized by
marked enlargement of the spleen due to proliferation of pleomor-
Avian Histopathology (4 th Edition) I 21
 Tahseen Abdul-Aziz • Oscar J. Fletcher
phic mononuclear cells. The tumors are composed of lymphocytes,
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lymphoblasts, plasma cells, and macrophages . Nerve lesions re-
sembling those seen in MD may be found .
Multicentric histiocytosis is characterized by proliferation of
spindle-shaped cells having abundant eosinophilic cytoplasm and
located in the periarteriolar lymphoid sheaths of the spleen. There is
marked expansion of the periarteriolar lymphoid sheaths that results
in a nodular pattern seen both grossly and microscopically. Similar
nodules composed of histiocytic cells can be found also in the liver
and kidneys. Multicentric histiocytosis is likely the same condition
as spindle-ce ll proliferative disease.
Metastatic tumors may be found implanted on the capsule of
the spleen, but they may also infiltrate the capsule. In poultry, ad-
enocarcinomas of reproductive tract (ovary, oviduct) or the pancreas
the most common tumor that metastasizes to the sp leen by intracoe-
lomic implantation.
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Histology, 3rd ed. Wiley-Blackwell : Chicester, W. Sussex. 342
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and plasma cells in paraocular and paranasal organ systems in
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Cheville, N . F. 1967. Studies on the pathogenesis ofGumboro
disease in the bursa of Fabricius, spleen, and thymus of the
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and bursa! lymphoid systems in avian tuberculosis. A111 J
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Cheville, N. F. and C. W. Beard. 1972. Cytopathology of
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lymphoid systems in the chicken. Lab invest 27: 129-143.
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in turkeys (Meleagris ga //opavo) with respiratory disease and
colisepticemia . Vet Pathol 14:567-581.
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ofbursal atrophy with infectious bursa! disease viruses. Vet
Pathol 15: 376-3 82 .
22 I American Association of Avian Pathologists
Chevi lle, N. F. 1979. Environmenta l factors affecting the immune
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John, J. L. 1994. The avian spleen: A neglected organ. Quart R e v
Biol 69:327-351.
Jones, Y. L. and D. E. Swayne. 2004. Comparative pathobiology
of low and high pathogenicity H7N3 Chi lean avian influenza
viruses in chickens. Avian Dis 48 : 119-128.
Nagy, N. , E. Bfr6, A, Takacs. M. Polos, A. Magyar, and I. Olah.
2005 . Peripheral blood fibrocytes contribute to the formation of
the avian spleen. D e vel Dynamics 232:55-66.
Nagy, N., B. Igyart6, A. Magyar, E. Gazdag, V. Palya, and I. Olah.
et al. 2005. Oesophageal tonsil of the chicken. Acta Vet Hung
53: 173-188.
Nair, V. and A. M. Fadly.2013. Leukosis/sarcoma group. In: D. E.
Swayne, J. R. Glisson, L. R. McDougald, L. K. Nolan, D. L.
Suarez, and V. Nair (eds .). Diseases of Po11lflJ 1, 13th ed. Wiley-
Blackwell: Ames, IA. 553-592, 644-661.
Nai r, V., G. Zavala, and A. M. Fadly. 2013 . Reticuloendotheliosis.
In: D. E. Swayne, J. R. Glisson, L. R. McDougalcl, L. K.
Nolan, D. L. Suarez, and V. Nair (eds). Diseases of Po11lflJ',
13th ed. Wiley-Blackwell: Ames, IA. 593-604, 661-669.
Nakamura, K. K. Waseda, Y. Yamamoto, M. Yamada, M.
Nakazawa, E. Hata, T. Terazaki , A. Enya, T. Imada, and K.
Imai. 2006 . Pathology of cutaneous fowl pox with amy loidosis
in layer hens inoculated with fowlpox vaccine. Avian Dis
50: 152-156.
Payne, L. N. and P. C. Powell. 1984 . The lymphoid system. In: B.
M. Freeman (eel.) Physiology and Bioche111isflJ' of the Domestic
Fowl. Academic Press, London. 277-321 .
Pope, C. R. 1991. Pathology of lymphoid organs with emphas is on
immunosuppression. Vet !111111111101 & /mm11nopathol 30:31-44.
Pope, C.R. 1996. Lymphoid system . In: C. Riddell (ed.) Avian
His topathology, 2nd ed. AAAP, New Bolton Center.17-44.
Press, C. M. and T. Landsvak. 2006 . The lymphoid system. In: J.
A. Eure II and L. Brain (eds .) D ellmann :S· Textbook of Veterina, y
Histology. Blackwell Publi shing: Ames, lA. 134-152.

Rose, M . E. 1981. Lymphatic system. In: A. S. Kin g and J.
McLelland (eds) Form and Function in Birds, Vol. 2. Academic
VetBooks.ir
Press : New York, NY. 34 1-3 84.
Sarver, C . F., T. Y. Morishita, and B. Mersessian. 2005. The effect
of route of inoculation and challenge dosage on Rie111ere /la
anatipestifer infection in Pekin ducks (Anas platyrhynchos).
Avian Dis 49: I 04-107 .
Schat, K. A. and V. Nair. 2013. Marek 's disease. In : D. E. Swayne,
J. R. Glisson, L. R. McDougald, L. K . Nolan, D. L. Suarez, and
V. Nair (eds). Diseases of Pou!IIJ', 13th ed. Wiley-Blackwell:
Ames, IA. 515-552, 623-664.
Smyth, J. , D . Moffett, R . T. Conno, and M. McNulty. 2006 .
Chicken anaemia virus inoculated by the oral route causes
lymphocyte depletion in the th ymus in 3-week-old and 6-week-
old chickens. Avian Pathol 35 :254-259.
Smyth, J. , D. A. Moffett, M . S. McNulty, D. Todd, and
D. P. Mackle. 1993. A sequential histopathologic and
irnmunocytochemical study of chicken anemia virus infection
at one day of age. Avian Dis 37:324-338.
lymphoid System
Smyth, J. , D. Soike, D. Moffett, J. H . Westo n, and D. Todd . 2005.
Circovirus-infected geese studied by in situ hybridization .
Avian Pathol 34:227-232.
I
Swayne, D. E. 1997. Pathobiology of H5N2 Mex ican avian
influen za virus infection of chickens. Vet Pathol 34:557-567 .
Talami , S., M. Goryo, T. Masegi, and K. Okada. 2004 .
Histopathological characteristics of spindle cell proliferative
disease in broiler chickens and its experimental reproducti on in
specific pathogen-free chickens. J Vet Med Sci 66:231-235.
Taylor, M .A., J. Catchpole, R. N. Marshall, and J. A. Green.
1996. The pathogenesis of experimental infections of
CiJ1ptosporidi11111 bailey i in chickens. J Protozoa/ Res 6: I- I 2.
Van Santen, V. L. , K . S. Joiner, C. Murray, N. Petrenko, F. J.
Hoerr, and H . Toro. 2004. Pathogenesis of chicken anemi a
virus: Comparison of the oral and the intramuscular routes of
infection. Avian Dis 48:494-504.
Williams, A. E. and T. F. Davison. 2005 . Enhanced
immunopathology induced by ve1y virulent infectious bursa (
disease virus. Avian Pathol 34:4- I 4.
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2.1. Bursa of Fabricius. Normal. 3-week-old. Typical fold or
plica is covered with epithelium and contains numerous lymphoid
follicles separated by thin bands of fibrous connective tissue.
2.2. Bursa of Fabricius. Normal. 3-week-old. The plicae are
covered with non-ciliated pseudostratified columnar epithelium.
Note the relative proportions of the outer, darkly stained cortex
and the inner medulla in the follicles. The thin bands of connective
tissue between the follicles are the interfollicular connective ti ssue.
24 J American Association of Avian Pathologists
2.3. Bursa of Fabricius. Normal. 21-day-old turkey. The
arrows identify the focal and highly specialized epithelium that caps
follicles and has pinocytotic activity important in the presentation
of antigenic material to lymphoid cells. Note that the cap is in direct
contact with the medulla . The insert is higher magnifi ca tion of the
specialized epithelium.
2.4. Bursa of Fabricius. Normal. 3-month-old backyard
chicken. Lymphoid follicle shows the cortex (C), medulla (M), and
cortico-medullaiy border (arrow). Note the blood capillaries in the
cortico-medullary border. Blood capillaries are also present in the
cortex but not in the medulla.

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2.5. Bursa of Fabricius. Normal. Chicken.
Jmmunohistochemical staining of section of bursa for PAX5, a
marker for B-lymphocytes, shows that the follicular lymphoid cell
pop ul ation is composed of B-lymphocytes.
2.6. Thymus. Normal. 60-day-old broiler. The thymus is
enclosed by connective tissue capsule. Septa from the capsule
incompletely divide the cortex and end at the cortico-medullary
junction. The dense lymphocyte population gives the cortex deep
basophilic staining in histologi cal sections. The large numbers
of epithelial cells and the smaller numbers of lymphocytes in the
medullae result in less basophilic staining.
Lymphoid System
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2.7. Thymus. Normal. Hassall's corpuscle. 60-day-old
broiler. Low-power view showing Hassall 's corpuscles consisting
of aggregates of large epithelial cells with abundant, lightl y
eosinophilic cytoplasm. Heterophils are present in some corpuscles.
2.8. Thymus. Normal. Hassall's corpuscle. 60-day-old
broiler. Hassall 's corpuscle consists of aggregate of large epithelial
cells with abundant, lightly eosinophilic cytoplasm. It is possible
that these cells are undergoing degeneration. Note the heterophils
in the corpuscle and the extravasated red blood cells in the medulla.
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2.9. Thymus. Normal. Hassall 's corpuscle. 60-day-old broiler. 2. 11. Thymus. Normal. 60-day-old broiler. Tiny masses of
Hassall 's corpuscle consisting of aggregate oflarge epithelial cells . eosi nophilic material in the medull a. These masses likely represent
Within the corpuscle are vac uoles conta ining necrotic granul ocyti c remnants of epithelial cells that underwent necrosis and lost their
leuk ocytes. nuclei. Note the nuc leus in one of the cell s (arrow).

2.10. Thymus. Normal. Hassa ll 's corpuscle. 4-month-old swan. 2.12 . Spleen. Normal. Arteriole with periarteriolar lymphoid
Hassall 's corpuscle co nsi sts of concentrically arranged epithelial sheath (PALS). Adult hen. Arteriole is surrounded by a sheath of
cells that are undergo ing cornification. T-lymphocytes that constitute the PALS. Note the prominent layer
of circular smooth muscle in th e wall of the a1teriole.

26 I Ameri can Association of Av ian Pathologists


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2.13. Spleen. Normal. 21-day-old chicken. Two arterioles
(arrows) are surrounded by a diffuse population of T-lymphocytes
that form the periarteriolar lymphoid sheath. There is a lso a
lymphoid fo llicle co mposed of B-lymphocytes (bursa-dependent
lymphoid follicle).
2.14. Spleen. Normal. 23-day-old chicken. Arteriole is
surrounded by lymphoid sheath of T-lymphocytes (periarteriolar
lymphoid sheath), with adjacent bursa-dependent lymphoid follicle
composed of B-lymphocytes. Two sheathed capillaries are in the
upper left.
Lymphoid System
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2.15. Spleen. Normal. 23-day-old chicken. Higher-power view
of the bursa-dependent lymphoid follicle within periarteriolar
lymphoid sheath. Note the very thin capsule aro und the follicle.
2.16. Spleen. Normal. Adult white leghorn hen. Ellipsoids.
Group of penicilliform capillaries are surrounded by eosinophilic
sheaths of large reticul ar cells. The sheath is known as the
ellipsoid or Schwei gger-Seidel sheath , and the reticular cells are
ca lled ellipsoidal reticular cells. Note the ring of B-lymphocytes
(periellipsoid lymphocyte sheath or PELS) around the ellipsoids. An
arteriole with prominent smooth muscle is in the lower ri ght corner.
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2.17. Spleen. Normal. Six-week-old turkey. Ellipsoids. Group
of penicilliform capillaries are surrounded by eosinophilic sheaths
of large reticular cells. The sheath is known as the ellipsoid
or Schweigger-Seidel sheath, and the reticular cells are called
ellipsoidal reticular cells. Note the ring of B-lymphocytes around
the ellipsoids (periellipsoid lymphocyte sheath).
2.18. Spleen. Normal. Six-week-old turkey. Ellipsoids. Higher-
power view of penicilliform capillaries. The capillaries have
plump endothelial cells and are surrounded by a thin sheath of
lightly stained reticular cells (thus called sheathed capillaries) with
prominent nuclei.
28 I American Association of Avian Pathologists
2.19. Reactive spleen. 13-week-old turkey. Several reactive
follicles (germinal centers) are present tlU'oughout this spleen.
Spleen with many lymphoid follicle is termed reactive spleen, and
the response is not disease-specific.
2.20. Spleen. Reactive lymphoid follicles. 13-week-old turkey
hen . Shown are two lymphoid follicles (germinal centers) consisting
of nodular collection of large lymphoblast-like cells surrounded by
thin c01mective tissue capsule. Reactive lymphoid follicles develop
in spleens and other secondary lymphoid tissues as a result antigenic
stimulation due to infection or following immunization.

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2.2 1. Spleen. Reactive lymphoid follicles. 13-week-old turkey
hen. Higher-power view of lympho id follicle (germinal center) with
connective tissue capsule enclosing large lymphoblast-like cells.
2.22. Spleen. Reactive lymphoid follicle. 13-week-old turkey.
Bursa-dependent follicle is encapsulated and consists mostly oflarge
B-lymphocytes (larger than naYve B-lymphocytes). An a1teriole and
a sheathed capillary are adjacent to the follicle. There is also splenic
plasmacytos is (note the numerous plasma cells aro und the follicle).
The large numbers of plasma cells indicate response to antigenic
sti mul at ion.
Lymphoid System
I
2.23. Spleen. Reactive lymphoid follicles. 21-day-old broiler.
Four encapsulated lymphoid follicles (germinal centers) are
assoc iated with an a1teriole. This response pattern is consistent with
reactive spleen. Reticular cells are prominent around penicilliform
capi llaries (sheathed capillaries).
2.24. Spleen. Reactive lymphoid follicle (germinal center).
21-day-old broiler. Higher-power view of reactive lymphoid
fo llicle. The follicle is encapsulated and consists of large
B-lymphocytes. The granular materials within vacuolar spaces are
debris of apoptotic cells. The B-lymphocytes in reactive follicles
proliferate extremely rapidly, and many of them undergo apoptosis.
Mitotic figures are usuall y seen. Several reactive follicles were
present in this spleen.
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2.25. Spleen. Reactive lymphoid follicle (germinal center). 2.27. Lung. Bronchus-associated lymphoid tissue. 18-day-old
2 1-day-old broiler. Same spleen as 2.24 . Hi gher-power view of turkey. Multiple nodul ar collections of lymphoid cells are in the
germinal center (see the legend of2.24) . mucosa I lamina propria of a seco ndary bronchus.

.., ,. ,.

2.26. Lower eyelid. Conjunctiva-associated lymphoid tissues 2.28. Lung. Bronchus-associated lymphoid tissue. 5-week-old
(CALT). 60-day-old broiler. The CALT is located beneath the turkey. Multiple nodul ar co ll ecti ons of lymphoid cells are in the
conjunctiva ! epithelium and consists of lymphoid fo llic les and mucosa! lamina propria of a seco nd ary bronchus.
diffuse population of lympho id cells.

30 I American Association of Avian Pathologists

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2.29. Esophageal tonsil. 3-month-old backyard chicken. 2.31. Duodenum. Peyer's patch. Turkey. Nodular and diffuse
Esophageal tonsil is a collection of diffuse and nodular lymphoid collections of lymphoid cells are in the lamina propria of villi. This
tissue located in the lamina propria of the esophagus at the is example of gut-associated lymphoid ti ssue (GALT).
junction with the proventriculus. It consists of lymphoid follicles
of B-lymphocytes. Between the follicles is diffuse population
co mposed mostly ofT-lymphocytes.

'l

,., .:}

' ... ,·
'; .~g_)

2.30. Esophageal tonsil. 3-month-old backyard chicken.
lmmunohistochemical staining for PAX5 , a marker for
B-lymphocytes, shows that the lymphoid follicles in the esophageal
tonsil are composed of large numbers of B-lymphocytes. Non-
staining cells in the diffuse population are T-lymphocytes.
2.32. Cecal tonsil. 4-month-old chicken. The cecal tonsil,
located at the junction with the small intestine, consists of diffuse
and nodular collections of lymphocytes.

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2.33. Meckel's diverticulum. 18-week-old turkey. The structure
shown in thi s image is Meckel 's diverticulurn, a remnant of the yolk
sac. Nodular and diffuse collections oflymphoid cells are prominent
in the wall of the diverticulurn. The amount of lymphoid tissue
easily could be interpreted as lymphoid hyperplasia, but probably
is within normal limits.
2.34. Liver. Ectopic lymphoid tissue. Hen. Encapsulated
lymphoid nodule is associated with the wall of blood vessels. This is
an example of scattered nodular aggregates (ectopic lymphoid foci)
normally found in visceral organs.
32 J American Association of Avian Patholog ists
2.35. Pancreas. Ectopic lymphoid tissue. Turkey. Two
encapsulated lymphoid nodules are in the pancreas. This is another
example of scattered nodular aggregates (ectopic lymphoid foci)
found in some organs.
2.36. Proventriculus. Ectopic lymphoid tissue. Chicken . Two
encapsulated lymphoid nodules are in the proventricular gland .
This is another example of scattered nodular aggregates (ectopic
lymphoid foci) found normally in some organs.

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2.37. Bone marrow. Ectopic lymphoid tissue. 3-week-old
broiler. One large and one small lymphoid nodules surrounded by
hematopoietic cells are in the bone marrow. This is an example of
ectopic lymphoid tissue considered to be normal.
2.38. Mural lymphoid aggregate. Normal. 5-week-old broiler.
Aggregate of lymphoid cells is associated with the wall oflymphatic
vessel adjacent to the pancreas. These aggregates are associated
with the walls of deep lymphatic vessels and are often overlooked.
lymphoid System
I
2.39. Mural lymphoid aggregate. Normal. One-year-old
backyard chicken. Lymphoid tissue is associated with the wall of
a deep lymphatic vessel that courses with deep femoral vein. This
tissue was incidentally found when the sciatic nerve was collected
for histopathology.
2.40. Avian lymph node. Normal. Goose. The avian lymph node
(found in ducks, geese, and swans) consists of cords and sinuses.
The cords are populated with lymphocytes and some plasma cells
and macrophages. The sinuses contain macrophages, red blood
cells, and some lymphocytes.
Avian Histopathology (4 1" Edition) I 33
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2.41. Avian lymph node. Normal. Goose. Hi gher magnification
of2.40. Shown are cords and sinuses of the lymph node. The sinuses
are lined by endothelial cells. Note th e macrophages with vacuolated
cytop lasm in the lumen of the sinuses.
2.42. Avian lymph node. Normal. Goose. Higher magnification
of2.41. Within the lumen ofa sinus are macrophages with vacuolated
cytoplasm, red blood cells, and few lymph ocytes.
34 I Ame ri ca n Association of Avian Pathologists
2.43. Harderian gland. Normal. Chicken. The Harderian g la nd
is a periocular gland that lies on the bulbus, near the temporal ang le
of the eye. It is a serous g la nd of the multilobulated tubuloalveol a r
type. The g land is surro unded by capsule , and septa from the ca psul e
divide the gland into lobules. The physiological function of gland
inc ludes lubrication of the ni ct itat ing membrane and secreti on of
immunog lobulins for local immunity.
2.44. Harderian gland. Normal. 4-month-old backyard
chicken. Two lobules of Harderian g land are shown. Individual
tubuloalveolar glands are se parated by very delicate stroma a nd are
lined by a single layer of secretory, hi g h columnar epithelial cells.
Coll ection s of plasma cells are fo und in the interstitium of the gland.
Few plasma cells are al so found between individual g lands.

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2.45. Harderian gland. Normal. 4-month-old backyard
chicken. High-power view showing the dense population of plasma
ce ll s between the tubuloalveol ar glands.
2.46. Bursa of Fabricius. Non-specific atrophy. 42-day-old
broiler breeder pullets. At thi s magnification, atrophy of all the
follicles within the plicae is seen. Bursa[ atrophy generally is not
specific lesion. Jhis bird was affec ted with severe coccidiosis.
lymphoid System
I
2.47. Bursa of Fabrics. Non-specific atrophy. 41-day-old
broiler. See the legend of2.48.
2.48. Bursa of Fabricius. Non-specific atrophy. 41-day-old
broiler. This legend is also applied to 2.47. In this atrophied plica,
there is loss of lymphoid follicles, in-folding of surface epithelium,
intraepithelial cysts, and increase in the interfolli cular fibrous ti ss ue.
The remaining follicles are depl eted of lymphoid cells and their
medullas have a vacuolated appeara nce.
Avian Histopathology (4 11, Edition) I 35
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2.49. Bursa of Fabriciu s. Non-specific atrophy. 41-day-old 2.51. Bursa of Fabricius. Non-specific atrophy. 42-day-olcl
broiler. Higher-power view of two follicles that are depleted of broiler breeder pullet. Illustrated is early infolding of the surface
lymphoid cells in both the cortexes and medullas. The medullae epithelium into damaged lymphoid follicle.
contain many macrophages with cytoplasm distended with
phagocytized debris . These macrophages give the medullae a
vacuolated appearance at low magnification. Note the prominent
zone of epithelial cells between the cortex and medulla.

2.50. Bursa of Fabricius. Non-specific atrophy. 41-clay- 2.52. Bursa of Fabricius. Non-specific atrophy. 42-day-old
old broiler. When the lymphoid follicles are severely dep leted broiler breeder pullet. Demonstrated is the infolding of the surface
and damaged, the plica collapses and the mucosa! epithelium on epithelium into damaged lymphoid follicle .
the surface starts to infold into the damaged foll icles. Because of
the plane of section, the infolding epithelium appears as ductal
structures w ithin the plica. As seen in this image, these ductal
structures are separated by fibrous connective tissue and lined by
epithelium similar to the epithel ium lining the plica.

36 I American Association of Avian Pathologists


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2.53 . Bursa of Fabricius. Non-specific atrophy. 41-old broiler.
Thi s is a severely atrophied plica in which lymphoid follicles
di sappeared and were replaced by ductal structures separated by
fibrous connective tissue and lined by epithelium similar to the
epithelium on the mucosa) surface of the plica.
2.54. Bursa of Fabricius. Infectious bursal disease. 23-day-
old chicken. Extensive necrosis of follicular lymphoid cells,
inflammation in follicles , and edema with heterophilic infiltrate in
the interfollicular connective tissue are lesions typical of the classical
form of infectious bursa! disease. Initially, some follicles may be
unaffected or only partially involved, but the lesion progresses to
involve all, or most, follicles.
Lymphoid System
I
2.55. Bursa of Fabricius. Infectious bursal disease. 23-day-
old chicken. Higher-power view of a lymphoid follicle in 2.54
illustrating the depletion of lymphoid cells in both cortex and
medulla and the expansion of interfollicular connective tissue by
edema and inflammatory cells.
2.56. Bursa of Fabricius. Infectious bursal disease. 23-day-
old chicken. Cystic space containing proteinaceous fluid is within
a damaged lymphoid follicle. The follicle is severely depleted of
lymphoid cells and contains nuclear debris, many macrophages, and
some heterophils. This is a common lesion in follicles during the
resolution stage following massive destruction of lymphoid cells.
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2.57. Bursa of Fabricius. Infectious bursal disease. 23-day-
old chicken. Expansion of th e interfolli cular spaces by edema and
inflammatory infiltrates of hetero phils and macrophages.
2.58. Bursa of Fabricius. Infectious bursal disease. 3-week-
old broiler. At low magnifi cat ion, th e lymphoid follicles appea r
depleted of lympho id cells, interstitial tissue is expanded, and the
pattern is diffu se.
38 I Amer ica n Association of Avian Pathologists
2.59. Bursa of Fabricius. Infectious bursal disease. 3-week-old
broiler. Another plica from the sa me section as in 2.59 show in g
the diffu se and marked depletio n of lymphoid cells accompanied by
ex pansion of interstitial tissue.
I
.' -
, ·:
\
\, ..
2.60. Bursa of Fabricius. Infectious bursal disease. 3-week-
old broiler. Expa nsion of the interfollicular spaces by edema. The
fo llicul ar cortexes and med ull ae are severely depleted of lymphoid
cells and populated only wi th reti cul ar cells, among which pykno tic
nuclei of necrotic lymphocytes are present. Due to the severe
lymph oid depletion, the zone of the e pithelial cells between the
cortex and medulla is ve ry prominent.

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2.61. Bursa of Fabricius. Infectious bursal disease. 3-week-old
broiler. Higher-power view of the follicle in the upper right corner of
2. 60. There is diffuse loss oflymphoid cells, and the follicle contains
only reticular cells and pyknotic nuclei of necrotic lymphoid cells.
Note the congestion of blood capillaries in the cortex and at the
cortico-medullary border. Due to the severe lymphoid depletion, the
zone of the epithelial cells between the cortex and medulla is very
prominent.
2.62. Bursa of Fabricius. Infectious bursa! disease. 3-week-old
broiler. In some follicles, destruction of the lymphoid cells results in
the formation of a medullary cystic cavity containing proteinaceous
material and necrotic debris.
Lymphoid System
I
2.63. Bursa of Fabricius. Infectious bursal disease. 3-week-old
broiler. Higher-power view of lymphoid follicles showing abundant
karyopyknotic and karyorrhectic debri s of necrotic lymphoid cells
in the cortex and medulla. The total destruction of the lymphoid cells
in the medulla results in the formation of cystic cavity containing
necrotic debris.
2.64. Bursa of Fabricius. Infectious bursa! disease (very
virnlent virns strain). 6-week-olcl table-egg pullets. Low-power
view showing hemorrhage and disruption of lymphoid follicles 111
plicae. (Glass slide cour/e5y of Rocio Crespo).
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2.65. Bursa of Fabricius. Infectious bursal disease (very
virulent virus strain). 6-week-old table-egg pullets. Necrosis of
lymphoid cells in the follicles, leaving necrotic debris, reticular
cells, proteinaceous fluid , and small cysts. lnterfollicular spaces are
expanded by edema and loose inflammatory infiltrate. (Glass Slide
Courtesy ofRocio Crespo).
2.66. Bursa of Fabricius. Infectious bursal disease (very
virulent virus strain). 6-week-old table-egg pullets. See the
legend of2.68.
40 I American Association of Avian Patholog ists
2.67. Bursa of Fabricius. Infectious bursal disease (very
virulent virus strain). 6-week-old table-egg pullets. See the
legend of2.68.
2.68. Bursa of Fabricius. Infectious bursal disease (very
virulent virus strain). 6-week-old table-egg pullets. This
legend is also applied to 2.66 and 2.67. Marked intrafollicular and
interfollicular hemorrhage. Extensive necrosis of follicular lymphoid
cells includes necrotic cells and reticular cells in the medullae.
Pool of proteinaceous material is in some follicles. Expansion of
interfollicular spaces is du e to edema with some inflammatory cells.
{Glass slide courtesy of Rocio Crespo).

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2.69. Bursa of Fabricius. Infectious bursa! disease (very
virulent virus strain). 6-week-old table-egg pullets. Higher-power
view of a lymphoid follicle demonstrating the marked necrosis of
lymphoid cells. The follicle contains necrotic debris and a pool
of proteinaceous fluid. There is marked hemorrhage. The zone of
ep ithelial cells between the cortex and medulla becomes prominent
due to loss of lymphoid cells.
2.70. Bursa of Fabricius. Adenovirus inclusions. 3-week-old
turkey. Adenovirus inclusion bodies are in the plical epithelium
(circles). The insert illustrates the inclusions at higher magnification.
Lymphoid System
I
2.71. Bursa of Fabricius. Chicken infectious anemia. 14-day-
old chicken. Marked loss of lymphocytes in both the cortexes and
medullae of the follicles.
2.72. Bursa of Fabricius. Chicken infectious anemia. 14-day-
old chicken. Higher-power view of lymphoid follicles in figure
2. 71. There is loss oflymphocytes in both the cortexes and medullae.
Many of the remaining lymphocytes have pyknotic nuclei (necrotic/
apoptotic cells). Note the absence of inflammation. The lesion is not
specific for chicken infectious anemia and should be interpreted in
conjunction with the lesions in bone marrow and thymus.
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2.73. Bursa of Fabricius. Chicken infectious anemia. 14-day-
old chicken. Loss of zonal demarcation between the cortex and
medulla due to lymphoid depletion and follicular atrophy. The
dark gr;rnular materials are pyknotic nuclei of necrotic/apoptotic
lymphocytes. The interfollicular spaces are expanded by fibrous
tissue.
2.74. Bursa of Fabricius. Circovirus infection. Pigeon. This
low-power view shows marked atrophy of follicles , with formation
of intrafollicular fluid-filled cystic spaces.
42 I American Association of Avian Pathologists
2.75. Bursa of Fabricius. Circovirus infection. Pigeon. The
follicles are atrophied and depleted of lymphoid cells, and some
of them have cystic spaces filled with proteinaceous fluid. Darkly
basophilic circovirus inclusion bodies are present mostly in epithelial
cells at the co1tico-medullary junction. The insert is higher-power
view of the inclusion bodies.
2. 76. Bursa of Fabricius. Circovirus infection. Pigeon. At
this low magnification, the lymphoid follicles appear depleted of
lymphocytes and contain darkly basophilic material representing
the large intracytoplasmic inclusion bodies of circovirus.

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2.77. Bursa of Fabricius. Circovirus infection. Pigeon.
Lymphoid follicle is almost totally depleted of lymphocytes and
infiltrated with macrophages, many of them have darkly basophilic
inclusion bodies that fill the cytoplasm and obscure the cells.
2.78. Bursa of Fabricius. Circovirus infection. Pigeon. Higher-
power view of lymphoid follicle that is markedly atrophied and
depleted oflymphoid cells and co ntains several circovirus inclusions.
The inclusions of circovirus appear as darkly basophilic bodies
occupying the cytoplasm and obscuring the cell . The inclusions are
likely in epithelial cells at the junction of the med ulla and cortex.
Lymphoid System
I
2.79. Bursa of Fabricius. Circovirus infection. 6.5-month-old
pigeon. Lymphoid follicle shows loss of lymphocytes and large,
deeply basophilic circovirus inclusions that obscure the infected
cells.
2.80. Bursa of Fabricius. Polyomavirus infection. 5-week-old
lovebird. Lymphoid follicle is depleted of lymphocytes and has
many enlarged nuclei (karyomegaly) filled with lightly basophili c
intranuclear inclusion bodies characteristic of pol yomav irus
infection. Nuclear debri s is present in the follicle.
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2.81. Bursa of Fabricius. Polyomavirus infection. 5-week-olcl
lovebird. The co1tex and medulla of a lymphoid follicle is depleted
of lymphocytes. Many intranuclear inclusions characteristic of
polyomavirus infection are present in the medulla. Polyomavirus
inclusion bodies are amphophilic or lightly basophilic, and they
completely fill and enlarge the nuclei. Nuclear debris is present in
the follicle.
2.83. Bursa of Fabricius. 16-clay-olcl broiler with necrotic
enteritis. The mucosa! surface of plica is necrotic and colonized
by numerous rod-shaped bacteria . Line of macrophages separates
the necrotic surface from the underlying submucosal tissues,
which were not infected in this case. The incidence of such bursa!
lesion is unknown as the bursae are not frequently collected for
histopathologic examination from chickens with necrotic enteriti s.

2.82. Bursa of Fabricius. Follicular heterophilic granuloma. 2.84. Bursa of Fabricius. 16-clay-olcl broiler with necrotic
21-clay-olcl broiler. Large focal area of caseous exudate is replacing enteritis. Bursa section stained with Gram stain shows the
a lymphoid follicle in a pattern typical of bacterial etiology. The colonization of the mucosa! surface of plica with Gram-positive,
lesion consists of caseous debris surrounded by a cellular zone rod-shaped bacteria morphologically resembling C!ostridi11111 spp.
of macrophages and heterophils. Bacterial colonies are present
within the caseous debris. This lesion commonly is called bursa!
heterophilic granuloma and there may be multiple such foci within
bursa. The lesion is usually incidental finding and likely represents
ascending infection from the cloaca. The lymphoid follicles around
the lesion appear intact.

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2.85. Bursa of Fabricius. 14-day-old broiler with necrotic
enteritis. The infection with C/ostridi11111 pe1ji'inge11s extends from
the mucosa! surface to the lymphoid follicles, which are necrotic
and ha ve many intralesional bacteria. The interfollicular spaces are
expanded by edema and inflammatory infiltrates.
2.86. Bursa of Fabricius. 14-day-old broiler with necrotic
enteritis. Gram stain shows numerous Gram-positive bacteria on
the necrotic mucosa! surface and within necrotic lymphoid follicles
in two plicae. The bacteria are rod-shaped and morphologically
resemble Clostridi11111 spp.
Lymphoid System
I
2.87. Bursa of Fabricius. 14-day-old broiler with necrotic
enteritis. Gram stain shows involvement of several plicae . The
mucosa! surface and lymphoid follicles are necrotic and colonized
by numerous rod-shaped, Gram-positive bacteria morphologically
resemble Clostridi11111 spp .
2.88. Bursa of Fabricius. 10-week-old backyard chicken.
Cryptosporidiosis. Many small, round, basophilic bodies
morphologically consistent with C1Jplosporidiu111 spp. are
associated with the surface of the hyperplastic mucosa! epithelium.
Epithelial cells are swollen and have rarefied cytoplasm.
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2.89. Bursa of Fabricius. 10-week-old backyard chicken.
Cryptosporidiosis. Cryptosporidi11111 organisms appear as small,
round , basophilic bodies associated with the surface of the mucosa!
epithelium . CiJ1p/osporidi11111 is intracellular but extra-cytoplasmic
protozoan parasite residing in host-derived parasitophorous vacuo le.
2.90. Bursa of Fabricius. Infection with Eimeria sp. Pheasant.
Developmental stages (three zygotes and one oocyst) of Eimeria
sp. are in mucosa! epithelial cells. This was an incidental finding in
pheasant with severe cecal coccidiosis.
46 I American Association of Avian Pathologists
2.91. Bursa of Fabricius. Infection with Eimeria tenella.
4-week-old backyard chicken. Developmental stages of Eimeria
lenel/a are in mucosa! epithelial cells . This was incidental finding in
this backyard chicken with cecal coccidiosis.
2.92. Bursa of Fabricius. Histomoniasis. 3-week-old broiler
breeder chicken. Histomoniasis. Variable sized regions within
plicae have destruction of bursa! follicles and expansion of
interfollicular tissue. Smaller regions with similar lesions are in two
adjacent plicae. Pale stained cells are Histomonads. Bird also had
cecal histo moniasis.

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2.93. Bursa of Fabricius. Histomoniasis 3-week-old broiler
breeder chicken. Histomoniasis. Higher magnification of 2.92
shows numerous histomonads both free and within the cytoplasm
of macrophages. Histomonads are in the interstitial tissue and some
degenerating bursa! follicles. Heterophils are scattered within the
les ion.
t<
2.94. Bursa of Fabricius. Marek's disease. 13-week-old
backyard chicken. Scanning view of bursa showing expansion ofa
plica by dense infiltrates of lymphoid cells.
Lymphoid System
I
2.95. Bursa of Fabricius. Marek's disease. 13-week-old
backyard chicken. In one plica, there is dense and extensive
interfollicular lymphoid cell infiltrates effacing and replacing
lymphoid follicles . Interfollicular infiltration of lymphoid cells is
characteristic lesion of Marek 's disease.
2.96. Bursa of Fabricius. Marek's disease. 18-week-old
chicken. Lymphoid follicles are replaced by lymphoid tumor
cells. Marek's disease lymphoid cells initially infiltrate and expand
interfollicular tissue with eventual destruction of follicles. The few
remaining follicles are atrophied. Higher power view of the boxed
follicle is shown in 2.97.
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2.97. Bursa of Fabricius. Marek's disease. 18-week-old
chicken. Expansion of the interfollicular interstitium is due to
infiltration by neoplastic lymphoid cells. Few remaining identifiable
follicles are atrophic.
2.99. Bursa of Fabricius. Lymphoid leukosis. 8-month-old
backyard chicken. All the lymphoid follicles in plica are enlarged
due to intrafollicular proliferation of lymphoid cell s.

2.98. Bursa of Fabricius. Lymphoid leukosis. Chicken.
Lymphoid follicle is markedly enlarged due to intrafollicular
proliferation of lymphoid cells (intrafollicular lymphoid tumor).
This is a characteristic lesion of lymphoid leukosis. One or more
follicles may be involved.
2.100. Thymus. Severe atrophy. Chicken. Severe atrophy of the
thymus with no inflammato1y response. The lesion in young chick
shou ld arouse suspicion of chicken infectious anemia.

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2.101. Thymus. Atrophy. Turkey. Cortical width is decreased
giving the appearance of increase in the medulla . These features
indicate thymic atrophy of moderate severity. The changes are not
di sease specific and may represent thymic regression due to age.
Note the scattered clear areas that contain small dark nuclei. This is
characteristic of apoptosis in lymphoid organs.
2.102. Thymus. Atrophy. Turkey. Very few lymphoid cells
remain in this remnant of thymus indicating diffuse, severe thymic
atrophy that could be age related. Thymic (Hassall 's) corpuscles are
prominent in the medulla.
Lymphoid System
I
2.103. Thymus. Chicken infectious anemia. 14-day-old chicken.
Shown is a severely atrophied thymus lobe. The lobules of the
lobe are atrophied, indistinct, and severely depleted of lymphoid
cells. Note the total absence of demarcation between co1texes and
medullae.
2.104. Thymus. Chicken infectious anemia. 14-day-old chicken.
Thymic lobe is severely atrophied and does not show distinct
lobules. The cortexes and medullae are depleted of lymphoid cells
and lack zonal demarcation.
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2.105. Thymus. Chicken infectious anemia. 14-da y-old chicken.
Thymic lobule is severe ly depleted of lymphoid cells and lacks th e
demarcati on between the cortex and medull a. There is hydrop ic
swelling and vacuolati on of th ym ic epithelia l cells, whi ch become
apparent du e to lymph oid depl eti on.
2.107. Thymus. Chicken infectious anemia. 5-week-old chicken.
Necrosis is extensive and acco mpani ed by hemorrhage. Some
thymi c lobules are relative ly norma l. Diffuse atrophy of the bo ne
marrow was another lesion fo und in the chickens from thi s fl ock.

2.106. Thymus. Chicken infectious anemia. 14-day-old chicken. 2.108. Thymus. Chicken infectious anemia. 5-week-old chicken.
The image shows hydro pic swelling of epithelial cell s in the medull a Some lobes are di ffusely affected and hemorrhagic while others are
of a thymi c lobule, which is atrophied and depleted of lympho id relati ve ly un affected.
cell s.

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2.109. Thymus. Chicken infectious anemia. 5-week-old chicken.
Loss of thymic lymphoid cells is diffuse and accompanied by
hemorrhage and fibrosis within the affected lobule as well as on the
capsul e of the thymus. There is no heterophilic infiltration.
2.110. Thymus. Chicken infectious anemia. 4-week-old chicken.
There is diffuse loss of cells in the bone marrow. Several cells have
enlarged nuclei with small intranuclear inclusion (insert).
Lymphoid System
I
2.111. Small Intestine. Chicken infectious anemia. Chicken.
Hyperplasia of the lymphoid tissue is associated with expansion
of the lamina propria. Arrows identify cells with enlarged nuclei,
some of which contain small eosinophilic inclusions characteristic
of infection with chicken anemia virus.
2.112. Small Intestine. Chicken infectious anemia. Chicken.
Higher magnification of 2.111. Arrows identify cells with enlarged
nuclei and small eosinophilic intranuclear inclusions within the
expanded lamina propria of the small intestine.
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2.113. Spleen. Reticular cell hyperplasia. 10-day-old broiler.
Hyperpl as ia of ellipsoidal reticular cells . The bird had bacterial
septicemia ca used by Pseudo111011as aernginosa. The spleen was
grossly enlarged. Enlargement of the spleen due to hyperplas ia of
ellipsoidal reticular cells is seen in some chi ckens with septicemia,
and the lesion is relatively common in young chicks with septicemia
caused by£. coli or Pse11do11101ws aeruginosa.
2.114. Spleen. Reticular cell hyperplasia. 7-day-old broiler
breeder pullets. Marked hyperplasia of ellipsoidal reti cul ar cells
around penicilliform ca pill aries. The lumens of peni cilliform
capillaries can be identified in the centers ofreticular cell collections.
The spleen was gross ly enlarged. The bird had bacterial septicemia
caused by£. coli.
52 I Ameri can Association of Av ian Pathologists
2.115. Spleen. Reticular cell hyperplasia. 44-day-old broiler.
Marked hyperplasia of ellipsoidal reticular cells. The bird was
affected with tenosynovitis caused by reovirus. Although the lesion
seems to be common in chi cken s affected with this di sease, it should
be considered as a non-specific response to infection, and should be
interpreted in co njunction with other lesions.
2.116. Spleen. Lipidosis of ellipsoidal reticular cells. 9-year-old
macaw. Marked deposition of lipid in the cytoplasm of ellipsoidal
reticular cells around the penicilliform capillaries. The cause and
significa nce of thi s lesion was not determined in this case.
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2.117. Spleen. Erythrophagocytosis. 26-month-old backyard
chicken. Small aggregates of erythrocytes are within the cytoplasm
of phagocytes (reticular/histiocytic macrophages). In some areas
onl y shadow of nuclei are seen in phagocytized erythrocytes, while
in other areas, phagocytized erythrocytes lost their nuclei and appear
as red bodies with no nuclei.
I
2.119. Spleen. Erythrophagocytosis. 2-year-old backyard
chicken. This legend is also applied to 2.118. The cytoplasm
of macrophages is distended with brownish, granular debris of
phagocytized, degraded red blood cells . Within macrophages, the
hemoglobin in red blood cells is broken down to globin and heme,
which contains iron that gives the brownish color to the debris and
the positive staining for iron. Extensive splenic erythrophagocytosis
indicates damage and fragility of red blood cells.

2.118. Spleen. Erythrophagocytosis.
chicken. See the legend of2.119.
3-year-old backyard 2.120. Spleen. Erythrophagocytosis. 2-year-old backyard
chicken. The iron in the heme molecules stains positive (blue) for
iron with Prussian blue stain. The intensity and extent of staining
depend on the degree of degradation of red blood cells within
macrophages.

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2.1 21. Spleen. Urate deposition. 10-month-old backyard
chicken. Multiple areas of severe necrosis of the splenic tissue.
Necrotic areas consist of deeply eosinophilic necrotic debri s, with
urate deposits in the ce nter. The necros is is caused by urate crysta ls.
The bird had urolithiasis and severe viscera l urate deposition
(v isceral gout).
2.122. Spleen . Urate deposition. 10-month-old backyard
chicken. Higher-power view showing focal area of severe necrosis
of the splenic tissue. The necrot ic lesion has a center of basophilic
material representing urate crystals.
54 I American Association of Av ian Pathologists
2.123. Spleen. Urate tophi. 8-month-old backyard chicken. Two
urate tophi have centers of feathery-appearing urates surrounded by
zo ne of macrophages, with early formation of multi nucleated giant
cell s.
2.1 24. Spleen. Amyloidosis. 3.5-year-old goose. Hyalinization of
th e walls of penicilliforrn (sheathed) cap illaries and th e ellipso ids
is due to the deposition of amorphous, eosi nophili c, proteinaceous
material characteristic of amy loid protein. Amyloid must be
di stin gui shed from fibrin .

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2.125. Spleen. Amyloidosis. 3.5-year-old goose. Higher
magnification of 2.124. Deposition of eosinophilic, amorphous,
arn yloid-like, proteinaceous material is expanding the walls of small
arterioles.
2.126. Spleen. Amyloidosis. 3.5-year-olcl goose. The deposition
of amyloid in the walls of small arterioles is demonstrated with
Congo red stain, which gives the amyloid orange color. Under
polarized light, Congo red-stained amyloid exhibited apple-green
birefringence considered pathognomonic for amyloid deposits.
Lymphoid System
I
2.127. Spleen. Amyloidosis. 7-week-old duck. Large amounts of
eosinophilic, amorphous material consistent with amyloid protein
efface and replace the splenic tissue. Amyloidosis is common in
waterfowl.
2.128. Spleen. Amyloiclosis. 6-week-old quail. Disruption and
effacement of the ellipsoidal and periellipsoidal white pulp by
amorphous, eosinophilic, proteinaceous material consistent with
amyloid. Note the lumens ofpenicilliform (sheathed) capillaries.
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2.1 29. S pleen. A my loido sis. 6-week-old quail . Same secti on as
2. 128 sta ined w ith Congo red. The stai n gives the proteinaceo us
materia l ora nge o r reddish-ora nge colo r that indicates the amy loid
nature of th e materi al.
2. 130. Spleen. Amyloido sis. 19-we ek-old broiler breeder pullet.
Severe and extensive di srupti o n of the spleni c ti ssue by homogeno us,
eos inophilic materi a l most suggesti ve of amyloid prote in .
56 I Am erica n Assoc iati on of Avia n Pathologists
2.131. Spleen. Amyloido sis. 19-week-old broiler breeder pullets.
Same sec ti on as 2. 130 stained with Congo red. In thi s case, th e
ora nge staining is not stro ng, but ora nge materi al tlu-oughout the
sect io n exhibited weak apple-g reen birefringe nce when vi ewed
under polari zed light.
2.132. Spleen. Am yloiclosis. 17-week-old chukar. D eposits of
hom oge no us, eos inophilic protei naceous mate ri al suggesti ve of
amy lo id protein are around peni cillifo rm capillari es. T he depos it io n
of am yloid was co nfirm ed wi th the Congo red stain.

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2.133. Spleen. Amyloidosis. 17-week-old chukar. Same section
as 2.132 stained with Congo red. The proteinaceous deposits stain
ora nge, but it exhibited weak apple green birefringence when
viewed under polarized light. Avian amyloid does not consistently
di splay apple-green birefringence under polarized light.
2.134. Spleen. Hemorrhagic enteritis. 6-week-old turkey.
Low-power view showing multifocal basophilic stained areas of
expanding white pulp. This multifocal lesion explains the enlarged
and mottling gross appearance of the spleens of turkeys affected
with hemorrhagic enteritis caused by adenovirus.
Lymphoid System
I
2.135. Spleen. Hemorrhagic enteritis. 6-week-old turkey.
Expansion of the while pulp with lymphoid cells. Several cells with
intranuclear inclusions can be seen, even at this magnification.
2.136. Spleen. Hemorrhagic enteritis. 6-week-old turkey.
Higher-power view of 2.135 . The lymphoid cell population
expanding the white pulp consists mostly of large lymphoblast-
like cells . The nuclei of several cells are enlarged and filled with
basophilic inclusions .
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2.137. Spleen. Hemorrhagic enteritis. 6-week-old turkey.
Lymphoblast-like cell s ex pand the white pulp. In two cell s in
the center of the image, the nuclei are enlarged and filled with
homogenous, basophilic inclusions cha racteri stic of aden ov irus.
2.138. Spleen. Duck viral enteritis. Adult Muscovy cluck.
Disruption of the splenic parenchyma by periarteriolar and
pericapillary deposits of fibrin , with areas of hemorrhage.
58 I Ameri can Assoc iation of Avian Pathologists
2.139. Spleen. Duck viral enteritis. Adult Muscovy duck. Marked
peri arteriolar and pericapillary fibrinous deposits. The lesion
indi cates damage to vascular endothelial cell s, with subsequent
leakage of serum proteins.
2.J 40. Spleen. Polyomavirus infection. 5-week-old macaw. There
is marked plas macytosis with many lightly basophilic, homogenous
inclusion bodies fillin g the enlarged nuclei of reticular cells. Clusters
of bacteria also are seen, indicating bacterial septicemia. Secondary
bacterial infection is not uncom mon in birds with polyomavirus
in fec ti on.

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2.141. Spleen. Polyomavirus infection . 6-month-old lovebird.
There is an increase in numbers of plasma cells, with several lightly
basophilic, homogenous inclusion bodies filling the enlarged nuclei
of reti cular cells.
2.142 . Spleen. Polyomavirus infection. 6-month-old lovebird.
Hi gher-power view of 2.141 shows polyomavirus inclusion bodies.
Many plasma cells are present.
Lymphoid System
I
2.143. Spleen. Colisepticemia. 35-day-old broiler. Shown are
multiple foci of effacement of the ellipsoids and periellipsoidal
lymphocyte sheaths by dense fibrinous deposits. The lumens of
penicilliform capillaries can be recognized in the center of the
deposits. The term "fibrinoid necrosis" is sometimes used to
describe this lesion . The lesion is not specific for Colisepticemia but
occurs in different septicemic diseases and some viral infections.
2.144. Spleen. Colisepticemia. 46-day-old broilers. Effacement
of the ellipsoids and periellipsoidal lymphocyte sheath by dense
fibrinous deposits. The lesion is characteristic, but not diagnostic,
for bacterial septicemia.
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2.145. Spleen. Colisepticemia. 5-clay-olcl broiler. The splenic 2.147. Spleen. Erysipelas. Turkey. Shown 1s a large region_of
parenchyma is disrupted by fibrinous ex udate, hemorrhage, and necrosis characteristic of erysipelas in turkeys.
abundant intralesional bacteria.

2.146. Spleen. Septicemia caused by Pse11do111011as aemginosa. 2.148. Spleen. Erysipelas. Turkey. Large necrotic zone is likely
6-clay-olcl broiler. Focal area of necrosis has bacterial aggregate in infarct, with congestion and hemorrhage at the margins.
the ce nter.

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2.149. Spleen. Erysipelas. Turkey. Eosinophilic hyaline deposits
of protein including fibrin form distinct bands around many of the
sheathed capillaries. Few lymphoid cells remain in the periellipsoidal
sheath.
2.150. Spleen. Erysipelas. Turkey. Bacteria (arrow) are 111 the
periphery of area of fibrinoid necrosis .
Lymphoid System
I
2.151. Spleen. Erysipelas. 34-week-old pheasant. Disruption of
the white pulp by multi focal to confluent, demarcated accumulations
of dense fibrinous material. The term fibrinoid necrosis may be used
to describe the lesion. Note the lumens of penicilliform capillaries
in the center of some deposits.
2.152. Spleen. Erysipelas. Adult pheasant. Higher-power view
showing the disruption of the ellipsoidal and periellipsoidal white
pulp by dense fibrinous material. Note the lumen of penicilliform
capillary in the center of the deposit.
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2.1 53. Sp leen. Erysipelas. Ad ult pheasant. Area of marked fibrin 2.155. Spleen. Erysipela s. Adu lt pheasant. The lumen of arterio le
ex udation is suggestive of bacterial infection, which was e1ysipelas in the spleen is filled with bacteria and some necrotic debris. There
in this case. is a lso arteriolitis.

2.154. Spleen. Erysipelas. Adu lt pheasant. Spleen section
sta ined with Gram stain showing clumps of Gram-positive bacteria
(E1J 1sipelothrix rlwsiopathiae) in the cytoplasm of macrophages.
These intracytoplasmic bacteria may be difficult to see w ith H&E
sta in, especially in tissues that are not we ll preserved.
2.156. Sp leen. Ulcerative enteritis. One-year-old quail.
Widespread, roughly round foci of disruption of the white pulp by
dense fibrinous deposits (fibrinoid necrosis). There is also focal area
of hemorrhage.

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2.157. Spleen. Ulcerative enteritis. One-year-old quail. Higher-
power view of dense, multifocal fibrinous deposits (fibrinoid
necrosis) involving the white pulp. The red pulp is congested.
2.158. Spleen. Ulcerative enteritis. One-year-old quail.
Demonstrated is the focal area of hemorrhage in 2.156. Note the
foci offibrinoid necrosis involving the white pulp.
Lymphoid System
I
2.1 59. Spleen. Ulcerative enteritis. One-year-old quail. Wide
zone of subcapsular hemorrhage. The red pulp is congested, and
there are possibly other areas of hemorrhage. Note the foci of
fibrinoid necrosis involving the white pulp.
2.160. Spleen. Mycobacteriosis. 2-year-old duck. Granulomatous
splenitis. Multiple, variably-sized nodules of macrophages
(histiocytes) are prominent. The center of coalescing nodules
contains caseous material (caseous necrosis).
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2.161. Spleen. Mycobacteriosis. 2-year-old duck. Splenic nodul es
are composed of a uniform popul ati on of large macrophages with
ab undant granular cytoplasm.
2.162. Spleen. Mycobacteriosis. 2-year-old duck. Acid-fast
stain reveals clumps of acid-fast positive (red), thin bacilli 111
the cytoplasm of macrop hages. This finding is diagnostic of
mycobac teriosis caused by A1ycobacteri11111 spp.
64 I American Association of Av ian Patholog ists
2.163. Spleen. Mycobacteriosis. 15-yea r-old parrot. Nodular
aggregate of histiocytes with abundant eosinophilic, so mewhat
foa my cytoplasm and large nuclei with prominent nucleoli . This is
one of several histi ocytic aggregates in the section. Acid-fast sta in
revea led small numbers o f ac id-fast positive, thin bacilli in the
histiocytic nodules.
2.164. Spleen. Mycobacteriosis. 2.5-year-old backyard chicken.
The lesion consists of coa lescing histiocytic nodules (histiocytic
gran ulomas). The histi ocytes have ab undant bluish-pink cytop lasm
that gives the nodul es the pinki sh color. In thi s case, only small
numbers of aci d-fast bacteri a were seen in the granulomatous
lesions.

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2.165. Spleen. Mycobacteriosis. 2.5-year-old backyard chicken.
Higher magnification of 2.164. Shown are coalescing histiocytic
nodules with caseous centers rinm1ed by multinucleated giant cells .
Some heterophils are also present among the histiocytes.
2.1 66. Spleen. Mycobacteriosis. 2.5-year-old backyard chicken.
Same section as 2.164 . Histiocytes in the nodules have abundant
bluish-pink cytoplasm. The center of the upper left nodule is
undergoing early caseous necrosis.
Lymphoid System
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2.167. Spleen. Chlamydiosis. 3-year-old parrotlet. Diffuse,
marked splenic plasmacytosis, with multifocal aggregates
of histiocytic macrophages, several of which have granular
hemosiderin pigment.
2.168. Spleen. Chlamydiosis. 3-year-old parrotlet. Higher-power
view demonstrates the marked plasmacytosis (plasma cells and
plasmablasts) and aggregate of histiocytic macrophages. Several
mitotic figures are present among the plasma cells. Note the
hemosiderin pigment in the cytoplasm of histiocytes.
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2.169. Spleen. Chlamydiosis. 3-year-old parrotlet. Higher-
powe r view ofhistiocytic aggregate with cell (a rrow) ha ving dee pl y
basophilic, smudgy cytoplasm characteri stic of intracytopl as mi c
Chla111ydia orga ni sms.
2.170. Spleen. Sarcocystosis. 12-year-olcl cockatoo. Diffusely,
there is marked increase in ce llularity. The splenic cell population
co nsists of plasma cells, hi stiocytes, and lymphoblast-like cells.
Schizo nts of Sarcocvstis sp. were prese nt in the lungs of thi s bird.
66 I America n Association of Avia n Pathologists
2.171. Spleen. Sarcocystosis. 12-year-olcl cockatoo. Higher-
power view demonstrates the increased population of plas ma cells,
histi ocytes, and lymphoblast-like cells. The cytoplasm ofhistiocytes
is distended w ith hemosiderin pigment and debris of phagocyt ized
red blood cells.
2.172. Spleen. Sarcocystosis. 12-year-olcl cockatoo. Area with
many hi stiocyte s (macrop hages), many of which have distended
cytoplasm filled with debri s of phagocytized red blood cells.

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2.1 73. Spleen. Atoxoplasmosis. 2-month-old canary. The
cytopla sm of mononuclear cells (c ircles) co ntains organisms
consistent with Atoxoplasma (Jsosporn) or To.mplasma.
Toxoplas mosis was ruled out by immunohi stochemical staining.
There is an increase in lymphoblast-like cells in the spleen.
Especia ll y note the mononuc lea r cell in th e red circle; the
in tracytop lasm ic Atoxoplasma organisms appear as round structures
fi lli ng the cyto plasm and displacing the nucleus to the periphery.
2.174. Spleen. Marek's disease. One-year-old backyard chicken.
Ex pansion of periarteriolar lymph oid sheaths by pleomorphic
lymphoid cells is a characteristic lesio n of Marek's disease in the
spleen. Only very few foci of this les ion may be present.
Lymphoid System
I
2.175. Spleen. Marek's disease. One-yea r-old backyard chicken.
Higher power of lymphoid infiltrate in 2. 174 demonstrating the
pleomorphic population oflymphoid cells around arteriole. Several
mitoti c fi gures are present.
2.176. Spleen. Marek's disease. One-year-old backyard
chicken. Immunohistochemica l staining of the spleen section fo r
th e T-lymphocyte marker CD3 shows positive cytoplasmic staining
of the periarteriolar lym phoid cell s. Only very few lymph oid
cells ex hibited positive nuclear sta ining for PAX5 , a marker fo r
B-lymphocytes.
Avian Histopatho logy (4 th Edition) I 67
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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2.177. Spleen. Marek's disease. 48-day-old broiler. Marked
expansion of periarteriolar lymphoid sheath by pleomorphic
lymphoid cells. The spleen was grossly enlarged.
2.178. Spleen. Marek's disease. 7-week-old chicken. As the
lesion advances, expanded periarteriolar lymphoid sheaths coalesce
and form more diffuse sheet of lymphoid cells that replaces splenic
tissue.
68 I American Association of Avian Pathologists
2.179. Spleen. Marek's disease. 5-month-old backyard chicken.
Infiltration of the ellipsoidal and periellipsoidal white pulp with
lymphocytes. Note the penicilliform capillaries.
2.180. Spleen. Marek's disease. 5-month-olcl backyard chicken.
Higher-power view of area in 2.178 demonstrating the pleomorphic
population oflymphocytes in the white pulp. Several mitotic figures
can be identified among the lymphocytes. Note the penicilliform
capillaries. Infiltrates of pleomorphic lymphocytes were present
in other organs and tissues. The diagnosis of Marek's disease was
confirmed by immunohistochemical staining.

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2.181. Spleen. Lymphoid leukosis. 25-week-old broiler breeder.
Multiple, variably sized, well-delineated nodules of neoplastic
lymphoid cells creates nodular pattern suggestive of the bursa!
(B-cell) origin of this type of lymphoid tumor.
2.182 . Spleen. Lymphoid leukosis. 25-week-old broiler breeder.
Higher power view of lymphoid cell nodule in 2.181. The splenic
parenchyma is effaced and replaced by relatively uniform population
of proliferating lymphoblast-like cells. Growth of the tumor
appears to be from expansion of smaller nodular tumors rather than
infiltration.
Lymphoid System
I
2.183. Spleen. Lymphoid leukosis. 25-week-old broiler breeder.
Nodular collection of neoplastic lymphoid cells is separated from
the adjacent parenchyma by a thin band of connective tissues.
2.184. Spleen. Lymphoid leukosis. 25-week-old broiler breeder.
Higher-power-view of the lymphoid cell collection in 2. 183. The
cell collection is composed of relatively uniform population of
lymphoblast-like cells with basophilic cytoplasm and large nuclei.
Autolytic changes are common.
Avian Histopathology (4 th Edition) I 69
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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2.185. Spleen. Lymphoid leuko sis. 8-month-old backyard 2.187. Spleen - Reticuloendotheliosis. Turkey. Nodular and
chicken. The normal architecture of the spleen is replaced by diffuse pattern results from proliferation ofpleomorphic tumor cells
diffuse, dense infiltration of uni fo rm population of lymphoid ( insert). Numerous apoptotic cell s are surro unded by clear space and
cells. The sheath of e llipsoida l reticular cell s around penicilliform fibrinoid necrosis is arou nd the sheathed ca pillaries.
capi llaries appear to be preserved. The spleen was remarka bl y
en larged. Lesions consiste nt with lymphoid neoplasm were present
in other orga ns and ti ssues. The diagnosis of lymphoid leukos is was
co nfirmed by immunohistochem ist ry.

2.186. Spleen. Reticulo endotheliosis. Turkey. Proli ferati ng
neoplast ic lymphoid cells are prominent aro und blood vessels.
There are areas offibrinoid necrosis (a rrows).
2.188. Spleen. Reticuloendoth eliosis. Turkey. Tumor growth
by expansion results in destruction of splenic architecture. Some
areas with relati ve ly normal architecture are at the periphery of the
proliferating tumor ce ll s. T he pleomorphic character of neoplastic
cells is illustrated in the insert.

70 I America n Association of Av ian Pathologists

 Ly111p/1oid System
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I
2.189. Spleen. Metastatic adenocarcinoma. 3-year-old backyard 2.191. Spleen. Metastatic adenocarcinoma. 3-year-old backyard
chicken. See the legend of2. I 90. chicken. Adenocarcinoma of reproductive tract origin is expanding
and re plac ing splenic parenchyma.

2.190. Spleen. Metastatic adenocarcinoma. 3.5-year- 2.192. Spleen. Metastatic aclenocarcinoma. 3-year-old
old backyard chicken. The legend is also app lied to 2.189 . backyard chicken. Higher-power view of the adenocarcinoma in
Adenocarcinoma of reproductive tract origin is implanted on the 2. 191 . Expa nding neoplasm re sults in co mpression and distortion of
spleni c ca psule. normal splenic tissue

Avian Histopathology (4 th Edition) I 71

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CHAPTER
Skeletal System
Oscar J. Fletcher • H. John Barnes • Tahseen Abdul-Aziz
Introduction
Bone is the core component of the skeletal system and serves as
the major reservoir for calcium and phosphorus. The term "bone"
refers to both an organ and a tissue. The organ is composed of the
ossified tissue (bone) as well as cartilage forming the articular sur-
fa ces and physes, connective tissues, blood vessels, marrow, and,
in some instances, air sacs . It can be easy when examining his-
tologic sections of bones to forget that bone is a highly active and
compl ex metabolic system . The skeletal system is cliviclecl into the
appenclicular skeleton and axial skeleton . The appenclicular skel-
eton, comprised of the long bones of the body, consists primarily
of compact ( cortical or lamellar) bone arranged in concentric layers
around Haversian canals . The axial skeleton includes the spinal col-
unrn and flat bones of the skull and is composed of cancellous bone
arra nged in a framework of bony struts. Birds also have pneumatic
bones that contain extensions of air sacs. Pneumatic bones develop
by replacement of bone marrow by air sacs. During this process
proliferating fibroblasts and osteoclasts erode bone. The proliferat-
ing fibroblast and osteoclast population resembles the proliferative
response seen in some forms of rickets and must be interpreted as a
normal developmental event. Egg-laying females have meclullary
bone in the marrow cavities of nonpneumatic bones in both appen-
clicular and axial skeletons. The three major cell types of bone are
osteoblasts that secrete matrix (osteoicl), osteocytes that are formed
when osteoblasts become entrapped in matrix, and osteoclasts, the
multinucleatecl giant cells responsible for bone resorption.
Cartilage is another major component of the skeletal system.
Long bones develop through the process of enclochonclral ossifica-
ti on in which cartilage serves as a template that is replaced by bone.
Longitudinal growth of bones is accomplished at the proximal and
di stal ends of long bones and the ends of vertebrae at the region of
the growth plate or physis. Young birds have extensive amounts of
ca rtilage filling the cliaphysis (meclullary cavity) of the long bones.
This core of embryonic cartilage is rapidly replaced during the first
few weeks (7-14 clays) oflife. The rate of replacement varies with
different avian species. For example, in young ostriches, the car-
tilage core can be found in the cliaphysis for several weeks after
hatching. Flat bones of the axial skeleton develop through the pro-
cess of intramembranous ossification with usually one or two cen-
ters of ossification in each flat bone. Appositional growth increases
bone diameter. It is accomplished by the activity of periosteal os-
teoblasts creating matrix followed by deposition of mineral, which
is balanced by enclosteal bone resorption by osteoclasts.
3
Articular surfaces of long bones are covered with cartilage.
I
Joints are surrounded by a capsule of fibrous connective tissue
having a lining of secretory (synovial) cells that form the synovial
membrane. Secretions of synovial cells, coupled with an ultra-fil-
trate derived from blood plasma, create joint fluid required for lubri-
cation. Tendons composed of dense collagenous connective tissue
connect bones to skeletal muscles through origins and inse11ions.
Tendons are discussed in Chapter 4, Muscular System .
Terminology used to describe enclochonclral ossification can
be confusing and acid to the difficulties of recogni z ing, describ-
ing, and interpreting lesions. The following terms describe the
regions that can be identified by examination of the ends of de-
calcified long bones cut in longitudinal section and stained with
H&E . Epiphysis is the cartilaginous region that caps the ends of
long bones and forms the articular cartilage . Some authors use
the term epiphyseal growth plate to include all of the regions of
enclochonclral ossification, but in this book, the above definition
will be used. Physis, or growth plate, lies immediately beneath the
epiphysis and is penetrated by blood vessels from the epiphysis.
The physis has several distinct zones or regions. Resting c/1011-
drocytes are the germinal or basal chonclrocytes that give rise to
the cells of the layer of proliferating chonclrocytes . These cells
are often not seen or appreciated in H&E sections . The zone of
proliferation is characterized by regular columns of chonclrocytes
stacked closely together thus resembling a stack of coins viewed
on edge . Each column of chonclrocytes is separated by extracellu-
lar cartilage matrix. Chonclrocytes become larger, more spherical,
and are in lacunae separated by increasing cartilage matrix with
distance from the epiphysis thus forming the zone of prehypertro-
phy (maturing/transitional chonclrocytes). Blood vessels from the
epiphysis descend to this transitional zone. The zone of hyper-
trophy consists of enlarged rounded chonclrocytes separated from
each other by extracellular cartilage matrix. Mineralization occurs
in the extracellular matrix around the hypertrophic chonclrocytes.
The term zone of mineralization is sometimes used for this region
between the zone of hypertrophy and metaphysis. However, as
mineralization cannot be assessed accurately by examination of
clecalcifiecl bone, the usual way that bone is prepared for diagnos-
tic histopathology, we do not use the term . There is no cortical
bone bridging the physis while the bone is growing; only dense
c01rnective tissue . Small ossifying masses of bone may be in the
physeal connective tissue, especially as it joins with cortical bone.
Intense remod eling is common in this area.
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 Oscar J. Fletcher • H. Jol,11 Ba mes • Tahsee11 Abdul-Aziz
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The Metaphysis is the region located beneath the physis. Min-
eralization has occurred and bone is being formed in this region.
Blood vessels from the metaphysis uniformly penetrate into the
zone of hypertrophy of the physis. Metaphyseal blood vessels do
not communicate with epiphyseal blood vessels. An a vascular zone
of approximately 15 cells thick separates the epiphyseal and me-
taphyseal vessels . This dual blood supply to the physis is important
in that infections in joints can extend through epiphyseal vessels
into the physis. The blind or closed ends of the epiphyseal and me-
taphyseal blood vessels (vascular sprouts) provide an ideal site for
bacteria to localize. Diaphysis, or the shaft, contains blood vessels
and bone marrow or air sacs, and trabecular bone surrounded by
cortical bone. Most long bones do not have centers of ossification
in the epiphysis. The only such ossification center in the epiphysis
of chickens is in the proximal epiphysis of the tibiotarsus .
Osteoblasts form the matrix on which inorganic salts of cal-
cium phosphate are deposited . Osteocytes are cells that are sur-
rounded by and trapped in the calcium phosphate (hydroxyapatite)
matrix. Osteoclasts are large, most are multinucleated, cells that re-
sorb bone. The process of bone resorption results in the creation of
lacunae or pits in the bone. Fibroblast proliferation indicates exces-
sive bone resorption or a response to fracture repairs. Bone is highly
active metabolically and responds or remodels through a series of
complex processes in response to the loads and stresses it experi-
ences. The endocrine system, especially parathyroid glands, and
kidneys play important roles in the complex metabolic processes
that take place in the skeleton. Rapid growth of broiler chickens
contributes to development of skeletal lesions.
Medullary Bone
Medulla1y bone is a non-structural woven bone that develops on the
endosteal surfaces and extends into the medulla1y cavity of mainly
long bones in female birds. Medullary bone develops under the
influence of androgens and estrogens as ovarian follicles begin to
mature. It is seen in the marrow cavity of bones having a vascular
bone marrow. Histologically, medullary bone stains pale blue to
gray with H&E in contrast to the bright eosinophilic staining of cor-
tical (lamellar) bone. It stains intensely with PAS and Alcian blue
and displays ~-metachromasia. Differences in staining are due to
differences in chemical composition between medullary and corti-
cal bone. Medullary bone is highly labile. It disappears rapidly as
calcium is needed for eggshell formation and redevelops as the next
follicle matures.
Polyostotic Hyperostosis
Polyostotic hyperostosis occurs in older female psittacines, espe-
cially budgerigars. It is related to estrogen, but the mechanism is
unknown. Hyperestrogenism is not a cause. Grossly, bones are
thickened and have exophytic masses that deform the affected bones
and displace adjacent tissues. Ribs are often fusiform because of
expansion of the diaphysis and effacement of bone marrow with
new bone. Exophthalmus caused by abnormal bone growth in the
orbit and blindness resulting from compression of the optic nerve
by deformed bones of the skull have occurred. Microscopically, the
abnormal bone is similar to medullary bone but differs from it by
74 J American Association of Avian Pathologists
occurrence in hens that are out of production, bones that normally
are not sites for meclullary bone (skull, sternum, synsacrum), and
periosteal as well as endosteal locations. The amount of bone also
is excessive even in sites where medulla1y bone normally occurs.
Rickets
Rickets is caused by deficiencies of calcium, vitamin 0 3, or phos-
phorus, calcium-phosphorus imbalance, amino acid deficiency, ex-
cess vitamin A (hypervitaminosis A), copper toxicity, and enteric
disease. ln vitamin 0 3 deficiency, the width of the physis is in-
creased because of expansion and disorganization of the zone of pro-
liferation and decreased vascular invasion by metaphyseal vessels.
" Muslu-ooming" of the physis resulting from compression and ex-
pansion may be present. This gives the physis an overall "U" shape.
Similar lesions result from calcium deficiency in rapidly growing
poults and chicks. Bone formation is reduced resulting in bones
that are easily bent, twisted, or deformed. Osteoid is prominent
around trabecular bone in the metaphysis, and fibrous connective
tissue often replaces bone marrow in cases of vitamin 0 3 or calcium
deficiency. Fibrosis (sclerosis) of the marrow cavity can be extreme
when there is a calcium-phosphorus imbalance. Bone strength is
similarly decreased when phosphorus is deficient. Physeal lesions
in phosphorus deficiency include expansion of the zone of hypertro-
phy with metaphyseal vascular invasion of the physis . The physis
does not expand laterally and retains its normal "V" shape. Physeal
changes in rickets associated with vitamin 0/calcium deficiency
and phosphorus deficiency are summarized in Table I.
Rickets in birds with diets adequate in vitamin 0 3, calcium, and
phosphorus can result from copper deficiency, magnesium toxicity,
hypervitaminosis A, excess dietary fat , and mycotoxicosis. ln such
cases, rickets is secondary to the primary etiology. Increased width
of the zone of proliferation, irregular vascular invasion or tunneling
in the zone of hypertrophy, thick irregular boney trabeculae, and
thinning of the periosteum with cortical bone loss are lesions found
in rapidly growing broilers with hypervitaminosis A. Slower grow-
ing leghorns with excess vitamin A have decreased width of the
zone of proliferation, increased width of the zone of hypertrophy,
and a thin periosteum with osteoporosis.
Increased width of the zone of hypertrophy with limited or lit-
tle vascular invasion and decreased numbers of bony trabeculae in
the metaphysis result from copper deficiency. These changes must
be differentiated from dyschondroplasia.
Rickets can also result from maldigestion or malabsorption
when birds have enteric disease (e.g., malabsorption syndrome,
runting-stunting, poult enteritis complex, intestinal coccidiosis). lf
the cause of rickets is dietary, most birds in a flock, and even multi-
ple flocks on different farms , are typically affected. When the cause
is clue to enteric disease, only a limited number of birds develop
rickets and the disease is usually flock specific. "Field rickets" or
"infectious rickets" are terns used to describe rickets resulting from
intestinal disease. Samples of intestine, especially duodenum and
jejunum, along with liver and pancreas, need to be included with
bone for histopathology when rickets is suspected.
Interpretation of physeal lesions depends on recognizing nor-
mal differences in physeal structure between different types and

Table 1. Histologic Characteristics of Rickets Caused by
Deficiencies of Vitamin D3/Calcium or Phosphorus.
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• Increased width of zone of proliferation
(ZP)
• Irregular ZP - loss of organized columns of
proliferating chondrocytes.
Vitamin D3/Calcium
• Reduced width of zone of hypertrophy
(ZH)
Defi ciency
• Limited vascular invasion
• Irregular base of physeal cartilage
..
• Few calcined trabeculae in metaphysis
Abundant osteoclasts
Fibrous tissue may replace bone marrow
• Increased width of zone of hypertrophy
(ZH)
Phosphorus • Normal vascular invasion
Deficiency
.
• Decrease in number of osteoclasts
Increase in number of osteoblasts
• Limited osteoid deposition
ages of birds. The physis of broilers is thicker, more irregular, and
bas poorer vascular penetration compared to the physis of leghorn
chickens. Age is an important consideration when interpreting phy-
seal lesions as long bone development occurs in a cartilage model.
Young chicks and poults have large amounts of normal cartilage in
the long bones for the first 7-14 clays of life. In most cases of natu-
rall y occurring rickets, a distinction between vitamin D/ calcium
defi ciency and phosphorus deficiency cannot be made. Typically,
th ere is a combination ofphyseal lesions suggesting involvement of
multiple factors in the etiology.
Fold fractures in the metaphysis occur in rapidly growing birds
that have rickets. The weight of the bird exceeds the ability of the
bone to support the weight. Fold fractures compromise blood to
the physis from metaphyseal vessels, further worsening the skeletal
di sease. A distinct zone of cartilage across the bone below the me-
taphysis is seen in birds that recover from rickets. Similarly, any
deformities that result from rickets can become ossified and persist
as the bird ages.
Other Lesions in Physeal Cartilage
Dysc/1011drop/asia
Dyschondroplasia is characterized by persistence of a mass of a vas-
cular cartilage in the physeal region of bones that extends into or
through the metaphysis. lt results from a failure of transitional
chondrocytes to differentiate into hypertrophic chondrocytes, which
results in a failure of vascular invasion. The lesion is common in
the proximal tibia (tibial dyschondroplasia) but can be found in any
bones that have a physis, including vertebrae. The cartilage mass
contains necrotic or apoptotic chondrocytes that stain pink with
H&E. Causes of dyschonclroplasia include feeding low calcium
or low calcium- high phosphorus diets to rapidly growing broil-
ers. Several toxic compounds including the Fusari11111 toxin fosa-
rochromanone also cause this lesion. Other causes include toxicity
from thiram, a fungicide used to treat seed, excess dietary levels of
cysteine and homocysteine, diets deficient in copper, and metabolic
acidosis. Genetics and rearing environment are factors that influ-
Skeletal System
ence the incidence of dyschondroplasia. Tibial dyschondroplasia is
an example of osteochondrosis 111a11ifesta. The term tibial dyschon-
clroplasia is so ingrained in the avian literature that it seems unwise
to change terminology for this well-recognized condition.
Osteoc/1011drosis
Osteochondrosis is defined as a focal failure of endochondral os-
I
sification. This can occur in epiphyseal or physeal cartilage or both.
The early lesion termed osteochondrosis fatens , is a focal area of
necrosis confined to the physis that is not detectable grossly._Os-
teochondrosis 111a11ifesta is a macroscopically visible focal failure of
endochondral ossification. Degenerative lesions that may be found
in physeal cartilage include the presence of eosinophilic streaks
across or parallel to the zone of proliferation, matrix necrosis, lakes
of amorphous material, tears or separation of cartilage, and tlu-om-
bosis of blood vessels. Endochondral ossification is abnormal. This
combination of osseous and cartilaginous lesions defines osteo-
chondrosis . Physeal cartilages on either side of the freely movable
vertebra between the notarium and synsacrum in the spine, and the
proximal femur (femoral head) are the most common sites for os-
teochondrosis in broiler chickens. In young birds, osteochondrosis
in the central area of vertebral physes is where the notochord was
located. Whether this continues to resolve as the bird grows or can
become a site for lesion development is unknown. The notochordal
area is small and is only seen in some sections. Osteochonclrosis of
the movable vertebra can cause deformation of the ve1tebra, stenosis
of the vertebral canal, and compression of the spinal cord. Osteo-
chondrosis lesions are sites for bacterial colonization, which predis-
poses to spondylitis in the spine and osteomyelitis in other bones .
Spondylolisthesis
Spondylolisthesis is a developmental disorder in which the crani-
al end of the freely movable thoracic vertebra is rotated ventrally,
which causes narrowing of the vertebral canal and compression of
the ventral spinal cord when the caudal end of the vertebra rotates
dorsally. The notarium and synsacrum are altered to accommodate
the rotated vertebra . Mild to moderate rotation does not cause clini-
cal signs, whereas marked rotation results in a characteristic lame-
ness and demyelination of the ventral tracts of the spinal cord and
neuronal degeneration in gray matter. Other deviations (lordosis,
kyphosis , scoliosis, etc.) affect the spine.
Chondrodystrophy
Failure of physeal chondrocytes to proliferate when mineralization
is adequate and appositional growth of bone is normal , results in
short long bones, wide physes, varus and valgus deformities of the
legs, vertebral shortening and deformities, and, in severe cases, dis-
placement of the gastrocnemius muscle tendon. Chondroclystrophy
replaces the older term perosis. The zone of proliferation is narrow
with disorganization of chondrocytes in regions distal to epiphyseal
blood vessels. Disorganization results when groups of chondrocytes
within the zone of proliferation become hypertrophic . Chondrodys-
trophy and displacement of tendons is associated with nutritional
deficiencies including manganese, zinc, choline, biotin , and pyri-
doxine, infections with Jvfycopfas111a mefeagridis and Jvf i01vae, and
high temperatures during incubation.
Avian Histopathology (4 th Edition) I 75
 Oscar J. Fletcher • H. Jol,11 Bames • Tahsee11 Abdul-A ziz
Responses of Bone to Injury
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Histopathology often is not done as a part of an investigation of
leg problems with specific clinical signs including valgus and varus
deformities, long bone distortion, rotated tibia, tibial bowing, and
shortened long bones. Many of these clinical conditions are assoc i-
ated with defects in physeal carti lage that include dyschondropla-
sia, osteochondrosis, or chondrodystrophy. Lesions of bacterial
I
osteomyelitis are under diagnosed without use of histopathology.
In addition, many clinical leg weakness problems are inaccurately
diagnosed because examination of the vertebral column and spinal
cord are not done.
Multiple lesions, so metimes in the sa me bone or in different
sites within the skeletal system (e.g. , long bones, vertebrae, ribs)
are often found in diagnostic material from field cases. Examples
include fractures associated with rickets or with dyschondroplasia,
fractures in bones with osteomyelitis, and fractures with lesions of
osteochondrosis in vertebrae. Lesions of rickets and dyschondro-
plasia are often seen together as are concurrent lesions of osteo-
chondrosis and dyschondroplasia. Tibial dyschondroplasia and os-
teomyelitis often occur together in the proximal tibiotarsal bones of
tom turkeys. Vascular sprouts that are unable to penetrate abnormal
cartilage in dyschondroplasia provide ideal sites for bacterial local-
ization and development of osteomyelitis.
Fractures and fracture repair
Fractures of wing bones are most common followed by ones in the
legs, ribs, keel, spine, and skull. Most result from trauma, often
because of collisions, however, pathologic fractures may occur in
various skeletal diseases. Keel and rib fractures in broiler breeders
and older laying chickens with osteoporosis are common pathologic
fractures. In birds, fractures are often compound (open) and com-
minuted, ends of broken bones are usually widely displaced and
overriding, and fracture repair occurs more rapid ly than it does in
mammals.
Except for a greater contribution of the endosteum to callus for-
mation, healing of fractures in birds fo llows a similar pattern to that
in mammal s. Initially, acute hemorrhage, clotting, and tluombosis
form a hematoma at the fracture site. During the next few days,
fibroblasts infiltrate the hematoma and produce collagen, which
generates a scaffold on which fibroplasia and angiogenesis occurs .
Eventually the clot is replaced by randomly organized granulation
tissue composed of fibrous tissue and small blood vessels. Cells
from the ends of the fractured bone, especially the periosteum pro-
liferate and develop into chondroblasts and osteoblasts via metapla-
sia in the fibrous tissue. Hyaline cartilage and woven bone produced
by these cells results in a mass of new tissue, the fracture callus,
which eventually unites the ends of the fractured bone. Gradually,
woven bone and ca1tilage undergo endochondral ossification to pro-
duce trabecular bone, which undergoes continuous remodeling via
the activity of osteoclasts and osteoblasts to form compact bone.
Ultimately, the bone is restored as nearly as possible to its original
condition. Marked displ ace ment of the fracture, osseous or carti-
laginous sequestra withi n conun inuted fra ctures, and osteomyelitis
delay healing. A fracture callus requires differentiation from an os-
teoma. Longitudinal , rather than transverse sections of the lesion
76 I American Association of Avian Pathologists
aid in identifying the ends of the broken bone or fragments of ma-
ture bone within a callus. Failure of adequate stabilization or wide
displacement of the fracture can result in pseudoarthrosis.
Osteomyelitis (bacterial chondronecrosis with osteomyelitis)
Osteomyelitis is an inflammation and infection of bone. Lesions
occur most frequently in the proximal tibiotarsus and femur, but
can be found infrequently in other locations. Osteomyelitis may
be located within the physis, metaphysis, bone marrow, or cortex
of long bones and vertebrae. Most often, initial lesions begin at
the physeal-metaphyseal (subchondral) junction. The term bacterial
chondronecrosis with osteomyelitis ("BCO") also has been used as
it describes the most frequent location, lesion, and cause of osteo-
myelitis in poul!Iy. Spondylitis is a specific term for osteomyelitis
in vertebrae. Bacteria, or rarely fungi (Table 2), cause osteomyeli-
tis. Staphylococcus aureus and Escherichia coli are the most com-
mon ca uses of osteomyelitis and spondylitis in commercial poultry.
Most cases of osteomyelitis in birds are hematogenous and a sequela
to systemic disease. Osteomyelitis in chickens serves as a model of
acute hematogenous osteomyelitis in infants and children. Deposi-
ti on of amyloid in periarticular tissues, synovial membranes, and
articu lar caiti lage can occur when osteomyelitis is caused by E11-
terococc11s .fc1eca /is.
Bacteria in the blood stream, either as a bacteremia or septi-
cemia, localize in the terminal metaphyseal vessels, adhere to car-
tilage, and proliferate causing necrosis and initiating fibrin exuda-
tion and heterophilic inflammation. Large bacterial colonies may
occ lude metaphyseal vessels. Bacteria spread along vascu lar chan-
nels and from one lac un ae to the next within cartilage. Initially,
there is necrosis and inflammation of metaphyseal vessels, which
may be foca l and involve on ly a few vessels or diffuse and involve
most or all of the vessels along the physis. Vascular necrosis and in-
flammation surrounds dyschondroplasic lesions, if they are present.
Early lesions may not visible gross ly and only seen microscopically.
Necrotic areas coalesce, often leaving fragments of bone and ca1ti-
lage (sequestra) within the lesion . The lesion continues to expand
until a cavity filled with a caseous mass of necrotic debris and in-
flammato1y exudate is formed . Collapse of the epiphysis (articu-
lar cartilage) into the osteomyelitis lesion can happen if the lesion
is sufficiently large and the bone can no longer support the bird 's
weight. lntralesional bacterial colonies, frequently associated with
or adhering to necrotic cartilage and bone, are generally numerous.
Staphylococci, a common cause of osteomyelitis, produces typical
botryoid colonies. Gram staining aids in identifying the causative
organism . Ultimately, resolution of the lesion is simi lar to fracture
repair. Bone surrounding the osteomyelitic lesion becomes sclerotic
and one or more calluses containing cartilage are formed , exudate
w ithin the lesion is slow ly resolved, and remodeling of surrounding
bone is extensive. The healing phase is aided by fusion of the physis
as the bird ages. Osteomyelitis in adult birds after physeal fusion
is uncommon. Inflammation of joints frequently accompanies os-
teomyelitis and is termed osteoarthritis. Collapse of the epiphysis,
and perhaps infection spreading via transphyseal vesse ls, faci litate
infections of adjacent joints. Livers of turkeys with osteomyelitis
have a patchy green di scoloration because hepatocyte swelling traps
 Skeletal System

Table 2. Causes of Osteomyelitis in Birds

Gram -positive Bacteria
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Staphvlococcus a11re11s . . Long bones* ; spine All birds, mostly poultry

S. hy ic11s . Long bones . Chickens, turkeys
Streptococcus ga//olyticus (bovis) . Long bones Chickens
Coagulase-negative staph . Long bones, spine . Chickens , turkeys
E11terococc11s cecomm . . Spine. . . . Broiler chickens & breeders
E11 terococc11sfaecalis, faeci11m durans, hirae, sp .. Long bones, spine. Chickens

I
Tmperella (Acti11omyce;) pyogenes . Long bones, spine. Turkeys

Gram-negative Bacteria
Escherichia coli . . Long bones; spine. All birds, especially poult1y
Sa/111011ella e11terica . . Long bones Chickens
Sa/111011e//a i11(a11tis, . . Long bones Chickens
Sa/111011e//a typhi11111ri11111 . Long bones Crow
Oth er Sa/111011e//a species
Yersi11ia pse11dot11berc11/osis . Long bones Turkeys
£11/embac/er sp. . . Long bones Chickens
Pasteurella 11111/tocida . . . Long bones , skull . Chickens, turkeys, quail
Rie111erella a1wtipestifer . Spine. Turkeys
Omithobacleri11111 rhinotracheale . . Skull. Red-legged partridges

Oth er Bacteria
Mycobacteri11111 avi11111 . Long bones Hobby and free-living birds
Jl,Jycobacteri11111 111berc11/osis . Long bones Macaw

Fun gi
Aspe1gi//11sfi1111igat11s . Cervical spine . . Chickens
Phycomycetes . . Cervical spine Chickens
Histop/asma caps11/at11m . Tibiotarsus, radius, ulna Eclectus parrot
C,yptococcus gal/ii . . Humerus Pesquet's parrot

*Femur, tibiotarsus, humerus

bile in small peripheral canaliculi. The constellation of osteomyeli-
ti s, synovial inflammation, and green liver discoloration is referred
to as turkey osteomyelitis complex ("TOC").
Enterococcal spondylitis differs from osteomyelitis in that ne-
crosis and inflammation begin in osteochondritic lesions within the
art icular cartilages of the freely movable vertebra in the thoraco-
lumbar spine. Lesions expand in one or both articular cartilages and
extend into the joint space (which lacks a synovial joint capsule and
di sc) and adjacent vertebra of the notarium (cranial) or synsacrum
(ca udal). Lesions contain intralesional bacteria and progress as in
osteomyelitis. Eventually the vertebral bodies of the affected ver-
tebrae collapse, which results in arching of the back (kyphosis) and
forcing the lesion into the ve11ebral canal compressing the spinal
cord. Proliferation of fibrous tissue and car1ilage, much like a cal-
lus, fuses the affected vertebrae together and attempts to stabilize
the spine. Damage to the spinal cord includes demyelination, neu-
ronal degeneration and necrosis, and hemorrhage (hematomyelia).
Occasional lymphocytic perivascular cuffs, most likely in response
to free myelin, are located in the spinal cord or meninges .
Lesions ranging from small clusters of macrophages located
anywhere within the bone marrow to large areas of necrosis sur-
rounded by giant cells and having an outer fibrous capsule are
characteristic of granulomatous osteomyelitis caused by !v!yco-
bacterium avium. Acid-fast stain reveals numerous red staining
organisms within the cytoplasm of macrophages and giant cells.
Mycobacterial osteomyelitis is more common in hobby or zoo
birds than commercial poultry flocks. Infrequently, fungi also
cause granulomatous osteomyelitis . Intralesional fungi can be
seen within the lesions .
Other causes of osteomyelitis are infected compound fractures ,
wounds, and extension of an infection in adjacent tissues to bones,
but these are infrequent compared to the occurrence of hematog-
enous osteomyelitis. Staphylococcus aureus caused osteomyelitis,
accompanied by arthritis and tenosynovitis, in young turkey poults
following trimming of toes at hatch. Osteomyelitis in the bones of
the jaw and skull resulted from chronic sinusitis, blepharitis, and
cellulitis in turkeys and cockatiels. Air sac infections frequently
extend into pneumatic bones resulting in osteomyelitis. Extension
of airsacculitis into bones of the skull occurs in chronic Pasteure11a
11111/tocida infection in older chickens. This is colloquially referred
to as "head cholera" . The related organism, Omithobacterium rhi-
notracheale, caused similar lesions in partridge.
Degenerative Joint Disease
Thinning of the articular cartilage with erosions, fissures, and areas
of necrosis are features of degenerative joint disease. Inflammation
usually is not present in these true degenerative diseases. Intra-
articular inflammatory exudates within the joint space often cause
degenerative and necrotic lesions in the articular car1ilage. Lesions
are common in older captive waterfowl that are lame .
Articular Gout
Swelling around joints with accumulation of eosinophilic to baso-
philic granular to amorphous material surrounded by giant cells,

Avian Histopathology (4 th Edition) I 77

 Oscar J. Fletcher • H. John Ba mes • Tahsee11 Abdul-Aziz
VetBooks.ir
macrophages, and fibrou s connective tissue are features of v isceral
(renal) or articular gout. Sometimes feathery basophilic deposits of
urates can be found within the lesions. Visceral gout with lesions in
the kidneys and urates in many organs besides joints is more com-
mon than articular gout.
Arthritis
Joint capsules are lined by a synovial membrane. Synovial cells
form the epithelial lining of the synovial membrane and normally
are 2 to 4 cells thick. Injury to synovial tissue results in hype1trophy
and hyperplasia of the synovial cells. Hyperplasia associated with
mycoplasmal infections, lvlycoplas111a synoviae (MS) being the clas-
sic examp le, can result in synovial epithelium that is up to 40 cells
thick and villous projections of the synov ial membrane. Reovirus
infections also cause significant synovial hyperplasia comparable
to that seen in mycoplasmal infections. In cases of synovitis, re-
gardless of the cause, necrotic and cellular debris is common on the
surfaces of the synovial membrane and articular cartilage.
Bacterial infections
Heterophils are the primary inflammatory cell in bacterial infections
of joints and tendons. Fibrinoheterophilic exudates with intral-
esional bacterial colonies are characteristic of bacterial infections.
Eventually caseation occurs, although it is much slower in joints
than in parenchymatous organs; possibly joint fluid being added to
the exudate delays the process. Exudate accumulates within the
joint cavity where it often is associated with erosion of articular car-
tilage, osteomyelitis, and inflammation of tendon sheaths . Staphy-
lococcus aure11s is most frequently isolated, but E. coli, Paste11re/1a
m11/tocida, Sal111one/1a, E,ysipelothrix, Enterococc11s, or Pse11domo-
11as also may be involved.
Viral and mycoplasmal infectious
Fibrinoheterophilic inflammation also occurs early (48-72 hours) in
viral arthritis caused by reoviruses , and in mycoplasmal infections
of the joints . This is followed by infiltration and proliferation of
lymphocytes and synovial hyperplasia. By 5-7 days post-infection,
lymphoid proliferation predominates and fewer heterophils are
seen . Recent reovirus isolates are associated with lesions that in-
clude regional accumulation of heterophils, frequently including
fibrin , making differentiation from bacterial infections challenging.
Hallmark histologic lesions of MS are synovial cell hyperplasia, sy-
novial villus formation , and dense infiltration of lymphocytes and
plasma cells. Both reovirus and MS infections are characterized
by increasing numbers of lymphocytes, plasma cells, and develop-
ment of lymphoid nodules (germinal centers), which is described
as a lymphofollicular response . Subjectively, plasma cells may be
more numerous in lesions caused by recent reovirus iso lates. Dif-
ferentiation based on histopathology between reoviral and myco -
plasmal a1thritis is difficult, if not imposs ible. The lymphocytic
and plasma cell respo nse with lymphoid nodule formation and the
degree of synovial hyperplasia is usually more extensive and dense
in mycoplasmal infections than in infection with classical reovirus
stains, but such differentiation is not see n in les ions caused by more
recent reovirus strain s.
78 f American Association of Avian Pathologists
Neoplasia
Perico1tical proliferation of osteoblasts in the mid-diaphysis of long
bones results in formation of hypercellular immature bone. This
lesion is caused by avian retroviruses and is termed osteopetrosis .
Osteopetrosis occurs infrequently in chickens and can be experi-
mentally produced in Guinea fowl. An osteopetrosis-like lesion
may be found in turkeys.
Tumors of bone and ca1tilage are uncommon , but include os-
teomas, osteosarcarcomas, chondromas, and chondrosarcomas.
Chondromas and chondrosarcomas occasionally develop on the
caudal aspects of feet and hocks of water birds (ducks, geese, cranes,
storks, etc.). Neoplasia of respiratory tract origin may extend into
pneumonic bones from tumor cells originating in the air sacs or by
extension of primaiy lung tumors tlu·ough the air sacs. Metastases
to bone, except for malignant melanomas in penguins, are rare . Pri-
mary tumors in the penguins usually involve the foot or hock.
Aneurysmal bone cysts may resemble tumors but they are
blood-filled cavities that lack an endothelium.
Tumors may arise from the synovial cells causing synoviomas
or synovial cell carcinomas, but they are rare.
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causing substantial losses in broiler production in France,
despite routine vaccination of breeders. Vet Rec 172:556.

Van Wettere, A. J. , D. H . Ley, D. E . Scott, H. D. Buckanoff, and
L. A. Degernes. 2013. Mycoplas111a corogypsi-associated
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polyarthritis and tenosynovitis in black vultures (Comgyps
a/ratus). Vet Pathol 50:291-298.
Van Wyhe, R. C., P. Regmi, B. J. Powell, R. C. Haut, M. W. Ot1h,
and D. M. Karcher. 2014. Bone characteristics and femoral
strength in commercial toms: the effect of protein and energy
restriction. Poult Sci 93 : 943-952 .
Waldenstedt, L. 2006. Nutritional factors of importance for optimal
leg health in broilers: a review. A11i111 Feed Sci Technol.
J 26:291-307 .
Webster, S. V. , C. Farquharson, D. Jefferies, and A. P. L. Kwan.
2003. Expression of type X collagen, Indian hedgehog and
parathyroid hormone related-protein in normal and tibial
dyschondroplastic chick growth plates. Avian Pathol 32:69-80.
Skeletal System
Wideman, R . F. and R. D. Prisby. 2012. Bone circulatory
disturbances in the development of spontaneous bacterial
chondronecrosis with osteomyelitis: a translational model
for the pathogenesis of femoral head necrosis. Frontiers
Endocrinol 3:183.
Wilson, S. , S. R. I. Duff, and C. C. Whitehead. 1992 . Effects of
age, sex and housing on the trabecular bone of laying strain
I
domestic fowl. Res Vet Sci 53:52-58.
Wu, W. D. , M . E. Cook, Q. L. Chu, and E. B. Smalley. 1993. Tibial
dyschondroplasia of chickens induced by fusarochromanone, a
mycotoxin. Avian Dis 37 :302-309.
Ytrehus, B ., C. S. Carlson, and S. Erman. 2007. Etiology and
pathogenesis of osteochondrosis. Vet Pathol 44:429-448.
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I E

p
3.2. Proximal tibiotarsus. Normal. 2-week-olcl turkey.
Higher-power view of 3. l shows the epiphysis (E) and the regions
of the phys is including th e zone of proliferation (ZP), zone of pre-
M hypertrophy (ZPH), and th e zo ne of hypertrophy (ZH). Tendon (T)
is show n also.

3.3. Proximal tibiotarsus. Normal. 2-week-old turkey. The

junction of the epiphysis and the physis shows resting chondrocytes
3.1. Proximal tibiotarsus. No rmal. 2-week-old turkey. and the stacked coin-like arra ngement of the cells in the zo ne of
Shown are the epiphysis (E), physis (P), metaphysis (M), diaphysis proliferation.
(D), and cortex (box and see Figure 3.8 fo r hi gh magnification). The
arrow identifies tendon and the * is on th e junction of the ep iph ysis
and physis. BM. Bone marrow.

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3.4. Proximal tibiotarsus. Normal. 2-week-old turkey. The 3.6. Proximal tibiotarsus. Normal. 2-week-old turkey.
zone of proliferation contains flat chondrocytes arranged in columns The zone of hypertrophy is characterized by round chondrocytes
creating stacked coin appearance. surrounded by relatively large amounts of matrix and by vascular
invasion by blood vessels from the metaphysis.

3.5. Proximal tibiotarsus. Normal. 2-week-old turkey. The

zone of pre-hypertrophy is characterized by rounded chondrocytes
separated by more matrix than those in the zo ne of proliferation.

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3.8. Proximal tibiotarsus. Normal. 2-week-old turkey.

Higher-power view of the region bounded by the box in Figure 3.1
showing the periosteum and corti ca l bone with prominent row of
osteob lasts.

3.7. Proximal tibiotarsus. Normal. One-day-old turkey.

Large plug of ca11ilage fills the metaphysea l region and exte nds
deeply into the diaphysis forming the cai1ilaginous template for 3.9. Proximal tibiotarsus. Normal. 2-week-old turkey.
bone development. This ca rtil age plug is normally present fo r Higher-power view of co rti cal bone showing osteoblasts (arrow) on
the first 7 - 14 days of life. The epiphysis (E) and phys is (P) are the surface of minerali zed bone matrix that contains osteocytes.
identified.

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3.10. Proximal tibiotarsus. Normal. 2-week-old turkey. 3.12. Medullary bone. Normal. 29-week-old broiler breeder
Trabecular bone and bone marrow are shown. Note the large number hen. Medullary bone is replacing bone marrow in these vertebrae.
of osteo blasts on the surface of the trabeculae and multinucleated The amount of medullaiy bone shown here may be excessive
osteoclast (box) . and can occur in hen that is ovulating but not forming egg shells
(impacted oviduct).

3.11. Proximal tibiotarsus. Normal. 2-week-old turkey. 3.13. Medullary Bone. Normal. 29-week-old broiler breeder
Higher-power view of3. l O showing multinucleated osteoclast (box) hen. Higher-power view of 3.12. Note the difference in staining
and bone marrow. characteristics between normal bone and medullaiy bone.

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3.14. Medullary bone. Normal. 29-week-old broiler breeder

hen. Higher-power view of 3. 13.

3.16. Proximal tibiotarsus. Rickets caused by vitamin 03/

calcium deficiency. 2-week-old turkey. Widening of the ph ys is
(P) below the epiphysis (E) and fa ilure of blood vessels fro m the
metaphysis (M) to invade the ph ys is.

ZP I,;
...
,.

>,

3.15. Medullary Bone. Normal. 29-week-old broiler breeder

hen. Higher-power view of 3. 14.
,·

3.17. Proximal tibiotarsus. Rickets caused by vitamin 03/

calcium deficiency. 2-week-old turkey. Higher-power view of
area in 3. 16 illustrates the increased width of the zone of pro Ii feration
(ZP). E: Epiphysis.

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3.18. Proximal ti biota rs us. Rickets caused by vitamin D3/
calcium deficiency. 2-week-old turkey. Higher-power view of
area in 3. 17 show ing increased width of the zone of proliferation
and di sorganization of the cells in the zo ne of proliferation.
.. . . . ..,
'
3.1 9. Proximal tibiotarsus. Rickets caused by vitamin D3/
ca lci um deficiency. 2-week-olcl turkey. Illustra ted are proliferation
of fibro us ti ssue in the metaphysis.
Skeletal System
I
3.20. Proximal tibiotarsus. Rickets caused by vitamin D3/
calcium deficiency. 2-week-old turkey. Higher-power view of
3. 19 showi ng the extensive proliferation of fibrous tissue and fai lure
of mineralization of degenerating ca rtil age .
3.21. Proximal tibiotarsus. Rickets caused by vitamin D3/
calcium deficiency. 2-week-olcl turkey. Higher-power view of
the corti cal region of the metaphysis from Fig ure 3.16 showing
relatively thin cortex, relati ve ly thin trabecular bone, and probab le
fracture.
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3.22. Proximal tibiotarsus. Rickets caused by vitamin D3/
calcium deficiency. 2-week-old turkey. Higher-power view of
area in 3.21 showing proliferation of fibrous ti ssue and osteoblasts.
Trabeculae are thin.
3.24. Proximal tibiotarsus. Rickets caused by vitamin D3/
calcium deficiency. 2-week-old turkey. Higher-power view of
area in 3.23 showing thin trabecular bone and the presence of large
numbers of osteoblasts.

3.23. Proximal tibiotarsus. Rickets caused by vitamin D3/

calcium deficiency. 2-week-old turkey. Higher-power view of
area in 3.22 shows large numbers of osteoblasts and thin trabecular
bone.

3.25. Proximal tibiotarsus. Rickets caused by phosphorus

deficiency. 18-day-old broiler. Relatively normal zone of
proliferation (ZP) beneath the epiphysis (E) and increased width of
the zo ne of hypertroph y (ZH) w ith vascular invasion of the physis
by blood vesse ls from the metaphys is are shown.

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3.26. Proximal tibiotarsus. Rickets caused by phosphorus
deficiency. 18-day-old broiler. Higher-power view of the phys is
in 3.25 show ing relatively normal orientation of the zone of
proliferation and increased width of the zones of prehypertrophy
and hypertrophy.
3.27. Proximal tibiotarsus. Rickets caused by phosphorus
deficiency. 18-day-olcl broiler. Higher-power view of area
in the physis in 3.26 showing increased width of the zones of
prehypertrophy and hypertrophy with vascular invasion.
Skeletal System
... _
I
!:tflift?Jf1~t
3.28. Proximal tibiotarsus. Rickets caused by phosphorus
deficiency. 18-day-old broiler. Higher-power view of area in 3 .27
showing blood vessel from the epiphysis is penetrating the zone of
proliferation.
3.29. Proximal tibiotarsus. Rickets .c aused by phosphorus
deficiency. 18-clay-old broiler. Higher-power view of area in
3.28 showing blood vessels in the zone of hypertrophy. There is no
mineralization.
Avian Histopathology (4 th Edition) I 89
 Oscar J. Fletcher • H. John Bames • Tahseen Abdul-Aziz
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3.31. Proximal tibiotarsus. Rickets. 2-week-old broiler.

Hi gher-power view of the physis in 3.30. The zone of proliferation
(ZP) is increased in w idth, but the arrangement of chondrocytes is
relati vely orderly. Ep iphys is is show n (E). The zone of hypertrophy
(ZH) is increased in width.

3.30. Proximal tibiotarsus. Rickets. 2-week-old broiler.

Illustrated are increase in the width of the physis beneath th e
epiphys is (E), distinct zone of proliferation (ZP), persistent zo ne of
hypertrophy, and invasion by blood vesse ls from the meta phys is.
The cortical bone is thin. See 3.3 1, 3.32, and 3.33 for higher-power
3.32. Proximal tibiotarsus. Rickets. 2-week-old broiler.
views of the physi s. This case has so me features of phosphorus
Higher-power view of the physis in 3.30. The zone of prolifera tion
deficiency as well as vitamin 03 /ca lcium deficiency.
(ZP) is relatively wide. Ep iphysea l blood vessel (a rrow) is invading
the ZP and thi s is normal. The epip hys is (E) and zo ne of hypertroph y
(ZH) are shown.

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3.33. Proximal tibiotarsus. Rickets. 2-week-old broiler.
Hi gher-power view of the physis in 3.30. The zone of pre-
hypertrophy (ZPH) is very thin and almost indistinct as it merges
with th e zone of hypertrophy below it.

3.34. Proximal tibiotarsus. Rickets. 2-week-old broiler. 3.35. Proximal tibiotarsus. Fracture and rickets. 4-week-old
Shown is the distal zone of hypertrophy with deposition of some turkey. This is sagittal section of.the tibiotarsus with the epiphysis
wea kly-stained matrix. Osteoblasts are numerous, and there is (E), physis (P), metaphysis (M), and diaphysis (D) identified.
proliferation of fibrous tissue. Folding fracture (arrow) is present at the junction of the physis (P)
and metaphysis (M). The zone of proliferation has increased width
as does the zone ofhype11rophy, thus rickets was diagnosed .

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3.36. Proximal tibiotarsus. Fracture and rickets. 4-week-old
turkey. Higher-power view of the fracture region in 3.35 showing
the distortion of the columns of hypertrophic chondrocytes in the
distal physis.
3.38. Proximal tibiotarsus. Fracture and rickets. 4-week-
old turkey. Another higher-power view of area in 3.36 showing
distortion (bending) of the columns of hype11rophic chondrocytes
consistent with fold fracture.

3.37. Proximal tibiotarsus. Fracture and rickets. 4-week- 3.39. Proximal Tibiotarsus. Fracture and rickets. 4-week-old
old turkey. Higher-power view of area in 3.36 showing distortion turkey. Osteoblast and fibroblast proliferation are extensive and
(bending) of the columns of hype11rophic chondrocytes consistent focal areas of necrosis and tluombosis are shown.
with fold fracture.

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3.40. Proximal tibiotarsus. Fracture and rickets. 4-week-old 3.42. Rib. Fracture with callus. Turkey. Higher-power view of
tu rkey. Higher-power view of the fracture region in 3.35 showing area in 3.41 showing the cartilaginous and fibrous connective tissue
multiple cell types including osteoblasts and osteoclasts. proliferation that forms the callus in response to fracture .

3.41. Rib. Fracture with callus. Turkey. Large call us (arrow) 3.43. Rib. Fracture with callus. Turkey. Higher-power view
developed in response to fracture in the rib. of area in 3.42 illustrating the large amount of fibrous tissue and
disorgani zed cartilage.

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 Oscar J. Fletcher • H. Jol,11 Ba mes • Tahsee11 Abdul-Aziz
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.>

I
3.44. Rib. Fracture with callus. Turkey. Higher-power views 3.46. Femoral head. Osteochondrosis. 5-week chicken,
of3.43 illustrating the di sorga ni zed carti lage. broiler. Shown is the ep iphysea l cartilage (E), physeal cartil age
(P), c left or fissure in the physeal ca rtil age (arrow), and small region
of necrosis (box). These lesions are examples of osteochondrosi s
late ns .

...
.'

3.45. Rib. Fracture with callus. Turkey. Higher-power view 3.47. Femoral head. Osteochondrosis. 5-week chicken,
of area in 3 .44. broiler. Higher-power view of 3.46 with epiphysis (E), phys is (P),
cleft in the physis (arrow) and region of necrosis in the distal physis
(box).This is osteochondrosis latens.

94 I American Association of Av ian Pathologists

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3.48. Femoral head. Osteochondrosis. 5-week chicken broiler. 3.50. Femoral head. Osteochondrosis. 5-week chicken,
Hi gher-power view of 3.47 shows the cleft (arrow) with increased broiler. Higher-power view of 3.48 shows the region of necrotic
cartilage matrix and erythrocytes and thrombocytes within cleft cartilage in more detail. Osteochondrosis latens.
lumen. Epiphysis (E) and physis (P) are labeled. Osteochondrosis
latens.

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3.49. Femoral head. Osteochondrosis. 5-week chicken broiler. 3.51. Femoral head. Osteochondrosis. 5-week chicken broiler.
Hi gher-power view of region in the box in 3.46 and 3.47 shows Higher-power view of 3 .48 shows region of the physeal cleft with
necrosis of cartilage. Necrotic cartilage is separating from the distal increased cartilage matrix and erythrocytes within the cleft lumen.
phys is. Osteochondrosis latens. Osteochondrosis latens.

Avian Histopathology (4 th Edition) I 95

 Oscar J. Fletcher • H. John Bames • Tahseen Abdul-A ziz
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I
3.53. Tibiotarsus. Tibial clyschondroplasia. Chicken. Higher-
power view of area in 3.52 showing the tip of the nonvasc ulari zecl
cartilage plug.

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3.52. Tibiotarsus. Tibial clyschonclroplasia. Chicken. This '
sagittal section of tibiotarsus shows the epiphysis (E), physis (P), . ...
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3.54. Tibiotarsus. Tibial dyschonclroplasia. Chicken.

Higher-power view of area in 3.53 showing the avascular zone of
hypertrophy and necrotic chondrocytes.

96 I American Association of Avian Pathologists

 Skeletal System

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3.55. Tibiotarsus. Tibial dyschondroplasia. Chicken . Higher-
power views of 3.54 shows the apoptotic/necrotic chondrocytes in
the zone of hypertrophy.

3.57. Vertebra. Osteochondrosis. Turkey. Cross section of

vertebra shows the persistence of cartilage. The lesion is consistent
with osteochondrosis (formerly termed dyschondroplasia) .

• • • •• •
•

3.56. Tibiotarsus. Tibial dyschondroplasia . Chicken. Higher- 3.58. Vertebra. Osteochondrosis. Turkey. Higher-power view
power view of area in 3.55 showing necrotic chondrocytes in the of area in 3 .57 showing the persistence of cartilage with no vascular
zone o f hypertrophy. mvas1on.

Avian Histopathology (4th Edition) I 97

 Oscar J. Fletcher • H. John Rames • Tahseen Abdul-Aziz

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of area in 5.58 showing the disorganized pattern of hypertrophic
chondrocytes with increased amounts of matrix material.
.
3.61. Vertebra. Osteochondrosis. Turkey. Higher-powerview of
area in 3.60 showing viable chondrocytes but increased intracellular
matrix. The lesion is osteochondrosis or chondrodystrophy, but
osteochondrosis is preferred.

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3.60. Vertebra. Osteochondrosis. Turkey. Higher-power view 3.62. Vertebrae. Osteochondritis. Turkey. This longitudinal
of area in 3.59 showing marked increase in the intercellular matrix. section of vertebral column shows distortion of vertebral body and
compression of the spinal cord (box A). Also seen are necrosis
of articular cartilage with underlying osteomyelitis (box B), and
persistence of caitilage (box C). Mycoplas111a ioll'ae was iso lated.
This co mbination of les ions co uld also be termed osteochondrosis
manifesta.

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3.63. Vertebrae. Osteochondritis. Turkey. Higher-power 3.65. Vertebrae. Osteochondritis. Turkey. Higher-power view
view of the area just below "box A" in 3.62 showing distortion and of the boxed area (box B) in 3.62 showing necrosis of the cartilage
necrosis of the cartilage with osteomyelitis. and osteomyelitis.

3.64. Vertebrae. Osteochondritis. Turkey. Higher-power view 3.66. Vertebrae. Osteochondritis. Turkey. Higher-power
of the region in "box B" in 3.62 showing necrosis of cartilage with view of the area in box C in 3.62 showing persistent cartilage
necrotic debris in the expanded intervertebral joint. See 03.65 for (dyschondroplasia or osteochondrosis) and expansion of tissue on
hi gher-power view of the boxed area (box B). the ventral surface of the vertebra.

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3.69. Tibiotarsus. Osteomyelitis. 9-week-old broiler breeder
chicken. Higher-power view of the osteomye litis lesion in 3.67
showing large area of nec rosis in the physis. Multiple bacterial
coloni es are prese nt in th e boxed area.

3.67. Tibiotarsus. Osteomyelitis. 9-week-old broiler breeder

chicken. This sagitta l section of tibi otarsus shows multiple
varia ble-sized areas of necros is in the ep iphysis (E), physis (P), and
metap hysea l (M) reg ions. The ca use was Staphylococc11s aureus.

I '
.• < • I - •.
,< ..

3.68. Tibiotarsus. Osteomyelitis. 9-week-old broiler breeder 3. 70. Tibiotarsus. Osteomyelitis. 9-week-old broiler breeder
chicken. Higher-power view of the osteo mye liti s lesion in 3.67 to chicken. Higher-power view of area in 3.69 showin g intra lesio nal
demonstrate necrosis in the epiphys is. bacteria.

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3.71. Tibiotarsus. Osteomyelitis. 9-week-old broiler breeder 3.73. Distal tibiotarsus. Osteomyelitis. One-week-old turkey.
ch icken. Higher-power view of area in 3.70 showing intralesional Higher-power view of the osteomyelitis lesion in the tibiotarsus in
bacteria within caseous debris. 3.72. Areas of necrosis in the epiphysis and physis are seen.

Distal Tibiotarsus Proximal

3.72. Distal tibiotarsus and proximal tarsometatarsus. 3.74. Distal tibiotarsus and proximal tarsometatarsus.
Arth ritis and osteomyelitis. One-week-old turkey. Sagittal Osteomyelitis. One-week-old turkey. Higher-power view of
section through the distal tibiotarsus and tibiotarsus shows lesions of region in 3.73 showing area of necrosis in the physeal cartilage.
synovitis and osteomyelitis caused by Staphylococcus aureus. The
intertarsal joint space (*) contains cellular exudate. Multiple areas
of necrosis are in the epiphysis and physis of the distal tibiotarsus.

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3.75. Distal tibiotarsus. Osteomyelitis. One-week-old turkey. 3.77. lntertarsal (hock) joint. Synovitis. One-week-old turkey.
Higher-power view of another region in 3.73 showing several areas Higher-power view of the synovial lesion in the intertarsal joint in
of necros is with accumulation of caseous necrotic debris. 3.72 showing fibrinoheterophilic synoviti s (arthritis) .

3. 76. Distal tibiotarsus. Osteomyelitis. One-week-old turkey.
Hi gher-power view of the les ion in 3.75 showing caseous granuloma
with central caseous debris surro unded by multinucleated giant
cells. Note the variably sized, dense bacterial colonies in the
caseous debris.
3.78. lntertarsal (hock) joint. Synovitis. One-week-old turkey.
Higher-power view of area in 3.77 showing increased thi ckness of
the synovium, with accumulation fibrinoh eterophilic exudate.

102 I American Association of Avian Pathologists

 - Skeletal System
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3.79. Intertarsal (hock) joint. Synovitis. One-week-old turkey. 3.81. Joint. Mycoplasma Sy11oviae infection. Chicken.
Higher-power view of the synovitis lesion in 3.72 and 3.77. Note Hyperplasia of synovial epithelial cells and multinodular collections
the beterophilic infiltration. Staphylococcus a11re11s was isolated of lymphocytes are features of Mycop/as111a synoviae infection.
from the joint.

3.80. lntertarsal (hock) joint. Synovitis. One-week-old 3.82. Joint. A1ycoplasma Synm•iae infection. Chicken. Same
tu rkey. Higher-power view of area in 3.79 showing accumulation slide as 3 .81. Shown are synovial hyperplasia and lymphocytic
of heterophils in the synovial space. infiltration.

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 Oscar J. Fletclter • H. Jol,11 Ba mes • Taltseen Abdul-Aziz
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3.83. Joint. Mycop/asma Synoviae infection. Chicken. Same 3.85. Joint. Articular gout. Chicken. Deposition of large
slide as 3 .81. Shown are heterophili c ex udate in synovial space, amo unts of urates in the synovial tissue and tendon sheath s.
sy novia l hyperplasia, and lymph ocytic synovitis. Absence of renal lesions and viscera l gout are condi tions needed
before artic ular go ut can be diagnosed.

3.84. Joint. Mycoplasma Sy1101 1iae infection. Chicken. Higher- 3.86. Joint. Articular gout. Chicken. Higher-power view of
power view of area in 3.83. area in 3.85.

104 I Ameri can Association of Avian Path ologists

 - Skeletal System
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3.87. Joint. Articular gout. Chicken. Higher-power view of 3.89. Bone. Osteopetrosis. 14-month-old backyard chicken.
area in 3.86 showing urates deposits and multinucleated giant cells. Cross section of tibia shows expansion of bone, with replacement of
the marrow cavity by bone.

3.88. Joint. Articular gout. Chicken. Higher-power view of 3.90. Bone. Osteopetrosis. 14-month-old backyard chicken .
urate deposits. Higher-power view of area in 3.89 showing periosteal and endosteal
bone proliferation.

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3.91. Bone. Osteopetrosis. 14-month-old backyard chicken. 3.93. Bone. Osteopetrosis. 14-month-old backyard chicken.
Higher-power view of area in 3.90. Higher-power view of area in 3.89 showing the central remnant of
the marrow cavity.

3.92. Bone. Osteopetrosis. 14-month-old backyard chicken. 3.94. Bone. Osteopetrosis. 14-month-old backyard chicken.
Higher-power view of area in 3.91. Higher-power view of area in 3.93 showing marrow fibrosis and
lining of bone by continuous layer of proliferating fibroblasts.

106 I American Association of Avian Pathologists

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CHAPTER4
Muscular System
H. John Barnes • Tahseen Abdul-Aziz • Oscar J. Fletcher
Muscle
Muscle comprises approximately half or more of the body weight
of a bird. Its primary function is to provide purposeful movement,
whi ch is accomplished through contraction and relaxation con-
troll ed by the nervous system and integration with the skeletal sys-
tem via origins, insertions, and tendons. A secondaty fi.mction is to
provide a store of nuh·ients that can be accessed when needed through
catabolism of muscle tissue. This is grossly evident when muscles un-
dergo atrophy in cases of anorexia and sta1vation. Muscle is affected by
numerous factors including genetics (rapid growth, glycogen storage),
environment (hype1thermia), exercise level (inactivity, disuse atrophy,
exertion), trauma (hemorrhage), nerve damage (neurogenic ah·ophy),
hypoxia (cardiovascular disease), nutrition (water deprivation [dehy-
drati on]), food deprivation, amino acids, selenium, vitamin E, rancid
fat) , toxins (ionophores, mycotoxins, plants), intectious agents (viruses,
bacteria, fungi) , and parasites (protozoa, metazoa).
Muscle is infrequently included with tissue samples submitted
for diagnosis making it difficult to know how frequently myopathy is
associated with different diseases. Samples from both breast and leg
muscles, identified separately, should be submitted from any birds with
lameness or neurological signs. It is conunon to find some degree of
muscle disease in any sick bird. Occasionally, clinically normal birds
will have isolated muscle fibers undergoing degeneration or even necro-
sis. How muscle responds to inju1y is limited to atrophy, hyperh·ophy,
degeneration, necrosis, regeneration, and fibrosis, which results in simi-
lar microscopic changes in most muscle diseases. Foci oflymphocytes,
usually perivascular, are conunon when muscle necrosis is severe. As a
result, a number ofmyopathies in poultty have been described, but the
pathogenesis of the lesions and limitations of histological descrip-
tion s make interpretation difficult. Sometimes, which muscles are
affected, or type of fiber affected, is characteristic of a specific disease,
but more often, lesions in other tissues, and use of additional clinical
and diagnostic information is necessary to make a diagnosis.
Histology
The basic unit of the muscular system is the muscle fiber (myo-
fib er), an elongated, unbranched , multinucleated, syncytial cell
bounded by an outer membrane, the sarcolemma, which rests on
a basement membrane. Cytoplasm (sarcoplasm) of the muscle
fiber contains numerous glycosomes (granules of stored g lyco-
gen) and myoglobin , a unique oxygen-binding protein. Nuclei
li e near the sarcolemma and are ovoid or elongated and oriented
parallel to the long axis. In avian muscl e cells, it is normal to find
a few nuclei in the central region of the fiber. The cytoplasm is
packed with myofibrils, which are elongated, cylindrical struc-
tures that lie parallel to one another. Myofibrils are composed
of thin myofilaments that contain actin, troponin , and tropomyo-
sin, and thick filaments composed of myosin . Each myofibril ex-
I
hibits a repeating pattern of cross-striations, which results from
the highly ordered arrangement of bands of contractile proteins.
Cross-striations of each myofiber are arranged in reg ister with
those of the other myofibers giving rise to alternating dark and
light bands seen with light microscopy in longitudinal sections.
Dark bands are called A (anisotropic) bands while light bands are
called I (isotropic) bands. A thin dark line called the Z band bi-
sects each I band. The area between two adjacent Z bands is the
contractile unit of the muscle cell and is termed the sarcomere .
Individual muscle fibers are surrounded by the endomysium, a
delicate supporting tissue composed primarily of reticulin . Indi-
vidual muscle fibers and satellite cells that accompany them are
grouped together to form fascicles. Fascicles are surrounded by
a perimysium of loose collagenous connective tissue . Groups
of fascicles are bound together by a sheath of dense collagenous
connective tissue, the epimysium. Blood vessels and nerves en-
ter through the epimysium and divide to ramify throughout the
muscle in the perimysium and endomysium. Muscle spindles are
sensory mechanoreceptors composed of thin muscle fibers , blood
vessels , and nerves within a capsule that are found in all muscles .
Motor end plates provide motor innervation , but are generally not
identifiable in routine histology.
Satellite cells (adult myoblasts, adult stem cells) are elon-
gated, spindle-shaped, quiescent, myoblast-like stem (precursor)
cells located adjacent to the sarcolemma beneath the basement
membrane. They are difficult to differentiate from sarcolemmal
nuclei by conventional light microscopy. Satellite cells retain the
ability to proliferate and regenerate myofibers following damage to
the muscle. They undergo mitosis after muscle damage and fuse
together to eventually form a differentiated muscle fiber. Regen-
erating muscle fibers tend to be smaller than normal fibers , have
a basophilic cytoplasm, and have increased enlarged open nuclei
with prominent nucleolus singly or in rows in the center of the fiber.
Proliferation of satellite cells contributes to the increased cellular-
ity seen in injured muscle.
Variation in th e color of normal avian muscle is well docu-
mented and is related to the prevalence of various types of fibers.
Avian Histopathology (4 1h Edition) I 107
 H. John Bames • Tahsee11 Abdul-Aziz • Oscar J. Fletcher
Based on function, chemical composition, and size, five muscle
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fiber types are recogni zed in birds (Types l, lIA, IIB , ll!A, and
IIIB) . A few muscles are composed almost entirely of a single
fiber type (e .g. type IIB fibers in pectoral muscles). However, the
majority of muscles have a mixture of fiber types, which explains
the variation in fiber size seen in microscopic sections. There are
two main types of fibers and one lesser type. Red fibers (Type
I) contract more slowly, are smaller, and contain high levels of
myoglobin, numerous mitochondria , and less glycogen Muscles
with a predominance of Type I fibers typically contain abundant
fat , have a rich blood supply, and are capable of sustained activ-
I
ity. In contrast to mammals, Type I fibers in birds are multiply
innervated . White fibers (Type II) are larger, contain less myo-
globin, glycogen, and have fewer mitochondria. Muscles com-
posed primarily of Type II fibers have less fat and a poorer blood
supply, but they are capable of sudden rapid movement. Type I
fibers derive their energy primarily from oxidation whereas Type
II fibers derive their energy primarily from glycolysis. Type III
fibers do not occur in mammals. They are slow contracting tonic
fibers that are intermediate between red and white fibers and keep
muscles in a prolonged contracted state (e.g. wings flexed against
the body).
Hereditary Muscular Dystrophy
The term " muscular dystrophy" should be used only for inherited
progressive muscular diseases of chickens, turkeys, Pekin ducks,
and Japanese quail. Hereditary muscular dystrophy of chickens is
characterized by initial hypertrophy of muscles followed by ir-
regular atrophy. Pectoral muscle lesions are most striking but leg
muscles are also involved. Affected birds are unable to right them-
selves when placed on their backs. Initial microscopic changes
include increased numbers of nuclei, variable fiber size, vacuola-
tion, and ringed fibers. Muscle fibers subsequently disappear and
are replaced by adipose tissue. Muscular dystrophy in chickens
is caused by a missense mutation in the ubiquitin ligase gene,
WWP 1, which causes a substitution of arginine to glutamine.
When the enzyme is abnormal, caveolae (vesicular invaginations
of plasma membranes) are not broken down , and the muscle-spe-
cific protein, caveolin-3, accumulates in the myofibers.
Initial muscle hypertrophy is not seen in affected turkeys .
Muscular dystrophy in turkeys is characterized by atrophy of pec-
toral and wing muscles. Numerous fibers become necrotic, vanish,
and are replaced by adipose tissue. Japanese quail of the mutant
LWC strain have an autosomal dominant trait for heredita1y muscular
dystrophy that is similar to myotonic dystrophy in humans. Char-
acteristic lesions in sections of pectoral muscles from mutant quail
include myofiber atrophy and replacement by adipose tissue, sar-
coplasmic masses, and ring fibers . Changes in the myofibers in-
dicate abnormalities in both plasma membranes and intermediate
filaments. Hereditary muscular dystrophy in Pekin ducks begins
in younger birds that often develop contractures of one or both
legs (arthrogryposis). Microscopically, focal degeneration and
necrosis of muscle fibers , occasionally accompanied by inflam-
matory cells, regeneration , and replacement of lost fibers by fat
cells are seen.
108 I American Association of Avian Pathologists
Nutritional Myopathy
Nutritional myopathy is due to a deficiency of vitamin E or sele-
nium or an excess of oxidants in rancid fat. Interactions between
selenium and other metals, especially copper, silver, and zinc, and
presence of antioxidants such as ascorbic acid in the diet affect the
occurrence of myopathy. Captive fish-eating birds are especially
prone to nutritional myopathy. Histological changes include loss
of cross striations, hyalinization, necrosis, and segmental fragmenta-
tion of fibers. There is proliferation of satellite cells and infiltration
of macrophages. Deposition of calcium (mineralization) in affected
fibers is conunon. When combined with exudative diathesis, lesions
are more severe and vascular changes are apparent. Thrombosis oc-
curs in capillaries and veins because of endothelial disruption and
fibrinoid degeneration of arterioles. lmmunohistochemical staining
for superoxide dismutases shows they are up-regulated to scavenge
oxidative radicals in affected muscle fibers.
Degenerative Myopathy of Superficial Pectoral
Muscle in Broilers
Several ill-defined disorders affecting the superficial pectoral breast
muscles (Pectoral is major) of high-yield broilers have emerged re-
cently including growth-associated myopathy, atypical poultry meat
(PSE, pale soft, exudative and DFD, dark firm, dry), "White Strip-
ing", and recently, " Wooden Breast". It is possible that some of
these may have a common cause, or diseases are occurring concur-
rently, as images of the histopathology of white striping, wooden
breast, and breast muscles of high-yield broiler phenotypes are simi-
lar. Lesions of white striping are linear and follow muscle bundles
while those of wooden breast are focally extensive in the thickest
part of the superficial pectoral muscle beneath the shoulder joint.
Myofibers show loss of striation, swelling and rounding up (Zenk-
er's degeneration and necrosis), hyalinization (coagulation of sarco-
plasm protein), vacuolation, fragmentation , and necrosis. There is
interstitial edema with mild infiltration of granulocytic leukocytes,
lymphocytes, and some macrophages. Necrotic muscle fibers, iden-
tified by sarcoplasmic granular and floccular debris , may be infil-
trated by mainly heterophils and macrophages. As the lesion ad-
vances, muscle fibers are lost, muscle cell regeneration, especially
fiber splitting, is apparent, there is increased loose fibroblastic tissue
or collagenous com1ective tissue in the interstitium, and there may
be focal inflammation consisting of heterophils, macrophages, and
some lymphocytes. lmmunohistochemistty indicates lymphocytes
are predominantly CD3+T-cells. Lymphocytic vasculitis is seen in
broilers with Wooden Breast. The epimysium covering the muscle
is thickened by loose connective tissue containing variable amounts
of collagen, edema, and mixed inflammatory cell infiltrates. Inter-
stitial fibrosis increases over time. Fat tissue increases in the inter-
stitium and muscle fasciculi.
Exertional (Capture) Myopathy
Exertional or capture myopathy was first described in flamingos and
now has been described in many other species of birds. Grossly,
there are large areas of pale edematous muscle, especially in the legs.
Lactic acid accumulations are believed to cause the muscle necrosis.
Acute and chronic lesions are similar to nutritional myopathy and

include loss of cross striations, hyalinization, fragmentation, and ne-
crosis of myofibers (rhabdomyolysis), and increased numbers of sat-
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ellite ce ll nuclei and infiltration of macrophages, which phagocytize
and remove necrotic debris. A history of recent capture or restraint
aids in making a diagnosis of exertional myopathy. Entrapment
may occur naturally as in waterfowl on hypersaline lakes that be-
come so encrusted with salt that they are unable to fly or broiler
breeders that get a leg caught in the slats.
Turkey leg edema syndrome is a form of exertional myopa-
thy seen at processing following transport of turkeys in coops to
the plant. It occurs most frequently when ambient temperatures are
low. Turkey leg edema is characterized by subcutaneous edema in
the inguinal space and around the leg . Typically, it is unilateral.
Legs w ith some degree of valgus deformity are more likely to
be affected . In the blood, creatine kinase levels are markedly
eleva ted. Microscopically, there is marked rhabdomyolysis char-
acteri zed by hyalinization and fragmentation of muscle fibers, inter-
stitial edema, infiltration of some macrophages and heterophils, and
deposition of mineral in some fibers. A similar disseminated focal
myopathy occurs in normal and lame chickens, turkeys, and ducks.
Lesi ons are more severe in lame birds, but it is unknown iflameness
resul ts from the lesions or vice versa.
A special form of myopathy attributed to exertion occurs in
the complexus muscle, commonly known as the "pipping" muscle,
whi ch is located dorsally at the base of the skull. The muscle ham-
mers th e egg tooth on the beak through the egg shell. There is swell-
ing and variable edema, hemorrhage, myofiber degeneration, and
rhabdomyolysis (necrosis) of the muscle in chicks that hatch, but the
myopathy is especially pronounced if hatching is difficult and pro-
longed or ernb1yos pip but do not hatch. Inflammation is not seen.
Deep Pectoral Myopathy (Green Muscle
Disease)
Deep pectoral myopathy has been described in broiler chickens, tur-
keys, and pigeons. It follows exertion but has a different patho-
genes is than exertional myopathy. Only the deep pectoral muscle
(111. supracoracoideus) is affected and changes are due to ischemia
rather than lactic acid accumulation. The deep pectoral muscles are
encased by the sternum and a thin, but tight fascia. The muscle
fon ctions to elevate the wing. Excess flapping of the wings leads to
overexe1tion of the muscle and swelling. As the fascia does not ex-
pand to the same degree as the muscle, blood vessels supplying the
musc le become compressed resulting in ischemia and ultimately
press ure necrosis. The central part of the muscle is most affected .
Initially it is swollen , pale, and friable. Eventually the affected area
becomes green ("Green Muscle Disease") because of the release
of rnyoglobin from necrotic muscle and hemoglobin from lysed
erythrocytes. Histologically, myofibers in necrotic muscle appear
intact but are seen as ghosts because no nuclei are apparent. Fibers
may show transverse splitting (discoid necrosis). Blood vessels in
the interstitium contain lysed erythrocytes. Necrotic muscle tissue
is sharply demarcated from viable muscle tissue by a reactive zone
of fibrous granulation tissue containing macrophages, multinucle-
ated giant cells, and regenerating muscle fibers. Vascular thrombi ,
considered secondary to ischemia and necrosis, can occur in the re-
Muscular System
active zone. Deep pectoral myopathy is an animal model of " March
Gangrene" in people.
Young male broiler breeders develop a similar muscle dis-
ease in their leg muscles following introduction of females, which
initiates vigorous active breeding.
Toxic Myopathies
Ionophore toxicity is an important and relatively common cause of
damage to skeletal muscle in poultry and other animals that ingest
medicated poult1y feeds . Ionophores, especially monensin, salino-
mycin, lasalocid, and narasin, are widely used in commercial poul-
try to control coccidiosis. These compounds can be toxic if used
improperly and cause significant m01tality in chickens, turkeys ,
guinea fowl , and ostriches. Affected birds may show paresis or be
paralyzed before death . Clinical signs result from degeneration and
necrosis of skeletal muscles in the legs. Breast muscles are not af-
fected. Some flocks may have altered vocalization because of le-
sions in tracheal muscles. Ionophores interfere with ion transfer at
the muscle cell membrane . Sodium ions from the sodium ionophore
monensin can increase uptake of Ca++ at the muscle cell membrane
by changing the integrity of the membrane resulting in muscle fiber
damage. Ca++ dependent phospholipases A2 help with movement
of Ca++ ions across the sarcolenuna membrane. Compounds like
ionophores disrupt this ion balance, which can result in skeletal
muscle damage. The amount of histological changes seen in muscle
fibers can va1y greatly. In some field outbreaks there is minimal or
no changes, while in others, Joss of cross striations, hyalinization,
and fragmentation of muscle fibers is seen, with occasional mineral
deposits in necrotic fibers. A marked increase in nuclei due to in-
filtration of macrophages and proliferation of satellite cells is typi-
cally seen. Regenerating myofibers with basophilic cytoplasm and
centralized nuclei may be seen in some areas depending on the level
and timing of exposure. The interaction of tiamulin, an antimicro-
bial used to treat lY!ycoplas111a, with ionophores enhances toxicity as
it prevents degradation of the ionophore. An experimental trial with
tiamulin and ionophores resulted in striking microscopic lesions in
muscle fibers. Hyalinization, fragmentation, and macrophage infil-
tration of fibers, with markedly enlarged nuclei associated with pale
to basophilic sarcoplasm in other fibers were seen. Affected nuclei
had prominent nucleoli. Lesions were restricted to the leg muscles.
Poisonous plants like Senna (=Cassia) occidentalis are
known to cause muscle degeneration in cattle and poult1y. All
paits of the plant are poisonous, but seeds are most toxic. The toxin
in the seed remains unidentified. Some studies demonstrated that
the external segment of the seed is most toxic. Grossly, affected
muscles are pale and edematous . Histological changes include
swelling and fragmentation of muscle fibers with proliferation of
satellite cells. Less severe changes include atrophy of type 1 and
type 2 fibers. Lipid storage in fibers and enlarged mitochondria
with disrupted or excessively branched cristae, characteristic of a
mitochondrial myopathy, are seen by electron microscopy.
Hyperthermia (Heat Stroke)
Birds often experience hype1thermia as a result of being in envi-
ronments with high ambient temperatures and humidity, when they
Avian Histopathology (4 th Edition) I 109
 H. Jol,11 Bames • Tahseen Abdul-Aziz • Oscar J. Fletcher
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are crowded together as occurs in transit to processing, " piling", or
experience overexertion. Birds selected for increased muscle mass
(e.g., broiler chickens vs. layer chickens) and older (larger) birds are
more affected. Meat quality also is affected; hyperthermia prior to
processing increases the occurrence of pale, soft, exudative meat.
Mortality is common in acute severe hyperthermia (heat stroke).
When broiler chickens are raised under hot conditions, myofibers
are smaller and myofiber degeneration is increased. Pectoral mus-
cles of chickens that die of heat stroke show severe diffuse rhab-
domyolysis and interstitial edema. Sarcolemma is disrupted and
proteins from the myofiber are in the interstitial tissue along with
I
edema. Lesions are similar to early lesions of exertional myopathy
in that there is little to no evidence of cellular proliferation, inflam-
mation, regeneration, or fibrosis.
Myopathies of Uncertain Etiology
Several other myopathies in poultry have been described , but the
pathogenesis of the lesions and limitations of histolo g ical de-
scriptions make interpretation difficult. An example is acute pec-
toral myopathy described in broil er breeders that die suddenly in
good body condition. A desc ription of the lesions included hya-
lini za tion and fragmentation of muscle fibers , which suggested an
exertional myopathy, taking into account the clinical aspects that
were reported.
A significant percentage of chickens with degeneration of the
p11bioischiofe1110ml (adductor) muscles have been identified at pro-
cessing. Most of the muscle was necrotic and contained large fibers
with internali zed and cluste red nucl ei.
Heavy broiler chickens were downgraded at process ing be-
cause of severe myodegeneration of unknown etiology in the anteri-
or latissi11111s dorsi muscle, a muscle composed of Type I myofibers.
Carcasses were otherwise normal and males and heavier birds were
more affected than females and lighter birds. In the lesion, most
myofibers were undergoing degeneration and necrosis. Also pres-
ent were basophilic fibers with rowing of central nuclei indicative of
regeneration, cell proliferation , extensive fibrosis, and replacement
of muscle tissue with adipose tissue.
Tom turkeys with degenerative polymyopathy occurring in
the first few clays of the photoperiod being increased have been
reported. Affected turkeys have paralysis of the neck and may
be unable to stand . Lesions include widespread degeneration of
musc les with cervical muscles being most affected . Because many
of the cervical muscles are surrounded by tight fascia , this may
represent an example of compartment disease like deep pectoral
myopathy. A focal myopathy occurring in turkeys at processing
also has been described.
Myopathies that are locali zed have been reported in clucks and
quail affected with idiopathic torticollis and in broiler chickens at
processing. In clucks, the bivenler cervicis and se111ispinalis muscles
have microscopic lesions consisting of fiber necrosis, mononuclear
cell infiltration, fatty infiltration, and thickening of the perimysium.
Repeatedly extending and stretching the wings of chickens 1-5
years produced a myopathy in the patagialis muscles, but not the
biceps brnchii muscles. Pathology was similar to hereditary mus-
cular dystrophy and included necrotic fibers exhibiting segmental
110 I American Association of Avian Pathologists
necrosis, abnormal shapes, enlargement, splitting, vacuolation, and
phagocytosis of myofibers.
Muscle Hemorrhage
A number of infectious and non-infectious factors cause hemor-
rhages in skeletal muscles. Hemorrhages are classified as petechial ,
striated, ecchymotic, or suffusive. Hemorrhages may result from
direct traumatic damage to vessels, endothelial degeneration or ne-
crosis, defective coagulation, or via diapedesis from post-capillary
venules associated with inflammation. Occurrence of hemorrhages
in muscles is typically part of a broader response and has limited
diagnostic value. Hemorrhages need to be distinguished from post-
mortem extravasations of blood, severe congestion, and vascular
tumors (hemangiomas, hemangiosarcomas).
Massive suffusive hemorrhages result from trauma, frac-
tures, and ruptured tendons or muscles, which often leads to for-
mation of hematomas. Blood within the hematoma slowly un-
dergoes lysis until just nuclei remain . The hematoma becomes
encapsulated and eventually fills with fibrous connective ti ss ue.
Other non-infectious causes of muscle hemorrhage include hy-
poxia , overexertion, hyperthermia, toxin s (e.g. , mycotox ins, ro-
denticicles), and nutrient deficiencies (e.g., selenium , vitamins
E and K). Hemorrhages may occur following euthanasia by
cervical dislocation or electrocution.
Infectious causes of muscle hemorrhage include viruses, bac-
teria, and protozoa. Most hemorrhages in viral and bacterial in-
fections result from either direct or indirect damage via toxins to
endothelial cells, or tlu·ombosis. Exceptions include hemorrhages
resulting from infections with chicken anemia virus and very viru-
lent infectious bursa ! di sease virus, which cause bone marrow de-
struction, thrombocytopenia, and defective clotting. Intramuscular
meronts of hemoprotozoa cause hemorrhages in some species of
birds. Cysts are filled with blood and contain numerous merozo ites.
Mortality may result from heavy infections.
Granulomatous Myositis (Injection Site Injury)
Intramuscular injection of oil-emulsion vaccines (bacterins) can re-
sult in severe necrosis and marked inflanunation. Characteristically,
there are multifocal caseous gra nulomas; each consisting of a cen-
ter of deeply eosinophilic, acellular caseous material surrounded by
multinucleated giant cells. Large round empty spaces represe nting
dissolved oil droplets from the bacterin are located within the case-
ous material and in other areas of the lesion. Spaces betwee n the
granulomas are edematous and contain mixed infiltrates of lympho-
cytes, plasma cells, macrophages, and occasional heterophils. Simi-
lar damage to the muscle can also result from injection of antibiotics.
Glycogen Storage Diseases
Glycogenosis II (acid maltase defici ency) occurs in inbred lines of
Japanese quail , which are used as an animal model of the di sease.
Glycogen accumulates in lysoso mes because of the enzyme defi-
ciency. Excess glycogen in musc le cells and cells in the liver, heart,
and brain is see n as intracytoplasmic pale foci that stain positive
with PAS. Ochratoxin ca uses storage of glycogen in muscle cells
analogous to Type X glycogen storage disease in humans.
 Muscular System

Infections that cause septicemia, may affect muscle. These include strep-
Viruses typica ll y cause primary muscle infections because muscle tococci , staphylococci , Pse11do111011as, and Sa/111011effa. Mul-
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fibers are suitab le host cells for virus infection and multiplication. tifocal muscle necrosis and heterophilic myositis caused by
[n contrast, bacterial and mycotic infections are usually secondary Streptococcus gaffofyticus (=S. bovis) affects young pigeons.

to spread from infections in adjacent tissues, septicemia, or injec-
tion s of live bacteria in vaccines or as contaminants. Lesions re-
sulting from viral infections are usually multifocal to diffuse and
Jymphocytic or lymphohistiocytic, whereas bacterial infections are
generally focal to multi focal , fibrinoheterophilic to heterophilic, and
accompanied by necrosis.
Microscopically, there is muscle necrosis, heterophilic inflam-
mation, and bacteria that are often intravascular.
Fungal infectio11s
Mycotic infections of muscle are uncommon . They usually result
by extension from adjacent infected tissues, contaminated intramus-
cular injections, or via hematogenous dissemination. Organisms

I
Viral infections involved include Aspe1gif/11s and Candida.
Degeneration of skeletal muscle, along with lesions in other organs,
Protowal i11fectio11s
occurs in Muscovy ducks infected with Muscovy duck-origin par-
Asexual stages (meronts [= schizonts]) of several protozoa occur in
voviru s. Following experimental infection at day I , the ducks had
the muscles of birds including Pfasmodi11111, Hae111oprote11s , Le11cocv-
swelling and loss of cross striation of myofibers with a reparative
tozoo11, and Sarcocystis. Meronts may be in endothelial cells where
prolife ration of fibroblasts by week 3. Chickens with avian en-
they obstruct blood flow or within muscle fibers. Large meronts,
cepha lomyelitis (AE) may have lymphocytic infiltrates, usually as
which may be visible grossly, are referred to as " megaloschizonts" .
multiple, variably-sized foci in skeletal muscles. Muscle lesions
Intramuscular meronts of Pfas111odi11111, Hae111oprote11s , and Le11cocy-
often are unrecognized, as samples of skeletal muscles are not usu-
tozoo11 are exo-erythrocytic stages from which merozoites enter the
ally among tissues collected for histopathology from birds suspected of
circulation and develop into gametocytes. Clinical disease and mor-
having AE. Multifocal myositis caused by enteric reoviruses occurs
tality may occur prior to the appearance of stages in the blood. ln
in conjunction with nerve lesions in chickens with central nervous
contrast, birds serve as intermediate hosts of Sarcocy stis . Predation of
system disease. Certain strains of highly pathogenic avian influ-
infected birds by definitive hosts permits completion of the life cycle.
enza virus produce severe, acute, necrotizing myositis in chickens,
Meronts are often found accidentally in skeletal muscles of differ-
ducks, and other birds. Involvement of muscle varies with differ-
ent avian species, or they may occur in birds experiencing lameness,
ent virus isolates and avian species. Extraocular muscles are often
increased mo1tality, or encephalitis. Haemoprote11s mefeagridis, H.
mo st affected. West Nile virus causes mild focal myodegeneration
fophortyx, and H. cofumbae cause mortality in turkeys, Bobwhite
to severe lymphohistiocytic necrotizing myositis in some species of
quail , and pigeons respectively. A few species of Sarcocystis cause
free- living birds, especially owls.
mortality in birds, but often the birds have concurrent encephalitis
In companion birds, polyomavirus infects muscle and
and not just muscle infections. A biphasic clinical course and high
causes myopathy. Amphophilic inclusions typical of polyoma-
mortality occur in pigeons infected with Sarcocystis cafchasi. Heavy
virns can be identified in sarcolemmal nuclei.
muscle infections are seen when the pigeons develop acute neurologic
Several viruses including infectious bronchitis virus, New-
disease 7-8 weeks after exposure. Sarcocystis rifeyi is a common in-
castl e disease virus, and infectious bursa! disease virus have
cidental finding in waterfowl with sometimes striking gross lesions in
been identified in muscles of both normal and affected chickens,
the pectoral musculature called "Rice Breast Disease" . Meronts of
but their relationship to muscle disease is unknown. Similarly,
Hae111oproteus and Sarcocystis develop within cysts in muscle fibers
viru ses have been detected in the muscles of companion and
and are similar to each other. They can have a smooth cyst wall, a
free-living birds by molecular methods, but the significance of
cyst wall lined by fine hair- or finger-like projections, or divided into
these findings is unknown .
compartments by septa. Molecular methods will specifically identify
Bacterial i11fectio11s the parasites. Similarly, Le11cocytozoon meronts are large and may be
Gan grenous myositis, caused by Cfostridi11111 septic11111, spreads to barely visible grossly as tiny, white spots. They develop within endo-
the superficial pectoral muscles of broilers from gangrenous der- thelial cells and contain numerous merozoites. Unless they rupture,
matitis in the overlying skin. Lesions are more severe in muscle there is no inflammato1y response to the any of the protozoa! meronts.
fibers close to the surface and are characterized by acute degenera- Both bradyzoites and tachyzoites of Toxopfas11w gone/ii oc-
tion and necrosis of myofibers, interstitial edema, lysed red blood cur in muscles of naturally and experimentally infected birds. Both
cell s, and minimal to absent inflammatory cells. lntralesional, forms of the parasite occur in multiple necrotic foci when infection is
large, Gram-positive rods, morphologically consistent with Cfos- acute. In chronic infections, only bradyzoites are seen within muscle
spp. , are seen.
tridi11111 cells. These are difficult to find in otherwise normal muscle, but use
"Lockjaw Syndrome" in cockatiels is a chronic sinusitis of a PAS stain may be helpful.
that spreads to adjacent jaw muscles. Often the disease is as-
Metazoal i11fectio11s
sociated with long-term Bordeteffa avi11111 infections. Affected
Nematode larvae are infrequently found in avian muscle. Af-
birds have necrotizing myositis, perineuritis, and osteomyelitis
fected birds may or may not have locomotor difficulty and be
affecting jaw muscles and cranial bones.nfrequently, bacteria

Avian Histopathology (4'h Edition) I 111

 H. John Ba mes • Tahsee11 Abdul-Aziz • Oscar J. Fletcher
more susceptible to predation and completion of the parasite 's
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life cycle. Larvae of Trichinella pse11dospiralis occur in muscles
of raptors and carrion-feeding birds. Chickens can be infected
experimentally with T pse11dospiralis, but not T spiralis. Lack
of a capsule distinguishes T pse11dospiralis from T spiralis in
muscle sections. Prey species such as quail serve as paratenic
hosts for spirurid (Physaloptera) and ascarid larvae (Baylisasca-
ris). Visceral larval migrans occurs in chickens experimentally
infected with embryonated Baylisascaris and Toxocara eggs.
Schistosome eggs associated with focal myositis may be found
in muscles of aquatic birds.
I
Subcutaneous mites, Laminosioptes cysticola, occasion-
ally occur in superficial muscles in addition to the subcutis.
Neoplasia
Lymphosarcoma, caused by Marek's disease virus, frequently in-
volves muscles of chickens. It is characterized by pleomorphic pop-
ulations of lymphoid cells, but multiple sections may need to be
examined to identify the characteristic variation in lymphoid cell
sizes. Lymphocytic neuritis may be seen associated with intramus-
cular lymphosarcomas. Avian leukosis viruses (ALY) cause my-
elocytomas in a variety of tissues including muscle. ALY also can
cause hemangiomas, fibromas, and fibrosarcomas in muscles, but
these are uncommon. ALY that predominantly cause hemangiomas
are termed " Avian Hemangioma Viruses" . Hemangiomas are most
common in layers and primarily affect the skin, but tumors also oc-
cur in muscle and visceral organs. Metastatic melanomas without
evidence of exogenous ALY occur infrequently in muscles of young
chickens. Spontaneous rhabdomyosarcomas and fibrosarcomas in-
volving the muscles of birds are rare.
Tendons
Tendons connect muscles to bone. They are composed of bands of
linear dense collagen fibers surrounded by connective tissue (en-
dotenon), which are bound together by a layer of thick peripheral
connective tissue (epitenon). Endotenon and epitenon correspond
to the perimysium and epimysium in muscle. Increasing amounts
of connective tissue and variably sized muscle fibers with central
nuclei are seen toward the myotendonousjunction. Tendons contain
blood vessels and nerves and are surrounded by a synovial mem-
brane, the tendon sheath adjacent to the paratendon . Two layers of
synovial cells line the synovial sheath. The inner (visceral) layer
covers the surface of the tendon while the outer (parietal) layer cov-
ers the inner surface of the paratendon. Fluid produced by synovial
cells lubricates the tendon and permits it to slide back and forth as
the muscle contracts and relaxes. Some tendons, including the ex-
tensor and flexor tendons of the wings and legs, undergo metaplasia
to cartilage and bone with aging. Bone in tendons is similar to that
in the skeleton, often containing bone marrow.
Birds with lesions in tendons, or more commonly tendon
sheaths, are usually Jame and in poor body condition. Frequent-
ly, only one leg is affected . Often abrasions and feather loss are
seen on wing tips as the birds are using their wings for balance
and locomotion.
112 I American Association of Avian Pathologists
Partial tears or complete rupture of tendons, most frequently
the gastrocnemius and flexor muscle tendons, result in hemorrhage
and acute inflammation. Rupture of the tendon often occurs just
proximal to the area of ossification. Tendon rupture can result from
reovirus infection (infectious tenosynovitis, see below) or trauma.
Malnutrition during growth will result in improperly formed weak
tendons that undergo spontaneous rupture, as they are unable to
support the weight of the adult bird. Selenium deficiency results
in decreased collagen , smaller collagen fibers, and degeneration of
fibroblasts in tendons of ducks. Heavier birds, breeders experienc-
ing overexertion, and hens being aggressively bred are prone to
ruptured tendons. Most often, only tendons in one leg are affected.
Microscopic lesions include extensive hemorrhage, disorganization
of collagen fibers , vascular thrombosis, necrosis of chondrocytes,
chondroid infiltration of collagen bundles, and fibrosis . Lack of
lymphocytes and lymphofollicular nodules is characteristic of
spontaneous tendon rupture. Focal hemorrhage is seen in partial
tendon tears. Hematomas undergoing resolution are seen if par-
tial tears precede complete tendon rupture. Extensive fibrosis and
collagen deposition during the repair process of both partial and
complete tendon rupture result in adhesions between the tendon
and tendon sheath .
Inflammation of the tendon is called tendinitis, which usu-
ally results from overexertion , trauma , or together with tenosy-
novitis and arthritis. Inflammatory processes in tendon sheaths
(tenosynovitis) are similar to and often occur concurrently with
synovitis (arthritis) in joints or osteomyelitis in bones . Causes
of tenosynovitis are the same as those that cause arthritis and
include viruses and bacteria, including mycoplasmas. The type
of inflammatory infiltrate can be helpful in establishing a pre-
sumptive etiologic diagnosis that can be confirmed by specific
diagnostic procedures.
Deposition of urates in synovial membranes lining tendon
sheaths may be primary (articular gout) or secondary to kidney dis-
ease (visceral or renal gout). Primary gout is genetic and is distin-
guished from renal gout by normal kidneys and lack of urate de-
posits in serous membranes and visceral organs. Tophi containing
characteristic faintly basophilic feathery starburst profiles where
urate crystals were located prior to dissolving in aqueous fixatives
(e.g. , formalin) are seen.
Tenosynovitis
Bacterial infections
Tenosynovitis caused by bacteria is characterized by fibrinohetero-
philic exudate that accumulates within the tendon sheath and syno-
vial cell hyperplasia. Heterophils, the primary inflammatory cells,
undergo degranulation, degeneration , and necrosis. Exudate gradu-
ally becomes caseated trapping and isolating the bacteria. Macro-
phages migrate from blood vessels and accumulate on the surface of
the caseous exudate where many fuse to form multinucleated giant
cells. Microscopically, this is seen as a palisade of macrophages
and giant cells surrounding the central mass of caseous exudate.
Eventually a heterophilic granuloma forms, which isolates the in-
flammatory exudate containing entrapped bacteria from viable tis-
sue. Small numbers of lymphocytes may be present around vessels.

Staphylococcus a11re11s is a frequent cause of bacterial tenosynovi-
tis, but Escherichia coli, Pasteure!!a multocida, Salmonella, E1 y sip-
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elothrix, Enterococcus, and Pseudomonas also are potential causes.
Some bacteria form characteristic colonies (e.g. bot1yoid colonies of
Staphy lococcus) , while others remain as individual or small clusters
of orga nisms. A Gram stain helps to identify the type of bacterium
causing the lesion.
Jdentifying intralesional bacteria in tenosynovitis lesions pro-
vides evidence for a causal role for the organism, but does not ex-
clude the possibility that concurrent mycoplasmal or viral infections
is also occurring.
Mycoplasmal i11fectio11s
Fibrinoheterophilic inflammation, indistinguishable from that
caused by bacterial infections, also occurs early (first 48-72 hours)
in tenosynovitis caused by mycoplasmas . The acute reaction is fol-
lowed by synovial hyperplasia and increasing numbers of lympho-
cytes and plasma cells. By 5-7 days post-infection, lymphoid pro-
liferation predominates and fewer heterophils are seen. Lesions are
characteri zed by development of multiple lymphoid nodules (ger-
minal centers). Presence of lymphoid nodules (termed a lymphofol-
licular reaction) is characteristic of Mycoplas111a synoviae infection,
but also can be seen in reovirus infections. Although less common,
similar tenosynovitis lesions can result from Aif. ga!lisepticu111 infec-
tion. Bacterial colonies are not seen in exudate unless concurrent
mycoplasmal-bacterial infection is occurring.
Viral infectious
Lesions of tenosynovitis caused by reoviruses develop similarly to
those caused by mycoplasmas. Recent reovirus isolates are associ-
ated with lesions that include regional accumulation of heterophils,
frequ ently including fibrin , thus making differentiation from bac-
terial infections challenging. Subjectively, lymphocytic foci , es-
pec ially lymphoid nodules, may be less apparent and plasma cells
more numerous in reoviral tenosynovitis. As lesions are similar in
both mycoplasmal and reoviral infections, additional diagnostic
procedures are necessary to specifically identify the cause of teno-
synoviti s. Tendon damage occurs in reovirus infections, which can
lead to rupture when the birds get heavier. Characteristic lympho-
cytic inflammation is seen when tendon rupture results from reovi-
ral infection. Adenoviruses have also been isolated from cases of
tenosynovitis and tendon rupture, but their role in disease has not
been defined.
Tenosynovitis caused by either bacteria or reovirus leads to
fibrosis of the flexor tendons making it difficu lt to identify the pos-
sible cause in this chronic stage .
Vaccine-associated granulomatous tenosy11ovitis
Highly adjuvanted vaccines (bacterins) can gravitate into the syno-
vial sheath following intramuscular injections into the leg where
they cause a granulomatous tenosynovitis. Lesions are character-
ized by intense diffuse inflammation, caseous exudate, and multiple
small granulomas in the tendon sheath.
Muscular System
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Sihvo, H.K. , K. lmmonen, and E. Puolanne. 2014.
Myoclegeneration with fibro sis and regeneration in the
pectoral is 111ajor muscle of broilers. Vet Patho/ 51 :619-623.
-
Muscular System
Siller, W. G. and P.A . L. Wight. 1978. The pathology of deep
pectoral myopathy of turkeys. Avian Pathol 7:583-61 7.
Simpson, C. F. , 8. L. Damron, and R. f-1. Harms. 1971. Toxic
myo pathy of chicks fed Cass ia occidental is seeds. Avian Dis
15 :284-290 .
Skarda, R., V. Konrad, and J. Marcanik. 1978. Pathological
changes in the skeletal musculature of chicks after experimental
hypokines is. Folia Veterinaria 22:25-35.
Soffer, D., N. Resnick-Rogue!, A. Elclor, and M. Kotler, M. 1990.
Multifoca l vascular tumors in fowl induced by a newl y isolated
retrovirus . Cancer Res 50:4787-93.
I
Sosnicki, A., R. G. Cassens, D. R. McIntyre, and R. J. Vi.mini . 1988.
Structural alterations in oedematous and apparently nonnal skeletal
muscle of domestic turkey. Avian Pathol 17:775-79 1.
Sosnick.i, A. A., R. G. Cassens, R. J. Vimini, and M. L. Greaser. 1991.
Histopathological and ultrastructural alterations of turkey
skeletal muscle. Poul! Sci 70:349- 357.
Tanaka, S. , I. S. Braga, 3rd, T. Kimura , K. Ochiai, C. Itakura,
and M. Mizutani. I 996. Inherited muscular disorder in
mutant Japanese quail (Cotumix cotumix japonica): an
immunohistochemica l study. J Comp Pathol_ 115: 139-150.
Umemura, T., H. Nakamura, M. Gotyo, and C. Itakura. 1984.
Histopathology of monensin-tiamulin myopathy in broiler
chicks. Avian Pathol 13:459-467.
Valberg, S. J. 2004. Pathophysiology of muscle disease, In: R.H.
Dunlop, and C-H Malbert (eels). VeterinalJ' Pathophysio/ogy.
Bl ackwe ll Publishing: Ames, Iowa . 259-276.
Van de Zancle, S. and E. M. Kuhn. (2007). Central nervous system
signs in chickens caused by a new av ian reovirus strain: a
pathogenesis study. Vet Microbiol 120:42-49.
Wight, P.A. L. and W. G. Siller. 1980. The pathology of deep
pectoral myopathy of broilers. Vet Pathol 17 :29-39.
Williams, S. M., G. Zavala, S. Hafner, S. R. Co llett, and S. Cheng.
2012 . Metastatic melanomas in young broiler chickens ( Gallus
gal/us do111esticus). Vet Pathol 49:288-291.
Wobeser, G. and J. Howard. 1987 . Mortality of waterfowl on a
hypersaline wetland as a res ult of salt encrustation . J Wild/ Dis
23 :127- 134.
Zava la G. , D. A. Anderson, J. F. Dav is, and L. Dufour-Zavala.
2011. Acute monensin toxicity in broiler breeder chickens.
Avian Dis 55:516-521.
Zimermann, F. C., L. C. 8 . Fallave na, C. T. P. Salle, H. L. S.
Moraes, R. A Soncini, M. H. Barreta, and V. P. Nascimento.
20 I 2. Downgrading of heavy broiler chicken carcasses clue to
myoclegeneration of the anterior latissimus dorsi: pathologic
and epiclemiologic studies. Avian Dis 56:418-42 l.
Avian Hi stopathology (4 th Edition) I 115
 H. Jol,11 Ba mes • Tal,see11 Abdul-Aziz • Oscar J. Fletcher
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I 4.1.
A

Normal skeletal muscle. Chicken. Both panels show

elongated sarcolemmal nuclei located centrally and peripherally.
B

4.3. Skeletal muscle. Neurogenic atrophy. 22-week-olcl

Central nuclei are normal in avian muscle. Cross-striations of
myofibers are evident in panel B. Striations are accentuated when
viewed with polarized light. Note motor end plate (arrowhead).
Motor end plates are rarely identified in H&E sections.
backyard chicken. Nerves in the perimysium are infiltrated with
lymphoid cells. Myofibers appear atrophic and are separated by
expanded endomysial spaces. The bird had Marek's disease with
lymphocytic neuritis involving the sciatic and other nerves.

4.2. Skeletal muscle. Atrophy. 15-clay-old broiler. Muscle
fibers are very small and thin, their nuclei are crowded, and appear
as if increased in number. The bird was from flock experiencing
runting-stunting syndrome. Myofiber atrophy in this case may be
due to malnutrition.
4.4. Skeletal muscle. Neurogenic atrophy. 22-week-olcl
backyard chicken. The majority of the myofibers are small
(atrophic), and the muscle fascicles are well defined clue to expansion
of perimysial spaces by fibrous tissue (perimysial fibrosis). The
muscle was supplied by nerves that were damaged by Marek's
disease virus (see 4.3).

116 I American Association of Avian Patholog ists


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4.5. Skeletal muscle. Neurogenic atrophy. 22-week-old
backyard chicken. The section illustrated in 4.4 was stained with
Masson's trichrome to demonstrate the perimysial fibrosis. The
collagenou s tissue in the perimysial spaces stains blue with this
sta in.
4.6. Skeletal muscle. Neurogenic atrophy. 22-week-old
backya rd chicken. Most of the myofibers are markedly atrophic
and so me assume roughly triangular shape. There is an apparent
expansion of the endomysial spaces. Nerves in the muscle had
lymphocytic neuritis caused by Marek 's disease virus (see 4.3).
Muscular System
4.7. Skeletal muscle. Lymphocytic myositis with muscle
atrophy and fat infiltration. 6-year-old backyard chicken.
I
Muscle fibers are variable in size. Some fibers are surrounded
by lymphocytes and others are missing and replaced by fat.
Replacement of muscle fibers by fat is characteristic for muscular
dystrophy. However, hereditary basis for this lesion could not be
established and the lymphocytic response is not usual feature of
muscular dystrophy. The definitive cause is unknown.
4.8. Skeletal muscle. Lymphocytic myositis with muscle
atrophy and fat infiltration. 6-year-olcl backyard chicken. This
Higher-power view of area in 4.7 shows the lymphocytic infiltration
and variations in myofiber sizes. Also note the replacement of
muscle by adipose tissue.
Avian Histopathology (4 th Edition) I 117
 H. John Bames • Tahseen Abdul-Aziz • Oscar J. Fletch er
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I 4.9. Superficial pectoral muscle. Myopathy. 42-day- old

broiler. Group of myofib ers are necrotic and their sa rcoplasm
4.11 . Myopathy. Superficial pectoral muscle. 44-day-olcl
broiler. There is necrosis of group of myofibers. The sa rcoplas m
is fragmented . Small num bers o f macroph ages and ve ry few is hya lini zed, fra gmented, an d undergoing lys is. This is another
heterophils are infiltrating the necroti c muscle fib ers. This les ion exampl e of myopath y as bas ic response fo llowing muscle injury.
is bas ic response fo ll owing damage to muscle, thus is not di sease
specific. Similar lesions are fo und in pectora l muscles affect ed with
the conditi ons referred to as " wooden breast' and " white strip ing".

4.10. Myopathy. Superficial pectoral muscle. 45-day-old
broiler. Myofibers are necroti c and swollen with so me showing
fragmentati on. There is an infi ltrati on of macropha ges and so me
heterophils.
4.1 2. Myopathy. Superficial pectoral muscle. 42-clay-old
broiler. Cross sectio n of pectoral musc le shows variability in
the size of myofibers. T he sa rco pl asm of several myofib ers is
vacuo lated. One myofib er is necroti c and infiltrated with very few
heterophil s. The endomys ium is ex panded by clear spaces and
contains fe w heterophils.

11 8 I Ameri ca n Assoc iati on of Av ian Pa th ologists

 Muscular System
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4.13. Skeletal muscle. Myopathy of the pectoralis major

("Wooden Breast"). 52-day-olcl broiler. Swelling and
4.15. Skeletal muscle. Myopathy of the pectoralis major
("Wooden Breast"). 52-clay-old broiler. Higher magnification of
I
fragmentation of muscle fibers in region of muscle are accompanied 4.14 shows lymphocytes and multifocal myofiber degeneration.
by multifocal scattered collections of lymphocytes and fibrosis.

4.14. Skeletal muscle. Myopathy of the pectoralis major 4.16. Skeletal muscle. Myopathy of the pectoralis major
("Wooden Breast"). 52-day-olcl broiler. Large collection of ("Wooden Breast"). 52-day-olcl broiler. Higher magnification of
lymphocytes in the expanded interstitial tissue, with degeneration affected region in the pectoralis major shows increased interstitial
of myofibers. space with fibrosis.

Avian Histopathology (4 th Edition) I 119

 H. Jol,11 Barnes • Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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I 4.17. Skeletal muscle. Myopathy of the pectoralis major
("Wooden Breast"). 52-da y-o ld broiler. Tri chrome stain shows
increased collagen in th e expa nded interstitial tissue.
4.18. Superficial pectoral muscle. Myopathy. 42-day-old
broiler. Regenerating myofiber with basophilic cytoplasm has
severa l ce ntrally located nuclei with prominent nucleoli. The nuc lei
are piled up or lined up in chai n. The space below the rege nerating
myofiber is probably created by lysis of myofibers and is infiltrated
w ith few heterop hil s.
120 I American Association of Avian Pathologists
4.19. Superficial pectoral muscle. Myopathy. 42-day-old
broiler. The myofibers at the top of the image are intact and show
cross striatio ns. The myofibers below the intact ones are ei ther lyt ic
or regenerating . Lytic myofibers are infiltrated by many heterophils.
The regenerating myofibers have basophilic cytoplasm and many
nuclei (some are lined up in chai n in the cen ter) with prominent
nu cleoli.
4.20. Superficial pectoral muscle. Myopathy. 33-week-old
broiler breeder hen. The sa rcoplasm of myofibers is undergo ing
necrosis and fragmentation and is infiltrated by few heterophil s. The
myofiber in the center is swo llen and its sarcoplasm is homogenous
and strongly eosinophilic (hya line degeneration). This was an
incide ntal findin g in the bird, and the ca use is unknown.

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4.21. Thigh muscle. Myopathy. 4-month-old backyard chicken.
Shown are loss of cross-striation, hyalinization, fragmentation, and
minerali zation of myofibers. Deposition of mineral was confirmed
with special stain. The lesion is not specific but compatible with
exertional myopathy. Microscopic lesions of exertional myopathy
are diffi cult to distinguish from those of nutritional myopathy due to
vitamin E deficiency.
4.22. Thigh muscle. Myopathy. 4-month-old backyard
ch icke n. This Higher-power view of area in 4.21 demonstrates
mineral deposits (dark blue areas) in degenerate myofibers.
Af11sc11/ar System
4.23. Skeletal muscle. Chronic myositis with mineralization.
28-week-old broiler breeder hen. Extensive necrosis and
I
mineralization of myofibers are accompanied by infiltration of
lymphocytes and macrophages. The insert illustrates mineralized
muscle fiber. The cause of this lesion is not known, but clu·onic
exertional myopathy is possibility.
4.24. Deep pectoral muscle. Myopathy (deep pectoral
myopathy). 40-week-olcl broiler breeder hen. Myofibers lack
nuclei, but otherwise have an intact sarcoplasm. The endomysial
spaces appear to be slightly expanded. The two blood vessels
contain nuclear debris and lysed necrotic erythrocytes . This is
characteristic lesion of ischemic necrosis.
Avian Histopathology (4 th Edition) I 121
 H. John Bames • Tahseen Abdul-Aziz • Oscar J. Fletcher
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4.25. Deep pectoral mu scle. Myopathy (deep pectoral
myopathy). 40-week-old broiler breeder hen. Hi gher-powe r
v iew of 4 .24 shows myofi bers w ith in tact sarcoplasm but abse nce
of nucle i.
4.26. Deep pectoral mu scle. Myopathy (deep pectoral
myopathy). 40-week-olcl broiler breeder hen. Longitudinal
secti on of deep pectora l mu scle shows ischemic necrosis
characteri zed by loss of the nuc lei in th e myofib ers. An in terstiti a l
blood vessel co ntain lyt ic erythrocytes and fibrin tlU'ombu s.
122 I A mer ica n Assoc iati o n of Av ian Patho log ists
4.27. Deep pectoral muscle. Myopathy (deep pectora l
myopathy). 40-week-old broiler breeder hen . Illustra ted is
di sco id necrosis in myofib er (the lower one) of deep pectora l
mu scle with myopath y (deep pecto ral myopath y). Di scoid
necrosis is characteri zed by tra nsverse fi ssures in myofibers. It is a
characteristic fea ture of ischemi c necros is.
4.28. Deep pectoral mu scle. Myopathy (deep pectoral
myopathy). 40-week-old broiler breeder hen. Artety w ith
tlu·ombu s is show n. There are loss of myofibers and fibropl as ia in
the area adjacent to the thromboti c artery.

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4.29. Deep pectoral muscle. Myopathy (deep pectoral
myopathy). 40-week-old broiler breeder hen. Shown is reactive
zone at the margin of ischemic myofibers. The zone consists of
fibrou s granulation tissue with mononuclear inflammatory cells and
small atrophied myofibers.
4.30. Add uctor muscle. Ionophore toxicosis. 8-week-old
meat-type turkey. There is swelling, sarcoplasmic hyalinization
and hypereosinophilia, segmental fragmentation and loss (necrosis)
of myofibers. Large numbers of macrophage infiltrate necrotic
myofibers to remove sarcoplasmic debris. Few heterophils are also
present. This is characteristic lesion of ionophore toxicity.
-
/1111sc11/ar System
4.31. Adductor muscle. Ionophore (narasin) toxicosis.
15-week-old turkey breeder hen. This field in the muscle section
I
demonstrates sarcoplasmic hyalini zation and segmenta l loss and
necrosis ofmyofibers . The increase in cellularity is due to infiltration
of macrophages to remove sarcoplasmic debris and proliferation of
satell ite cells to initiate regeneration of myofibers.
4.32. Adductor muscle. Ionophore (narasin) toxicosis.
15-week-old turkey breeder hen. Cross sections of muscle
demon strates hyaline degeneration, necrosis, and fragmentation of
myofibers and infiltration of macrophages and heterophils. Note the
macrophages infiltrating necrotic myofibers to remove sarcop lasmic
debris.
Av ian Histopathology (4' h Edition) I 123
 H. John Bames • Tahsee11 Abdul-A ziz • Oscar J. Fletcher
VetBooks.ir

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4.33. Trachea with tracheal muscle. lonophore toxicosis.
Tnrkey. This section of trachea shows diffuse trachea l muscle
damage with lesio ns characterized by loss of myofibers and
infiltration of macrophages.
4.35. Skeletal muscle. Oil-emulsion vaccine injection site.
14-week-old broiler breeder pullet. Breast muscle at the inj ection
si te of oi l-emulsion vaccine has multi focal areas of caseous necrosis
rimm ed by macrop hages and multinu cleated giant ce lls. The empty
spaces in the centers of caseo us necrosis are the mineral oil droplets
in the vaccine that were dissolved during tissue processing. Most
of the myofi bers in the area are replaced by edema and infiltrates of
mononuclear inflammatory cell s, including many plasma cells . The
term "o il granulomas" may be used to refer to thi s lesion.

4.34. Trachea with tracheal muscle. Ionophore toxicosis.
Turkey. This Higher-power view of area in trachea l muscle in
4.33 illustrates degeneration, necros is, and loss of myofibers wi th
increase in number of nuc le i due to infiltration of macrophages and
possibl y proliferation of satellite cells.
4.36. Skeletal muscle. Oil-emulsion vaccine inj ection site.
14-week-old broiler breeder pullet. Oil droplets (e mpty spaces)
and caseous debri s are rimmed by multinucleated giant cells and
surroun ded by wide, li ghtly stained areas of fibrobl astic reaction.
There are loss of myofibers, edema, and scattered mononuclear cell
infiltrates in the muscle tissue around the lesions.

124 I American Assoc iation of Avia n Pathologists


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4.37. Skeletal muscle. Oil-emulsion vaccine injection site.
14-week-o ld broiler breeder pullet. Typical caseous oil-granuloma
consists of caseous debris with an empty space in the center
(disso lved oil droplet) rimmed by macrophages and multinucleated
giant ce lls. Loss of myofibers, edema, and loose mononuclear cell
infilt rate are evident around the granuloma.
4.38. Skeletal muscle. Oil-emulsion vaccine injection site.
28-week-old broiler breeder hen. The oil adjuvant in the vaccine
has caused intense granulomatous inflammation in the muscle. The
clear spaces represent oil droplets that were dissolved during tissue
processing. Adjacent muscle fibers are variable in size with many
being necrotic.
--
Muscular System
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4.39. Skeletal muscle. Oil-emulsion vaccine injection site.
28-week-old broiler breeder hen. There are multiple caseous
granulomas, each consists of central core of caseous necrosis
surrounded by multi nucleated giant cells. Marked lymphohistiocytic
infiltrate is evident around the caseous granulomas . Note the clear
spaces that represent dissolved oil droplets.
4.40. Skeletal muscle. Oil-emulsion vaccine injection site.
28-week-old broiler breeder hen. This higher power view of
an area in 4.39 illustrates granulomatous myositis. Note the
multinucleated giant cells, loss of myofibers, and lymphohistiocytic
infiltrate.
Avian Histopathology (4 th Edition) I 125
 H. John Bames • Tah see11 Abdul-Aziz • Oscar J. Fletcher

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I 4.41. Skeletal (lumbar) muscle. Avian encephalomye litis.
18-day-old broiler. Multi foca l collectio ns of lymph ocytes are
,I

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I

scattered throu gh thi s secti on of lumbar musc le . Lymphocytes are
show n at hi g her magnifi cati o n in the inse rt.
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4.43. Skeletal mu scle. Gangrenous dermatitis. 11-week-old
chukar partridge. Gra m-stained secti on shows many intral es ional
Gra m-pos iti ve rod- shaped bacteri a morph ologica ll y resembling
Clostridi11111 spp. in areas of myofib ers undergoing lytic necrosis.

4.42. Skeletal mu scle. Gangrenou s dermatitis. 11 -week-
old chukar partridge. T he les ion is characterized by co mpl ete
di ssolutio n (lys is) of the sa rcoplasm of myofib ers, w ith many
intra les ional rod- shaped bacteria mo rph ologica lly rese mbling
Closlridi11111 spp. The bird had gross lesions of ga ng reno us
derm atiti s fro m whi ch Clostridi11111 septic11111 was isolated . The lyt ic
necrosis of myofibers is ca used by th e Clostridi11111 toxin . Note the
absence of infl amm ato ry respo nse.
4.44. Skeletal mu scle. Gan grenous dermatitis. 42-clay-old
broiler. Show n is partia l or compl ete lys is of the sarco plasm
of myofib ers, with many intra les io na l rod-shaped bacteri a
morph ologicall y rese mbling Clostridiw11 sp . Blood vesse l (lower
left co rner) contains nu clei of lysed erytlu-ocytes. The necrosis of
myofi bers and the intravasc ular hemo lys is are caused by Clostridi11111
tox in . T he bird had seve re les ions of ga ngreno us derm at itis, and
Clostricli11111 septic11111 and Streptococc11s sp. were isolated from
lesions in the subcutaneous ti ssue .

126 I Ameri ca n Assoc iati on of Av ian Path olog ists

 !H11sc11/ar System
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4.45. Skeletal muscle. Gangrenous dermatitis. 42-day-olcl

broiler. Gram-stained section demonstrates many intralesional
Gram-positive rod-shaped bacteria morphologically resembling
C/ostridi11111 spp. in an area with damaged myofibers. See figure
4.44 fo r H&E stained section.
4.47. Bacterial myositis. 4-day-old broiler breeder pullet.
Area of necrosis in the breast muscle, with intralesional bacteria
I
morphologically compatible with Pse11do111onas sp. This is one of
several necrotic foci in the section . The bird also had pericarditis
and hepatic serositis (septicemia), and Pse11do111011as aeruginosa
was isolated from the pericardia! sac.

4.46. Skeletal muscle. Gangrenous dermatitis. 45-day-old
broiler. The fascia of superficial pectoral muscle is necrotic and
contain numerous rod-shaped bacteria, which are also present in the
expanded endomysial spaces. Myofibers show coagulative necrosis
and seg mental lysis. Blood vessels are filled with the nuclei oflysed
erytlU'ocytes, an indication of hemolysis caused by the C/ostridi11111
toxin.
4.48. Skeletal muscle. Mycotic myositis. 5-week-old broiler
breeder pullet. Large area of necrosis has prominent peripheral
infiltrate of lymphocytes and macrophages. This lesion was one
of multiple lesions in various organs including kidneys and air
sacs. The muscle lesion likely was an extension of severe mycotic
infection in air sacs .

Avian Histopathology (4 th Edition) I 127

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 H. Jol,11 Ba mes • Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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I 4.49. Skeletal muscle. Mycotic myositis. 5-week-old broiler

breeder pullet. This Higher-power view of area in 4.48 shows the
zone of lymphohistiocytic infiltrates between necrotic ti ssue and
viable myofibers .
4.51. Skeletal muscle. Sarcocyst. One-year-old backyard
turkey. Sarcocyst of the protozoan Sarcocystis sp. is within the
sarcoplasm of myofiber. The cyst has relatively thick wall and is
packed with braclyzoites . Note the absence of any inflammatory
response.

-. -:. ..
•
•

4.50. Skeletal muscle. Mycotic myositis. 5-week-old broiler

breeder pullet. This high-power view of section of the same muscle
in 4.48 and 4.49 demonstrates necrotic debris and necrotizing
myofibe rs. Fragments of fungi (arrow) are visible. Occasional
longer hyphae (insert) may be seen within the lesion.
''
4.52. Skeletal (tracheal) muscle. Sarcocyst. 1.5-year-old
aracari (toucan). Sarcocyst of the protozoan Sarcocystis sp.
is with in the sarco plasm of myofiber. The cyst is packed with
bradyzoites. Note the absence of any inflammatory response.

128 J Ameri can Association of Avian Pathologists


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4.53. Skeletal muscle. Marek's disease. 31-week-old broiler
breeder hen. Area in the muscle is infiltrated, effaced and replaced
by dense population of pleomorphic lympho id cells. Skeletal
muscle is not common site of Marek's disease tumors.
4.54. Skeletal muscle. Marek's disease. 31-week-old broiler
breeder hen. Most of the myofibers are replaced by neoplastic
lymphoid cells. There is segmental loss of myofibers. Remaining
myofibers are thin (atrophied).
--
A1uscular System
4.55. Skeletal muscle. Marek's disease. 31-week-old broiler
breeder hen. Skeletal muscle. Marek's Disease. 31-week-old
broiler breeder hen. The lymphoid cell infiltrate in Marek 's disease
consists of pleomorphic lymphoid cells. Segment of myofibers is
still present.
4.56. Skeletal muscle. Rhabdomyosarcoma. 9-year-old
conure. The tumor is composed of elongated to fusiform cells that
are arranged haphazardly. The cells have abundant eosinophilic
to lightly basophilic cytoplasm that lacks cross striation.
Multinucleated cells are common and their presence is characteristic
feature of rhabdomyosarcoma.
Avian Histopathology (4 th Edition) I 129
 H. Jol,11 Bar11es • Tah see11 Abdul-Aziz • Oscar J. Fletcher
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Proximal Tarsometatarsus
Distal Tibiotarsus

I 4.57. Distal tibiotarsus and proxim al tarsometatarsus.

Relatively normal. One-week-old turkey. This sagitta l section
4.59. Digital flexor tendon. Tenosynovitis. One-week-old
turkey. Hi gher-power view of area in the synov ial space in 4 .58
illustrates the rel at ionships between the distal tibiotarsus and showi ng heterophilic tenosynovitis.
proximal tarsometatarsus and shows the j oint space (J S) of the
intertarsa l joint, portion of the synovium (S), and the digital flexor
tendons. Ca rtil age (*) is normal for thi s early age.

4.58. Digital flexor tendon. Tenosynovitis. One-week-old 4.60. Digital flexor tendon. Normal. One-week-old turkey.
turkey. Mild teno synovitis characterized by mild accumul at ion of Low-power view of the histological appearance of tendon.
heterophil s in sy novia l space (*). This tenosynovitis was ca used by
Staphy lococcus a11re11s.

130 I America n Assoc iat io n of Av ian Patho logists

 Muscular System
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4.61. Digital flexor tendon. Normal. One-week-old turkey.

Hi gher-power view of the histological appearance of tendon.
4.63. Tendon. Bacterial tenosy novitis. 18-week-old broiler
breeder pullet. Hig her-power view of the boxed area in 4.62
I
showi ng th e caseous necrosis and intrales ional bacteria.

4.62. Tendon . Bacterial tenosynovitis. 18-week-old broiler 4.64. Tendon. Bacterial tenosynovitis. 18-week-old broiler
breeder pullet. Lyrnphocytic and heterophili c ex udate expands the breeder pullet. Higher-power view of area in 4.63 showing
tendo n sheath s and peritendonal region. Region of caseous necrosis necrosis and numerous intralesional bacteria.
is within the box. Staphylococcus aureus was isolated.

Avian Histopathology (4 th Edition) I 131

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4.65. Tendon. Bacterial tenosynovitis. 18-week-old broiler 4.67. Tendon. Reovirus tenosynovitis. 14-day-old· broiler.
breeder pullet. Higher-power view of area in 4.64 showing caseous Higher-power view of area in 4.66 showing lym phocytic and
necrotic debris with bacteria, and some fibrinoheterophilic exudate. fibrinoheterophilic tenosynovitis .

4.66. Tendon. Reovirus tenosynovitis. 14-day-old broiler. 4.68. Tendon. Reovirus tenosynovitis. 14-day-old broiler.
Lymphocytic and heterophilic infiltrates expand the synovial space Higher-power view of area in 4.67 showin g lymphocytic infiltrate
and synovia l sheath . Small amounts of fibrin are present. and fibrinoheterophili c exudate.

132 I American Association of Avian Patholog ists

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4.69. Tendon. Reovirus tenosynovitis. 14-day-old broiler. 4. 71. Tendon. Reovirus tenosynovitis. 21-day-old broiler.
illustrated is fibrosis around and within tendon. Higher-power view of 4. 70 showing fibrinoheterophilic component
in addition to lymphocytes and synovial hyperplasia.

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4.70. Tendon. Reovirus tenosynovitis. 21-day-old broiler. 4.72. Tendon. Reovirus tenosynovitis. 21-day-old broiler.
Thickening of the synovium clue to hyperplasia ofsynovial epithelial Higher-power view of area in 4.71 showing fibrinoheterophilic and
cell s and infiltration of lymphocytes. Small amount of fibrin is in lymphocytic tendonitis and synovitis.
the sy novial space.

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 H. Jol,11 Barnes • Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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'
\

'

I 4.73. Tendon. Reoviru s tenosynovitis. 21-day-olcl broiler.

Higher-power view of area in 4.72 showing fibrinoheterophilic
4.75. Tendon. Reoviru s tenosynovitis. 21-clay-olcl broiler.
Hi g her-power v iew of area in 4.74 showing hyperplasti c and
exudate. lymphocytic synovitis with fibrin and heterophils in this tendon
sheath.

4.74. Tendon. Reovirus tenosynovitis. 21-day-old broiler. 4. 76. Tendon. Reovirus tenosynovitis. 10-day-olcl broiler.
Higher-power view of region in 4 .73 w ith synovial hyperp lasia and Thrombus is in blood vessel adjacent to tendon. Lymphocytic
lymphocytic synovitis. tenosynovitis is a lso seen.

134 I A merican Assoc iation of Avian Patholog ists

 Muscular System
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4.77. Tendon. Reovirus tenosynovitis. 10-day-old broiler. 4. 79. Tendon. Reovirus tenosynovitis. 35-day-old broiler.
Higher-power view of the thrombus in 4.76 . Note the adjacent Higher-power view of area in 4.78 showin g the heterophilic exudate
infl ammation. in synovial space.

4. 78. Tendon. Reovirus tenosynovitis. 35-clay-olcl broiler. 4.80. Tendon. Reovirus tenosynovitis. 35-clay-old broiler.
The tendon sheath is markedly thickened due to fibrosis and Higher-power views of the heterophilic exudate in the synovial
lymphohistiocytic infiltration. Large region of heterophilic space in 4.79 .
infiltration is also seen.

Avian Histopathology (4' h Edition) I 135

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 H. Joh11 Barnes • Tahsee11 Abdul-A ziz • Oscar J. Fletcher
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\i)\\:· · t/'',
• I
(A

I 4.81. Tendon. Reovirns tenosynovitis. 35-day-old broiler.

Higher-power views of the heterophilic exudate in 4 .80 .
)r,_·;r·/f'.,·
.-:-· ~,\- '?I'. •. ·
~\~·t=~~~~ ..:).Jj; ,·
4.83. Tendon. Reovirns tenosynovitis. 53-day-old broiler.
Hi gher-power view of the region is the larger box in 4.82 showing
synovial hyperplasia (arrow) and nodular collection of lymphocytes
(box). Note the tendon in lower left area is replaced by fibrou s
tissue.

4.82. Tendon. Reovirns tenosynovitis. 53-day-old broiler. 4.84. Tendon. Reovirns tenosynovitis. 53-day-old broiler.
Tendons are replaced and surrounded by fibrous tissue . Two regions Higher-power view of the region at the arrow in 4.83 showing
(boxes) show synovial hyperplasia. synovial hyperplasia.

136 I American Association of Avian Pathologists

 Muscular System
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4.85. Tendon. Reovirus tenosynovitis. 53-day-old broiler. 4.87. Tendon. Reovirus tenosynovitis. 53-day-old broiler.
Hi gher-power view of the region in the smaller box in 4.82 showing Higher-power view of the boxed area in 4.83 showing the nodular
synovial hyperplasia and fibrosis of tendons. collection of lymphocytes (box) and plasma cells (arrow).

4.86. Tendon. Reovirus tenosynovitis. 53-day-old broiler. 4.88. Tendon. Reovirus tenosynovitis. 14-day-old broiler.
Hi gher-power view of area in 4.85 and the small box in 4.82 shows Lymphoplasmacytic tenosynovitis and synovial hyperplasia are
synovial hyperplasia. prominent lesions .

Avian Histopathology (4 th Edition) I 137

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 H. Jol,11 Bames • Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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I 4.89. Tendon. Reovirus tenosynovitis. 14-day-old broiler.
Higher-power view of area in 4.88 demonstrates lymphoplasmacytic
tenosynovitis and synovial cell hyperplasia.
4.90. Tendon. Reovirus tenosynovitis. 14-day-old broiler.
Shown are fibrosis of the tendon and lymphoplasmacytic
tenosynovitis.
138 I American Association of Avian Path ologists
4.91. Tendon. Reovirus tenosynovitis. 14-clay-olcl broiler.
Nodular collection of lymphocytes is surrounded by diffuse
population of lymphocytes . These lesions cannot be differentiated
from those caused by ivfycoplas111a synoviae.
4.92. Tendon. Reovirus tenosynovitis. 21-day-old broiler. The
tendons are surrounded by thick sheath of lymphocytes in nodul ar
and diffu se patterns. Fi brinoheterophilic exudate is also present in
the synovial space.

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4.93. Tendon. Reovirus tenosynovitis. 21-day-old broiler.
Hi gher-power view of area in 4.92 demonstrates the dense
infiltration of synovial sheath with lymphocytes.
[J
4.94. Tendon. Reovirus tenosynovitis. Chicken. Acute
hemorrhage (box), peritendonal fibrosis , and scattered nodular
collections of lymphocytes (arrows) are lesions associated with
older (classical) isolates of Reovirus.
M11sc11/ar System
4.95. Tendon. Reovirus tenosynovitis. Chicken. Higher-power
view of the boxed area in 4.94 showing foci of acute hemorrhage,
I
fibrosis, and two nodular collections of lymphocytes.
4.96. Tendon. Reovirus tenosynovitis. Chicken. Higher-power
view of area (left arrow) in 4.94 shows two nodular collections of
lymphocytes .
Avian Histopatbology (4 th Edition) f 139
 H. John Barnes • Tahseen Abdul-Aziz • Oscar J. Fletcher
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I 4.97. Tendon. Reoviru s tenosynovitis. Chicken. Hi gher-power

v iew of area (box) in 4.94 show ing hemorrhage with thrombocytes.
4.99. Tendon. Reovirus tenosynovitis. Chicken. Higher-power
view of nodular collection of lymph ocytes in 4.96.
Thi s region co uld be the edge of ruptured tendon.

4.98. Tendon. Reoviru s tenosynovitis. Chicken. Hi gher-power 4.100. Tendon. Ruptured tendon. 44-week-old broiler
view of4.97. breeder chicken. Multiple thrombi are in the edge of this tendon.
Lymphocytic inflammation is minimal, suppotting the idea that the
ca use may be mec hani ca l and not infectio us.

140 I American Association of Av ian Patholog ists


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4.10 1. Tendon. Ruptured tendon. 44-week-old broiler breeder
chicken. Higher-power view of area in 4.100.
4.102. Tendon. Ruptured tendon. 44-week-old broiler breeder
chicken. Higher-power view of area in 4.101.
--
Muscular System
4.103 . Tendon. Mycoplasma sy1101'iae infection. 23-week-
old broiler breeder chicken. Nodular and diffuse collections
of lymphocytes expand the tendon sheaths. Synovial epithelium
is hyperplastic. This lesions cannot be diffe rentiated from those
caused by Reovirus .
4.104. Tendon. Mycoplasma synol'iae infection. 23-week-old
broiler breeder chicken. Higher-power view of area in 4.103
demonstrates nodular and diffuse lymphocytic infiltrates.
Avian Histopathology (4 th Edition) I 141
 H. Jo/,11 Ba mes • Ta/,see11 Abdul-Aziz • Oscar J. Fletc/,er
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4.105. Tendon. Mycop!asma sy11011iae infection. 23-week-old

broiler breeder chicken. Hi g her-power v iew of 4.104 show ing
nodu lar and diffuse collections of lymp hocytes.

4.106. Tendon. Mycoplasma sy11011iae infection. 23-week-old

broiler breeder chicken. Higher-power view of 4.105 with nodular
and diffuse collections of lymphocytes.

142 I Amer ica n Association of Av ian Pathologists

VetBooks.ir
CHAPTER
Cardiovascular System
Tahseen Abdul-Aziz • Oscar J. Fletcher
Anatomy and Histology of Heart
The ca rdiovascular system includes the heart and the arteries, veins,
capill ari es, and lymphatics that are distributed throughout the body.
The av ian heart is conical, lies in the midline within the thoracic
cavi ty, just behind the thoracic inlet, and is enclosed within the peri-
cardia! sac that contains serous fluid . It has four chambers, two
ventricles and two atria. The left ventricle is approximately 4 times
larger than the right. The right ventricle extends only about two
thirds of the way to the apex of the heart; the apex is formed solely
by the left ventricle. The left atrioventricular valve of birds lacks
defined cusp s and appears as a membranous sheet attached to chor-
dae tendineae, which in turn are attached to papillaty muscles on
the wa ll of the left ventricle. The right atrioventricular valve is a
tri angular muscle flap or plate that arises from the muscle wall of the
right ventricle and closes against the interventricular septum. The
anatomy of the right atrioventricular valve makes birds susceptible
to va lvular insufficiency and right heart failure. The major blood
vessels that enter or leave the heati include the aorta, pulmonary
arte1y, common pulmonary vein, anterior vena cava, and posterior
vena cava. The exit from the left ventricle to the aorta is controlled
by the aortic valve, which consists oftlu·ee semilunar cups . A simi-
lar va lve controls exit of the pulmonary artery from the right ven-
tricl e. Dense connective tissue that undergo es cartilagenous meta-
plasia with age is located at the base of the valves and extends into
the adjacent myocardium.
The histologic structure of the left atrioventricular valve in
chickens differs from that of mammals . In sections stained with
H&E, the peripheral zona spongiosa of the valve has a characteris-
tic edematous, fibrillar appearance and consists of spindle-shaped
fibrobl asts, mesenchymal-like cells, and small bundles of thin col-
lage n fibers embedded in homogenous edematous-looking ground
substance. The centrally located zona fibrosa is composed predomi-
nantly of collagen bundles, which appear thicker and more compact
than those in the zona spongiosa.
Heart muscl e (myocardium) consists of bundles of muscle fi-
bers (cardiac myocytes) bound together by small amounts of con-
nec tive tissue. Cardiac myofibers are long, cylindrical, branching
cells with usually a single, ovoid to elongated nucleus located cen-
trally within each cell. The long axis of th e nucleus is parallel to that
of the fibers. Cardiomyocytes in birds have smaller diameters than
those in mammals. This permits faster depolarization and more rap-
id heart rates. Each muscle fiber is made of numerous myofibrils,
whi ch lie parallel to each other within the sarcoplasm (cytoplasm)
5
and are enclosed by sarcolemma (plasma membrane). Spaces be-
tween muscle fibers are filled by a delicate network of suppo1iing
tissue that contains an extensive network of capillaries . A large
amount of fat is sometimes found in the myocardial interstitium of
obese birds .
The inner layer of the heart is the endocardium, the surface
of which consists of a single-cell layer of endothelial cells that is
continuous with the endothelium of vessels entering and leaving the
heart. There is a thin, delicate suppo1iing layer of collagenous and
elastic tissue in the subepithelium. The external surface of the heart
is the epicardium (also called visceral pericardium), which consists
of a single-cell layer offlat epithelial cells, the mesothelium. These
cells also line the parietal surface of the pericardia! sac. Variable
amounts of adipose tissue and small parasympathetic ganglia may
be found in the epicardium . A focal area of epicardial fibrosis may
be found near the apex of the heart where it touches the sternum.
This accumulation of loose connective tissue is referred to as a "fric-
tion rub" or " callous" as it results from rubbing of the heati against
the sternum as the heart beats.
Large specialized cardiac muscle fibers called Purkinje fibers ,
which comprise the conducting system of the heart, are found be-
neath the endocardium, both as single fibers or well-developed
tracts, and within the myocardium, usually in association with blood
vessels. Purkinje fibers in birds are relatively larger than those of
mammals, and they are easy to recogni ze because of their large si ze
and pale cytoplasm . Collections of extramedullary hernatopoietic
cells within the interstitium are normal in the avian heart. Occasion-
al small , discrete nodular aggregates of lymphoid cells are found
in the myocardium of clinically normal birds. Both hematopoietic
cell foci and lymphoid cell foci may be mistakenly interpreted as
lesions.
Histology of Blood Vessels
Blood vessels can be divided into elastic arteries , muscular arteries,
arterioles, veins, venules, and capillaries. Walls of large blood ves-
sels are composed from inner to outer of 3 concentric layers: tunica
intima, tunica media, and tunica adventitia. The tunica intima is
often thin and may be identifiable at low magnification. It consists
of a single-cell layer of endothelial cells supported by subendo-
thelial connective tissue. The tunica media of muscular arteries
is comprised predominantly of circularly arranged smooth muscle
between which pass a few elastic fibers. The ti.mica media of elastic
arteries is broad and consists of concentrically fenestrated sheaths of
Avian Histopathology (4 th Edition) I 143
 Tahseen Abdul-Aziz • Oscar J. Fletcher
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elastic fib ers separated by some coll age nous tissue and rel atively few
muscle fibers. The tunica adventitia is co mposed of lo ose co nnec-
ti ve tissue of predominantly collagen fibers with fewer elastic fibers;
the cellular co mponent of thi s layer consists mainly of fibroblasts.
The tunica adventitia of some large blood vessels contains numerous
small mterioles (vasa vasorum), which provi de nutrients to the walls
of the vessels.
Condensed elastic fibers form a well-defined lamina (internal
e lasti c lamina) that se parates th e tunica intima from the tunica me-
di a . A less-defi ned external elastic lami na separates the tunica media
from the tuni ca adventitia. In small mu scul ar arteries and large ar-
terioles, e lastic fibers are decreased and only a thin internal e lastic
lamina may be recog ni zed, there is no external elasti c lamin a. The
tunica adventitia may be as thi ck as the tuni ca medi a and merge
with surrounding collagenous ti ssues. In small arteri oles, the tu-
I
ni ca intima is only di sting ui shed by nuc lei of endotheli a l cells. The
tuni ca medi a consists of a layer of smooth muscle cells 2 to 3 cells
thick, and an adventiti a that merges imperceptibly with surrounding
suppo11ing tissues. In the lung, and perhaps elsewhere, sma ll muscu-
lar arteri o les respond to pressure by hypertrophy of mu scle ce ll s
reducing the size of th e lumen.
Veins have thinner walls, relati ve ly less mu scle tissue in the tu-
ni ca medi a, and a tuni ca adventiti a thicker than the ti.mi ca media .
Because of these feat ures, veins do not reta in their shape. They
often appear irregular in histol ogic sections, and their lumen may
not appear to be patent. Lymphatic vesse ls have s imil ar feat ures.
Sma ll- and medium-sized ve ins have a thin tunica medi a of ci rcu-
larl y arranged smooth muscle fibers and a thi ck tunica adventitia of
longi tudin a ll y arranged colla ge n fibers. Medium-sized veins have
a relatively thick tuni ca media consisting of several layers of smooth
mu scle separated by laye rs of collagen fibers and a ti.mica adventiti a
that is composed of a thick layer of collage n and elastic fibers. In
large veins, the tunica media is reduced to a thin muscular layer, but
the adventiti a is a thi ck la yer of co ll agen fibers between w hi ch are
thick elastic fibers .
In capillarie s, a o ne-cell thickness layer of endothelial cells
is discernible but mu scul ar and adventitial layers are absent. Oc-
casionally embracing the endothelial cells are flattened cells called
pericytes that have contractile fun ctions. The diameter of capillar-
ies is usually that of red blood cells except in the lung where ca pillaries
have a sma ller diameter than erythrocytes . Capillaries in the spleen
have hi gh endotheli al cells, fenestrations between the endothelial
cell s, and are su rrounded by shea th s of phagocyti c hi stiocytes and
dendritic cells.
Cardiomyopathies
Ca rdiomyo pat hy is defined as a disease of the myocard ium that is
associated w ith cardiac dysfunction. It usually reflects impaired
cardiac performance or cardiac failure. Cardiac myocytes do not
proli ferate but ca n undergo hype rtrophy in response to increased
wo rk load . Increased cardi ac wo rk load results from increased de-
mands for oxyge n, and/or increased resistance to blood flow fol-
lowin g constriction, ste nosis, obst ru cti o n, o r obliteratio n of arter-
ies, arterio les, and cap illari es. Hypertrophy of cardiac myocytes
res ults in thi ckenin g of the ventri cu lar wall, which leads to a redu c-
144 I Ameri can Assoc iati on of Avia n Pathologists
tion in ventricular volume. Card iac enlargement due to hypertro-
phy ofmyofibers is ca lled hypertrophic cardio111yopathy, which ca n
lead to heart failure. Dilated cardiomyopathy is characteri zed by
dilation of one or both ventricles and thinning of the walls of af-
fected ventricles. Dilated ventricles are unab le to effectively pump
blood from the hea rt. As a result , blood backs up into the atri a and
blood vessels, which results in pulmonary congest ion and edema,
generali zed venous co ngesti on, and in th e worst cases, asc ites. Re-
stricti ve (ob literative) cardio111yopathy refers to any disorder of
the hea rt in which th e ventricles do not adequate ly fill w ith blood
between heai1 beats beca use of les ions in the myocard ium, pericar-
dium , or endoca rdium .
T he terms hypertrophic card iomyopathy and dilated cardiom y-
opathy are more useful in gross pathology than they are in hi stopa-
thology as there are no defining hi stol ogic changes. In some cases
of dil ated ca rdiom yopathy, myofibers become thinner than normal,
wavy, and disorgani zed, and th ere may be loss ofmyofibers with an
increase in interstitial connective tissue. Cha racteri stic, althou gh
not typ ica l, microscopic les ions in severe cases of hype11roph ic
cardiomyopathy include, di sa rray, hypertrophy, and increased cyto-
plasmi c basophilia of myofibers, with interstitial fibrosis. Fibrosis
is see n in restrictive ca rdiom yopathy. Frequently thi s is the res ult of
clu·oni c pericarditis when inflamm ation undergoes orga ni zation and
the subsequent fibrous ti ssue co ntracts.
Pulmonary hypertensio n syndrom e (PHS ) in broiler chi ckens
is a c lass ic example of ri ght ve ntricular hype11rophy and failure.
The structure of the av ian heart (thin-wall ed right ventricle and mu s-
cular right at rioventricular valve) and the structi.ire and physiology
of the avia n lungs are important fac tors that contribut e to the sus-
ceptibility of birds to ri g ht ventri cul ar fa ilure secondary to pulmo-
nary hypertension . In clu-onic cases of PHS in broiler chickens, th e
myoca rdium may have histol ogic lesions characteri zed by variabl e
degrees of myofiber degeneration (swelling and fragmentation ),
occasional hya line depos its within myofibers, multifocal necrosis,
edema, and fibro sis. These les ions result from, rather than cause,
pulmonary hypertensio n and may be seen in ri ght ventricular failure
from other causes.
Spontaneous ca rdiomyopathy of turkeys (round-heart disease),
is an example of dilated cardiomyopathy characterized in young
turkeys by dilation of both ventri cles, with the ri ght ventricle often
more d il ated than the left. The dilated ri ght ventricle has a thin ,
flabb y wall. The primary hi sto pathologic lesion is foca l myofi-
ber degeneration wi th vacuol at io n. E nl argement of muscle nuc lei
and dil ation of capillaries may be present as seco nd ary lesions. In
chronic cases, endocardial fibroelastosis that can include fibro ca rti -
lagenous ti ssue may occur in the left ventricle.
Card iac lesions in adult turkeys affected w ith round-hea11 di s-
ease are enlargement and hypertrophy of the left ventricle. Fura-
zolidone-i nduced card iomyopathy is another exa mpl e of dilated
cardiomyopathy and the hi stologic lesio ns are simil ar to those of
spo ntaneo us cardiomyopathy of turkeys.
Endocardial Fibroelastosis
Endocard ial fibro elastosis is usually a foca l, but sometimes diffuse,
increase in collagenous and elastic fibers immediately beneath the

endoca rdium. It is a common lesion in the left ventricle in dilated
cardi omyopathy (e.g., cardiomyopathy in turkeys). The lesion like-
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ly res ults from increased prolonged pressure within the ventricle.
Microscopically, advanced lesions are characterized by a thick hy-
poce llular layer of collagen and elastic fibers of normal structure
just beneath the endocardium . Collagen and elastic fibers usually
extend into and disrupt the myocardium. Early lesions consist of
subendotheli al edema and fibroblast proliferation.
Myocardial Scarring
Cardiac myocytes cannot regenerate following irreversible dam-
age. Following acute injury to cardiac muscle, necrotic tissue is
progressively removed by heterophils and macrophages and re-
placed by granulation tissue which eventually forms a fibrous , col-
Jagenous scar.
Valvula r Endocardiosis
Valvul ar endocardiosis in birds refers to noninflammatory thicken-
ing of a heart valve, usually the left atrioventricular valve . Affected
val ves appear grossly thickened and are usually firm and smooth.
Hi stologic lesions include fibrous tissue proliferation, extracellular
depos ition of mucinous material, and sometimes chondroid meta-
plasia. True myxomatous valvular degeneration (also known as en-
doc ardiosis), which occurs in mammals has not been documented
in birds. The normal edematous, mesenchymal appearance of the
avian left atrioventricular valve may be mistakenly interpreted as
endoca rdiosis.
Toxicities
Certain toxicoses may be associated with myocardial lesions that
include myofiber degeneration (swelling, loss of cross-striation,
hyalini zation), fragmentation , multifocal necrosis, interstitial ede-
ma, and/or fibrosis. Ionophore toxicosis may produce a range of
degenerative changes in myofibers but usually without the mineral-
ization that is frequent in degeneration and necrosis resulting from
vitamin E/selenium deficiency. Other causes ofmyofiber degenera-
tion and necrosis include furazolidone toxicosis, toxic fat syndrome
(dioxin toxicosis), silver and cobalt toxicoses, selenium toxicosis,
copper deficiency, and poisonous plants (e.g. , Cassia, Crotalaria,
etc.) toxicoses. Epicardial and subendocardial fibrosis are chronic
lesions that follow edema and may be changes caused by toxicosis
from monensin, rapeseed oil or meal when used as a protein source,
soybea n oil, or polychlorinated biphenyls . Fat can accumulate in
myofib ers in fatty-hemorrhagic liver syndrome and in rapeseed oil
(erucic acid) toxicosis. In Vitamin D3 toxicosis, calcium deposits
occur in the wall of a1teries. Avocado (Persea americana) is car-
diotoxic for several species of birds including budgerigars, canaries,
cockatiels, and ostriches. Histologically, there is myocyte degenera-
tion with variable inflammatory infiltrates.
Atherosclerosis
Atherosclerosis refers to thickening of arterial walls through the
accumulation of lipids and sometimes lipid-laden macrophages
(foamy macrophages with fine cytoplasmic lipid droplets) with or
without collagenous tissue. In birds, the lesion occurs most often in
the thoracic aorta and brachiocephalic arteries. The microscopic ap-
Cardiovascular System
pearance depends largely on the severity and stage of development
of the lesion . Atheromatous plaques are characterized by accumu-
lation of lipid in arterial walls. Atheromatous plaques with col-
lagenous fibers are termed fibroatheromatous plaques. Chondroid
metaplasia is a conunon and sometimes the most obvious lesion in
the walls of affected arteries . Mineral deposition in the lesions is
sometimes seen. Lesions can be produced by diets high in choles-
terol and genetic factors influence their occurrence. Marek 's di sease
herpes viral infection is associated with atherosclerosis in chickens.
Arterial Fibromuscular Dysplasia
Fibromuscular dysplasia (FMD) is a non-inflammatory, non-athero-
sclerotic lesion in the wall of a1teries that ultimately leads to nar-
rowing of the vessel lumen. Lesions of FMD vaiy depending on
the predominant arterial wall layer involved. Tluee primary types
are identified: intimal fibroplasia, medial dysplasia, and adventitial
(periarteriolar) fibroplasia. Medial FMD can be further divided into
medial hyperplasia/hypertrophy and medial fibroplasia. Fibromus-
cular dysplasia can be found as incidental observation at almost any
age and is more commonly found in turkeys than chickens.
Miscellaneous Non-Infectious Conditions
The epicardium is a common site for urate deposition in visceral
gout. Visceral gout results from renal failure or metabolic disorders.
Mild deposits may be completely dissolved in formalin fixative and
disappear in histologic sections. However, in severe cases, urates
are seen as a layer of faintly basophilic and amorphous, feathe1y, or
crystalline material on the epicardial surface .
Lipofuscin appears as yellow-brown granules in the cytoplasm
of cardiac myocytes in the heaits of old birds.
Fat infiltration in the myocardium may be excessive in obese
birds. Adipose tissue usually replaces subendocardial myocytes but
may infiltrate deeply in the myocardium.
Amyloidosis is characterized by deposition of amorphous, eo-
sinophilic material (amyloid) in tissues and walls of blood vessels
and sinusoidal vascular spaces.
Infections
Viral infections
Some viral infections can result in myocardial hemorrhage, edema ,
necrosis, and, if the bird survives the acute phase, inflammation
and fibrosis. Alternatively, significant damage to the myocardium
with limited or subtle microscopic changes also can result from vi-
ral infections of the heart. Avian influenza (AI) virus can cause
edema and multifocal degenerative and necrotic changes in myofi-
bers. Inununohistochemistry reveals much more AI viral antigen in
both nuclei and cytoplasm of myofibers than one might expect from
the changes seen in H&E-stained sections. Some viruses, includ-
ing parvovirus of geese and polyomavirus, produce inclusions in
the nuclei of myofibers. Myocardial hemorrhage occurs in cases of
acute polyomavirus myocarditis. Avian encephalomyelitis (AE) vi-
rus causes increased lymphoid foci in the myocardium. In some cases
of AE, diffuse lymphocytic myocarditis of the atrial walls can be
extensive . Lymphocytic myocarditis and pericarditis is often found
in young chickens and turkeys infected with reoviruses that also
Avian Histopathology (4th Edition) I 145
 Tahseeu Abdul-A ziz • Oscar J. Fletcher
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cause vira l arthriti s/tenosynovitis. Ly111phohistiocytic 111yocarditis
with myofiber necrosis caused by reovirus has been rep01ted in 9- and
I I-clay-old broiler breeder pullets. Reovirus can cause severe multifo-
cal or regionally extensive myocarditis in turkey poults. The lesion
consists of marked infiltration of the myocardiu111 with ly111phocytes
mixed with macrophages, plas ma cells, and sometimes heterophils.
There may be areas of 111yoca rdial degeneration and necrosis with
similar cellul ar infiltrates as well as multi nucleated giant cells. East-
ern equine encephaliti s virus, Highlands J virus, and West Nile virus
cause necrosis and lymphocytic inflammati on in the myocardium .
Lymphoplasmacytic infiltrates may be found in the myocardium and
Purkinje fibers of birds affected with proventricular dilatation dis-
ease caused by bornavirus. Vi ra l matri x inclusions are so111etimes
found in cardiomyocytes and Purkinje fibers of chickens infected
with leukosis viruses .
I
Bacterial infections
Pericarclitis is a common lesion in some systemic bacterial in fec-
tions, especiall y E. coli (colisepticemia) and Sa/111011ella in yo ung
birds. It is characteri zed by the accumulation of inflammatory
exudate on the epicardium with or without in vo lvement of the sub-
epicarclial myoca rdium . In early lesions of colisepticemia, the in-
flammatory exudate is composed mainly of heterophil s and fibrin
with many intralesional bacteri a. Later, lymphoid cells and mac-
rophages, usually admi xed with fibrin , predominate. In so111e se-
vere cases of colisepticemia, les ions are characterized by caseous
necrotic debri s and fibrin surrounded by multinucleated giant ce lls,
macro phages, and ly111phocytes. Bacteri al colonies may be m1mer-
ous in the necrotic debris. Foca l mononuclear myocarditis ma y oc-
cur in the subepicardial muscle. If the bird survives, the fibrin-rich
exudate on the epicardial surface usuall y undergoes fibrov asc ular
orga ni zation in which endothelial cells and fibrobla sts grow from
the surface of the epicardium and replace fibrin with gra nulation tis-
sue. Lymphoid cells and macrophages are common in the granula-
tion ti ssue. Granul ation ti ssue matures to form fibrous tissue, which
results in extensive adhesions between the parietal and vi scera l peri-
cardium and can lead to constrictive pericarditis. Fibrous scarring
and thickening of the peri cardium obliterates the fluid-fill ed space
within the pericardia! sac and restricts expansion and fillin g of the
heart chamber during the dias tolic phase of the cardiac cycl e, result-
ing in restricti ve cardiomyo path y.
Riemerel/a anatipestife r infection in tu rkeys and clucks, and
chlamydiosis in turkeys are other diseases in which pericarditis is
the main lesion. With Riemerel/a anatipest/fer infection, typically
there is marked fibrinoh eterophilic pericarditis. Chlamydiosis should
be suspected when bacterial infection has been ruled out and peri-
cardia! lesions consist of fibrin ous exudate with large nu111bers of
lymph oid ce lls and re lati ve ly few heterophils.
In acute bacterial septicemias, bacteria, and less frequentl y, fi -
brin th ro mbi may be seen in capillaries of the myocardiu111, with or
without va rying degrees ofvasculitis and 111yocardial necrosis. Bac-
terial colonies may be identified within necrotic foci. Staphy lococ-
cus a11re11s can cause septicemi a, resulting in large areas of necrosis
in the myoca rdium . Vasculiti s is pro111inent with bacteria observed
in 111ultiple blood vessels in the myocardium . Extensi ve degenera-
146 I American Assoc iation of Avian Pathologists
tion and necrosis of myofibers acco111panying a severe inflam111a-
tory response are common lesions in birds with septicemic fo r111 of
listeriosis caused by Listeria 111011ocytogenes . Sa/111011e//a p111/om111
can cause multipl e vari able-sized areas of myocardial necrosis and
infla111mation. The inflammatory response is lymphoid and includes
many large cells with foa my cytoplasm (macrophages) and some
multinucleated giant cell s sufficient to justi fy a diagnosis of granu-
lomatous myocarditis. Endocardiosis or endocardial fibro elastosis
are likely secondary lesions.
Infections with !vlycobacteriu111 spp. can involve the heart, but
lesions usually are fo und in other tissues. Aggregates of large mac-
rophages with finely gra nular, faintl y basophilic cytopl as m should
arouse suspicion of mycobacteriosis. Necroti zing granulomas are
the predominant lesions in mycobacterios is in some avi an species.
Mycobacteriosis is diagnosed when ac id-fast bacteri a are demon-
stra ted by special stains in the lesions.
Val vular endocarclitis or vegetati ve valvular endocarditi s is
usuall y a large lesion that most often involves left atrioventricular
and ao rtic valves. The mass on the surface of the va lve is com -
posed of fibrin containing abundant bacterial colonies . A granul o-
111atous inflammatory reaction is typica l located at the base of the
les ion. Bacteria associated with enclocarditi s include Streptococcus,
Enterococcus, Staphy lococcus, Ervsipe/othrix, Avibacteri11111, and
Pasteurel/a . Focal to multi focal necroti zing myocarcliti s is fre quent
with these bacterial in fec tions because emboli from valvular lesions
are swept into the coronary arteries causing thrombosis.
Fungal infections
Mycotic infections of the hea1t are relati vely unco111111on and occur
as part of systemic infection or as the result of extension from air
sacs. Lesions are regionally extensive, effacing and replaci ng large
areas of 111yocardiu111 . Typically, multi nucleated giant cells are numer-
ous among the ly111phocytic and histiocytic cellular infiltrates. Funga l
ele111ents can be fo und in the cytoplas m of multinucleatecl giant cells.
Adjacent myocardium may have fo ca l areas of lymphocytic myo-
carcliti s.
Parasitic infections
Sa rcocysts (ti ssue cysts of Sarcocystis spp. ) are fo und in the
myoca rdium of different av ian spec ies. Cysts in myocy tes usu-
all y are not associated with any infl a111matory reaction unless they
rupture. Infection of the myocardium with Toxop/as111a gondii is
uncommon but, when seen, is likely a component of systemic in-
fection. There is extensive myofiber nec rosis and mi xed-ce ll in-
filt ra te in the myoca rdium . Orga ni sms may or ma y not be vi sibl e
within the lesions. Caseo us necrosis 111ay occur in young pigeons
with systemic tricho111oni as is. In mute swans affected with schisto-
so111i asis caused by Trichobilharzia sp., intestinal and portal blood
vessels show hyperplastic endophlebitis, characterized by myointi -
mal hyperplasia, often with severe narrowing or even obliteration of
the vascular lu111en. Adults and 111icrofil aria of Sarco11e111a, a filari d
heartworm that infec ts geese and swans, cause fatal myocarditi s.
Severe lymphohistiocytic myocarditis and myocardial degeneration
and necrosis are associated with adult wo r111s located within vesse ls
and mi crofilaria .

Vasculitis, Thrombosis, Embolism
Vascu liti s is characterized by inflammation and damage to the walls
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of bl ood vessels. Concurrent tluombosis is common. Arteritis
refers to inflammation of an artety, phlebitis to inflammation of a
vein , an d the prefi x endo- is used when inflammation is confined
to the endothelium. Phlebitis occurs more frequently than arteritis
as the post-capillaty venule is the site of inflammation. Fibrinoid
necrosis refers to necrosis of the tunica media and accumulation of
homoge nous, eosinophilic, proteinaceous material resembling fibrin
in vessel wa lls. Leakage of high protein content fluid , including
fibri,1 , from the blood or deposition of inumme complexes is re-
sponsible for fibrinoid changes in the vessel wall. In addition to
the fibrinoid material, breakdown products of cells and vessel wall
components usually occur in the lesion. Vasculitis lesions result
from segmental or diffuse infiltration of vessel walls with inflam-
matory cells. Necrotizing vasculitis is characterized by necrosis of
the vesse l wall accompanied by intact and necrotic heterophils or
lymphocytes. Vasculitis may be caused by bacteria, viruses, fungi ,
protozoa , or helminthes (e.g., schistosomiasis). Aspergi1/11sfi1111iga-
tus has a tendency to invade blood vessel walls and cause extensive
necroti zing vasculitis and, occasionally, thrombosis. Dissemination
of the fungus to other organs results from vascular invasion.
A thrombus is a blood clot that forms within the vascular lu -
men, is attached to the vessel wall , and obstructs blood flow. It
may totally or partially occlude the lumen of the blood vessel.
Thrombi that only partially obstruct blood flow are termed mural
thrombi. Lack of blood to downstream tissues initially causes an-
oxia followed by necrosis and infarction. The histologic appearance
of thrombi depends on their duration. Thrombi need to be distin-
guished from postmortem blood clots . Usually, thrombi contain
large agg regates of tluombocytes. Granulation tissue and re-canal-
ization is possible in cluonic lesions. The most frequent cause of
tlu·ombo sis is injury to the endothelial lining, which triggers a series
of cascading reactions resulting in formation of a clot composed of
fibrin and thrombocytes. Fibrin thrombi develop in arterioles and
sinusoids of birds that have septicemia, which can be caused by sev-
eral different bacterial species . Bacterial colonies may or may not
be present. Bacterial toxins or endotoxins cause the endothelial cell
damage necessary for initiation of thrombus formation. If sufficient
space is available, thrombi can become quite large as in valvular
endocarditis. Fibrin thrombi in blood capillaries in the cerebellum
are an important diagnostic feature of nutritional encephalomalacia
caused by vitamin E deficiency. Endothelial cells in the capillaries
are damaged by free radicals .
An embolus is an abnormal mass (solid, liquid, or gas) that is
free in the lumen of blood vessels, is transported tluough the vascu-
lar system, and lodges in a different site from where it was formed.
Emboli usually cause obstruction or occlusion of blood vessels
(thromboembolism). Most emboli are fragments of thrombi that
separate from the original mass and are carried in the blood stream
to sma ller arterial vessels where they lodge and cause tluomboem-
boli sm. Veins are not affected as they increase, rather than decrease,
in diameter. An exception is pulmonary embolism as veins in the
lungs also progressively decrease in size. In septicemia, bacterial
emboli (septic emboli) may be seen in the lumen of small vessels
--
Cardiovascular System
and capillaries in different organs and tissues. Emboli from vegeta-
tive valvular heart lesions are important so urces of septic embo li.
Yolk embolism occurs when free yolk enters the vascular system.
Lesions are most common in the lungs. Yolk embolism needs to
be distinguished from yolk in airways, which results from free yolk
entering torn air sacs.
Neoplasia
Lymphoid tumors of Marek's disease are the most common tumors
found in the hearts of chickens. Marek's disease lymphomas are
characterized by a pleomorphic lymphoid cell infiltration of the peri-
cardium or myocardium. Lymphoid leukosis tumors in chickens and
lymphoid tumors induced by reticuloendotheliosis virus in turkeys
may involve the heart. Primary tumors of the heart include rhabdo-
myosarcoma, myxoma, fibroma , and fibrosarcoma . Tumors of blood
vessels include hemangiomas and hemangiosarcomas. Vascular tu-
mors are included among the tumors that can be caused by avian
retroviruses.
Additional Readings
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Valdes . 2005. Use of the chicken as an experimental animal
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Balamurugan, V. and J. M. Kataria. 2004. The hydropericardium
syndrome in poultiy -- a current scenario. Vet Res Com 28: 127-
148.
Balog, J. M. 2003. Ascites sy ndrome (pulmonary hypertension
syndrome) in broiler chickens: are we seeing the light at the end
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Bezuidenhout, A. J. 1983. The valva atrioventricularis dextra of the
avian heart. Anal Histol Emb,yol l 2: I04-108.
Bickford, A. A., R. E. Corstvet, and A. S. Rosenwald. 1978.
Pathology of experimental etysipelas in turkeys. Avian Dis
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Biesiadecki, B. J. and J.P. Jin. 2002. Exon skipping in cardiac
troponin T of turkeys with inherited dilated cardiomyopathy. J
Biol Chem 277: 18459-18468 .
Biesiadecki , B. J., K. L. Schneider, Z. B . Yu, S. M. Chong, and J.
P. Jin. 2004. An RI 11 C polymorphism in wild turkey cardiac
troponin T accompanying the dilated cardiomyopathy-related
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Bougiouklis, P.A., G. Brellou, I. Georgopoulou, P. Iordanidis, and I.
Vlenm1as. 2005. Rupture of the right auricle in broiler chickens.
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Chadfield, M. S. , A . M. Bojesen, J.P. Christensen, J. Juul-
Hansen , S. S. Nielsen, and M. Bisgaard. 2005 . Reproduction
of sepsis and endocarditis by experimental infection of chickens
with Streptococcus galli11ace11s and Enterococcus hirae.
Avian Pathol 34:238-247.
Chapman, M. E. and R. F. Wideman, Jr. , 2001. Pulmonmy
wedge pressures confirm pulmonary hypertension in broilers
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resistance. Pou// Sci 80: 468-473 .
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Systemic trichomoniasis in a squab operation. Avian Dis 35:426-
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72: 1233-1235.
Avian Histopathology (4 th Edition) I 149
 Tahseen A bdul-Aziz • Oscar J. Fletch er
VetBooks.ir
5.1. Myocardium . No rmal. 5-day-old broiler. The ca rdi ac
myocytes appear as long, cylindrica l, branching cells, ofte n with
centrally-l ocated, si ng le, and ovoid to elongated nucleus. The long
axis of the nu cleus is para lle l to that of th e fibers. As with skeletal
myocytes, cardiac myocytes in lon gitudinal section have cross
st ri at ions, which are not obvious in thi s image. The endomysium
between individual myocytes is rich in blood capillaries.
5.2. Left atrioventricular valve. Normal. 41-clay-olcl broiler
breeder male. The periphera l spong iosa and central fibrosa are
seen in the secti on of va lve attached to th e hea rt wall.
150 I A merican Assoc iation of Av ian Pathologists
. . .. , , .
) . ... ' :• ·,.., ...,.... " ,f
. . · ". _: ·.rtt:.'·>\.:). .
5.3. Left atrioventricular valve. Normal. 41-clay-old broiler
breeder male. Higher-power view illustrates the peripheral
spongiosa and th e central fibrosa of the valve. The peripherall y-
located zo na spo ngiosa consists of spindle-shaped fibroblasts,
mesenchy rnal-like cells, and small bundles of thin co ll agen fib ers
embedded in homogeno us, edematous-looking gro und substa nce.
The centrally- located zo na fibro sa is co mposed predominantl y of
collagen bundles, w hi ch appear thicker and more compact than those
in the zona spongiosa . The histolog ic appearance of zo na spongiosa
and zona fibrosa vari es w ith their loca ti on within the valve.
;·';,'~2!)J!)7
'"'/·.
,,.,., . ' '
5.4.
T!:~:.;;:f:t//i\I.:~,\
Left atrioventricular valve. Normal. 41-clay-olcl broiler
breeder male. This area of th e va lve appears to be compo sed
entirely of mese nchyma l- like cells embedded in edemato us-lookin g
gro und substan ce. Suc h appearance should not be interpreted as
les io n of endocardiosis. T he small pieces of eosinophilic tissue on
th e ri ght of the image are chordae tendineae. The appearance of the
va lve in histologic sec ti ons varies w ith the plane of cut and the area
of the va lve.
 Cardiol'{tscular System

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., • I _ ,. "

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5.5. Left atrioventricular valve. Normal. Adult backyard 5.7. Aorta and aortic valve. Normal. Turkey. Sagittal section
chicken. Two areas of the valve are shown. The area on the right through base of the aorta illustrates the aortic va lves and the normal
consists predominantly of collagen bundles. The area on the left cartilage at the base of the aorta.
is composed entire ly of mesenchymal-like cells embedded in an
edematous-looking ground substance. Such ap peara nce should not
be interpreted as lesion of endocardiosis.

5.6. Left atrioventricular valve. Normal. Adult backyard 5.8. Aortic valve - normal. Turkey. Higher-power view of area
ch icken. The area of th e valve beneath the endothelial surface is in the 5.7 illustrates the aortic valve and the cartilaginous tissue at
composed of sma ll bundles of collagen fibrils , fine collagen fibrils , the attachment of the aorta to the myocardium.
ground sub sta nce of mucopol ysaccharide-pro tein complex, and
cellular elements consisting of fibroblasts and mesenchymal-like
cells.

Avian Histopathology (4 th Edition) I 151

-
 Tahsee11 A bdul-A ziz • Oscar J. Fletch er
VetBooks.ir

5.9. Heart. Purkinje cell s. Emu. G ro up of Purkinje cells around 5.11. Heart. Extramedullary hematopoiesis. 55-clay-old
blood vesse l in the myoca rdium. The cells are characteri sti ca ll y chicken. Collecti on of g ranul ocyti c mye loid cells (immature
large and have pale cytopl asm and prominent nuclei . gra nul ocytes) 111 the myocardium . Such extra medullary
hematopoietic cell s are see n commo nl y and mu st not be co nfu sed
w ith inflammato ry cells. Granulocyti c mye loid ce lls have non-
lo bulated nuclei and the ir cytoplasm is packed w ith brig htl y
eos inophilic g ranul es.

5.10. Heart. Purkinje cells. 5-month -old peacock. Large 5.12. Heart. Subenclocardial fat. 23-week-old broiler breeder
subendoca rdi al collectio n of Purkinj e cells. Note the mo rph ology pullet. Illustrated is the subendocardial fa t accumul at ion. Thi s
of the cell s. especially is seen in obese birds.

152 I America n Assoc iati on of Av ian Path ologists

 Cardiol'(tscufar System
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5.13. Heart. Fatty infiltration. 10-week-old backyard chicken.

Fatty infiltration of the myocardium. This is particularly seen in
obese birds. Grossly, areas of fatty infiltration appear pale and must
be differentiated from other pale lesions such as necrosis.
5.15. Heart. Calcium deposits. 4-week-old duckling. Focal
area of disruption of cardiac myocytes by calcium deposits, which
appear as faintly basophilic granular material. Definitive diagnosis
was not established but toxicity was suspected. The bird also had
degeneration and necrosis of skeletal myocytes.
I

5.1 4. Heart. Myocardial lipofuscinosis. 18-year-old parrot. 5.16. Heart. Calcium deposits. 4-week-old duckling. The heart
Golden brown granules of lipofuscin pigment are visible in the section was stained with Von Kossa stain, which stains calcium
cytoplasm of cardiac myocytes. Lipofuscin is an endogenous dark-brown to black. With this stain, the calcium deposits appear
lipopigment characteristic of aging process. It accumulates more extensive than with H&E stain.
exclusively in the lysosomes, and it is the end product of
physio logical degradation caused by oxidative damage to the
un saturated fatty acids in cell membranes. It is also sometimes seen
in chronically ill, emaciated birds.

Avian Histopathology (4th Edition) I 153

 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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I 5. 17. Heart. Urate deposition. 6-month-old backyard chicken.

Focal area of myocardial necros is containing basophilic materia l
consistent with urate. This bird had viscera l urate deposition (a lso
called viscera l gout).
5.19. Heart. Dilated cardiomyopathy (round-heart disease).
3-day-old turkey. Marked rarefication and vacuolation of the
cytoplasm of card iac myocytes is in thi s region of the myocardium.

5.18. Hea rt. Urate deposition. Backyard chicken. Prominent 5.20. Heart. Dilated cardiomyopathy (round-heart disease).
layer of urates on the epicardial surface of the heart. Norma lly, 10-day-old turkey. Vacuolation of the cytoplas m of cardiac
urates are di ssolved during fixation in for malin solution, but if the myocytes is evident in this region of the myocardium .
deposition is heavy (as in this case), then it appears as basop hilic
material of va rying thickness, density, and staining intensity on the
epicardial surface .

154 I American Association of Avian Pathologists

 Cardiovascular System
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5.21. Heart. Cardiomyopathy. 9-year-old backyard chicken.

Cardiac myocytes are thin and separated by ex panded interstitial
spaces. Both heart ventricles were dilated and the bird had severe
ascites.
5.23. Heart. Cardiomyopathy. 38-clay-olcl macaw. Area of
loss of cardiac myocytes and replacement by collagenous fibrou s
tissues, which stains blue with Masson 's tri chrome stain. I

5.22. Heart. Carcliomyopathy. 38-day-olcl macaw. The 5.24. Heart. Myocardial scarring. 7-year-old barboun
interstitium is expanded by clear spaces (edema), and some cardiac turkey. Area of replacement of cardiac myocytes by hypocellul ar
myocytes appear thinner than normal. This bird died of congestive co llagenous fibrous tissue.
heart fa ilure and had severe anasarca and ascites.

Avian Histopathology (4 th Edition) I 155

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 Tahseen Abdul-Aziz • Oscar J. Fletcher
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5.25. Heart. Myocardial scarring. 7-year-old barboun turkey. 5.27. Heart. Cardiomyopathy. Macaw. Adult. High-power
The collagen fibers in the area of myocardial fibrosis stains blue view of area in 5.26 demonstrates the "boxcar" nuclei of cardiac
with Masson 's trichrome stain. myocytes.

5.26. Heart. Cardiomyopathy. Macaw. Adult. Subjectively, 5.28. Myocardial glycogenosis. Quail. The cytoplasm of
cardiac myocytes appear enlarged, and several of them have large, cardiac myocytes is distended with single, circumscribed vacuolar
triangular-shaped nuclei, which are descriptive ly called "boxcar" space containing homogenous gray material representing glycogen.
nuclei and are considered characteristic feature of cardiac myopathy.
The bird had severe ascites and carcinomatous lesion of uncertain
tissue of origin in the spleen and air sacs.

156 I American Association of Avian Patholog ists

 Cardiol'(tscular System

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secti on of myocardium shows disruption of the cardiac myocytes of myocardium stained with PAS stain in combination with the
by intracytoplasmic accumulation of gray material repre senting en zyme diastase, which hydrolyzes glycogen and results in loss of
glycogen. positive staining with PAS. Note that the hydrolysis of glycogen is
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5.30. Heart. Myocardial glycogenosis. Quail. Cross section of 5.32. Heart. Endocardial fibroelastosis. 7-year-old red
myoca rdium stained with PAS stain . The intracytoplasmic material barboune turkey. The endocardium is expanded and elevated by
that appears gray with H&E stain (see 5.28) is PAS-positive (stains loose connective tissue consisting of fibroblasts and their fibers of
purple) . collagen and elastin.

Avian Histopathology (4,1, Edition) I 157

 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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5.33. Heart. Endocardial fibroelastosis. 10-day-old turkey.
The endocardium is thickened and the subendocardial myoca rdium
is di srupted by loose co nnective ti ss ue co nsisting of fibroblasts
and their fibers of coll agen and elas tin . This turkey had dilated
cardio myopath y (round-h ea rt disease).
5.34. Heart. Endocardial fibroelastosis. 41-day-old broiler.
The endoca rdium is thickened and elevated, and the subendocardi al
myocardium is disrupted by loose conn ective tissue consists of
fibroblasts and their fibers of co ll agen and elastin .
158 I A meri can Associa ti on of Av ian Pathologists
5.35. Heart. Endocardial fibroelastosis. 41 -day-old broiler.
Hi g h-power view of endoca rdial fibroelastosis lesion demonstrates
th e fibroblasts and th eir fibers of collagen and elastin.
5.36. Heart. Endocardial fibro elastosis. Adult backya rd
chicken. The endocardium is thickened and slightly elevated, and
th e subendocardial myocardium is disrupted by loose co nn ecti ve
tissue co nsisting of fibroblasts and their fibers of coll age n and
elastin .
 Cardiovascular System
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5.37. Heart. lonophore toxicity. Chicken. Extensive 5.39. Avian influenza (virus strain A/Pigeon/Thailand/IB/04).
dege neration and necrosis of cardiac myocytes. These degenerative 4-week-old chickens. Edema and degeneration of cardiac myocytes
and necrotic lesions are not diagnostic for ionophore toxicity. in epicardial area . See 5.40-5.43 for additional views. (Glass slide
courtesy of David Swayne).

5.38. Heart. lonophore toxicity. Chicken. Myocardial 5.40. Avian influenza (virus strain A/Pigeon/Thailand/IB/04).
degeneration and necrosis are characterized by loss of striations, 4-week-old chickens. Subendocardial edema and degeneration
va cuolation, fragmentation , and loss of cardiac myocytes, with of muscle fibers in the wall of the ventricle. lnse1t is a higher
intrace llular accumulation of hyaline material (insert) and magnification of the boxed area . Note the absence of inflammatory
proliferation of myofiber nuclei. Note the relative absence of cells. This lesion may be easily overlooked. (Glass slide courtesy
inflammatory cells. ofDavid Swayne).

Avian Histopathology (4 11, Edition) I 159

 Tahseen Abdul-Aziz • Oscar J. Fletcher
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I 5.41. Avian influenza (virus strain A/Pigeon/Thailand/18/04).

4-week-old chickens. Scattered cardiac myocytes show focal
swelling and vacuolation, but the lesions appear relatively
mild . Large amounts of viral antigen were demon stra ted by
immunohistochemistry in this area. (Glass slide courtesy of David
Swayne).
5.43. Avian influenza (virus strain A/Pigeon/Thailand/I 8 /04).
4-week-old chickens. Focal area of vacuolation of cardiac
myocytes. (Glass slide courtesy of David S1vay11e).

5.42. Avian influenza (virus strain A/Pigeon/Thailand/lB/04).
4-week-old chickens. lmmunohistochemical staining reveals large
amounts of influenza virus antigen in the nuclei and cytoplasm
(insert) of cardiac myocytes. (Glass slide courtesy of David
S1vay11e).
5.44. Heart. Avian encephalomyelitis. 11-day-old chicken.
Area of diffuse infiltration of the myocardium by lymphocytes
and plasma cells. Chickens in this flock had characteri sti c
histopathological lesions of avian encephalomyeliti s in the brain
and spinal cord, and avian encephalomyelitis virus was isolated
from affected birds.

160 I American Association of Avian Pathologists

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5.45. Heart. Avian encephalomyelitis. 11-day-old chicken.

Diffuse and nodular lymphocytic infiltrate in the wall of atrium.
Chickens in this flock had neurological signs and brain and spinal
cord lesions characteristic of avian encephalomyelitis. Avian
encephalomyelitis virus was isolated from affected birds.
5.47. Heart. 28-day-old broiler with reovirus tenosynovitis.
Focal area of subepicardial lymphocytic myocarditis, with formation
of lymphoid nodules . The epica rdium appears slightly edematous. I

5.46. Heart. 28-day-old broiler with reovirus tenosynovitis. 5.48. Heart. 28-day-old broiler with reovirus tenosynovitis.
Foca l area of lymphocytic epicarditis, with formation of lymphoid Epicarditis characterized by expansion of the epicardium by clear
folli cle. spaces (edema) and loose infiltrate oflymphocytes. Small lymphoid
nodule is present in the expanded epicardium.

Avian Histopathology (4 th Edition) I 161

 Taftsee11 A bdul-A ziz • Oscar J. Fletcher
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I 5.49. Heart. 14-day-o lcl broiler with reovirus tenosynovitis.

Focal area of marked lymphoplasmacytic ep ica rditis, w ith extens ion
of the cellul ar infiltrate into the adjacent myocardium. The bird had
tenosy nov iti s ca used by reovirus.
5.5 1. Heart. Reovirus myocarditis. 9-day-old broiler breeder
pullet. Higher-power view of area in 5.50 showi ng myocardi al
necrosis with dense infiltration of gra nulocytic leukocytes and
mono nu clea r infl ammato ry ce lls. Th ere is a lso pericarditi s.

5.50. Heart. Reovirus myocarditis. 9-day-old broiler breeder 5.52 . Heart. Reovirus myocarditis. 9-day-olcl broiler
pullet. Area of myoca rdi a l necrosis w ith dense infilt rat io n of breeder pullet. Area in the myoca rdium is densely infiltrated with
gra nul ocytic leukocytes and some monon uclear inflammatory cells. lymphocytes .
Reovirus isolated from broilers in thi s case had genome sequence
that was different from that of classica l reovirus isolates.

J62 I A me ri ca n Association of Avia n Patho logists

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5.53. Heart. Reovirus myocarditis. 17-day-old turkey.

Area with lymphocytic myocarditis characterized by infiltration
of lymphocytes with disruption and segmental loss (necrosis) of
cardiac myocytes. (Image courtesy of'H. L. Shivaprasad).
5.55. Heart. Reovirus myocarditis. 17-day-olcl turkey. Area
of disruption and loss (necrosis) of cardiac myocytes with marked
infiltration by of lymphocytes. Few multinucleated giant cells are
present in the lesion. (Image courtesy of' H. L. Shivaprasad).
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5.54. Heart. Reovirus myocarditis. 17-day-old turkey. Area of 5.56. Heart. Epicardial neuroganglion. Proventricular
myocardial necrosis and dense infiltration of primarily lymphocytes dilatation disease. 2-year-old parrot. Very mild
with formation of lymphoid nodules. (Image courtesy of' H. L. lymphoplasmacytic infiltrate in epicardial neuroganglion. This bird
Shivapmsad). had other lesions characteristic of proventricular dilatation disease
caused by bornavirus.

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 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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I 5.57. Heart. Epicardial neuroganglion. Proventricular

dilatation disease. 2-year-old parrot. Same heart as 5.56.
Epicardial neuroga ngli on with more prominent lymphopl asmacytic
infiltrate than that in 5.56 .
5.59. Heart.v Subendocardial purkinje cells. Proventricular
dilatation disease. 4-month-old conure. This legend is al so
applied to 5.58. Subendocardial Purkinje cell s are infiltrated
by lymphocytes. This bird had other les ions characteristi c of
proventricular dilatation disease caused by bornavirus.

5.58. Hea rt. Subendocardial purkinje cells. Proventricular 5.60. Heart. Polyomavirns infection. Young ring-necked
dilatation disease. 4-month-old conure. See the legend of 5.59 . parrot. Area of e pica rdi al hemorrh age.

164 I America n Association of Av ian Pathologists

 Cardiowtscular System
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5.61. Heart. Polyomavirus infection. Young ring-necked 5.63. Heart. Polyomavirus infection. 6-week-old macaw.
parrot. Area of endocardial hemorrhage. Note the few Purkinje Multi focal areas of myocardial hemorrhage .
cells among the red blood cells.

5.62. Heart. Polyomavirus infection. Young ring-necked
parrot. Area of epicardial and myocardial hemorrhage.
5.64. Heart. Epicarditis. Colibacillosis. 16-week-old turkey.
The pericardium is markedly expanded by fibrinoheterophilic
exudate and clear spaces (edema), with congestion of blood vessels.
The lower insert shows heterophils in the exudate (small box), and
the upper insert shows fibrin (large box with arrow).

Avian Histopathology (4 th Edition) I 165

 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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I 5.65. Heart. Epicarditis. Colibacillosis. 3-week-old turkey.

The ep ica rdium is ex panded by fibrin ocellular exudate. The les ion
is typical of bacterial etiol ogy, especiall y£. coli (colisepticemia).
5.67. Heart. Epicarditis. Colibacillosis. 9-week-old turkey.
Severe epicarditis characteri zed by ix pansion of the ep ica rdiu m
by fibrinocellular ex udate and caseous necrotic debri s. The insert
shows bacterial co lo ni es at the marg in of the necroti c debris.

5.66. Heart. Epicarditis. Colibacillosis. 13-week-old turkey.
The ep ica rdium is ex panded by fibrin and cellular inti ltrates of
heteroph ils and inflammatory monocul ar cells that are prominent
around blood vesse ls (insert). This les io n is characteri sti c, but not
specific, of£. coli septicem ia.
5.68. Heart. Epicarditis. 8-day-old broiler. Thick layer of dense
fibrinous exudate on the epicardial surface. There is subepica rcli al
myocarditis characteri zed by disruption of the myocard ium by
inflammato1y infiltrates and fibrin ous ex ud ate.

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5.69. Heart. Epicarditis. Riemerella a11atipestifer infection.

8-week-old turkey. The epicardium is expanded by edema and
cellular infiltrates . Layer of dense fibrin is on the surface. Large
fibrin thrombus is in a dilated blood vessel.
5.71. Epicarditis. Colibacillosis. 5-week-old turkey.
epicardium is markedly expanded by dense cellular infiltrate of
The

predominantly heterophils . The cellular infiltrate on the surface is

undergoing caseation.
I

5.70. Heart. Epicarditis. Sal111011ella e11teritidis infection. 5.72. Epicarditis. Colibacillosis. 5-day-old chicken. Layer of
10-day-old broiler. The epicardium is expanded by edema, fibrin , fibrin mixed with inflammatory cells is on the surface of the heart.
and ce llular infiltrate. Note the extension of the cellular infiltrate to
the myocardium (subepicardial myocarditis).

Avian Histopathology (4'h Edition) I 167

 Tahseen Abdul-Aziz • Oscar J. Fletcher
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I 5.73. Hea rt. Epicarditis. Pse11do111om1s a11mgi11osa infection.

2-week-old chicken . The epicardiurn is markedl y expanded
by cellular infiltrate of mononucl ea r inflammatory cells and
heterophils. Fibrobl asts and newly fo rmed blood capillari es are
present among the cellular infiltrate, indi ca ting ve,y early stage of
fibrin organi zation and gra nul ation tissue formation. Layer of fibrin
5.75. Heart. Epicarditis. Chlam~'diosis. Turkey.
Fi brinolymphocyti c exudate expands the pericardium . The insert
shows lymphoid cells.

mi xed with inflammatory cells is on the surface.

5.74. Heart. Epicarditis. Pse11do111011as aer11gi11osa infection.
5-day-old chicken. Hi gh-power view of an area in 5.73 shows
many spindle-shaped fibroblasts and ve,y fin e strands of connective
tissue fibers among heterophils and mononuclear inflammatory
cells. On the left of the image, note th e blood vessel w ith many
heterophil s in the lumen.
5.76. Heart. Organizing epicarditis. 42-old broiler. Early
formation of gra nulation tis sue in the fibrinocellular exudate.
Fibroblasts from the myocard ial interstitium nea r the surface
proli fe rate and invade the exudate. Note the di sruption of the
ca rdi ac myocytes near the surface by the granulation tissue. The
lesio n is a clu-onic sequela of bacterial ep icarditis, likely ca used by
E.coli .

168 I Ame ri ca n Association of Av ian Patholog ists


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5.77. Heart. Organizing epicarditis. 34-day-olcl broiler.
Fibro vascular granulation tissue is replacing the exudate on the
epicardial surface. Two foci of fibrinous exudate are still present
among the granulation tissue.
5.78. Heart. Organizing epicarclitis. 42-clay-old broiler. This
stage of granulation tissue formation is more advanced than that in
5.76. With time, most of the blood capillaries regress and collagen
is laid down by fibroblasts, many of which are still seen. The
numbers of mononuclear inflammatory cells are markedly reduced.
Cardiol'(tscular System
5.79. Heart. Organizing epicarditis. 42-clay-old broiler.
Contiguous with the epicardial surface of the heart is a thick layer
of fibrovascular granulation tissue composed of fibroblasts , loose
c01mective tissue matrix, and perpendicularly-oriented blood
capillaries . Many mononuclear inflammatory cells are still present .
I
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5.80. Heart. Organizing epicarditis. 44-day-old broiler. Over
a period of time, fibroblasts continue to produce collagen . Thick
layer of collagenous tissue covers the epicardial surface of the heai1
and appears to be contiguous with the underlying myocardium.
The early-formed granulation tissue and the collagenous fibrous
tissue fill the pericardia! sac, causing constrictive epicarditis which
restricts the normal function of the heart and results in cardiac
insufficiency and eventually heart failure.
Avian Histopathology (4 th Edition) I 169
 Tahseen Abdul-Aziz • Oscar J. Fletcher
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I 5.81. Heart. Organizing epicarditis. 44-day-old broiler.

Masso n's trichrome stain was used to demonstrate the collagen
fibers, which stain blue.
5.83.
__,
Heart. Bacterial septicemia. 2-week-old turkey. Blood
vessel in the myocardium contains clusters of bacteria. The dark
nuclei in the blood vesse ls are likely of thrombocytes. This bird
was septicemic, and Streptococc11s galloly tic11s subsp. paste11ria1111s
(formerly Streplococc11s bovis) was isolated from the liver and
spleen of affected turkeys.

5.82. Heart. Pasteurellosis (fowl cholera). SO-week-old broiler 5.84. Heart. Erysipelas. 16-week-old quail. Clusters of thin,
breeder hen. Blood capillary in the interstitium of the myocardium somewhat filamentous bacteria are in the myocardium, possibly
is filled with bacteria (Paste11rella 11111/tocida). within interstitial blood capi llaries . E1:vsipelothrix rh11siopathiae
was isolated from the li ver and spleen of this quail.

170 I Ameri ca n Association of Avian Pathologists


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5.85. Hea rt. Erysipelas. 16-week-old quail. Clusters of Gram-
positive, thin bacteria that morphologica ll y resemble E,ysipe!othrix
rhusipathiae.
5.86. Heart. Bacterial septicemia. 21-year-old blue and
gold macaw. Large colonies of coccus-shaped bacteria in the
myocardium . Note the absence of any inflammatory reaction or
necrotic lesion around the colonies. This bird died of bacteri al
septicem ia caused by Streptococc11s eq11i subsp. zooepidemicus.
-
Cardio11asc11/ar System
5.87. Heart. Bacterial septicemia. 21-year-old blue and gold
macaw. Two large colonies of cocci bacteria in the myocardium .
Note the absence of any inflammato ry reaction or necrotic lesion
arou nd the colonies. This bird died of bacterial septicemia caused
by Streptococc11s equi subsp. zooepide111ic11s.
5.88. Heart. Bacterial septicemia. 6.5-year-old African gray
parrot. Cluster of bacteria in the interstitium of the myocardium.
Note the absence of any inflammato ry reaction or necrotic lesion
around the co lonies. Thi s bird died of bacterial septicemia caused
by Pasteurella 11111/tocida.
Avian Histopathology (4'h Edition) I 171
 Tahseen Abdul-Aziz • Oscar J. Fletch er
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I 5.89. Heart. Bacterial septicemia. 6.5-year-old African gray

parrot. Abundant bacteria coloni ze the epicardium and extend into
the m yoca rdi al interstitiurn beneath the endocardium. Epicardial
blood vessel is dilated and co loni zed with bacteria and shows
ev idence of early fibrinou s thrombo sis. This bird died of bacterial
septicemi a caused by Pasteurella 11111/tocida.
5.91. Heart. Listeriosis. 4-month-old backyard chicken.
Higher-power view of area in 5.90 show ing an area of necrotic
cellul ar debris surrounded by dense inflammatory infiltrate
that almost totally replaces ca rdi ac myocytes. The infiltrate co nsists
mostly ofmacropa hges with many lymph ocytes and heterophils and
very few small rnultinucleated giant ce lls.

5.90. Heart. Listeriosis. 4-month-old chicken. Multiple
variably sized areas of myocardial necros is characteri zed by loss
and replacement of ca rdi ac myocytes by intensely eosinop hili c
necrotic cellular debri s. The necrotic areas are surrounded by dense
inflammatory infiltrates that effaces and replaces cardiac myocytes.
Cultures of the heart and liver yielded heavy growth of Listeria
111011ocytogenes.
5.92. Heart. Listeriosis. 4-month-old backyard chicken.
Higher-power view of inflammatory infi ltrate aro und necroti c
areas. The infiltrate consists mostl y of macropahges with many
lymph ocytes and heterophils. Small multinucleated g iant cells may
be present.

J72 J Ame ri can Assoc iation of Avian Pathologists


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5.93. Heart. Listeriosis. 4-month-old backyard chicken.
Gram satin shows many intralesional Gram-positive short bacilli
and coccobacilli morphologically compatible with Listeria spp.
Listeria 111011ocy toge11es is not discernible in H&E-stained sections,
but it ca n be demonstrated with tissue Gram stain.
5.94. Heart. Listeriosis. 4-month-old backyard chicken.
Irnrnunohistochemical staining for Listeria monocytogenes shows
strong and extensive immunoreactivity. The dark areas are clumps
of the bacteria. lmmunohistochemical staining shows way more
orga nisms than with Gram stain .
Cardiovascular System
5.95. Heart. Bacterial septicemia. One-day-old broiler. Focal
area of myocardial necrosis with numerous intralesional bacteria
(stain blue). This bird had yolk sacculitis and was septicemic.
Culture of the liver yielded heavy growth of Pse11do111011as
aernginosa.
I
5.96. Heart. Bacterial septicemia. 42-week-old broiler
breeder hen. Area of myocardial necrosis with infiltration of
heterophils. Necrotic cardiac myocytes exhibit homogeneously
eosinophilic sarcoplasm and have pyknotic nuclei . This bird had
liver and spleen lesions consistent with septicemia, and the culture
of the liver yielded pure growth of a-hemolytic Streptococcus sp.
that was identified as resembling S. acido111ini11111s. The lesion is
not etiology-specific but should arouse suspicion of an infectious
process.
Avian Histopathology (4th Edition) I 173
 Tahsee11 Abdul-A ziz • Oscar J. Fletch er
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I 5.97. Heart. Bacterial septicemia. 42-week-old broiler breeder

hen. Same slide as 5.96. Another area of myocardial necros is with
infiltration of heterophil s, lymphocytes, and macrophages. Necro tic
cardi ac myocytes have bri ghtl y eosinophilic cytoplasm and pyknoti c
nuclei.
5.99. Heart. Myocardial necrosis. Staphylococcus rmreus
infection. Muscovy cluck. Large area of necrotic cardi ac myocytes
in the lower right co rner is less eosinoph ilic than the adj acent viab le
myocy tes.

5.98. Heart. Bacterial septicemia. 42-week-old broiler breeder
hen. Same slide as 5.96 . In thi s lesion, necroti c cardiac myocytes
di sappea red and th e area is large ly occupi ed by macrophages and
some heterophil s. The necrotic cardiac myocytes in the area were
removed by th e phagocytic acti vity ofneutro phils and macrophages.
5.100. Heart. Bacterial septicemia . Staphylococcus aureus
infection. Muscovy duck. C luster of bacteri a is within small blood
vesse l in the myocardium. Note that the intra vascular bacteri a are
not associated with necros is or inflammation .

174 I Ameri ca n Assoc iati on of Av ian Patho logists


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5.101. Heart. Myocarditis. Sal111011ella p11llor11111 infection.
3-week-old chicken. Myocarditis is extensive and characterized
by infiltration and effacement of the myocardium by lymphocytes
and macrophages.
5.10 2. Heart. Myocarditis. Sa/111011ella p11llor11111 infection.
3-week-old chicken. Lymphohistiocytic infiltrate effaces and
replaces the myocardial tissue. The insert shows the mixed cell
population including macrophages with foamy cytoplasm.
Cardiow1sc11/ar System
5.103. Heart. Vegetative valvular endocarditis. Chicken. Large
mass of necrotic tissue on the right atrioventricular valve. The box
encloses the left atrioventricular valve that is enlarged.
5.104. Heart. Vegetative valvular endocarditis. Chicken.
This large lesion of endocarditis has three areas. A. The surface
of the valve contains numerous bacteria. B . Prominent acellular
eosinophilic band separates the necrotic material on the surface
from the viable tissue that is expanded by inflammation. C. The
inflammatory process extends into the myocardium.
Avian Histopathology (4 th Edition) I 175
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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I 5. 105. Heart. Vegetative valvular endocarditis. 45-week-

old broiler breeder hen. Mass composed of massive number of
bacteria w ith fibrin is attached to the left atrioventricular va lve. Thi s
is characte ri stic lesio n of va lvul ar endocarditi s. Different bacteri a
may cause such lesion, but Pasteurel!a 11111/tocida was isolated from
the liver of thi s particular bird.
5. 107. Heart. Granulomatous mycotic myocarditis
(phycomycosis). Backyard chicken. Large area of gra n\:ilomatous
inflammati on with necrosis and loss of myocytes is prominen t
in the endocardiurn and myocardium of the left ve ntricle. The
gra nul omatou s lesion extends into the chamber of the left ventricl e.
The causative fungus was Phy comyces sp. (phycomycosis).

•j

5. 106. Heart.
--Vegetative valvular endocarditis. 45-week-
old broiler breeder hen. Higher-power v iew of the valv ul ar
5.108. Heart. Granulomatous mycotic myocarditis. Backyard
chicken . Higher-power v iew of area in 5. 107. T he myoca rdiu m
endocard itis les ion. Note the mass ive number of bacteri a in the is effa ced by severe gra nul omato us les ion containing many
lesion. multinucleated giant cells.

176 I American Associat ion of Av ian Pathologists

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5.1 09. Heart. Granulomatous mycotic myocarditis. Backyard

ch icken . Higher-power view demonstrates several multinucleated
giant cells in the myocardial granulomatous lesion. The insert
shows giant cell with fungal hyphae in the cytoplasm.
5.111. Heart. Granulomatous mycotic myocarditis. 5-week-
old broiler breeder pullet. Higher-power view of area in 5.110
demonstrates granulomatous lesion composed of histiocytes and
multinucleated giant cells, some of which surround small collection
of heterophils that are undergoing necrosis and caseation . Scattered
heterophils are also present throughout the lesion.
I

5.110. Heart. Granulomatous mycotic myocarditis. 5-week-old 5.112. Heart. Granulomatous mycotic myocarditis. 5-week-old
broiler breeder pullet. Region in the myocardium is effaced and broiler breeder pullet. Same heart as 5.110. PAS stain highlights
replaced by severe granulomatous lesion. The heart was not cultured intralesional fungal hyphae.
but Aspe1gil/11s .f11111igat11s, A,pe1g il/11s .flavus, and Aspe1gil/11 niger
were isolated from the lung, which had severe granulomatous
bronchopneumonia and intralesional fungal hyphae.

Avian Histopathology (4th Edition) I 177

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 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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5.113. Heart. Sarcocyst. Kestrel. Tissue cyst of Sarcocystis sp. 5. 11 5. Heart. Marek 's disease. 5-month-old backyard chicken.
(sarcocyst) in the myocardium . Note the absence of both necrosis Large area in the myocardium is effaced and repl aced 15y a den se
and inflammation. population of lymphoid ce lls.

5.114. Heart. Marek's disease. 20-week-old chicken. Area in 5.116. Heart. Marek's disease. 5-month-old backyard
th e myocardium is hea vi ly infiltrated by pleomorphi c lymphoid chicken. High-power view of an area in the 5.115 demonstrates the
cell s (see insert). The ca rtil ag inous base of the ao rta is also show n. pleomorphic population of lymphoid cell s in the myocardium . Few
shrunken cardi ac myocytes are see n.

178 I American Association of Avian Pathologists

 Cardiovascular System
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5.117. Heart. Marek's disease. 6-month-old backyard chicken.

Infiltration of the myocardium with pleomorphic lymphoid cells .
5.119. Venule in the lung. Mineral deposition. 40-week-old
turkey breeder hen. Multifocal areas of mineral deposition (bluish
areas) in the wall oflarge venule in the lung. This was an incidental
finding. The cause is unknown .
I

5.11 8. Venule in the liver. Mineral deposition. 8-month-old 5.120. Blood vessel. Mineral deposition. 3-year-old pigeon.
backyard chicken. Marked mineral deposits in the wall of the Mineral deposition in the ti.mica media of an arteriole in the
venul e. Similar deposits were present in blood vessels of other myocardium. The cause is unknown.
tissues. The cause is unknown.

Avian Histopathology (4th Edition) I 179

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 Tahsee11 Abdul-Aziz • Oscar J. Fletc/1er
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I 5.121. Blood vessel. Mineral deposition. 4-year-old chicken.
Focal area of mineral deposition in the tuni ca media of ovarian
artery is acco mpanied by g iant cells.
5.122. Muscular artery. Medial hyperplasia. 30-year-old
cockatoo. Branch of th e coronaiy arte ry in the myocardium shows
thickening of the ti.mi ca medi a due to hyperpl as ia of th e smooth
muscle, with narrow ing and irregul ar o utline of the lumen. Medial
hyperplas ia is subty pe of medi al fibromu scular dysplas ia, w hi ch is
one the tlu-ee types of arteri al fibromu sc ul ar dysplas ia. The les ion
may be age- re lated.
180 I A meri ca n Associati o n o f Avian Path ologists
5.123. Muscular artery. Medial hyperplasia. 30-year-old
cockatoo. Branch of th e coronaiy artery in the myoca rdium shows
thi ckening of the tuni ca media due to hyperplasia 8f the smooth
mu sc le, with polypoid protrusion of tuni ca medi a smooth mu sc le in
the lumen of the artery.
Muscular artery. Segmental medial hyperplasia.
6-year-old backyard chicken. The intraluminal protrusion, w hi ch
nea rl y fill s the lumen of the arte1y , consists of smooth muscle ce ll s
ori ginating from tuni ca media. Medi al hyperpl as ia is a subtype
of medi al fibromu sc ul ar dysplas ia, whi ch is a type of arterial
fibromu scular dysplas ia.
 Cardiol'(/scular System
VetBooks.ir

5.125. Muscular artery. Segmental medial hyperplasia. 6-year-

old backyard chicken. Higher-power view of 5.123 illustrates the
intraluminal projection, which consists of proliferating smooth
muscle ce lls oftunica media.
5.127. Muscular artery. Medial hyperplasia.
chicken. The plug of fibromuscular tissue seems to have no
4-week-old

connection to the artery wall. This is a common observation in

arterial fibromuscular dysplasia and results from the plane of the
section. This is a subtype of medial dysplasia of arteries.
I
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5.126. Muscular artery. Segmental medial hyperplasia. 5.128. Muscular artery. Medial hyperplasia. 4-week-old
15-week-old broiler breeder pullet. Polypoid-like projection of chicken. Muscular a11ery in the lung shows eccentric thickening of
tuni ca media is in the lumen of an artery. the wall caused by hyperplasia of the smooth muscle of the tunica
media. This lesion may be found in pulmonary hypertension .

Avian Histopathology (4 th Edition) I 181

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 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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5.129. Muscular artery. Intimal hyperplasia. 4-year-old
chicken . Muscular artery in the ovary has greatl y narrowed lumen
due to uniform increase in the tunica intima thi ckness (intimal
hype rpla sia). The tuni ca med ia appears to be of normal thickness.
,
~,
5.131. Elastic artery. Atherosclerosis. 25-year-old Ama zon
parrot. This early lesion of at heroscleros is is characterized by the
accumul ation of lipid-laden macrophages (foam cells) in the intima
of the artery. Note the blue, foamy appearance of the cytoplasm of
th e lipid-laden macrophages.
C

.,
. . : .,.
•. ~ ~ . ....v ·· •

-
. ..
~ '.

,, '

5. I 30. Elastic artery. Atherosclerosis. Adult Amazon parrot.
There is circumferential thi cken ing of the tunica intima by
atherosclerotic lesion that co mpresses the tunica media. The empty
space in the thickened intima is area of mineralization in which
minera l deposits can be recogni zed at the edges.
5.132. Elastic artery. Atherosclerosis. Adult Amazon parrot.
The intima of the artery is markedly thickened and di srupted by an
atherosclerotic les ion. Layer of lipid-laden macrophages is fo ll owed
by hypoce llular layer co nsisting mostly of lipid debris derived from
the dead macrophages. Some lipid deposits are sti ll present in the
mu sc ul ar layer.

182 I American Association of Av ian Patholog ists

 Cardio11asc11/ar System
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5.133. Elastic artery. Atherosclerosis. Adult Amazon parrot.
The intima of the artery is markedly thickened and disrupted by
an atherosc lerotic lesion. Layer of lipid-laden macrophages is
follow ed by a thi ck layer consisting mostl y of lipid debris deri ved
from the dead macrophage .
I
5.135. Elastic artery. Atherosclerosis. Adult Amazon parrot.
Thin layer of lipid-laden macrophages at the surface covers a thi ck
layer of hypoce llular material co nsisting mostly of lipid debris
derived from the dead macrophages. Deep layer of cholesterol
c lefts is present. There is an area of what appears to be ca rtilagi nou s
metapl as ia.

' ..

5.134. Elastic artery. Atherosclerosis. Adult Amazon parrot.
Early lesion of atherosclerosis is characterized by the accumulati on
of li pid- laden macrophages in the intima. As the les ion advances
(as seen in this image), macrophages start to di e and release the
lipid in their cyto plasm. Foam (lipid-laden) macrophages are still
recogni zable in the superfici al layer of the lesion.
5.136. Elastic artery. Atherosclerosis. 21-year-old Amazon
parrot. The ath erosclerotic lesion consists of lipid (empty spaces)
and fat debris. There is an area of what appears to be ca11ilaginous
metapl asia.

Avian Histopathology (4 th Edition) I 183

--
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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5.137. Elastic artery. Atherosclerosis. 5-year-old Quaker
parakeet. The lumen of the artery is severely narrowed by the
atheroscleroti c lesio n. Thin laye r of lipid-l aden macrophages
is sti ll present at the surface and is followed by a thi ck layer of
hypocellular material consisting mostly of lipid debris der ived from
the dead macrophages. Several collections of cho lesterol c lefts are
present in the les ion.
5.139. Muscular artery in myocardium. Atherosclerosis.
5-year-olcl Quaker parakeet. The lumen of th e artery is almost
completely obliterated by an at heromato us plaque co nsisting of
lipid- laden macrophages and lipid debris.
C

5.138. Elastic artery. Atherosclerosis. 15-year-old African gray
parrot. The tunica intima is ex panded by atherosclerotic lesion
consisting mostly of amo rphous necrotic lipid. Lipid droplets and
cholestero l clefts are still present in some areas. The mu scular layer
(t uni ca med ia) is compressed .
5.140. Muscular artery in myocardium. Atherosclerosis. Adult
Amazon parrot. The tunica intima is markedly thi ckened by lip id
deposits and eos inophilic deb ri s, w ith narrowing of the lumen . Note
that th e tunica medi a appears intact.

184 I Am eri ca n Associati on of Av ian Patholog ists

 Cardiol'(lscular System
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5.1 41. Muscular artery. Atherosclerosis. 21 -year-old African 5.143. Elastic artery. Atherosclerosis. Adult parrot.
gray parrot. Lipid-laden macrophages are not seen in this lesion, Circumferential thickening of the wall and marked narrowing of the
which consists mostly of lipid debris derived from the macrophages lumen of the artery by an atherosclerotic lesion in the intima.
that co mprise the early lesion but die as the lesion advances.
Granular, blue material deposits are present in the lesion .

5.142. Elastic artery. Atherosclerosis. Adult Amazon parrot. 5.144. Elastic artery. Atherosclerosis. Adult parrot. Higher-
As the atherosclerotic lesion progresses, areas of cartilaginous power view of area in 5.143 shows that the atherosclerotic lesion
tissue (catiilaginous metaplasia) may develop 111 the lipid debris. consists of different components.
Many chondrocyte-like cells are present.

Avian Histopathology (4'" Edition) I 185

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 Tahsee11 Abdul-A ziz • Oscar J. Fletcher
VetBooks.ir

~'.,.
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I 5.145. Elas tic artery. Atherosclerosis. Adult parrot. High-

power view of area in 5.144 shows that the atherosclerotic lesion
consists of an outer (subendotheli al) layer offibrous ti ssue fo llowed
by a thicke r layer of lipid. Chondrocyte-like cell s are seen within
and at the periphery of the lipid debris. No te the tunica medi a on
the left.
5.147. Elastic artery. Atherosclerosis. 21-year-olcl African
gray parrot. Masso n's trichrome stain demonstrates the collagen
fibers in the fibro cartilaginous ti ssue that replaced the atheromatous
lesion. Cartilag inous tissue is not identifi able at this magnificati on.
Note the narrowin g of the lumen.

5.1 46. Elastic artery. Atherosclerosis. 21-year-old African
gra y parrot. In this adva nced lesion, the atheromatous deposit is
replaced by fibrocartilag inous tissue that protrudes into and narrows
the lumen of the artery. Free lipid depos its are still present in the
wall of the artery.
5.148. Elastic artery. Atherosclerosis. 21-year-old African gray
parrot. This adva nced les ion of atherosclerosis is characteri zed
by replacement of the atheromatous les ion by hya line cartilage
consisting of chond rocytes and eosinophilic hyaline matri x.

186 I American Assoc iati on of Avian Pathologists

 Cardiomscular System
VetBooks.ir

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5.149. Elastic artery. Atherosclerosis. 21-year-oldAfrican gray
parrot. High-power view of area in 5.148 showing the hyaline
cartilage in the wall of the atheromatous elastic arte1y.
5.151. Spleen. Vascular fibrinoid necrosis. 45-day-old broiler.
The walls of small arterioles and the surrounding splenic tissue
are disrupted by dense deposits of amorphous, eosinophilic,
proteinaceous material. This lesion is commonly seen in bacterial
septicemia and indicates injury to the walls of the vessels, with
subsequent leakage of serum proteins.

5.1 50. Hepatic artery. Necrosis. Turkey. Artery in the liver has
necrosis and hemorrhage in the media. The cause is not known.
The insert is higher-power view of the lesion in the boxed area.
5.152. Spleen. Vascular amyloid deposits. 3.5-year-old
swan. Hyalinization of the walls of small arterioles by deposits
of amorphous, fibrillar or homogenous, eosinophilic material
resembling amyloid . Amyloid protein must be distinguished from
non-amyloid serum proteins that leak through injured blood vessels
(fibrinoid necrosis).

Avian Histopathology (4th Edition) I 187

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 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
VetBooks.ir

5. 153. Spleen. Vascular amyloid deposits. 3.5-year-old swan. 5.155. Lung. Occluding thrombus. Broiler. Thrombus
The amyloid in the walls of small arteriol es stains red orange with composed of fibrin and thrombocytes is filling the lumen of an
Congo red stain. a11eriole in the lung. The cause is unknown , but likely related to
bacteri al septicemi a.

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5. 154. Brain. Fibrinous capillary thrombi. Chicken. Blood 5.156. Liver. Fibrinous thrombus . 50-week-old broiler.
capi llaries in the cerebellum contain fibrin thrombi and are Fibrinous tluombu s is in a large blood vesse l in the li ver. Note the
associated w ith malacia ca used by vitamin E deficiency (nutritio nal short rod-shaped bacteria in the thrombus. This bird had severe
encephalomalacia). The insert is higher-power view of blood peritoni tis and bacterial septicemia caused by E. coli.
capillary w ith fibrin thrombus.

188 I Ame ri ca n Association of Avia n Pathologists

 Cardiovascular System
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5.157. Lung. Venous thrombus. Bald eagle. Thrombus in a 5.159. Lung. Thrombus. 3-year-old backyard chicken. Early
large ve in in the lung. The thrombus is composed of dense fibrin, tlu·ombus composed of thrombocytes and fibrin. This bird had
numerou s thrombocytes, and red blood cells, with a layer of bacteria bacterial septicemia caused by Gal1ibacterti11111 analis serovar
on the endothelial surface. This bird was septicemic. hemoly tica .

5.1 58, Lung. Venous thrombus. Bald eagle. Thrombus adheres 5.160. Lung. Thrombus. 3-year-old backyard chicken. Same
to the wall of a large vein in the lung. The thrombus is composed case as 5.159. Early thrombus composed mostly of numerous
of dense fibrin , many tlu-ombocytes, and red blood cells, and it thrombocytes. The thrombus is filling the vascular lumen and
contains numerous bacteria. trapping fibrin.

Avian Histopathology (4 th Edition) I 189

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 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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5.161. Spleen. Septic thrombus. Adu lt pheasant. Arteri ole in
the spleen is filled with thrombus composed of bacteria and necrotic
debri s. The wall of the arteriole appears di srupted. The term septic
thrornboarteriolitis may be used. The pheasant was affected with
erysipelas caused by E,:vsipelothrix rhusiopathiae.
5.163. Mesenteric blood vessel. Ade novirus inclusio ns.
Cockatiel. Nuclei of endothelial cell s are enlarged (karyomegal y)
and filled with deep ly basophi lic inclusion bodies characteri stic of
adenovirus infection . This was an incidental finding of uncertain
significance.

5. 162. Brain (cerebral hemisphere). Bacterial vasculitis. 6-day- 5.164. Artery. Toxoplasmosis. Backyard chicken. Diffuse
old broiler breeder pullet. The wall of a sma ll blood vessel and a necrosis of the wall of an artery, with numerous intralesional
narrow zo ne of brain tissue aro und it are heav ily colonized by thin, To.roplas111a tissue cysts containing bradyzo ites.
elongated bacteria. The wall of the vessel is disrupted, although
endothelial cells can still be identified. The tissue surrou nding
the vessel appears necrotic and is infiltrated by mononuclea r
inflammatory cells . Note the bacteria in the neuropil around the
blood vessel. This bird had yolk sac infection and septicem ia
ca used by Pse11do111011as aem ginosa.

190 f American Assoc iati on of Avian Pathologi sts

 Cardiovascular System
VetBooks.ir

5.165. B rain. Intraendothelial organisms. Muscovy duck 5.167. Lung. Necrotizing mycotic vasculitis. African gray
dis ease. Numerous small organisms are in endothelial cells of a parrot. The wall of a blood vessel in the lung is invaded and
blood vessel in the brain. Insert. Higher-power view showing damaged by fungal hyphae of Asp erg illus.fumigatus, which has the
orga ni sms. (Image co11r/e5y of Richard Julian) . tendency to invade blood vessels walls.

5.166. Lung. Intraendothelial organisms. Muscovy duck 5.168. Lung. Necrotizing mycotic vasculitis. 5-month-old
dis ease. Capillaries of the lung contain numerous small parasitic parakeet. The wall of large blood vessel at the hilum of lung
organisms. Insert. Higher-power view showing organisms. (Image (likely pulmonary artery) is severely necrotic and invaded by fungal
courtesy of Richard Julian). hyphae, which are visible in the image. Remnant of the blood vessel
wall is still recognizable. The lumen is filled with necrotic debris.
The lesion was caused by A5p ergillus .fi1migatus, which has the
tendency to invade blood vessels walls.

Avian Histopathology (4 th Edition) I 191

 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
VetBooks.ir
5.169. Vennie in intestine serosa. Schistosomiasis. 4-week-
old swan. Venule in the intestinal serosa has marked myointimal
hyperplas ia, with almost complete obliteration of the lumen. The
bird was affected with schistosom iasis ca used by Trichobilharzia
sp .
5.170. Vennie in liver. Schistosomiasis. 4-week-old swan.
Venule in the lung has marked myointimal hyperp lasia, w ith almost
comp lete obliteration of the lumen . The bird was affected with
schi stosomias is caused by Trichobilharzia sp.
192 I American Association of Avian Pathologists
5.171. Venule in liver. Schistosomiasis. Goose. Portal ven ule ha s
marked myo intimal hyperplas ia, with a lm ost complete obliteration
of the venule lumen. The bird was affected with sc hi stoso mi asis
caused by Trichobilharzia sp . Two bile ductules are seen.
:!
.-,,-,
~1
·.~·
5.172. Venule in liver. Schistosomiasis. 3-week-old duckli ng.
Venule in the mesentery between pancreatic lobes shows marked
myoi ntimal hyperplasia w ith almost complete obliteration of the
lumen . Note that the artery adj acent to the vein is unaffected.
 Cardiol'(tscular System
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5.173. Venule in liver. Schistosomiasis. 3-week-old duckling.
Terminal hepatic venule shows segmental endophlebitis
cha rac terized by expansion of the intima by proteinaceous material
containing nuclear debris.
5.175. Venule in liver. Marek's disease. 8-month-old backyard
chicken. The wall of terminal hepatic venule is diffusely infiltrated
with pleomorphic lymphoid cells. The bird was affected with
the classic (neural) form of Marek's disease, in which diffuse or
segmental infiltration of the wall of venules in the liver seems to be
a relatively common lesion.

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5.1 74. Venule in liver. Schistosomiasis. 3-week-old duckling. 5.176. Venule in liver. Marek's disease. 2.5-year-old backyard
Higher- power view of the lesion in the terminal hepatic venule m chicken. Segmental, dense infiltration of the wall of terminal
5.173 . Note the disruption of the endothelial cells. hepatic venule with lymphoid cells. This bird was affected with the
classic (neural) form of Marek 's disease.

Avian Histopathology (4 th Edition) I 193

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 Tahseen Abdul-Aziz • Oscar J. Fletcher
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I 5.177. Vennie in liver. Marek's disease. One-year-old backyard

chicken. Another image of segmental, dense infiltration of the
wall of terminal hepatic venu le with lymphoid cells. This b ird was
affected with the classic (neural) form of Marek 's disease.
5.179. Heart. Hemangiosarcoma. 12-year-old parrotlet.
Higher-power view of the hemangiosa rcoma showing groups of
immature endothelial cells that tend to form vascular spaces.

5.178. Heart. Hemangiosarcoma. 12-year-old parrotlet.

Area in the myocardium has neoplastic tissue composed of
inm1ature endothelial cells that tend to form small vascular spaces,
some of which contain red blood cells. The bird had metastatic
hemangiosarcoma. The primary site of th e neoplasm was uncertain.

194 I American Association of Avian Pathologists

VetBooks.ir
CHAPTER
Respiratory System
Oscar J. Fletcher • Tahseen Abdul-Aziz
Anatomy and Histology
The respiratory system begins at the nares and includes the nasal
chamber, larynx, trachea, syrinx, lungs, air sacs, and associated si-
nuses and glands . The nasal chamber contains cartilaginous turbi-
nates (conchae) that provide support and divide the chamber into
rostral , middle, and caudal compat1ments. The rostral nasal chamber
is lined by squamous epithelium having a distinctive scalloped sur-
face resembling the pattern of a tile roof. The middle nasal chamber
is lined by pseudostratified columnar ciliated (respiratory) epithe-
liUtn. Variable numbers of lymphocytes and numerous intraepithe-
lial mu cous glands containing goblet cells are in the lamina propria .
The caudal nasal chamber begins with a respiratory epithelial lin-
ing that changes to specialized olfactory epithelium comprised of
basal cells, supporting cells, and sensory cells . This arrangement of
turbin ates and chambers increases the respiratory surface area and
facilitates the critical filtering function as well as providing for tem-
perature and humidity modifications that occur as air moves from
the envtronment into the gas exchange system in the lungs. Nasal
(salt) glands and their ducts are located lateral to the nasal cavity.
Large nasolacrimal ducts drain secretions of the Harderian and lac-
rimal glands. They are lined by respiratory epithelium and enter
the lateral walls of the middle nasal chambers. Paired infraorbital
sinuses are located ventral and anterior to the orbit, occupy a large
area in the head, and are lined by squamous or low to medium cili-
ated columnar epithelium with a few simple mucous glands. The
number of glands and amount of ciliated epithelium increases near
the entrance of the sinus into the nasal cavity. Communication of
infraorbital sinuses with the nasal cavity is located caudally and
dorsall y, thus the sinuses discharge onto the ventral p011ion of the
olfact01y epithelium in the caudal nasal chamber. This anatomi-
cal arrangement makes drainage from the infraorbital sinus difficult,
and explains the swelling of the sinus that is common in sinusitis as-
sociated with many respiratory infections. The choanal cleft in the
floor of the nasal chamber provides direct communication between
the nasal and oral cavities and forms the oropharyngeal region. The
latynx is lined by cuboidal to columnar ciliated epithelial cells.
The trachea is lined by ciliated pseudostratified columnar epi-
thelium similar to that found in the middle and posterior nasal cham-
bers. The lamina propria of the normal tracheal mucosa is relatively
thin and contains large numbers of simple alveolar mucous glands.
Goblet cells are more prominent in the distal portions of the tra-
chea. The ciliated epithelium, mucus, and mucous secreting cells
in the respiratory tract comprise the mucociliary blanket (mucocili-
--
6
my escalator), which constitutes an essential mechanism for entrap-
ment and clearance of particulate material from the respiratory tract.
The wave-like, propulsive action of cilia moves entrapped pat1icles
through the mucus layer toward the phatynx where they can be
swallowed. Damage to the respiratory mucosa! epithelium impairs
this functional capacity to clear inhaled particles. Defective clear-
ance by the upper respiratory tract is a significant factor enabling
I
bacteria, e.g., Escherichia coli, to colonize and damage the lower
respiratory tract and, in some cases, to invade the blood stream and
cause septicemia. Cartilaginous rings that are complete and over-
lap with adjacent ones support the trachea. Thin, strap-like tracheal
muscles along either side of the trachea provide tension as the neck
is extended and contracted and contribute to vocali zations.
The avian lung has a characteristic structure that is very dif-
ferent from that of mammals. Primary bronchi are lined by pseu-
dostratified columnar ciliated epithelium, with variable numbers
of mucous glands and focal areas of lymphoid tissue in the lamina
propria. Secondary bronchi that arise from primary bronchi also are
lined by similar epithelium but have few or no car1ilaginous rings.
Parabronchi, also termed tertiary bronchi, arise from secondary
bronchi and form the core of the hexagonal respiratory units or lob-
ules where gas exchange occurs in the surrounding air-blood capil-
lary bed. Parabronchi are supported by smooth muscle, which is
usually prominent beneath the parabronchial epithelium. Air flows
from parabronchi into atria that open off the parabronchus. Atria
are separated from each other by interatrial septa. Septa are com-
posed offibrovascular connective tissue and have smooth muscle on
their surface. By contracting and relaxing, smooth muscle controls
airflow into the atria. Macrophages are often found in the intersti-
tiutn at the base of septa. Air from atria flows into infundibula that
extend off of the atria and connect with air capillaries where gas
exchange occurs. Respiratory lobules consisting of a para bronchus,
atria, infundibula, and air-blood capillary bed are separated by thin
interstitial tissue that contains blood vessels, nerves, and occasion-
ally small parasympathetic ganglia.
Parabronchi are lined by a simple cuboidal to squamous epithe-
lium that continues into the atria and infundibula . Air capillaries are
lined by simple squamous epithelium. Parabronchi anastomose and
form extensive networks, thus creating a continuous flow system
with no blind endings. Endothelial cells of blood capillaries are
separated from epithelial cells of air capillaries by a single base-
ment membrane, thus forming a highly efficient arrangement for gas
exchange. There are two types of parabronchi, paleopulmonic and
Avian Histopathology (4 th Edition) J 195
 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
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neopulmonic, but they cannot be differentiated by histology as they
have similar diameter and structure. Epithelial cells lining atria and
infundibula respond quickly to injuty by becoming hypertrophic,
hyperplastic, and, in some cases, resulting in the generation of nu-
merous phagocytic cells. This pattern is a proliferative response in
contrast to an exudative response characterized by fibrin, hetero-
phils, histiocytes (macrophages), and lymphoid cells. Exudative
and proliferative responses often occur together.
Air sacs originate from the ends of primary and some second-
ary bronchi . Small air saccules extend from parabronchi on the sur-
face of the lung. Air sacs are lined by simple squamous epithelium ,
but there are scattered patches, also called tracts, of ciliated colum-
nar epithelium that are more numerous at the openings (ostia) of the
air sacs from the bronchi. Tracts of mucociliary epithelium extend
from the ostia caudally but they are difficult to appreciate in routine
histologic sections. These patches or tracts of respiratory epithe-
lium provide sites for attachment of organisms, e.g., mycoplasma.
The number of air sacs varies from 7 to 9 among avian species.
The cervical, clavicular, and cranial thoracic air sacs are grouped
together as the cranial air sacs. The caudal thoracic and abdominal
air sacs are grouped together as the caudal air sacs. This grouping
is important because air entering the cranial air sacs is filtered by
passing through portions of the lung, whereas air entering the cau-
dal air sacs does not have this filtration step. This makes caudal air
sacs more likely to be sites of infections. Air sacs extend into the
pneumonic bones, and air sac infection can extend into these bones,
resulting in osteomyelitis. Air sacs serve as a bellows system to
move air through the fixed lungs. Air moves in a unidirectional pat-
tern through the lung - caudal to cranial - with the air flowing in a
countercurrent direction to the flow of blood in the blood capillary
network. This large and efficient gas-blood exchange surface results
in increased susceptibility to inhaled toxic substances. Practical ap-
plication of this fact was the earlier use of canaries for detection of
toxic gases in mines.
Responses to Injury
Changes that suggest or establish a diagnosis based on histopathol-
ogy primarily include the distribution and type oflesions within the
respiratory system. Lesion pattern recognition requires identifica-
tion of specific changes, relating the lesions to normal structures,
and identifying the extent and severity of the changes. Focal, mul-
tifocal, and diffuse are terms used to describe extent. Mild, moder-
ate, and severe are terms frequently used to describe tbe severity
of lesion, but these terms need to be defined so that the meaning is
clear to the reader.
Histologic evidence of injury to the respiratory epithelium
includes loss of cilia (deciliation), swelling and hydropic vacuola-
tion of cells, desquamation, necrosis, hyperplasia, and metaplasia.
Mucous glands may be hypertrophic or hyperplastic or may show
loss (depletion) of mucus, necrosis, or atrophy. Inflammatory le-
sions are primarily characterized by hyperemia, deposition of fibrin ,
and infiltration of inflammatory cells that include heterophils, lym-
phocytes, macrophages, and plasma cells. Hemorrhage may occur,
but care must be exercised in interpreting the presence of blood in
airways of the trachea, bronchi, and parabronchi, as blood readily
196 I American Association of Avian Pathologists
flows through tears in the air sacs during postmortem examination,
and is a common artifact.
Epithelial cell hyperplasia, particularly evident in trachea ,
but also seen in primary and secondary bronchi , can result in 5-6
layers of undifferentiated cells that later may differentiate into
ciliated cells and mucous gland cells. Epithelial cell hyperplasia
is not a unique disease-specific lesion, but rather a general re-
sponse triggered by epithelial cell damage. This lesion indicates
the regenerative or repair phase following injury to the respiratory
mucosa. Regeneration of the epithelium occurs rapidly, begin-
ning within 48 hours. Repair with restoration to relatively normal
epithelium may be accomplished within a few to several days,
depending on the nature and severity of the injury and on th e
presence of secondary or synergistic infections . Increased num-
bers of lymphocytes, macrophages, and plasma cells in the lamina
propria are frequently found in the reparative/ regenerative phase.
Lymphoid cells may aggregate to form lymphoid nodules, some
with germinal centers.
Basic responses of the respiratory system to inju1y can be initi-
ated by environmental insults e.g., excess ammonia and dust, spray
administration of live vaccines, infection with respiratory viruses,
bacteria, fungi, parasites, etc. Environmental insults and respiratoty
viruses (including viruses in live vaccines) frequently result in dam-
age to the defense mechanisms of the respiratory system leading
C
to bacterial infections. A single cause of respiratory pathology is
usually the exception when dealing with clinical material. In many
cases, it is a challenge to establish a specific etiologic diagnosis of a
respiratory disease on the basis ofhistopathology alone.
Although some lesions in the respiratoty system are specific,
e.g. , intranuclear inclusion bodies in syncytial epithelial cells in in-
fectious laryngotracheitis or presence of identifiable infectious and
parasitic agents, most lesions are not disease specific. The patterns
of injury and response provide guidelines as to possible etiology.
For example, the transition between squamous epithelium lining the
anterior nasal chamber and respiratory epithelium lining the middle
nasal chamber is a common site for squamous metaplasia that oc-
curs in vitamin A and some B-vitamin deficiencies . Histologic ex-
amination of cross sections of the head that include the sinuses and
nasal cavities can provide insights into the spread of inflammatory
processes between various interconnected compartments.
Non-Infectious Conditions
Mechanical injury to the nasal chamber and associated turbinates
can be caused by trauma that may occur in the beak trimming pro-
cess or during placement of chicks or poults. Lesions include ne-
crosis with loss of epithelium, inflammation, and, in some cases,
necrosis of the underlying turbinate cartilage. Colonies of bacteria
may be seen in the necrotic tissue. Plant material may be found in
the nasal chambers and is associated with increased amounts of mu-
cus, inflammation, necrosis, and regeneration of epithelium. This
foreign material likely originates from the litter.
Inhalation of ammonia, dust, or other noxious gases can cause
lesions and most often makes the respirato1y system more suscep-
tible to infection, especially bacterial infection. Alterations in the
morphology of cilia or loss of cilia, attenuation of the mucosa I epi-

theliu m, mucosa[ gland and goblet cell hypersecretion and hyper-
plasia, and accumulation of excess mucus in the lumen of airways
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occurs in response to ammonia exposure . The severity of lesions
depends on the cumulative exposure, which may result from a high
level of short duration or low level for a long period of time.
In the lungs, dust material may be found free or within macro -
phages adjacent to parabronchi and atria and may not be associated
with any other responses. A modest histiocytic response may occur.
Lymphocytes may indicate an inunune response to antigenic materi-
al in th e dust, such as feather dander. Dust material usually appears
as irregular, retractile, brown particles that are often variably bifre-
fringent with polarized light. Carbon particles produce a similar
tissu e res ponse but are black and relatively uniform. They typically
result from smoke inhalation including second-hand tobacco smoke.
Larger plant pa1iicles in the lungs cause granuloma formation in
the wall s of para bronchi. They are readily identified by their thick
cell wa lls and are strongly PAS positive but variably bifrefringent.
Inhaled silica stimulates granuloma formation and fibrosis. Lesions
are m ultifocal and contain characteristic strongly bifrefringent,
non-sta ining crystalline, pa1iicles. Urates retained because of renal
failure may become deposited in vessel walls , and in the capillary
network of the respiratory lobules . Necros is, heterophilic and his-
tiocyti c infiltration, and the typical feathery, starburst pattern left by
the urate crystals, which dissolve in aqueous solutions during tissue
process ing, are seen. Diffuse deposition of mineral along basement
membranes (metastatic mineralization) in the lungs may occur in
chronic renal failure.
Tox ic gas injury is exemplified by polytetrafluoroethylene
(PTFE) released when Teflon® coated surfaces are overheated .
This injury is characterized by accumulation of protein rich fluid
includi1ig fibrin in bronchi, especially in parabronchi and secondary
bronchi. Pneumocytes become hyperplastic frequently resulting in
accumulation of large numbers of macrophages. Exogenous lipid
pneumonia has many of the same features with accumulation of lip-
id in th e cytoplasm of macrophages and/or proliferation of adipose
cells within lobules.
Infections
Viral infections
Infectious bronchitis virus , avian influenza virus , certain types of
avian paramyxoviruses (including Newcastle disease) , metapneu-
movirus, poxvirus, adenovirus, and laryngotracheitis virus are
important viral pathogens of the avian respiratory system. Viral
infections may result in minimal and transito1y lesions unless com-
plicated by environmental factors and/or secondary bacterial infec-
tion s. Initial damage and impairment of the respiratory defense
mechani sm frequently lead to complications caused by a second-
a1y bacterial invaders, e.g. , E. coli. Adenoviruses produce large,
irregular, basophilic, intranuclear inclusions in respiratory epithelial
cells with minimal, if any, inflammatory response in turkeys. Quail
bron chitis is an adenoviral infection that causes severe damage and
inflammation of the tracheal mucosa. There may be similar necro-
ti zing and proliferative lesions in the epithelia of the nasal mucosa,
prima1y and seconda1y bronchi, nasal passages, and air sacs. Air
sacs often contain necrotic debris and have regions of epithelial
--
Respimto1J' System
hyperplasia associated with increased thickness of the airsac wall.
Multifocal necrosis with intranuclear inclusion bodies also may be
found in visceral organs, especially liver.
Infectious laryngotracheitis, a herpes virus infection of
chickens, causes extensive necrosis of epithelial cells, frequently
with hemorrhage . Necrosis leads to regenerative hyperplasia of
the epithelium in birds that survive the initial acute phase of infec-
tion. Intranuclear inclusions in individual cells and in character-
istic large syncytial epithelial cells may be found in conjunctiva!
epithelium, epithelium of the middle nasal chambers and infraor-
bital sinuses, tracheal epithelium, and/or in bronchial epithelium,
especially at the junction with air sacs, and in air sacs. Syncytial
cells with intranuclear inclusions also may be present in the mu -
cosa of the upper alimentary tract. Typically a single large, finely
granular, basophilic inclusion body fills the entire nucleus, but
inclusions can be small, eosinophilic, and surrounded by a halo.
Margination of nuclear cluomatin is often prominent. Marked het-
erophilic infiltrates and intraluminal fibrinoheterophilic exudates
are common in the early, acute phases of infection. Exam ination
I
of exudate in the tracheal lumen may reveal single cells or syncy-
tial cells with inclusion bodies when none can be found in the mu-
cosa. Areas of epithelium that are not necrotic show loss of cilia
and increased mucous production. Lymphoid cell infiltrates in the
lamina propria of the tracheal mucosa are a common response if
affected chickens survive several days. It is usually necessary to
examine multiple sections of trachea and conjunctiva, preferably
from several chickens with clinical signs of respiratory diseases, in
order to find syncytial cells with inclusion bodies characteristic of
the disease. Syncytial cells with inclusion bodies may be difficult
to identify in birds in the recovery phase, or in birds with exten-
sive necrotic and inflammatory lesions as inclusion bodies are only
present for a few days .
Avian influenza, infectious bronchitis, and infection with cer-
tain avian paramyxoviruses, especially avian paramyxovirus type 1
(Newcastle disease virus), cause similar lesions in the respirato1y
system and thus diagnosis of a specific viral etiology cannot be
made by histopathology alone. Loss of cilia and swelling, hydropic
degeneration, and necrosis of epithelial cells are followed by epi-
thelial regeneration, in which multiple layers ofregenerating, undif-
ferentiated epithelial cells line the mucosa. The associated inflam-
matory response results in edema, and heterophilic and lymphocytic
infiltrate in the lamina propria. Heterophils, especially those in the
luminal exudate, usually degranulate, and become difficult to recog-
nize. Mucous gland hype1irophy and hyperplasia are frequent. The
trachea is a primary target site for both avian paramyxovirus type
1 and infectious bronchitis virus. Influenza virus is likely to cause
lesions in lungs and sinus, in addition to the trachea. Infectious
bronchitis tends to cause necrosis of widely scattered individual epi-
thelial cells that may be phagocytized by macrophages resulting in
a pattern of hyperplastic epithelium containing vacuoles. Increased
thickness of the tracheal mucosa due to epithelial hyperplasia and/or
increased numbers of lymphoid cells in the lamina propria are char-
acteristic lesions of infectious bronchitis and avian paramyxovirus
type 1 infections; however, it is important to emphasize that those
lesions are not diagnostic for either disease.
Avian Histopathology (4' h Edition) I 197
 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
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The diphtheritic form of avian pox is characterized by hy-
perplasia and ballooning degeneration of epithelial cells, with the
presence of large, eos inoph ilic, intracytoplasmic inclusion bod-
ies in infected cells . Epithelial hyperplasia frequently results in
prominent projections of cells into the tracheal lumen . Necrosis,
varying degrees of inflammation, and secondary infecting bacteria
are present.
Bacterial i11fectio11s
Bordetella avi11111, Avibac/eri11111 paragallinan1111 (formerly Hae-
111ophil11s paragallinarn111) , Ornithobacleri11111 rhino/racheale
(ORT), Pas/e11rella 11111/tocida, E. coli, Staphylococcus spp., Rie-
merella analipestife,; Gallibac/eri11111 analis, Mycobac/eri11111 spp. ,
other less frequently occurring bacteria, mycoplasmas (Mycoplas-
ma galliseplic11111, M. synoviae, M. meleagridi;), and Ch la111ydia
psillaci are bacterial agents that share many common tissue re-
sponses to injury, yet have so me distinctive features that aid in
their identification. The infraorbital sinus is a primary site of in-
fection with Avibaclerium paragallinarn111 ; a characteristic feature
I
is the presence of numerous bacteria associated with cilia. The
trachea is a primary s ite of infection with Borde/el/a avi11111 , with
bacteria characteristically closely associated with cilia of the mu -
cosa[ epithelium in acute infections. Degenerative lesions (loss
of basophilia) in the tracheal carti lage may be present in chronic
cases ofbordetel losis and lead to marked deformity of the trachea l
rings. Hyperplastic bronchial-associated lymphoid tissue in the
lung is another feature of avian bordetellosis.
Pasleurella 111111/ocida, ORT, E. coli, and staphylococci pro-
duce major lesions in the lungs. Lesions caused by P 111111/ocida
and ORT are characterized by large areas of necrosis with edema
and accumulation of fibrin and heterophils in interstitial tissues,
capi ll ary beds, and bronchi. Necrotic areas often contain visible
basophilic bacterial colonies . In E. coli pneumonia, necrosis also
is a prominent feature , but lesions are usually centered on para-
bronchi with less involvement of the capil lary bed and interstitial
tissues. Bacterial colonies are usually visible in exudate and ne-
crotic areas. Characteristic coliform colonies are composed of
bacilli , are round with a thin densely stained margin , and have
irregular lack of staining centrally. In acute infections in young
or immunosuppressed birds, macrophages with large numbers of
intracytoplasmic bacteria may be seen . Epithelium of primary
and secondary bronchi is likely to have loss of ci li a and show
degenerative, necrot ic, and hyperplastic changes. Activated epi-
thelial cells of the atria and infundibu la become hypertrophic,
hyperplastic, and result in an increased cell ularity within affected
parabronchi. Heterophils usually are numerous. Parabronchial
casts composed of caseous exudate conta inin g typical colonies
are characteristic of co li form pneumonia. A thick layer of fibrino-
heterophilic exudate may be present on the pleural surface (pleu-
ritis). Air sacs are common lesion sites in respiratory colibacil-
losis, with ep ithelial cell necrosis and regeneration, edema, fibrin,
heterophil s, and lymphoid cells accumulating that increase the
thicknes s of the affected air sacs. Staphylococcus may produce
multifoca l granulomatous les ions that resemb le mycotic infec-
tions both gross ly and micro scopically. However, intralesional
198 I American Association of Avian Patholog ists
botryoid colonies composed of gram-positive cocc i readily di s-
tinguishes staphylococcal lesions from those produced by fun g i.
Other bacteria may cause similar lesions in the lungs and air sacs
so that identification of a specific bacterial agent may not pos-
sible. Isolation and identification should be done in conjunction
with histopathology.
Infection with Nlycobacteri11111 can result in multiple histiocytic
granulomas in the lungs. They usually have a central area of case-
ous necrosis surrounded by large macrophages (epithelioid cells)
and multinucleated giant cells, or they may be composed on ly of
aggregates of primarily large macrophages. ln either case, macro-
phages in the granu lomas usually have abundant cytoplasm with a
finely granular appearance. An acid-fast stain reveals numerou s ac-
id-fast bacilli in the cytop lasm of few or many macrophages. Simi-
lar lesions are likely in the digestive tract and may also be found in
other organs including the skin.
Chlamydiosis caused by Chlamydia psiltaci often causes in-
filtration of lymphoid cells in parabronchi and interstitial tissue, ac-
companied by hyperplasia of epithelial cells in atria and infundibula.
Airsacculitis, characterized by the presence of fibrin , heterophils, and
lymphoid cells, with epithelial cell hyperplasia, is common in chla-
mydiosis. lntracytoplasmic colonies of the organism appear as cyto-
plasmic basophilic smudges, but are not common and difficult to defin-
itively identify. They stain bright red w ith Macchiavello or Gimenez
C
stain. lmmunohistochemishy is used to confirm the diagnosis.
The most common sites for lesions caused by A1ycoplas111a are
sinuses, trachea, and air sacs, although lungs also are often involved.
Lymphocytic tracheitis and sinusitis and mucus gland hyperplasia
in sinuses are characteristic lesions of M. galliseptic11111 infection in
chickens and turkeys, but they are not diagnostic. Presence of many
lymphocytes in diffuse and nodular collections (lymphofollicular
reaction), in lungs and air sacs is suggestive of mycoplasmal infec-
tion. Marked hyperplasia of bronchial-associated lymphoid ti ssue
in lungs should arouse suspicion of mycoplasmal infection. Acute
inflammation, characterized by fibrin and infiltration of large num-
bers of heterophils with few, if any, lymphocytes, is prominent in
the early stages of mycoplasmal infections. Epithelia l regeneration
fol lowing initial damage by mycoplasma is common. Additional
microbiologic or serologic testing should be done to confirm myco-
plasmal infections .
Fungal i11fectio11s
Mycotic infections of the respirato1y system are common. Asper-
gillus spp. and Ochroconis gallopava are the fungi most frequently
infecting turkeys and chickens. Phycomycetes may occasionally be
isolated. Lesions caused by fungi are most common in the lungs
and air sacs but they may also be found in trachea (mycotic trache-
itis). Mycotic granu lomas usua ll y occur as multiple, variably sized
areas of caseous necrosis surrounded by macrophages and multi-
nucleated giant cells. Non-caseous granulomas consisting ofh istio-
cytes and multinucleated giant cells are also a histologic feature of
mycotic infection. In some granulomas, fungal hyphae are present
within the necrotic areas . Visua li zat ion of fungal hyphae, enhanced
by special stains such as periodic acid Schiff (PAS) or Gomori 's
methenamine silver (GMS), is diagnostic.

Parasitic i11fectio11s
Parasitic infections are diagnosed by identifying the agents in re-
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spiratory lesions. Cryptosporidiosis is an example of a protozoan
disease that causes loss of cilia and pronounced hyperplasia of epi-
thelial ce ll s. Cryptosporidia are round to ovoid, basophilic bodies,
about 4-6 pm in diameter, and are intimately associated with the
surface of mucosa! epithelium. In pet birds infected with the proto-
zoan Sarcocystis falcatula, there is interstitial pneumonia and areas
of necrosis and fibrin deposition in the lung. Oval or long, sinuous
meront s are found in the vascular endothelium of blood capillaries
in the capillary bed. Gametocytes of leucocytozoon, and meronts
of Plasl/lodiu//1, Haemoproteus, and l eucocytozoon may be found
in the lung where they plug blood capillaries. Presence of protozoan
parasites in the lungs is suspected when the pattern of e1ythrocytes
in the air capi llaries is altered with the erythrocytes not being "lined
up" to pass through the blood capillaries in the usual pattern.
The nematode Syngamus trachea can cause epithelial cell hy-
perplasia and loss of cilia with increased thickness of tracheal muco-
sa due to lymphoid cell infiltration. The buccal cavity of the parasite
can invade tracheal cartilage. The air sac mite Cytoc61tes 1111dus may
be found in bronchi , lungs of chickens, turkeys, and few other avian
species. Other mites infect the respiratory passages of other avian
species. Notable among these is Stemoslol/la tracheacolum, which
infects canaries, finches, and other passerine species.
Neoplasia
Although relatively uncommon in poultry, primary or metastatic tu-
mors may occur in the respiratory system, particularly in the lung.
Primary tumors are reported as arising from respiratory epithelium
of primary or secondary bronchi , and from air sac epithelium. Ad-
enocarcinomas, including those of reproductive tract origin, may
metastasize to the lung. Squamous cell carcinomas and melano-
sarcomas are described in the lung. Lymphoid tumors of Marek 's
disease are the most common tumors found in the lungs of chickens.
Additional Readings
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Ackermann, M. R. and N. F. Cheville. 1991. Ultrastructural
studies of the lung of turkeys (Meleagris gallopavo) inoculated
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Arp, L. H. and N. F. Cheville. 1984. Tracheal lesions in young
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Bang, B. G. and F. B. Bang. 1959. A comparative study of the
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Bang, B. G. and F. B. Bang. 1969. Experimentally induced changes
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Bang, B. G. , F. B. Bang, and M. A. Foard. 1972. Lymphocyte
depression induced in chickens on diets deficient in vitamin A
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-
Respiraf01J 1 System
Bang, B. G. and B. M. Wenzel. 1985. Nasal cavity and olfactory
system . In: A. S. King and J. Mclelland (eds.) Form and
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225.
Bang, F. B., B. G. Bang, and M. Foard. 1975 . Acute Newcastle
viral infection of the upper respiratory tract of the chicken. II .
The effect of diets deficient in vitamin A on the pathogenesis of
the infection. Al/I J Pathol 78:417-426.
Bang, F. B., M. Foard, and B. G. Bang. 1974. Acute Newcastle
viral infection of the upper resp iratory tract of the chicken.
I. A model for the study of environmental factors on upper
res piratory tract infection. Am J Patho/ 76:333-348.
Beernaert, L.A. , F. Pasmans, L. Van Waeyenberghe, F.
Haesebrouck, and A. Martel. 20 I0. Aspe,gillus infections in
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Benyeda, Z., L. Szeredi, T. Mato, T. Suveges, G. Balka, Z.
Abonyi-Toth, M. Rusvai, and V. Palya. 2010. Comparative
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Massachusetts and 793/B serotypes of infectious bronchitis
I
virus infection in chickens. J Col/Ip Pathol 143:276-283 .
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lesions induced by two strains of infectious bronchitis virus. J
Comp Pathol 145:319-326.
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Brackenbury, J. H. 1971. Airflow dynamics in the avian lung
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Brackenbury, J. H. 1972. Physical determinants of air flow pattern
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Brash, M. L. , J. N. Swinton, A. Weisz, and D. Ojkic. 2009.
Iso lation and identification of duck adenovirus I in ducklings
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Avian Histopathology (4'h Edition) I 199
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560 .
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Dis 48:34-49.

Jiijis, F. F. , S. L. Noll, D. A. Halvorson, K. V. Nagaraja, and D . P.
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63 .
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169.
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I
United States. Avian Pathol 38:47-53.
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Soriano-Vargas. 20 I 0. Histopathologic findings in chickens
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and J. Gelb, Jr. 2002. Nephropathogenic infectious bronchiti s
in Pennsylvania chickens I 997-2000. Avian Dis 46:847-858.
 Respiratory System
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6.1. Upper respiratory system. Normal. Chicken. The 6.3. Upper respiratory system. Normal. Chicken. Structures
relation ships of the compartments of the avian upper respiratory identified in this cross-section posterior to the plane of figure 6.2 are:
system are shown in this sagittal section. A. naris; B. rostral nasal A. choanal opening; B. infraorbital sinus; C . middle nasal chamber;

I
chamber; C. middle nasal chamber; D. caudal nasal chamber; E . D . nasolacrimal duct; E. nasal gland; F. caudal nasal chamber and
Harder ian g land ; F. infraorbital sinus; G. nasolacrimal duct. the nasal septum.

6.2. Upper respiratory system. Normal. Chicken. Structures 6.4. Naris and rostral nasal chamber. Normal. Chicken. A.
identified in this cross-section are: A. infraorbital sinus; B . The rostral nasal chamber is lined by squamous epithelium. B. The
na solacrimal duct; C. middle nasal chamber; D . dorsal region of the infraorbital sinus is lined by simple or low cuboidal epithelium.
middle nasal chamber; E. nasal gland; NS. nasal septum.

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 Oscar J. Fletcher • Tahseen Abdul-Aziz
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6.5. Junction of rostral and middle nasal chambers. Normal. 6.7. Rostral concha (turbinate). Normal. Chicken. The
Chicken. The change from squamous to ciliated pseudostratified squamous epi thelium has characteristic scalloped appearance.
ep ithelium is illustrated (a rrow). This is a site for sq uamous

I
metaplasia in vita min A deficiency.

C.

6.6. Junction of rostral and middle nasal chambers. Normal.
Chicken. The rostral nasal chamber is lined by squamous
epithelium and the middl e nasa l chamber is lined by respiratory
(ci li ated pseudostratified) epithelium containing mucus g lands.
Note the abrupt tran siti on .
6.8. Infraorbital sinus and related structures. Normal.
Chicken. Sagittal section to illustrate: A. rostral nasal chamber; B.
infraorbital sinus; C. nasolacrimal duct; D. middle nasa l chamber;
E. duct of the nasa l gland.

204 I America n Associat io n of Av ian Pathologists

 RespimtolJ' System
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Sinus Middle
Nasal
Chamber

6.9. Nasolacrimal duct and infraorbital sinus. Normal. 6.11. Middle nasal chamber and posterior region of the
Chicken. The normal respiratory mucosa of the nasolacrimal infraorbital sinus. Normal. Chicken. Note the numerous mucous
duct is compared to the normal mucosa of the infraorbital sinus. glands in the respirato1y epithelium of the middle nasal chamber.

I
Lymphocytes within the mucosa are expected finding.

6.10. Posterior region - nasal Cavity. Normal. Chicken. 6.12. Caudal nasal chamber and Harderian gland. Normal.
Sagittal section to illustrate : A. posterior nasal cavity; B. middle Chicken. Sagittal section to illustrate: A. caudal nasal chamber. B.
nasal chamber; C. infraorbital sinus; D. nasal gland; E. Harderian Harderian gland.
gland. The area bounded by the box is illustrated at higher
magnification in 6.11.

Avian Histopathology (4th Edition) I 205

 Oscar J. Fletclter • Taltsee11 A bdul-A ziz
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- ,.· t i
, •
• •
I
;
\
·~
1,
·. ,,' . . . ':
...._
=
6.13. Ca udal nasal chamber. Normal. Chicken. Mucosa is 6.15. Middle nasalchamber. Normal. Chicken. Therespi ratory
composed of highly speciali zed olfacto ry epithelium. Detail s of thi s e pithe lium contains num erous mucous g lands. T he surface area is
senso ry epithelium are show n in 6.14. increased due to th e scroll-like arrange ment of the middl e co ncha
(turbin ate) .

6.14. Caudal nasal chamber. Normal. Chicken. Hi gh-power 6.16. Nasal septum. Normal. Chicken. Note th e c iliated
view shows the specia li zed epithelium of the caudal na sal chamber. pseudostratifi ed columnar epithelium, the numerou s mucous glands,
and the surface mucus layer.

206 I A meri ca n Associat io n of Av ian Pathologists


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6.17. Nasal gland. Normal. Chicken. The nasal gland is
composed of tightly packed acini and ducts. See 6. I 8 for higher
magnific ation.
6.1 8. Nasal gland. Normal. Chicken. Note the tightly packed
gl and s and the ducts.
Respiratol)' System
. - . ....
. ..·.
~
". ~
6.19. Choanal cartilage. Necrosis. Chicken. The choanal
cartilage (turbinate) is pink-stained (loss of basophilia) indicating
necrosis. The rostral nasal chamber is on the upper left corner and
the middle nasal chamber is on the lower right corner. The necrosis
was thought to be related to improper beak trimming.
6.20. Middle nasal chamber. Rhinitis. Poult. Large amounts
of mucus are present in the middle nasal chamber. Note the large
amounts of plant material. Choanal cartilage is necrotic and the
nasal septum is deviated. Cause is not known , but may be related to
trauma at placement.
Avian Histopathology (4 th Edition) I 207
 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
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6.21. Nasa l gland. Heterophilic inflammation. Ponlt. The

nasal gland has heterophili c ex udate in the lumen of duct. Pou It had
foreign body rhinitis (see 6.20).

I 6.23. Sinusitis and rhinitis. Laryngo tracheitis. Broiler

breeder chicken. Higher-power view of the infraorb ital sinus on
the left side of figure 6.22 showing the intraluminal exudate and the
increased thickness of the mucosa.
C

6.24. Sinusitis and rhinitis. Laryngotracheitis. Broiler

breeder chicken. Higher-power view of the luminal exudate in the
sinus in 6.23 show in g syncytial cell w ith intranuclear herpesvirus
inclusio ns (box).

6.22. Sinusitis and rhinitis. Laryngotracheitis. Broiler breeder

chicken. Exudate is in the infraorbital sinuses (*) and middl e nasal
chambers of this 6 week old broiler breeder ch icken with infect ious
la1y ngotracheitis.

208 I Ameri can Associatio n of Av ian Pathologists


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6.25. Infraorbital sinus, nasal cavity, and nasolacrimal duct.
Fowl pox. 5-week-old backyard chicken. This cross section of
the bead region shows infraorbital sinus (IOS), rostral nasal chamber
(R), mi ddl e nasal chamber (M), and nasolacrimal duct (NLD). Note
the hyperplasia of the epithelium of the NLD.
6.26. Infraorbital sinus, nasal cavity, and nasolacrimal duct.
Fowl pox. Backyard chicken. Higher-power view of 6.25
showing infraorbital sinus (IOS) with relatively normal epithelium,
unaffected rostral nasal chamber (R), and nasolacrimal duct (NLD)
with ductal epithelial hyperplasia and infiltration of lamina propria.
RespimtoJJ' System
6.27. Infraorbital sinus, nasal cavity, and nasolacrimal
duct. Fowl pox. Backyard chicken. Higher-power view of the
nasolacrimal duct in 6.26 showing hyperplasia with numerous
I
intracytoplasmic poxvirus inclusions.
6.28. Infraorbital sinus, nasal cavity, and nasolacrimal Duct.
Fowl pox. Backyard chicken. Higher-power view of hyperplastic
epithelium of the nasolacrimal duct in 6.27 showing numerous large
intracytoplasmic inclusion bodies that are diagnostic for fowl pox.
Avian Histopathology (4 th Edition) I 209
 Oscar J. Fletcher • Tah seen Abdul-Aziz
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6.29. lnfraorbital sinus, nasolacrimal duct, and middle nasal
chamber. Bacterial sinusitis and rhinitis. Backyard chicken.
The infraorbi tal sinus (IOS) and middle nasal chamber (M) contain
I
luminal exudate. The nasolacrimal duct (NLO) is relatively normal.
6.30. lnfraorbital sinus, nasolacrimal duct, and middle nasal
chamber. Bacterial sinusitis and rhinitis. Backyard chicken.
Same section as 6.29 . Higher-power view of the lumen and mucosa
of the infraorbital sinus showi ng fibrinoheterophilic luminal exudate
and expansion of the wa ll of the si nus with fibrin and heterophi ls.
21 0 I American Assoc iation of Av ian Patho logists
6.31. lnfraorbital sinu s, nasolacrimal duct, and middle nasal
chamber. Bacterial sinusitis and rhinitis. Backya rd chicken.
High-power view of the luminal exudate in the infraorb ital sinus in
6.30 show ing the fibrin and heteroph il s with desquamated epithelial
ce ll s.
6.32. lnfraorbital Sinus, nasolacrimal duct, and middle nasal
chamber. Bacterial sinu sitis and rhinitis. Backyard chicken.
Same section as 6.29. High-power view of the caseous debris in
the midd le nasa l chamber show ing the intralesional bacteria. This
is probably E. coli, but bacterial cu lture is requi red to determine
etio logy.
 Respin1to1J1 System
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6.33. Jn fraorbital Sinus. Chronic sinusitis. Chicken . Caseous 6.35. Middle nasal chamber. Rhinitis. Mycoplasma
necrotic material within the lumen of the infraorbital sinus is typical galliseptic11111 infection. 2-month-old backyard chicken. Marked
of chronic bacterial infections of the infraorbital sinus. lymphoplasmacytic infiltration of the middle nasal chamber mucosa.

I
Mucous glands appear enlarged and increased in numbers, and there
is exudate in the lumen.

6.34. Infraorbital sinus. Sinusitis and rhinitis. Mycoplasma
gal!iseptic11111 infection. Chicken. Mycoplasma gallisepticw11
infection (experimental case). Lymphocytic infiltration and
lymphoid nodules in the wall of the infraorbital sinus .
6.36. Middle nasal chamber. Rhinitis. Mycoplasma
galliseptic11111 infection. 2-month-old backyard chicken. Higher-
power view of area in 6.35 showing thickening of the middle
nasal chamber mucosa by lymphoplasmacytic infiltrates. Note the
enlargement and increased numbers of mucous glands.

Avian Histopathology (4 th Edition) I 211

 Oscar J. Fletcher • Tabsee11 Abdul-Aziz
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6.37. lnfrao,·bital sinus. Sinusitis. Mycoplasma galliseptic11111 6.39. lnfraorbital sinus. Sinusitis. Mycoplasma galliseptic11111
infection. 6-month-old backya rd chicken. Thickening of the infection. IO-week-old bronze turkey. Sinus mucosa is thickened
sinus mucosa by lymphoplasmacytic infiltrate, with accumulation due to infiltration of lymphocytes and plasma cells and hyperpl asia

I
of exudate in the lumen . of mucou s glands.

.
:·.···.
,. , ',.,
\

:t· · ..
. ·. .:,.:
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,:··.•

6.38. lnfraorbital sinus. Sinusitis. Mycoplasma galliseptic11111
infection. 6-month-old backyard chicken. Higher-power
view of the nasa l sinus in 6.37 showing mucosa! thickening by
lymphoplasmacytic infiltrates, swelling of the mucosa! epithelium,
and luminal exudate of proteinaceous material admixed with
heterophils.
6.40. Infraorbital sinus. Sinusitis. Mycoplasma gallisepticum
infection. 10-week-old bronze turkey. Lymphoplasmacytic
infiltration and mucous glands hyperplasia cause thickening of
the sinus mucosa. Mucosa! epithelial cells are swollen and have
rarefied cytoplasm.

212 I American Association of Avian Pathologists

 Respiratory System
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6.41. l nfraorbital sinus. Sinusitis. Mycop/asma galliseptic11111 6.43. Infraorbital sinus. Cryptosporidiosis. 3-week-old
infection. 10-week-old bronze turkey. Higher-power view to duckling. Higher-power view of area in 6.42 showing, in addition
demonstrate swelling, cytoplasmic rarefaction, and vacuolation of to the lesions described in 6.42 , mild infiltrate of mononuclear

I
mucosa! epithelia cells. inflammato1y cells. Even at this magnification, the very small
C1 ypto5poridi11111 organisms associated with the surface of the
mucosa and mucus glands are barely discernible.

6.42. Infraorbital sinus. Cryptosporidiosis. 3-week-old 6.44. Infraorbital sinus. Cryptosporidiosis. 3-week-old
duckling. Hype1trophy of mucous glands, hyperplasia of mucosa I duckling. In this area of the sinus mucosa, epithelial cells are swollen
epithelium, and dysplasia of mucosa. with somewhat rarefied and vacuolated cytoplasm. Small, round,
basophilic bodies morphologically consistent with C1)plosporidiw11
organisms are associated with the surface of epithelial cells.

Avian Histopathology (4 th Edition) I 213

 Oscar J. Fletcher • Tahsee11 Abdul-A ziz
VetBooks.ir

,, ,
•
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6.45. Trachea. Normal. Turkey. Note the thin mucosa! lining, 6.47. Trachea. High ammonia. 20-day-old broiler. Attenuat ion
the overl apping rings of cartilage, and the skeletal muscle outside of the mucosaI epithelium and increase in numbers of goblet cells.
the trachea.

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6.46. Trachea. Normal. Chicken. The trachea is lined by 6.48. Trachea. High ammonia. 45-day-old turkey. Attenuation
pseudostra tified cili ated co lumnar epithelium with numerous of the mucosa! epithelium and increase in numbers of goblet cell s.
mucous glands.

214 I Ameri ca n Associati on of Avian Pathologists

 Respirato1J' System
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6.49. Trachea. High ammonia. 20-day-olcl broiler. Mucous 6.51. Trachea. High ammonia. 28-week-olcl broiler breeder
gland hyperplasia, disruption of the mucosa, and c lumping of cilia. hens. Attenuation of the mucosa, with diffuse loss of cilia. Grossly,
there was excess of mucus in the tracheal lumen. Poor ventilation
was problem in the house.

>'

6.50. Trachea. High ammonia. 20-day-old broiler. High- 6.52. Trachea. High ammonia. 20-day-olcl broiler. Depletion
power view of area in 6.49. of the mucous glands. Depleted mucus glands are dilated and lined
by thinned epithelium.

Avian Histopathology (4 th Ed ition) J 215

 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
VetBooks.ir

, . .. . . ' :",. ~
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6.53. Trachea. Epithelial hyperplasia. Chicken . Epithelial 6.55. Trachea. Infectious bronchitis. 36-day-old broiler.
hyperplas ia is characteri sti c of regenerati on follo w ing tracheal Loss of cilia, lymphoplas macytic infiltration in the mu cosa, and
damage. Metaplas ia of trac heal epithelium also is common. The necros is of muc osa ! indi vidual cells. N ecrotic cells appea r as

I
lesion is not specific as it occurs followin g injury to tracheal muc osa. vacuoles containing debri s. These lesions should arou se suspicion
of in fec ti ous bronchitis. The trachea was pos it ive by PCR test fo r
in fec tious bronchitis virus.

6.54. Trachea. Squamou s metaplasia. Chicken . Squamous
metaplas ia and hyperplasia are indicative of chro ni c tracheiti s. Note
loss of mu co us glands.
6.56. Trachea. Infectious bronchitis. 28-day-old broiler.
Marked lymphoplasmacyti c infi ltration in the mucosa, loss of ci lia,
and necrosis of mucosa ! indi vidual cell s. Necrotic cells appear as
vacuo les containing debri s. The trachea was positive by PCR test
for infecti ous bronchitis virus.

216 I Ameri ca n Assoc iati on of Avian Path ologists

 Respimto,J' System
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-~..
, ., . .,
I•

6.57. Trachea. Infectious bronchitis. 41-day-old broiler. 6.59. Trachea. Infectious bronchitis. 42-day-old broiler.
Hydropic swelling of mucosa! epithelial cells, patchy loss of cilia, Marked mucosa! and submucosal lymphoplasmacytic infiltration,
and mild mucosa! lymphoplasmacytic infiltration. The trachea was necrosis and hydropic degeneration of mucosa! epithelium, some

I
positi ve by PCR test for infectious bronchitis virus. fibrin exudation, and loss of cilia. The trachea was positive by PCR
test for infectious bronchitis virus .

.. ..... .. . r
: '.
,. •- . 4
·~- ·•
6.58. Trachea. Infectious bronchitis. 28-day-old broiler. Early 6.60. Trachea. Infectious bronchitis. 28-day-old broiler.
lesion consists of vacuolar degeneration of mucosa! epithelial cells, Marked mucosa! and submucosal lymphoplasmacytic infiltration
loss of cilia, and mild mucosa! infiltration of lymphocytes and and mucosa! individual cell necrosis, with formation of vacuolar
plasma cells. The trachea was positive by PCR test for infectious spaces containing debris of necrotic cells.
bronchitis virus.

Avian Histopathology (4,1, Edition) I 217

 Oscar J. Fletcl,er • Tal,see11 Abdul-A ziz
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6.61. Trachea. Infectious laryngotracheitis. 55-da y-old 6.63. Trachea. Infectious laryngotracheitis. 63-day-old boiler.
broiler. Large syncytial cell with intranuclear inclusion bodies in As the lesion progresses, mucosa! epitheli al cells desquamate, and
the mucosa . The syncytial cell is still cil iated but eventuall y will contribute to the exudate that accumulates in the lumen. Shown

I
desquamate into the lumen. No te that the mucosa on either side of
the syncyti al cell is still intact. There is mild infl ammatory infiltra te
in the submucosa. Insert in upper right shows higher magnification
of the syncytial cell.
are loss of the mucosa! epithelium, mononuclear cell infiltration of
the lamina propria and submucosa, congestion of blood vesse ls, and
fibrin ocellular exudate with several epithelial syncytial cell s in the
lumen.

··~.
.... .."'-f.," i- .... .},. .,;.:. :.
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.,., 'I
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6.62. Trachea . Infectiou s laryngotracheiti s. 55-day-old broiler. 6.64. Trachea. Infectious laryngotracheitis. 48-day-old
The mucosa! epithelium is irregular and contains syncytial epi thelial boiler. Heterophils and syncytial cells with intranuclear inclusion
cells with intranuclear inclusion bodies. Some syncytial cells are bodies are seen in the lumen. The mucosa! epithelium is replaced
still assoc iated with the mucosa whil e others are desquamating by hyperplastic, undiffe rentiated, and dys plastic epithelium arising
into the lumen. Mild mononuclear infl ammatory infiltrate is in the from basa l cells. Heterophil s and mononuclear inflammatory cells
lamina propria. Small amount of fibrin oheterophilic ex udate is 111 infiltrate the lamina propri a and submucosa .
the trac hea l lumen.

2 18 I American Associat ion of Av ian Pathologists

 RespirntolJ' System
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6.65. Trachea. Infectious laryngotracheitis. 54-day-old
broiler. There is loss of the mucosal epithelium. The lumen contains
exudate comprised of fibrin , sloughed epithelium, heterophils,
mononuclear inflammatory cells, and red blood cells. Syncytial
cells with intranuclear inclusion bodies may be found within the
luminal exudate.
6.67. Trachea. Infectious laryngotracheitis. Chicken. Layers
of regenerating, undifferentiated cells are replacing necrotic
epithelium . Large amount of fibrinoheterophilic exudate is still
present in the tracheal lumen. Syncytial cell with intranuclear
inclusion bodies is seen in the exudate.

6.66. Trachea. Infectious laryngotracheitis. 54-day-old 6.68. Trachea. Infectious laryngotracheitis. Chicken. Higher-
broiler. Syncytial cell with intranuclear inclusion bodies is among power view of the syncytial cell with intra nuclear inclusion bodies
the fibrinoheterophilic exudate in the tracheal lumen . It is common in the luminal exudate in 6.67 .
to find syncytial cells in the luminal exudate but not in the mucosa[
epithelium, especially when the mucosa! epithelium is severely
damaged .

Avian Histopathology (4 th Edition) I 219

 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
VetBooks.ir

.. . .
D
..' -· ...._.
6.69. Trachea . Infectious laryngotracheitis (repair stage). 6.71. Trachea. Adenovirus infection (quail bronchitis).
58-day-old broiler. The lining epithelium is comprised of several Higher-power view showing di sorgani zed mucosa, with basoph ilic
layers of regenerating, hyperpla stic, non-differentiated epithe lium inclusion bodies (box) of adenovirus fillin g the enlarged nuclei of

I
that has squamous appearance. Basal cells, and possibl y mucous few epithelial cells.
gland cells, are responsible for th e repair. These cells proliferate
and eventually differenti ate into normal mucosa! epithelium . Dense
monon uclea r cell infilt rate is still in the mucosa.

6.70. Trachea. Adenovirus infection (quail bronchitis). Quail. 6.72. Trachea. Aclenovirus infection (quail bronchitis). Quail.
Low-power view show ing large amount of fibrinoheterophilic Higher-power v iew of the luminal exudate showing two cells wit h
ex udate in the lumen of this trachea. enlarged nuclei filled with basophilic inclusions characteristic of
adenov irus infection .

220 I American Association of Av ian Path ologists


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6.73. Trachea. Aclenovirus infection (quail bronchitis).
36-clay-olcl quail. Three mucosa! epithelial cells contain enlarged
nuclei filled with basophilic inclusion bodies characteristic of
adenov irus infection.
6.74. Trachea. Aclenovirus infection. Turkey. Hyperplasia of
the mucosa! epithelium, loss of cilia, and the presence of vacuoles
containing eosinophilic debris. Some epithelial cells have enlarged
nu clei filled with deeply basophilic inclusion bodies typical of
adenovirus infection.
RespiratOIJ' System
6.75. Trachea. Fowl pox. Chicken. Hyperplasia of the mucosa!
epithelium and large, granular, eosinophilic intracytoplasmic
inclusion bodies are diagnostic of the diphtheritic form of fowl pox.
I
6.76. Trachea. Fowl pox. Chicken. Higher-power view of area
in 6.75 showing epithelial cells (box) containing intracytoplasmic
inclusions that are large, eosinophilic, and diagnostic for poxvirus
infection.
Avian Histopathology (4 th Edition) I 221
 Oscar J. Fletcher • Tahseen Abdul-A ziz
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6.77. Larynx. Diphtheritic pox. Backyard chicken. Low-
power view show ing squ amous hyperpl as ia of the mucosa !
epi thelium, w ith superfic ial mucosa! necros is and accumul atio n of
I
necroti c debri s o n the surface.
6.78. Larynx. Diphth eritic pox. Backyard chicken. Hi ghe r-
power view of area in 6.77 show ing marked squ amous hyperpl as ia of
the mucosa! epithelium , superfi cial mucosa ! necrosis, accumul ati on
of necroti c de bri s o n the surface, and marked infiltrati o n of
mononuclea r inflamm atory ce lls.
222 I A meri ca n Assoc iatio n of Av ian Patho logists
6.79. Larynx. Diphtheritic pox. Backyard chicken. Higher-
powe r view of area in 6. 78 demonstrating intracytoplasm ic inclusion
bodi es of poxviru s. T he inclusions are large, round , eos inophilic,
and usuall y have clea r or faintly stained centers. The hyperplastic
squamo us cells are large and have a bundant basophilic cytoplasm
and large nuclei with single prominent nuc leolus.
6.80. Trachea. Acute tracheitis. Bordetella avi11111 infection.
Turkey. Bacteria are closely assoc iated w ith the cilia . Adjacent
epithelial cells show loss of cilia. Vacuolated cells with eos inophi lic
debris are present in th e mucosa.

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6.81. Trachea. Chronic tracheitis. Bordetella avi11111 infection.
Turkey. Diffuse inflanunation and necrosis, with necrotic debris
in the trachea l lumen. Tracheal cartilage is necrotic and the
inflam mat io n ex tends into connective ti ss ue and muscle surrounding
the trachea.
6.8 2. Trachea. Chronic tracheitis. Bordetella avi11111 infection.
Turkey. Higher-power view of area in Figure 6.81 showing necrotic
debri s that contains many bacterial colonies. Necrotic cartilage is
in th e lower left area.
Respirato1:,1 System
6.83. Trachea. Mycoplasma galliseptic11111 infection. Chicken.
Tracheal mucosa is increased in thickness du e to diffuse lymphocytic
cell infiltration. Layer of mucu s that contains heterophils is on the
I
surface, and cilia are absent. Lesions were experimentally produced
with M. gallisepticwn.
6.84. Trachea. Mycoplasma galliseptic11111 infection.
8-month-old backyard chicken. Chronic tracheitis caused
by M. galliseptic11111 is characterized by marked thickening and
disruption of the mucosa by den se lymphoplasmacytic infiltrates in
which lymphocytes predominate. There is loss of cilia. This is a
characteristic but not diagnostic lesion of/11. gallisepticum infection.
Some hete rophil s and mucus are in the lumen. The trachea was
positive for M. galliseptic11111 by PCR.
Avian Histopathology (4'h Edition) I 223
 Oscar J. Fletcher • Tahseen Abdul-Aziz
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6.85. Trachea. My coplasma galliseptic11111 infection. 8-month-
old backyard chicken. Same section as 6.84. Higher-power
showing thi ckening and di srupti on of the mucosa by den se
I
lymphopl as macytic infil trates in whi ch lymph ocytes predominate.
The tra chea was positi ve fo r M. ga/liseptic11111 by PCR.
6.86. Trach ea. Mycoplasma galliseptic11111 infection. 6-month -
old backyard chicken. Chro ni c tracheiti s caused by M
ga//iseptic11111. The mucosa is markedl y thi ckened and di srupted
by dense lymphoplasmacyti c infi ltra tes . Cilia are absent. The re
is eviden ce of earl y regenerati ve proli ferat ion of epithelial
ce lls. Incli vi clual necroti c cells and fe w hetero phil s are present
in the mucosa near the surface. The trachea was posi tive for M.
ga//iseptic11111 by PCR .
224 I Ameri ca n Assoc iat ion of Av ian Path ologists
6.87. Trachea. Mycoplasma galliseptic11111 infection. 9-yea r-
old backyard chicken. Acute catarrhal tracheiti s characteri zed
by enl argement of mucous g lands, increased mucus secretion,
loss of mucosa! epithelium, mucosa! indi vidual cell necrosi s, and
early infiltrat ion of lymphocytes. The trachea was positive fo r M.
ga//iseptic11111 by PCR.
6.88. Trachea. Mycoplasma galliseptic11111 infection. 9-year-old
backyard chicken. Acute tracheitis characteri zed by swelling of
mucous gland cells, loss of the lining epi thelium, mucosa! indi vidua l
cell necrosis, and earl y infiltration of lymphocytes . The trachea was
positive fo r M. ga//iseptic11111 by PC R.

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6.89. Trachea. Aspergillosis. Turkey. Large numbers of fungal
hypb ae are mixed with fibrin and heterophils in the luminal exudate.
Hyperplastic, undifferentiated epithelial cells are replacing the
tracheal respirato1y epithelium.
6.90. Trachea. Aspergillosis. Turkey . Higher-power view
of area in 6.89 showing the squamous metaplasia of the tracheal
mucosa. This finding is not characteristic or diagnostic of any
disease but rather indicative of chronic tracheitis and regeneration
of the mucosa! epithelium.
Respirato1:i1 System
6.91. Trachea. Aspergillosis. Turkey. High-power view of the
luminal exudate showing fungal hyphae consistent with Aspergillus
sp .
I
6.92. Trachea. O:iptosporidiosis. Turkey. Hyperplasia of the
mucosa! epithelium is characteristic and the presence of small,
round, basophilic organisms (arrow and box) on the mucosa! surface
is diagnostic of C1J,ptosporidi11111 infection.
Avian Histopathology (4 th Edition) I 225
 Oscar J. Fletcher • Tahseen Abdul-Aziz
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6.93. Trachea. CJJ']Jtosporidiosis. Turkey. Higher-power view 6.95. Trachea. Respiratory mite (Stemostoma tracheacolum).
showing OJ1ptosporidiu111 organisms associated with the surface of Gouldian finch. In this area of the trachea, the mucosa! epithelium
hyperplastic epithelial cells (box). Heterophil s are scattered among is mildly hyperplastic and disorgani zed . Sections of arthropods

I
the epithe lial cells. (mites) are in the lumen, which also conta ins excess of mucus.

6.94. Trachea. Respiratory mite (Stemosto11u1 tracheacol11111). 6.96. Trachea. Respiratory mite (Stemostoma tracheacol11111).
Gouldian finch. Sections of arthropods (mites) are in the lumen Gouldian finch. Higher-power view showing sections of arthropods
of the trachea . The mucosa ! epithelium is di srupted , and there is (mites) associated with the surface of the severely di srupted mucosa.
excess of mucus.

226 I American Association of Avian Pathologists


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6.97. Trachea. Tracheal worm. Swan. Several sections of
nematodes in the tracheal lumen. This is Cy alhos/oma /rachealis .
6.98. Trachea. Tracheal worm. Swan. Higher-power view
of area in 6.97 showing section of nematode in the lumen. There
is tracheitis characterized by squamous hyperplasia of the lining
epithelium, with inflammatory infiltrates and necrotic eosinophilic
necrotic.
RespiratOJJ' System
6.99. Lung. Normal. Turkey. Respiratory lobules are composed
of air and blood capillaries that surround parabronchi (tertia1y
bronchi). Interstitial tissue contains larger blood vessels and is
I
relatively thin.
6.100. Lung. Normal. Turkey. Higher magnification of 6.99
showing the relationship between parabronchus (P), atrium (A), and
infundibulum (I). The arrow identifies smooth muscle in the wall of
the parabronchus. Note the air-blood capillary network, sometimes
referred to as the capillary bed.
Avian Histopathology (4 th Edition) I 227
 Oscar J. Fletcher • Tahseen Abdul-Aziz
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B
6.101. Lung. Normal. Turkey. The junction of secondary
bronchus (A) with parabronchus (B) is illustrated. Atria (C) connect
the air capillaries to parabronchi . The arrow points to lymphoid
I
aggregate that is part of the bronchial-associated lymphoid tissue
(BALT).
6.102. Lung. Normal. Turkey. Blood in parabronchi 1s not
indicative of disease because blood often enters the bronchi through
torn air sacs during necropsy. Smooth muscle just beneath the
parabronchial epithelium is visible . Simple squamous respiratory
epithelium lines the parabronchus, atria, and infi.mdibulae.
228 I American Association of Avian Pathologists
t I
••
,.
6.103. Lung. Normal. Turkey. Higher-power view showing the
simple squamous epithelium lining atrium and the smooth muscl e in
the wall of the parabronchus.
6.104. Lung. Cartilaginous nodule. Broiler. Cartilaginous
nodule is within respiratory lobule. The arrow identifies hya line
deposit characteristic of early stage in development of cartilaginous
nodule or it may be small nodule of bone (osteoid). Randomly
scattered cartilaginous nodules are considered normal findin gs in
the lungs of broilers.

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6.105. Lung. Pneumoconiosis. Backyard chicken. Dense
aggregates of dust particles, which appear as brown pigment, are in
the wall of secondary bronchus.
6,106. Lung. Dust granuloma (pneumoconiosis). Backyard
chicken. Nodul ar collection of histiocytes (histiocytic granuloma)
in th e wall of parabronchus effaces the atria and infundibulae. The
brown pigment in the granuloma is the inhaled dust particles that
incited the gra nuloma formation.
Respirato1J>System
6.107. Lung. Dust granuloma (pneumoconiosis). Backyard
chicken. Large, pigmented lesion in the wall of parabronchus is
effacing the atria, infundibulae, and probably the adjacent capillary
I
bed. The lesion consists of dense collections histiocytes and
inhaled dust particles, which appear as gra nular brown pigment. It
is difficult to discern the location of the dust particles, but they are
probably intracyto plasmic and extracellular.
6.108. Lung. Dust granuloma (pneumoconiosis). Backyard
chicken. Dense collection of histiocytes (histiocytic granuloma) is
just beneath the mucosa of secondary bronchus. Note the attenuation
of the lining epithelium and the segmental effacement of the muscle
in the bronchu s wall. Inhaled du st particles are present in the lesion.
Dust granulomas are mostly found in the wall ofparabronchi but are
occasionally seen around seco ndary bronchi .
Avian Histopathology w· Edition) I 229
 Oscar J. Fletcher • Tahseen Abdul-Aziz
VetBooks.ir

6.109. Lung. Dust granuloma (pneumoconiosis). Backyard 6.111. Lung. Mineral deposition. Turkey. Numerous basophilic
chicken. Higher-power view the dust granuloma in 6.108 deposits of mineral are in the interstitial tissue between lobules
demonstrating the large histiocytes and the intralesional dust and within the capillary beds. Note the absence of well-defined

I
material , which in this case appear as brown particles and retractile parabronchi and lobules. These lesions are consistent with area of
crystals. Most of the crystals are probably silicates. It is difficult collapse or atelectasis.
to discern the location of the dust particl e, but they are probably
intracytoplasmic and extracellu lar.

6.110. Lung. Dust granu loma (pneumoconiosis). Backyard 6.112. Lung. Mineral deposition. Turkey . Higher-power view
chicken. Dust granuloma viewed under polarized light. The of area in 6.111 showing the loss of para bronchial and capillary bed
intralesional crystals exhibit white birefringe nce. structure with accumulation of multiple and variably sized mineral
deposits.

230 I American Association of Avian Pathologists

 Re:.pirat01J1System
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6.11 3. Lung. Pulmonary calcinosis (mineralization). 9-month- 6.115. Lung. Pulmonary calcinosis (mineralization). 9-month-
old backya rd chicken. Disruption of the capillary bed and old backyard chicken. Von Kossa stain for calcium shows marked
thickening of the wall of the capillaries by deposits resembling and extensive mineral deposition in the capillary bed around a

I
min era l. Ca lcium deposition was also present in other organs and parabronchus.
tissues. T he cause was unknown in thi s case, but excess dietary
calcium and/or vitamin D and severe renal disease should be
considered as possibilities.

6.11 4. Lung. Pulmonary calcinosis (mineralization). 9-month- 6.116. Lung. Pulmonary calcinosis (mineralization). 9-month-
old backyard chicken. Higher-power view showing thickening of old backyard chicken. Higher-power view of area in 6.115 showing
the walls the capillaries by deposits resembling mineral. Note the the marked calcium deposition in the walls of capillary bed.
di sruption of the capillary bed

Avian Histopathology (4 th Edition) I 231

 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
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6.117. Lung. Pulmonary calcinosis (mineralization). 9-month-
old backyard chicken. Same lung as 6.11 3. Extensive linear
mineral deposits in th e lamina propria of secondaiy bronchus. In
I
one area, th e mineral deposits appea r damag ing the epithelium 's
basement membrane, res ulting in the detac hment of the epithelium.
6.118. Lung. Pulmonary calcinosis (mineralization). 9-month-
old backyard chicken. Higher power view of area in 6. 11 7 showing
th e linear minera l deposits in the lamina propria of secondary
bronchu s, the damage to th e epithelium 's basement memb ra ne, and
the loss of epi thelium .
232 I America n Associatio n of Av ian Patho logists
6.119. Lung. Fibrinous pneumonia. Inhalant toxicity. Qu aker
parakeet. Parabronchi are fill ed w ith eosinophilic material
presumed to be fibrin . Thi s Quake r developed respira tory signs
shortly a ft er be ing moved into new home. Lesions are ty pica l of
th ose ca used by inhaling toxic gases such as pol ytetrafluoroethylene.
Actua l ca use was not identified in thi s case.
6.120. Lung. Fibrinous pneumonia. Inhalant toxicity. Qu aker
parakeet. Higher-power vi ew of area in 6. 119 showing fibrin
w ithin the lumen of para bronchus. N ote the hypertrophy of the
respi ratory epithelia l cells.
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6.1 21. Lung. Fibrinous pneumonia. Inhalant toxicity. Quaker 6.123. Lung. Food aspiration. Parrot. The lumens ofparabronchi
parakeet. Same section as 6.119. Regional accumulation of are filled with plant material.
histiocytic cells likely originating from respiratory epithelial cells .
These changes are seen when birds survive for period following
exposure. In many cases, death is very acute and this proliferative
respo nse is not seen.

6.1 22. Lung. Fibrinous pneumonia. Inhalant toxicity. Quaker 6.124. Lung. Food aspiration. Parrot. Higher-power view of
pa rakeet. Higher-power view of area in 6.121 showing the area in 6.123 showing proteinaceous and plant material in the lumen
vacuolated histiocytic cells, many of which contain hyaline droplets of para bronchus .
of prote in indicative of active phagocytosis.

Avian Histopathology (4'11 Edition) I 233

 Oscar J. Fletcl,er • Tal,seen Abdul-A ziz
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6.125. Lung. Food aspiration. Parrot. Hi gher-power view of 6.127. Lung. Foreign-body granulomas. Turkey. Multiple areas
another area in 6.123 show ing gray, particul ate plant materi al and of caseous necrosis conta in brown pigment presumed to be dust.
pink prote inaceous materi al in the lumen of para bronchus.

6.126. Lung. Food aspiration. Parrot. The same fi eld in 6.1 28. Lung. Foreign-body granuloma. Turkey. Higher-
fi gure 6.1 25 viewed un de r polarized li ght. The plant materia l is power vi ew of area in 6. 127 show ing th e gra nulomatous response
birefringe nt. assoc iated with the presence of fo reign materi al.

234 I America n Assoc iati on o f Avi an Patho logists

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6.1 29. Lung. Endogenous lipid pneumonia. 26-year-old 6.131. Lung. Endogenous lipid pneumonia. 26-year-old
African gray parrot. Multiple regional collections of macrophages African gray parrot. Higher-power view of the boxed area in 6.130
with foa my cytoplasm. showing macrophages with foamy cytoplasm filling parabronchus

I
and adjacent capillary bed.

6.130. Lung. Endogenous lipid pneumonia. 26-year-old 6.132. Lung. Endogenous lipid pneumonia. 26-year-old
African gray parrot. Higher-power view of area in 6.129 showing African gray parrot. Higher-power view of area in 6.131.
the ma crophages with foamy cytoplasm filling parabronchi and
extending into the capillary beds in multiple lobules. The region
within the box is shown at higher magnification in 6. 131.

Avian Histopathology (4 th Edition) I 235

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 Oscar J. Fletcher • Tahseen Abdul-A ziz
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6.133. Lung. Normal and proliferative response. Turkey . 6.135. Lung. Proliferative response. Turkey. Hypertrophy
Illustrated are relatively normal area (P) and area of increased of smooth muscle and epithelial hyperpl as ia and metaplasia are
cellularity (box). Vari ati ons in shape of respi rato1y lobul es and in characteri stic features of pro li ferative responses. Blood in the

I
cellularity are comm on in lungs removed, fixe d in form a lin, and lumen o f the pa ra bronchu s is not lesion.
ro utinely processed.

6.134. Lun g. Proliferative response. 1\ll'key. Hi gher-power
view of the boxed area in 6. I 33 showing hypertrophy of smooth
muscle and increa sed cellulari ty around th e para bronchus due to
hyperplasia and metapl as ia (from simple squamous to cuboidal) of
epithelium lining the parabronchu s, atria, and in fundibul ae.
6.136. Lung. Proliferative response. Turkey. Hi gher-power
view of area in 6. 134 show ing hyperpl as ia and metaplasia of the
respi ratory epithelium lining the parabronchus

236 I Ameri ca n Assoc iati on of Av ian Pathologists

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6.1 37. Lung. Proliferative response. Turkey. Higher-power view 6.139. Lung. Atrial epithelium hyperplasia. One-year-old
of area in 6.135 showing hyperplasia and metaplasia of respiratory chicken. Hyperplasia and hypertrophy of the epithelium lining the
epithelium of parabronchus. Also shown are smooth para bronchial atria. Proliferating epithelial cells have abundant, foamy cytoplasm

I
muscle and infiltrating lymphohistiocytic cells. and are assumed to be phagocytic. Proteinaceous material is present.

6.138. Lung. Proliferative response. 9-day-old broiler. 6.140. Lung. Parbronchial epithelium hyperplasia. One-
Obliteration of atrial and infundibular spaces of parabronchus by year-old chicken. Higher-power view of area in 6.139 illustrates
prolife rating lining epithelium, with extension of the lesion to the proliferating epithelial cells with abundant, foamy cytoplasm.
adjacent capillary bed. The lesion in this lung section was multi focal
and its significance was uncertain . Not the smooth muscle of the
parabronchus.

Avian Histopathology (4 th Edition) f 237

 Oscar J. Fletcl,er • Tal, see11 Abdul-A ziz
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6.141. Lung. Infectious laryngotracheitis. Chicken. Large
syncytial cell with numerous nuclei and intranuclear inclusion
bodies is fo rmed from respi ratory epithelium lining parabro nchus.
I
Thi s is earl y stage of lesion development in the lung.
6.142. Lung. Infectious laryngotracheitis. Chicken. Hi gher-
power view of the epithelial syncytial cell with intranuclear
inclusion bodies in 6. 14 1. Note the variability in size and co lor
among the intra nuclear inclusions.
238 J American Assoc iation of Avian Pat hologists
6.143. Infectious laryngotracheitis. Chicken. Syncytial cell
with intra nuclear inclusion bodies is among the luminal exudate in
parabro nchus. Note the fibrin in the lower right area.
6.144. Lung. Infectious laryngotrach eitis. Chicken. Thi s low-
power view shows more di ffuse pattern with multiple les ions of
infectious laryngotracheiti s. Lesions include luminal exudate i11
para bronchi and marked interstitial expansion with edema, fib ri ll
and cellular exudate.
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6.145. Lung. Infectious laryngotracheitis. Chicken. Higher- 6.147. Lung. Adenovirus infection (quail bronchitis). Quail.
power view of area in 6.144 showing disruption of the lung Lesions include necrosis of bronchial epithelium, exudate in the
parenchyma with heterophilic and lymphohistiocytic exudate. Also bronchial lumen, and intranuclear inclusions.

I
prese nt are several syncytial cells.

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•

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6.146. Lung. Infectious laryngotracheitis. Chicken. Syncytial 6.148. Lung. Adenovirus infection (quail bronchitis). Quail.
cell with intranuclear inclusion bodies is among the exudate in the Higher-power view of area in 6.146 showing several cells (arrows)
lumen of parabronchus. with intranuclear inclusions.

Avian Histopathology (4 th Edition) I 239

 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
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6.149. Lung. Fibrinoheterophilic pneumonia. Turkey. Most 6.151. Lung. Pasteurella 11111/tocida infection. Turkey.
parabronchi are filled with fibrin mixed with some heterophils. This Parabronchus, atria, and infondibulae are expanded by the
is acute fibrinoheteroph ilic pneumonia. Lesions are not diagnostic accumulation of fibrin with necrotic cellular debris in the lumen.

I
but typical of acute bacterial pneumonias such as Ornithobacteri11111 Adjacent air capillaries are obliterated by the inflammatory and
rhinotracheale. However, the lesion in this case was caused by necroti zing lesions.
A1ycoplas111a synoviae, which was detected in this lung by PC R.

6.150. Lung. Fibrinoheterophilic pneumonia. Turkey. Higher- 6.152. Lung. Pasteurel/a 11111/tocida infection. Turkey. Hi gher-
power view of area in 6.149 showing fibrinoheterophilic exudate power view of area in 6.151 showing necrotic debris with bacterial
typical of acute bacterial pneumonias. colonies in the parabronchial lumen .

240 J American Association of Avian Pathologists

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6.1 53. Lung. Pasteurella 11111/tocida infection. Turkey. Higher- 6.155. Lung. E. coli pneumonia (colibacillosis). Turkey.
power view of area in 6.152 showing bacterial colonies among the Parabronchi are filled with fibrinoheterophilic exudate, and some
fibrin onecrotic exudate in the parabronchial lumen. parabronchi have necrotic debris filling the lumens. Interstitial

I
tissue is expanded by inflammatory exudate.

6.154. Lung. E.coli pneumonia (colibacillosis). Turkey. Diffuse, 6.156. Lung. E. coli pneumonia (colibacillosis). Turkey.
necroti zing and fibrinoheterophilic bronchopneumonia extends to Same section as 6.155. Shown is caseous debris surrounded by
the pleura. The fibrin and cellular components of the exudate in the multinucleated giant cells, with several bacterial colonies among
pleura result in significant expansion. the caseous material.

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6.157. Lung. E. coli 1rneumonia (colibacillosis). 30-day-old
broiler. Parabronchus shows ci rcumfe rential, severe destruction
of its wa ll , with cellul ar ex udate consisting of heterophil s and
I
mononuclear cells fillin g the lumen and extends to adjacent capillary
bed. Only some of para bro nchial smooth muscles are spared from
destruction.
6.158. Lung. E. coli pneumonia (colibacillosis). 29-clay-old
broiler. Within the lumen of a parabronchus is caseous necrotic
debri s rimmed by multi nucleated giant. Note the bacterial co lonies
in the caseous debris. There is destruction of the parabronchi al wa ll,
but bands of the wa ll smooth muscles are still present. Cul ture of
this lung yielded pure growth of E. coli.
242 I Ameri ca n Associati on of Av ian Pathologists
6.159. Lung. £. coli pneumonia (colibacillosis). 29-day-old
broiler. Same lung as 6. 158. Within the lumen of parabro nchus
is caseous necrotic debri s rimmed by multinucleated giant cell s.
Bacterial colonies are not seen in the exudate. Note the destruction
of the para bronchus wall and the loose ce llular infiltrate aroun d the
caseous debris. This les ion may be mistaken for fun ga l gra nuloma.
6.160. Lung. E. coli pneumonia (colibacillosis). 29-clay-
old broiler. Necrotizing and fibrin oheterophilic parabro nchitis
characteri zed by destruction of the para bronchi al wa ll and
accumulation of fibrin oheterophilic exudate in the parabronchial
lumen, atria, and infundibulae. The interlobul ar septa are edemato us
and infiltrated with heterophil s.

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6.1 61. Lung. E. coli pneumonia (colibacillosis). 29-day-old
broiler. Caseous debris with intralesional bacteria fills the lumen
of para bronchus.
6.1 62. Lung. E. coli pneumonia (colibacillosis). 28-day-old
broiler. Shown is one of several caseous granulomas involving
parabronchi. There is destruction of the wall of the parabronchus.
The caseo us debris is rimed by macrophages and multinucleated
giant cells. Several bacterial colonies are in the exudate.
Respirato1J' System
6.163. Lung. Omithobacteri11111 rhinotrac/1eale infection.
10-week-old turkey. Accumulation of fibrin mixed with many
heterophils in the lumen of parabronchus and in the atria and
infundibulae.
6.164. Lung. Omithobacteri11111 rhinotracheale infection.
10-week-old turkey. Expansion of the interlobular septa by
fibrinoheterophilic exudate, which is also present in the lumen of
para bronchus.
Avian Histo pathology (4'h Edition) I 243
 Oscar J. Fletcher • Tahsee11 A bdul-Aziz
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6.165. Lung. Omit/10bacteriu111 rhinotmcheale infection. 6.167. Lung. Omithobacteri11111 rhi11otrac/1eale infection.
10-week-old turkey. Accumulation of fibrin mixed w ith some 10-week-olcl turkey. The lumens of the air capillari es in thi s area
heterophil s in the lumen of parabronchus and around adj acent are fill ed and di stended w ith fibrin oheterophilic ex udate.

I
arteri ole.

6.166. Lung. Omithobacterium rhinotmcheale infection. 6.168. Lung. Omithobacterium rhinotmch eale infection.
IO-week-old turkey. Wide zone of proteinaceous fluid is around IO-week-old turkey. The lumens of the atria of a parabronchus
the wall of arteriole with edematous intima. The proteinaceous fluid are fill ed and markedly di stended with fibrin oheterophilic exudate.
is also seen in air capillaries on the left of the arteriol e.

244 I Ameri ca n Assoc iati on of Av ian Pathol ogists


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6.169. Lung. Pasteurellosis (fowl cholera). 17-week-old turkey.
Fibrinous exudate mixed with some heterophils fills and expands
the lumens of air spaces. The capillary bed is severely disrupted by
inflammatory exudate .
6.1 70. Lung. Pasteurellosis (fowl cholera). 17-week-old turkey.
Atri a are filled with exudate composed of fibrin and necrotic
inflammatory cells. The blue areas in the exudate are bacterial
coloni es
Respirato1J' System
6.171. Lung. Pasteurellosis (fowl cholera). 16-week-old turkey.
Dense fibrinoheterophilic exudate is destroying the wall and filling
the lumen ofparabronchus and its atria and infundibulae.
I
6.172. Lung. Pasteurellosis (fowl cholera). 16-week-old
turkey. The lumen and atria ofa parabronchus are filled with dense
fibrinoheterophilic exudate . Several bacterial colonies are seen in
the exudate. The wall of the parabronchus is effaced and only a
fragment of the parabronchial smooth muscles remains.
Avian Histopathology (4 th Edition) I 245
 Oscar J. Fletc!,er • Ta!,see11 Abdul-Aziz
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6.173. Lung. Septicemia caused by Streptococcus gallolyticus 6.175. Lung. Mycobacteriosis. Finch. Nodular mass composed
subsp. pasteuria11us (formerly Streptococcus b011is). 10-day-old of large macrophages (epithelioid cells / histiocytes) having finely
commercial turkey. Pulmonary capillaries are filled with dense granular, basophilic cytoplasm is located in the capillary bed of this

I
clusters of bacteria, which appear as aggregates of baso philic lobule . Note the absence of necrosis. Note also the finely granular
materi al in the capillary bed. dark particles of inhaled dust just beneath the lumen ofparabronchi.

6.174. Lung. Septicemia caused by Streptococcus gallo()'ticus 6.176. Lung. Mycobacteriosis. Finch. Higher-power view of the
subsp. pasteuria11us (formerly Streptococcus bol'is). 10-day- tumor-like mass of histiocytes in the capillary bed. Dust particles
old commercial turkey. Same lung as 6.173. Gram stain shows are seen in the upper left and lower right areas.
Gram-positive bacteria filling the lumens of blood capillaries. Also,
note the clusters of bacteria in the lumen of small blood vessel in
interlobular spaces.

246 I American Association of Avian Pathologists


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6.1 77. L ung. Mycobacteriosis. Finch. Acid-fast stain shows
large numbers of acid-fast positive bacteria within histiocytes.
6.1 78. Lung. Mycobacteriosis. Adult lady gouldian finch.
Effacin g the capillary bed is sheet of macrophages with basophilic,
fin ely granular cytoplasm.
Respimto1:v System
6.179. Lung. Mycobacteriosis. Adult lady gouldian finch. Same
section as 6.178. Higher-power view demonstrating macrophages
with cytoplasm distended with basophilic, finely granular materia l,
which was found to be acid-fast bacilli morphologically resembling
Mycobacteri11111 spp.
6.180. Lung. Nocardiosis caused by Nocardia sp. Sparrow.
Caseous granuloma consists of caseous debris surrounded by zone
granulomatous reaction. Filamentous, faintly stained organisms
morphologically consistent with Nocardia sp. are among the
caseous debris. The lesion was multifocal.
Avian Histopathology (4 th Edition) I 247
 Oscar J. Fletcher • Tal,see11 Abdul-Aziz
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6.181. Lung. Nocardiosis caused by Nocardia sp. Sparrow. 6.183. Lung. Nocardiosis caused by Nocardia sp. Sparrow.
Lung section stained with Gram stain. No cardia appears as Gram- No cardia stains positive (black) with Gomori methenamine silver
positive, branching, filamentous organisms that have beaded (GMS) stain.

I
appearance. Nocardia is classically Gram-variable.

6.182. Lung. Nocardiosis caused by Nocardia sp. Sparrow.
Lung section stained with Fite stain (modified-acid-fast stain).
Nocardia appears as acid-fast branching, fi lamentous organisms.
Nocardia is typically modified-acid-fast-variable. The modified-
acid-fast-positive character of Nocardia sp. helps to differentiate it
from A cti110111yces sp ., which is modified-acid-fast-negative.
6.184. Lung. Pneumonia. Mycoplasma sy1101,iae infection.
Turkey. Lymphofollicular reaction characterized by multiple,
variably sized nodular infiltrates oflymphocytes is highly suggestive
of Mycop/asma infection.

248 I American Association of Avian Pathologists

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6.185. L ung. Mycotic bronchopneumonia. Aspergillosis. 6.187. Lung. Aspergillosis caused by Aspergil!us fi1111igat11s.
Turkey. Scanning view of lung within the thoracic cavity showing 3-week-old broiler breeder pullet. Low-power view showing
the peripheral distribution within the lung of granulomas caused by multifocal, well-delineated caseous granulomas, each with large
Aspe1gil/11s sp. center of caseous debris.

6.1 86. Lung. Mycotic bronchopneumonia. Aspergillosis.
Tu rkey. Higher-power view of area in 6.185 showing several
granulomas in various stages of organization located in the periphery
of th e lung adjacent to ribs. Granuloma with caseous necrosis (A)
and another (B) with more giant cells are identified .
6.188. Lung. Aspergillosis caused by Aspergil!us fi1111igat11s.
6-day-old broiler. This magnification shows a well-circumscribed
mycotic granuloma consisting of caseous center surrounded by
granulomatous reaction.

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 Oscar J. Fletcher • Tah seen Abdul-Aziz
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6.189. Lung. Aspergillosis caused by Aspergillus ji1111igat11s.
6-day-old broiler. Higher-power view of the caseous gran uloma
in 6.188. Central area of caseous debri s is ringed by multinucleated
I
giant ce ll s and surrounded by a zone of macrophages and other
mononuclear inflammatory cel ls. Faintly stained fungal hyphae are
seen in the caseous debris.
6.190. Lung. Mycotic pneumonia. Aspergillosis. Turkey. PAS
stain revea ls many hyphae typical of Aspe1gil/11s sp . (A). Sometimes
fruiting bodies can be seen if oxygen levels are appro priate (8).
250 I American Associati on of Avian Pathologists
6.191. Lung. Granulomatous mycotic pneumonia cau sed
by Aspergillus jfm//lS , 6-week-old broiler breeder pullet.
Gran ulomatous les ion consists of co llecti on of large multinucleated
giant cell s and mi xed inflammatory infiltrate that includes
gran ulocytic leukocytes. Some of the multinucleated cell s are of
bi za rre shapes.
6.192. Lung. Granulomatous mycotic pneumonia caused by
Asp erg illus jfavus. 6-week-old broiler breeder pullet. Another
gra nulomatous lesion consists of multinucleated giant cells and
mixed inflammatory infiltrate, with foca l area of early caseation
surrou nded by multinucleated cells.

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6.193. Lung. Granulomatous mycotic pneumonia caused
by Asp ergilfus jfavus. 6-week-old broiler breeder pullet.
Granulomatous lesion consists of bizarre mul tinucleated giant cells
and infl ammatory infi ltrates of mostly macrophages.
6. 194. Lung. Granulomatous mycotic pneumonia caused
by Asp ergilfus jfavus. 6-week-old broiler breeder pullet.
Caseogranulomatous lesion consists of foc i of caseous debris,
bi za rre-m ultinucleated giant cells, and inflammatory infiltrates of
mostl y macrophages.
Respirato1J' System
6.195. Lung. Granulomatous mycotic pneumonia caused by
6-week-old broiler breeder pullet. Fungal
Asperg illus jfavus.
hypha within large, bizarre mul tinucleated giant cel l. Fungal
elements are not always easy to find in these lesions, especially with
H&E stain .
6.196. Lung. Granulomatous mycotic pneumonia caused by
Aspergillusjfal'ltS. 5-week-old broiler breeder pullet. Thi s PAS-
sta ined section shows fungal hyphae, some of which are within
multinucleatecl giant cells.
Avian Histopathology (4 1h Edition) I 251
 Oscar J. Fletcher • Tahseen Abdul-Aziz
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6.197. Lung. Sarcocystosis. 3-year-old eclectus parrot. 6.199. Lung. Sarcocystosis. 12-year-old cockatoo. Interstiti al
Fibrinous exudate is in the lumen of parabronchi. pneumonia characterized by thickening of the capillary-bed
walls by infiltrates of mononuclear inflammatory cells. Note the

I
proteinaceous material in the lumens of air capillaries.

6.198. Lung. Sarcocystosis. 2.5-year old eclectus parrot. The
capillary bed is disrupted by exudate of proteinaceous material
resembling fibrin. There is mild infiltration of mononuclear
inflammatory cells.
6.200. Lung. Sarcocystosis. Pigeon. Meronts (arrows) of
Sarcocystis are located within blood capillaries. These mero nts
usually follow the shape of capillary and appear as elongated or
to1tuous basophilic structures containing granules, the merozo ites.
Clusters of tiny merozoites are occasionally found in the lumens of
blood capillaries.

252 I American Association of Avian Pathologists

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6.201. Lung. Leucocytozoonosis. 10-month-old turkey. See the 6.203. Lung. Toxoplasmosis. Chicken. Characteristic are the
legend of 6.202. large zones of necrosis within which are cysts containing Toxop/asma
bradyzoites. Postmortem autolytic changes are common and make

I
finding organisms difficult.

6.202. Lu ng. Leucocytozoonosis. 10-month-old turkey. This 6.204. Lung. Toxoplasmosis. Chicken. Higher-power view
legend is also applied to 6.201. Within the lumen of blood capillary showing the characteristic Toxop/asma cyst (box) with bradyzoites.
is a blood cell containing a gamont of Leucocytozoon sp. (arrows) .
Note the dark band formed by the cell on each side of the parasite.

Avian Histopathology (4 th Edition) I 253

 Oscar J. Fletcl,er • Tal,see11 Abdul-Aziz
VetBooks.ir

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6.205. Lung. Respiratory mite (Stemostoma tracl,eaco/11111). 6.207. Lung. Respiratory mite (Stemostoma tracl,eaco/11111).
Gouldian finch. Sections of mites are within the lumen of secondary Gouldian finch. Mite is surrounded by gra nulomatous reaction
bronchus. There is segmental destruction of the bronchus by intense consisting of macrophages and few mul tinucleated giant cells. The

I
inflammatory reaction composed of mononuclear inflammatory mite is likely within the lumen of parabronc hus, the wall of which is
cells and some multinucleated giant cell s. effaced by the gra nul omatous reaction .

6.206. Lung. Respiratory mite (Stemostoma tracl,eacol11111).
G ouldian finch. Severa l sections of mites are surrounded
by gra nulornatous reaction consisting of macrophages, other
mononuclear inflammatory ce ll s, and few multinucleated giant cells.
Remnants of the bronchial smooth muscles can still be identified in
the lesion.
6.208. Lung. Respiratory mite (Stemostoma tracl1eacol11111).
Gouldian finch . Mite-occupying space is surrounded by zo ne
of intense gran ulomatous reaction consisting of predominantly
macrophages with several large multinucleated giant cells. The
space most likely is the lumen ofparabronc hus, the wall of which is
effaced by the gran ul omatous reaction.

254 I Ameri can Associatio n of Avian Pathologists

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6.209. Lung. Respiratory mite (Cytodites 1111d11s)). 10-month- 6.211. Lung. Respiratory mite (Cytodites 111u/11s)). 10-month-
old backyard chicken. Mite is within the lumen ofparabronchus. old backyard chicken. Mite is in the lumen of parabronchus . The
luminal surface of the parabronchus is disrupted by desquamation of

I
pneumocytes and mild infiltration of inflammatory cells.

6.210. Lung. Respiratory mite (Cytodites 111ulm)). 10-month-
old backyard chicken. Three mites are within the lumen of
parabronchus, which has mild, segmental inflammatory reaction in
its wall.
6.212. Lung. Respiratory mite (Cytodites 111u/11s)). 10-month-
old backyard chicken. Mite is within the lumen of parabronchus.
The wall of the parabronchus is focally effaced by granulomatous
lesion consisting of epithelioid macrophages and multinucleated
giant cells.

Avian Histopathology ( 4,1, Edition) I 255

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6.213. Lung. Primary adenocarcinoma. Pigeon . This tumor 6.215. Lung. Marek's disease. Chicken. Neoplastic lymphocytes
originates from the epithelium ofparabronchi and atria and replaces have infiltrated capillaty beds of numerous lobules and are causing
the capillary bed. expansion of interstitial tissue.

6.214. Lung. Primary adenocarcinoma. Pigeon. Higher-power 6.216. Lung. Marek's disease. Chicken. Higher-power vi ew of
view showing transition from normal atrial epithelium to neoplastic area in 6.215 showing replacement of capillary beds and expansion
cells. of interstitial tissue by neoplastic lymphocytes.

256 I American Association of Avian Pathologists

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6.217. Lung. Marek's disease. Chicken. Higher-power view of 6.219. Lung. Marek's disease. 5-month-old backyard chicken.
area in 6.216 showing the neoplastic lymphocytes filling capillary The wall of parabronchus and the surrounding parenchyma is
bed of lobule. The pink material is fibrin within the lumen of densely infiltrated by sheet of pleomorphic lymphoid cells. Several

I
para bronchus . mitotic figures can be seen in the infiltrate .

.• .
.>:•.

6.218. Lung. Marek's disease. Chicken . Higher-power view of 6.220. Lung. Metastatic squamous cell carcinoma. Chicken.
area in 6.217 showing complete replacement of the capillary bed by This nodule located just beneath the respiratory epithelium of
neoplastic, pleomorphic lymphocytes. The pink material is fibrin. parabronchus is metastatic squamous cell carcinoma. The neoplasm
Note the smooth muscles in the parabronchus wall. originated in the esophagus .

Avian Histopathology (4 th Edition) I 257

 Oscar J. Fletcher • Tahsee11 Abdul-A ziz
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6.221. Lung. Metastatic squamous cell carcinoma. Chicken. 6.223. Lung. Metastatic ovarian carcinoma. 5-year-old
Hig her-power vi ew o f the tumor nodul e in 6.220. The nodule is backyard chicken. Shown is o ne of severa l areas of metastatic
located beneath the parabronchi al lumen and replacing the capillary aden oca rcinoma in the lung . T he bird had ova ri an adenocarc inoma

I
bed. Note th e absence of response in the adj acent lung ti ss ue. with extensive intracoelomic metastas is.

6.222. Lung. Metastatic squamous cell carcinoma. Chicken. 6.224. Lung. Metastatic ovarian carcinoma. 5-year-old
Hi g her-powe r view of area in 6.22 l show ing multipl e nests of backyard chicken. Higher-power view of area in the ca rcinomato us
neoplasti c squamou s epithelial cell s. les io n in 6.223.

258 I Ameri ca n Assoc iati o n of Avia n Patho logists

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6.225. Lung. Melanoma. Chicken. Multiple collections of cells 6.227. Lung. Melanoma. Chicken. Higher-power view of the
with black pigment are in several lobules. melanoma in 6.226 showing neoplastic melanocytes replacing the
capillary bed.

6.226. Lung. Melanoma. Chicken. Higher-power view 6.228. Air Sac. Normal. Chicken. Air sacs are thin-walled
of melanoma in 6.225 showing the pigment-containing cells and lined by simple squamous epithelium with patches of ciliated
(melanocytes) filling capillary bed. Note the absence of well- epithelium (box). This is section of air sac adjacent to the kidney
defined margins. and ureter.

Avian Histopathology (4 th Edition) I 259

 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
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6.229. Air Sac. Normal. Chicken . Higher-power view of air sac 6.231. Air Sac. Infectiou s laryngotracheitis. Chicken. Hi gher-
in 6.228 show ing the thin walled air sac lined by simple squam ous power view of area in 6.23 0 showing hyperplasti c epithelium
epithelium. The lumen is identified (L). Region with ci li ated containing several multinucleated syncyti al cells with intranuclear

I
epithelium is see n. inclusion bodies cha racteristi c of herpesviru s infectio n.

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6.230. Air Sac. Infectious laryngotracheitis. Chicken. The 6.232. Air Sac. Infectious laryn gotracheitis. Chicken. Hi gher-
air sac epithelium is hyperplastic, and the lumen contains cellular power v iew of area in 6.231 showing syncytial cells (boxes) with
ex ud ate. The wall is increased in thickness in this affected region. intranuclea r inclusion bodies.

260 I A meri ca n Association of Av ian Pathologists

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6.233. Air Sac. Aclenovirus infection (quail bronchitis). Quail. 6.235. Air Sac. Aclenovirus infection (quail bronchitis). Quail.
Thi s air sac contains necrotic debris (box) in the lumen. Areas of Higher magnification of 6.233 showing necrotic debris within the
epithelial hyperplasia and increased thiclrness of the wall are seen. lumen. Inclusion bodies can be difficult to find , but the presence of
necrotic cells and debris are consistent with quail bronchitis.

6.234. Air Sac. Aclenovirus infection (quail bronchitis). Quail. 6.236. Air Sac. Aclenovirus infection (quail bronchitis). Quail
Higher-power view of the boxed area in 6.233 showing cells with Among the luminal necrotic debris are several cells (boxes) with
intra nu clear inclusion bodies (box) in the luminal necrotic debris. diagnostic intranuclear inclusion bodies.

Avian Histopathology (4 th Edition) J 261

 Oscar J. Fletcher • Tahseen Abdul-Aziz
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6.237. Air sac. Infectious bronchitis. 35-day-old broiler. 6.239. Air sac. Infectious bronchitis. 35-clay-olcl broiler. Same
Expansio n of the air sac wa ll by edema and heterophili c infiltrate . case as 6.237 . The lining e pithelial cells appear hypertrophi c, and
The bird had tracheitis, and infectious bronchitis virus was detected th e wall is thickened and infi ltrated by man y heterophil s.

I
in the trachea by PCR.

6.238. Air sac. Infectious bronchitis. 35-clay-olcl broiler. 6.240. Air Sac. Infectious bronchitis. Ch icke n.
Hi g her-power vi ew of area in 6.237. Fibrino heterophili c ex udate in the lumen with scattered lymphocytes
and foca l nodul ar collecti on of lymphocytes. The air sac wal l is
increased in thickness. Les ions are not di agnosti c, but th is chi cken
was positive by PCR fo r infectious bronchitis virus.

262 I Ameri ca n Assoc iati on of Av ian Patho logists

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6.241. Air Sac. Infectiou s bronchitis. Chicken. Higher-power 6.243. Air Sac. Infectiou s bronchitis. Chicken. Higher-power
view of area in 6.240 showing the luminal exudate and single view of another area in 6.241 showing the fo ca l nodular collection
nodu lar co llection of lymphocytes. of lymphocytes in the air sac wall. Some plasma ce lls are present.

6. 242. Air Sac. Infectious bronchitis. Chicken. Higher-
power view of area in 6.241 showing luminal exudate with mi xed
heterophilic and hi stiocyti c cell population. Hyperplasia of air sac
epithelium is present. The pink materi al is likely collagen, but could
he fib rin .
6.244. Air Sac. Airsacculitis caused by E. coli. Chicken.
Extensi ve region of necrosis is associated with increased thickness
of the air sac due to inflammation and accumulation of exudate.

Avian Hi stopathology (4th Editi on) I 263

 Oscar J. Fletcher • Tal,see11 Abdul-A ziz
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6.245. Air Sac. Airsacculitis caused by£. coli. Chicken. Higher- 6.247. Air Sac. Airsacculitis caused by £. coli. 39-day-old
power view of area in 6.244 showing the junction between the chicken. Airsacculitis characteri zed by edema, marked heterophil
region of caseogranul omato us inflammati on and air sac epithelium . infiltrati on, and dil ati on and congesti on of blood vessels.

6.246. Air Sac. Airsacculitis caused by £. coli. 39-clay-old 6.248. Air Sac. Airs acculitis caused by £. coli. 39-d ay-old
chicken. The wall of air sac is hyperemi c and thi ckened by edema chicken. Large amount of fibrinoh eterophilic exudate in air sac
and mild hetero phil ic infiltrates. with thickened wa ll.

264 I Ameri ca n Associati on of Av ian Path ologists


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6.249. Air Sac. Airsacculitis caused by E. coli. 39-day-
old chicken. Higher-power view of area in 6.248 showing
fibrin oheterophilic exudate mixed with macrophages in the lumen
of air sac. The wall of the air sac is thickened by inflammatory
infilt ra tes and fibrin , with hypertrophy of the lining epithelium.
6.250. Air Sac. Airsacculitis caused by E. coli. 5-week-old
turkey. Expansions of the air sac wall by heterophilic infiltrate.
Respimto,J' System
6.251. Air Sac. Airsacculitis caused by E. coli. 5-week-old
turkey. Area of necrosis and caseation of the heterophils in the
wall air sac.
6.252. Air Sac. Airsacculitis caused by E. coli. 5-week-
old turkey. Area of marked expansion of the air sac wall by
fibrinoheterophilic exudate, with loss of the lining epithelium.
Avian Histopathology (4 th Edition) I 265
 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
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6.253. Air Sac. Airsacculitis. Mycoplasma sy11oviae 6.255. Air Sac. Airsacculitis. Mycoplasma sy1101 1iae infection.
(experimental infection). Chicken. Air sac is increased in Chicken. Higher-power view of area in 6.254 showing hyperp las ia
thi ckness due to hyperplasia of epithelial cell s, exudation of fibrin , of the lining epithelium and marked thicken ing of the wall by edema

I
and infiltration of heterophils, lymphocytes, plasma cell s, and fluid and fibr in. Lymphoid nodules are prominent.
macrophages . Four days post-infect ion .

6.254. Air Sac. Airsacculitis. Mycoplasma sy11m,iae infection. 6. 256. Air sac. As pergillosis. Owl. Caseous nodule containi ng
Chicken. Higher-power view of area in 6.253 showing marked fungal hyphae (not seen at this mag nificat ion) is in the wall of air
thickening of the air sac wa ll by fibrinobeterophilic and lymphocytic sac.
exudate with fibroplasia. Exudate is also present on the surface and
in the lumen of the air sac. The lining epithelial cel ls are hyperplastic.
Numerous lymphoid nodules (lymphofollicular reaction) are present
in the connective tissue of the expanded air sac wa ll.

266 I American Association of Avian Pathologi sts

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6.257. A ir sac. Respiratory mite (Ste/"llostoma trac/1eacolu111). 6.259. Air sac. Respiratory mite (Stel"llostoma tracheaco/11m).
Go uldian finch . This is the wall of the air sac on the inner surface Gouldian finch. Higher power-view of area in 6.257 showing the
of the keel bone . The wall of the sac is markedly thickened mite and the brownish granular mite excreta just beneath the keel

I
by mononuclear inflammatory infiltrate and what looks like bone.
proteinaceous material. Few multinucleated giant cells are also
prese nt in some areas. The dark material is mite excreta. Section of
mite is within the wall.

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6.258. Air sac. Respiratory mite (Stel"llostoma tracheaco/11111).
Go ulcl ian finch. This is the wall of the air sac on the inner surface of
the kee l bone . There is thick layer of fibrin-like material containing
some necrotic debris. On each side of this material , inflammatory
infiltrates consisting of lymphocytes, plasma cells, and macrophages
are seen. The dark material just under the keel bone is mite excreta.
Earl y fibroplasia is evident on the left side.
'
6.260. Air sac. Respiratory mite (Stel"llostoma tracheaco/11m).
Gouldian finch. Higher-power view demonstrating the appearance
of mite excreta in the wall of air sacs. The inflammatory infiltrate
consists mostly of lymphocytes and plasma cells. Note the
proteinaceous material in the wall.

Avian Histopathology (4 th Edition) I 267

 Oscar J. Fletcher • Tahsee,, Abdul-Aziz
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-nr
6.261. Air sac. Respiratory nematodiasis (Cyathostoma sp.).
Broad-winged hawk. Area of seve re airsacculitis with many
intralesional nematode eggs, some o f which are surrounded by
I
multinucleated giant ce lls . This is likely Cyathostoma a111erica1111111 .
6.262. Air sac. Respiratory nematodiasis (Cyathostoma sp.).
Broad-winged hawk. Large collection of nematode eggs in air
sac, which also contain some eosinophilic debris. Thi s likely is
Cyathosto111a a111ericam1111.
268 I Ameri ca n Associati on of Av ian Patholog ists
6.263. Air sac. Carcinoma. 4-year-old budgeriga r.
Carcinom atous lesion originating fro m air sac is on th e sur face of
the kidney.
6.264. Air sac. Carcinoma. 4-year-old budgerigar. Higher-
power v iew of th e carci nomatous lesion in 6.263. Tumor is
co mposed of tubulopapill ary structure s and is on the peri toneal
surface of the kidney. The cell s formin g the tubulopapillary
structures are cuboidal and have abundant eosinophilic cytoplasm
and large, nuclei wi th prominent nucleoli . Nu clea r atypi a and
aniso karyos is are prominent, and there are several mitoti c fi gures.
Rudimentary cilia are occasionall y seen on the surface of neo plastic
epithelial cells.
 RespiratoJJ' System
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6.265. Air sac. Cystic neoplasm. 13-year-old budgerigar. Low- 6.267. Air sac. Cystic neoplasm. 13-year-old budgerigar.
power view shows fluid-filled cystic spaces and area of dense tissue. Higher-power view showing well-differentiated, low-cuboidal ,
ciliated epithelium lining the wall of cyst.

6.266. Air sac. Cystic neoplasm. 13-year-old budgerigar. 6.268. Air sac. Cystic neoplasm. 13-year-old budgerigar.
Higher-power view showing cystic spaces filled with eosinophilic Noncystic area in the neoplasm consists of markedly thickened air
proteinaceous fluid and lined by low-cuboidal , ciliated ep ithelia l sac lined by flat to low-cuboidal epi thelial cells.
cells covering a wall of fibrous tissue stroma.

Avian Histopathology (4 th Edition) I 269

VetBooks.ir

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VetBooks.ir
CHAPTER
Alimentary System
Oscar J. Fletcher • Tahseen Abdul-Aziz
Beak
The beak or bill has an essential role comparable to the lips and teeth
of mammals in the initial process of feeding. It is also the principle
organ of manipulation functioning much like a hand. Beak lesions
are usually evaluated by gross observation and histopathology is
not done. The stratified squamous epidermal layer of the beak is
covered by a thick, hard, cornified layer (stra/11111 come11111). The
dermi s of the beak is relatively thin and contains prominent sensory
organs, Herbst corpuscles. The inner core of the beak is bone. Beak
lesions in young chickens and turkeys in commercial flocks usu-
ally results from improper beak trimming. Improper beak trimming
results in necrosis and inflammation with heterophils, lymphocytes,
and macrophages expanding the dermis. Dermal fibrosis may be
extensive. Necrotic debris containing bacteria often replaces the
beak while maintaining beak outlines. Necrotic and inflammatory
lesions in severe cases may extend into the oral and nasal cavities.
Beak necrosis in older birds is associated with impaction of fine
feed in palatine ridges and salivary gland ducts in the oral mucosa in
whi ch bacteria or fungi proliferate. Feed impaction also contributes
to osteomyelitis of bones at the commissure of the mouth. Erosions
or ul cers on the upper beak between the nares are associated with
tryptophan deficiency.
Oral Cavity, Esophagus, Crop, and
Proventriculus
Interpretation of the significance of lymphocytes in the upper diges-
tive tract, especially the lamina propria of the proventriculus, is dif-
ficult because a significant population of lymphoid cells is normal.
Autolytic changes that result in dilation ofproventricular glands and
epithelial changes occur rapidly in the proventriculus and need to be
differentiated from antemortem lesions.
Toxicities and Deficiencies
Chemicals (quaternary ammonium compounds, copper sulfate, ac-
ids and bases, disinfectants), trichothecene mycotoxins, and plant
toxins produce erosions and ulcers in the oral cavity. Feeding fine
mash feed may cause focal necrosis with fibrin , necrotic cells, and
debri s on the epithelial surface of the oral cavity, but these lesions
generally are not as severe as those caused by toxic injury. Edema in
the lamina propria , distention of mucous glands, and fluid accumula-
7
tion in the lumen of the proventriculus can be caused by ochratoxin,
biogenic amines - especially gi zzerosine, trichothecene mycotoxins,
and cyclopiazonic acid. Excess water consumption following ape-
riod of water deprivation may lead to acute hemorrhage and necrosis
in multiple glands . Edema and hemorrhage in the proventricular
mucosa and/or glands are associated with rubratoxicosis, vitamin
K deficiency, copper sulfate toxicity, and anticoagulant rodenti-
cicles. Squamous metaplasia of mucous glands and their ducts in the
esophagus is characteristic of vitamin A deficiency. Affected glands
become distended, cystic, and filled with keratin debris. Squamous
metaplasia in mucous glands of the upper alimentary system of un-
known etiology also has been observed in broiler breeders having
no evidence of vitamin A deficiency. If glands rupture, release of
keratin stimulates an intense inflammatory response in surrounding
connective tissues .
Infections
Vim! infections
Viruses cause a spectrum of lesions including ballooning degen-
eration, erosions, and ulceration with accompanying inflammatory
cellular infiltrates. Hemorrhage frequently accompanies epithelial
lesions and may be the primary lesion observed. Hemorrhage clue
to viral infection must be differentiated from that caused by toxic
or caustic injury or systemic bacterial infection. Hemorrhages, es-
pecially in areas of lymphoid tissue, can result from viral diseases
including exotic Newcastle Disease, highly pathogenic avian influ-
enza, and duck viral enteritis. Systemic bacterial infections (e.g.,
pasteurellosis) may cause similar lesions. Herpesvirus infection of
ducks (duck viral enteritis), pigeons, and owls is characterized by
necrosis, hemorrhage, ulceration of the esophageal mucosa, inflam-
mation, and intranuclear inclusion bodies in epithelial cells. Muco-
sa! necrosis and ulceration occur rarely in the esophagus of chick-
ens infected with infectious laryngotracheitis virus. Hyperplasia,
ballooning degeneration, and large, eosinophilic intracytoplasmic
inclusions characterize pox virus infections in the upper digestive
tract. Ulceration of the surface of pox lesions provides a suitable en-
vironment for proliferation of bacteria and fungi. Rarely, inclusions
of psittacine beak and feather disease can be found in esophageal
mucosa I epithelium, but lymphoplasmacytic inflammation of auto-
nomic ganglia in the esophagus and crop is more common.
Necrosis of proventricular glandular epithelium, lymphocytic
infiltration, and ductal epithelial hyperplasia that replaces lost glan-
dul ar epithelium are characteristic features of transmissible viral
Avian Histopathology (4' 11 Edition) I 271
 Oscar J. Fletcher • Tahseen Abdul-Aziz
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proventriculitis in broilers and broiler breeders. Focal necrosis in
the proventricular mucosa, edema in the lamina propria, dilation of
proventricular glands, mild to moderate ductal hyperplasia without
lymphoid cell infiltration, variable degrees ofsubductal fibrosis, and
inflammation of the serosa of the proventriculus are lesions in broil-
ers and broiler breeders that are not associated with a specific cause.
Rarely, usually involving single birds in multi-bird submissions,
extensive fibrosis around glands is seen. Fibrous bands may leave
isolated islands of glandular tissue surrounded by fibrous connec-
tive tissue. Ductal hyperplasia is usually significant in these cases
of chronic fibrosing proventriculitis. Gross changes in the proven-
triculus often are not linked to histologic lesions.
Lymphocytic proventriculitis involving the lamina propria,
glands, and interstitial tissues, and autonomic ganglioneuritis or
neuritis of visceral nerves on the serosal surface of the proven-
triculus are characteristic lesions of Marek's disease. Lesions in
glands may be extensive and result in mucosa! ulceration. Reticu-
loendotheliosis virus infections in turkeys is associated with lym-
phocytic proventriculitis .
Bacterial infections
Extensive necrosis of the proventricular mucosa with the presence
of a mixed population of Gram-positive and Gram-negative bacteria
is seen in Clostridium perfi-ingens and Escherichia coli infections.
Vasculitis and thrombosis of vessels with necrosis of the proventricu-
lar mucosa occurs in erysipelas. Systemic infection with virulent
Pasteurella 11111/tocida can result in proventricular necrosis and hem-
orrhage similar to that occurring in highly virulent viral infections .
lntralesional bacteria are numerous but do not form distinct colonies.
Infection of finches and other passerine birds with Sa/111011ella ty-
phi11111ri11111 causes multifocal to coalescing necrosis and fibrinohet-
erophilic inflammation esophagitis and ingluvitis. Mixed mononu-
clear cells and heterophils, fibrin , and intralesional bacterial colonies
are associated with areas of necrosis in the esophagus and crop.
Fungal infections
Epithelial hyperplasia with accumulation oflarge amounts of keratin
on the epithelial surface is typical of mycotic infections that mostly
occur in the crop, but can also involve the oral cavity and the esoph-
agus. Pseudohyphae and blastospores of yeast (Candida spp.) are
present in the keratin debris and are readily demonstrated by fungal
stains. Typically, the organisms are perpendicular to the mucosa!
surface and either barely penetrate the viable stratum ger111i11ativ11111
or remain confined to the keratin layer. Yeasts are generally grouped
together and occur in the surface keratin. In the proventriculus, zy-
gomycetes, Candida, and Rhizopus cause mycotic proventriculitis.
Presence of many large Gram- and PAS-positive, long, filamentous
organisms typically occurs in parallel or as bundles is characteristic
of megabacteriosis caused by the yeast !Ylacrorhabdus omithogas-
ter. Lesions usually are most frequent at the junction of the proven-
triculus and ventriculus.
Parasitic infections
Protozoa! organisms within foci of necrosis and fibrinoheterophilic
exudate in the upper alimentary system may be numerous, but are
272 I American Association of Avian Pathologists
often difficult to identify in conventional H&E sections. Wet smears
or cytology is preferable for diagnostic purposes. Outlines of ova l
or pear-shaped organisms are characteristic of Trichomonas gal-
linae, an important pathogen of pigeons and free-living passerine
birds. Details of the protozoa! structure, especially the flagella and
undulating membrane, are not visible even in well preserved ti ss ues
with acute lesions. Chronic lesions and poorly fixed , autolytic ti s-
sues are unlikely to yield sufficient information for a confirmed di-
agnosis oftrichomoniasis. Bodian's silver stain can be used to help
identify trichomonads and may reveal numerous organisms within
the lesions. Necrosis of the epithelium of the upper alimentary tract
can be caused by Toxoplasma and the diagnosis is dependent upon
demonstration of the organisms in the lesions. Protozoa I parasites,
including Cryptosporidi11111 and Toxoplasma, may be found in pro-
ventricular lesions of heterophilic inflammation, hyperplasia and/or
epithelial necrosis.
Erosions and ulcers with necrotic debris on the epithelial sur-
face of the proventriculus and intralesional nematodes occur in pro-
ventricular nematodiasis. Epithelial hyperplasia and hyperkeratosis
with the presence of nematode parasites and parasite eggs is the
characteristic lesion of Capi/laria sp. in the crop and sometimes the
esophagus. Other nematodes that may invade the upper alim en-
tary tract include Gongylonena i11g/11vicola and Echinuria unci-
nata (waterfowl). Mucosa! papillary projections adjacent to areas
invaded by the nematodes are associated with Dispha1J111x nasuta
infection. Heavy proventricular infections of pigeons with larval
Omithostro11gy/11s quadriradiatus can result in mo1tality from blood
loss. Tetmmeres spp. invade glands of the proventriculus where
they distend and fill the lumens. Degeneration of glandular epi-
thelium with edema and lymphoid cell infiltration are features of
Tetmmeres fissispina in ducks. Species of Eustrongylides that in-
fect a variety of shorebirds penetrate through the proventricular wall
and cause fatal verminous peritonitis. A number of other parasites,
many of which are pathogenic, occur in the proventriculi of birds,
but a full discussion of these is beyond the scope of this book.
Ventriculus ("Gizzard")
Many birds ingest foreign objects that assist with grinding food in
the ventriculus. Usually these are stones and not harmful. Occa-
sionally, sharp objects such as nails or screws are ingested. These
can puncture the wall of the ventriculus and cause traumatic ven-
triculitis. If complete penetration occurs, necrosis and inflamma-
tion of adjacent organs including liver, lung, and peritoneal cav ity
occurs. Often lesions are black because of the release of iron as
the objects disintegrate. Migration tracts characterized by necrosis,
inflanmrntion, and fibroplasia are seen. Other sharp objects (cricket
and grasshopper legs, plant seeds, etc.) can cause traumatic ven-
triculitis, especially in small passerine birds, but they rarely affect
other organs.
Toxicities and Deficiencies
Erosions and degeneration of the koilin layer of the gizzard are
seen frequently. There are several possible causes including

defi ciency in su lfur-containing ami no acids, diets deficient in
vitamin B6, excess copper su lfate , zi nc oxide, coba lt, and exposure
VetBooks.ir
to litter treated with ferrous sulfate hepatahydrate . In addition
to ul ceration s of the koilin layer, g lands of the mucosa may be
di stended or may have a flattened ep ithelium indicating atrophy.
Erosions and ul ce rs of the gizzard ep ithelial mucosa are features of
tri chothecene mycotox ins, cyclopiazonic acid or biogenic amin es
like gizzerosine. Myopathy of the mu sculari s of the gizza rd occurs
in vitam in E and selenium defi cienci es.
Infections
Viral i1!fectio11s
Natural cases of gizza rd erosion assoc iated with fowl adenoviru s
occur in layer chi cke ns, broiler chi ckens, and quail. Necros is with
the presence of intranuclear inclusions in gizzard glandular epithe-
lial cell s is seen . Avian encephalomyelitis virus causes infiltration
of lymphocytes that form multipl e nodules in the mu scularis.
Fungal i11fectio11s
Gi zzard ca ndidiasi s (mycosis) caused by Candida sp. is an impor-
tant di sease in finche s. The infection has been reported to be the
cause of mortality. The disease needs to differenti ated from mac-
rorhabdosis.
Parasitic i11fectio11s
Nodul es of fibrous connective tissue are characteristic of infections
with the nematode Chei/ospimra ha11111/osa.
Intestine
Histology and Histopathological Evaluation
Microscopic evaluation of the intestines is best done with longitudi-
nal sections that provide more surface area of the intestine compared
to exa mination of cross sections. The lymphoid cell population in
the lamina propria of the mucosa varies but considerable numbers
of lymphocytes and plasma cells with fewer granular leukocytes are
normal. Histologic distinctions between duodenum , jejunum, and
ileum are not always easy, although villi become shorter and wider
and crypt depth decreases with distan ce from the g izza rd. The duo-
denum distinctly has long villi. The pancreas is embedded in the
duod enal loop, and including pancreas adjacent to the duodenum
on slides is a practi cal way to identify this region. Meckel 's diver-
ticulum is used as the arbitrary marker to separate the jejunum from
the ileum. Great variation exists in the shape, size, and hi stology of
the ceca among the avia n species. Most birds have paired ceca, but
some have only a single cecum, double pairs of ceca, or lack ceca
(woodpeckers, hummingbirds, sw ifts, kingfishers, pigeons, mouse-
birds, cuckoos, and parrots). Ceca may be simple or sacculated.
Galliformes have a simple tubular intestinal type ceca with well-
developed villi in the proximal portion (pa11 closest to the terminal
ileum). The mid-portion of gallinaceous ceca has prominent lon-
gitudinal folds or plicae . These are poorly developed in the distal
ceca and villi in this region are short and blunt. Lymphoid foci are
abundant and may deve lop into nodules in the ceca l mucosa. The
large intestine has a thick muscul ar wall, and villi of the mucosa are
Ali111e11fmJ' System
relatively short and blunt. The c loaca is lined by columnar epitheli-
um hav in g a villus arrangement si milar to that in the large intestine.
Villi decrease in hei ght with progress ion toward th e vent and the ep-
ithelium becomes si mple tall columnar without goble_t cells. Small
glandular crypts are present. The columnar epithelium changes to
stratified sq uamou s epithelium characteristic of a muco-cutaneous
junction at the lips of the vent. Herbst corpuscles are located in the
connective tissue beneath the lips of the vent.
Post-mortem autolysis occurs quickly in the intestines and
leads to separation of epithelial cells from the lamina propria of the
villi. Villus ep ithelial cells are totally lost as autolysis progresses
usuall y from the tips of vi lli first and then to the crypts. Autolytic
changes are com mon in diagnostic sa mpl es and they complicate
identification and interpretation oflesions. Detachment of epithelial
cells from th e surface of villi is a common artifact that occurs
during processing of the tissue, and caution should be exercised in
interpreting this as a lesion. Good fixation with minimal a11ifacts is
best achieved by opening the intestine along its longitudinal axis.
The opened section may be applied, serosa side down, to a firm
support such as a piece of cardboard and clipped to the support
at the ends. Intestines placed into I 0% neutral buffered formalin
at approximately IO parts fixative to I part intestine should be
adequately preserved with minimal artifacts. Sections should
maintain proper relationship between crypts and villi and permit
measurement of villus to crypt ratios.
It is important in establishing patterns of injury in the
intestinal tract to determine whether the primary lesion site is
the villus epithelium or crypt epi thelium. Edema, hemorrhage,
granular leukocyte (heterophils and/or eosinophils) infiltration,
and lymphoid cell hyperplasia are lesions that ex pand the lamina
propria causing increased width of villi and increased mucosa!
thickness. Goblet cells in the villous epithelium become prominent
due to distention with mucu s. Some chemicals, mycotoxins, viral
or other infec ti ous agents including some sp ecies of coccidi a have
an affinity for rapidly di v iding cells in crypts. Necrosis of crypt
epithelial cells leads to dilation of crypts and filling of the cystic
crypts by mucus and necroti c cellular debri s. The remaining crypt
e pithelium beco mes flattened. Increased numbers of macrophages
that contain necrotic deb ris , frequently with a vacuolated
cytoplasm, are ofte n present in the lamina propria. Hemorrhage,
vasculitis, and thrombosis are lesions associated with systemic
bacterial infections. Hemorrh ages in the intestines and other organs
are features of sulfonamide toxicity, anticoagulant rodenticides,
and some mycotox ins. Duck v iral enteritis and Eastern equine
encephalitis virus in ratites can cause acute hemorrhage in the sma ll
intestine and ceca. Hypersecretion by enterocytes can contribute
significantly to the amount of fluid in the intestinal lumen and thu s
contribute to clinical diarrh ea. Hypersecretio n is generally not
appreciated by li g ht microsco py. Increased apoptosis is another
mechanism contributing to loss of mature enterocytes. Apoptotic
cha nges in enterocytes are underappreci ated based on light
microscopy. Mild alterations in length, width, and shape of villi
are difficult to interpret. C hanges in the shape of villi probably
are not important in determining a specific ca use of enteritis. Villi
in the avian intestine are ellipsoidal rather than cylindrical. Villi
Avian Histopathology (4 th Edition) I 273
 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
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can appear shorter and have accordion-like folds , which is likely
ca used by the presence of large amounts of fluid in the intestinal
lumen . Villus:crypt ratios are important indicators of di sease if
well fixed, longitudinal are examined.
lt is common for multiple agents to be involved in producing
injury to the alimentary system. It is tempting to rely on a specific
observation, e.g., presence of coccidia, to make a disease diagnosi s
when, in fact , multiple etiologies are involved and etiological
diagnosis is not simple or straight forward.
Catarrhal enteritis is characterized by excess mucu s production
and increased secretions of enterocytes that cause accumulation
of fluid in the intestinal lumen . Necrosis of enterocytes may be
scattered along the surface of villi and be difficult to recogni ze or
differentiate from autolytic changes. Lymphocytes, along with
variable numbers of granular leukocytes, often expand the lamina
propria. Edema may also contribute to expansion of the lamina
propria. Loss of mature enterocytes at the tips and sides of the upper
portions of villi leads to hyperplasi a of crypt epithelium because of
the need to produce new cells to replace lost mature enterocytes.
Villus length is decreased when mature enterocyte loss exceeds
replacement of enterocytes generated in the crypts. The presence
of focal to diffuse hemorrhage in the lamina propria indicates more
seve re injury.
I
Infections
Viral i11fectio11s
Shortening, blunting, and fusion of villi (villous atrophy), usually
accompanied by expansion of the lamina propria with increased
cell populations, are associated with enteric virus infections but
are not diagnostic for a specific viral etiology. Malabsorption
sy ndrome in broilers and poult enteritis complex, of which poult
enteritis mortality syndrome (PEMS) is a severe form, are exam-
ples of di seases that have both crypt and villus lesions. These
enteric diseases can be reproduced with intestinal homogenate s
from clinically affected birds, but si ngle agent inoculation does
not reproduce the full range of clinical sig ns, gross lesions, and
microscopic changes. Cystic dilation of crypts and villous atrophy
are characteristic lesion s seen in runting-stunting (malabsorption)
syndrome of broilers . Vacuolar degeneration , apoptosis of entero-
cytes at the tips of vi II i, and loss of enterocytes also are present in
runting- stunting syndro me. Viruses associated with ma labsorp -
tion syndrome include astrovirus, avian nephritis viru s, enterovi-
ru s, parvovirus, reovirus , and rotavirus. Ballooning degeneration
and necrosis of lymphoid or reti cul ar cells in the lamina propria,
some degree of heterophil infiltration, and edema expanding the
lami na propria of the sma ll intestine of chickens are found in spik-
in g mortality of young broilers. Enterocytes are intact and rela-
tively und amaged. Vacuolated cells in the lamina propria contain
necrotic debris. lntralesiona l viruses include adenovirus, reovi-
rus , rotavirus , and herp es virus . Viral inclus ion bodies are not
found . Long-segmented filamentous gram-positive bacteria (or-
ganisms) may be associated with enterocy tes in some segme nts of
the small intestine and attaching bacteria are frequently found in
the cecum. Fibrinoid necrosis of the tunica media of sma ll arter-
ies in the serosa of the intestines is found rarely in some cases of
274 I American Association of Avian Patholog ists
spiking mortality of broilers. Dilated crypts may be present, but
are not common to all cases. The pattern of dilated crypts, villous
atrophy, and expansion of the lamina propria serves to differentiate
runting- stu nting sy ndrome from spiking mortality.
Villus atrophy and c1ypt hyperplasia are features of coronavirus
infection of turkeys. Villous atrophy, hyperplasia ofcrypt enterocytes,
loss of enterocytes from tips of villi, fusion of villi, club-shaped vi lli,
and compression of villi resulting in an accordion-like appearance,
with expansion of the lamina propria by a predominately lymphoid
cell population are typical lesions found in turkeys with poult
enteritis complex. These lesions are not diagnostic as to etiology but
often specific and probable contributing causes to the overall clinical
syndrome can be identified, which includes cryptosporidia, attaching,
effacing enteropathogenic E. coli, flagellated protozoa, coccidia, and
long, segmented filamentous bacteria. Viruses associated with poult
enteritis complex include turkey coronavirus, astrovirus, reovirus,
rotavirus, parvovirus, and enterovirus.
Small, eosinophilic, intranuclear inclusions (Cowdry Type
A) or the more common large, basophilic, intranuclear inclusions
(Cowdry Type B) of Aviadenovirus (formally Gro up I avian
adenovirus) may be found in ente rocytes in the intestine of turkeys.
These intranuclear inclusions are more commonly found in cecal
enterocytes and usually are seen with no associated les ions,
although other segments of the digestive tract may have a vari ety of
lesions including coccidiosis. Type A and B intranuclear adeno viral
inclusions in enterocytes of Cotumix quail are associated with
enteritis including expansion of the lamina propria by lymphocytes.
Large, intranuclear, eosinophilic inclusions containing viral
particles characteri stic of parvovirus can be found in enterocytes
at tips and sides of villi, but not in crypt enterocytes, in the ileum
of turkeys. These inclusion s are not associated with villus atrophy
or expansion of the lamina propria and their role in enteric disease
of turkeys is not known. lmmunohi stochemical sta ining could
be used to differenti ate these inclusions from similar appearing
adenoviral inclusions.
Large, pale g rey or c lear (ground-glass appearance)
intranuclear inclusions typical of polyomavirus may be found in
cecal enterocytes in chick.ens . The role ofpolyomavirus in intestinal
disease in chick.ens in unknown , but it is a significant pathogen
in many av ian species. Hemorrhagic enteritis and necrosis of
crypt enterocytes are characteristic lesions of geese infected with
hemorrhagic nephritis-enteritis virus, a polyomavirus. However,
intranuclear inclusio ns in enterocytes are not seen in thi s di sease.
Mucosa! hemorrha ge that is especially prominent in lymp hoid
tissue of the annular bands, and elevation and separa tion of the
overlying mucosa acco mpanied by large amounts of blood and
cellular debris are seen in the intestinal lumen of ducks , geese,
and swans with duck virus enteritis, a herpesvirus infectio n.
Both intranuclear and I/C eosinophilic inclusions are present in
degenerating epithelial cells. Hemorrhagic enteriti s in turkeys,
caused by siadenovirus (formally Group II avian adeno viru s),
is characterized by severe congestion of the mucosa , necrosis
of th e tips of the vi lli , and hemo rrhage into the lamina propria
and intesti nal lumen. In creased numbers of lymphoid cells,
plasma ce lls, and heterophils expand the lamina propria . Ce lls

with intranuclear inclusion bodies may be observed in the lamina
propria , but are more common in the spleen.
VetBooks.ir
Eastern equine encephalitis virus causes fatal hemorrhagic
enterocolitis in emus and ostriches. Turkeys develop the disease
atler ex perimental inoculation with the virus.
Bacterial i11fectio11s
Diffuse necrosis of the mucosa that involves at least the upper one-
third of the villi is characteristic of necrotic enteritis caused by Clos-
tridi11111 pe1:fri11gens. Lesions of necrotic enteritis can extend to the
crypts and, in some cases, involve the tunica muscularis. Endog-
enous stages of coccidia are often present in cases of necrotic en-
teritis. Focal to multifocal necrosis of the full thickness of the mu-
cosa is characteristic of ulcerative enteritis caused by Closlridi11111
coli1111111. Numerous large rods that are positive on Gram staining,
are present in the necrotic debris, especially at the margin between
necroti c and viable tissue. In ulcerative enteritis, fibrinoheterophilic
exudate and lymphocytic cellular infiltrate is found at the base and
margins of the ulcers and extends into the serosa. In sub-acute or
chroni c cases, fibroplasia may be evident at the base of the ulcers.
Attaching-effacing bacteria multifocally attach to the brush
border of enterocytes and cause micro erosions in the mucosa!
surface. The surface epithelium becomes irregu lar due to the loss
of individual or groups enterocytes. In turkeys, Escherichia coli are
the most important attaching-effacing bacteria (mainly found in the
ceca). Co-infection with turkey corona virus results in poult enteritis
morta lity syndrome (PEMS), which is characterized by marked
stunting and high mortality. Gram-pos iti ve enterococci attached to
surface of enterocytes in the duodenum or small intestine are seen in
enterococcal-associated enteritis.
A dense basophilic layer of organisms covering the surface of
enterocytes in the cecum is characteristic of spirochetosis caused
by Bm chyspirn spp. Spirochetes are oriented perpendicular to
the surface of the enterocytes and aligned paral lel to each other
creating a finger-like pattern. The lamina propria is expanded by
lymphocytes and plasma cells.
Infections with Jvfycobacteria spp. often involve the digestive
tract as well as other organs including liver and sp leen. Large
numbers of histiocytic (epithelioid) cells, which typically show a
basophilic, granular cytoplasm, infiltrate focal , multi focal or diffuse
areas of the lamina propria. Multiple nodules composed ofhistiocytic
cells may involve the muscularis and serosa of the alimentaiy tract.
Acid-fast stain ing usually reveals many acid-fast positive bacteria
filling the cytoplasm of the epithelioid cells. Giant cells vary in
number and may not be present. Intestinal mycobacteriosis needs to
be differentiated from neoplasia .
Parasitic il(/'ectio11s
Protozoa! parasites are common in the intestines and ceca and are
signifi cant causes of damage to the intestinal tract. Ei111eria spp.
invade enterocytes and replicate through a series of asexua l (me-
rogony) and sexual (gamogony or gametogony) cycles. Ingestion
of sporulated oocysts releases sporozoites that are carried in macro-
phages and/or migrate to invade susceptible enterocytes . Meronts
(schi zonts) containing merozoites are formed within enterocytes.
Ali111e11ta1J' System
Merozoites that are released when meronts rupture enter new host
enterocytes and another generation ofmeronts is formed. The m1111-
ber of asexual generations and locations of infection within the in-
testinal tract varies among Ei111eria species. Gamogony begins after
penetration of enterocytes by merozoites. In stead of developing
into meronts, they differentiate into either female (macrogameto-
cytes) or male (microgametocytes) gametocytes (gamonts). Mac-
rogametocytes are more numerous than microgametocytes. Mac-
rogametocytes are densely basophilic and increase in size but do
not undergo distinct morphologic changes as they mature into mac-
rogametes. Microgametocytes differentiate into numerous flagel-
lated sperm-like microgametes that are released through the process
of exflagellation . Sexual fertili zation occurs when a microgamete
fuses with a macrogamete to form a zygote . Zygotes develop evenly
spaced peripheral eosinophi lic granules called wall-forming bodies
as they mature. Wall-forming bodies spread out and fuse to form
the oocyst wall. At this stage, the oocyst contains an undifferenti-
ated sporoblast, which is the stage that is shed into the intestine and
passes out of the bird in its feces. When developmental stages of
coccidia occur deep in the lam ina propria (e.g., E. tenella, the cause
of cecal coccidiosis in chickens), oocysts may not be able to exit the
mucosa and become trapped. A crescent-shaped sporoblast is seen
in these oocysts .
I
Presence of endogenous developmental stages of coccidia in
enterocytes or lamina propria, accompanied by varying degrees and
combinations of congestion, edema, hemorrhage, heterophilic and
lymphocytic inflanunation, necrosis and loss of epithelial cells, and
vi llous atrophy are characteristic lesions of coccidiosis. The location
of developmental stages and lesion pattern often provide sufficient
information to justify a diagnosis of infection with a pa11icularspecies.
For example, in the chicken, £. acervulina infects the duodenum and
developmental stages occur as large aggregates in enterocytes at the
tips and along the sides of villi. E. 11ecatrix lesions are deep within
the lamina propria, occasionally extending into the submucosa,
often granulomatous and hemorrhagic. Lesions destroy and replace
crypts in the jejunum and ileum. These lesions contain many large
meronts packed with merozoites. Gamogony of£. necatrix occurs
in the ceca and not in conjunction with the asexual stages in the small
intestine ; oocysts are found in the ceca although severe lesions are
present in the small intestine. E. 111axi111a produces large oocysts
in the lower duodenum, jejunum, and upper ileum. The protozoan
develops in the lamina propria adjacent to the basement membrane
of the enterocytes. Lesions are characterized by large numbers of
zygotes. E. tenella develops in the lamina propria and enterocytes
in the ceca. Lesions are characterized by congestion, hemorrhage,
numerous developmental stages that replace crypts and enterocytes,
and extensive destruction of surface enterocytes. Meronts are large
and contain numerous large close ly packed merozoites. Expansion
of the lumen and formation ofa cecal core commonly occurs in cecal
coccidiosis. Oocysts and bacteria are often numerous in cecal cores.
E. bmnetti is located in the lower ileum and rectum. Lesions are
characterized by large first generation meronts located about half
way down from the vi llus. Asexua l stages of first- and second-
generation meronts of£. bmnetti occur in the upper small intestine.
The location of Ei111eria species in the intestinal tract of chickens,
Avian Histopathology (4 th Edition) I 275
 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
with the exception of E. tenella, can vary from the "classica l" regions
VetBooks.ir
of the intestine, especially if the infection is heavy. Infections with
multiple species of coccidia are common.
Gra nul omatous nodules in the oral cavity, esophagus, and
cloaca of cranes can be caused by Ei111eria reichenowi and Ei111eria
grnis. Granulomas are composed of mononuclea r cells (lymphocytes
or monocytes) filled with asexual stages of coccidia. Vasculitis is
a characteristi c feature. These coccidia also infect oth er organs
including heart, liver, trachea, lung, and eyelids.
Crypto sporidi a are seen in the H &E sta ined sect ions as
round to ovoid basophilic bodies, about 4-6 ~1111 in diameter, on the
sur face and within th e brush border of villi. In severe infecti ons,
villi are reduced in height and mononuc lear cells ex pand the
lamina propria. Cryptosporidiosis is an especially devastating
di sease in quail.
Extensive expansion of the lamina propria of the cecum
with large numbers of lymphocytes, macrophages, giant cells,
and intralesional protozoa [ parasites (trop hozoites), often in
groups of 2, 4, or 8 are characteristic of Histo111011as 111eleagridis
infection. Lesions often extend into the tunica musc ularis and may
be transmural resultin g in fibrinoheterophilic and lymphocytic
inflammation of the serosa. Histomonads commonly invade the
liver, but also are occasionally found in other organs including
I
kidney, lung, and bursa Fabricius.
Villous atrophy and expansion of the lamina propria by edema,
lymphoid cells, and so me heterophil s are see n in infections with
certain flagellated protozoa . F lagellated protozoa may be found in
the lumen, between villi, along the border of villi , and/or wi thin crypt
lumens. Spironucleus (Hexa111ita) 111eleagridis is characteristica lly
found in the lumen of intestinal crypts. Flagellated protozoa located
along villi, but not usually in crypts are typical of Giardia sp. and
Cochloso111a anatis. Giardia occurs most frequently in the upper
small intestine of companion birds whereas Cochloso111a is fo und
in commerc ial birds, especially ducks and turkeys, and infects the
middle and lower small intestine and ceca. Significant les ions are not
associated w ith these protozoa as their pathogeni city deri ves from
their attachment to the mucosa[ surface by sucker-like structures and
blocking absorption of nutrients. In mi crosporidiodis , caused by the
protozoan Encephalitozoon helle111, th e cytoplasm of enterocytes is
distended with the tiny spores of th e microorga nism, which may
also be found in large numbers in the lumen. Spores of E. helle111
are Gra m-p ositive. Trichomonads, especially in the ceca, usually
fill th e lumens of crypts, and relatively few orga nisms are found
along the sides of villi or in the intestinal lumen. They may or may
not be pathogenic but are typically numerous in cases of enteritis.
The type of the flagellated protozoa usually is difficult to determine
in most H&E-stained hi stologic section s. Unstained wet smears and
cytological smears of intestina l contents and mucosa! surface are
preferred for identificati on of protozoa. The term protozoa ! enteritis
may be used for cases of enteriti s caused by any protozoan.
Flukes, tapeworms, and nematode paras ites ca n cause variable
degrees of enteritis and damage to th e intestinal mucosa . Diagno-
sis req uires identification of the parasite and/or ova in th e intestinal
tract. Ascaridia, Heterakis, and cestodes are com monl y found in
chickens. Exposure of birds to hi gh numbers of infective Ascaridia
276 J Ameri can Assoc iatio n of Avian Pathologists
eggs can result in numerous larvae penetrating the intestinal wa ll
si multaneo usly, which results in severe enteritis that may be fata l.
Infection with larva l Ascaridia can a lso predispose to clostridial in-
fections. Heterakis isolonche infection in pheasants causes nodular
typhlitis in pheasants. Granulomas and mucosa! tumors, considered
to be of smooth muscle ori g in, occur in the ceca .
Cloaca
C hroni c inflammation of the cloaca characterized by ulceration of
the mucosa, increased numbers of lymphocytes and focal aggre-
gates of giant cells, variable numbers of heterophils, and extensive
sub mucosa! fibro sis characterize c loaciti s seen in com mercial lay-
ers and broiler breeder hens. This condition is term ed vent glee! in
o lder literature. Cloacitis uncomplicated by persecution has foca l
to multi foca l acute hemorrhage, edema, mixed inflammatory cell
infiltration of mucosa and underly ing tissues including heterophi ls
and lymphocytes, dilation of g lands, and epithelial hyperplasia in
the vagina, urodeum, and proctodeum . A specific etiology has not
been identified although bacteria are seen mi croscopically.
Proliferation of cloaca I enterocytes (enterocyte hyperplasia), di-
lat ion of glands due to mucus and heterophil accumulation, and an
intense mixed-cell (heterophils, lymphocytes, plasma cells, and mac-
rophages) inflanunation of the lamina propria and sub mucosa ! ti ssue
are seen in emus with Lawsonia intracellu/aris infect ion. Traumatic
injuiy to the vent and cloaca due to persecution leads to ulcerati on of
the mucosa and chronic inflammati on, usuall y with hemorrhage.
Neoplasia of Alimentary Tract
Prima1y neoplasia of the alimentary tract is less common than tu-
mors of Marek's disease and leukosis/sarcoma (such as heman-
gioma and hemangiosarcoma). Adenocarcinomas of ovarian or
reproductive tract origin frequently implant on and proliferate in
the serosa of the intestines. Primary papillomas or squamous cell
carcinomas can ori gi nate from the squamous epithelium of the oral
cavity, esophagus, or crop. Papillomas also occur in the cloaca with
many, but not all, associated with herpes or papilloma viruses.
A tumor composed of long spindle-shaped cells enve loped the
gizzard, merged into the remaining smooth muscle layer and re-
placed most of the gizzard structure. The neoplastic mass had areas
w ith a fingerprint pattern , produced mucus, and was diagnosed as a
myxo id leiomyosarcoma.
In psittacines, mucosa! papillomas occur primarily in the clo-
aca (cloaca! papilloma), occasionall y in the oral cavity/orophaiy nx
and la1yn x, and rarely in esophagus, crop, proventriculu s, ventriculus,
and conjunctiva . Cloaca[ papi llomas in Amazon parrots are usually
co nfined to the cloaca. Macaws typically have papillomas in the clo-
aca as we ll as in the oral cavity/orophmynx. The ca use of mucosa[
papillomas is unknown. Clinical observations and epidemiological
data suggest an infectious cause. Herpesviral sequences have been
detected by in situ hybridi zation ill cloaca! papillomas in parrots.
Histologicall y, cloaca[ papillomas co nsists of frond-like projections
with a fib rovascul ar core covered by a layer of hyperplastic stratified
cuboidal to columnar epithelial cells of few to many cells in thi ckness.

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Erdogan, S. , H. Sagsoz, and M. E. Akbalik. 2012. Anatomical
and histological structure of the tongue and hi stochemical
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Fitz-Coy, S. H. , and S. A. Edgar. 1988. Additional details of
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I
Gjevre, A.-G. , M. Kaldhusclal, and G. S. Eriksen. 2013. Gizzard
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Robbins, K. M. , W. Ye, and 0. J. Fletcher. 2011. Identification
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40:139-144.
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japonica) intravenously inoculated with Jvlycobacteri11111 avi11111.
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143.
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1288.
Zekarias, B. , N. Stockhofe-Zurwieden, J. Post, F. Balk,
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7.1. Head. Sagittal section. Chicken. Shown are the tip of
beak (arrow), anterior oral cavity at the tip of the tongue (A), and
mid-section of the dorsal surface of the tongue (B). Salivary glands
are located in the roof and floor of the oral cavity. The cartilage of
the ton gue is visible.
7.2. Tongue. Vacuolar degeneration. Chicken. The surface of
the tongue has numerous micro projections. Vacuolar degeneration
is seen in epithelial cells. The micro projections are normal, but the
vacuolar degeneration suggests toxic injury. The cornified ventral
surface of the tongue is normal.
Ali111e11t(//J' System
7.3. Tongue. Normal taste buds and vacuolar degeneration.
Chicken. Higher-power view of area in 7.2. Normal taste buds
(boxes) are scattered in the epithelial surface. Some epithelial cells
undergoing vacuolar degeneration are seen on the left side.
7.4. Tongue. Normal taste buds and vacuolar degeneration.
Chicken. Normal taste buds (box) and scattered vacuolar
degeneration are shown.
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7.5. Tongue. Normal ta ste buds and vacuolar degeneration. 7.7. Oral cavity and ton gue. Normal. Chicken . Hi gher-power
Chicken. Hi gher-power view of the region wi thin the box in 7.4 view of the region B in fi gure 7. 1. The dorsal region of the oral
shows taste bud. cav ity co ntains many sa liva ry g lands (box). The mi cro project ions
on the do rsa l surface of the tongue (a rrow) are norma l.

7.6. Ton gue. Normal structures and vacuolar degeneration. 7.8. Oral cavity. Toxic injury. 30-day-old chicken . The
C hicken. The posteri or region of the tongue contains cartilage in epithelium of th e roof of th e mouth is eroded, and large zo ne of
th e co re(*), area of vacuolar degenera ti on of epi thelial ce lls (a rrow), necrosis separates the epithelium from th e underl ying tissue . This
and sa livary glands (box) . is early oral ulcer suggestive of toxic injury.

282 I Ameri ca n Assoc iati on of Av ian Path ologists

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7.9. Oral cavity. Toxic injury. 30-day-old chicken. Large 7.11. Oral Cavity. Toxic injury. 30-day-old chicken. Higher-
region of caseous necrosis (box) and chronic inflammation is in the power view of area in 7.10 showing bacterial colonies.
floor of the oral cavity. Also shown is vacuolar degeneration of
the surface epithelium. These lesions are not disease specific but
suggestive of toxic injury.

7.10. Oral cavity. Toxic injury. 30-day-old chicken. Higher- 7.12. Oral cavity. Diphtheritic pox. 37-week-old turkey. Large
power vi ew of area in 7.9 showing necrosis and intralesional nodule of hyperplastic epithelial cells is in the upper oral cavity.
bacteria.

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7.13. Oral cavity. Diphtheritic pox. 37-week-old turkey. 7.15. Oral cavity (mouth floor). Diphtheritic pox. Backyard
Higher-power view of area in 7. 12 showing pronounced epithelial chicken. Marked squamous hyperplasia of the mucosa! epithe lium,
hyperplasia, vacuolar degeneration, and intracytoplasmic inclusions with superficial mucosa! necrosis and accumu lation large amount of
bodies. necrotic debris on the surface.

7.14. Oral cavity. Diphtheritic pox. 37-week-old turkey. 7.16. Oral cavity (mouth floor). Diphtheritic pox. Backyard
Higher-power view of area in 7.13 . Note the numerous UC chicken. Higher-power view of area in 7.15 showing marked
inclusions. squamous hyperplasia of the mucosa! epithelium, with superfic ial
mucosa! necrosis and adherent exudate on the surface.

284 I American Association of Avian Pathologists

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7.17. Oral cavity (mouth floor). Diphtheritic pox. Backyard 7.19. Oral cavity. Ulcer. Candidiasis. Turkey. Higher-power
chicken. Higher-power view ofarea in 7 .16. Hyperplastic squamous view of 7. 18 showing the ulcer with intralesional bacteria and
cells are large and have abundant basophilic cytoplasm, large fungal spores.
nucl eo li with prominent nucleus, and intracytoplasmic inclusions
characteristic of poxvirus inclusion bodies. Note the infiltration of
heterophils, with mucosa! erosion and adherent fibrinoheterophilic
exudate on the surface.

7.J 8. Oral cavity. Ulcer. Candidiasis. Turkey. Oral ulcer is 7.20. Oral cavity. Ulcer. Candidiasis. Turkey. Higher
shown at low magnification. Salivary glands are in the upper left. magn ification of 7.19. Intralesional spores and bacteria are seen
more easily at thi s magnification.

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 Oscar J. Fletcher • Tahsee11 Abdul-A ziz
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7.21. Oral cavity. Ulcer. Candidiasis. Turkey. Hi gher-power 7.23. Esophagus. Vitamin A deficiency. Pheasant. Hi gher-
view of area in 7.20 showing spores of Candida sp . (box) and powe r view of area in 7 .22 showing squ amous metaplas ia of mucus
intral es ional bacteri a. g lands characteri sti c of Vitamin A defi ciency.

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7.22. Esophag us. Vitamin A deficiency. Pheasant. Mucus
glands in thi s esophagus have sq uamous metaplasia and epithe lial
hyperpl asia.
7.24. Esophagus. Squamous metaplasia. 30-week-old broiler
breeder chicken. Mucus g land in the esophagus is replaced with
squ amous e pithelial ce ll pro li fe ration (squamous hyperpl as ia).
Vitamin A defi ciency was e liminated as the cause for thi s case. The
ca use is unknown .

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7.25. Esophagus. Squamous metaplasia. 30-week-old broiler 7.27. Esophagus. Ulcer. 45-day-old broiler. Higher-power
breeder chicken. Hi gher-power view of area in 7 .24. view of area in 7.26 showing edge of ulcer, intralesional bacteria,
and vacuolation in adjacent epitheli al cell s.

7.26. Esophagus. Ulcer. 45-day-old broiler. Ulceration of the 7.28. Esophagus. Vacuolar degeneration. Fowl pox. Backyard
esophageal mucosa is suggestive of toxic injury. Mucosa! erosion chicken. Region of vacuolated epitheli al cells is shown.
is adjace nt to the ulcer.

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7.29. Esophagus. Vacuolar degeneration. Fowl pox. Backyard 7.31. Esophagus. Vacuolar degeneration. Fowl pox. Backyard
chicken. Higher-power view of the vacuolated region in 7.28 chicken. The lesions consist of epithelial hyperplas ia, vacuolar
showin g eosi nop hili c intracytoplasmic inclusions. degeneration of epithelial cells, and intracytop lasm ic inclusion
bodies.

7.30. Esophagus. Vacuolar degeneration. Fowl pox. Backyard 7.32. Esophagus. Vacuolar degeneration. Fowl pox.
chicken. Higher-power view of vacuolated cells show ing Backyard chicken. Hi gher-power view of area in 7 .31 showing
eos inoph ilic intracytoplasmic inclusions. large eosinophilic intracytoplasmic inclusions characteristi c of fow l
poxvirus inclusion bodies.

288 I America n Association of Avian Pathologists

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7.33. Esophagus. Infectious laryngotracheitis. 12-month- 7.35. Esophagus. Infectious laryngotracheitis. 12-month-
old backyard chicle The epithelium is hyperplastic, and there is old backyard chick. Higher-power view of area in 7.34 showing
focal region of necrosis and ulceration. Syncytial cells (boxes) are syncytial cells with intranuclear inclusions characteristic of
numerous. herpesvirus.

7.34. Esophagus. Infectious laryngotracheitis. 12-month-old 7.36. Esophagus. Infectious laryngotracheitis. 12-month-
backyard chicle Higher-power view of7.33 showing edge of ulcer old backyard chicken. Another Higher-power view of area in
with intralesional syncytial cells. 7.34 showing syncytial cells with intranuclear inclusions (boxes)
characteristic of herpesvirus.

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7.37. Esophagus. Duck viral enteritis. Canada goose. Foca l
area of mu cosa ! ul ceration . Intranuclea r inc lusi o ns characteristic
of herpesv irus inc lusion bodies were seen in mucous g lands in th e
ul cerated area.
7.38. Esophagus. Duck viral enteritis. Muscovy duck. Severe
necrosis of the mucosa. Normal mucosa! epithe lium is seen 111
the upper ri g ht corner. lntranuclear inclusions characteristic of
herpesv irus inclusion bodie s were seen in mucous g lands.
290 I Amer ican Assoc iatio n of Av ian Pathologists
7.39. Esophagus. Duck viral enteritis. Muscovy duck. Hi gher-
power- view showin g severe and extensive necrosis of the esophagea l
mucosa. lntra nuc lear inclusions characteri sti c of herpesvirus
inc lusion bodies were see n in muco us g lands. The necroti c mucosa
is heavi ly coloni zed by bacteria .
7.40. Esophagus. Mycobacteriosis. 6.5-year-old qua il.
Esophageal epi th elium is ulcerated, with caseo us necroti c material
on the surface. Extensive infiltrat ion of large hi sti ocytes is
expa nding the underlying co nnective tissue.

VetBooks.ir
7.4 1. Esophagus. Mycobacteriosis. 6.5-year-old quail. Higher-
power view of area in 7.40 showing histiocytic infiltration.
7.42. Esophagus. Mycobacteriosis. 6.5-year-old quail. Higher-
power view of area in 7.41.
Ali111e11ta1;i1System
7.43 . Esophagus. Mycobacteriosis. 6.5-year-old quail. Higher-
power view of area in 7.42 showing histiocytes with large amounts
of cytoplasm.
7.44. Esophagus. Trichomoniasis caused by Tricl10111011as
gallinae. 6-month-old backyard turkey. Scanning view of two
sections of the esophagus showing focal , deep necroulcerative
lesion. Grossly, several roughly round ulcers covered with necrotic
debris were present in the mucosa of the esophagus and crop .
Microscopic examination of wet smears from lesions revealed
numerous flagellated protozoa morphologically consistent with
trichomonads .
Avian Histopathology (4 th Edition) I 291
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7.45. Esophagus. Trichomoniasis caused by Tricho111011as 7.47. Esophagus. Mycosis caused by Candida sp. 6.5-year-
gallinae. 6-month-old backyard turkey. Necroulceratri ve les io n old quail. Hyperplas ia of the mucosa) epithelium with thi ck layer
invo lving mos t of eso phagea l wa ll. Protozoa within the nec roti c of surface debri s co nsisting of desquam ated epitheli al cell s and
materi al are no t seen at thi s magnifi ca ti on. necroti c cell ular debris.

7.46. Esophagus. Trichomoniasis caused by Tricho111011as
gallinae. 6-month-old backyard turkey. Hi g her-power v iew of
area in 7.45. O rgani sms morphologica ll y consistent w ith protozoa
are present w ithin th e necroti c debris. Tricho111onas may be difficult
to find or identi fy in H &E stained secti o ns.
7.48. Esophag us. Mycosis cau sed by Candida sp. 6.5-year-
old quail. PAS staining. Large numbers of Candida spores and
pse udohyphae are highli ghted with PAS stain.

292 I Ameri ca n Assoc iation of Avi an Pathologists

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7.49. Esophagus. Capillariasis caused by Capillaria sp. One- 7.51. Esophagus. Capillariasis caused by Capillaria sp. One-
year-old quail. N umerous sections of Capillaria sp. are in the year-old quail. Higher-power view of area in 7.50.
hyperp last ic esophagea l epithelium.

7.50. Esophagus. Capillariasis caused by Capillaria sp. 7.52. Esophagus. Capillariasis caused by Capillaria sp. One-
One-yea r-old quail. Higher-power view of area in 7.49 showing year-old quail. Higher-power view of area in 7.51. Note the
Capillaria with ova. bipolar caps in some eggs in this field.

Avian Histopathology (4 11, Edition) I 293

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7.53. Esophagus.
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Capillarid
.
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(E11cole11s sp.).
nematode 7.55. Esophagus. Squamous cell carcinoma. Backyard
3-month-old Muscovy duck. Man y section s ofcapillarid nematode chicken. Neoplastic squamous epithelial cell s occupy large reg ion
are within the mucosa ! epithelium of the esophagus. of the esophageal co nnective ti ss ue.

7.54. Esophagus. Capillarid nematode (E11cole11s sp.). 7.56. Esophagus. Squamous cell carcinoma. Backyard
3-month-old Muscovy duck. Eggs of ca pillar id nematodes are chicken. Hi gher-power view of area in 7.5 5 showi ng expansion of
associated with cellular debri s. Sections of cap illarid nematodes the subepith elial ti ssue by neop lastic cells.
admixed with mucus are seen in the lumen. Note the disruption of
the mucosa! epithelium .

294 I American Association o f Avi an Pathologists

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7.57. Esophagus. Squamous cell carcinoma. Backyard 7.59. Crop. Physiologic hyperplasia of mucosal epithelium
chicken. Higher-power view of area in 7.56 showing nests of ("Crop Milk"). Adult pigeon, Higher-power view of7.58.
neoplastic epitheli al cells.

7.58. Crop. Physiologic hyperplasia of mucosal epithelium 7.60. Crop. Physiologic hyperplasia of mucosal epithelium
("Crop Milk"). Adult pigeon. Hyperpla sia of the crop epithelium ("Crop Milk"). Adult pigeon. Higher-power view of7 .59 showing
is diffu se and normal when feeding of squabs is required . junction of surface desquamated ep ithel ium and hyperplastic
mucosa.

Avian Histopathology (4 th Edition) I 295

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7.61. Crop. Thickening of lining epithelium. Bird not eating.
3-year-old backyard chicken. Thickening of the superficial cell
layer of the lining pseudostratified epithelium is extensive in this
bird that was not eating. The cells of the superficial layer are
continuously desquamated in birds that are eating.
7.63. Crop. Fenbendazole toxicity. Adult pigeon. Dysplasia
of basal cells of the lining epithelium, with formation of syncytial
cells.

I .'

7.62. Crop. Fenbendazole toxicity. Adult pigeon. The lining 7.64. Crop. Proventricular dilatation disease. 6-year-
epithelium is thin and composed of di sorgani zed dyspl ast ic basa l old eclectus parrot. Infiltration of rnyenteric ganglion with
cells, which exhibit cellular and nuclear pleomorphism and have lymphocytes and plasma cells.
prominent nucleoli. There is formation of syncytial cells.

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7.65. Crop. Proventricular dilatation disease. 2-year-old 7.67. Crop. Sal111011ella typhi11111ri11m infection. Wild gold
pa rrot. Focal area of lymphoplasmacytic infiltrates in the crop finch. Higher magnification of7.66 . The wall of the crop is necrotic
smooth muscle and serosal nerves. and replaced by cellular debris and dense inflammatory infiltrate.
Abundant bacteria are present.

7.66. Crop. Sal111011ella typhi11111ri11111 infection. Wild gold 7.68. Crop. Mycosis caused by Candida sp. Guinea fowl.
finch. Severe transmural necrosis is accompanied by accumulation Epithelial hyperplasia is accompanied by a wide zone of ballooning
of cellular debris consisting of necrotic tissue and abundant intact degeneration of epithelial cells, with a layer of surface debris
and necrotic inflammatory cells. containing numerous pseudohyphae.

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7.69. Crop. Mycosis caused by Candida sp. Guinea fowl. 7.71. Crop. Mycosis caused by Candida sp. Guinea fow l.
Higher-power view of area in 7.68 showing pseudohyphae at the Higher-power view of7.70.
region of ballooning degeneration.

7.70. Crop. Mycosis caused by Candida sp. Guinea fowl. 7.72. Crop. Mycosis caused by Candida sp. Backyard chicke n.
Gomori 's methenamine silver (GMS) stain revea ls numerous Epithelial hyperplas ia, with di sruption of the superficial cell layer
pseudohyphae in the superficial layer of the lining epithelium. by heterophilic infiltrate and numerous pseudohyphae of Candida
sp. Note the zone of vacuolation and vesiculation in the epithelium.

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7.73. Crop. Mycosis caused by Candida sp. Backyard chicken. 7.75. Crop. Mycosis caused by Candida sp. Quail. The
Higher-power view of area in 7.72 showing numerous heterophils superficial layer of the lining epithelium is severely damaged and
and Candida sp. pseudohyphae in the thickened and disrupted contains numerous blastospores (yeast cells), some of which show
superficial layer of the lining epithelium. Zone of vacuolation and budding.
vesiculation are seen.

7.74. Crop. Mycosis caused by Candida sp. 35-day-old guinea 7.76. Crop. Mycosis caused by Candida sp. 6-month-
fowl. The superficial layer of the lining epithelium is disrupted and old guinea fowl. PAS stain. The superficial layer of the lining
colon ized by numerous pseudohyphae of Candida sp. Contiguous epithelium is markedly thickened, and is colonized and penetrated
with the epithelium is a thick layer of necrotic and inflammatory by numerous pseudohyphae of Candida sp. The surface of the
debri s. epithelium appears necrotic.

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7.77. Crop. Capillariasis. Backyard chicken. Several sections 7.79. Crop. Capillariasis. Backyard chicken. Hi gher-power
of Capillaria sp. are w ithin th e hyperplasti c lining epithe lium. view o f area in 7.78 .

7.78. Crop. CapiUariasis. Backyard chicken. Hi gher-power 7.80. Crop. Capillariasis. Backyard chicken. There is
view of area in 7.77 . epithelial hyperpl as ia, w ith section of Capillaria and cluster of
Capillaria eggs w ithin the hyperplasti c epithe lium.

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7.81. Crop. Capillariasis. Guinea fowl. Capillaria eggs are 7.83. Proventriculus. Necrohemorrhagic proventriculitis.
embedded in the epithelium of the crop. The eggs are oval-shaped 16-week-old broiler breeder male. Necrosis and hemorrhage are
and have bipolar caps, which are seen in some eggs. in proventricular gland.

7.82. Proventriculus. Necrohemorrhagic proventriculitis. 7.84. Proventriculus. Necrohemorrhagic proventriculitis.

16-week-old broiler breeder male. At this magnification, 16-week-old broiler breeder male. The lumen of the glandular
proventricular gland appears necrotic with hemorrhage. This duct is filled with heterophils and fibrin . The glands around the duct
proventricular lesion is sometimes seen in dehydrated birds after contain necrotic debris and heterophils.
water is provided. Usually, a few gland lobules are affected.

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7.85. Proventriculus. Necrohemorrhagic proventriculitis. 7.87. Proventriculus. Necrohemorrhagic proventriculitis.

8-day-old broiler breeder pullets. Two severely hemorrhagic 8-day-olcl broiler breeder pullets. Higher-power view showing
and necrotic glands are shown. The flock had high mortality due to loss of glandular epithelium and accumulation of heterophils in the
dehydration . See 7.86 and 7.87. lumens of glands and proventricular duct.

7.86. Proventriculu s. Necrohemorrhagic proventriculitis. 7.88. Proventriculus. Copper toxicity. 13.5-week-o ld turkey
8-day-old broiler breeder pullets. Higher-power view of 7.85 breeder replacement hen. See the legend of7.89 .
shows necros is of proventricular glands, with marked hemorrhage,
fibrin exudation, and heterophil infiltration.

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7.89. Proventriculus. Copper toxicity. 13.5-week-old turkey
breeder replacement hen. This legend is also applied to 7 .88 .
Low-power view of gland lobules showing hemorrhage and necrosis
of glands, with accumulation of fibrin in the lumen of the glandular
duct.
7.90. Proventriculus. Copper toxicity. 13.5-week-old
tu rkey breeder replacement hen. Higher-power view showing
hemorrhage and necrosis with desquamation of the glandular
epithelium, accumulation of fibrin , and some heterophils in the
lumen of gland ular duct.
Afi111e11ta1J' System
7.91. Proventriculus. Copper toxicity. Few-clay-old broiler.
Blebbing, individualization, rounding and early detachment
of glandular epithelial cells. (Glass slide courtesy of PoulflJ1
Diagnostic and Research Cente1; Geo,gia, USA) .
7.92. Avian Encephalomyelitis. Proventriculus. 14-clay-olcl
broiler. Nodular collections of lymphocytes within the muscularis
of the proventriculus are a feature of avian encephalomyelitis.
Avian Histopathology ( 4 th Edition) I 303
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7 .93. Proventriculus. Transmissible viral proventriculitis. 7.95. Proventriculus. Transmissible viral proventricu litis.
Backyard chicken. Ductal hyperplasia, loss of glandular e pithelial Backyard chicken. Hi g her-power v iew of area in 7.94 showing
ce lls, and lymphoid cell infiltration are seen. ductal hyperp lasia and lymphocyte infiltration, with rep lacement of
glandul ar epi thelium with ductal epithelium.

7.94. Proventriculus. Transmissible viral proventriculitis. 7.96. Proventriculus. Transmissible viral proventriculitis.
Backyard chicken. Higher-power view of area in 7.93. Backyard chicken. Higher-power view of area in 7.95.

304 I American Association of Avian Pathologists


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.
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7.97. Proventriculus. Proventricular dilatation disease.
6-year-old eclectus parrot. Lymphoplasmacytic infiltration of
the neuroganglion in the serosa of the proventriculus. This is a
characteristic lesion of proventricular dilatation disease.
7.98. Proventriculus. Pasteurellosis caused by Pasteurella
11111ltocida. 24-week-old pheasant. Hemorrhage is extensive in the
lymphoid tissue at the junction of the esophagus and proventriculus.
Thi s lesion was caused by systemic infection with Pasteurella
11111ltocida, but also suggests viral infection such as highly pathogenic
avian influenza or Newcastle disease.
Ali111e11ta1J' System
7.99. Proventriculus. Pasteurellosis caused by Pasteureffa
11111ltocida. 24-week-old pheasant. Higher-power view of area
in 7.98 showing hemorrhage within the lymphoid tissue at the
esophagus~proventriculus junction.
7.100. Proventriculus. Mycotic proventriculitis. Backyard
chicken. Large region of granulomatous inflammation with caseous
necrosis on the serosal surface. There is also caseous necrosis in
gland (box).
Avian Histopathology (4th Edition) I 305
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7.101. Proventriculus. Mycotic proventriculitis. Backyard 7.103. Proventriculus. Mycotic proventriculitis. Backyard
chicken. Higher-power view of the gland in the box in 7.100 chicken. Hi gher-powe r view of area in 7. I 02. Many hyphae of
showi ng extensive caseous necros is. Aspergillus are seen with PAS stain.

7.102. Proventriculus. Mycotic proventriculitis. Backyard 7.104. Proventriculus-gizzard junction. Macrorl,abdus

chicken. Higher-power view of area in 7.10 1 showing hyphae omit!,ogaster infection Backyard chicken. Large numbers of M.
within the les ion. omithogaster (former name megabacteria, avian gastric yeast) are
on the surface of the mucosa at the junction of proven tri cu lus and
gizzard.

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7.105. Proventriculus-gizzard junction. Macrorlwbdus 7.107. Proventriculus-gizzard junction. Macror/1abd11s

omithogaster infection. Backyard chicken. Higher-power view omithogaster infection. Backyard chicken. Gram staining show s
of area in 7. I 04. See 7. I 06 for hig her magnification of the boxed that M. omithogasler is partially Gram-positi ve (Gra m-va riable).
area.

7. 106. Proventriculus-gizzard junction. Macrorhabdus 7.108. Proventriculus-gizzard junction. Macrorhabdus

omithogaster infection. Backyard chicken. Hi gher-power view omithogaster infection. Backyard chicken. PAS staining show s
of the boxed area in 7.105 . In hi stologic sections, M. omilhogas/er that M omilhogasler is PAS positive.
appears as rod shaped, filamentous organisms that usuall y occur in
bundles often parallel to each other.

Avian Histopathology (4 th Ed ition) I 307

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7.109. Proventriculus-gizzard junction. Macrorhabd11s 7.111. Proventriculus. Nematodiasis. Pigeon . The lumen of a
omithogaster infection. Backyard chicken. Oomori 's pro ventricul ar gland is di stended by large nematode. The nematode
methenamine silver (OMS) stain shows that M. omithogaster is is the femal e o f Tetra111eres sp . The fe male of thi s paras ite is
OM S-positi ve. globular in shape and has long ovary/uterus with numero us coils
fillin g the body cavity. The ovary/uterus is fill ed w ith eggs, which
are embryonated when laid.

7.110. Proventriculus. Nematodiasis. Pigeon . The lumens of
tluee pro ventricular gland s are di stended by large nematodes. The
nematode is the g lobular- shaped fe mal e ofTetrameres sp. Also seen
are pieces of the longitudinal-shaped male Tetrameres around the
fe males in the g landular ducts.
7.112. Proventriculus. Nematodiasis. Pigeon . The lu men
of a proventricular g land is distended by globular shaped fema le
of Tetra111eres sp. , whil e the lumen of another gland co ntains
longitudinal-shaped nematode, which is the male of Tetra111eres sp.
Male and female are commonl y fo und in the lumen of same g land.
Tetrameres sp. represents an exa mpl e of extreme sex ual dimorp hism
among paras ites.

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7. 113. Proventriculus. Nematodiasis. Pigeon. Higher-power 7.115. Proventriculus. Nematodiasis. 4-week-old backyard
vi ew showing embryonated, thick-walled eggs of Tetrameres sp. in turkey. Section of the nematode DisphmJ'llX 11as11ta is in the lumen
the uterus of female . The eggs contain firs-stage larvae when laid. ofproventriculus. The nematode contains embryonated eggs. Note
the excess of mucus in the lumen of the gland.

7. 114. Proventriculus. Nematodiasis. 4-week-old backyard 7.116. Gizzard. Vitamin E/selenium deficiency myopathy.
turkey. Section of the nematode Disphmynx 11as11ta is in the lumen 2-week-old turkey. Myopathy is multifocal and regional and
of a proventricular gland . characterized by swelling and fragmentation of muscle fibers.

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7.117. Gizzard. Vitamin E/selenium deficiency myopathy. 7.119. Gizzard. Erosion of koilin. 2-week-old turkey. Hi gher-
2-week-old turkey. Higher-power view of 7 . 116. power view of 7. 11 8 showing breakdown of the koilin laye r and
infiltration of heterophil s between the mucosa[ epithelium and the
koilin layer.

7.118. Gizzard. Erosion of koilin. 2-week-old turkey. The 7.120. Gizzard. Erosion of koilin . 2-week-old turkey. Severe
koilin is fragmented and separated fro m the mucosa[ epitheli um of breakdown in region of the koi lin crea tes cavitation. The ca use was
the gizza rd. unknown.

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7. 12 1. Gizzard. Erosion of koilin. 2-week-old turkey. Higher-
po wer view of7 .120.
7.123. Gizzard. Copper toxicity. Few-day-old broiler. Loss
of integrity and fragmentation of the koilin. There is loss of the
superficial glandular mucosa , with many degenerate and necrotic
mucosa! epithelial being trapped within the koilin layer. (Glass
slide courtesy ofPou Illy Diagnostic and Research Ce11te1; Georgia,
USA).

7.122. Gizzard. Copper toxicity. 13.5-week-old turkey 7.124. Gizzard. Adenovirus infection. Quail. Large region of
breeder replacement hen. Fragmentation and loss of integrity of necrosis is in the mucosa.
the superficial layer of the koilin. Many degenerate and necrotic
mucosa! epithelial cells are trapped within the koilin layer.

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7.125. Gizzard. Adenovirus infection. Quail. Higher- 7.127. Gizzard. Adenovirns infection. Quail. Hi gher-power
power view of area in 7. 124 show ing necrosis with intral esional vi ew of area in 7 .126 showing necrosis w ith intranuclear inclusion
intranuclear, large, basophilic inclusion bodies characteri stic of bodies characteri stic of adenovirus infection.
adenovirus infection .

7.126. Gizzard. Adenovirus infection. Quail. Hig her-power 7.128. Gizzard. Avian encephalomyelitis. 14-day-old ch icken.
view of area in 7.125. Multiple nodular collections of lymphocytes in the gizza rd muscle
are characteristic of av ian encepha lomye litis.

312 I Ameri ca n Association of Avian Pat hol ogists

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7.129. Gizzard. Avian encephalomyelitis. 14-day-old chicken. 7.131. Gizzard. Proventricular dilatation disease. 4-month-old
Hi gher-power view of7 .128. conure. Higher-power view of area in 7.130 showing disruption of
the muscular later by mononuclear inflammatory infiltrates.

7. 130. Gizzard. Proventricular dilatation disease. 4-month-old 7.132. Gizzard. Proventricular dilatation disease. 4-month-old
conure. Low-power view showing infiltration of the muscular layer conure. Higher-power view of area in 7.131 showing mononuclear
of the gizzard by mononuclear inflammatory cells infiltrate is. inflammatory infiltrate in the gizzard muscle consisting of
lymphocytes, plasma cells, and macrophages .

Avian Histopathology (4 th Edition) I 313

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...
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7.133. Gizzard. Proventricular dilatation disease. 2-year-old 7.135. Gizzard. Candidiasis. 4-month-old finch. Many Candida
parrot. Lymphoplasmacytic infilt rate in the neuroganglion in the blastopores and pseudohyphae are in the koilin laye r. Note that
serosal surface of the gizza rd . clusters ofblastospo res are in vacuolar spaces and indi vidual spores
are surro unded by halo.

7.134. Gizzard. Candidiasis. 3-year-old finch. The koilin 7.136. Gizzard. Ca ndidiasis. 8-week-old finch. Candida
layer of the gizza rd is heavily colon ized by yeast (Candida sp.). pseudo hyphae and spores are in th e koi lin layer of the gizza rd.
Pseudohyphae and blastospores of the yeast are seen . C lusters of
blastopores occur w ithin vacuo lar spaces near the surface. Areas of
the superfi cia l mucosa ! epithelium appear di srupted .

3 14 I Amer ica n Association of Av ian Pathologists

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7.137. Gizzard. Candidiasis. 8-week-old finch. PAS stain 7.139. Gizzard. Candidiasis. 3-month-old Muscovy duck.
showing pseudohyphae and blastospores in th e koilin laye r. C luste rs of blastospores of Candida sp. are in clear spaces in the
koilin.

7. 138. Gizzard. Candidiasis. 3-month-old Muscovy duck. The 7.140. Gizzard. Candidiasis. 3-month-old Muscovy duck. The
koilin layer is disrupted and damaged from candid iasis. Many blastospores and pseudohyphae of Candida sp . stain positi ve with
intra les ional blastospores and pseudohyphae are prese nt. PAS stain.

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7.141. Nematode. Gizzard. 4-week-old turkey. Nematodes,
possibly Cheilo5pimra sp. are located in the mucosa beneath the
koilin layer.
7.142. Nematode. Gizzard. 4-week-old turkey. Higher-power
view of7.141.
316 I American Association of Avian Pathologists
7.143. Gizzard. Hadjelia tnmcata. Pigeon. Several sections oJ
nematodes identified as Hadjelia lmncala are located between the
g landular mucosa and the koilin layer, which is severely fragm ented
and vacuolated. The superficial mucosa appears disrupted, an d
gizza rd glands are distended with eosinophilic glandular secretion.
(Glass slide co11r/e5y of C. Gabriel Se11ties-C11e).
7.144. Gizzard. Hadjelia tr1111cata. Pigeon. Higher-power view
of area in 7. 143 showing sections of nematodes (Hadjelia tmncata)
between the glandular mucosa and the koilin layer, which is severely
disrupted. (Glass slide courtesy of C. Gabriel Senties-C11e).
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7.1 45. Gizzard. Hadjefia tnmcata. Pigeon. Same section as

7.143. Higher-power view showing sections of nematodes (Hadjelia
truncata) between the glandular mucosa and the koilin layer.
Gi zzard glands are dilated and filled with eosinophilic glandular
secretion. (Glass slide courtesy of C. Gabriel Senties-Cue).

7.147. Duodenum. Normal. 3-week-old turkey. Higher-power

view of area in 7.146 showing the tip of villus.

7.146. Duodenum. Normal. 3-week-old turkey. Normal

7.148. Small intestine. Compression of villi. 22-week-old
duodenum collected and fixed immediately after euthanasia shows
broiler. The villi show the effects of compression with accordion-
lon g villi relative to the short crypts.
like folds. Reduction in villi height secondary to compression is
difficult to differentiate from villous atrophy. The small intestine
was dilated grossly.

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7.149. Duodenum. Fenbendazole toxicity. Adult pigeon. Low- 7.151. Duodenum. Catarrhal enteritis. Turkey. Increased
power view showing dilation and necrosis of crypts. Postmortem numbers of vacuolated enterocytes (gob let ce ll s) are co nsistent with
changes prec luded optimal eva luation , but th ere appears to be catarrhal enteriti s.
increa se in mononu c lea r cells in the lamin a propria.

7.150. Duodenum. Fenbendazole toxicity. Adult pigeon. The 7.152. Duodenum. Catarrhal enteritis. Turkey. Hi gher-power
crypts are dilated and denuded of ep ithelia l cells and contain luminal view of area in 7 .15 1 showing increased numbers of gob let cell s on
cellular debris. villi.

318 I Ameri can Association of Avian Pathologists

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7.1 53. S mall intestine. Viral enteritis. Small intestine. 2-week-

olcl tu rkey. Villous atrophy, moderate ex pansion of the lamina
7.154. Small intestine. Viral enteritis. 2-week-olcl turkey.
Hi gher-power view of7.153 showing di stortion (blebbing) at tip of
I
propria by mononuclear cell infiltrate, and blebbing (arrow) of villus.
enterocytes at the tips of villi consistent with viral enteriti s, but are
not etiology spec ific.

7. 155. Small intestine. Aclenovirus infection. 17-week-olcl

quail. Large, basophilic inclusion is filling and enlarging the
nucl e us o f enterocyte. The morphology o f the inc lusion body is
typi ca l of adenovirus inclusions .

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7.156. Small intestine. Adenovirus infection. Turkey. 7.158. Small intestine. Poult enteritis complex. 2-week-old
lmmunoperox idase staining for avian adenovirus antigen is positive. turkey. Higher-power view of 7 . 15 7 showing villous atrophy and
loss of enterocytes from tips of villi.

7.157. Small intestine. Poult enteritis complex. 2-week-old 7.159. Small intestine. Viral enteritis. 8-week-old tu rkey.
turkey. The lesions include severe vi llous atrophy, hyperp lasia Villous atrophy is severe and the lamina propria is expanded with
of crypt ep ithe lium, and expansion of the lam ina propria by many vacuolated histiocytic cells.
lymphohistiocytic cells.

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7.1 60. Small intestine. Viral enteritis. 8-week-old turkey.
Higher-power view of 7. 159. Lesions are consistent with viral
etiology, but specific agents cannot be determined on the basis of
these changes.
7.161. Small intestine. Runting-stunting (malabsorption)
syndrome. 2-week-old broiler. Lesions include severe villous
atrophy, dilation of crypts, and expansion of the lamina propria by
mononuclear cell infiltrate.
Ali111e11ta1J' System
7.162. Small intestine. Runting-stunting (malabsorption)
syndrome. 2-week-old broiler. Higher-power view of 7.161
showing atrophic villi, dilated crypts, and expanded lamina propria.
The dilated crypts are lined by attenuated epithelium and contain
intraluminal cellular debris in the lumens.
7.163. Small intestine. Hemorrhagic enteritis. Turkey. The
lamina propria is expanded in multiple areas by hemorrhage.
Avian Histopathology (4 th Edition) I 321
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.
7.164. Small Intestine. Hemorrhagic Enteritis. Turkey. Higher- 7.166. Small intestine. Proventricular dilatation disease.
power view of area in 7 . 163 showing acute hemorrhage. 6-year-old eclectus parrot. See the legend of7. l 67.

7. I 65. Small intestine. Hemorrhagic enteritis. Turkey. Another 7.167. Small intestine. Proventricular dilatation disease.
Higher-power view of area in 7. 164 show ing lymphohistiocyti c 2-year-old parrot. This legend is also applied to 7. 166 . Infiltration
cells in lamina propri a with intranuclear inclusion bodies (box) . of the myenteric ga nglion with lymphocytes and plasma cells.

322 I American Assoc iat ion of Av ian Pathologists

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7.168. Jejunum/ileum. Attaching-effacing E. coli. 28-day- 7.170. Duodenum. Attaching-effacing E. coli. 37-day-old
old tu rkey. Pits (micro-erosions) in the mucosa! epithelium are turkey. Tissue Gram-stain shows heavy colonization of mucosa[
colonized by bacteria. Note the few heterophils in the lamina micro-erosions by Gram-negative bacteria.
propna.

7.1 69. Duodenum. Attaching-effacing E. coli. 10-week-old 7.171. Cecum. Attaching-effacing E. coli. 24-day-old turkey.
tu rkey. Pits (micro-erosions) in the mucosa[ epithelium are heavily The mucosa! surface of villi is eroded and colonized by numerous
colonized by bacterial. Note the many heterophils in the lamina bacteria. Note the heterophils in the lamina propria.
propria beneath the eroded mucosa.

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7.172. Cecum. Attaching-effacing £. coli. 24-day-old turkey. 7.174. Duodenum. E11terococc11s-associated enteritis. 20-day-
Higher-power view showing pits (micro-erosions) colonized by old turkey. Cocci bacteria are difficult to see at low magnifications
many bacteria (£. coli) in the mucosa! surface of villous. Such but are numerous and attached to enterocytes at tips and sides of
lesion should be interpreted in the context of clinical history. villi. Crypts are dilated.

7.173. Cecum. Attaching-effacing E. coli. 5-week-old turkey. 7.175. Duodenum. E11terococc11s-associated enteritis. 20-day-
Giemsa stain. Two pits in the mucosa[ surface are colonized by old turkey. Higher-power view of 7.174 showing cocci bacteria
bacteria (£. coli) . Note that the erosions do not appear to breach the assoc iated with enterocytes at the tip of villus.
basement membrane of the mucosa! epithelium.

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7.1 76. Duodenum. Enterococcus-associated enteritis. 20-day- 7.178. Small intestine. Necrotic enteritis. 4-week-old chicken.
old turkey. Higher-power view of area in 7.175 showing cocci Necrotic enteritis caused by Clostridium perfi·ingens is characterized
bacteria associated with enterocytes on sides of villus. by necrosis and hemorrhage extending downward from the tips of
villi.

I
..

7.177. Duodenum. E11terococc11s-associated enteritis. 20-day- 7.179. Small intestine. Necrotic enteritis. 4-week-old chicken.
old turkey. Gram stain reveals Gram positive cocci bacteria Higher-power view of 7.178 showing numerous bacterial colonies
associated with enterocytes. in the necrotic debris and several coccidial oocysts.

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,
7.180. Small intestine. Necrotic enteritis. 4-week-old chicken .
Hi g her-powe r view of area in 7.1 79 show in g surface necroti c debri s
w ith bacteri a and cocc idia l oocysts.
7.181. Small intestine. Ulcerative enteritis. Quail. Two mu cosa !
ulcers are seen. The ulcer on the rig ht side in vo lves th e entire depth
of the intestine wall (tran smural ul cer).
326 I A meri ca n Assoc iati on o f Av ian Patholog ists
7.182. S mall intestine. Ulcerative enteritis. Quail. Low-power
view showing mucosa ! ulcer in the small intestine.
7.183. Small intestine. Ulcerative enteritis. Quail. Hig her-
powe r view of the ul cer in 7. 182 . The necrotic mucosa is rep laced
by gra nular, acellular, dee pl y eosinophilic debris, w ith nume rous
bacteri a on the surface . The outer margin of the ulcer co nsists of
zone necroti c cell s fo ll owed by w ider band of mi xed inflamm atoty
ce lls. ln more chroni c cases, granulat io n ti ssue fo rm ati o n may be
seen at th e base of the ul cer.
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7.184. Cecum. Salmonellosis. 3-day-old turkey. The cecal lumen 7.186. Small intestine. Mycobacteriosis. 6.5-year-old quail.
is fill ed with necrotic debris (necrotic core). The cecal mucosa is Diffuse infiltration and expansion of the lamina propria and tunica
expanded by lymphohistiocytic infiltrates, and the inflammation muscularis by dense infiltrate of histiocytes.
extends into the muscularis.

7. 185. Cecum. Salmonellosis. 3-day-old turkey. Higher- 7.187. Small intestine. Mycobacteriosis. 6.5-year-old quail.
power view of 7. I 84 showing numerous bacterial colonies in the Higher-power view of 7. I 86 showing histiocytes with large pale
luminal necrotic debris. The mucosa is distorted by the extensive cytoplasm.
lymphohistiocytic cell infiltration .

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7.188. Small intestine. Mycobacteriosis. 6.5-year-old quail. 7.190. Cecum. Brnchyspira infection. Chicken. Higher-power
Acid-Fast (Fite) stain shows many bacteria within the lesion. view of?. I 89. (Image courtesy of H. l. Shivaprasad) .

I
I

7.189. Cecum. Brachyspirn infection. Chicken. Large numbers 7.191. Cecum. Brac/1yspira infection. Chicken. Higher-power
of spirochetes are assoc iated with the surface of enterocytes. (Image view of?. I 90. (Image courtesy of H. L. Shivaprasad).
courtesy of H. L. Shivaprasad) .

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7.192. Duodenum. Coccidiosis, Ei111eria acen//lli11a. Chicken.
Trophozoites of£. acen111/ina appear as basophilic granules within
the ap ical cytoplasm enterocytes. These trophozoites can be easily
differe ntiated from the nuclei but may be overlooked.
7.193. Duodenum. Coccidiosis, Eimeria ace1w1/i11a. Chicken.
Numerous endogenous stages of E. acerv11/i11a are in enterocytes
of villi.
Ali111e11tmy System
7.194. Duodenum. Coccidiosis, Ei111eria acerl'ltlina. Chicken.
Higher-power view of 7 .193 showing developmental stages of E.
acervulina in the cytoplasm of enterocytes. Zygotes/rnacrogametes
have characteristic peripheral granules. Oocysts have thick wall
and centrally located nuclei. Few trophozoites are also present and
appear as small basophilic bodies surrounded by halo.
7.195. Duodenum. Coccidiosis, Eimeria acerl'ltli11a. 36-day-
old broiler. The mucosa! epithelium appears to be replaced by
dense sheet of macrogamete/zygotes with characteristic peripheral
eosinophilic granules.
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7.196. Duodenum. Coccidiosis, Ei111eria acerv11li11a. 14-day- 7.198. Jejunum/ileum. Coccidiosis, Ei111eria necatrix. 6-month-
old broiler. The epithelium of villous is severely di srupted by olcl chicken. Hi gher-power view o f area in 7. 197 showing meronts
deve lopmenta l stages of E. acervulina. Seen are macrogametes/ containing merozo ites.
zygotes w ith cha racteri stic peripheral gra nul es, oocysts wi th thi ck
wa ll and central nucleus, and large baso phili c structures that were
interpreted to be microga metocytes containing mi croga metes .

7.197. Jejunum/ileum . Coccidiosis, Ei111eria 11ecatrix. 6-month-
old chicken. Clusters of meronts co nta ining many merozoites
are replac ing crypt and extendin g into the musculari s. C lusters of
mero nts effacing crypts in the deep mu cosa of small intestine are a
characteri sti c lesion of in fec ti on with £. nectarix.
7.199. Jejunum/ileum. Coccicliosis, Ei111eria 11ecatrix. 5-mon tb-
olcl broiler breeder pullet. Meronts of E. necatrix appea r to be
replac ing th e crypt epithelial cell s in the deep mucosa. The center
of th e crypt is fill ed w ith granul ocyti c leukocytes. TM: Tu nica
musc ul ari s.

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7. 200. Jejunum/ileum. Coccidiosis, Eimeria necatrix. 5-week-
old broiler breeder pullets. Area of effacement and replacement
of the deep mucosa by severe hemorrhage encircled by coccidial
meron ts and surrounded by mixed inflammatory infiltrate. Note the
extension of the lesions into the tunica muscularis.
7.201. Jejunum/ileum. Coccidiosis, Eimeria maxima. 5-week-
old broiler. Numerous developmental stages of Eimeria are in the
lamina propria .
AfimentmJ' System
7.202. Jejunum/ileum. Coccidiosis, Eimeria maxima. 5-week-
olcl broiler. Higher-power view of area in 7.201 showing Eimeria
developmental stages including zygotes with prominent eosinophilic
peripheral wall-forming granules .
7.203. Jejunum/ileum. Coccicliosis, Eimeria maxima. 5-week-
old broiler. Higher-power view of area in 7 .202. The location
of the coccidial developmental stages in the lamina propria is
characteristic of feature of infection with E. maxima.
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7.204. Jejunum/ileum . Coccidiosis, Eimeria maxima. 5-week- 7.206. Small intestine. Coccidiosis. Turkey. Higher-power view
old broiler. Higher-power view of area in 7 .203. Arrows : Zygotes. of area in 7.205 showing trophozoites (box) and zygote (arrow).
Other developmental stages are present and most are within
en terocytes.

7.205. Small intestine. Coccidiosis, Eimeria 111eleagri111itis. 7.207. Small intestine. Coccidiosis. Turkey. Macrogametes/
Turkey. Villi are shorter than normal, and there are many zygotes and oocysts of Ei111eria sp. are in epithelial cells of villi.
developmental stages of Ei111eria sp. in villous epi thelial cells. Macrogametes/zygotes have characteristic periphera l eosinophi lic
granules. The oocysts have thick wall and centrally located nu cleus.

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7.208. SmaH intestine. Coccidiosis, Ei111eria 111eleagri111itis.
Tu rkey. Epithelial cells of villi are heavily parasitized by coccidial
oocysts, which appear as sheet replacing the villous epithelium and
overly ing the lamina propria. The oocysts look well developed and
are about to be released from the epithelial cells.
7.209. Small intestine. Coccidiosis, Ei111eria 111eleagrimitis.
Turkey. Higher-power view of area in 7.208. The nuclei of
some epithelial cells can be recognized among the oocysts . The
lam ina propria is infiltrated with granulocytes and mononuclear
inflam matory cells.
Ali111e11tmJ>System
7.210. Small intestine (duodenum). Coccidiosis. Pigeon. The
mucosa! epithelium of villi is disrupted by many developmental
stages of Ei111eria sp. Eimeria labecme is the most frequently
occurring Eimeria in pigeons.
7.211. Cecum. Coccidiosis, Ei111eria tenella. Cecum. 6-week-
old chicken. Low-power view showing necrotic debris and blood
filling the lumen .
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7.212. Cecum. Coccidiosis, Eimeria te11e/la. 6-week-olcl chicken. 7.214. Cecum. Coccidiosis, Eimeria te11e/la. 6-week-old
Higher-power view of 7.211 showing di sruption of the mucosa by chicken. Higher-power view of area 7.2 13 showing the meronts,
hemorrhage and large numbers of deve lopmental stages (mostly within which are large numbers of merozoites.
meronts) of£. tenella in enterocytes and in th e lam ina propria.

7.213. Cecum. Coccidiosis, Eimeria te11e/la. 6-week-old 7.215. Cecum. Coccidiosis, Eimeria te11e/la. 34-clay-old broiler.
chicken. Hi gher-power view of area in 7 .212 showing large Developmental stages of£. tene/la are in the cytoplasm of crypt
meronts containing merozoites. epithelial cells.

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7.216. Cecum. Coccidiosis, Eimeria tenella. 47-day-old broiler.
The mucosa is severely disrupted by developmental stages of E.
tenel/a . Epithelial cells are parasitized by zygotes with characteristic
peripheral granules. Oocysts are in the lumens of crypts and are
shed into the cecal lumen, which is filled with blood admixed with
oocysts.
7.217. Cecum. Coccidiosis, Eimeria tenella. Crypts are dilated
and contain many coccidial oocysts. Few zygotes are also present.
Ali111e11ta1J1 System
7.218. Cecum . Coccidiosis, Ei111eria tenella. 47-day-old broiler.
The lumens of all the crypts in this field are filled with intact and
degenerating oocysts. Epithelial cells of c1ypts, especially the one
in the lower left corner, have zygotes and newly developed oocysts.
7.219. Cecum. Coccicliosis, Eimeria tenella. 38-day-old broiler.
Compressing the mucosa and filling the lumen of the cecum is
caseous debri s (cecal core) containing numerous oocysts of E.
tenella.
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7.220. Cecum. Coccidiosis, Eimeria tenella. 3-week-old broiler 7.222. Cecum. Coccidiosis, Eimeria tenella. 3-week-old broiler
breeder chicken. Cystic dilation of crypts is prominent and cluster breeder chicken. Hi gher-power view of area 7.22 1 showing
of oocysts are in submucosa. Lesions are co nsistent with chroni c degenerating oocysts in the submucosa l tissue.
cecal cocc idiosis.

7.221. Cecum. Coccidiosis, Eimeria tenella. 3-week-old broiler 7.223. Cecum. Coccidiosis. Pheasant. Many crypts are sbown
breeder chicken. Hi gher-power view of area in 7.220. in this field , and it appears that every sing le epithelial cells contains
developmental stages of Ei111eria sp.

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7.224. Cecum. Coccidiosis. Pheasant. Higher-power view
showing developmental stages of Eimeria sp. in the cytoplasm of
crypt epithelial cells. Different stages can be identified.
7.225. Cecum. Coccidiosis. Pheasant. Enterocytes in upper
portions of villi contain intracytoplasmic developmental stages of
Ei111eria sp. Multiple stages are seen.
Ali111e11tary System
7.226. Small intestine. Cryptosporidiosis caused by
Cryptosporidi11111 sp. 3-week-old turkey. Numerous small,
basophilic, ovoid to round bodies (cryptosporidia) are associated
with the brush border of the villi.
7.227. Small intestine. Cryptosporidiosis caused by
C1J1plosporidi11111 sp. 4-week-old quail. Many small, basophilic,
ovoid to round bodies (Cryptosporidia) are associated with the
brush border of the villi. Cryptosporidiosis may cause very high
mortality in young quail.
Avian Histopathology (4th Edition) I 337
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7.228. Small intestine. Cryptosporidiosis caused by 7.230. Cecum. Histomoniasis. 4-week-old turkey. Higher-power
CIJ 1JJlosporidi11111 sp. 39-day-old turkey. Higher-power view view of area in 7 .229 showing marked mononuclear inflammatory
showing the association of the cryptosporidia with the brush border infiltrates and numerous trophozo ites ofHisto111011as in the mucosa!
ofvillous. Cryptosporidia resides within host cell-derived vacuoles lamina propria .
(parasitophorous vacuoles), and thus they are intracellular but
extracytoplasmic. The parasitophorous vacuole is connected to the
host cell, rather than residing within the cytoplasm.

7.229. Cecum. Histomoniasis. 4-week-old turkey. Marked 7.23 l. Cecum. Histomoniasis. 4-week-old turkey. Higher-power
expansion of the lamina propria, submucosa, and tunica muscularis view of area in 7.230 demonstrates mononuclear inflammatory
by mononuclear inflammatory infiltrate and numerous organisms infiltrates and many trophozoites of Histo111011as in the submucosa
morphologically consistent with trophozoites of Histo111011as . and tunica musculari s.

338 I American Association of Avian Pathologists

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7.232 . Cec um. Histomoniasis. 4-week-old turkey. Higher- 7.234. Cecum. Tetmtric/10111011iasis. 9-week-old turkey. Hi gher-
power view of area in 7 .23 1 showing mon on uclea r inflammatory power view of th e crypts in 7.233 show ing flagellated protozoa in
infiltrates and trophozoites of Histo111011as in the tunica muscul ar is. the lumens of crypts.
In we ll-fi xed ti ssues, the trophozo ites a ppea r as round bodies w ith
single, centra ll y located nuc leus. Note the clea r space (halo) around
the trophozo ites.

7.23 3. Cecum. Tetmtricho111011iasis. 9-week-old turkey. 7.235. Small intestine. Cochlosomiasis. Turkey. Low-power
N um erous flagellated protozoa are in cecum crypts. The protozoa view showing shortening of villi. The ca usative protozoan is
are ass um ed to be tri chomonads, poss ibl y Tetmlricho111011as (former Cochloso111a analis.
name: Tricho111011as). This usuall y is incidental finding of uncerta in
diagnost ic significa nce.

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7.236. Small intestine. Cochlosomiasis. Turkey. Numerous
organisms morphologically consistent with protozoa are on the
surface of villi. Based on the morphology and location, the
protozoan was identifi ed as Cochlosoma anatis.
7.237. Small intestine. Cochlosomiasis. Turkey. Numerous
protozoa, identified as Cochlosoma anatis , are between villi and in
the lumen. C. anatis has flattened or concave region consistent with
adhes ive di sc. Note also the tiny round bodies associated with the
brush border; these are C,yptosporidi11111 organisms.
340 I American Association of Avian Pathologists
7.238. Jejunum/ileum. Spironucleosis. 17-week-old qua il.
Scanning view of jejunum/ ileum showin g marked atrophy of the
villi . The causative protozoan is Spiron11cle11s meleagridis . The
former name of the protozoan is Hexamita meleagridis , and the
former name of the di sease is hexa mitiasis.
7.239. Jejunum/ileum. Spironucleosis. 17-week-old qua il.
Atrophy of villi and expansion of the lamina propria by inflammatory
infiltrates.

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7.240. Jejunum/ileum. Spironucleosis. 17-week-old quail.
The lumens of crypts are filled with organisms morphologically
consistent with fla ge llated protozoa. The morphology and location
of the protozoa are consistent with infection with Spiro1111cle11s
111e/eagridis. The inflammatory infiltrate in th e lamina propria
consists of lymphocytes and plasma cells, many of which have
eosinophilic intracytoplasmic Russell bodies.
7.241. Jejunum/ileum. Spironucleosis. 17-week-old quail.
The lumens of crypts are filled with organisms morphologically
co nsistent with flagellated protozoa. The morphology and location
of the protozoa are consistent with infection with Spiro1111cle11s
111e/eagridis. Note the marked lymphoplasmacytic infiltrate in the
lamina propria.
Ali111e11ta1J1System
7.242. Small intestine. Capillariasis. 43-week-old broiler
breeder chicken. Several sections of Capi!laria sp. are embedded
in the mucosa. Their location within the mucosa is characteristic of
Capi!laria sp.
7.243. Small intestine. Capillariasis. Pigeon. Several sections
of small nematodes and their eggs are within the mucosa . The size
and location of the nematodes are consistent with Capillaria sp.
Developmental stages of Eimeria sp. are present in epithelial cells
of villi .
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7.244. Small intestine. Capillariasis. Pigeon. Higher-power
view of area in 7.243 showing sections of Capillaria sp. and their
eggs in the mucosa. Capillaria eggs have characteristic bipolar caps.
Note the developmental stages of Eimeria sp. in the epithelium of
villi, especially in th e villous on the left side of the image .
7.246. Small intestine. Ascaridia larvae. 16-week-old broiler
breeder pullets. Several cross sections of Ascaridia galli are in
the mucosa.

7.245. Small intestine. Ascaridia larvae. 8-week-old turkey. 7.247. Small in testine. Ascaridia larvae. 16-week-olcl broiler
Sections of Ascaridia dissimilis larvae are in the mucosa. Note the breeder pullets. Longitudinal sect ion of Ascaridia galli is in the
lateral alae in the cross section of two larvae. There is extensive mucosa.
vacuolation of enterocytes.

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7.248. Small intestine. Ascaridia larva e. Pigeon. Section of
Ascaridia co/11111bae within the mucosa. Note the lateral alae, lateral
cords and the centrall y located intestine.
7.249. Small intestine. Ascaridiasis. 13-month-old backyard
chicken. Several sections of adu lt Ascaridia galli are in the lumen
of the intestine.
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1"1.-_
7.250. Small intestine. Adult ascarid. 4-month-old backyard
chicken. Adult Ascaridia galli is in the lumen of the small intestine.
Note the cords, coelomyarian musculature, and the intestine lined
with columnar cells with brush border and basally located nuclei.
7.251. Cecum. Hetemkis galli1wr11111 infection. 28-week-old
broiler breeder chicken. Numerous sections of the nematode
Heterakis galli11aru111 are in the mucosa and the lumen. Note the
latera l alae. The lamina propria is markedly ex panded by lymphoid
cell s. Although true tissue phase has been reported not been reported
to occur in the life cycle of Heterakis, adult and larvae may be seen
with in the mucosa.
Avian Histopathology (4 11, Edition) I 343
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7.252. Cecum. Heterakis gal/ill(trm11 infection. 28-week-old 7.254. Cecum. Hetemkis isolonclte. 2-year-old pheasant.
broiler breeder chicken. Higher-power view of two sections of Hi gher-power view of the nodule in 7.253. The nodul e is composed
Heterakis in 7.251. Note the lateral cords and alae. of histiocytes.

7.253. Cecum. Hetemkis isolonclte infection. 2-year-old
pheasant. The mucosa is markedly elevated by well-orga ni zed
cellular nodule containing sections of nematodes.
7.255. Cecum. Heterakis isolonclte infection. Pheasan t.
Between the mucosa and tunica musc ularis is dense collection
of epithelioid histiocytes with abundant eosinophilic cytoplas m.
Within the nodule is section of nematode (Heterakis iso/011c/1e) .
Another nematode section is within depression in the mu cosa!
surface.

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.
7.256. Cecum. Hetemkis isolo11clte infection. 2-year-old 7.258. Small intestine. Cestodiasis. Small intestine. Broiler.
pheasant. Remarkably expanding the submucosa and extending into Large segmented cestode (tapeworm) with characteristic segments
the tunica muscularis is dense collection of epithelioid histiocytes, and calcareous corpuscles is in the lumen of small intestine.
within which sections of nematodes (Heterakis isolonche) are seen.
There is loss of the mucosa! epithelium .

7. 257. Cecum. Heterakis isolonclte infection. 2-year-old 7.259. Duodenum. Cestodiasis. 6-month-old backyard
pheasant. Higher-power view showing the morphology of chicken. Segments of tapeworms are embedded in the mucosa .
epithelioid histiocytes in the nodules in 7 .256. The cells are large These duodenal tapeworms are very small and can be overlooked
and have abundant, eosinophilic, somewhat fibrillar cytoplasm. On on necropsy. Note the segmented appearance of worms.
close examination, the lesion appears to consist of multiple small
collections of cells that coalesce to form the large nodule. Note the
section of H. iso/onche at the bottom margin.

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7.260. Duodenum. Cestodiasis. Backyard chicken. Parasitic
worms with morphologic features consistent with tapeworms are in
the mucosa of duodenum.
7.261. Duodenum. Cestodiasis. 2.5-year-old backyard chicken.
The head seg ment of tapeworm is embedded in the mucosa. This
small segment may be overlooked on histological examination of
th e section. The tapeworm was identified as Davainea proglottina.
346 / American Association of Avian Pathologists
7.262. Jejunum/i leum. Cestodiasis. Adult backyard chicken.
Nodular gran ulomatous lesion is in the tunica mu scular of th e small
intestine. Portion of cestode is in the center of the les ion. Caseo us
debris is around th e parasite. This is a characteristic les ion caused
by Rallietina echinobothrida .
7.263. Jejunum/ileum. Cestodiasis. Adult backyard chicke n.
Nodular fibro-granulomatous lesion and caseous debris are in the
tunica muscular of the sma ll intestine. Part ofcestode is in the ce nter
of the lesion. This is a characteristic lesion caused by Ral!ieti11a
echinobothrida.

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7.264. Jejunum/ileum. Cestodiasis. Adult backyard chicken.
Hi gher-power view of the lesion in 7.263.
7.265. Jejunum/ileum. Cestodiasis. Adult backyard chicken.
Rallietina echi11obothrida extends from the lumen into the muscular
layer and causes marked fibro-granulomatous lesion. There is also
adjacent area of caseous necrosis.
Ali111e11fmJ' System
7.266. Jejunum/ileum. Cestodiasis. Adult backyard chicken.
Fibro-granulomatous and caseo-granulomatous lesions are in
the hmica muscularis. Cestodes (Rallietina ec/1i11obothrida) are
not present in the caseous granulomas. The empty spaces most
likely contained parts of cestodes that were lost during trimming/
processing of the ti ss ue . Two sections of cestodes are seen in one
area.
7.267. Jejunum/ileum. Schistosomiasis. Swan. Round
struchires morphologically consistent with sch istosome eggs are in
the mucosa, which has significant postmortem autolysis.
Avian Histopathology (4 th Edition) I 347
 Oscar J. Fletcher • Tahsee11 Abdul-Aziz
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....

.I

7.268. Cloaca. Normal. 27-week-old broiler breeder chicken. 7.270. Cloaca. Cloacitis. 35-week-olcl broiler breeder hen
Scanning view showing the vent Uust above the vertical box), Focal area of ulceration and necrosis, with large numbers o-
the proctodeum with the dorsal region outlined (horizontal box), heterophils in the necrotic area and serofibrinous exudate admixec
urodeum (vertical box), and ureter (circle). with heterophils in the submucosa.

7.269. Cloaca. Normal. 27-week-old broiler breeder chicken. 7.271. Cloaca. Cloacitis. 35-week-olcl broiler breeder hen.
Hi gher-power view of the dorsa l proctodeum showing the deep Most of the cloaca! mucosa! epithelium is lost, and there is extensive
branched glands and normal lymphoid tissue. hemorrhage and fibrin exudation in the area.

348 I American Association of Avian Pathologi sts

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7.272 . Cloaca. Cloacitis. 32-week-old broiler breeder hen. 7.274. Cloaca. C/oacotaenia mega/ops. Adult swan. Cestode,
Severe necrosis and loss of the mucosa is associated with marked identified as C/oacotaenia mega/ops, is attached to the " lip" of the
exudative and infiltrative inflammatory reaction in the wall of the cloaca .
cloaca .

7.273. Cloaca. Cloacitis. 32-week-old broiler breeder hen. 7.275. Cloaca. C/oacotaenia mega/ops. Adult swan. Higher-
Hi gh-power view of area in 7 .272 showing the intense inflammatory power view of7 .274.
infiltrate that includes dense population ofheterophils and numerous
mononuclear inflammatory cells, with exudation of fibrin .

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7.276. Proventriculus. Marek's disease. Chicken. Expansion 7.278. Proventriculus. Marek's disease. 6-month--old backya n
of the outer muscular layer and the serosa of the proventriculus by chicken. Proventricular glands are effaced and replaced by dens<
dense infiltrate of lymphoid cells. infiltrate of pleomorphic lymphoid cells. Glandul ar duct is in th1
lower right corner.

7.277. Proventriculus. Marek's disease. One-year-old 7.279. Proventriculus. Marek's disease. Chicken. Hi gher-
backyard chicken. Proventricular gland- lobule is infiltrated by power view of the lymphoid infiltrates in 7.277. The lymphoid
dense population of pleornorphic lymphoid cells that efface and infiltrates appear pleomorphic and comprised mostly of small - and
replace the glands. The infiltrates are composed of mostly sma ll- medium-sized lymphocytes.
and medium-sized lymphocytes.

350 / American Association of Av ian Pathologists

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7.280. Proventriculus. M ucosal carcinoma. Chicken. 7.282. Proventriculus. Mucosal carcinoma. Chicken. Higher-
Adenoca rcinoma is infiltrating and expandi ng the submucosa at the power view of area in 2.28 1 wi th nests and cords of neoplastic
proventriculus-gizza rd junction . The mucosa is ulcerated. epitheli al cells.

7.281. Proventriculus. Mucosal carcinom a. Chicken. Higher- 7.283. Proventriculu s. Mucosal carcinoma. Chicken. Higher-
Jower view of area in 7.280 showing ul ceration of mucosa with power view of the submucosal adenocarcinoma in 7.28 I showing
iclenocarcinoma in the submucosa. region wi th neoplastic cells for ming glandular and ductal structures.

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7.284. Proventriculus. Mucosa! carcinoma. Chicken. Hi gher-
power view of the ade nocarci noma in 7 .282.
7.285. Duodenum. Adenocarcinoma of reproductive tract
origin. Chicken. Multiple variable sized nodular collectio ns of
neop last ic epithelial cells (arrows) expand the serosa and infiltrate
the muscu laris of the duodenum .
352 I American Association of Av ian Pathologists
7.286. Duodenum. Aclenocarcinoma of reproductive tract
origin. Chicken. Higher-power view of the neoplas m in 7.28 5.
7.287. Hemangiosarcoma. Small intestine. Chicken. Neopl ast ic
tissue composed of cavernous spaces filled with blood and
proliferating endothelial cells is contiguou s with the serosa l sur face
of the small intesti ne. This bird had metastatic hemangiosarcoma in
d ifferent organs.
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7.288. Hemangiosarcoma. Small intestine. Chicken. Higher- 7.290. Cloaca. Cloacal papilloma. 30-year-old macaw. See the
power view of area in 7.287. legend of7 .291.

7.289. Cloaca. Cloacal papilloma. 26-year-old macaw. The 7.291. Cloaca. Cloacal papilloma. 30-year-old macaw. This
mucosa is thrown into frond-like projections. legend is also applied to 7.290. The frond-like mucosa[ projections
have fibrovascular core and are lined by pseudostratiified columnar
epithelium.

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7.292. Cloaca. Cloaca) papilloma. 30-year-old macaw. Higher- 7.294. Cloaca. Cloaca! papilloma. 26-year-olcl macaw. Th is
power view of the pseudostratified co lumnar epithelium lining the legend is also applied to 7.293. In this area , the epitheliu m li ning
frond-like mucosa! proj ections. Note the fibrovascular core. the mucosa! projections appea rs as sheet- li ke layer of cells. Note
the fibrovascular core of the projections.

7.293 . Cloaca. Cloaca! papilloma. 26-yea r-olcl macaw. See the

legend of7 .294 .

354 I American Association of Avian Pathologists

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CHAPTER
Hepatobiliary System
Tahseen Abdul-Aziz • Oscar J. Fletcher
Histology
The hepatobiliary system consists of the liver, gallbladder, and bile
du cts. The liver in birds has two lobes, right and left. The anterior
part of each lobe surrounds the apex of the heart. The left lobe
in chickens and turkeys is subdivided into a lateral and a medial
part. The right lobe carries the gallbladder, in those avian species
that have a gallbladder, in its dorsal surface, and this lobe is perfo-
rated by the caudal vena cava. There are variations in the shape of
the liver among different species of birds. Each lobe of the liver is
drained by a separate bile duct, and the two ducts are joined on the
vi sceral surface of the right lobe to form the hepatoenteric duct. The
hepatic duct from the right lobe gives a branch to the gallbladder.
The cysticoenteric duct drains the gallbladder. The hepatoenteric
and cysticoenteric ducts open into the distal part of the ascending
limb of duodenum close to the pancreatic ducts . The pigeon has
no gallbladder, and the right and left hepatoenteric ducts (one from
each lobe) open into the duodenum; the right duct empties into the
ascending limb of the duodenum, while the larger left duct empties
into the descending limb. Also, no gallbladder is found in ostriches
and so me parrots. The major bile pigment is biliverdin (most mam-
mals produce bilirubin).
The outer surface of the liver is composed of a thin layer of
dense connective tissue termed the liver capsule that is covered by a
peritoneal layer of flattened mesothelial cells. The avian liver lacks
th e true lobular structure of the mammalian liver because it lacks
interlobular septa . Hepatocytes are arranged in plates that are two
ce ll s thick in many avian species including chickens and turkeys.
Bile canaliculi are located between adjacent hepatocytes - the bile
side of the hepatocytes. Between the hepatic plates are sinusoids
- the vascular side of the hepatocytes. ln histologic sections, the
avian liver appears as a mass of hepatocyte plates between which
are the sinusoids . In some sections, plate formation is not appar-
ent and hepatocytes appear as groups of roughly triangular cells ar-
ranged around bile canaliculi. A discontinuous layer of endothelial
cells and larger, irregular, phagocytic cells called Kupffer cells that
are not always discernible in histologic sections line sinusoids. The
zone between the sinusoidal endothelium and hepatocytes is the
space of Disse that is not apparent histologically. Hepatic stellate
cells, also referred to as Ito cells or fat-storing cells, constitute a
smaller population of perisinusoidal cells.
The portal vein, which drains visceral organs, enters the liver
and terminates in an anastomosing network of sinusoids that drain
into the intralobular branches of the hepatic vein (terminal hepatic
8
venule or centrilobular venule - central vein in older literature).
Each portal tract contains a relatively large interlobular branch of
the portal vein (terminal portal venules), interlobular branches of
the hepatic artery, and bile ductules. Blood flows from the hepatic
artery and portal vein in the portal tracts to the terminal hepatic ven-
ule (central vein). Bile flows from the central vein area through
bile canaliculi to the portal ductules and eventually the bile ducts.
The pattern of microcirculation is the basis of the acinus concept
of hepatic histology. In the acinus concept, the portal tracts are at
the center and hepatic plates radiate to the terminal hepatic venules
(classical central veins) . Zones ofhepatocytes are recognized with
zone 1 being closest to the portal tract, zone 3 being closest to the
terminal hepatic venule, and zone 2 between zones 1 and 3. The
classical lobule concept of hepatic histology places the central vein
(terminal hepatic venule) at the center with the hepatic plates radiat-
I
ing to the portal areas. The lobule model is the foundation for the
terms centrilobular and peripo11al.
Small, usually well-circumscribed nodular aggregates of lym-
phoid cells are occasionally found in the liver and should be consid-
ered normal. They can occur in the walls of blood vessels and proj-
ect into the lumen. It is impo11ant to differentiate normal aggregates
of lymphoid cells from neoplasia . Also, there may be focal areas
of extramedullary hematopoiesis (EMH), especially around blood
vessels and in portal areas. EMH is often common and prominent
in the livers of pigeons.
Collecting Liver Samples for Histopathology
Avian liver is dense; formalin does not diffuse quickly through it.
It is important that pieces collected for histopathologic examina-
tion should not exceed 0.75 cm in thickness. Slices about 0.5 cm
in thickness are good samples for quick fixation. Samples need to
be obtained from different areas of both lobules and placed imme-
diately into 10% buffered formalii1 solution. Warming the formalin
solution will hasten fixation. In birds that have been dead for a
while, avoid collecting samples from the area in contact with the
gallbladder as diffusion of bile through the wall of the gallbladder
after death lyses the hepatic tissue. Pathologists need to be famil-
iar with different changes caused by postmortem autolysis and poor
fixation and be able to differentiate these changes from antemor-
tem lesions. Early postmortem changes include individualization,
slu·inkage, rounding, and increased cytoplasmic eosinophilia of he-
patocytes. Nuclear changes can resemble inclusion bodies. Mucosa
of the gallbladder rapidly decomposes after a bird dies.
Avian Histopathology (4' 11 Edition) I 355
 Tahsee11 Abdul-A ziz • Oscar J. Fletcher
Ascites and Hypoxic Injury
In crease in the thickness of the liver capsul e is a common les io n in
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birds with ascites (accumul ati o n of fluid in perito neal cavities). T he
increased thi ckness is ca used by proli fe rati o n of peritoneal meso-
theli al cells o n the sur face of the li ver capsul e, w hich results in fo r-
matio n of a layer of spindle-shaped cells with intercellular spaces.
Careful exa mination of the ce llular layer reveals points of attach-
ment to the underly ing capsule.
Hypoxic injury to hepatocytes, such as occurs in pulmonary
hypertension-ascites syndrome in broilers, is characteri zed hi sto-
log icall y by patchy or bridg in g coagulative hepatocellular necrosis
that mainl y involves hepatocytes around te rminal hepati c ve nul es
(centra l ve in). Varying degrees of sinusoidal fibro sis is ev ident in
some cases.
Kupffer Cell Hypertrophy and Hyperplasia
and Bile Ductular Hyperplasia
Hype1troph y and hyperplas ia ofKupffer cells is a common response
to hepatic injury. Mi crog ranul omas ofKupffe r cells al so are a non-
spec ific les io n found in va ri o us pathol ogical conditions. Vari ab le
amounts of hemosiderin pigment are ofte n found in these mi cro-
gra nul omas. Presence o f hemosiderin in the g ranulomas suggests
iron-containing inju red hepatocytes have been phagocyti zed by the
Kupffe r ce lls.
Pro li fe rati on of bile du ctul es in portal tracts also is a no n- specif-
ic les ion in response to injury of the hepatic parenchyma. Althoug h
bile ductular hyperplasia often consists of a modest dupli ca ti on of
I
normally appearing bile ductules, other evidence of cluctul ar hyper-
plasia includes sprouting o f preexisting cluctules and to rtuosity of
elongated cluctules. In areas with marked bile ductular hyperpl as ia,
small proliferating bile cluctul es may have small, barely di scernible
lumens. Bile cluctular hyperplas ia usu ally is accompanied by other
lesio ns such as degenerati on and necrosis of he patocytes and vary-
ing degrees of fibropl as ia. Bil e cluctul ar hyperplasia is a comm on
findin g in chronic toxic injury, especiall y w hen ca used by certain
mycotox ins particularl y afl atoxin.
Hemosiderosis and Iron-Storage Disease
Hepati c hemosiderosis is characteri zed by acc umulation of go lden-
yellow to go lden-brown granules or g lobules in the cyto plasm of
hepatocytes and K upffer cells. In cell s, iron is usuall y stored as
ferritin , a protein-iron complex, but when large amounts of fe rritin
are present; aggregates of fe rritin called hemosiclerin are fo rmed.
Hemosiderin accumulates in the liver w hen th ere is a systemi c
increase in iron level, such as when brea kdown of erythrocytes is
excessive as occ urs in hemolytic anemi a . T he term " hepatic hemo-
siderosis" is used to denote a relatively benign accumulatio n o f iron
in hepatocytes and Kupffer cells. " Hepati c hemochromatos is" and
" hepati c iron storage di sease" are term s th at have been used inter-
changea bl y to refer to excessive accumul ati o n of iron resulting fro m
cell injury, organ dysfun cti on, and clinica l di sease in mynah birds
and to uca ns. Hepatic iron storage di sease is the preferred term be-
cause hemoclu-omatosis has a genetic basis in oth er animal species,
whi ch has not been proven fo r birds. Iro n in excessive amo unts is
tox ic to cell s, and can ca use hepatic necrosis with fibro sis in severe
356 I Ameri ca n Associati on of Av ian Path ologists
cases . Hemosiclerin stains purple with Prussian blue stain . Scat-
tered dense aggregates of hemosiderin gra nul es w ithout assoc iati on
w ith di sease and for un known rea sons are often seen in li vers of pet
birds. These aggregates likely represe nt collections ofKupffer ce lls
that are so heav ily laden with hemosiclerin that it is impossible to
identi fy individual cells. Some avian species, especiall y waterfow l,
have re lati vely large amounts of iron in hepatocytes in the abse nce
of ev idence of di sease.
Amyloidosis
Deposition of an eos inophilic, fibrill ar or ho mogenou s, hya line-li ke
material is characteri stic of amy loid de pos ition in the liver (hepati c
am ylo iclosis). A my lo idosis is a well-recogni zed path ologica l dis-
order in birds, especiall y clucks , swans, and flamin gos. A my loid
A (AA ) is the form of amyloicl th at is recogni zed in birds. A my-
loicl A is derived from an acute-phase reactive protein ca lled serum
amy loid A (SAA) that is synthe sized in th e liver. Serum amyloid A
is produced in excess in response to chronic antigenic stimulat ion.
SAA is normally co mpl ete ly degraded, but in amyloidosis th ere is
incomplete break.clown, w hi ch results in depositio n o f an insolu ble
fragment of the am yloid-associated (a myloid A) prote in . A lthough
amy loiclosis in birds is known to occ ur seco ndarily to chroni c in-
flamm atory processes, it also may be idiopathic where no under ly-
ing inflammatory conditi on is found . He patic amylo idosis, necro-
sis, and hemorrhages have been reported in chi ckens w ithin a few
wee ks of fo llowing co-administration of di ffe rent oil-emul sion vac-
cines . Am yloicl depos its in sinusoidal spaces cause compress ion,
atroph y, and effa cement of hepato cytes th at in severe cases ca n lead
to he patic failure. Co ngo reel stain is used to differenti ate amyloi cl
fro m fibrin and other extracellular, ace llular eosinophilic material.
Amy loicl stains pale-red to orange w ith Co ngo red dye and ex hi bits
app le-g reen birefrin gence when vi ewed under polari zed li g ht. In-
creas in g the li g ht intensity o n the mi cro scope helps identi fy amyloid
when polari zed li g ht is used.
Urate Deposition
Deposition of urate crysta ls on the ca psular surface of th e li ver
occurs in severe cases of visceral gout, usually due to renal fa il-
ure. Urates are di ssolved in water during fi xation in fo rmalin solu-
tion. They can be preserved by fi xing ti ssues in absolute a lcohol
and using special stains th at do not require ti ssue hydration . Oc-
casionally, focal m ate deposits are sca ttered throughout the hepat ic
parenchyma . Urate crystals injure hepatocytes leading to foci of
necrosis th at contain the characteri sti c radi atin g basoph ilic, fi brillar
or feathery-looking casts remainin g after the needle-sha ped crysta ls
have di ssolved . U rate depos its in vesse l walls may accompany fo-
cal necrosis . Some urate deposits may be surrounded by g iant cells
and hi sti ocytes and thu s co nstitute tophi .
Fatty Liver
Hepatocellular fatty vac uo lation or dege neration of he patocytes re-
fers to the excessi ve acc umulation of globules of tri glycerides and
oth er lipid metabo lites within the cyto plas m of hepatocytes . T hese
changes may be termed fa tty li ver, hepati c lipidosis, or hepati c ste-
atosis. Beca use lipid is clisso lvecl durin g the process ing of ti ssues by

para ffi n-embedding procedures, the lipid vacuoles appear as empty
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spaces in the cytoplasm of hepatocytes. Macrovesicular steatosis
refers to the accumulation of variably sized, single, round , well-de-
fined , smoothly contoured vacuoles that displace the nucleus. Large
multi cellular fat vacuoles result when walls of heavily laden cells
breakdown and fat vacuoles coalesce. Microvesicular steatosis re-
fers to the accumulation of multiple, vaguely defined vacuoles with-
in the cytoplasm, without displacement of the nucleus. Both types
of vacuolation may be seen in the liver. Hepatocytes overloaded
with lipid undergo necrosis. In birds, excessive lipid accumulation
in hepatocytes is usually due to high dietary fat , poor utilization of
fee d, or hepatocellular injury.
Young (few-day-old) chickens and turkeys normally have
large amo unts of fat in the liver that was transported from the yolk.
Fatty liver-hemorrhagic syndrome in chickens and hepatic lipidosis
in turkeys are two diseases in which the primary lesion is exces-
sive accumulation of lipid in hepatocytes, which results in necrosis
of hepatocytes and sometimes hemorrhage. In turkeys with he-
patic lipidosis, there may be massive hepatocellular necrosis, with
marked hemorrhages and bile ductule hyperplasia. Fatty livers are
seen in pet birds consuming hig h-energy diets or with a metabolic
di sturbance, and variable degrees of fibrosis are usually associated
with chronic lipidosis.
Toxicities
Among the toxins that produce lesions in the liver are certain my-
cotoxins, heavy metals, and plants. Lesions in the liver of chickens
with aflatoxicosis include fatty vacuolation and necrosis of hepato-
cytes, karyomegaly with prominent nucleoli, bile ductule hyperpla-
sia, fibrosis, and occasionally p01ial heterophilic and mononuclear
cell infiltration. Basophilic, regenerative, karyomegalic hepatocytes
may be present. Nodules of regenerative hepatocytes notably occur
in aflatoxicosis of turkeys. Ochratoxin causes rarefaction and non-
vesicular vacuolation of the cytoplasm of hepatocytes due to ex-
cess ive accumulation of glycogen. Pyrrolizidine alkaloid toxicosis
produces liver lesions similar to those caused by aflatoxins. Seeds
of crotalaria contain pyrrolizidine alkaloids that cause fatty vacu-
olation of hepatocytes, marked bile ductule proliferation, and fibro-
sis. Early lesions of rapeseed toxicosis include foci of hemorrhage
and necrosis, followed by extensive centrilobular fibrosis and bile
du ctule hyperplasia . Birds dying of lead toxicosis usually have ex-
cess ive accumulations of hemosiderin pigment in hepatocytes and
Kupffer cells. Organic arsenic intoxication is characterized by nec-
roti zing intrahepatic cholangitis. The large bile ducts are distended
and may have transmural necrosis with leakage of bile and necrosis
of adjacent hepatocellular parenchyma. With time, the intrahepatic
ducts may be dilated with marked hyperplasia of the lining epithe-
lium . Periportal bile ductule proliferation also may occur.
Iatrogenic Granulomas
Iatrogenic granulomas may form in the liver following misapplica-
tion of injected oil-adjuvant vaccines. Injections of vaccine that
are too deep may enter the coelomic space and involve the liver,
inciting granulomatous inflammation, with canalicular and ductular
bi le stasis.
Hepatobili£11J' System
Infections
Viral infections
Hepatocellular degeneration and necrosis are often very acute with
minimal inflanmrntory cell infiltrate in viral infections involving the
liver. Viral infections also may cause significant inflammation with
mixed inflammatory cell infiltrates that include heterophils, imma-
ture granulocytes, and lymphocytes . Kupffer cells may be enlarged
and bile ductules show hyperplasia as part of the general response
to hepatic injury. Degeneration and coagulative hepatocellular ne-
crosis with or without inclusion bodies in hepatocytes are common
lesions in viral-induced hepatitis. Identity of the causative virus
may be tentatively or even accurately determined, by the appearance
of inclusion bodies.
Inclusion body hepatitis of chickens is a classic example of
viral- induced (Aviadenovirus, formally avian adenovirus Group
I) hepatic injury with diagnostic intranuclear inclusions in hepa -
tocytes. Adenovirus inclusions are deeply basophilic and fill the
entire nucleus, which is usually enlarged (karyomegaly). Adeno-
virus inclusions also can be eosinophilic and surrounded by a halo
making them difficult or impossible to differentiate from inclusions
of herpesviruses. Herpesviruses cause eosinophilic intranuclear in-
clusion bodies that tend to be small. Nuclear chromatin is usually
located at the periphery of the nucleus creating the appearance of
a halo around the viral inclusion . Duck viral enteritis in water-
fowl , herpes virus infection in pigeons, and Pacheco 's disease in
psittacines are examples ofherpesviral infections with intranuclear
inclusions in hepatocytes.
Viral infections that cause hepatic necrosis, mixed cell inflam-
matory response, and intranuclear inclusions in hepatocytes include,
in addition to those mentioned above, adenovirus hepatitis of gos-
lings, pigeons, pheasants, and, in some cases, turkeys (Aviadenovi-
rus, not Siadenovirus, the cause of hemorrhagic enteritis) and her-
pesvirus infections in falcons, owls, and other raptors. In duck viral
hepatitis, acute liver lesions consist of hepatocellular degeneration
and necrosis, with varying degrees of inflammato1y cell response
and hemorrhage, but no inclusion bodies are found . In parvovirus
infections of goslings (Derzsy 's disease), there is widespread vacu-
olation and degeneration of hepatocytes, with small eosinophilic,
intracytoplasmic inclusion-like bodies occasionally seen in degen-
erating hepatocytes.
Birds with polyomavirus infection usually have vaiying de-
grees of hepatic necrosis and hemorrhage. In some cases, the hepa-
tocellular necrosis is so severe that only hepatocytes around portal
areas are spared. Hepatocytes with enlarged nuclei (karyomegaly)
that have marginated chromatin and large lightly basophilic to am-
phophilic (clear) inclusion bodies may be present. One should keep
in mind that not all birds with polyomavirus infection have inclu-
sion bodies in the liver. Polyomaviral infection is a multisystemic
disease and other organs including skin, spleen, bursa of Fabricius,
myocardium, kidneys, and esophagus should be examined.
Turkey viral hepatitis is characterized by vacuolation of he-
patocytes, infiltration of large numbers of mononuclear cells and a
few heterophils, and some proliferation of bile ductules. Over time,
multifocal hepatocellular necrosis becomes prominent with infiltra-
tion of the necrotic areas by lymphocytes, macrophages, and a few
Avian Histopathology (4 th Edition) I 357
 Tahsee11 Abdul-Aziz • Oscar J. Fletch er
heterophils. Large syncyt ial (multinucleated) hepatocytes may be
seen. Later, necrotic areas are infiltrated and repl aced by den se in-
VetBooks.ir
filtrates of macroph ages.
Hepatic necrosi s can occur in cases of av ian influenza and ex-
otic Newcastle disease . Hepatic necrosis may occur in reovirus in-
fection, but this is not a usu al finding in chickens. Eastern equine
encephalitis virus (EEE) ca uses hepatic necros is and hepatitis in
em us and whooping cranes with necrosis being massive in emus.
Avian hepatiti s-E-virus infecti on in broiler breeders and tab le-
egg layers is characterized by coagul ative and fibrinoid necrosis,
hemorrhages, perivascul ar and portal lymphocytic infiltration, ac-
cumulati o n of gra nulocytic mye loid cells, segmental lymph ocytic
phle bitis, deposition of amyloid in sinusoids and pools of hom og-
enous, acellular or hypocellular eosinophilic material of un ce rtain
nature.
Bacterial infections
Bacterial hepatitis generally is characte ri zed by multi focal to con-
fluent necros is that may be attended by fibrin -like material and
ce llular infiltrates of heterop hil s and mononuclear inflammato ry
ce ll s, with dissociation of th e hepat ic plate structure. There may
be diffu se widening of s inusoids du e to co ngestion , le ukostas is,
and acc umulation of fibrin . lnt ras inuso idal fibrin deposition , with
o r without vascular thrombi , and ev idence of damage to vessel
wall s are co mmon findings in se pti ce mic diseases. C lusters of
bacteria are found commonly in necrotic areas or within blood
vessels and sinusoids. Several Gram-negative and Gram-positive
bacteria may cause septicemia with li ve r les ions in birds . Salmo-
nella, E. coli, S1aphylococc11s a11re11s , Pasle11rella 111111/ocida, a nd
E1J1sipelolhrix rhusiopathiae ca use septice mia in poultry. Multi-
foca l areas of necrosi s with intrales iona l bacteria may be found in
li vers of qu a il affected with ul cera tive ente riti s caused by Clos1rid-
i11111 coli1111111. Fibrinous serositis of the hepati c capsule (hepatic
seros iti s, capsulitis, or perih epatiti s) is common with se pti cemi a
ca used by E. coli in Gall/fom,es and Riemerella analipestifer in
du cks. ln fibrinous he pati c seros iti s (perihepatitis), th e capsular
surface is covered with fibrin inter mi xed with variable numbers
of heterophils and mononucl ea r ce lls. Bacteria may be seen in th e
fibrinocellular exudate.
Caseous gra nul oma s are characteris ti c of bacterial infection s.
Gran ulomas consist of centers of caseous debris rimmed by mul-
tinuc leated g iant cells with an o uter zone of macrophages, lym-
phocytes, and heterophil s. In chroni c cases, the peripheral ce llul ar
inflammation is circumscribed by fibrous tissue. The causative bac-
teria may be seen in the necroti c ce nters. E11bacteri11111 tort11os11111
is a filamentous, anaerobic, Gra m-po sitive bac illus that spec ifi call y
ca uses liver gra nulomas in turkeys. E. tort11os11111 does not stain with
H& E stain , but can be demonstrated w ith Gram or silver stains.
Mycobacteriosis caused by Mycobacteri11111 spp. typically oc-
c urs as caseo us or non- caseo us gra nul o mas. Caseous gra nulomas
have a ce nter of caseous, amorph o us necro ti c debri s rimm ed by
multinuc leated gi ant ce ll s and surround ed by large numbers of
mac rophages and heterophil s. In psittacine birds, mycobacteri osis
presents as non -caseo us granulomas co ns isting of den se co ll ec-
tions of ep ithelioid macrop ha ges with ab undant faintly baso phili c,
358 I American Association of Av ian Pathologists
finely gra nular cytoplasm . An ac id-fas t stain revea ls few to nu-
merous acid-fast bacilli in the caseous debris and cytoplasm of
e pithelioid cells.
In chickens, liver les ions caused by Clostridi11111 perfi"i11ge11s
are characterized by ac ute cholangiohepatitis and cholecystiti s.
Large, irregularly shaped area s of necrotic hepatocytes are replaced
by eosinophilic material containing few cells. Extrahepatic bi le
ducts , and some intrahepatic bile ducts, are distended by large m11n-
bers of heterophil s and mon onuclea r inflammat01y cells. Walls of
affected ducts may be necrotic o r lined by attenuated epithelium.
The wall of the ga llbladder may also be necrotic, and man y large
bac illi morphologica ll y consistent w ith clost ridia are presen t on the
luminal wa ll. In subac ute to chronic cases, there are multi fo cal,
dense cellular infiltrates of predom inantly lymphocytes and plasma
cells, with extensive bile ductule proliferation, fibrosi s (porta l, peri-
portal, and bridging), and multiple gra nulomas. The lumen of some
bile ducts may contain intact and dege nerating necrotic heterophil s.
Peridu ctal fibro sis and mi xed heterop hili c and lymphoplasmacytic
infiltrates are frequently present adjace nt to affected bile ducts. Ne-
crosis and loss of indi vidual hepatocytes may be noted. Caseo us
gra nulomas, presumabl y in intrahepati c bile ducts, are co mposed of
eos inophilic necroti c centers rimmed by multinucleated g iant cell s
and surrounded by a layer offi brous ti ssue followed by cellular infil-
trates of mainly lymphocytes and plasma cells. Hyperplasia of bi le
ductules is usually extensive aro und gra nulomas.
Chlamydiosis caused by Chla111ydia psillaci is characteri ze d
by intrasinusoidal acc umulation of mononuclear cells and pl asma
cell s, acco mpanied by infiltration of portal areas by large num bers
of macrophages that usuall y encroac h into adjacent hepatocytes.
Multifocal nec rosi s ofhepatocytes ca n occur. Usuall y th ere is sli ght
to marked bile ductul e hyperp lasia. Accumulation of hemosiderin
pigment in individual or gro ups of Kupffer cells may be found. In
H&E-stained ti ssue sections, aggregates of elementary bodies of
Chla111y dia may be see n as basop hili c smudges within the cytoplasm
of macrophages and/or hepatocytes.
F1111gal iufections
Necroti zing granulomatous lesio ns composed of a necroti c ce nter
surrounded by macrophages, lymphocytes, and multinu cleated gi-
ant cells, with intrales iona l fragments of hyphae are characteri stic
of mycoti c infection of the li ver. Mycotic infection of the li ver is
uncommon, but the li ver may be involved in systemi c asperg illos is.
Microsporidiosis ca used by E11cephali1ozoo11 helle111 is an im-
portant di sease of pet and aviary birds, especially passe rin es and
parti cularly lovebirds. Microsporida were previously class ified
as protists, but based on mol ecul ar phylogenetic anal ys is, are now
known to be fun gi. In the liver, th ere are multiple foci of coag ula-
tive necrosis with hemo siderin pigment. Mononuclear cell infi ltra-
tion and biliaiy hyperplasia may be present. fn H&E-stained sec-
tions, mi crosporidia appea r as sma ll thin-walled, I 0-20 pm cyst-Iike
stru ctures filled with basop hili c gra nul es. C lose examination show
that these cyst-like structures are he patocytes with cytopl asm di s-
tended by cluste rs of mi crosporidia. Usuall y only a few cyst-like
stru ctures are prese nt; usua ll y adj acent to necrotic areas. Gra m
staining of li ver section s revea ls small Gram-positive structures

morphologically cons istent with spores of microsporidia, wh ich are
VetBooks.ir
diffi cult to identify in H&E-stained sections. Clusters of organisms
are a lso found in the tubular epithe lium of the kidneys and villous
enterocytes of the smal l intestine, where they cause di stension of the
cytoplasm. Large numbers of free organisms are often present in the
lu111en of renal tubules (see Chapter 9, Urinary System).
Protozoa/ i11fectio11s
Multifocal necrosis with numerou s intralesional trophozoites of
His/011101,as 111eleagridis is characteristic of the early stages of
hi sto111oniasis. Early, inftam111atory infiltrate is mild to moderate
and consists of predominantly ly111phocytes with lesser numbers
of heterop hil s and macrophages. As the lesion progresses, macro-
phages and numerou s multinucleated gian t cells are the predomi-
nant ce ll types. Trophozoites are seen singly or in clusters freely
or within the cytoplasm of macrophages and multinucleated giant
cell s. Characteristica ll y, trophozoites of H. 111eleagridis appear
in H& E-stained tissue sections as round to ovoid, faint ly eosino-
philic bodies, about I 0-20 ~1111 in diameter, usually with in lacunae
(surrounded by a halo). A sin gle nucleus may be di scernible. In
advanced lesions, trophozoites are scant and may be difficult to
recog nize as they degenerate and appear as faintly eos inophili c,
granu lar bodies within lacunae. Trophozoites are strongly period-
ic-acid-Schiff (PAS) positive.
Other protozoa that cause liver lesions include Atoxop/as111a ,
Sarcocyslis, Toxop/asma gondii, Le11cocylozoo11, and Plas1110-
di11111. Lesions caused by Atoxop/asma, Sarcocystis, and Toxo-
p/as111a are simi lar and inc lude multiple foci of coagu lative necro-
sis, wit h marked perivascular accumu lation of mononuclear cells
(l ymphocytes, macrophages, plasma cells), particularly in and
around portal areas. Sin usoids are distended with variable num-
bers of mononuclear cells. A characteristic feature is the presence
of large numbers of mononuclear cells within the lumen of blood
vesse ls. Individual tachyzoites of T gondii are difficu lt to iden-
tify and their morphology is difficult to discern in H&E-stainecl
tiss ues . Typically, smal l groups of Toxop/as 111a tachyzoites are
found in mononuclear ce lls, especially macrophages and Kupffer
cell s. Tissue cysts with thin, well-defined walls and 111any brady-
zo ites occur in he patocytes. Bradyzo ites are PAS positive. lm-
munohistochemical staining with anti-T gondii antibodies can be
used on tissue sections.
A!oxoplasma must be differentiated from Toxoplas111a. A!oxo-
plas111a does not stain with anti-T gondii antibodies. ln H&E-
stained sections, Atoxoplasma is seen wi thin the cytoplasm of
mononuclear phagocytic cells as tiny lightly basophilic, spherica l
bodies with a clear halo. Merozoites of Sarcocyslis .fcilca/11/a are
not usually seen in the liver, but, when they occur, they are in the
vascular endothe li al cells.
Metawal i11fectio11s
Gra nulomas composed of central necrotic areas surrounded by a
ce llul ar zone of primarily macrophages and num erous multinucle-
ated giant cells are characterist ic lesions of ascaricl larvae migra-
tion in the liver. lntral es ional fragment s of the nematode are oc-
cas ionally found . In turkeys , larvae of the roundworm Ascaridia
Hepatobili<11J1 System
c/issi111i/is may aberrantly migrate from the intestine to the liver
and cause multifocal granulomas that are often associated w ith
porta l triads. Multiple granulomas characteristica ll y composed of
co llections of large foreign body-type giant cel ls with or without a
center of necrotic debris occur in the liver of pigeons clue to aber-
rant migration of larvae Ascaridia co /11111bae. Fragments of the
nematode may be found in the les ion. Foci of granu locytic leuko-
cyte infiltration that represent an ac ute, early response to the larvae
may be seen in granu lom atous lesions. With heavy infections in
the duodenum, Ascaridia may enter the bile ducts and reach the
liver or ga llbl adder. Sections of the parasites are found in necrotic
bile ducts and liver parenchyma and may be associated with large
areas of necrosis co nta ining abunda nt bacteria that are li ke ly car-
ried by the worms.
Several species of trematodes infect the liver of free-living
birds. Bile ducts are distended and become increasingly fibrotic.
Heavy infections can cause mortality. Eggs of avian schistosomes
in mesenteric vesse ls are occasionally swept back into the liver in-
stead of penetrating the intestinal wa ll where they cause focal granu-
lomas. Eggs can be recognized by their large size, thick walls, and
presence of a miracidium wi thin the egg.
Neoplasia
Lymphoid tumors of Marek 's disease and lymphoid le ukosis fre-
quently involve the liver. Tumors are multifocal , but may coalesce
resulting in a diffuse appearance. Lymphoid tumors of lymph oid
leukosis usua ll y are expansive rather than infiltrative . As neo-
I
plastic cells proliferate, neoplastic nodules expand, displacing
and compressing surrounding parenchyma rather than infiltrating
between hepatocytes. Lympho id leukosis tumors are composed
of a uniform population of large lymphoid cells (lymphoblasts)
that show sli ght variation in size, whi le Marek's disease tumors
consist predominantly of small-to-medium size lymphocytes, with
lymphobl asts, primitive reticulum cells, rare plasma cells, and a
few macrophages. Marek 's lymphoid tumors have a pattern of
infiltration rather than expansion, althou gh this dist in ction can be
difficult to discern in many cases. Also, the re lat ive uniformity of
the tumor cell population in lymp hoid leukosis is not a lways easy
distinguish from the pleomorphic cell population in Marek's, espe-
cially in sections with postmortem auto lytic changes. The liver is
infiltrated with neoplastic lympho id cells in reticuloendotheliosis
of turkeys . Myelocytomatosis, caused by avian leukosis serotype
J virus, is characterized by proliferation of granu locytic myeloicl
cells (mye locytes) in which their cytoplasm conta ins eosinophilic
granules. Neop lastic myeloid cell s accu mulate around blood ves-
sels and extend into the hepatic parenchyma. Caut ion must be ex-
ercised to differentiate hyperplasia of myeloid ce ll s in extrameclu l-
lary hematopo iesis from myeloid neoplasia.
Primary tumors of the li ve r are rare, and they include hepa-
toce llular aclenorna, hepatocellular carcinoma, cholangiocell ular
adenoma, and cholangiocellular carcinoma. The liver may be also
a site of metastasis and implantation of tumors originated in other
organs, such adenocarcinomas of reproductive tract origin .
Hepatic and biliary carcino mas developed in Pekin ducks fo l-
low ing exposure to aftatoxin 8 I.
Av ian Histopathology (4 th Edition) I 359
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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Anderson, W. I., E. P. Dougherty, and H. Steinberg. 1989.
Cholangiocarcinoma in a 4-month-old double yellow-cheeked
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Beasley, J. N. , R. A. Norton, J. K . Skeeles, G. R. Bayyari, and W.
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Cullen, J. M. , P. L. Marion, G. J. Sherman, X. Hong, and J. E.
Newbold. 1990. Hepatic neoplasms in aflatoxin BI-treated,
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Davison, S., K. A . Converse, A, N. Hamir, R. J. Eckroade.
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Ga zdzinski , P. , E. J. Squires, and R. J. Julian. 1994. Hepatic
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Graham, D. L. A color atlas of avian chlamydiosis. 1993. Se111
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Avian Exotic Pet Med 2: 184-189.
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hepatic fibrosis with cholestasis in immunohistochemistry of
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Avian Histopathology (4 11, Edition) I 361
 Tahseen Abdul-A ziz • Oscar J. Fletcher
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8.1. Liver. Normal. 35-day-old broiler. Each hepatic pl ate is 8.3. Liver. Norm al. 21 -year-old African grey parro t.
two cell s thick, with bile canaliculus in the middle. In some areas, Ani sokaryosis, ka ryo mega ly, and cytomega ly of indi vidual
the plate fo rmation is not obvious, but hepatocytes are grouped hepatocytes occur with age.
around bile canaliculus. Sinusoids lie between the hepatic plates.

8.2. Liver. Normal. 27-week-old broiler breeder hen . Higher- 8.4. Liver. Normal portal tract. 4-week-old turkey. Po11al
power view showing hepatic pl ates. Each plate has bile canaliculus area containing termi na l po11al ve nule, bile ductules, and bra nch of
in the middle. the hepatic artery.

362 I American Assoc iati on of Avian Pathologists


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8.5. Liver. Normal. 4-week-old turkey. Two encapsulated
lymphoid nodules are in a portal area . Few of such nodules may be
found in avian livers and are considered normal ectopic lymphoid
nodules.
8.6. Liver. Extramedullary myelopioesis. 56-clay-old broiler.
Large collection of granulocytic myeloicl cells with characteristic
red cytoplasmic granules (myelocytes) is around a terminal hepatic
venule (central venule ).
Hepatobili(//J' System
8.7. Liver. Kupffer cell hypertrophy. 4-week-olcl turkey.
Kupffer cells are hypertrophic and seen as prominent sinusoidal
lining cells. Because Kupffer cells react to many different stimuli,
this finding is very nonspecific and should be interpreted in the
context of other more specific lesions.
8.8. Liver. Kupffer cell hypertrophy. 4-week-old turkey.
Kupffer cells around terminal hepatic venule are enlarged and very
prominent.
Avian Histopathology (4 th Edition) I 363
 Tahseen Abdul-A ziz • Oscar J. Fletcher
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8.9. Liver. Kupffer cell micronodule. 4-week-old turkey.
Small collecti on of enl arged Kupffer cells.
8.10. Liver. Kupffer cell micronodule (microgranuloma).
4-week-old turkey. Tiny collecti on of enl arged Kupffer cells
results in the formati on of a nodul e th at is termed Kup ffe r cell
mi crogra nul oma. Kupffer cell mi crogranulomas have little
independent di agnosti c significa nce as they represent a nonspecific
les ion th at occ urs in response to vari ous intrahepati c and extra hepati c
stimuli .
364 I Am eri ca n Assoc iati on of Av ian Patho logists
8.11. Liver. Bile ductular proliferation. 10-week-old turkey.
Di sruption of the hepatic parenchyma by ductul ar structures
resembling bile ductul es with or without di stinct lumens. The lesio n
is not eti ology- or di sease-specific but should arouse suspicion of the
poss ibility of hepatotox in. In thi s case afl atox icosis was suspected.
A lso see the next three fi gures.
8.12. Liver. Bile ductular proliferation. 31-day-old tu rkey.
Typica l bile ductul ar proli fera ti on in p ortal area. Ductul ar lumen is
recogni zable in the proli fera ting ductules. The cause was un know n
but afl atoxicosis was suspected.

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8.13. Liver. Ductular reaction. 4-week-old turkey. This
atypica l ductular proliferation is characterized by cluster of ductular
epithelium-like cells in the parenchyma. For lesion like this, the
term ductular reaction may be better than ductular proliferation.
The term ductular reaction implies reaction of ductular phenotype
that may or may not be of ductular epithelial cell origin. The cause
was unknown but aflatoxicosis was suspected.
8.14. Liver. Ductular reaction. 4-week-old turkey. Atypical
ductular proliferation characterized by formation of ductular
structures with poorly discernible lumens. The term ductular
reac tion may be used to describe this lesion. There is also
lymphoplasmacytic infiltrate in the area. The cause was unknown
but aflatoxicosis was suspected.
Hepatobilh11J 1 System
8.15. Liver. Lipogranuloma. Adult Quaker parakeet. Two
lipogranulomas are shown . Each is composed of lipid droplets and
infiltrates of lymphocytes and macrophages. Two multinucleated
macrophages are present among the infiltrate in the granuloma on
the top .
8.16. Liver. Lipogranuloma. Adult Quaker parakeet.
Higher-power view of 8.15 shows a lipogranuloma consisting
of lipid droplets of different sizes, with infiltrate of lymphocytes
and macrophages and possibly proliferating Kupffer cells. The
pathogenesis and clinical significance of lipogranulomas 111 avian
livers are uncertain.
Avian Histopathology ( 4th Edition) I 365
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8.17. Liver. Hemosiderosis. Swan. G ra nular, go lden-brow n
aggregates of hemosiderin in the cytoplasm of hepatocytes.
8.18. Liver. Hemosiderosis. Swan. Pruss ian blue stain is used
to demonstrate the iron in the hemos iderin. The iron is stained
purple with thi s stain .
366 I A meri ca n Assoc iati on of Av ian Path ologists
8.19. Liver. Nodular Kupffer-cell hemosiderosis. I O-year-011
lov ebird. See the legend for 8.20.
8.20. Liver. Nodular Kupffer-cell hemosiderosis. 5-year-old
ostrich. The legend is also applied to 8. 19. Multifoca l, well-
demarcated aggregates of hemosiderin-laden cells that are assumed
to be Kupffer cell s. The les ion is usuall y see n in assoc iation
wi th hepatoce llul ar hemos idero sis (the liver in 8.19 had mi ld
hepatocellular hemos iderosis and the li ver 8.20 had moderate
hepatoce llula r hemo sidero sis) .

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8.21. Liver. Iron-storage disease. 14-year-old parrot.
Disruption of the hepatic plates and loss and individualization of the
hepatocytes. The cytoplasm of the remaining hepatocytes is filled
with brownish granules of hemosiderin. The darkly stained areas
are collections of Kupffer cells with cytoplasm filled with dense
dark-brown aggregates of hemosiderin that obscure the histologic
details of the cells.
8.22. Liver. Iron-storage disease. 14-year-old parrot. The area
on the left side of the image consists ofhepatocytes with cytoplasmic
hemosiderin granules. On the right side of the image, hepatocytes
are replaced by collections of Kupffer cells filled with dense dark-
brown aggregates of hemosiderin.
Hepatobi/h11J 1 System
8.23. Liver. Iron-storage disease. 14-year-old parrot. Higher-
power view of 8.22 showing fine hemosiderin granules in the
cytoplasm of hepatocytes and dark-brown, dense aggregates of
hemosiderin in collections of Kupffer cells. The histologic details
of Kupffer cells are obscured by the hemosiderin aggregates. Note
the individuali zation of hepatocytes.
8.24. Liver. Iron-storage disease. 14-year-old parrot. Masson 's
trichrome stain shows area of fibrosis (blue areas) . Hepatocytes and
hemosiderin-laden macrophages are present in the area.
Avian Histopathology (4'h Edition) I 367
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8.25. Liver. Hepatic steatosis (Fatty Liver) - macrovesicular
fatty vacuolation. 3-year-old backyard chicken. The norma l
hepati c architecture is di storted by num erous round , di screte,
variably sized cytopl asmi c vacuoles with smooth, sharp contour.
These vacuo les represent di ssolved lipid dropl ets in the cytoplas m
of hepatocytes.
8.26. Liver. Hepatic steatosis (Fatty Liver) - macrovesicular
fatty vacuolation. 3-year-old backyard chicken. Hi gher-power
vi ew of 8.25 showing lipid vac uoles di stendin g the cytoplasm of
hepatocytes and di splac ing the nuclei to the periphery of the cells.
The few rema ining hepatocytes with no vacuo les are slmmken.
368 I Ameri ca n Assoc iati on of Av ian Patho logists
8.27. Liver. Microvesicular fatty vacuolation. 8-m onth-
old backyard chicken. The cytopl as m of the hepatocytes i,
distended with multiple small lipid droplets (clea r spaces). The
nuclei of hepatocytes are still centrall y loca ted. No te th e narrowing
or obliteration of sinusoidal spaces due to the di stension of the
cytoplasm of the hepatocytes. Microvesicular fa tty vacuol ati on is
more di ffic ult to recognize than the macrovesicular vac uolati on.
8.28. Liver. Microvesicular fatty vacuolation. 3-day-old
broiler. The cytoplas m of hepatocytes is di stended with mul tip le,
vari abl y-s ized lipid vacuoles. The nu clei of hepatocytes are
di splaced to the sinusoidal border of the cells, and the compressed
cytopl asm is around the di splaced nucl ei. A lthough hepatocell ular
fa tty vac uolati on is considered to be norm al in fe w-d ay-o ld
chi ckens (because of absorption of yolk), the changes in thi s liver
are probabl y excess ive.

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8.29. Liver. Fibrosis and fatty vacuolation. 15-year-old female
cocka tiel. There is loss of hepatocytes and replacement by bands
of co ll ageno us tissue. Remaining hepatocytes show macrovesicular
fatty vacuo lati o n.
8.30. Liver. Fibrosis and fatty vacuolation. 15-year-old female
cockatiel. Masson 's triclu-ome stain demonstrates the fibrosis.
Lipid vacuoles are seen in hepatocytes.
HepatobilimJ 1 System
8.31. Liver. Steatosis and fibrosis. Adult Amazon parrot.
Exte nsive fibrosis, loss of hepatocytes, hepatocellular fatty changes
of la rge-droplet type, and mild to moderate c hroni c inflammatory
infi ltrate . The bird had severe atherosclerosis of th e great arteries
of the heart.
8.32. Liver. Steatosis and fibrosis. Adult Amazon parrot. In
addition to the les ion described in 8.3 1, the cytoplasm ofhepatocytes
contains dark brown pigment suggest ive of hemosiderin.
Avi an Histopathology (4 th Ed ition) I 369
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8.33. Liver. Chronic-active hepatitis. Adult Amazon parrot.
Scanning view demonstrating multifoca l nodular regenerati ve
hyperplasia of hepatocytes. The regenerati ve nodules are of
va riable sizes, and indi vidual nodules have fi brous capsule. Tn the
areas between the regenerati ve nodules, there is marked fibrosis,
pro minent bile ductular pro li fe ration, mi xed inflammatory infiltrate
that include many granulocyti c leukocytes, and foc i of hemorrhage.
See the next seven fi gures.
8.34. Li ver. Chronic-active he1>atitis. Adult Amazon parrot.
Low-power view showing encapsulated regenerati ve nodule
surrounded by dense fi brous ti ssue with numerous bile ductules
(bil e ductular proli fe ration).
370 I Ameri can Assoc iation of Av ian Pathologists
8.35. Liver. Chronic-active hepatitis. Adult Amazon parrot.
On the ri ght is an encapsulated regenerative nodule consisting of
degenerate, vacuolated hepatocytes that lack plate arrangement.
Outside the nodule is a dense fib rous tissue with pro li fe rating bile
ductules and mi xed inflammatory infiltrate.
8.36. Liver. Chronic-active hepatitis. Adult Amazon parrot.
Encapsulated regenerati ve hepatocyte nodule consists of degenera te,
vacuolated hepatocytes and lacks sinusoids, terminal hepatic venule
(central venule), and portal tract.
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8. 37. Liver. Chronic-active hepatitis. Adult Amazon 8.39. Liver. Chronic-active hepatitis. Adult Amazon parrot.
pa rrot. Higher-power view of the hepatocytes in a regenerati ve Marked fibro sis and prominent bile ductular proliferation are shown
nodul e. There is marked vacuolar degeneration of the cytoplasm in thi s area between regenerative hepatocyte nod ul es.
of he patocytes. Thin strands of fibrous ti ssue separate gro ups of
the hepatocyte s that lack plate arrangement. The lack of normal
blood c irculation in th e nodule attribute to the severe degeneration
of hepatocytes.

8.38. Liver. Chronic-active hepatitis. Adult Amazon parrot. 8.40. Liver. Chronic-active hepatitis. Adult Amazon parrot.
Hi gher-power view of the hepatocytes in another rege nerative Shown is an area of marked fibrosis and bile ductular proliferation,
nodule showin g the marked cytoplasmic vacuolar degeneration of with prominent inflammatory infiltrates predominated by
th e he patocytes, with marked intracytoplasmic accumulation of gra nulocyti c le ukocytes.
gra nul ar hemosiderin pigment.

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8.41. Liver. Hepatic ischemia (hypoxic injury). 7-week-old
free-range broilers. Severe necrosis of the hepatocytes around
terminal central venule, which is engorged with blood and shows
evidence of extravasation of red blood cells. The bird had severe
asc ites caused by congestive heart failure due to pulmonary
hypertensio n syndrome (ascites syndrome).
8.42. Liver. Hepatic ischemia (hypoxic injury). 7-week-old
free-range broilers. Severe necrosis of the hepatocytes around
terminal hepatic venule, with extravasated red blood cells in the
necrotic areas. The bird had severe ascites caused by congestive
hea rt failure due to pulmona1y hypertension syndrome (ascites
sy ndrome).
372 I American Association of Avian Pathologists
8.43. Liver. Hepatic ischemia (hypoxic injury). 9-week-old
broilers. Bridging, centrilobular necrosis of hepatocytes. This is a
characteristic lesion of hypoxic injury. Several birds in a small flock
of 170 birds died of pulmonary hypertension syndrome. The flock
was in high-altitude area (about 2000 teet). The owner stated tbat
"this batch of birds was growing rapidly".
8.44. Liver. Hepatic ischemia (hypoxic injury). 3-day-old
broiler. Zone of necrotic hepatocytes is around the terminal hepatic
venule. There was very high mortality in only one house on a far m
with four houses. Carbon monoxide poisoning was suspected in
that house.

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8.45. Liver. Sinu soidal dilation and proteinosis. 3.5-year-old
backyard chicken. Sinusoids around terminal hepatic venule are
dilated and co ntain eosinophilic proteinaceous material. The bird
had severe ascites due to congestive heart failure caused by dilated
cardiomyopathy.
8.46. Liver. Sinusoidal dilation and proteinosis. 3.5-year-old
backyard chicken. Higher-power view of area around terminal
hepatic venule showing dilation of sinusoids, with intrasinusoidal
accumulation of eosinophilic proteinaceous material. The bird
had severe ascites due to congestive heart failure caused by dilated
cardio myopathy.
Hepatobiliwy System
8.47. Liver. Hepatic lipidosis. 14-week-old breeder turkey
hen. Low-power view showing diffuse, marked vacuolation
of hepatocytes and areas of hemorrhage. Hepatic lipidosis Ill
commercial turkeys is a disease entity of uncertain etiology.
8.48. Liver. Hepatic lipidosis. 14-week-old breeder turkey hen.
Groups of markedly vacuolated hepatocytes (fatty degeneration) are
separated by areas of hemorrhage and loss of hepatocytes.
Avian Histopathology (4 11, Edition) I 373
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8.49. Liver. Hepatic lipidosis. 14-week-old breeder turkey 8.51. Visceral gout. Urate Deposition. 4-day-old broiler.
hen. Hi gher-power view show ing area of hemorrhage adjacent to Focal area of necrosis with center of basophilic, radiating materia l
area of necrotic and vacuolated hepatocytes (fatty dege nerati on). co nsistent with urate deposits. This broiler had viscera l urate
deposition (v iscera l gout) and neph ropathy ca used by dehydration .

8.50. Liver. Hepatic lipidosis. 14-week-old breeder turkey 8.52. Liver. Hepatic amyloidosis. 17-week-old chukar. This is
hen. D emonstrated is bile ductular proliferation which is a common a seve re case of hepat ic amyloidosis. The depositio n of amy loid in
lesion of hepatic lipidosis in turkeys, in addition to fatty vacuolation, spaces ofD isse results in effacement of hepatocytes. The remaining
necro sis, and hemorrh age. he patocytes ae co mpressed and atrophied.

374 I A meri ca n Association of Avian Pathologists


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8.53. Liver. Hepatic amyloidosis. 17-week-old chukar.
Hi gher-power v iew of the amyloid deposition in 8.52. Sinusoidal
deposi ts of eos inophilic, amorphous, hyaline material (amyloid)
di srupt the hepati c plates and compress hepatocytes. Because
amy loid is deposited in the space of Disse, the term "peri sinusoidal
amy loidosis" is sometimes used to describe the les ion .
8.54. Liver. Hepatic amyloidosis. 17-week-old chukar.
Amy loid protein stains light orange with Congo red stain. The
orange-stained material exhibited apple-green birefringence under
polarized li ght. Avian amyloid does not consistently stain well with
Congo red and does not always exhibit strong birefringence under
polarized li ght.
Hepatobi/i(IIJ' System
8.55. Liver. Reaction to oil-emulsion vaccine. 20-week-old
broiler breeder hen. Severe sinusoidal co ngestion with possibly
hemorrhages . Hepatic cords and hepatocytes are compressed and
atrophi ed due to accumulation ofproteinaceous material, interpreted
to be amy loid, in the sinusoids. Two different oil-emulsion vaccines
were administered at 18 weeks of age, and th e mortality started to
increase four days after vaccination. Dead birds had severe liver
les ions and yellow or sanguineous fluid in the coe lomic cavity.
8.56. Liver. Reaction to oil-emulsion vaccine. 20-week-old
broiler breeder hen. Severe sinusoidal congestion and area of
severe hemorrhage. Sinusoidal deposits of amyloid-like material
disrupt and cause atrophy of the hepatic co rd s and hepatocytes.
Avian Histopathology (4 11, Edition) I 375
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8.57. Liver. Reaction to oil-emulsion vaccine. 20-week-old
broiler breeder hen. Area of severe sinusoidal congestion with
deposition of amyloid-like material, ca using compression and
atrophy of the hepati c cords and hepatocytes.
8.58. Liver. Reaction to oil-emulsion vaccine. 20-week-old
broiler breeder hen. Area of severe hemorrhage, with depositio n
of amyloid-like materi a l in si nu soids, causing compressio n and
atrophy of the hepatic cords and hepatocytes .
376 I American Association of Avian Pathologists
8.59. Liver. Thickened peritoneum in ascites. Backyard
chicken. Contiguous with the surface of the li ver capsule is thi ckened
peritoneum composed of mesenchyma l-like, proliferating peritoneal
mesothelial cells in proteinaceous eosinophilic intercellular matrix.
Note the di stension of sinusoids by eosinophilic proteinaceous fluid.
Such a lesion is seen in birds with ascites. This chicken had severe
peritoneal effusion (ascites) of undetermin ed cause.
8.60. Liver. Aftatoxicosis. 2-week-old duckling. Severe
macrovesicular and mi crovesicular fatty vacuolation ( degeneration)
ofhepatocytes around term inal hepati c venule. Proliferation of bile
ductules is evident around the degenerate hepatocytes.
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8.6 1. Liver. Aflatoxicosis. 2-week-old duckling. The hepatocytes 8.63. Liver. Aflatoxicosis. 2-week-old duckling. Areas of
around a terminal hepatic venule (cen tra l venule) are swollen and marked proliferat ion of bile ductul es.
have de nse, deep-pink cytoplasm. This is a characte ri stic lesion of
afl atox icosis in ducks. Single large lipid vacuole can be seen in
some hepatocytes.

8.62. Liver. Aflatoxicosis. 2-week-old duckling. Area of marked 8.64. Liver. Aflatoxicosis. 2-week-old duckling. Higher-power
swe lling and mi crovesicular fatty vacuolation ofhepatocytes. Note view of area of bile ductular proliferation. The hepatocytes around
th e dense, deep-pink cytoplasm of the non-vacuolated hepatocytes. proliferating bile ductules have dense or vacuolated cytoplasm.

Avian Histopathology (4 th Edition) I 377

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8.65. Liver. Aflatoxicosis. 2-week-old duckling. Area ofacinus- 8.67. Liver. Afla toxicosis. IO-week-old quail. Marked
li ke stru ctures are formed by ce lls th at have deeply basophilic hemo rrh age a nd hepatocyte degeneratio n and coagulative necrosis,
cytoplasm and ex hibit a ni soka ryosis . Three mitotic fi g ures (not w ith mild proliferatio n of bile ductules in the portal area in the
clearly discernib le at this mag nification) are present in this fi eld. ce nter.
It is un ce rtain what th ose ce lls are and whether they represent
regenerating hepatocytes. Note the dense , deep-pink cytoplas m of
the hepatocytes.

8.66. Liver. Aflatoxicosis. IO-week-old quail. Severe 8.68. Liver. Aflatox icosis. 10-week-old quail. Severe
fatty vacuolation and coagulative necrosis of hepatocytes, with fatty vacuolation and coagulative necros is of hepatocytes, with
parenchymal hemorrhages that resulted from the collapse of the hemorrhages and porta l bile ductul ar pro li feration (bile ductular
supporting reticular ne twork . hy perplas ia) .

378 I American Association of Avian Patho logists


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8.69. Liver. Aflatoxicosis. 10-week-old quail. Higher-power
vi ew demonstrating hepatocellular fatty vacuolation and necrosis
and bile ductular proliferation.
8.70. Liver. Arsenic toxicity. 7-week-old broiler breeder
pullet. Dilated bile duct has segmental necrosis of epithelium with
leakage of bile and necrosis of adjacent hepatocytes. The flock was
simultaneously dosed with 4-nitrophenylarsonic acid in the feed and
3-nitro-4-hydroxy phenylarsonic acid in the water. See also the next
three figures. (Image a11d lege11d Courtesy of D1: Fred Hoe/'/).
Hepatobili{//J' System
8.71. Liver. Arsenic toxicity. 7-week-old broiler breeder
pullet. Another liver had widespread moderate hyperplasia of bile
ductules. (Image a11d legend courtesy of Fred Hoen) .
8.72. Liver. Arsenic toxicity. 7-week-old broiler breeder
pullet. Liver collected weeks later. Dilated bile duct contains
cast of eosinophilic coagulum lined by giant cell macrophages and
regenerated ductular epithelium . (Image and legend courtesy of
Fred Ho e/'/).
Avian Histopathology (4 th Edition) I 379
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8.73. Liver. Arsenic toxicity. 7-week-old broiler breeder
pullet. The sequela to the preceding lesions, this bile duct was
dilated an d had severe villous hyperplasia of lining epithelium.
(Image and legend courtesy of Fred Hoen).
8.74. Liver. Copper toxicity. 13.5-week-old turkey breeder
replacem ent hen. Sinusoids co ntai n distorted erythrocytes, so me
of which appea r undergo ing lys is. Kupffer ce ll s are swoll en and
co ntai n brownish materia l most suggestive of iron-rich heme th at
res ulted fro m the degradation ofphagocytized erytlu·ocytes.
380 I Ameri ca n Association of Av ian Pathologists
8.75. Liver. Copper toxicity. Few-day-old broile1
Di sintegration an d clumping of the cytoplasm of hepatocyte:
around terminal hepa ti c venules . (Glass slide courtesy of po11IIIJ
Diagnostic and Research cente1; Georgia, USA) .
8.76. Liver. Copper toxicity. Few-day-old broiler. Area of
bili ary ductular hyperplas ia, w ith extramedullary gra nulopoiesis.
(Glass slide courtesy of poult, y Diagnostic and Research ce11te1;
GeOJg ia, USA).

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8.77. Liver. Copper toxicity. Few-day-old broiler. Rhodanine
stain reveals accumulation of copper in the cytoplasm ofhepatocytes
and Kupffer cells. Copper appears as red-brown cytoplasmic
granules . (Glass slide courtesy ofpou/t, y Diagnostic and Research
ce11te1; Geo1gia, USA).
t78. Liver. Inclusion body hepatitis. 14-day-old broiler.
Small focal area ofhepatocyte degeneration and necrosis. The large
Jeeply basophilic structures are adenovirus inclusion bodies filling
rnd enlarging the nuclei ofhepatocytes.
Hepatobilir11J> System
8.79. Liver. Inclusion body hepatitis. 21-day-old broiler.
Focal area of degeneration and necrosis of hepatocytes, with large,
deeply basophilic, homogenous intranuclear adenovirus inclusion
bodies filling and enlarging the nuclei of hepatocytes . Note the
margination of the nuclear clu·omatin by the inclusions.
8.80. Liver. Inclusion body hepatitis. 14-day-old broiler.
Focal area of degeneration and necrosis ofhepatocytes. Adenovirus
inclusions are not present in this lesion but can be found in other
areas of this section . One must keep in mind that only few inclusion
bodies may be present, and careful examination of the section 1s
necessary to find them.
Avian Histopathology (4'h Edition) I 381
 Taflsee11 Abdul-Aziz • Oscar J. Fletcfler
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8.81. Liver. Inclusion body hepatitis. 16-day-old broiler. Area 8.83. Liver. Inclusion body hepatitis. 11-clay-o lcl broile1
of marked degeneration and necrosis of hepatocytes. The dark Area of lytic necrosis characterized by loss of hepatocytes an,
round structures are intranuclear adenovirus inclusion bodies filling replacement by eosinoph ilic necrotic debris. The dark roun,
and enlarging the nuclei of hepatocytes. structures are adenovirus intranuclear inclusion bodies filling an,
enlarging the nuclei of hepatocytes.

8.82. Liver. Inclusion body hepatitis. 14-clay-old broiler. 8.84. Liver. Inclusion body hepatitis. 18-clay-olcl broiler. Area
Low-power view showing extensive necrosis of hepatocytes. of hepatocyte necrosis, with several enlarged nuclei filled wi th
deeply basophilic intranuclear inclusion bodies characteri stic of
adenovirus infection.

382 / American Association of Avian Pathologists

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8.85. Liver. Turkey viral hepatitis. 26-day-old turkey. In 8.87. Liver. Turkey viral hepatitis. 30-day-old turkey.
this earl y lesion , focal area of hepatocellular necrosis is replaced Illustrated are severa l intralesional multinucleated (syncytial) cells
with eosi nophilic proteinaceous material and infiltrated with small that are li ke ly formed by fu sion of hepatocytes.
nu mbers of granulocytic leukocytes and mononuclea r inflammatory
cells.

8.86. Liver. Turkey viral hepatitis. 30-day-old turkey. Area 8.88. Liver. Turkey viral hepatitis. 35-day-old turkey. Area
of loss of hepatocytes and replacement by infiltrate of mononuclear of necrosis containing many mononuclear inflammatoty cells and
inflammatory cells and some heterophil s. Intact and degenerate degenerate multinucleated (syncytial) cells .
multinucleated (syncytial) cells are seen in the lesion .

Avian Histopathology (4 th Edition) I 383

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8.89. Liver. Turkey viral hepatitis. 35-day-old turkey.
Higher-power view of the lesion in 8.88 showing the mononuclear
inflammatory infiltrate and large degenerate multinucleated
(syncytial) cells.
8.90. Liver. Turkey viral hepatitis. 35-day-old turkey. Area of
loss of hepatocytes and replacement by mononuclear infl ammatory
infiltrate. Note the large degenerate multinucleated (syncytial) cell.
384 I American Association of Avian Patholog ists
8.91. Liver. Turkey viral hepatitis. Turkey poult. This is an
advanced lesion characterized by dense lymphohistiocytic infil trate
that effaces and replaces hepatocytes.
8.92. Liver. Reovirus vaccine. 3-day-old broiler. One of several
areas of severe hydrop ic vacuolar degeneration of hepatocytes.
Chicks in the flock started to die at 3 days of age following
inadvertent administration in the hatchery ofS 1133 reovirus vaccine
labeled for water ad ministration in JO- to 17-week-old chi cken.
(Glass slide courtesy o_f So11ia Che11ie1).

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8.93. Liver. Reovirus vaccine. 3-day-old broiler. Same case as
8.92. See the legend of 8.94.
8.94. Liver. Reovirus vaccine. 3-day-old broiler. Same case
as 8.92 . Th is legend is also applied to 8.93. One of severa l areas
of se vere necros is and degeneration of hepatocytes, with minimal
infla mmatory infiltrates. The lesion is not etiology-specific but
should arouse suspic ion of vira l etiology.
Hepatobilia1J' System
8.95. Liver. Polyomavirus Infection. Fledgling ring-necked
Parrot. Massive necrosis ofhepatocytes, with only the hepatocytes
around venules are spared. There are foci of hemorrhage. Numerous
cells with enlarged nuclei containing polyomav irus inclusions were
prese nt in renal glomeruli and in the spleen of this bird, but no
inclusions were found in the liver sections.
8.96. Liver. Polyomavirus Infection. Fledgling ring-necked
Parrot. Extensive Necrosis of hepatocytes, with hemorrhages.
Note that the hepatocytes around terminal hepatic venule are spared.
Avian Histopathology (4 th Edition) I 385
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8.97. Liver. Polyomavirus infection. 7-week-old macaw. 8.99. Liver. Polyomavirus infection. 4-week-old conure.
Exten sive necrosis of hepatocytes w ith sparing of the hepati c ti ssue A reas of di sruption o f th e hepatic ti ss ue by hemorrhages. The lesion
around he pati c and portal venul es. in thi s case was hemorrh ag ic rather than necroti c.

8.98. Liver. Polyomavirus infection. 6-month-old lovebird. 8.100. Liver. Polyomavirus infection. 4-week-old conure.
Area of hepatocyte necrosis with marked hemo rrhage. Hepatocytes Two enl arged nuclei (ka ryomega ly) of hepatocytes are fi lled with
in other areas of the secti o n have fa tty vacuolati on of th e cytoplas m. ampho philic inc lusion bodi es typical of polyomaviru s inclusions.

386 I A meri ca n Associati o n of Avi an Patho logists

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8.1 01. Liver. Polyomavirus infection. 12-year-olcl parrotlet. 8.103. Liver. Herpesvirus infection. 4-week-olcl pigeon. Higher-
Area of hepatocyte degeneration and necrosis, wi th severa l glassy, power view of area of necrosis and hemorrhage.
faint ly basophilic inclusion bodies filling the enlarged nuclei of
hepatocytes. The morphology of these inclusions is diagnostic
of polyo ma virus infection. These polyomavirus inc lusions were
incidentally found in thi s section of liver with hemangiosa rcoma
(sa me case as 8.237-8.239) .

8. 102. Liver. Herpesvirus infection. 4-week-olcl pigeon. Low- 8.104. Liver. Herpesvirus infection. 4-week-olcl pigeon.
power view showing multifocal, coalescing areas of necrosis, with Multiple foci of necrosis characterized by loss of hepatocytes with
sinusoidal congestion and hemorrhages . accumulation ofproteinaceous, fibrin-like material.

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8.105. Liver. Herpesvirus infection. 4-week-old pigeon. Area
of necrosis characterized by a lmost total loss of hepatocytes and
replacement by proteinaceous, fibrin-like material. Sinusoids at the
periphery of the necrotic area appear congested.
8.106. Liver. Herpesvirus infection. 4-week-old pigeon. Higher-
power view of area of necrosis and loss of the hepatocytes, with
small amount of fibrin-like materi al. The ye llow-green pigment
is retained bile (chol estasis). The small, darkly basophilic, round
bodies around the necrotic area are hepatocyte nuclei filled with
virus inclusion bodies.
388 I American Associatio n of Avian Pathologists
8.107. Liver. Herpesvirus infection. 4-week-old pigeon. Many
intranuclear inclusion bodies are present in this area of hepatocyte
degeneration and necrosis. The inclusio n body may or may not fi ll
the entire un cles and may be basophilic or eosinophilic. Nu clei
of necroti z ing hepatocytes are condensed and fill ed with deeply
basophilic inclusion bodies and have marginated chromat in and
nucleoli. Large basophilic inclusio n bodies that may be mi staken
with ade nov irus inclusions sometimes are seen.
8.108. Liver. Herpesvirus infection. Hawk. One of severa l areas
of loss (necrosis) of hepatocytes and replacement by proteinaceous
material.

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8. 109. Liver. Herpesvirus infection. Hawk. Area of hepatocyte
degeneration and necrosis with accumulation of hemosiderin
pigment, likely in the distended cytoplasm of Kupffer cells.
8.110. Liver. Herpesvirus infection. Hawk. Area of marked
hepatocyte degeneration, with cell conta111111g intranuclear,
eosinophilic inclusion surrounded by clear halo (circle). Inclusion
bodies in this case were not many and mainly seen in areas of
hepatocyte degeneration.
Hepatohilia1J' System
8.111. Liver. Duck viral enteritis. Muscovy duck. Focal area of
necrosis characterized by loss of hepatocytes with accumulation of
proteinaceous, fibrin-like material and infiltration offew heterophils.
Only few foci of necrosis were present in the histological sections of
thi s liver. lntranuclear inclusion bodies characteristic ofherpesvirus
were identified in the sections.
8.112. Liver. Herpesvirus infection. 7-year-old cockatoo.
One of several areas of loss of hepatocytes and replacement by
proteinaceous material. Numerous hepatocytes have basophilic
inclusion bodies characteristic of herpesvirus infection. Infection
with herpesvirus was confirmed by in si/11 DNA hybridization .
Avian Histopathology (4th Edition) I 389
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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8.113. Liver. Herpesvirus infection. 7-year-old cockatoo. Same
li ver as 8. 112. Numerous hepatocytes have basophilic int ra nuclea r
inclusion bodies characteristi c of herpesv irus infecti on. These
inclusions fill the nu clei and marginali ze th e chromatin . There was
widespread degeneration and necrosis ofhepatocytes (ev ident in the
upper left area of th e image).
8.114. Liver. Herpesvirus infection. Parrot. One of several foci
of hepa tocyte degeneration and necros is.
390 I A meri ca n Associat ion of Avian Pathologists
8.115. Liver. Herpesvirus infection. Parrot. Same li ver as
8. 114. In the center of th e image are hepatocytes w ith intranuclem
inclusio n bodies surrounded by a halo. In clusion bodies were hard
to find in th e sections of thi s liver.
8.116. Liver. Herpesvirus infection. Parrot. Same li ver as 8.11 4.
Two hepatocytes w ith deeply basophilic inclusion bodies filli ng the
nucleus and marginalizing the nucleolus. Note the morphology of
the inclusion bodies compared to those in 8. 11 5.
 Hepatobili<11J' System
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8.117. Liver. Acute fibrinous hepatic serositis (capsulitis).
7-day-old broiler. The capsular surface of the li ver is covered
with a thic k layer of fibrin conta ining heterophil s. T he bird had
sept icemia caused by £. coli.
8.119. Liver. Acute fibrinous and caseous serositis. 28-day-
old chicken. The capsular su rface of the li ver is covered with a
layer of fibrin fo llowed by a layer of caseated heterophilic exudate.
Bacterial colon ies are usually found in the caseo us material. The
bird had septi cemi a ca used by E. coli .

8.11 8. Liver. Acute fibrinoheterophilic hepatic serositis.
51-day-old chicken. The capsular surface of the liver is covered
with a layer of heterophils follo wed by a layer of fibrin mi xe d with
few heterophils. T he bird had septicem ia ca used by E. coli.
8.120. Liver. Fibrinous organizing hepatic serositis. 61-day-old
broiler. Early stage of fibrou s organization of the fibrinous exudate
on the li ver surface. Fibroblasts grow from the capsule and replace
the fibrin. A thin la yer of inflammatory cells is still on the surface
of the fib rin.

Avian Histopathology (4 th Edition) I 391

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8.1 21. Liver. Serosal organizing fibrosis. 61-day-old broiler. 8.123. Liver. Sinusoidal fibrin thrombi. 19-day-da y old broiler.
Thick laye r of fibro us ti ss ue is conti guous with th e underlyin g Fibrino us deposits in sinusoids. This is a characteri sti c les ion
he pati c parenchyma . The fib rous ti ssue results fro m fibrou s of bacteri al septice mia . T he bird in thi s case was affected with
o rga ni za ti o n of the fibrin ous exudate on th e surface. septice mi a caused by£. coli (colisepti ce mi a) .

8. 122. Liver. Sinu soidal fibrin thrombi. 30-week-old broiler 8.124. Liver. Sinu soidal fibrin thrombi. 4-week-old turkey.
breeder hen. Sinuso ids contain fi brinous deposits. T he les io n D ense fibrin thro mbi in sinusoids. Clusters of bacteri a (arrow and
should arou se suspicion of bacteri a l septicemi a. Bacteria may be hi gher magnifi catio n in the inse rt) are present al so in sinusoid. These
fo und within the fibrin . findin gs are common in chickens and turkeys with coli septi cem ia.

392 I Am eri ca n Assoc iati on of Av ian Patho logists

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8.125. Liver. Colisepticemia. 14-day-old broiler. Adjacent 8.127. Liver. Colisepticemia. 45-day-old broiler. Dense cluster
sinusoids are dilated and conta in fibrin. of bacteria (E. coli) is in sinusoids. Culture of this liver yielded
pure, heavy growth of E. coli.

B.126. Liver. Colisepticemia. 14-day-old broiler. Fibrinous 8.128. Liver. lntravascular fibrin thrombus. 50-week-old
:leposits in sinusoids . The nuclei of individual hepatocytes are broiler breeder hen. Bacteria are present w ithin a fibrin tlu·ombus
karyorrhectic, and there is focal area of nuclear debris. that occludes a blood vessel in this liver. Fibrin thrombi are
relatively common in colisepticemia and may be found in other
septicemic infections. This bird had salpingitis, peritonitis and
septicemia caused by E. coli.

Avian Histopathology (4 11, Edition) I 393

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8.1 29. Liver. Pasteurellosis. 29-week-old broiler breeder hen. 8.131. Liver. Pasteurellosis. Duck. The center of an area of
Dense, almost amorphous cluster of bacteria (Paste11rella 11111/tocida) severe necrosis contains dense clusters of bacteri a (Pasfe11rella
in sinusoids. Note the absence of necrosis or inflammatory response. 11111/tocida). Bacteria also are numerous around the necrotic tissue.
Such a lesion indicates bacteremia.

8.130. Liver. Pasteurellosis. Phea sant. Large numbers of bacteria 8.132. Liver. Sal111011 el/a enteritidis infection . 21-day-olcl
(Pas te11rella 11111/tocida) in sinuso ids. Nec rosis and inflammati on broiler. Focal area of necrosis with fibrin exudation and mi xed
may be absent or minimal in birds that die very acutely fro m infiltrate of heterophil s and mac rophages .
septicemi c di sease.

394 I American Associati on of Avian Pathologists


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8.133 . Liver. Salmonella enteritidis infection. 21-day-old
bro iler. High-power view of the necrotic focus in 8. 132 showing
hepatocellular necrosis, fibrin exudation, and heterophils and
macrophages infiltration .
8. 134. Liver. Erysipelas. 17-week-old turkey. Large area
of necrosis characterized by replacement of hepatocytes by
eosinophilic, proteinaceous, fibrin-like material. Sinusoids around
the area are dilated and congested . The lesion is not specific for
erysipelas but should arouse suspicion of bacterial etiology.
HepatobilimJ' System
8.135. Liver. Erysipelas. 17-week-old turkey. Marked
dissociation of hepatocytes results in disruption of hepatic cords.
Expanded sinusoids and intercellular spaces contain eosinophilic
fibrillar material suggestive of fibrin .
8.136. Liver. Erysipelas. 17-week-old turkey. Cluster of rod
shaped bacteria in sinusoids with no or minimal inflammatoty
response is a feature of acute bacterial septicemias and must
be differentiated from post-mortem bacterial growth. Note the
disruption of hepatic cords and individualization of hepatocytes.
Avian Histopathology (4 th Edition) I 395
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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8.137. Liver. Erysipelas. 17-week-old turkey. Fibrin thrombu s 8.139. Liver. Erysipelas. Pheasant. The cytop las m of the circled
nea rl y occludes branch of the hepati c artery in this porta l area . This cells (likely Kupffe r cell s) is di stended with bacteria-like organ isms
lesion is suggestive of bacterial septi cemia, but it is not etiology that were interpreted to be E,ysipelothrix rh11siopathiae.
specific.

8.138. Liver. Erysipelas. Pheasant. Fibrin thrombus occludes 8.140. Liver. Erysipelas. Pheasant. Same section as 8. 139 stained
a blood vessel (like ly terminal hepatic venul e). Intravascular with Gram stain. Gram-positive bacteria distend the cytoplasm of
fibrinou s thrombosis is common lesion in turkeys, pheasants, and cells that are considered to be Kupffer cell s.
possibly other types of birds affected with erysipelas.

396 I American Association of Av ian Pathologists


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8.14 1. Liver. Ulcerative enteritis. Quail. Area of necrosis with
intralesional large, rod-shaped bacteria morphologically resembling
C/ostridi11111 spp.
8.142. Liver. Sal111011ella typhi11111ri11111 infection. Gold finch.
Multiple areas ofKupffer cell hyperplasia and hypertrophy resulting
in granuloma-like lesions.
Hepatobili<11J' System
8.143. Liver. Sal111011ella typhi11111ri11111 infection. Gold finch.
The cytoplasm of Kupffer cells is distended with rod-shaped
bacteria. Culture of this liver yielded pure growth of Sa/111011e!la
typhi11111ri11111.
8.144. Liver. Cholangiohepatitis. 3-week-old broiler breeder
chicken. Bile ductule is distended with heterophilic exudate and
is segmentally denuded or lined by attenuated epithelium. There
is necrosis of hepatocytes and accumulation of fibrin. The bird had
necrotic enteritis caused by C/ostridi11111 perfi·ingens.
Avian Histopathology (4 th Edition) I 397
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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8.145. Liver. Cholangiohepatitis. 3-week-old broiler breeder
chicken. Portal tract with three bile du ctul es distended with
heterophil s and lined with attenuated epithelium . There is
periductul a r fibrosis and sparse infiltrate of mi xed inflammatory
ce lls. The bird had necroti c enteriti s caused by Clostridi11111
perfi-ingens.
8.146. Liver. Cholangiohepatitis. 18-month-old backyard
chicken. Portal tract shows bile du ctule with heterophils in th e
cen ter and marked peridu ctular concentri c fibrosis. There is dense
infiltrate of g ranulocytic leukocytes a nd mononuclear infl a mmato ry
cells in the a rea . The ca use was undetermined. Note the portal
ve nul e and the branch of the hepati c arte ry in th e portal tra ct.
398 I American Assoc iat ion of Avia n Patho logists
8.147. Liver. Cholangitis caused by Clostridi11111 pe1fri11gem.
28-day-old broiler breeder. Acute c ho lang itis res ults in marke,
di stenti o n of intrahepatic bile duct with ce llular exudate of in tac
a nd necrotic heterop hils and mononuclear inflammato ry cell s. T h,
lining e pithelium is marked ly attenuated.
8.148. Liver. Cholangiohepatitis caused by Clostridium
pe1fri11ge11s. 34-day-old broiler. T he acellular, eos in ophilic
necro ti c debri s in th e lumen of bile duct is rimmed by multinucleated
g iant cells and surrounded by fibrou s ti ss ue followed by zo ne of
lymphop lasmacytic infiltrate. There is pro liferation of bile du ctules
a t th e periphery of the lesio n.

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8.149. Liver. Cholangiohepatitis caused by Clostridium
pe1:fi'i11ge11s. 34-day-old broiler. Portal area has dense cellular
infiltrate of predominantly lymphocytes and plasma cells with
so me myeloid cell s. There are fibroplasia and proliferation of bile
ductu les. Bile ductule is distended with heterophils.
8.150. Liver. Cholangiohepatitis caused by Clostridium
perfi-i11ge11s. 34-day-old broiler. Hi gher power vi ew of area 8. 149
showing portal area with dense lymphoplas macyti c infiltrate and
marked bile ductular proliferation.
Hepatobi/ia,J' System
8.151. Extrahepatic bile duct and gallbladder.
Cholangiocholecystitis caused by Clostridium pe1ji·i11ge11s.
28-day-old broiler. Extrahepatic bile duct is filled with
heterophilic ex udate and its wa ll is infiltrated by many mononuclear
inflammato1y cells. There is segmental loss of the lining epi thelium .
The fibrinocellular exudate around the duct extends to the necrotic
wa ll of the ga llbladder (bottom ri g ht of the image) .
8.152. Extrahepatic bile duct and gallbladder.
Cholangiocholecystitis caused by Clostridium pe1ji·i11ge11s.
28-day-old broiler breeder chicken. Higher-power view of area in
8. I 51 sho w ing necrosis of th e lining ep ithelium of the ga llblad de r.
Many large, rod-shaped bacteria are assoc iated with the necrotic
ep ithelium . Culture of the ga llbladder content y ielded pure, heavy
growth of Clostridi11111 p erfhngens.
Avian Histopathology (4 11, Ed ition) I 399
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8.153. Gallbladder. Cholecystitis caused by Clostridi11111
pe1fi'i11ge11s. 34-day-old broiler. Layer of necrotic cellular debri s
is on the surfac e of th e ga llbl adder epithelium, which a ppea rs intact
but hyperpl asti c and proba bl y is rege nerating. Increased numbers
of m ononuclear cells are in the mucosa I lamin a propria . C ulture of
the ga llbladder content yield ed pu re, heavy gro wth of Closlridi11111
Perfi'ingens.
8.155. Liver. Granuloma caused by filamentou s bacteria.
20-week-old turkey tom. Same case as 8. 153 . A nother caseous
granul oma w ith hi stomorphologica l fea tures similar to those
desc ribed in 8.1 53. Note the lymph oid fo llicles at th e periph ery of
the gra nul oma.

8.1 54. Liver. Granuloma caused by filamentou s bacteria. 8.156. Liver. Granuloma caused by filamentous bacteria.
20-week-old turkey tom . Gra nul oma consists of a ce nter of 20-week-old turkey tom. Higher-power view of the gra nuloma
necroti c cellular debri s surrounded by large multinucleated giant in 8. 153 show ing large multinucleated giant cells with abu nda nt
cells fo ll owed by a zo ne of lympho hi sti ocyti c infiltrates, with vac uolated cytopl as m surrounding centra l necrotic cellular debris.
lymph oid fo llic les at the periphery. The multinucleated g iant cells
are large and have abundant vacuolated cytoplasm. The history
prov ided w ith the case stated th at li vers from a flock of turkey to ms
were condemned at th e process ing plant beca use they have white
spots . T he morphology of the hepatic gra nul oma arouses suspicio n
of in fec ti o n w ith E11bac/eri11111 lor/11os11111 .

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8.157. Liver. Granuloma caused by filamentous bacteria.
20-week-old turkey tom. Waithin-Starry stain reveals numerous
filamentous , to1tuous organisms in the granulomas. The organisms
are morphologically compatible with Eubacterium lor/uos11111 that
ca uses hepatic granulomas in turkeys.
8.158. Gallbladder. Cholecystitis. 4-day-old broiler. The
gallbladder mucosa is multifocally ulcerated and replaced by
necrotic debris and fibrin, with granulation tissue proliferation at the
base of the ulcers.
HepatobilimJ> System
8.159. Gallbladder. Cholecystitis. 4-day-old broiler. Same
gallbladder as 8.158. Higher-power view of mucosa! ulcer showing
numerous rod-shaped bacteria in the fibrinonecrotic debris. The
bird had bacterial septicemia caused by Pseudo111011as aernginosa.
8,160. Gallbladder. Cholecystitis caused by Campylobacter.
14-week-old broiler breeder pullets. Multifocal superficial
mucosa! necrosis and replacement with dense necrotic debris.
Culture of the bile yielded heavy growth of Ca111pylobaclerjeju11i.
Avian Histopathology (4 th Edition) I 401
 Tal,see11 Abdul-Aziz • Oscar J. Fletcl,er

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8.161. Ga llbladder. Cholecystitis caused by Campylobacter.
14-week-old broiler breeder pullets. Higher-power view of
area in 8. 160 showing the mucosa( necrosis and necroti c debris.
Warthin Starry stain revea led abundant intra lesional g ull -w ing-
shaped and spiral-shaped bacteria morph ologica ll y compatible with
Campylobac/er spp.
8.163. Liver. Mycobacteriosis. Quail. Higher-power vi ew
of o ne of the nodules in 8. 162. The nodule is composed of large
epithe lio id cells with abundant eosi nophili c cytoplasm. The center
of the nod ule is undergo in g necro sis and contains many heterophi ls.

8.162. Liver. Mycobacteriosis. Quail. Hepatic paren chyma is 8.164. Liver. Mycobacteriosis. Quail. Caseous gra nul oma
replaced by nodular, well-demarcated agg regates of epitheli oid consists of a center of caseo us necrosis surrounded by wide zone of
macroph ages with abundant eos inophili c cytoplasm . epithelioid macrophages. Multinuc leated giant cel ls are present at
the marg in of the caseous debri s.

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8.1 65. Liver. Mycobacteriosis. Quail. Fite stain, an acid-fast
stain used to demonstrate ac id-fast bacteri a, revea ls c lusters of acid-
fa st-positi ve (red) stainin g of bacteri a, many of which appear to be
within the cytoplasm of epithelioid macrophages.
8.1 66. Liver. Mycobacteriosis. IS-year-old pionus parrot.
Discrete, well-demarcated histiocyti c gra nul omas composed of
large epitheli oid macrophages and fo reign-body type multinucleated
giant ce lls.
H epatobilir11J• System
8.167. Liver. Mycobacteriosis. 15-year-olcl pionus parrot.
Hi gher-powe r view of we ll-demarcated gra nul oma composed
mostly of large fo reign-body type g iant cells. A lso present are so me
epithelioid mac roph ages with abundant eosinophilic cytoplasm.
8.168. Liver. Mycobacteriosis. 15-year-olcl pionus parrot.
This well-demarcated granuloma is co mp osed of epithelio id
macrophages w ith abundant eosinophilic cytoplasm. Note the
abse nce of multinucleated giant ce ll s. Histi ocyti c gra nul omas 111
bi rds should aro use suspicion of mycobacteri osis.
Av ian Histo pathology (4 th Editi on) I 403
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8.169. Liver. Chlamydiosis. 2-month-old conure. Area of
di sruption of the hepati c ti ss ue due to hepatocyte degenerati on and
necrosis.
8.170. Liver. Chlamycliosis. 2-month-old conure. Area of
hepatocyte degeneration and necrosis with infiltration of some
granulocytic and mononuclea r leukocytes. Erytlu-ophagocytosis,
likel y by Kupffer cells, is in the lesio n.
404 I America n Association of Avian Pathologists
8.171. Liver. Chlamydiosis. 2-month-old conure. Area of
degeneration and necrosis of hepatocytes, with mild mononuclear
inflammatory infiltrates. There is a large cell, likely hepatocyte,
with basophilic smudge indicative of intracytoplas mi c Chla111ydia
organisms. Definitive diagnosis of Chla111ydiosis can only be made
histol ogically if intracellular Chlamydia is identified in the tissue.
8.172. Liver. Chlamydiosis. 2-month-old conure. Hi gher-power
view of area in 8.1 7 1 demonstrating hepatocyte degenera tion and
necrosis and the basop hilic, smudgy appearance of Ch/a111ydia
within the cytoplasm of a cell (likely hepatocyte ).

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8.1 73. Liver. Chlamydiosis. 8-week-old cockatiel. Focal area
of hepatocellular necrosis with macrophage infiltration and some
intralesional hemosiderin pigment within macrophages.
8.1 74. Liver. Chlamydiosis. 8-week-old cockatiel. Enlarged
cell , likely hepatocyte (arrow), has basophilic smudge consistent
with intracytoplasmic Chlamydia organisms.
HepatobilimJ' System
8.175. Liver. Chlamydiosis. 2-month-old conure. Warthin-
Starry staining. With Warthin-Starry stain, Chlamydia appears
as black, discrete fine granules in the cytoplasm of infected
hepatocytes. The boxed cell is a hepatocyte with intracytoplasmic
Chlamydia organisms.
8.176. Liver. Microsporidiosis. 18-month-old lovebird. Small
focal area ofcoagulative necrosis ofhepatocytes, with accumulation
of some hemosiderin granules, probably in the cytoplasm ofKupffer
cells. Based on molecular phylogenetic analysis, microsporidia are
not considered protozoa but rather closely related to fungi.
Avian Histopatho logy (4' 11 Edition) I 405
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8.177. Liver. Microsporidiosis. I 8-month-old lovebird. 8.179. Liver. Microsporidiosis. 18-month-old lovebird. This
Small focal area of necrosis and loss of he patocytes, with marked legend is also applied to 8. 178. Hepatocyte with di sp laced nucleus
accumulation of bemosiderin gra nul es, probabl y in the cytoplasm and cytoplasm fill ed and di stended with th e mi crosporidiu m
ofKupffer cells. E ncepha/itozoon he//e111 . Note the accumul at ion of hemosideri n
gran ul es and probab ly Joss (necrosis) of few hepatocytes in the
vicinity of the infected ce ll.

8.178. Liver. Microsporidiosis. 18-month -old lovebird. See the 8.180. Liver. Microsporidiosis. 18-month-old lovebird . See the
lege nd of 8. 179. legend of 8.18 1.

406 I American Association of Avian Pathologists


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8.1 81. Liver. Microsporidiosis. 18-month-old lovebird.
Th is legend is also applied to 8. 180. The thin-walled cyst-like
structure packed with fine basophilic granules is a cluster of the
microsporidium Encephalitozoon hellem within the distended
cytoplasm of hepatocytes. Note the displ acement of the nucleus of
the hepatocyte in 8.181.
8. 182. Liver. Microsporidiosis. 18-month-old lovebird. Gram
sta ining. Spores of Encephalitozoon are Gram-positive. The spores
are usu ally difficult to identify in H&E stained sections.
Hepatobilimy System
8.183. Liver. Mycotic hepatitis. 7-week-old broiler breeder
pullet. One large and several small granulomas, each with center
of caseous necrosis rimmed by multinucleated giant cells and
surrounded by fibrous tissue and cellular infiltrates of predominantly
macrophages. Fragments of fungal hyphae are present among the
caseous debris and shown with H&E stain in the left corner insert.
The right corner inse11 shows hyphae with Gomeri Methenamine
Silver (GMS) stain.
8.184. Liver. Histomoniasis. 4-week-old broiler breeder male.
Hepatic tissue is severely disrupted by numerous trophozoites of
Histomonas meleagridis, which appear as individual or groups of
eosinophilic round bodies located within clear lacunae. In well
preserved tissues, as in this section, darker stained nucleus is
discernible in the trophozoites. Inflammatory infiltrate is absent or
minimal in this early lesion.
Avian Histopathology (4' 11 Edition) I 407
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8.185. Liver. Histomoniasis. 4-week-old broiler breeder 8.187. Liver. Histomoniasis. 87-day-old turkey. Severe
male. Illustrated is the characteristic hi stol ogic morphology of di srupti on of the hepa ti c tissue by num ero us trophozoites of
trophozoites of Histo111011as 111eleagridis. The tropbozo ite is round Histo111011as me/eagridis located with lacun ae, wi th infiltra ti on of
in shape, co ntains darkl y stai ned nucleus, and is surrounded by lymphocytes and macrop ha ges.
c lear space. Trophozoites lose their morphol ogic detai ls and may
be diffi cult to identify in auto lyti c tissues.

8.186. Liver. Histomoniasis. Peafowl. Focal area of necros is 8.188. Liver. Histomoniasis. 4-week-old broiler breeder pullet.
co ntainin g numerou s round-shaped trophozoi tes of Histo111011as PA S stain . Trophozoites of Histo111011as 111e!eagridis stains positi ve
111e!eagridis. Note that the organisms are located within lacunae. with PAS stain, especiall y in well preserved tissues.

408 I Amer ican Association of Avian Pathologists

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8.1 89. Liver. Histomoniasis. 4-week-old broiler breeder 8.191. Liver. Toxoplasmosis. Vulture. Focal area of necrosis
pu llet. Several Histomonas organisms are associated with marked with loose inflammatory infiltrate of mononuclear and granulocytic
lyrnphohistiocytic infiltrates . Single, two, or multiple organisms are leukocytes. Tissue cysts ofToxoplasma gondii are in the lesion.
seen within lacunae.

8.190. Liver. Histomoniasis. 11-week-old turkey. In this advanced 8.192. Liver. Toxoplasmosis. Vulture. Higher-power view of
lesion, there is loss ofhepatocytes, with several multinucleated cells area of necrosis with several intralesional tissue cyst of Toxoplasma
containing multiple trophozoites of Histomonas in cytoplasm. gondii. The tiny basophilic bodies inside the cysts are bradyzoites.

Avian Histopathology (4 th Edition) I 409

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8.193 . Liver. Atoxopla smosis. 2-month-old canary. Focal
area of loss of hepatocytes and replacement by mononuclear
inflammatory infiltrate.
8.194. Liver. Atoxopla smosis. 2-month-old canary. Foca l
area of mild mononuclear inflammatory infiltrate that disrupts the
hepatic parenchyma , wi th small vacuole containing basoph ilic
dots representing merozoites of Atoxopla.1·11w sp. (l sospora sp.)
in the cytopl asm of mononuclear inflam matory cell (circle).
Toxo pl as mosis was ruled out by immunohistochemica l sta ining.
4 10 I Ame ri can Assoc iati on of Avian Pathologists
8.1 95. Liver. Atoxop las mosis. 2-mo nth-old canary.
Mononuclear infl ammatory infiltrate involving porta l tract
and adjacent area of hepatocyte loss. There is small cyst-like
structure filled with basophi lic dots representing merozoites of
A toxoplas111a sp. (lsospom sp .) in the cytoplasm of mononuclear
ce ll can be identified (c ircle) . Toxop lasmos is was ruled out by
immunohistochemical staining.
8.196. Liver. Sarcocystosis. 12-yea r-old cockatoo. Sinusoids
are expanded by mononuclear infiltrates composed of plasma cell s,
lymphocytes, and macrophages. Merozoite-containing meronts of
Sarcocystis sp. (likely Sarcocystis fa lcatula) were present in the
lungs.
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8.1 97. Liver. Sarcocystosis. 12-year-old cockatoo. Higher-power 8.199. Liver. Aberrant migration of Ascaridia co/11111bae larvae.
view illustrating the accumulation of plasma cells, lymphocytes, Pigeon. Dense infiltrate of granulocytes is associated with giant cell
and macrophages in sinusoids. Merozoite-containing meronts of granuloma. Note the large multinucleated giant cells constituting
Sarcocystis sp. were present in the lungs. the granulomas.

8. 198. Liver. Sarcocystosis. Hawk. Accumulation of plasma 8.200. Liver. Aberrant migration of Ascaridia co/11111bae larvae.
cells, lymphocytes, and macrophages around terminal hepatic Pigeon . Two giant-cell granulomas have center of necrotic debris
venule, with disruption of the perivenular hepatocytes. Note the or possibly degenerate larvae of A. co/11111bae.
bile ductule with bile (ductular cholestasis).

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 Tahsee11 Abdul-A ziz • Oscar J. Fletcher
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8.201. Liver. Aberrant migration ofAscaridia col11111bae larvae.
Pigeon. Two section s o f ascarid larvae (a rrows) are in the li ver, and
they appea r to be located within sinusoids.
8.202. Liver. Aberrant migration of Ascaridia columbae. Pigeon.
H epati c ti ss ue in the mi grati on tract of thi s aberrant Ascaridia is
de stroyed. The border of the tract is co mposed of necroti c debris
surrounded by cellular infilt rate of predominantl y macrophages.
There are numerous of bacteri a in the tract (the basophilic granul ar
material ).
41 2 I Ameri ca n Assoc iatio n o f Avi an Path o log ists
8.203. Liver. Aberrant migration of adult Ascaridia col11111bae.
3-year-old pigeon. Secti on of adult asca rid nematode (A. co/11111 bae)
is w ithin what was interpreted to be distended, necroti c bile duct.
The necroti zing cholangitis is characteri zed by severe necrosis of
the bile duct wall with acc umulati on o f caseous debri s rimmed by
multinuclea ted giant cells. The brown-green materi al is bile. There
are ce llular infiltrate in the parenchyma around the duct. Adul t
asca rids in the duodenum enter the bil e duct opening and reach the
li ver. Wo rm s may al so be fo und in the ga llbladder.
8.204. Liver. A berrant migration of adult Ascaridia columbae.
3-year-old pigeon. Secti o n of degenera te adult asca rid surrou nded
by cellular exudate is in th e lumen of di stended maj or intra hepatic
bile duct. There is marked periductal fi brosis. The ductal e pithelium
is foca ll y eroded.

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8.205. Liver. Aberrant migration of adult Ascaridia col11111bae.
3-year-old pigeon. Section of adult ascarid nematode (A. colwnbae)
is within the lumen of distended bile duct with necrotic wall. This
small intestine of the pigeon was heavily infested with Ascaridia sp.
8.206. Liver. Aberrant migration of adultAscaridia sp. 11-week-
old chukar. The severe necrosis and hemorrhage of bile ducts in
portal area are caused by aberrant migration of adult Ascaridia from
the duodenum to the liver through the bile duct opening. The blue
areas among the eosinophilic necrotic debris are bacterial colonies.
Bacteria are carried by ascarids and cause further damage.
Hepatobilic11J1 System
8.207. Liver. Aberrant migration of adultAscaridia sp. 11-week-
old chukar. Sections of adult Ascaridia in intrahepatic bile ducts
are associated with marked fibroplasia , necrosis, accumu lation of
caseous debris, and bile ductular proliferation.
8.208. Liver. Aberrant migration of adult Ascaridia sp.
11-week-old chukar. Section of adult ascarid is occupying a space
in the hepatic tissue. In this case, the ascarid does not seem to be
within bile duct. Note the absence of inflammatory response or
necrosis.
Avian Histopathology (4 th Edition) I 413
 Tahseen Abdul-Aziz • Oscar J. Fletcher
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8.209. Liver. Schistosomiasis. Swan . Degenerate schistosome
egg is surrounded by foreign body-type multinucleated giant cells.
The schistosome infection was likely caused by Trichobilharzia sp.
8.210. Liver. Schistosomiasis. Adult Muscovy duck. Within the
portal tract, the branch of the portal vein has marked myointimal
hyperplasia, with virtual occ lusion of the lumen. Bile ductule (short
arrow) and branches of the hepatic artery (long arrows) are shown.
4 14 I American Association of Av ian Pathologists
8.211. Liver. Marek's disease. 2-year-old backyard chicken.
There is mild bile duct hyperplasia and lymphocytic infiltratio n
of the portal tract. Multifocal , perivascular and random dense
infiltrates of lymphoid tumor cell is characteristic lesion of Marek 's
disease.
8.212. Liver. Marek's disease. 2-year-old backyard chicken.
Higher-power view of area in 8.207 showing the perivascular
infiltrate of lymphoid cel ls.

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8.2 13. Liver. Marek's disease. One-year-old backyard chicken.
Mu ltifocal and coalescing, well-delineated, irregularly shaped
areas of effacement and replacement of the hepatic tissue by dense
infiltrates of lymphoid cells. Most of infiltrates appear to be around
venules. See the next four figures .
8.214. Liver. Marek's disease. One-year-old backyard
chicken. This is higher-power view of area of dense population of
pleomorphic lymphoid cells. Several mitotic figures are present.
Hepatobilimy System
8.215. Liver. Marek's disease. One-year-old backyard chicken.
Higher-power view showing the pleomorphism of the lymphoid cell
infiltrate in Marek's disease.
8.216. Liver. Marek's disease. One-year-old backyard chicken.
Immunohistochemical staining for the T-lymphocyte marker CD3
shows positive cytoplasmic staining of the lymphoid cells for
this marker. The lymphoid infiltrates of Marek's disease consists
predominantly ofT-lymphocytes.
Avian Histopathology (4 th Edition) I 415
 Ta!tsee11 Abdul-Aziz • Oscar J. Fletcher

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8.217. Liver. Marek's disease. 2-year-old backyard chicken .
On th e left of the image is the lumen of terminal hepatic ve nul e
(ce ntral venule) . The wall of the venule is infiltrated and effaced by
dense infiltrate of lymphoid cells. Infilt ra ti o n of the wall s of hepati c
and portal venules with lymph oid cell s is characteristic fea ture of
Marek's disease.
8.219. Liver. Marek's disease. Backyard chicken. Segmentally
effac in g the wall of terminal hepatic venule and adj acent hepatic
parenchyma is well-del ineated dense infiltrate of pleomorphic
lymphoid cells.

8.218. Liver. Marek's disease. Backyard chicken. Dense
population ofpleomorphic lymphoid cells infiltt:ates seg ment of the
wall of terminal hepati c venul e and extends to the adjacent hepati c
parenchyma, forming nod ular aggregate. The bird had the neu ra l
form ofMa rek's disease.
8.220. Liver. Marek's disease. 5-month-old backyard chicken.
Dense infiltrate of pleomorphic lymphoid cells involving the wa ll
of portal venule and narrow zone of th e hepatic tissue around
it. Dense lympho id infiltrates consistent with Marek's di sease
were present in other viscera l organs, particularly the lun gs and
pancreas. The diagnosi s of Marek's di sease was confirmed by
immunoh istochemi stry (sta ining for CD-3 marker).

416 I American Association of Av ian Pathologists


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8.221. Liver. Marek's disease. 5-month-old backyard chicken.
Higher-power view of the lesion in 8.220 demonstrating the
pleomorphic population of lymphoid cells.
8.222. Liver. Lymphoid leukosis. 30-week-old broiler breeder
hen. The hepatic parenchyma is almost totally effaced and replaced
by dense, fairly monomorphic population oflymphoblast-like cells.
Only straps and groups of atrophied hepatocytes are present.
Hepatobifi(//y System
8.223 . Liver. Lymphoid leukosis. 30-week-old broiler breeder
hen. Higher-power view of area in 8.222 showing the fairly
monomorphic population oflymphoblast-like cells that replaces liver
parenchyma. Immunoreactivity to CD3, seen with T lymphocytes,
was present only in the cytoplasm of only rare neoplastic lymphoid
cells ; this indicates that the neoplastic lymphoid cells are of B cell
lineage.
8.224. Liver. Lympiloid leukosis. 30-week-old broiler breeder
hen. Same liver section as 8.223 . Immunohistochemical staining
for the B-lymphocyte marker PAX5 shows positive nuclear staining
of the lymphoid cells for this marker. The lymphoid infiltrates of
lymphoid leukosis consists predominantly ofB-lymphocytes.
Avian Histopathology (4 th Edition) I 417
 Tahsee11 Abdul-Aziz • Oscar J. Fletch er
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8.225. Liver. Myelocytomatosis. 30-week-old broiler breeder
hen. Area in the liver is effaced and rep laced by immature mye loid
cells with characteristic intracytoplasmi c eos inophilic granul es and
round , non-lobulated nuclei with prominent nucleoli.
8.226. Liver. Myelocytomatosis. 30-week-old broiler breeder
hen. Higher power view of mye loid cells demon strating th e
characteristic intracytoplasm ic eosinophilic gra nules.
418 I Ameri ca n Association of Avian Patholog ists
8.227. Liver. Myeloproliferative disease. 2-year-old budgerigar.
Hepa ti c parenchyma is infiltrated and effaced by gra nul ocytic
mye lo id cells (immature gra nulocytes).
8.228. Liver. Myeloproliferative disease. 2-year-old budgerigar.
Higher-power v iew showin g g ranul ocytic mye loid cells at di frerent
stages of differentiati o n that include large blast cells and myelocytes
with characteristic eos inophilic cytoplasmic granules. A bnormal
proli fera ti on of gra nulocytic mye lo id cells occurs in the bone
marrow, which should be exa min ed hi stolog ica lly to confirm the
di agnosis.

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8.229. Liver. Metastatic adenocarcinoma. 3-year-old backyard
chicken. Nodule of metastatic adenocarcinoma of ovarian origin.
The bird had ovarian adenocarcinoma, with extensive intracoelomic
metastasis.
8.230. Liver. Metastatic adenocarcinoma. 3-year-old backyard
chicken. Terminal portal venule is distended with tumor embolus.
Small tumor nodules are seen in the upper right area of the figure .
HepatobilimJ' System
8.231. Liver. Adenoma or microhamartoma of bile ductules.
81-day-old meat-type tom turkey. Area in the liver lacks
hepatocytes and consists only of well differentiated bile ductules of
varying shapes embedded within dense fibrous stroma and lined by
well differentiated bile ductular epithelium.
8.232. Liver. Intrahepatic cholangiocarcinoma. 5-year-old
backyard chicken. The neoplasm is composed of ductal structures
and pockets of cells embedded in fibrous stroma. The ductular
structures are of irregular sizes and shapes and lined by epithelium
of single or multiple cell thickness. Necrotic cells are seen in the
lumens of some ductules.
Avian Histopathology (4 th Edition) I 419
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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8.233. Liver. Intrahepatic cholangiocarcinoma. 4-year-old
backyard chicken. Well-differentiated ductal structures in dense
fibrou s stroma containing mixed inflammatory infiltrate. The single-
layer epithelium is low cuboidal and show only mild cellular and
nuclear pleomorphism . The nuclei are large and have prominent
nucleoli. Proteinaceous material is in the lumens of some ducts.
8.234. Liver. lntrahepatic cholangiocarcinoma. 4-year-old
backyard chicken. Same case as 8.233. In this area, the neoplastic
ducts are dilated forming cystic structures and contain proteinaceous
material. Note the inflammatory infiltrate in the abundant fibrous
stroma.
420 I American Association of Avian Pathologists
8.235. Liver. Intrahepatic cholangiocarcinoma. 4-year-old
backyard chicken. Same case as 8.233. The neoplastic bile ducts
are tortuous and appear to be anastomosing. There are cellular
and nuclear pleomorphism, loss of nuclear polarity, and crowding
and foci of piling of nuclei . The nuclei of some cells are open or
vacuolated and have marginated chromatin and nucleolus. The
fibrous stroma is loose and edematous.
8.236. Liver. lntrahepatic cholangiocarcinoma. 4-year-old
backyard chicken. Same case as 8.233. The ductal struct·ures
are less defined than in other areas. This likely represe nts early
formation of ductal structures by proliferating neoplastic ductular
epithelium . Cellular and nuclear pleomorphism and c lustering
and haphazard arrangement of nuclei are prominent. The nucl ei of
several cells are open or vacuolated and have marginated chromatin
and nucleolus . Note the abundant fibrous stroma .

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8.237. Liver. Hemangiosarcoma. 12-year-old parrotlet.
Hepatic tissue is effaced and replaced by neoplastic tissue composed
of immature endothelial cells that form small clefts, some of which
contain red blood cells. Group of degenerate hepatocytes are seen
at the upper left corner. The bird had hemangiosarcoma in other
organs and tissue, and the primaiy site of the neoplasm could not
be determined.
8.238. Liver. Hemangiosarcoma. 12-year-old parrotlet. Same
case as 8 .23 7. In this area, the neoplastic tissue is highly cellular and
the vascular clefts are not as distinguished as in 8.237. There is mild
ductular reaction in the area. The hepatocytes and the bottom of the
figure are swollen and have homogenous, eosinophilic cytoplasm.
Hepatobi/ia,J' System
8.239. Liver. Hemangiosarcoma. 12-year-old parrotlet. Higher-
power view of area in 8.238 demonstrating the high cellularity of
the neoplasm and the immature endothelial cells that tend to form
vascular spaces containing red blood cells.
8.240. Liver. Malignant melanoma. 3-year-old backyard
chicken. Large region of hepatocytes is replaced by neoplastic
tissue composed ofmelanocytes with melanin pigment. The cellular
details of some melanocytes are obscured by the large amounts of
melanin pigment in the cytoplasm. The chicken also had melanomas
in the lung and on the intestinal serosal surface.
Avian Histopathology (4 th Edition) I 421
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VetBooks.ir
CHAPTER
Urinary System
Tahseen Abdul-Aziz • Oscar J. Fletcher
Anatomy and Histology
The urinary system consists of the paired kidneys and ureters. The
kidneys lie on either side of the vertebral column and are embedded
in the fused synsacrum (renal fossa). The ureters empty into the
cloaca. Each kidney has tlu·ee divisions - cranial (anterior), mid-
dle; and caudal (posterior). The boundaries between these divisions
are not always distinct. The outer surface of the divisions are not
smooth but rather have small projections, which represent the renal
lobules. Renal lobules, are the architectural unit of each division,
thus are also called renal units. Numerous lobules are distributed
throughout the kidney. A group of lobules that drain into the same
secondary branch of a ureter is called a lobe. Each lobule has a wide
cortical region and tapering medullaty region (medullaty cone). The
distinction between cortex and medulla is not well-defined in birds
in contrast to the clear distinction in mammals. The number of
medullary regions or cones varies among species and are greater in
avian species that are successful at conserving water. The cortical
area of each lobule is composed of closely packed neplu-ons, blood
vessels, initial collecting tubules, and small amounts of interstitial
connective tissue. Each nephron consists of the glomerulus (renal
corpuscle), proximal convoluted tubule, and distal convoluted tubule.
Nephrons in the avian kidney are of two basic types: those with
and those without loops of Henle. Non-looped nephrons are reptil-
ian types. They are most numerous constituting 70% or more of
the nephrons. Nephrons with loops of Henle are manunalian type
and are capable of concentrating urine using a mechanism similar to
that of mammals of counter-current flow to the collecting tubules
and collecting ducts in the medullary cones. Glomeruli of reptilian
neplu-ons are smaller with fewer mesangial cells than glomeruli of
mammalian nephrons and are located more superficially in the
lobules. The distal tubule of each reptilian nephron empties into a
primaty (initial) collecting tubule within the cortex that connects to a
perilobular collecting tubule at the periphery of the c01tex of the lob-
ule. There also are transitional neplu·ons. Distal tubules of transitional
nephrons empty into secondary collecting tubules .
In some histologic sections, renal lobules appear as pear-shaped
areas that may contact the surface or are located at variable distances
from the surface. Each lobule has a cortical region and a medullaty
cone (medullaty tract). The histologic arrangement of a cortical lob-
ule from the periphety to the center is: (I) a surrounding network of
collecting ducts and interlobular veins of the renal pottal system, (2)
a zone of proximal convoluted tubules, (3) a zone ofglomeruli, (4) a
zone of primarily distal convoluted h1bules, and (5) a central efferent
9
vein that drains the lobule. A branch of the intra lobular renal arte1y
may be seen midway between the central vein and the peripheral
network of veins. Medullary cones contain collecting ducts, looped
h1bules of the manunalian neplu-ons, ureteral branches, and a network
of blood capillaries in interstitial connective tissue.
Glomeruli consist of supporting cells called the mesangium,
capillary loops, and the visceral and parietal epithelium. Between
the visceral and parietal layers of the capsule lies the capsular (Bow-
man 's) space. The surface ofglomeruli (visceral layer) is covered by a
single layer of irregular cells, almost cuboidal in shape, containing
large nuclei. The parietal epithelium of glomeruli usually is squa-
mous, but is cuboidal in about I 0% of 2-5 week old male broilers.
The epithelium of the proximal tubules is higher than that of the
distal tubules and has a brush border that is PAS-positive. Distal
tubules have a low cuboidal epithelium without a brush border. Col-
lecting tubules and collecting ducts have epithelial cells with api-
cal acid mucopolysaccharide (mucin) granules that stain positive with
PAS and alcian blue stains. Mucin and protein are required to keep
uric acid in the form of variable-sized spheres that prevent precipita-
I
tion and clogging of the collecting tubules. The juxtaglomerular ap-
parah1s (JOA) is a specialized region where the afferent arteriole is
in contact with the distal convoluted tubule of that nephron. The
JOA includes the macula densa, the region of elongated or larger
epithelial cells in this contact zone of the distal convoluted tubules,
and specialized juxtaglomerular cells (lacis cells) located between
the vascular pole of the glomerulus and distal convoluted h1bules.
Extra-glomerular mesangial cells in this location are the third com-
ponent of the JGA in both reptilian and manunalian glomeruli. The
JOA is believed to regulate glomerular filtration rates.
Ureters and their primaty branches are lined with non-ciliated
pseudostratified columnar epithelium, with some cuboidal basal
cells. The apices of the colunmar cells are filled with numerous
vacuoles containing PAS-positive mucopolysaccharide. The epithe-
lium is surrounded by a thick layer of smooth muscle consisting of
an inner longitudinal layer and outer circular layer. External to the
muscular layer is a thin adventitia of loose connective tissue.
Kidneys of young birds contain multiple areas of immature
nephrons . These must be recognized as normal structures and not
interpreted as lesions. Immature nephrons are more frequently
found beneath the capsule, but some are scattered in the renal
parenchyma. Foci of lymphoid cells are normal in the renal pa-
renchyma and care must be exercised before interpreting these
lymphoid aggregates as lesions. Focal areas of extramedullary
Avian Histopathology (4' h Edition) I 423
 Tahseeu Abdul-Aziz • Oscar J. Fletcher
hematopoiesis can be observed and are especially common in the
kidneys of pigeons.
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Kidneys receive blood from both the aorta and renal portal ve-
nous system that drains the legs and lower body. Blood from the
aorta is delivered to the glomeruli through the afferent arterioles.
Blood supplying the tubules of the nephrons, the collecting tubules and
ducts , and interstitial tissue comes from the efferent arterioles as
well as the renal pmtal system. This dual blood supply ensures that
glomerular damage does not cause injury to the tubular components
of the nephrons.
Birds, like reptiles, are uricotelic, i.e ., the end product of ni-
trogen metabolism is excreted as uric acid, which is synthesized in
the liver and excreted by the kidney. Uric acid is excreted from
the blood mainly by tubular secretion but some is also removed by
glomerular filtration. Urate forms colloid with concentrations up
to a 2% solution, which allows it to move through tubules, ducts,
and ureters. Precipitation can obstruct the collecting ducts. In the
ureters, urine is viscous and stringy. Mucus secreted by ureter epi-
thelium is needed to lubricate movement ofurate through the ureter.
Gross observation of enlarged kidneys is frequently not corre-
lated with the presence of histologic lesions. Identification of mi-
croscopic lesions in avian kidneys is complicated by autolysis that
occurs rapidly after death . Epithelium of the proximal tubules is
affected first and characterized by detachment from basement mem-
branes. Nuclei become small and darkly stained (ka1yopyknosis), and
the cytoplasm may appear vacuolated or empty. Autolytic changes
are common in diagnostic laboratory material and should be ex-
pected in kidney samples collected from dead birds.
Pigments, Mineral, and Amyloid Deposits
Large, hyaline (eosinophilic) droplets of protein may accumulate in
I
the cytoplasm of epithelial cells of proximal convoluted tubules. The
accumulation of these droplets may occur when there is damage to
glomeruli that resulted in leakage of protein, or when there is protein
spillover into the glomerular filtrate. Fat droplets are sometimes seen
in the renal tubular epithelium. Brownish droplets of bile may be
present in the cytoplasm of tubular epithelial cells of birds with severe
liver damage. Hemosiderin granules may be seen in the cytoplasm of
renal tubules, especially birds with hepatic hemosiderosis. Accumu-
lation of hemoglobin in the renal tubules results from excessive de-
struction of erythrocytes (intravascular hemolysis). Excessive hemo-
globin is toxic to renal tubular epithelium and causes nephrosis called
hemoglobinuric nephrosis. Mineral deposits, usually in the form of
calcium salts, are found relatively frequently in the lumen of renal
tubules and may be associated with tubular necrosis. Amyloidosis is
characterized by deposition of a homogeneous eosinophilic material
in glomeruli, basement membranes of tubules and/or interstitial tis-
sues in cortices and medullae, with loss ofrenal tissue in severe cases.
Glomerulopathies
Glomerulopathy refers.to a group ofnon-inflammatmy lesions in glom-
eruli. They are classified according to the histopathologic appearance
of glomeruli. Three types of glomerulopathy are generally found in
poultiy: (I) proliferative glomerulopathy (POP) characterized histologi-
cally by increase in the size and cellularity of glomeruli due to increased
424 I American Association of Avian Pathologists
mesangial cells with or without recruitment of circulating macrophages,
(2) membranous glomerulopathy (MOP) characterized histologically
by increased thickness of the basement membranes of the capillmy
loops due to deposition of PAS- and silver stain-positive protein, and
(3) membranoproliferative glomerulopathy (MPGP) which is a com-
bination POP and MOP. The term mesangioproliferative is used to
denote POP that is characterized histologically by increased mesan-
gial cells only (without macrophages). In general, glomerulopathy
is not an etiology- or disease-specific lesion and should be interpreted
within the context of clinical histmy and gross and microscopic lesions
in other organs and tissues.
Glomerular morphology can be difficult to interpret. Mesan gial
cells may be increased or appear to be increased depending on the
plane of section. The mixed population of reptilian and mamma-
lian glomeruli can create confusion because of the differences in glo-
merular size and cellularity of the mesangium. Enlarged glomeruli
with ve1y cellular mesangium and enlarged visceral epithelial cells is
a response to estrogen in I 0- to 12-week-old chickens. Proliferative
glomerulopathy is a feature ofinumme-mediated injury. Mesang iop-
roliferative glomerulopathy may be seen in clinically normal broiler
chickens and in broilers affected with tenosynovitis caused by reo-
virus. Excess sodium chloride in the diet, systemic hypertension,
administration of desoxycorticosterone acetate, and aflatoxicosis in
turkeys and ducklings cause membranous glomerulopathy. Mem-
branous glomerulopathy may result from water deprivation or de-
hydration due to birds being sick, so that a direct cause and effect
relationship does not always exist between the primary disease and
renal lesion. Membranoproliferative glomerulopathy may be ob-
served in various diseases in chickens, including infectious bursa l
disease and Jvlycoplas111a ~ynoviae infections. A high incidence of
membranoproliferative glomerulopathy with variable degrees of
glomeru losclerosis (mesangial fibrosis) was found in the kidneys of
20- to 28-day old chickens affected with inclusion body hepatitis, an
Aviadenovirus infection. Membranous glomerulopathy in young
chicks caused by high dietary sodium chloride may progress to a
membranoproliferative lesion with epithelial crescent formation ,
and ends as glomerulosclerosis and periglomerular fibrosis. Glo -
merular lesions do not cause direct damage to the proximal and distal
tubules due to the dual blood supply (arterial and portal venous
system) as described above.
Baby Chick Nephropathy
Two types of lesions are seen in chicks with nephropathy (baby chick
nephropathy), which likely is caused by dehydration. One type is char-
acterized primarily by dilation ofureteral branches and collecting ducts
in medulla1y cones, with interstitial edema. The other type is character-
ized by tubular necrosis, urate deposition in renal parenchyma, and cel-
lular casts in renal tubules and ducts, with deposition ofurate on serosal
surfaces, especially the heait, in severe cases. Both types of lesions
may be found in kidneys. Turkey poults have a similar nepluopathy.
Visceral and Renal Gout
Urates are excreted by the active metabolic processes of renal tubu-
lar epithelium, so injury to this epithelium can cause hyperurice-
mia. Hyperuricemia can result in urate deposition on the surfaces

of visceral organs, especially the epicardium. These depos its are not
associated with an inflammato1y response and represent a terminal
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event. Urates dissolve in aqueous-based fixatives and leave a layer of
fa intly basophilic material on visceral surfaces.
The term renal gout is used for the subacute or clll'onic nephritis
that results when urates are released into the interstitium of the kid-
ney, resulting in damage to the renal tissues. Characteristic lesions in
renal gout include tubular necrosis, deposition of urate crystals, to-
phi formation, infiltration of lymphocytes, and interstitial edema or
fibrosis. The appearance oftophi (singular - tophus) depends on the
stage of development. Early lesions consist offeathe1y-looking baso-
philic urate deposits, with variable degrees of granulocytic response.
The site of urate deposition may be poorly defined or can be recogniz-
able as intratubular. In advanced lesions, tophi typically have a cen-
ter of a feathe1y, basophilic material (urate) rimmed by multinucle-
ated giant cells, with macrophages, lymphocytes, and fibroblasts at the
periphe1y. Some tophi may form a palisading granuloma-like pattern.
U rolithiasis
Urolithiasis is the formation of solid, stone-like, concretions of cal-
cium urate or monosodium urate in the kidneys. The ureters, ureter
branches, and major collecting ducts are dilated and filled with whit-
ish, firm or chalky stones. Blockage of urinary outflow results in
dilation of the collecting ducts and tubular necrosis, with variable
numbers of heterophils in some tubules. Fibrosis and atrophy and
loss ofrenal tissue occur in advanced cases . This condition is com-
monly found in turkeys and laying hens. The cause is not known,
but the condition has been attributed to water deprivation, excess
dietary calcium during the growing period, and nephrotropic strains
of infectious bronchitis virus. Vitamin A deficiency can cause squa-
mous metaplasia with keratin production in the ureters and lead to a
blockage and urolithiasis.
Obsh·uction of the ureter in birds does not result in hydronephro-
sis as it does in mammals because birds do not have a renal capsule,
the peritoneum forms the s111face covering of the kidneys. Without a
capsule, pressure necrosis does not occur in birds as it does in mam-
mals. However, kidney tissue atrophies and becomes fibrotic when the
ureter draining it becomes occluded. Remaining functional renal tissue
undergoes compensat01y hype1trophy. Microscopically, glomeruli and
tubular epithelium are enlarged.
Nephrosis vs Nephritis
Nephrosis is characterized by degenerative and necrotic changes in
the epithelium of renal tubules and ducts in the absence of appre-
ciable inflammation. Many infectious and noninfectious agents cause
neplu-os is in the initial stages. If damage to the epithelial lining is
mild and does not breach the basement membrane, there is little to
no inflammatory response and lesions are repaired. Histologic evi-
dence of repair include tubular dilation, epithelial hyperplasia, vari-
ation in the size of nuclei ( anisoka1yosis ), and increased mitotic fig-
ures. If the injurious agent persists, greater damage occurs. Severe
tubular necrosis with damage to the basement membrane results in
exposure of the interstitium and vascular compartments to necrotic
cellular debris and a subsequent inflammatory reaction. Progres-
sion of the lesion from nephrosis to nephritis is more rapid in birds
UrinlllJ' System
than in mammals due to the presence ofurates in the tubular debris.
Acute water-deprivation in chickens demonstrates this progression
of lesions: dilation of tubular lumen --> formation of intra-tubular
casts composed of urate spherules and sloughed epithelial cells -->
development ofurate crystals in tubular lumen--> damage to tubular
basal membrane --> exposure of interstitium to necrotic debris and
urate crystals --> damage to interstitium and inflammato1y response.
Proliferation of fibroblasts in the interstitium (interstitial fibrosis) is
evident in some cases of subacute and chronic nephritis .
Multiple foci of severe tubulointerstitial necrosis are com-
monly attributed to water deprivation in young and adult chickens .
Typically, there are relatively large, roughly spherical necrotic foci
composed of coalescing necrotic tubules that are replaced by amor-
phous eosinophilic debris containing variable numbers of intact and
necrotic granulocytes. Over time, macrophages and multinucleated
giant cells cover the surface of the necrotic debris. They appear as a
rim surrounding the central area of necrosis in microscopic sections .
Hyaline, eosinophilic or basophilic spherules are sometimes
seen in the lumen of tubules and they represent remnants of urates.
Tubular epithelium may show evidence of tubular regeneration.
Toxicities
Chemicals, some antimicrobials (e.g. , sulfonamides, aminoglyco-
sides), and mycotoxins cause nephrosis characterized by acute tu-
bular necrosis, which may evolve into nephritis if the affected birds
survive the initial injmy. Lead poisoning is diagnosed by finding
acid-fast intranuclear inclusions in renal tubular epithelial cells.
Cadmium, vanadium, methyl mercury, thallium, zinc phosphate, po-
tassium dichromate, uranium, 3-chloro-p-toluidine, aldrin, dieldrin,
alloxan, acetone, and phenol are tubular toxins. A brown pigment
that polarizes red located in the cytoplasm of epithelial cells in dam-
aged tubules is seen in ethoxyquin toxicity. Dimethylnitrosamine
causes mesangiolysis (loss of cellularity of the mesangium) in ducks .
Karyomegaly and anisokaryosis have been observed in the tubular
epithelium of turkeys with copper poisoning. Neplu·otoxic mycotox-
ins include aflatoxin, oosporein, orclu-atoxin, citrinin, and rubratoxin.
Aflatoxin causes membranous glomerulopathy as described above.
Oosporein, oclu·atoxin, and citrinin in particular are nephrotoxic and
can cause degeneration and necrosis of tubular epithelium. Ochra-
toxin usually causes liver lesions (necrosis or biliaiy hyperplasia) in
addition to tubu lar degeneration and necrosis, while oosporein le-
sions tend to be limited to the kidney. There are species variations
in susceptibility to some mycotoxins. For example, low doses of
citrinin cause tubular necrosis in turkeys and ducklings, but do not
cause lesions in chickens. However, higher doses of citrinin do cause
tubular necrosis in chickens. Ethylene glycol toxicosis is character-
ized by fan-shaped birefringent oxalate c1ystals in necrotic tubules.
Lesions caused by toxicities may be complicated by dehydration.
Infections
Viral infections
Neplu-itis caused by viral infections is typically lymphocytic and in-
terstitial. Usually there also is tubular degeneration and necrosis.
Virus-induced damage frequently is complicated by inflammation
that occurs due to the release of urates into the interstitial tissue.
Avian Histopathology (4 th Edition) I 425
 Tahseen Abdul-A ziz • Oscar J. Fletcher
Infectious bronchiti s virus (IBV) is the most common world-
wide cause of nephriti s in chickens . IBV strains vary in kidney
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tropism. The epithelium of distal and proximal tubular epithelium
and collecting duct epithelium are the sites of IBV replication . Le-
sions are focal to multifocal in di stribution with affected tubules
and ducts being distended and fill ed with mucus, urates, and cel-
lular casts. Vacuolati on, clumping of cytoplasm, and desquama-
tion of tubul ar epithelial cells are associated with a heterophilic re-
sponse that quickly becomes lymphocytic. Multifocal interstitial
lymphocytic infiltration with formation of nodular aggregates of
lymphoid cells is a characteristic feature of IBV infection. Miner-
alization of tubules also is common. A similar disease is caused by
a closely related IS-like coronavirus in pheasa nts.
Avian nephriti s virus causes similar interstitial lymphocytic
nephriti s in chickens with protein casts and mineral deposits in
renal tubul es. Lymphocytic interstitial nephritis is a characteristic
lesion of avian influenza virus in fec tion in chickens and pigeons
infected with avian paramyxovirus type I. Jntranuclear inclu-
sions of aviadenovirus and siadenovirus are incidental findin gs
in tubular epithelial cells of kidneys of severa l species of birds.
In companion birds, adenoviral inclusions may be so large that
resemble tissue stages of blood parasites; there is no associated
inflammation or eviden ce of tubular damage. Typically, adenovi-
ral inclusions are basophilic, homogenou s, contain one or more
deepl y stained foci, and completely fill enlarged nuclei. Systemic
herpesvirus infection in pigeons is characterized by intranuclear
inclusion s in renal tubular epithelial cells adjacent to or within foci
of necrosis and inflammation . Similar lesions with intranuclear in-
clusions are found in other ti ssues, especiall y liver. Polyomavirus
causes systemic disease. Viral inclusion bodies can be found in re-
nal tubular epithelium and glomeruli. Polyo ma virus inclusions are
I
large, opaque, faintly bluish or gray ish and fill markedly enlarged
nuclei . Inclusions are also present in other tissues.
Bacterial i11fectio11s
Fibrin thrombi in glomeruli (microthrombi) and interstiti al blood
vessels is indicative of bacterial septicemi a. Few or numerou s
bacteria may be found in thrombotic and non-thrombotic inter-
stitial blood vessels, and small bacterial colonies may be seen
lodged in capillary tufts of few to several glomeruli. Such les ions
are common in septi cemia caused by Erysipelas rhus iopathiae,
Streptococcus spp. , Staphy lococcus a11re11s , and sometimes
Pasteurella 111111/ocida . Occasionally, in cases of chl amydiosis,
there is extensive tubular de ge neration and necrosis, and Chla-
mydia organisms appear as a basophilic smudge in the cytoplasm
of tubular ep itheli al ce ll s. Interstitial nephriti s wi th a mixed het-
erophilic and lymphocytic cell infiltrates are typical of bacterial
septicemi as . Hete rop hili c inflammation ascending throu gh med-
ullary cones has been ca lled pye lonephriti s, but this term should
not be used because birds do not have a renal pelvis . Ascending
tubular nephriti s is a better term . The likely cause is an ascend-
ing bacteri al infecti on from the cloaca. A similar di sease process
ca n affect the ureter and lead to blockage. Escherichia coli is
iso lated most frequently from heterophilic tubular or tubuloint-
erstitial nephritis .
426 I American Association of Avian Pathologists
Fungal i11fectio11s
Fungal infections, most commonly Asperg illosis, may extend fro m
air sacs into the kidney causing a typical gra nulomatous inflammato,y
response with caseous necrosis ringed by giant cells. The microspo-
ridium Encephalitozoon hellem causes extensive, severe tubular ne-
crosi s. With H&E staining, organisms are seen as faintly basophilic
dots or fine granules in the lumen of necrotic tubules and cytoplasm
of tubular epithelium. It is Gram-positive and can be easily rec-
ognized in tissue sections stained with Gram stain. Microsporiclia
have been previously classified as protozoa, but based on molecu lar
phylogenetic analysis, they are now considered to be a unique phy-
lum of fungi.
Protowal i11fectio11s
Renal coccicliosis of geese, clucks, and swans is characteri zed by
developmental stages of Eimeria truncata in renal tubular epithe-
lial cells. Many developmental stages from gamonts to oocysts usu-
ally are present simultaneously. Tubular epithelium is hyperplastic,
moderate numbers of lymphoid cells are evident, and granulomas
may develop around collections of oocysts. E. somateriae infects the
kidneys of ducks. Other Eimeria species infect different types of birds.
Renal c1y ptosporidiosis caused by C1yptosporidi11111 sp. is rare in birds.
Developing stages of C,ypto.1poridi11111 are seen closely associated with
the apical swface of epithelial cells lining ureters, collecting ducts,
collecting tubules, and distal convoluted tubules, with extensi ve lym-
phoplasmacytic ureteritis and marked hyperplasia of the ureter epithe-
lial cells. Lesions of histomoniasis occasionally involve kidneys and
cause regionally extensive, severe nephritis consisting of effacement
of renal tissue by dense lymphocytic or lymphohistiocytic infiltrates,
with many intralesional trophozoites of Histomonas. Lesions may be
found in the kidneys of birds infected with Sarcocystis. There are
lymphocytic tubulointerstitial nephritis, marked hypertrophy and
hyperplasia of endothelial cells lining intralobular and interl obu lar
veins, segmental lymphocytic phlebitis, and in some cases wide-
spread fibrin mi crotlu-ombi of glomerul ar capillaries.
Metazoal i11fectio11s
In birds, trematodes may be found in the ureters and collecting ducts
of the kidneys. Trematodes of the genus Paratanaisia parasitize the
collecting ducts and ureters of different bird species and cause gran-
ulomatous nephriti s. Clinical signs and mortality are seen in heavy
infections with renal flukes.
Neoplasia
Nepbroblastoma is often caused by avian leukosis/sarcoma virus-
es. Tumors are composed of both epithelial and mesenchymal tis-
sues in which abortive tubules and glomeruli are found . Lymphoid
tumors ofMarek's disease and lymphoid leukosis commonly involve
the kidneys as well as other organ s in chickens. Morphology of
Marek 's disease and lymphoid leukosis lesions in the kidney are
typical of those seen in other ti ssues. Reticuloenclotheliosis vi-
rus of turkeys may cause lymphoreticular neoplasia in kidneys and
other organs. Avian leukosis virus type J causes myelocytomas (my-
elocytomatosis), which often involve the kidneys. Sheets of immature
ce lls with eosinophilic cytoplasmic granules are seen. Variati on in

the stage of myeloid cell differentiation and tumors composed of
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different cells types are conunon. Renal adenocarcinomas are more
commonly found in companion birds, especially budgerigars, than
commercial chickens and turkeys. Tumors have a lobulated pattern
with neoplastic epithelial cells lining tubules separated by a fine, fibro-
vascular stroma. Mitotic figures are often numerous. Differentiation of
adenocarcinomas and nephroblastomas can be difficult.
Malignant seminomas often metastasize to the kidneys. Meta-
static tumors retain the same morphology as the tumors in the testes.
Additional Readings
Abbassi , H. , F. Coudert, Y. Chere! , G. Dambrine, J. Brugere-
picoux, and M. Naci..ri. 1999. Renal c1yptosporidiosis
( C!J1ptosporidiu111 baileyi) in specific-pathogen free chickens
experimentally infected with Marek's disease virus. Avian Dis
43 :738-744 .
Barton, J. T., A. A. Bickford, G. L.Cooper, B . R. Charlton, and C. J.
Cardona. 1992. Avian paramyxovirus type I infections in racing
pigeons in California. I. Clinical signs, pathology, and serology.
Avian Dis 36:463-468.
Boykin, S . L. and E. J. Braun. 1993. Entry ofneplu-ons into the
collecting duct network of the avian kidney: a comparison of
chickens and desert quail. J Mo1phol 216:259-269.
Braun, E. J. 1998. Comparative renal fi.mction in reptiles, birds, and
manunals. Sem Avian Exotic Pet lvfed 7: 62-71.
Braun, E. J. 1999. Integration of renal and gastrointestinal function.
J Exp Zoo/ 283:495-499 .
Braun, E. J. and P. R. Reimer. 1988. Structure of avian loop of Henle
as related to countercurrent multiplier system. Am J Physiol
255:F500-512 .
Brown, T. P. 1996. Urinaty system. In: Avian Histopathology. C.
Riddell (ed.). New Bolton Center, AAAP. pp. 167-181.
Brummermann, M . and E. J. Braun. 1995. Effect of salt and water
balance on colonic motility of White Leghorn roosters. Am J
Physiol 268 :R690-698 .
Casotti, G . and E . J. Braun. 1995. Structure of the glomerular
capillaries of the domestic chicken and dese1t quail [Callipepla
gambelii]. J Mo,ph 224:57-63.
Casotti, G . and E. J. Braun. 1995. Structure of the glomerular capillaries
of the domestic chicken and dese1t quail. J Mo1phol 224:57-63 .
Casotti , G. and E. J. Braun. 1996. Functional morphology of
the glomerular filtration b[\tTier of Gallus gallus . J lvfo1phol
228:327-334.
Casotti, G . and E. J. Braun. 1997. Ionic composition ofurate-
containing spheres in the urine of domestic fowl. Comp Biochem
and Physiol A 118:585-588.
Casotti, G. and E. J. Braun. 2004. Protein location and elemental
composition of urine spheres indifferent avian species. J E,p Zoo!
A CompExpBio/301:579-587.
Casotti, G. , K. K. Lindberg, and E. J. Baun. 2000. Functional
morphology of the avian medullary cone. A111J Physiol Regul
Integr Comp Physiol 279:Rl 722- 1730.
Chandra, M ., V. Marius, M. Michele, G. Bennejean, J. Lamande, and
M . Sternberg. 1986. Nephrotoxic serum nephritis in chickens.
Avian Pathol 15:39-56.
Urinw:11 System
Goldstein, D. L. and E. J. Braun. 1989. Structure and concentrating
ability in the avian kidney. Am J Phy siol 256:R501-509.
Gonlis, S., A. B. Didiuk, J. Neufield, and G. Wobeser. 1996. Renal
coccidiosis and other parasitologic conditions in lesser snow
goose goslings at the A.trne River, West Coast Hudson Bay. J
Wildlife Dis 332:498-504.
Hodges, R. D. 1974. Th e Histology of the Fowl. New York,
Academic Press. pp. 648
Janes, D. N. and E. J. Braun. 1997. Urinaty protein excretion in red
jungle fowl Gallus gallus. Comp Biochem Physiol A 118:1273-
1275.
Jolrnson, 0 . W. 1979. Urinary organs. In: Form and Function in Birds,
A. S. King and J. Mclelland (eds). New York, Academic Press.
I: 183-235.
Kinde, H. , B. M. Daft, A. E . Cortes, A . A . Bickford, J . Gelb, Jr.,
and B. Reynolds. 1991. Viral pathogenesis of a nephroh·opic
infectious bronchitis virus isolated from commercial pullets.
Avian Dis 35:415-421.
Layton, H . E., J. M . Davies, G . Casotti, and E. J. Baun. 2000.
Mathematical model of an avian urine concentrating mechanism.
Am J Physiol Renal Phy siol 279:FI 139-1160.
Lee, C. W. , C. Brown, D. A. Hilt, and M. W. Jackwood. 2004.
Nephropathogenesis of chickens experimentally infected with
various strains of infectious bronchitis virus. J Vet Med Sci
66:835-840.
Mehdi, N. A. Q. , W.W. Carlton, and J. Tuite. 1983. Acute
toxicosis of citrinin in turkeys and ducklings. Avian Pathol
12:221 -233 .
Morild, I., R . Mowinckel, A. Bohle, and J. A. Christensen. 1985.
The juxtaglomerular apparatus in the avian kidney. Cell Tissue
Res 240:209-214.
I
Nishimura, H. , C . Koseki, M. Imir, and E. J. Braun. 1989. Sodium
chloride and water transpo1t in the thin descending limb of Henle
of the quail. Am J Phy siol 257:F994-l002.
Puette, M . and W. A. Crowell. 1993. Histologic and morphometric
exanlination of avian glomeruli from normal and swollen kidneys
of broilers at slaughter. Avian Dis 37:874-879.
Puette, M ., W. A. Crowell, and W. S. Hefner. 1994. Ultrastructural
examination and cell count determinations of avian glomeruli
from grossly normal and grossly swollen kidneys of broilers at
slaughter. Avian Dis 38:515-522.
Purcell, D . A . and J.B. Mcferran. 1972. The histopathology of
infectious bronchitis in the domestic fowl. Res Vet Sci 13: I 16-
122.
Raj , G.D. and R. C. Jones. 1997. Infectious bronchitis virus:
immunopathogenesis of infection in the chicken. Avian Patho/
26:677-706.
Reece, W. 0 . 2004. Kidney Function in Birds . In: Dukes
Physiology ofDomestic Animals, W. 0 . Reece (ed). Ithaca,
Comstock Publishing Associates. I 07-113.
Shirai, J., K. Nakamura, H. Nozaki, and H. Kawamura. 1991.
Differences in the induction of urate deposition of specific-
pathogen-free chicks inoculated with avian nephritis virus
passaged by five different methods . Avian Dis 35:269-275.
Avian Histopathology (4'11 Edition) I 427
 Tahseen Abdul-Aziz • Oscar J. Fletcher
Siller, W. G. 198 1. Renal pathology of the fowl: A review. Avian
Pathol l 0: 187-262.
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Swayne, D. E. and M. J. Radin 1991. The pathophysiological
effects of water and feed restriction in chickens. Avian Patho/
20:649-66 1.
Trampe!, D. W. , T. M. Pepper, and B. L. Blagburn. 2000. Urinary
tract c1yptosporidiosis in commercial laying hens. Avian Dis
44:479-484.
428 I American Assoc iation of Avian Pathologists
William, S. M., S. Hafner, and Y. Sundram. 2007. Liver granulomas
due to Eubacteri11111 Tort11os11111 in a 7-week-old bobwhite quail.
Avian Dis 51 :797-799.
Wilson, F. D. , R. W. Wills, C. G. Senties-Cue, W. R. Maslin,
P. S. Stayer, and D. L. Magee. 2010. High incidence of
glomeruloneplu·itis assoc iated with inclusion body hepatitis in
broiler chickens: Routine histopathology and histomorphometric
studi es. Avian Dis 54:975-980.
 Urinary System
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9.1. Kidney. Normal. 7-day-old turkey. The close association 9.3. Kidney. Normal. 56-day-old broiler. Nest of embryonic
of the kidney with the ve11ebrae and ribs is illustrated. Arrow nephrons and glomeruli is located at the periphery of the co11ex of
po ints to the division between the left and right kidney, and the box lobule.
encloses ureter.

9.2. Kidney. Normal. 7-day-old turkey. Demonstrated is the 9.4. Kidney, Normal. 56-day-old broiler. Higher-power view
ureter (box) on the ventral surface of the kidney. The basophilic of the embryonic nephrons and glomeruli in 9.3 .
areas in the periphery of the lobules (arrows) are embryonic
neplll'ons.

Avian Histopathology (4 th Edition) I 429

 Tahseen Abdul-Aziz • Oscar J. Fletcher
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9.5. Kidney. Glomerulus of mammalian-type nephron. 9.7. Kidney. Glomerulus. Normal. 52-week-old broiler
Normal. 19-week-old broiler breeder pullet. The glomerulus breeder hen. Kidney section stained with PAS stain to highlight
consists ofcapilla1y tuft, Bowman 's space, and Bowman's capsule. the basement membrane of the blood capillaries in the glomerular
The cluster of nuclei in the center of the tuft is mostly mesangial capillary tuft.
cells in mesangial matrix. The red blood cells at the periphe1y of the
tuft are in the lumens of blood capillaries. Between the glomerular
tuft and the capsule is the Bowman 's space. The capsule consists
of flattened epithelial cells and thick basement membrane. The
large nuclei on the surface of the glomerular tuft are podocytes, the
cytoplasm of which wraps around the blood capillaries.

I
9.6. Kidney. Normal glomerulus of reptilian-type nephron.
19-week-old broiler breeder pullet. This image and the one
in 9.5 are taken at the same magnification. The glomeruli of the
reptilian-type nephrons are smaller than those of the mammalian-
type nephrons, but otherwise have the same structure. Note the red
blood cells in the lumens of blood capillaries at the periphery of the
glomerulus.
9.8. Kidney. Macula densa. 19-week-old broiler breeder
pullet. Distal convoluted tubule is closely associated with
glomerulus and shows the macula densa, which consists of region
of closely packed, highly specialized senso1y cells in the epithelial
lining of the tubule. The macula densa faces the glomerulus and its
nuclei are more basophilic than those of the tubular epithelial cell s.
The cluster of cells between the distal tubule and the glomerulus
is probably of extraglomerular mesangial cells (also called Lac is
cells).

430 I American Association of Avian Pathologists

 Urill(IIJ' System
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9.9. Kidney. Macula densa. 31-week-old broiler breeder
hen. Higher-power view of a macula densa in distal convoluted
tubule closely associated with glomerulus. Note that the macula
densa faces tbe glomerulus and consists of closely packed sensory
cells with nuclei that are more basophilic than those of the tubular
epithelial cells.
9.11. Kidney. Normal. 31-week-old broiler breeder male. Area
adjacent to intralobular vein has proximal and distal convoluted
tubules surrounded by peritubular capillary sinuses. See 9.12 for
additional description.

I
9.10. Kidney. Normal. Cockatoo. Intralobular vein is 9.12. Kidney. Normal. 31-week-old broiler breeder male.
surrounded mostly by distal convoluted tubules, with glomeruli and Higher-power view of area adjacent to intralobular vein . The
proximal convoluted tubules at the periphery. proximal and distal convoluted tubules are surrounded by peritubular
capillary sinuses. The proximal tubules have rounded or elongated
profile and very narrow or almost totally occluded lumens, and they
are lined by low columnar epithelial cells with abundant cytoplasm
and luminal brush border consist of closely packed microvilli. The
distal tubules are smaller than the proximal tubules, have distinct
lumen, and are lined by cuboidal epithelial cells.

Avian Histopathology (4 th Edition) I 431

 Tahseen Abdul-Aziz • Oscar J. Fletcher
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9.13. Kidney. Normal. 31-week-old broiler breeder male. 9.15. Kidney. Normal. 52-week-old broiler breeder male.
3-micron section shows the brush border of proximal convoluted PAS-stained kidney section . Higher-power view demonstrates th e
tubules. The luminal brush border consists of closely packed PAS-positive brush border of the proximal convoluted tubules.
microvilli and appears as eosinophilic line around the lumen.

I
9.14. Kidney. Normal. 31-week-old broiler breeder male. 9.16. Kidney. Normal. 25-week-old quail. Demonstrated are
3-micron section stained with PAS stain. The luminal brush border proximal convoluted tubules and collecting tubules. The collecting
of the proximal convoluted tubules is PAS positive (stains purple). tubules are lined by high cuboidal epithelial cells with basa ll y
The tubules without brush border are distal convoluted tubules, located nuclei and somewhat basophilic and rarefied or vacuolated
which have large lumen and their epithelial cells are shorter than cytoplasm containing mucin .
those of the proximal tubules. The PAS stain also highlights the
basement lamina on which the epithelial cells of the tubules are
standing.

432 I American As sociation of Avian Pathologists


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9.17. Kidney. Normal. Turkey. Low-power view showing renal
lobules and medullaty cone.
9.18. Kidney. Normal. 25-week-old quail. Medullaty cone
is comprised of collecting ducts descending from the cortex and
neplu·onal loops of mammalian-type nephrons (loops of Henle).
The collecting ducts are lined by columnar epithelial cells with
basally located nuclei and rarefied, somewhat basophilic cytoplasm
that contains mucin. The nephronal loops are lined by cuboidal
epithelial cells with more densely stained eosinophilic cytoplasm
and with nuclei located close to the apex of the cell.
Uri11mJ' System
9.19. Kidney. Normal. 31-week-old broiler breeder male.
Area in medullaty cone shows large collecting duct surrounded by
nephronal loops of mammalian-type nephrons. The cytoplasm of
the epithelial cells lining the collecting ducts is vacuo lated due to
the presence of mucin. The epithelium of the nephronal loops is
cuboidal and does not contain mucin.
9.20. Kidney. Major ureter branch. Normal. 26-day-old
broiler. From inside out, the wall of the major ureter branch consists
of mucin-filled pseudostratified columnar epithelium, subepithelial
connective tissue containing some lymphoid and plasma cells, and
thick outer consisting of fibroblasts, collagen fibers, and smooth
muscle.
Avian Histopathology (4' 11 Edition) I 433
 Tahseen Abdul-Aziz • Oscar J. Fletcher
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9.21. Kidney. Major ureter branch. Normal. 26-day-old
broiler. Higher-power view of area in 9.20 showing the lining
pseudostratified columnar epithelium and the thick fibrocoll ageno us
and smooth muscle wall. Note the mucus in the lumen .
I
9.22. Kidney. Major ureter branch. Normal. 26-day-old
broiler. Higher-power view of area in 9.2 1. The lining epithelial
cells ap pear with double row of nuclei, and have densely basophilic
cytoplasm filled with mucin, which is also seen as irregul ar
basophilic material on the luminal surface. Mucin is present in the
lumen.
434 I Ameri can Association of Avian Pathologists
9.23. Kidney. Primary ureter branch. Normal. 19-week-
old broiler breeder pullet. The primary ureter branch is lined
by pseudostratified columnar epithelium . Most of the nuclei of
the epithelial cells are basally located. The lining epithelial cells
produce mucin, thus appear rarefied or clear. The thick wall consists
of co llagen fibers, fibroblasts, and smooth muscle.
9.24. Kidney. Ureter. Normal. 7-day-old chicle The ureter is
lined by tall pseudostratified columnar epithelium that is thrown up
into folds in the relaxed state. The cytoplasm of the cells contains
mucin, thus stains basophilic and appears vacuolated. Beneath the
epithelium is layer of connecti ve tissue containing blood vessels and
variable amounts of lymphoid cell s. The muscularis is thick and
consists of circularl y arranged smooth muscle.

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9.25. Kidney. Extramedullary hematopoiesis. Pigeon. Large
collection of hematopoietic cells is in the cortical interstitium. The
collection consists mostly ofmyeloid cells, many of which have red
cytoplasmic granules (granulocytic myeloid cells) . For unknown
reason, such collections are particularly common in the kidneys of
pigeon.
9.26. Kidney. Proximal tubular epithelial hyperplasia.
1.5-year-old backyard chicken. Hyperplasia of epithelial cells of
proximal convoluted tubules. Note the crowding of the nuclei of
the tubular epithelium. This section was of the right kidney, which
was noticeably enlarged. There was almost total aplasia of the left
kidney. This is an example of compensat01y hyperplasia.
Uri11my System
9.27. Kidney. Proximal tubular epithelial hyperplasia.
1.5-year-old backyard chicken. Another section of the same
kidney in 9.26. Crowding of the nuclei of tubular epithelial
cells due to hyperplasia. Nuclear hyperplasia and cytoplasmic
hypereosinophilia are seen in some h1bules.
9.28. Kidney. Proximal tubular epithelial hyperplasia.
2-year-old pigeon. The proximal convoluted tubule in the center
of the image shows marked epithelial cell hyperplasia as evidenced
by crowding and piling up of the nuclei of the cells. The bird had
chronic nephritis with loss of some renal h1bules.
Avian Histopathology (4t11 Edition) I 435
 Tahsee11 A bdul-A ziz • Oscar J. Fletcher
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9.29. Kidn ey. Hemosiderin granules. One-year-old backyard 9.31. Kidney. Bile droplets. Chicken. The brow n droplets in th e
chicken. Brown hemosiderin gra nules are in the cytoplasm of cytoplasm of tubul ar epitheli a l cells are bile dropl ets. Such dropl ets
prox imal convo luted tubules. Re nal deposits of iron suggest may be seen in the kidneys of birds w ith severe and extensive li ver
patholog ica l condition involving intravascular hemol ys is. dam age.

I
9.30. Kidney. Hemosiderin granules. One-year-old backyard 9.32. Kidney. Bile pigment. 4-year-old backyard chicken.
chicken. T he iron in the hemos iderin gra nules stains blue with Brow n pigment co nsistent w ith bile is in the cytopl asm of tubul ar
Prussian blue stain . epithe li al cells. The bird had serve hepati c steatosis.

436 I Ameri ca n Association of Av ian Patho logists


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9.33. Kidney. Bile droplets. 5-week-old chicken. The epithelial
cells of proximal convoluted tubules contain dull-red to brown-red,
fine cytoplasmic droplets that were interpreted to be bile absorbed
by the tubules . The same kidney had a few bile casts in the lumen
of tubules (see 9.34).
9.34. Kidney. Intratubular bile cast. 5-week-old chicken. Bile
cast is within the lumen of renal tubule (likely distal convoluted
tubule). Tubular bile casts may be seen in the kidneys of birds with
severe and extensive liver damage.
Urill(IIJ' System
9.35. Kidney. Intratubular hemoglobin casts. Guinea fowl.
The lumens of renal tubules are dilated with red-orange stained
hemoglobin casts. Hemoglobin casts in renal tubules indicate
intravascular hemolytic crisis. The hemoglobin is filtered by
glomeruli and accumulates in the lumens of renal tubules. Note the
intravascular hemolysis in interstitial blood vessels. Hemoglobin is
absorbed by proximal convoluted tubules and may cause injury to
the tubular epithelium (hemoglobinuric kidney).
9.36. Kidney. Hemoglobin droplets. 11-month-old backyard
chicken. Numerous hemoglobin droplets are in the cytoplasm
of renal tubules . The bird had severe hemolytic anemia of
undetermined cause.
Avian Histopathology (4 th Edition) I 437
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9.37. Kidney. Intratubular urate spherules. 3-year-old
backyard chicken. Renal tubules are lined by attenuated epithelium
and filled with eosinophilic urate spherules. The accumulation of
such spherules is occasionally seen in tubular lumens of dehydrated
birds .
I
9.38. Kidney. Intratubular calcium deposits. 4.5-year-old
pion us parrot. Dense ca lci um deposits within the lumen of a renal
tubule. Few other tubules in the section had sim ilar deposits. This
was incidental finding of unknown cause.
438 I American Assoc iati on of Avian Pathologists
9.39. Kidney. Intratubular calcium deposits. 65-week-old
turkey. Calcium is deposited (dystrop hic calcifi cation) in multiple
tubules. The interstitial tissue is ex panded by mild mononuclear cell
infiltrates. The insert shows minera l deposit at hi ghe r magnification.
9.40. Kidney. Glomerular calcinosis. 9-month-old backyard
chicken. Calcium deposits in the glomeru lar mesangium. Calcium
deposition was confirmed with Von Kossa stain. There was some
calcium deposition in the basement membrane of on ly very few
tubules. The bird had system ic ca lcinosis of unknown cause.
 UrilutlJ' System
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9.41. Kidney. Oxalate nephropathy. IS-year-old pionus
parrot. Dilated renal tubules are filled with oxalate c1ystals and
lack lining epithelium . The interstitium around injured tubules is
infiltrated by mononuclear inflammatory infiltrates, and there are
multinucleated giant cells. The cause was unknown but excessive
consumption of oxalate-rich food was suspected.
9.43. Kidney. Glomerular amyloidosis. 9-year-old goose.
Occupying the mesangium and effacing mesa ngial cells is deposit
of eosinophilic, homogenous, hyaline material most suggestive of
amyloid protein.

I
9.42. Kidney. Oxalate nephropathy. 15-year-old pionus 9.44. Kidney. Glomerular amyloidosis. 9-year-old goose. The
parrot. Ethylene glycol crystals appear birefringent when viewed tissue section was stained with Congo red. The amyloid in the
with polarized light. glomeruli stains orange and may exhibit apple green birefringence
with polarized light.

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9.45. Kidney. M embranou s glomerulopathy. 56-day-
old broiler. This g lo merulu s has thi ck capillary loops witho ut
increase in cellularity. T hi s is characteristi c les ion of membrano us
g lo merul opathy th at is usually ca used by subepitheli al loca li zati o n
of immune co mplexes. Several hya line dropl ets are in the cytoplasm
of parieta l e pithelia l ce lls. The ca use was not determin ed in thi s
case.
9.46. Kidn ey. Membranous glomerulopath y. Aflato xicosis.
Duck of unknown age. Thickenin g of the glomerul ar capillary
loo p. Note that th ere is no associated increase in cellularity of the
g lo merulus. The bird also had severe liver lesio n characteristi c of
afl atoxicos is.
440 I Ameri ca n Associa ti on of Av ian Pathologists
9.47. Kidney. Membranous glomerulopath y. Aflatoxicosis.
Duck of unknown age. T he kidney sect ion was stained with PAS
stain. The stain hi ghli ghts the thi ckening of the glo merular capill ary
wall s .
9.48. Kidney. Membranous glomerulopath y. 26-day-old
broiler. Glo merulu s shows thi ckening of the basement membrane
of the glomerul ar capillaries without increase in cellul arity. T he bird
was affected w ith inclusion body hepatitis. Mesang ioprolifera ti ve
and memb ra no us glo merul opathy have been desc ribed in bro iler
affe cted w ith thi s di sease (see 9.53 and 9.54).

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9.49. Kidney. Mesangioproliferative glomerulopathy. 35-day-
old broiler. The glomeruli are large and hypercellular due to
increase in mesangial cells that give increased degree of basophilic
staining. Bowman 's spaces are almost totally obliterated. The
les ion in this bird was not associated with clinical signs or renal
disease and its significance is uncertain.
9.50. Kidney. Mesangioproliferative glomerulopathy. 35-day-
old broiler. Higher-power view of glomerulus showing increased
glomerular cellularity due to mesangial cell proliferation. Also,
proliferating podocytes form cellular crescent over the glomerular
tuft and fill the Bowman's space.
Urinmy System
9.51. Kidney. Mesangioproliferative glomerulopathy. 44-day-
old broiler. Glomeruli are hypercellular due to proliferation
of mesangial cells. Bowman's spaces are totally obliterated.
There appears to be also mild proliferation of podocytes.
Mesangioproliferative glomerulopathy is not etiology- or disease-
specific lesion and should be interpreted in conjunction with other
gross and microscopic lesions and other ancillary tests. The bird
was affected with tenosynovitis caused by novel reovirus, and this
lesion is sometimes seen chickens with this disease.
9.52. Kidney. Mesangioproliferative glomerulopathy. 44-day-
old broiler. Same case as 9.51. Hypercellularity of the glomerulus
due to proliferation of mesangial cells. The arrow points to focal
area of podocyte proliferation and segmental crescent formation.
In histological sections, the appearance of the crescent may vary,
depending on the plane of the section.
Avian Histopathology (4 th Edition) I 441
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9.53. Kidney. Mesangioproliferative glomerulopathy. 26-day- 9.55. Kidney. Glomerular sclerosis. 8-year-old macaw.
old broiler. At thi s magnifi cation , g lomeruli show increase in The mesa ngium of the g lomerulu s is ex panded by amorphous
mesangia l cellulari ty, w ith o bliteration of Bowman 's space. So me eos ino philic materi al th at was suspected to be collagen. The bird
renal tubul es are dilated and fill ed w ith pro teinaceous fluid . The bird had other renal les ions co nsistent with chroni c renal di sease.
was affec ted with inclusion body hepatiti s. Mesangiop ro li fe rative
and memb ra nous glomerulopathy have bee n described in bro ilers
affected with thi s di sease.

I
9.54. Kidney. Mesangioproliferative glomerulopathy. 9.56. Kidney. Glomerular sclerosis. 8-year-old maca w.
26-clay-old broiler. Hi gher-power view of a glomerulu s in 9. 53 . Masson 's triclu-ome staining of the sa me secti o n as 9. 55 shows that
Proli fera ti on of mesa ng ial cell s and ex pansion of mesa ngial matrix th e eos inophilic materi al in the mesa ng ium is collage n (stained
characterize mesa ngiopro lifera ti ve g lomerulopathy are seen in these blue) .
g lomerulu s. T he Bow man's space is almost totall y oblitera ted. The
wa ll of ca pillari es in o ne g lomerulus appea rs thi ckened.

442 I Ameri ca n Associati on of Av ian Pathologists


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9.57. Kidney. Glomerular lipidosis. Adult blue-fronted
Amazon parrot. The glomernlar mesangium is occupied and
expanded by lipid that appears to be mostly extracellular. It is
possible that some of the lipid is in the mesangial cell cytoplasm.
The bird had severe atherosclerosis of great arteries of the heai1.
9.58. Kidney. Glomerulus. Columnar parietal cells;
glomerular lipidosis. Blue-fronted Amazon parrot. The arrow
points to a glomerulus with normal parietal (capsular) epithelium.
In the glomerulus on the upper right corner, the parietal cells of
the Bowman's capsule are columnar rather than flattened, and the
Bowman's space appears expanded and contains proteinaceous
material. The capilla1y tuft has lipid vacuoles that indicate fat
deposition.
Urill(IIJ' System
9.59. Kidney. Baby chick nephropathy, dehydration. 3-day-
old broiler. Several renal tubules in the cortical area are necrotic
and contain dense urate deposits.
I
9.60. Kidney. Baby chick nephropathy - dehydration. 3-day-
old broiler. Higher-power view of area in 9.59. Renal tubules are
necrotic and contain blue- or pink-stained urate material surrounded
by some heterophils. Other tubules are lined by thinned epithelial
cells and contain some cellular debris. The cause of this lesion is
dehydration.
Avian Histopathology (4 th Edition) I 443
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9.61. Kidney. Baby chick nephropathy, dehydration. 9.63. Kidney. Baby chick nephropathy, dehydration. 3-day-
3-day-old broiler. Renal tubules are necroti c and contain urates old broiler. See the legend of9.64.
surrounded by so me heterophil s. The urate material is pink in the
ce nter and deeply basophili c at the periphe1y. Note the ex pansion of
th e interstitium by clear spaces (edema).

I
9.62. Kidney. Baby chick nephropathy, dehydration. 5-day-
old broiler. Renal tubules in the cortical area are necrotic and
co ntain pink- and blue-stained urate material surrounded by some
heterophils. The interstitium is expanded by clear spaces (ede ma).
9.64. Kidney. Baby chick nephropathy, dehydration. 4-day-
old broiler. This legend is also applied to 9.63. Medullary cone and
the cortical area aro und it are shown. In this form ofnephropathy in
baby chi cks, collecting ducts in the medulla1y cone are dilated and
lined by thinned epi thel ial cells and contain some urate. Tubul es in
the cortex also appear mildly dilated.

444 I American Association of Avian Pathologists


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9.65. Kidney. Baby chick nephropathy. 6-day-old broiler.
Collecting ducts in the medullary cone are dilated and lined by
thinned epithelial cells. There are also few necrotic tubules with
blue staining urate. Near the upper right corner is dilated ureter
branch with some mucinous material and very few cells in the
lumen.
9.66. Kidney. Urate nephropathy. Dehydration, water
deprivation. 21-week-old-broiler breeder male. Several
tubules are necrotic and contain eosinophilic deposits surrounded
by macrophages and multinucleated giant cells. Other tubules are
lined by thinned epithelium. This lesion should arouse suspicion of
dehydration due to water deprivation.
Urinmy System
9.67. Kidney. Urate nephropathy. Dehydration, water
deprivation. 21-week-old-broiler breeder male. Foci of loss
(necrosis) of renal tubules and replacement by urate deposits, each
of which is surrounded by macrophages and multinucleated giant
cells with some heterophils. Urate deposits are basophilic in the
center and eosinophilic at the periphery. The differences in staining
probably reflect the density of the deposit (more dense in the center).
There is also interstitial inflammatory infiltrate.
I
9.68. Kidney. Urate nephropathy. Dehydration, water
deprivation. 21-week-old-broiler breeder male. Relatively large
area of tubular loss and urate deposition rimmed by multi nucleated
giant cell. The term urate granuloma or tophus may be used to
indicate this lesion. Note the changes in tubules around the urate
granuloma .
Avian Histopathology (4th Edition) I 445
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9.69. Kidney. Urate nephropathy. Dehydration, water
deprivation. Chicken. A: This necroti c tubul e has basophilic center
of fibrill ar appea rance characteristi c ofurate deposits and is rimm ed
by heterophil s and surrounded by macroph ages and multinucleated
g iant cells. These are fea tures th at characterize toph us. B: Higher-
power vi ew of the tophus showing the centra l urate deposition and
surrounding inflammatory cells, including macrophages.
9.7 1. Kidney. Dehydration, water deprivation. Chicken.
Large area of necrosis co nsists of gra nul ar eosinophilic debris and
necro ti c inflammatory cells. Thi s necrotic area is li ke ly fo rmed by
the conflu enc e of adj acent nec roti c tubul es. Also see n is a small
m ate-containi ng necrotic area that appears evolv ing into a tophu s.

I
9.70. Kidney. Urate nephropathy. Dehydration, water 9.72. Kidney. Renal gout. 7-week-old turkey. There is a di ffuse
deprivation . Chicken . A: Large area of necrosis with accumul ati on pattern of necrosis, inflammation, urate deposition, and fib rosis.
of cellular debri s is in co llecting tubul e. The necroti c area represents Initial ca use was unknown, but wa ter depri va tion was suspected.
coa lescing necrotic tu bules. Note the absence of inflam mati on in the
adj acent ti ssue B : Hi gher-power view of the necroti c area showing
ce llular and karyorrhec ti c debri s and numero us heterophil s.

446 I America n Associa ti on of Av ian Path o logists


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9.73. Kidney. Urate tophus. Renal gout. 7-week-old turkey.
A. Urate tophus consisting ofurate deposit rimmed by macrophages
and multinucleated giant cells and surrounded by fibrous tissue. B .
Higher-power view of panel A showing the basophilic, feathery
appearance of the urate deposits.
9.74. Kidney. Urate tophus. Water deprivation. 35-week-old
broiler breeder hen. Early formed tophus consisting of a center
of basophilic, feathe1y urate deposits surrounded by mononuclear
inflammatory cells and some heterophils, with early formation of
multinucleated giant cells. Note the interstitial edema (clear spaces)
around the tophus.
Urill(IIJ' System
9.75. Kidney. U rolithiasis. 24-week-old white leghorn
chicken. The ureter is markedly dilated and has round contour and
flattened mucosa! surface. The lumen contains mineral material
admixed with mucus. The division of the kidney drained by this
ureter was atrophic.
9.76. Kidney. Urolithiasis. 24-week-old white leghorn chicken.
The collecting ducts in medullary cone are dilated and their lining
epithelium is flattened. Loops of Henle are compressed and the
interstitium is expanded by fibrous connective tissue. Dilation
of the collecting ducts is caused by impediment to the urine flow
tlu·ough the ureters.
Avian Histopathology (4 th Edition) I 447
 Tahsee11 Abdul-Aziz • Oscar J. Fletch er
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9.77. Kidney. Urolithiasis. 24-week-old white leghorn chicken.
Cortical region shows press ure compression . Some tubules are
dilated while others are small. There is increase in the interstitia l
fibrou s tissue.
I
9.78. Urolithiasis. 24-week-old white leghorn chicken. Hi gher-
power view of the compressed cortical region. Note the crowding
of the glomeruli and the d ilation or co mpression of the tubules.
Dilated tubules are lined by thinned epithelial cells.
448 I American Associati on of Avian Pathologists
9.79. Kidney. Ureteritis. 15-day-old turkey. Co llectin g ducts
in the 111edulla1y cone are dilated, lined with thinned epithe lial cell s,
and co ntain granul ocyti c leukocytes. There is also so me interstitial
heterophilic infiltrati on.
9.80. Kidney. Chronic renal disease. 8-year-old macaw. The
interstitium is expanded by fibrou s ti ss ue. There is loss of renal
tubul es, and remaining tubules are dilated and irregu lar in size
and shape. The capillaiy tuft of the g lomerulu s in the upper ri ght
corner shows hya lini zation due to the deposi tion of collagen in th e
mesa ng ial matri x (glomerular sclerosis- see 9.55 and 9.56).

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9.81. Kidney. Chronic renal disease. 8-year-old macaw.
Features include loss of tubules, interstitial fibrosis , and dilation
and irregularity of remaining tubules. Mineral (calcium) deposits
are present in the lumens of three tubules (yellow arrows). There
are two foci of necrosis with urate deposition in the center and
heterophilic infiltration at the periphery (red arrows).
9.82. Kidney. Lead toxicity. Turkey buzzard. Small,
eosinophilic intranuclear inclusions are in many tubular epithelial
cells (box). The insert shows positive acid-fast staining of the
inclusions.
Uri11a1J 1 System
9.83. Kidney. Copper toxicity. 13.5-week-old turkey.
Karyomegaly and anisokaiyosis of tubular epithelial cells. There
was high mortality in the flock. Very high level of copper was
detected in the livers of dead birds.
I
9.84. Kidney. Copper toxicity. 13.5-week-old turkey.
Accumulation of hemoglobin globules in the lumen of a renal tubule.
This indicates hemolytic crisis associated with copper toxicity.
Avian Histopathology (4 th Edition) I 449
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9.85. Kidney. Copper toxicity. 13.5-week-old turkey. Renal
tubul e is necroti c and contains hemoglobin mi xed with necrotic
cells.
I
9.86. Kidney. Aflatoxicosis. Membranou s glomerulopath y.
2-week-old duckling. See th e legend of 9.85 .
450 I Ame ri ca n Assoc iat ion of Avian Pathologists
9.87. Kidney. Afl atoxicosis. Membranous glom erulopathy.
2-week-old duckling. This legend is also applied to 9. 86.
Thi cke ning of the g lomerular capillary loop. Note that there is no
assoc iated increase in cellulari ty of the g lomerulu s. The bird also
had severe liver les ion chara cteri sti c o f afla toxicosis.
9.88. Kidney. Aflatoxicosis. Membranou s glom erulopathy.
2-week-old duckling. See the legend of 9.89.

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9.89. Kidney. Aflatoxicosis. Membranous glomerulopathy.
2-week-old duckling. This legend is also applied to 9.88 . The
kidney section was stained with PAS stain that highlights the
thickened wall of glomerular capillaries.
9.90. Kidney. Infectious bronchitis. Chicken. Disruption of
the medullaiy cone by marked interstitial lymphocytic infiltrates
(medullary lymphocytic interstitial nephritis). Tubules and
collecting ducts appear distended. The cortex in this section is
relatively unaffected .
Urinary System
9.91. Kidney. Infectious bronchitis. Chicken. Higher power-
view of region in 9.90 showing extensive lymphocytic infiltration
that effaces renal tubules and ducts in the medulla1y cone. The
lesion is characterized as medullary lymphocytic interstitial
nephritis . Remaining ducts and tubules appear dilated.
I
9.92. Kidney. Infectious bronchitis. 55-day-old broiler. One
of several areas in the cortex that are markedly infiltrated with
lymphocytes. The lesion is characterized as cortical lymphocytic
interstitial nephritis. The kidneys of affected birds were positive for
infectious bronchitis virus by PCR test.
Avian Histopathology (4' 11 Edition) I 451
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9.93. Kidney. Infectious bronchitis. 48-day-old broiler. 9.95. Kidney. Infectious bronchitis. One-year-old backyard
Medullary co ne shows nephriti s characteri zed by infiltrati on and chicken. Same kidney as 9.94. ln th e co1tex, hvo tubul es are
severe di sruption of tubules by many gra nul ocytic leukocytes . The dilated, lined by thinned epithelium and disrupted and infiltrated
kidney was positive fo r infectious bronchitis virus by PCR test and by granulocyti c leukocytes among which urate sp heru les can
virus iso lation. be identified. Two adjacent tubules are dil ated, lined by thinn ed
epithelium, and filled with urate spherules and eosinophilic
proteinaceo us material.

I
9.94. Kidney. Infectious bronchitis. One-year-old backyard 9.96. Kidney. Infectious bronchitis. One-year-old chicken.
chicken. In the c01tex, there are two foci (red arrows) of severe Same kidney as 9.94 . Several tubules in the cortex are lined by
disruption of the tubulointerstiti a l ti ssue by dense infiltrates of thinned epithelium and contain urate material and some gran ulocyti c
gra nulocyti c leukocytes. Also see n are small tubules (yellow leukocytes.
arrows) co ntaining gran ulocytic leukocytes with or without urate
spherules. The kidney was positive for infectio us bronchiti s virus
(IBV) by PCR test and virus iso lation . The IBV isolate from the
kidneys was ge notyped and found to share genet ic identi ty of 96%
with IBV Delmarva isolate DMV/5642/06.

452 I American Association of Avian Pathologists


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9.97. Kidney. Infectious bronchitis. 4-year-old backyard
chicken. See the legend of9.98.
9.98. Kidney. Infectious bronchitis. 4-year-old backyard
chicken. This legend is also applied to 9.97. Interstitial infiltration
of a region in the cortex with lymphocytes (lymphocytic interstitial
neplU'itis). Tubules are dilated and contain degenerate and necrotic
heterophils. Several birds in a small flock of backyard chickens died,
and enlargement of the kidneys was a consistent necropsy finding in
dead and sick birds. Infectious bronchitis virus was isolated from
the pool of kidney samples collected from affectedbirds.
Urinmy System
9.99. Kidney. Infectious bronchitis. 4-year-old backyard
chicken. Higher-power view of area in 9.97 showing interstitial
lymphocytic infiltration and accumulation of heterophils in dilated
tubules.
I
9.100. Kidney. Avian paramyxovirus-1 (APMV-1) infection.
Pigeon. Interstitial infiltrates of lymphocytes are in cortical region
of the kidney (lymphocytic interstitial nephritis). This is a common
and characteristic, but not diagnostic, lesion of APMV-1 infection
in pigeons.
Avian Histopathology W' Edition) f 453
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9.101. Kidney. Avian paramyxovirus- 1 infection. Pigeon.
Higher-power view of area in 9. 100 showin g interstiti al lymph ocyti c
infiltration (l ymphocytic interstitial nephritis) . The inse rt shows
accumul ati on of lymph ocytes around tubul e.
9.102. Kidney. Herpesviru s. Pigeon. Large area of increased
cell ulari ty and tubul ar dilati o n involv in g the enti re renal lobule
including th e medullary co ne. T here are severa l other va riable-sized
areas sca ttered tlU'o ugh the section that have increased cellularity.
454 / Ameri ca n Assoc iat ion of Avian Pa th ologists
9.103. Kidney. Herpesvirus. Pigeon. A : Hi g her-power view
of area in 9. I 02 show ing di sruption of the normal hi sto logica l
architecture of renal tissues due to tubul ar loss and lymphocytic
infi ltrate. B: Higher-power view show in g loss of tubules and
ex pansion of interstiti al ti ss ue by lymphocytic infiltrate.
9.104. Kidney. Polyomavirus inclusion. Rin g-n ecked parrot.
M esa ngial cells are enlarged (karyomegaly) and co ntain fa intl y
basoph ilic inc lusion bodi es . The bird had other hi stopatho logic
les ions characteri sti c of po lyoma virus infection.

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9.105. Kidney. Karyomegaly and intranuclear inclusions. One-
year-old parakeet. Nuclei of epithelial cells (arrows) are markedly
enlarged and filled with homogenous, basophilic inclusion bodies
that were interpreted to be adenovirus or polyomav irus inclusions.
9.106. Kidney. Glomerular fibrin microthrombi. One-year-old
quail. Fibrin microthrombi in the capillary tuft of the glomerulus.
Several glomeruli in this kidney section had similar lesion, and
bacteria cou ld be identified in some of these microtluombi . The
bird was septicemic, and Pasteure/la 11111/tocida was isolated from
the liver.
Uri11mJ' System
9.107. Kidney. Glomerular fibrin microthrombi. 23-day-old
broiler. Fibrin microthrombi are seen in the capillary tuft of the
two glomeruli in this field. Several g lomeruli in this kidney section
had similar lesion, and bacteria could be identified in some of the
mi crothrombi . The bird had bacterial septicemia caused by E. coli.
I
9.108. Kidney. Glomerular bacterial embolus. 43-week-old
pheasant. The dark blue area in the glomerulus is a bacterial embolus
in the capillaty tuft. Bacterial emboli indicate bacteremia. In this
case, the causative bacterium was E1J1sipelothrix rhusiopathiae.
Avian Histopathology (4th Edition) I 455
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9.109. Kidney. Bacterial septicemia. 5-week-old macaw. 9.111. Kidney. Chlamydiosis. 2-month-old conure. Tubules
Numerous bacteria are within blood capillaries of the glomerulus. are necrotic and distended with lymphocytes and plasma cells.
The bird was septicemic. Note the two karyomegalic cells (likely The smudgy, blue materials (arrows) are intracellular Chlamydia
mesangial cells) with intranuclear inclusion bodies characteristic of psilfaci.
polyomavirus.

I
9.110. Kidney. Necrogranulomatous nephritis. Pigeon. Shown 9.112. Kidney. Chlamydiosis. 2-month-old conure. Tubules
are two of multiple necrotizing granulomas of varying sizes are necrotic and distended with lymphocytes and plasma cells.
distributed through this section of kidney. Individual lesions consist The smudgy, blue materials in the cytoplasm of remaining tubular
of center of eosinophilic necrotic debris rinuned by multinucleated epithelial cells are clusters of intracytoplasmic Chlamydia psittaci.
giant cells and surrounded by mononuclear inflammatory infiltrate.
Blue-stained bacterial colonies are seen in the necrotic debris.
The kidneys were not cultured, but Gram stain showed that the
intralesional bacteria are Gram-negative.

456 I American Association of Avian Pathologists

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9.113. Kidney. Chlamydiosis.
legend of 9. l 14.
2-month-old conure. See the 9.115. Kidney. Chlamydiosis. 2-month-old conure. Kidney
secti on stained with Waithin-Starry stain . Within the lumen of
tubules are cells with cytoplasm packed with black granular materia l
representing Chlamydia organisms. Warthin-Stany stain seems to
be a good stain to highlight Chlamy dia in histological sections.

I
9.114. Kidney. Chlamydiosis. 2-month-old conure. This legend 9.116. Kidney. E11cephalitozao11 infection. 18-month-old
is also applied to 9.113. Necrotic tubule is di stended with necrotic lovebird. Renal tubules are necrotic and their lumens are packed
cells, several of which have intracytoplas mic smudgy-looking fill ed with eosinophilic materi al and tiny basophilic bodies
materia l representing clusters of Chlamydia psittaci. representing Encephalitozoon he//e111 .

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9.117. Kidney. E11cephalitozao11 infection. 18-month-old 9.119. Kidney. E11ceplwlitozao11 infection. 18-month-old
lovebird. The lumens of necrotic renal tubules are filled with lovebird. Kidney section stained with Gram stain. Renal tubules
eosinophilic material mixed with tiny basophilic bodies representing are necrotic and packed with Gram-positive tiny organisms
Encephalitozoon helle111. representing Encephalitozoon hellem.

9.118. Kidney. E11ceplwlitozoo11 infection. 18-month-old
lovebird. Renal tubules, some of which are still lined by epithelial
cells, are filled with eosinophilic material and tiny basophilic bodies
representing Encephalitozoon hellem. The arrows point to tubular
epithelial cells with intracytoplasmic organisms.
9.120. Kidney. Renal Coccidiosis. Goose. At this magnification,
renal tubules appear distended and their lining epithelial cells are
heavily parasitized by developmental stages of Eimeria truncata.

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9. 121. Kidney. Renal Coccidiosis. Goose. Higher-power view
of area in 9.120 showing multiple endogenous stages of Eimeria
tmncata within tubular epithelial cells. Some tubules are filled and
di stended with oocysts.
9.122. Kidney. Sarcocystis sp. infection. 2.5-year-old eclectus
parrot. Interstitial lymphocytic infiltration is lesion commonly
seen in birds infected with Sarcocyslis sp.
Uri11mJ' System
9.123. Kidney. Sarcocystis sp. infection. 2.5-year-old eclectus
parrot. Blood vessel in the kidney shows what looks like
proliferation of lining endothelial cells, with almost complete
obliteration of the vascular lumen. Small numbers of lymphocytes
are in and around the wall of the vessel.
I
9.124. Kidney. Sarcocystis sp. infection. 12-year-old cockatoo.
Segmental lymphocytic phlebitis in a vein. Sloughed tubular
epithelium and mononuclear inflammatory cells are in the lumen
of the vein.
Avian Histopathology (4 th Edition) I 459
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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,,,
; ., "
~.,·
. .·~
,..,

9.125. Kidney. Sarcocystis sp. infection. 12-year-old cockatoo. 9.127. Kidney. Leucocytozoon sp. infection. 8-month-old
Another vein in the kidney shows segmental lymphocytic phlebitis. backyard turkey. Schizont containing merozoites is present in the
Some mononuclear inflanmrntory cells and sloughed tubular kidney. The schizont is within the distended cytoplasm of tubular
epithelium are in the lumen . epithelial cell, but the intracellular location is not discernible.

I
9.126. Kidney. Sarcocystis sp. infection. 2.5-year-old eclectus 9.128. Kidney. Leucocytowo11 sp. infection. 8-month-old
parrot. Fibrin microthrombi are seen in glomerular capillary tuft. backyard turkey. Schizont containing merozoites.
The bird did not have bacterial septicemia, which typically causes
this lesion.

460 / American Association of Avian Pathologists


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9.129. Kidney. Trematodiasis. Partridge. Ureter or one of its
major branches is distended by two trematodes. Note the absence
of inflammation. This is likely Paratanaisia sp.
9.130. Kidney. Trematodiasis. Partridge. Higher-power view of
area in 9.129 showing trematode with eggs in the lumen of ureter or
one of its major branches.
Urill(IIJ' System
9.131. J(jdney. Trematodiasis. 3-year-old pigeon. Ureter
branches are dilated trematodes containing eggs with brown wall.
The trematode is Paralanaisia sp. (likely Paratanaisia bragai).
I
9.132. Kidney. Trematodiasis. 3-year-old pigeon. Demonstrated
are the eggs of Paralanaisia sp. (likely P. bragai) in a dilated ureter
branch. The eggs are emb1yonated and have brown wall. Another
characteristic feature of Paralanaisia sp. eggs is the presence of
operculum at one end.
Avian Histopathology (4 th Edition) I 461
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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9.133. Kidney. Tubular adenoma. 9-year-old lovebird. Low- 9.135. Kidney. Tubular adenoma. 9-year-old lovebird. High-
power view shows tubular structure of the adenoma. The adjacent power view demonstrating well differentiated tubular structures
renal parenchyma is compressed. lined by low cuboidal epithelial cells and containing proteinaceous
material.

I
9.134. Kidney. Tubular adenoma. 9-year-old lovebird. This 9.136. Kidney. Tubular adenoma. 9-year-old lovebird. Another
magnification shows that the adenoma consists of variab ly-sized area of the adenoma consists of dilated tubules lined by fl at
tubular structures lined by epithelial cells and contains proteinaceous epithelium.
material. Note the compression of the adjacent renal parenchyma
by the adenoma.

462 I American Association of Avian Pathologists


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9.137. Kidney. Tubular adenoma. Adn lt Amazon parrot. At
low magnification the tubular adenoma appears as basophilic area
that is well demarcated from the surrounding normal renal tissue.
9.138. Kidney. Tubular adenoma. Adult Amazon parrot.
Higher-power view of the adenoma in 9.13 7. The adenoma consists
of small tightly packed tubules with near-solid appearance. Small
lumen is recognized in some tubules. Note the cellular and nuclear
monomorphism and the prominent nucleoli. Normal tubules are on
the right.
Urill(IIJ' System
9.139. Kidney. Tubular adenoma. Adult Amazon parrot.
Higher-power view of the adenoma in 9.138.
I
9.140. Kidney. Nephroblastoma. Chicken. A. Large, nodular
tumor is compressing adjacent renal tissue. B. Higher magnification
shows tubule formation and fibrous stroma as well as the compression
of kidney.
Avian Histopathology (4 th Edition) I 463
 Tahseen Abdul-Aziz • Oscar J. Fletcher
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9.141. Kidney. Nephroblastoma. 9-month-old backyard 9.143. Kidney. Nephroblastoma. 9-month-old backyard
rooster. Area of the neoplasm consists of keratin pearls and variably rooster. See the legend of9.145.
sized tubular structures in collagenous stroma.

I
9.142. Kidney. Nephroblastoma. 9-month-old backyard 9.144. Kidney. Nephroblastoma. 9-month-old backyard
rooster. See the legend of9 .1 45 . rooster. See the legend of9.145 .

464 I American Association of Avian Pathologists

 Urill(IIJ' System
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9.145. Kidney. Nephroblastoma. 9-month-old backyard 9.147. Kidney. Nephroblastoma. 3.5-year-old backyard
rooster. This legend is also applied to 9.142, 9.143 , and 9.144. rooster. Group of primitive, poorly formed embryonic tubules,
Area of the neoplasm consists of embryonic tubules at various most of which do not have distinct lumens . This lesion represents
stages of differentiation in collagenous stroma. Embryonic tubules early differentiation of immature (blastema) cells into primitive
are irregular in shapes and branching, have lumens of various sizes, tubular epithelial elements.
and lined by single or double-cell layer of cuboidal to low colunmar
cells with hyperchromatic nuclei and prominent nucleoli. Poorly
formed tubules may appear as primitive, rosette-like structures.
There is interstitial accumulation of some immature (blastema)
cells.

I
9.146. Kidney. Nephroblastoma. 9-month-old backyard 9.148. Kidney. Nephroblastoma. 3.5-year-old backyard
rooster. Demonstrated is the so-called pseudoglomerulus or rooster. Occasionally seen are ductal structures that resemble
glomeruloid formed by tuft of lining epithelium that invaginates collecting ducts and contain colloid-like material.
into the lumen.

Avian Histopathology (4 th Edition) J 465

 Tahseen Abdul-Aziz • Oscar J. Fletcher
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9.149. Kidney. Nephroblastoma. 9-month-old backyard
rooster. Tubular structures in fibrocollagenous stroma. The tubules
are lined by flattened or squamous cells and contains eosinophilic
proteinaceous material. Few small nests of squamous epithelial
cells are present. Note the keratin pearl.
9.151. Kidney. Marek's disease. Backyard chicken. This
kidney is infiltrated by a dense population of neoplastic lymphoid
cells, resulting in loss of tubules.

I
9.150. Kidney. Nephroblastoma. 9-month-old backyard 9.152. Kidney. Marek's disease. Backyard chicken. Higher-
rooster. Nest of squamous epithelial cells adjacent to a keratin pearl. power view of area in 9.151 showing pleomorphic lymphoid
The keratin pearl indicates differentiation of a group of blastema cells. The pleomorphism of the neoplastic lymphoid cells is best
cells into squamous epithelial cells, which become keratinized and discernible in well preserved tissues.
forming concentric layers of keratin.

466 I American Association of Avian Pathologists


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9.153. Kidney. Marek's disease. LS-year-old backyard rooster.
Marked infiltration of the wall of a major ureter branch with
lymphoid cells.
9.154. Kidney. Marek's disease. LS-year-old backyard rooster.
Higher-power view of area in the wall of the ureter branch in 9.153 .
Urill(IIJ' System
9.155. Kidney. Lymphoid leukosis. 8-month-old backyard
chicken. Expanding the interstitium and separating renal tubules is
a dense infiltrate of lymphoid cells.
I
9.156. Kidney. Lymphoid leukosis. 8-month-old backyard
chicken. Same section as 9.155. This higher-power view shows
that the lymphoid infiltrate consists predominantly of large,
lymphoblast-like cells.
Avian Histopathology (4 th Edition) I 467
 Tahseen Abdul-Aziz • Oscar J. Fletcher
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9.157. Kidney. Lymphoid leukosis. 8-month-old backyard
chicken. Immunohistochemical staining shows that the lymphoid
cell infiltrate in the kidney is diffusely positive for FAX5, which is
marker for B lymphocytes. The cells were negative for CD3, which
is a marker for T-lymphocytes that comprise the lymphoid infiltrates
in Marek's disease.
I
9.158. Kidney. Lymphosarcoma and adenovirus inclusion.
Parakeet. This kidney had multiple areas ofneoplastic lymphocytic
infiltration. Scattered tubular epithelial cells contain intranuclear
inclusions typical of adenovirus inclusion bodies (arrow). Inse1t.
Higher-power view of adenovirus inclusion body in h1bular
epithelial cell.
468 I American Association of Avian Pathologists
9.159. Kidney. myelocytomatosis. Chicken. Neoplastic
myelocytes with characteristic eosinophilic cytoplasmic granules
are infiltrating and effacing the renal parenchyma. The insert shows
myelocytes at higher magnification.
9.160. Kidney. Metastatic hemangiosarcoma. 12-year-old
parrotlet. Area in the kidney has neoplastic tissue composed of
immature endothelial cells that tend to form small vascular spaces,
some of which contain red blood cells. The bird had metastatic
hemangiosarcoma in other organs. The primary site of the neoplasm
was uncertain.
VetBooks.ir
CHAPTER
Nervous System
David E. Swayne • H. John Barnes • Tahseen Abdul-Aziz • Oscar J. Fletcher
Introduction
To minimize postmortem artifacts, the brain and spinal cord need to
be removed and placed into fixative as soon as possible after the bird
dies. Ten volumes of I 0% neutral buffered formalin is adequate for
fi xation, but concentrations up to 20% can be used if needed to aid
fi xation. Allow adequate time for complete fixation to occur. Poor
sections that have an exploded appearance result from inadequately
fi xed CNS tissues. Incubating tissues at 42° C during fixation de-
creases the time required for complete fixation. Make one or more
transverse cuts in large brains to ensure fixation. In cases of lame-
ness, lumbosacra l spinal cord and sciatic nerves need to be exam-
ined. Spinal cord can be fixed in situ if the spine is trimmed as much
as possible. The spine can be decalcified and spinal cord trimmed
to provide both transverse and sagittal sections. Fixation of sciatic
nerves can be improved by isolating them at the beginning of the
necropsy, putting some formalin on them by filling the pocket cre-
ated by the elevated adductor muscle, and leaving them to fix in situ
until the necropsy is completed. Alternatively, they can be stretched
along a wooden tongue depressor or piece of cardboard, allowed to
dry slightly so the nerves adhere, and then placed into fixative with
the nerve down. Clamping or stapling is an alternate way to attach
nerves so that contraction artifacts are minimized.
Trimming brain tissue for optimal histologic evaluation pres-
ents a dilemma. Two methods are used 1) multiple transverse sec-
tions or 2) a single midline sagittal section. The former method
maximizes the potential for finding lesions but results in addition-
al cost and microscopic sections to evaluate. However, multiple
transverse sections are recommended when a thorough examination
of the brain is needed. Making a midline sagittal section is more
popular and quicker but, potentially, lesions could be missed, e.g.,
encephalomalacia in the entopallium [=ectostriatum] due to sodium
chloride toxicity. Both methods are possible if brains from multiple
affected birds are available.
Interpreting histopathologic changes in the avian brain requires
distinguishing pathologic lesions from normal structures, necropsy
a1iifacts, and postmortem or fixation atiifacts. This is not always
easy. There may be variation in normal anatomic structures due
to type of avian species, age of the bird, or individual bird varia-
tion within a population. Presence of an external granular cell layer
in the cerebellum and paraventricular hypercellularity consisting of
glial rests are common in young birds. Foci of myelopoiesis may
be observed in peripheral nerves of birds of any species. Having
access to similar birds and tissues for comparison is helpful but may
10
not be possible if the bird is an uncommon species. A1iifacts of
careless necropsy technique include loss of the pineal gland, which
is attached to the dura mater, presence of bone fragments or tissue
damage within the neuropil, and tearing and bleeding a1iifacts of
the medulla following cervical dislocation. Brains from birds eu-
thanized by blunt force trauma to the head are of little value for his-
tology. Artifacts of inunersion fixation and/or prolonged postmor-
tem interval include expanded clear Virchow-Robin spaces around
blood vessels and around neurons, shrunken dark angular neurons,
especially in the Purkinje cell layer of the cerebellum, separation of
molecular and granular cell layers of the cerebellum, and increased
vacuoles within white matter tracts, especially in the cerebellar
arbor vitae adjacent to the fourth ventricle. Vacuolation of white
matter and loss of myelin during processing can be confused with
antemortem demyelination.
Another problem is how to interpret the presence of mi-
nor proliferative or degenerative lesions in otherwise clinically
"healthy" or "normal" individuals, i. e., background histologic
changes. It is possible to see fibrosis and lymphoid foci in the
interstitium of the choroid plexus, scattered small foci of gliosis,
hypertrophied vascular endothelium of small arteries, isolated
small clusters of hemosiderin-laden macrophages, and cuffing of
occasional blood vessels with a few mononuclear cells in the CNS.
Lymphocytic foci in nerve sheaths, lymphocytes around vessels or
between axons, and mild Schwann cell hyperplasia are seen oc-
casionally in peripheral nerves.
Histology
The nervous system of birds is similar to that of mammals as it is
composed of two major paiis, the central nervous system (brain and
spinal cord) and peripheral nervous system (sensory, motor, and
autonomic nerves, ganglia, and specialized sensory nerve recep-
tors). Recently, the classical anatomy of the avian brain has been
revised to better coincide with the structure of the mammalian brain
and account for the intellectual abilities of birds. Most changes in
understanding the structure of the avian brain are in the complex
organization of the cerebrum (telencephalon) (see http://avianbrain.
org/atlases.html). In this chapter, the current terminology for the
anatomy of the brain is followed by the classical nomenclature in
parentheses.
Compared to mammals, the brains of birds have propo1iion-
ally larger cerebral hemispheres that lack fissures, gyri, and sulci
(i.e. , they are lissencephalic), and usually have a rudimentary olfac-
Avian Histopathology (4 th Edition) I 469
 David E. Swayne • H. Jol,11 Ba mes • Tal,see11 Abdul-Aziz • Oscar J. Fletcher
tory cortex, which accounts for the relatively poor sense of smell
in most birds. Each cerebral hemisphere is divided into a dorsal
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pallium, which accounts for approximately 75% of the volume of
the cerebrum, and a ventral subpallium. Layers comprising the pal-
lium from outer to inner include the hyperpallium (hyperstriatum),
mesopallium (hyperstriatum ventrale), nidopallium (neostriatum),
and arcopallium (arcostriatum). The pallium contains the hippo-
campus, olfactory cortex, and parahippocampal area. The ventral
subpallium consists of the striatum and pallid um and includes the
basal ganglia. With the exception of the hyperpallium, which is
unique to birds, evolution of the telencephalon has been highly
conserved among vertebrates .
The thalamus forms the central part of the diencephalon. A
distinct pineal gland is present dorsally within a triangular fissure
between the cerebral hemispheres and cerebellum and a slender in-
fundibulum connects the hypothalamus to the pituitary gland locat-
ed in the sella turcica caudal to the optic chiasma. The avian mid-
brain or mesencephalon has two very large optic lobes, or tectum.
A large medulla oblongata and minimal pons characterize the avian
rhombencephalon. The cerebellum is relatively large and composed
of a single median structure, the body of the cerebellum, which cor-
responds to the mammalian vermis. Lateral lobes of the cerebellum,
as observed in mammals, are small, or rudimentary, in birds. Ven-
tricles in the brain and central canal in the spinal cord are similar to
mammals, but they vary in size according to the area of the central
nervous system in which they are located. Choroid plexuses arise
in the 3rd and 4th ventricles. Those in the 3rd ventricle extend into
the lateral ventricles. Like mammals, birds have 12 pairs of cranial
nerves of which the optic nerves are the largest. Complete decus-
sation occurs at the optic chiasma. Unlike mammals, spinal nerves
extend laterally from the spinal cord and there is no cauda equina.
Meninges cover the brain and spinal cord. Melanin may be present
in the meninges of some birds, especially the dura mater covering
the cranial cerebrum. Melanin needs to be distinguished from he-
mosiderin, which is found in the cytoplasm ofphagocytic cells. The
dura mater fuses with the periosteum in the cranium but not in the
cervical and anterior thoracic vertebral canal. A cavernous rhom-
boidal sinus located dorsally at the lumbosacral intumescence of the
spinal cord contains the glycogen body, an ovoid clear gelatinous
mass . It is normal for myelin sheaths and axons to have differing
diameters in peripheral nerves.
Degeneration and Necrosis
Degeneration and necrosis of the nervous system are conunonly
associated with nutritional deficiencies or toxicities. Necrosis fre-
quently accompanies inflammatory lesions caused by infectious and
parasitic agents (see Inflammation).
Nutritional Deficiencies
Vitamin A deficiency
Vitamin A deficiency produces ataxia in young poultry, but in mature
poultry, nervous signs are usually lacking or inconsistent. Typically,
gross CNS changes are more profound than histologic changes in
young chicks. These include herniation of the olfactoty bulbs into
the cranial portion of the venous sinus, herniation of the caudoven-
470 I American Association of Avian Pathologists
tral cerebellar folia through the foramen magnum , herniation of the
rostroventral cerebellar folia under the tentorium cerebelli, flatten-
ing of all cerebellar folia, and transverse ridging of the cervical sp i-
nal cord. Histologically, the brain is edematous, cerebellar foli a are
flattened, and axons in the ventral and lateral white matter columns
of the cervical spinal cord are swollen. Cerebrospinal fluid (CSF)
pressure is increased . The increased pressure and CNS lesions result
from reduced growth of the calvarium while CNS growth remains
unaffected, but this process has not been consistently demonstrated
experimentally. CNS lesions occur simultaneously with early squa-
mous metaplasia of nasal respirato1y epithelium.
Vitamin E/selenium deficiency
Nutritional encephalomalacia in young birds of several species re-
sults from a deficiency of vitamin E. Affected birds show tremors,
incoordination, and recumbency. Historically, spontaneous cases
have been categorized microscopically into ischemic, vacuol ar,
sclerotic, and vasculoproliferative forms. However, for diagnos-
tic purposes, lesions are best classified as either acute or chronic.
The acute clinical disease represents an ischemic event. Grossly,
cerebellums are soft, swollen with flattened folia , and pale or red
from hemorrhage. Malacia is most severe on the folial tips but may
involve the entire cerebellum. Histologically, cerebellums are ne-
crotic and have numerous intralesional fibrin thrombi in capillar-
ies, edema, and hemorrhage. Necrotic lesions are less frequent in
the cerebral hemispheres and rare in the optic tectum. In young
turkeys, the lumbar spinal cord is most often affected. Lesions in-
clude bilaterally sy mmetrical necrosis of spinal cord gray matt er,
associated vascular thrombosis, and hemorrhage. In milder form s,
gross lesions may be lacking but, histologically, vacuolation due to
edema is present in the tips of the cerebellar arbor vitae and granular
cell layers, as well as the medulla and posterior commissure. In
the chronic form , necrosis is replaced by marked disorganization
of the cerebellar architecture, fibrous connective tissue from intral-
esional blood vessels, astrogliosis (increased number of astrocytes),
astrocytosis (swollen, pale astrocytes), dystrophic calcification, and
proliferation of capillaries in the cerebellum, or, less frequently, the
cerebrum. Primary selenium deficiency does not directly produce
encephalomalacia but can result in pancreatic lesions and secondary
vitamin E deficiency through maldigestion and malabsorption.
B-J1itami11 deficiencies
Chicks and turkey poults with riboflavin deficiency exhibit a "curl ed
toe" posture, leg paralysis, and dystonia. Affected pigeons show pa-
ralysis but do not have curling of the toes. In severe cases, brachia!
and sciatic nerve plexuses are grossly enlarged and have a yellow
discoloration. Histologically, lesions in nerves are segmental and
include separation of nerve fibers, interstitial edema, Schwann cell
hypertrophy and hyperplasia, demyelination, axonal degeneration,
and mild to moderate perivascular lymphoplasmacytic infiltrates.
More recently, lesions in experimental riboflavin deficiency in
young, rapidly growing chickens occmTed mainly in sciatic, cervi-
cal, and lumbar spinal nerves, sparing the spinal cord, spinal nerve
roots , and smaller distal nerve branches to muscle and skin. Acute
thiamine deficiency produces a "star-gazer" posture in young birds

but definitive histologic lesions are lacking in the CNS and periph-
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era l nervous system (PNS). In chronic thiamine deficiency, leg
we akness and mild degenerative changes, similar to riboflavin de-
fi ciency may occur. Experimental thiamine deficiency in chickens
is a model of beriberi polyneuropathy in humans. Pantothenic acid
deficiency produces severe myelin and mild axonal degeneration in
all white matter columns of the spinal cord.
Toxicities
Sodium chloride
Excessive intake of sodium chloride or other sodium salts in the
diet or water induces ataxia, incoordination, tremors, and sudden
death in turkeys, pheasants, and waterfowl. Bilateral necrosis of
the entopallium [ectostriatum J with vascular congestion and edema
occ ur in severe cases; however, most birds have only CNS conges-
tion and edema.
Feed additives
Excesses of certain preventative, therapeutic, and growth promot-
ing feed additives can produce nervous signs. Ionophore antibiotics
(narasin, salinomycin, lasalocid, monensin, etc.) produce severe my-
opathy in chickens and turkeys, but vacuolization and demyelination
also occur in the brain and spinal cord. Organic arsenicals, given at
twice the intended level for turkeys, produce "curled-toe" paralysis
and ataxia, which is clinically similar to riboflavin deficiency. Pe-
ripheral myelinated nerves have myelin and axonal degeneration,
as well as demyelination and swollen Schwann cells. Excess of 3,
5-dinitro-o-toluamide (zoalene), nitrophenide, and dimetridazole
produce neurological signs in poult1y but unequivocal histologic le-
sions have not been identified. At doses that do not cause neuro-
logic disease in poultiy, zoalene produces fine tremors, rolling gait,
and incoordination in pigeons (Co/u111ba /ivia). There is necrosis
of Purkinje cells in the cerebellum and an associated glial reaction,
but caution must be exercised in differentiating neuronal necrosis
from postmortem a11ifact, especially in Purkinje cells. Al1emisinin,
a promising drug for prevention and control of coccidiosis, can cause
toxic effects in broiler chickens at high doses. Brain lesions include
central clu-omatolysis of neurons, scattered neuronal necrosis, and
mild spongy changes that are most severe in the cerebrum, but also
can be found in cerebellar, midbrain, and hindbrain nuclei.
Ketamiue!Xy/azine
Ketamine/xyline combination is used for anesthesia in birds. Ket-
amine produces vacuoles in cortical neurons, cytoplasm of large
neurons, and neuropil. Yohimbine minimizes these effects.
Organoplwsplrntes (OP)
Exposure to organophosphates (OP) can result in one of two clinical
syndromes: 1) peracute/acute neurologic disease or 2) organophos-
phate-induced delayed neuropathy (OPIDN). In peracute toxicity,
clinical signs develop rapidly because of inhibition of acetylcholin-
esterase and histologic lesions are absent. In OPIDN, ataxia and
weakness develop slowly over days to weeks . Microscopically,
initially there is degeneration of peripheral nerve axons of large
myelinated fibers in spinocerebellar tracts and dorsal and ventral
columns of the spinal cord. Spheroids may be seen within axon
Nervous System
spaces. Advanced lesions include axonal and myelin degeneration
in the cerebellar peduncle and cerebellar arbor vitae, and necrosis
of neurons in the Purkinje cell layer, cerebellar and gracile nuclei,
and ventral horn of the lumbar spinal cord. The ability to produce
severe, delayed neurotoxicity depends on the individual OP com-
pound. Tri-o-cresyl phosphate (TOCP) is found in numerous in-
dustrial products and has been studied extensively in chickens, the
preferred animal model for OPIDN. Compared to adults, young
birds are more resistant to delayed neurotoxicity.
Senna (=Cassia) occideuta/is
In addition to mitochondrial myopathy characterized by generalized
muscle necrosis, ingestion of Senna (=Cassia) occidenta/is seeds,
results in a peripheral neuropathy. Degeneration, occasional loss of
axons, and irregularity of myelin sheaths are seen in affected birds.
Lead
Lead causes wasting, nervous signs, and lesions. Peripheral neurop-
athy and encephalopathy following ingestion of lead affects mainly
waterfowl and pet birds. Waterfowl accidentally ingest lead shot or
sinkers whereas pet birds are usually exposed by picking up lead
from their environment. Lead most commonly produces swelling
and fragmentation of myelin sheaths in peripheral nerves and motor
nerve degeneration in the spinal cord. Although less frequent, lead
can also cause loss of axons with minimal demyelination. In free-
living ducks, demyelination of peripheral nerves and vacuolization
at the junction of the molecular and granular cell layers in the cer-
ebellum occur. Capillary tlu-ombosis, hemorrhage, and Purkinje cell
necrosis are also present.
Methyl mercury
Methyl mercmy, which used to be a common agricultural seed
dressing, causes a subacute syndrome of head-tremor, ataxia, and
incoordination. The consistent lesion in mercury poisoning is fibri-
noid necrosis of blood vessels, especially in the cerebellum, cranial
meninges, and gray matter of the spinal cord. Peripheral myelinated
nerves have perineural and epineural edema and Wallerian degener-
ation. Axonal swelling and ellipsoid formation are present in spinal
cord white matter, cerebellar arbor vitae, and medulla. Occasional
degenerating neurons are present in the paleostriatum (globus palli-
dus), entopallial nucleus (ectostriatum), nidopallium (neostriatum),
and hyperpallium (hyperstriatum), with associated neuronophagia
and mild gliosis .
Organic arsenica/s
Organic arsenicals have been used as feed additives to improve
growth, feed efficiency, and prevent or treat histomoniasis. Toxici-
ties happen because of their relatively low toxicity index. Micro-
scopically, peripheral neuropathy characterized by demyelination,
axonal fragmentation, and Schwann cell hypertrophy and hyperpla-
sia is seen.
Avian vacuolar myelinopathy (AVM)
The condition was first recognized in 1994 in bald eagles and later
in coots and several other species of waterfowl , is characterized by
the presence of multiple vacuoles within the white matter (myelin-
Avian Histopathology (4 th Edition) I 471
 Da11id E. Swayne • H. Jol,11 Bames • Tahseen Abdul-Aziz • Oscar J. Fletcher
ated tracts) of the CNS . Lesions in the optic lobes are common,
but can be found in other myelinated tracts within the cerebrum,
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cerebellum, medulla, and spinal cord. Vacuoles result from intra-
myelinic edema and are not associated with inflammation or dam-
age to neurons. Oral gavage of extracts from aquatic plants, most
frequently hydrilla (Hydrilla 11erticillata), that contain Aetokthonos
hydri/lico/a, a previously unknown epiphytic cyanobacterial spe-
cies, consistently reproduces the disease in mallards. Chickens are
susceptible to AVM.
Trauma
Collisions with stationary or moving objects are common in birds.
Head injuries occur when birds fly into stationary objects that are
unexpected, e.g. , clear glass windows or doors. Skull fractures with
hemorrhage that is usually subdural are seen. If the bird survives,
hemorrhage may completely resolve or be marked by an area of
fibrosis with hemosiderin-filled macrophages. Dislocation of the
occipitoatlantaljoint, which frequently occurs in head-on collisions,
can be identified by hemorrhage around the joint with possible ex-
tension through the foramen magnum over the surface of the cau-
dal cerebellum. Damage to the spinal cord from the dislocation is
generally severe and fatal. Lesions are best appreciated when the
joint is fixed , demineralized, and sagittally sectioned. Fractures in-
volving the base of the skull often resolve, but hydrocephalus is a
possible sequela. Hemosiderin-filled macrophages mark the site of
the previous fracture.
Spinal Cord Injury
Trauma
Handling large turkeys or fractious captive birds can result in pa-
resis or paralysis within the following week. Birds that fail to re-
cover show a variety of traumatic lesions in the spinal cord includ-
ing compression, hemorrhage (contusions), and partial to complete
transection. Lesions are usually in the vicinity of the free-thoracic
vertebra (FTV). Cai1ilaginous and osseous emboli causing infarc-
tion and myelomalacia may be seen. Fractures and dislocations are
additional possible causes of spinal cord trauma. Calluses that de-
velop after a fracture may cause stenosis of the ve11ebral canal and
impinge on the spinal cord.
Spondylolisthesis
Commonly called "kinky back", spondylolisthesis is a frequent
cause of lameness in some commercial broiler and turkey flocks.
There is a progressive ventral deviation of the notarium that culmi-
nates at the free thoracic vertebra causing it to be displaced ventrally
at its cranial articulation. This forces the free thoracic vertebra to be
angled dorsocaudally, which causes stenosis of the vertebral canal
and compression of the spinal cord at the caudal articulation of the
FTV. Hemorrhage and malacia are present where the spinal cord
has been compressed; demyelination and occasional swollen axons
in the ventral tracts, and distorted degenerating neurons in the gray
matter are seen.
Spondylitis
Inflammation and necrosis of the ve11ebral bodies (spondylitis) of
the FTV and adjacent vertebrae in the notarium and synsacrum are
472 I American Association of Avian Pathologists
caused by bacteria, especially Staphy lococcus aureus, Enterococ-
cus cecorum, and Escherichia coli. Kyphosis develops as the ver-
tebral bodies erode away and inflammatory lesion expands dorsally
causing vertebral canal stenosis and compression of the spinal cord .
Microscopic lesions in the spinal cord are the same as those seen
in spondylolisthesis. Occasionally, lymphocytic cuffs are present;
most likely in response to free myelin.
Metabolic Diseases
Long-lived cells such as neurons are susceptible to the accumula-
tion of metabolic products that cannot be catabolized by lysosomal
enzymes because the mechanism to digest and remove them from
the cells does not exist or is overwhelmed. They accumulate during
the life of the bird and increase in amount with age.
Ceroid and lipofuscin
Conm1on among these are the "wear and tear" or "aging" pigments,
ceroid and lipofuscin, which are lipoproteins that arise from the
breakdown and oxidation of unsaturated lipids in cell membranes.
Lipofuscin is a golden-brown to dark brown granular pigment lo-
cated in the cytoplasm of neurons, glial cells, and other cells in the
body. It tends to accumulate in one area of the cytoplasm of the cell
and varies in amount among neurons. It can be especially abundant
in large neurons in certain nuclei in the brain stem . Lipofuscin var-
ies in composition, but generally stains well with acid-fast and PAS
stains. Ceroid is an early form of lipofuscin. While lipofuscin in
neurons of older birds is considered part of the normal aging pro-
cess and not clinically relevant, the presence of ceroid and lipofus-
cin in young birds is indicative of neuronal ceroid lipofuscinosis,
which has been described in a 9-month-old Peach-faced Lovebird
(Agapornis roseicollis). Lipofuscinosis also has been associated
with "pinching off syndrome", a generali zed feather abnonnality in
White-tailed sea eagles (Haliaeetus albicilla), but the nature of th e
relationship remains unknown. Diets high in rancid fats or deficient
in antioxidants promote lipofuscin development in other animals,
but whether or not this occurs in birds is unknown.
Lysosomal stomge diseases
When a lysosomal enzyme is absent or functioning abnormall y,
substrate accumulates within the lysosomes resulting in a group of
diseases known as lysosomal storage diseases (LSD). Most LSDs
are prima1y due to genetics, but they can be acquired because of
interference by plant toxins or drugs on lysosomal enzyme fun c-
tion. Highly inbred populations with restricted gene pools are at
highest risk of primary LSDs. As substrate accumulates within
lysosomes, neuronal function decreases until the cell is no longer
functional. Birds with an inherited LSD typically exhibit progres-
sively worsening neurologic disease and eventually die while still
relatively young. Microscopically, changes are most evident in the
large neurons in the brain stem, mid-brain, and ventral horns of the
spinal cord . Affected cells are swollen, nucleus is displaced, normal
cytoplasmic organelles (Niss! substance) are compressed around
the nucleus, and the remaining cytoplasm is filled with numerous
small inclusions that give the cell a "foamy" appearance. Inclusions
stain weakly with hematoxylin and eosin, but usually stain well with

PAS and variably with Luxol-fast blue stains. LSDs identified in
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birds include probable metachromatic leukodystrophy in Hawaiian
geese (Bran/a sandvicensis) , GM2 gangliosidosis (Tay-Sachs dis-
ease) in American flamingos (Phoenicopterus rube,') , an uncharac-
terized LSD in Costa 's hummingbirds, and mucopolysaccharidosis
IIIB (Sanfilippo Syndrome) in emus. LSDs in birds have value as
models of human diseases. A possible acquired sphingolipidosis,
considered secondary to chloroquine treatment, affected a captive
colony of Humboldt penguins (Sphenisc11s h11111boldti).
Developmental Conditions
Parvovirus infection of embryos has been associated with cerebellar
hypoplasia and hydrocephalus in day-old broiler chickens, which
exhibited nervous signs, impaired mobility, and diarrhea . Histologi-
ca lly, irregular shape and reduced size was noted for cerebellar folia ,
which were accompanied by distended ventricles (hydrocephalus).
Focal areas along the base of folia lacked an internal granular cell
layer, and the associated Purkinje cells were disorganized and lo-
cated within the molecular layer. Similar lesions have been pro-
duced experimentally via yolk sac inoculation of embryos with fowl
glioma avian leukosis virus.
Infections
Viral infections
Lesions in the nervous system caused by viral infections are pre-
dominantly inflammatory, but may also be necrotic or neoplastic.
They can be placed into 5 categories: I) lesions exclusively or pre-
dominately in the nervous system, including avian encephalomy-
elitis virus, paramyxovirus type 1 in pigeons, and certain arbovi-
ruses (togaviruses and flaviviruses); 2) systemic diseases with major
nervous system involvement, such as virulent strains of Newcastle
disease virus, highly-pathogenic avian influenza (Al) virus, and the
inflammatory phase ofMarek's disease virus infection; 3) systemic
diseases with minor nervous system involvement, including certain
mildly virulent strains of Newcastle disease virus and mildly patho-
genic Al viruses; 4) primary tumors, such as retrovirus-induced
gliomas; and 5) metastatic tumors, such as Marek's disease virus-
induced lymphosarcoma. Malacia (necrosis) of the central nervous
system releases free myelin , which provokes an immune-mediated
lymphocytic inflammation.
He1pesviruses
Marek 's disease (MD), caused by an alpha herpesvirus, infects pri-
marily chickens and occasionally Japanese quail, and turkeys. Ner-
vous signs occur frequently because of lesions in the central (CNS)
and peripheral nervous systems (PNS), and from transient paralysis
(TP). In the nervous system, MD is evident as either polymorphic
mononuclear cell inflammatory lesions or, infrequently, neoplastic
infiltrates ofT-lymphocytes secondaiy to systemic metastasis. Sev-
eral clinical forms of MD occur including neurologic (classical),
visceral (acute), ocular, and cutaneous. In neurologic MD, major
lesions are found in autonomic and motor nerves of the PNS and
are associated with progressive unilateral, or occasionally bilateral,
ascending paralysis. Grossly, affected nerves are enlarged, lose nor-
mal cross striations, and may be discolored yellow. Histologically,
Nen 1011s System
PNS lesions in myelinated motor nerves are classified as either type
A or B lesions. Type A lesions are typically neoplastic. Peripheral
nerve lesions are composed of massive infiltrations oflymphoblasts,
some medium and small lymphocytes, scattered .large basophilic
mononuclear cells (Marek 's disease cells), mild to moderate demy-
elination, and occasional Schwann cell proliferation. Type B lesions
are inflammatory and are characterized by separation of nerve fibers
because of edema and infiltration by small lymphocytes, immature
and mature plasma cells, and occasional lymphoblasts. Demyelin-
ation and Schwann cell proliferation may be present, but are typical-
ly associated with areas of severe interneuritic edema. Lymphocytic
ganglioneuritis of dorsal root ganglia and lymphocytic neuritis of
visceral autonomic nerves, including sympathetic and parasympa-
thetic ganglia associated with visceral organs, are common.
Involvement of the CNS is less frequent than involvement
of the PNS . Lesions are typically mild and include perivascu-
lar mononuclear cell cuffs and, occasionally, focal demyelinating
plaques, predominantly in the cerebellar arbor vitae or brain stem.
Lesions are typically angiocentric and do not involve the neuropil
between vessels, which aids in differentiating MD from other viral
encephalitides in birds. Lymphocytic meningitis and gliosis ad-
jacent to mononuclear cell cuffed blood vessels are occasionally
present, but neuronal degeneration rarely occurs. A few ataxic or
paralyzed chickens are typically seen in visceral (acute) MD. No
gross lesions are seen in the CNS and PNS of these birds, but there
are histologic changes similar to those observed with neurologic
(classical) MD. Rarely, there may be tumors (lymphosarcomas)
in the neuropil.
Demyelinating lesions in peripheral motor nerves likely rep-
resent an autoimmune reaction to nerve fiber proteins, such as
myelin basic protein . These lesions are histologically similar
to experimental allergic neuritis. Additionally, MD-free Rhode
Island Red chickens have been reported to develop lymphocytic
neuritis histologically similar to type B MD nerve lesions . This
change results from an autoimmune reaction to the nerve and is
not associated with MD virus infection (see Immune-mediated
Diseases).
Two forms of TP are recognized - classical (cTP) and acute
(aTP) . cTP or "pseudobotulism" is an acute reversible generalized
paralytic syndrome primarily observed in laying chickens. Resis-
tance to development of cTP is associated with genes in or closely
linked to the major histocompatibility complex. The principle histo-
logic lesions are located in the CNS, especially the cerebellar arbor
vitae and medulla. These lesions include 1) vasculitis with intra-
mural phagocytized cluomatin debris, heterophils, and pseudocysts,
and endothelial cell hypertrophy and hyperplasia, 2) widening of
extracellular spaces or linear to spherical vacuolization primarily
due to vasogenic edema, 3) widespread mononuclear cell perivascu-
lar cuffs, 4) mild astrocytosis and gliosis, and 5) swollen astrocytic
nuclei due to intracellular and intranuclear edema. Chickens with
cTP have decreased brain density, particularly in the cerebellum.
Peripheral nerves may have mild lymphocytic neuritis, but clinical
signs of TP do not result from PNS lesions. cTP can be differenti-
ated from botulism, because chickens with cTP do not have paraly-
sis of eyelids, and clinical recove1y from cTP occurs within 24-72
Avian Histopathology (4 th Edition) I 473
 Da11id E. Swayne • H. Jol,11 Eames • Tal,see11 Abdul-Aziz • Oscar J. Fletcl,er
hours. Microscopically, no lesions are seen in the brains of chickens
with botulism. Clinical recovery from cTP is associated with reso-
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lution of vasogenic and cytotoxic edema. Acute transient paralysis
(aTP) can be produced by inoculating 3-week-old chickens with
very virulent MD virus strains, which results in flaccid paralysis
of the neck and limbs. Principle lesions include acute vasculitis
with vasogenic edema and lymphocytic perivascular cuffing in the
brain. Pathogenicity of the virus and genotype of the chicken are
the major factors that contribute to aTP. The more virulent the virus,
the greater the number of chickens that die from aTP. Unlike cTP,
birds with aTP are affected at an earlier age, onset is more acute, and
they do not recover.
Reports ofneurologic di sease in pigeons caused by a herpesvi-
rus have not been substantiated. Such cases have been identical in
signalment and lesions to neuropathologica l disease caused by avian
paramyxovirus type I (pigeon paramyxovirus).
Polyo11,avi1·uses
Polyomaviruses produce systemic disease in fledgling budgerigars.
Brains may contain lesions most prominently in the cerebellum, fol-
lowed by the cerebrum, and finally the optic lobes and brainstem.
Neuronal cell bodies are vacuolated, especially in the Purkinje and
molecular cell layers, and cerebellar arbor vitae. Karyomegaly with
intranuclear inclusion bodies are present in vacuolated cells and cer-
ebellar meninges. Inclusion bodies are lacy and faintly basophilic.
Blood vessels in the cerebrum and cerebellum may have mural and
perivascular mononuclear cells, as well as hypertrophy and prolif-
eration of endothelial cells.
Adenoviruses
Parrotlets experiencing hemorrhag ic enteritis and encephalitis had
non-heterophilic encephalitis and hemorrhage. Large homogenous
eosinophilic intranuclear inclusion bodies in endothelial cells were
numerous in the brain. On EM, adenovirus was demonstrated in th e
inclusio n bodies, and, although initially negative, inclusion bodies
were positive for aviadenovirus (Group I avian adenovirus) on im-
munohistochemist1y.
Picomavimses
Avian encephalomyelitis (AE) virus, a picornavirus, produces neu-
rologic signs primarily in chickens less than 6 weeks of age but
can occasionally be observed in Japanese quail (Cotumixjaponica) ,
pheasa nts, and turkeys. Older chickens can be infected, but the in-
fec tion is typically subclinical and localized to the alimentary tract.
Clinically, young birds may be ataxic or have head tremors; paraly-
sis may occur in advanced cases. In the peracute stage or in chicks
less than one week of age, histologic lesions may be lacking. In
acute to subacute stages, central chromatolysis of large neurons is
prominent in nuclei isthmi , ruber, reticularis, rotundus and cerebel-
laris, and in the ventral horns of the spinal cord. In subacute-to-
chroni c stages, microgliosis of the spinal cord and brain, particu-
larly in the nuclei cerebellaris, ovoidalis, and rotundus, is common .
Multifocal microgliosis of the Purkinje cell layer, with triangular
or flame-like extensions into the molecular layer, is suggestive of
AE. Less frequent lesions include mild widespread mononuclea r
474 I American Association of Avian Pathologists
cell perivascular cuffs, especially in the optic tectum, edema of th e
Purkinje cell layer, neuronophagi a, and neuronal satellitosis. In-
creased numbers of lymphoid follicles in the tunica muscul ari s of
the proventriculus and ventriculus and in the pancreas are usuall y
present and may aid in diagnosis. Meningitis is rarely associated
with AE. Cataracts can follow infection of adults.
Pancreatitis and encephalitis affecting Muscovy ducklings has
been tentatively ascribed to a variant duck hepatitis I virus. In-
fection of Muscovy ducks with duck hepatitis I virus is normall y
asymptomatic.
01·tho111yxoviruses
Highly-pathogenic avian influenza (HPAI) viruses frequently pro-
duce CNS lesions, but the lesions vary in severity depending on indi-
vidual virus strain and host species. In general, chickens and turkeys
develop multiple small to large foci of necrosis in all areas of th e
brain, both in gray and white matter. Additionally, individual ne-
crotic neurons with neuronophagia may be prominent in the Purkinje
cell layer of the cerebellum, nucleus cerebellaris, and ventral horns
of the spinal cord. Frequently assoc iated lesions include severe lym-
phohistiocytic encephalomyelitis (evident as perivascular cuffs of
lymphocytes and macrophages), microgliosis, edema, and vascular
endothelial swelling. With certain HPAI stra ins, only mild nonhet-
erophilic meningitis may be present. Historically, one HSN9 low
pathogenic AI virus was reported to have produced minimal-to-mild
lesions in the nervous system of inoculated turkeys, but the isolate
was likely a mixture of low and highly pathogenic HSN9 viruses.
Emergence and maintenance of HSN I HPAI in poultry
populations in Asia since 1996 has resulted in altered pathobi -
ology of HPAI infections and the lesions they produce. Prior
to 2002, infection resulted in systemic disease, including neu-
rological lesions in gallinaceous poultry, but rarely in domesti c
waterfowl or wild birds. Since 2002, HSN 1 strains ha ve emerged
that can infect and cause syste mic les ions in wild birds and do -
mestic waterfowl. Typically, such severe disease and death in
avian species has been associated with high virus titers in th e
brain. For example, A/chicken/Hong Kong/220/97 (HSN l )
HPAI virus caused multi-organ lesions and death in intranasa l-
ly inoculated chickens, turkeys, quail , guinea fowl, pheasants,
partridges, house finches, and budgerigars, while infections or
deaths were not observed in domestic clucks, pigeons, or g ull s.
However, after a period of tim e, HSN! HPAI viruses caused hi gh
mortality in experimentally- and natural infections of mute and
whooper swans, in addition to other wild waterfowl. Pi geo ns and
crows have brain lesions with Af viral antigen, as demonstrated
by immunohistochemistry, but infection of pigeons requires hi gh
close exposure apparently because of their natural resistance to
AI viral infections. Lesions in the brain caused by these HSN I
HPAI viruses include lymphoplas macytic or lymphohi st iocyti c
ence phalitis and neuron a l necrosi s. Glial nodules may also be
found. Immunohistochemical demonstration of AI viral antigen
in affected brains is need ed to rul e o ut other neurotrophi c v iru s-
es. Often, numerous neurons, including Purkinje cells, and g lial
cells contain Al viral antigen , which can be demon strated using
immunohistochemistry.

Para111yxovi1·11ses
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In turkeys and chickens, pathogenic strains of avian paramyxovirus
J (previously referred to as velogenic or mesogenic viruses, but now
called Newcastle disease viruses [NDV]) produce CNS signs and
lesions. Low or non-pathogenic strains of avian paramyxovirus 1,
previously known as lentogenic strains, do not produce pathology
in the CNS. They are no longer called Newcastle disease viruses;
only avian paramyxovirus 1 (APV 1) v iruses . Highly virulent neu-
rotropic pathotypes produce the most frequent and severe lesions in
the nervous system, followed by highly viru lent viscerotropic and
mildly pathogenic (mesogenic) pathotypes. Not all mildly patho-
genic pathotypes produce lesions in the nervous system.
In general, NDV produces a pantropic, nonheterophilic en-
cephalomyelitis with chromatolysis of neurons, gliosis (astrocyto-
s is), hypertrophy and hyperplasia of endothelial cells, and perivas-
cular mononuclear cell cuffs. Chromatolysis is most prominent in
neurons of the spinal cord, nuclei cerebellaris, and medulla of chick-
ens. Additionally, proliferative vasculitis is a prominent chronic
change, especially in the molecular layer of the cerebellum. Large
necrotic foci , as occur in highly pathogenic AI, are infrequent in
ND, but certain strains do inconsistently produce small foci of ne-
crosis. Infections with mildly pathogenic (mesogenic) NDV can
cause perivascular cuffing without neuronal changes. Lesions are
most frequently observed in the cerebellum, but no part of the brain
is excluded . Demyelination is not a feature of ND caused by any of
the pathotypes. More severe lesions are observed at 10 days post
inoculation (DPI) than 5 DPI suggesting a role for immunity in le-
sion development.
In pigeons, a type I avian paramyxovirus similar to NDV pro-
duces torticollis, ataxia , tremors, disordered vision, and balance.
Most birds have widespread, nonheterophilic panencephalitis or en-
cephalomyelitis. Myelitis is most prominent in the ventral horns of
the cervical and lumbar spinal cord. Leptomeningitis is infrequent
for this viral infection. Mild degenerative changes and lymphocytic
neuritis are present in the PNS ; the brachia! plexus more often af-
fected than the sciatic plexus. Neuronal degeneration and neurono-
phagia, especially of Purkinje neurons, as well as gliosis and endo-
thelial cell proliferation, occur with the pigeon virus. Occurrence
of these lesions is more frequent with viruses that are more virulent.
Eosinophilic intracytoplasmic inclusion bodies and enlarged
nuclei of neurons and glial cells with marginated chromatin and eo-
sinophilic intranuclear inclusion bodies are characteristic in passer-
ine and psittacine birds infected with avian paramyxovirus 3.
Alphaviruses
Alphaviruses are in the family, Togaviridae. Together, alphaviruses
and flaviviruses are referred to as arboviruses as they are usually
transmitted by arthropods, although direct fecal-ora l transmission
can occur. Several alphaviruses cause asymptomatic infections in
wi ld birds and domestic poultry raised on range .
Eastern equine encephalo111yelitis (EEE) virus produces a fulmi-
nating neurologic disease in capt ive pheasants and occasionally
in chukars, partridges, ducks, pigeons, and turkeys. In pheasants,
vasculitis is the most frequent lesion. Nonheterophilic meningo-
Nen,o us System
encephalomyelitis, especially in the rostral portions of the telence-
phalic complex, is present; however, vascular endothelial hypertro-
phy and hyperplasia are more frequent lesions and are distributed
equally throughout the brain. Accompanying lesions may inc lude
neuropil necrosis associated with vasculitis, microgliosis, especially
in the molecular cell layer, and occasionally neuronal degeneration
and neuronophagia. In whooping cranes and emus, EEE virus pro-
duces a fulminating disease with visceral organ necrosis but no CNS
lesions. Highlands J virus causes neurologic disease similar to EEE
virus infection, but is less severe. High lands J virus is a close rela-
tive of EEE virus.
Western equine e11cephalitis (WEE) virus produces nonheterophilic
meningoencephalitis in poultry but infections are infrequent com-
pared to infections with EEE virus.
Buggy creek virus is related to WEE virus. In contrast to most
a lphaviruses that do not cause clinical disease or pathology in wild
birds, house spatTows are clinically affected, experience mortality,
and have CNS lesions of encephalitis characterized by lympho-
plasmacytic perivascular cuffing and gliosis. Lesions also occur
in the spinal cord, but are mild. The normal avian host for Buggy
creek virus is the cliff swallow, which remains asymptomatic fol-
lowing infection.
Flaviviruses
West Nile virus (WNV), a member of the Flaviviradae family, is an
example of a viral infection having neurotropism in addition to sys-
temic effects. Infections with WNV first appeared in the United
States in New York City in 1999. Since then, the virus has spread
throughout the continental United States and into Canada, Mexico,
Central America, and parts of South America. Many avian species
are susceptible including crows, blue jays, ow ls, goshawks, hawks,
pelicans, and geese. Infection has occurred in a wild turkey. Le-
sions in the central nervous system include multifocal lymphoplas-
macytic and histiocytic perivascula r cuffing and formation of glial
I
nodules in the brainstem, cerebellum, and spinal cord, with neuro-
nal necrosis. lmmunohistochemistry is used to demonstrate WNV
antigen in the cytoplasm of neurons, including Purkinje neurons ,
glial cells, and endothelial cells. Necrosis and inflammatory lesions
may be present in other organs of the most severely affected species,
especially heart, eye, and kidneys. Among poult1y, domestic geese
are most severely affected, but disease has been reported in breeder
turkeys, pheasants, and partridges.
Israel Turkey lvleningoencephalitis Virus. In the Middle East, tur-
key meningoencephalitis virus, a flavivirus distinct from WNV, pro-
duces nonheterophilic meningoencephalitis in turkeys.
Bagaza virus is a flavivirus in the Ntaya virus group, which also
includes the avian pathogens Israel turkey meningoencephalitis vi-
rus and Tembusu virus. Previously unknown outside of Africa and
Asia and as a cause of m01tality in birds, Bagaza virus emerged in
southern Spain in 2010 where it caused neurologic disease and high
mortality in red-legged partridges and pheasants. Encephalitis and
lesions similar to those ofWNV were reported. Complete sequenc-
Avian Histopathology (4 th Edition) I 475
 David E. Swayne • H. John Ba mes • Tahseen Abdul-Aziz • Oscar J. Fletcher
es of Bagaza virus and Israel Turkey meningoencephalitis virus in-
dicate they are the same virus. Avian meningoencephalomyelitis
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virus has been proposed as the name for both viruses.
Te111busu virus causes an infectious disease of ducks and geese in
southeastern China characterized by very high morbidity, moder-
ate to high mortality, hemorrhages in the brain and other organs,
egg-drop in breeders, and neurologic disease (ataxia and paralysis) .
Microscopic lesions in the brain consist of multifocal perivascular
lymphoplasmacytic cuffing, scattered glial nodules, and central
chromatolysis and neuronophagia of neurons. Both glial cells and
neurons stain positive with immunohistochemistJy. The virus has
recently been isolated from laying chickens experiencing an acute
drop in egg production.
Sitiawan virus, a close relative of Tembusu virus, causes encepha-
litis, growth retardation, and hyperglycemia in young chickens in
Southeast Asia.
Usutu virus, a mosquito-borne African flavivirus of birds in the
Japanese Encephalitis group, has emerged as a significant cause of
encephalitis among free-living and captive birds in Europe. Infec-
tion, but no clinical disease, developed in experimentally inoculated
chickens and geese. Histologic lesions are similar to those in WNV
infection. Neurons stain positive for Usutu virus by specific im-
munohistochemistry. Positive staining may also occur when poly-
clonal antibodies to WNV are used.
Louping ill virns. Louping ill virus is a tick borne flavivirus that
infects mammals and birds, especially red grouse. The virus oc-
curs at higher elevations in Great Britain and Scandinavia where
the host tick (Ixodes ricinis) is found . In brains of experimentally
infected red grouse, there was focal lymphocytic meningitis ini-
tially, which was followed by encephalitis, predominantly in the
cerebrum, consisting of perivascular mononuclear cell accumula-
tions. Lesions were similar to those in pheasants infected with EEE
virus. Immunostaining can be used to obtain a specific diagnosis.
The brains from 32 grouse inoculated with louping-ill virus
were examined. The earliest changes observed were those of focal
non-suppurative meningitis at 5 days after inoculation. Birds dying
after 8 days also showed encephalitis, predominantly in the fore-
brain, consisting of perivascular accumulations of mononuclear
inflammatory cells. The distribution and character of these lesions
differed from those of louping-ill in sheep, but resembled lesions
which have been described in pheasants infected with eastern equine
encephalitis virus.
Reoviruses
Reoviruses are not normally associated with neurologic disease.
However, a specific enteric reovirus strain caused high mo11ality,
stunting, and nervous signs (head shaking, tremors, torticollis) af-
ter experimental inoculation of SPF chickens. Infected chickens
had roughly symmetrical dark red spots in the caudal cerebrum that
corresponded to a severely congested choroid plexus. Microscopi-
cally, there was focal gliosis, perivascular cuffing with mononuclear
cell s, and congestion of the choroid plexus. lmmunohistochemistry
476 I American Association of Avian Pathologists
confirmed presence of the virus in the brain, but the virus was also
identified in the spinal cord including spinal ganglia .
Bornaviruses
A syndrome of proventricular dilatation (Macaw Wasting Syn-
drome, Proventricular Dilatation Syndrome [PDS] or Disease
[PDD], Leukoencephalomyelitis, Ganglioneuritis) and neurologic
disease caused by at least 13 genotypes of avian bornaviruses has
been identified in many bird species including macaws, cockatoos,
conures, parrots, cockatiels, ducks, geese, swans, and canaries. In-
fected birds have myenteric and submucosal lymphocytic ganglio-
neuritis with associated atrophy of neurons in the proventriculus,
ventriculus, descending duodenum, and celiac ganglion. In some
birds, there is peripheral neuritis. Lymphoplasmacytic leukoen-
cephalomyelitis frequently occurs concurrently with lesions in auto-
nomic nerves. Lesions in the brain occur, in descending frequency,
in the medulla1y region of brain stem, cerebrum, and cerebellum.
Immunohistochemistly is useful in confirming the diagnosis and
identifying infected cells.
Retroviruses
Experimental Rous-associated virus (RAV)-7 or RAV- I infection of
chicken embryos produced ataxia, lethargy, and imbalance in chicks
at hatching. Histologic lesions included non-heterophilic perivas-
cular panencephalomyelitis, meningitis, and astrocytic hype11roph y
and hyperplasia. Demyelination and vacuolation did not occur in
the CNS and lesions in the PNS were absent. Virus was present in
neurons of the cerebellar granular layer, endothelial cells of CN S
blood vessels, and epithelium of the choroid plexus. Naturally oc-
curring cases with CNS or PNS lesions have not been reported.
Avian leukosis viruses. Ce11ain strains of avian leukosis virus cause
gliomas and tumors of peripheral nerves naturally and meningiomas
experimentally (see Neoplasia).
Lymphoproliferative disease. Peripheral nerves 111 turkeys with
lymphoproliferative disease may be slightly enlarged and, histo-
logically, have focal lymphoplasmacytic neuritis similar to mild
Marek 's disease neuritis.
Reticu/oendothe/iosis. Progeny of viremic chickens develop inco-
ordination, leg paralysis, and feather defects. In these progeny, ac-
cumulation oflymphocytes in the perineurium of sciatic nerves, and
perivascular and widespread focal accumulations of mononuclear
cells in the telencephalic complex and cerebellar arbor vitae are
present. In adult chickens, turkeys, and ducks, gross nerve enlarge-
ment may be present, especially in the cervical portion of the va-
gus nerve. Histologically, neuritis with pleomorphic lymphocytes,
plasma cells, edema, and, occasionally, perivascular lymphocytic
encephalitis, especially in the cerebellar peduncles, are present. The
neuritis is histologically similar that in Marek's disease but gener-
ally has a higher proportion of plasma cells.
Bacterial i11fectio11s
A variety of Gram-negative and Gram-positive bacteria produce in-
flammatory lesions in the nervous system of birds, usually in th e

CNS (although the spinal cord is not frequently examined) . Gram-
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negative bacteria, including Salmonella spp., Escherichia coli, En-
terobacter spp. , and Pse11do111011as aer11gi11osa, and Gram-positive
bacteria, including Staphylococcus spp., Streptococcus spp., and
E11terococc11s spp., produce similar acute and chronic lesions, usu-
ally secondary to sepsis or, in the case of Gram-positive organisms,
valvular endocarditis. Lesions associated with Gram-positive bacte-
ria are generally less heterophilic and more histiocytic in character.
Acute lesions include fibrinous , fibrinoheterophilic, heterophilic,
or necrotizing meningitis, encephalomyelitis, or meningoencepha-
lomyelitis. Chronic lesions usually include heterophilic or histio-
cytic granulomas. The latter are more often associated with chronic
fungal infections or, rarely, A1ycobacteri11111 avium . Pathogenesis
of bacterial CNS lesions usually involves one of the following
mechanisms : I) septicemia, especially secondary to omphalitis and
yolksacculitis, 2) embolism from vegetative valvular endocarditis,
3) penetrating trauma including embryo and chick vaccination, 4)
extension from cranial osteomyelitis, 5) extension from otitis me-
dia/interna, or 6) migration along cranial nerves (ganglioneuritis).
Coliform bacteria (Enterobacteriaceae)
Coliform bacteria, especially Sal111011ella enterica subspecies en-
terica serovar Typhimurium and Sal111011ella enterica subspecies
Arizonae, are frequent causes of bacterial meningoencephalitis, usu-
ally secondaty to omphalitis, yolksacculitis, and sepsis. Focal areas
of necrosis with bacterial colonies, numerous degenerating hetero-
phils, fibrin , and, in adjacent tissue, gliosis and perivascular cuffs
of inflammatory cells occur in the brain. The subarachnoid space
is filled with degenerating or necrotic heterophils, fibrin, necrotic
debris, and bacterial colonies . Salmonella enterica subspecies Ari-
zonae has a tendency to produce severe granulomatous ventriculitis,
especially of the lateral ventricles, erosion of ependyma, periven-
tricular edema, and perivascular cuffs of mononuclear cells. Other
serovars of Sal111onella enterica subspecies enterica can cause me-
ningoencephalitis.
Pseudomonas
P aeruginosa causes extensive disseminated necrosis in the CNS of
young birds following sepsis. Omphalitis, trauma, and contaminat-
ed injections, including vaccines, are the most common ways that
infections occur. Necrotic vessels surrounded by numerous bacteria
that are not aggregated into colonies and heterophilic inflammatory
changes extending into the adjacent neuropil are characteristic of
Pse11do111onas infections.
Encephalitis and meningoencephalitis result from natural and
experimental infections with P pse11do111allei (melioidosis), but the
disease is rare in birds, even in endemic areas.
Pasteurella muftocida
CNS lesions occur in some cases of chronic fowl cholera in broiler
and turkey breeders, and layers. CNS lesions develop by spread
from otitis media or infected air spaces of the calvarium to the me-
ninges. This is commonly referred to as "head cholera". Tmticollis
is the primaty nervous sign seen in affected birds. Fibrinoheterophil-
ic to heterophilic, granulomatous meningitis is present. Meningitis
Ner11011s System
is most severe over the medulla and cerebellum, and heterophilic
encephalitis is present adjacent to areas of severe meningitis. Con-
current lesions in the ears and cranial bones accompanying menin-
gitis aid in identifying chronic fowl cholera. Pasteurella does not
normally form colonies but organisms are often numerous making
identification of the small, Gram-negative rods in exudate possible.
Riemerella anatipest/fer
R. anatipestifer produces fibrinous polyserositis mainly in growing
ducks, although geese, turkeys, and other species of birds are less
frequently infected. Sick ducks may have head tremors, ataxia, and
diarrhea. CNS signs are associated with fibrinous to fibrinohetero-
philic meningitis and ventriculitis. Fibrin tends to be more evident
in lesions caused by Riemerella than those caused by P multocida,
although this is not sufficient to fully differentiate the infections. Le-
sions in the subpial and periventricular neuropil may be associated
with meningitis, but generalized encephalitis is not characteristic.
Often, there is vasculitis and vessels with perivascular cuffs of mixed
inflammatory cells. Intralesional bacteria can usually be identified.
Ornithobacteriw11 rhinotracheale
Although the respiratory tract is the primary site for 0. rhinotra-
cheale infection, if septicemia occurs, it can result in fibrinous to
fibrinoheterophilic meningitis. Exudate tends to be more fibrinous
compared to that in fowl cholera. Bacteria are usually not seen.
Listeria 111011ocytoge11es
Listeriosis is uncommon, not contagious, and tends to occur sporad-
ically. Free-range birds and confined poultty in wet environments
are most likely to develop the disease; probably because of their
contact with soil where the organism is found. Two forms oflisteri-
osis occur in birds - visceral listeriosis and neural listeriosis. Neural
listeriosis tends to affect young birds whereas mature birds typically
develop the visceral form of the disease. Usually birds have only
one form, but occasionally, they may have both. Newly hatched
chicks become septic and have necrosis of multiple visceral organs
and nervous signs including incoordination, tremors, drooping and
paralysis of one or both wings, and unilateral or bilateral toe paraly-
sis. The brain has congested meninges, edema in the subarachnoid
space, a few lymphocytic perivascular cuffs, extensive neuronal de-
generation and satellitosis, and spongifonn changes in the cerebellar
arbor vitae. Broilers and hobby chickens infected with L. 1110110-
cytogenes show incoordination, torticollis, anorexia, and lethargy.
Lesions in the CNS consist of extensive multifocal necrosis, large
perivascular lymphocytic cuffs, axonal degeneration, heterophilic
granulomas covered with multinucleated giant cells, diffuse gliosis,
thrombosis, and hemorrhage in the brain, especially the brain stem,
and spinal cord. Intralesional small Gram-positive rods are identi-
fied, but they are not uniformly distributed within the lesions. Facial
trauma followed by migration of bacteria along cranial nerves to the
CNS has been proposed as a method of infection.
Streptococcus
Sepsis and meningitis occur in turkey poults and ducklings infected
with S. gallolyticus subsp. pasteurianus (=S. bovis). Meninges are
thickened because of fibrin and infiltration of inflammato1y cells,
Avian Histopathology (4' h Edition) I 477
 David E. Swayne • H. John Ba mes • Tahseen Abdul-Aziz • Oscar J. Fletcher
and bacteria, usually in colonies, are numerous when brain sections
are stained with Gram stain.
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Bacterial thrombosis
Various bacterial species, especially enterococci and streptococci,
produce vascular embolism secondary to valvular endocarditis.
Bacterial colonies in blood vessels in the brain are associated with
transmural necrosis, thrombosis, infarction, hemorrhage, and peri-
vascular cuffs of inflammatory cells. Inflammatory cells are mostly
heterophils and macrophages, but there may also be multinucleated
giant cells and gliosis. Gram-positive cocci are associated with
variably sized foci of malacia in cerebral peduncles, optic lobes,
medulla, and cerebrum. Intravascular bacterial colonies are usually
not located within vessels in malacic foci , but are present in vessels
in unaffected tissue away from the lesions. Enterococcus durans is
associated with this pattern of injury. E. hirae can cause meningo-
encephalitis. Gram-stains of tissue sections aid in identifying the
causative organisms. Multiple sections may be needed to find intra-
vascular bacterial colonies.
/v!ycobacteriw11
Both A1. avi11111 and Atl genavense rarely produce granulomatous le-
sions in the meninges, brain, and spinal cord. Infection of autonomic
ganglia in the intestine has been described. Lesions va1y from menin-
gitis without involvement of the brain to marked perivascular cuffing
of virtually all cerebral and spinal vessels. Cells are plump histiocytes
with granular eosinophilic cytoplasm. Acid-fast staining reveals nu-
merous positive-staining bacteria in the cytoplasm of the histiocytes.
Mycoplas111a spp.
1n addition to respiratory and arthritic signs, mycoplasmal infections
can occasionally produce nervous signs including ataxia, opisthoto-
nos, disturbances of equilibrium, retrograde movements, torticollis,
and twisted necks. ln ducklings, M.ycop!asma anatis produces lym-
phohistiocytic meningitis and cerebroventriculitis. Infection of the
nervous system with M. galliseptic11111 in turkeys results in moder-
I ate to severe lymphoplasmacytic meningoencephalitis with fibrinoid
necrosis of vessels, especially in the basal and cerebellar meningeal
vessels, and acute to subacute, focal to multifocal necrosis in the neu-
ropil. M :,:)//1oviae in turkeys produces mild to severe vasculitis in
meningeal vessels, but does not affect vessels in the brain. Vascular
changes range from fibrinoid necrosis without perivascular cuffing to
lymphoplasmacytic intramural infiltrates with vascular necrosis. Vas-
culitis also occurs in vessels of many visceral organs. Tlu·ombosis is
occasionally present. Capillaiy endothelial swelling that occludes the
vessels causing ischemia is responsible for the CNS lesions.
Other bacteria
Chlamydia psittaci rarely produces CNS lesions in naturally occur-
ring poult1y cases. Experimental studies in chickens and turkeys
inconsistently identified lymphohistiocytic meningoencephalitis,
vasculitis, and occasional necrotic foci.
A Coxiella-like organism infects multiple tissues , including
brain, ofpsittacines. The organism is found within cytoplasmic vac-
uoles of macrophages. Vacuoles contain a cluster of small slightly
basophilic cocco-bacilli .
478 I American Association of Avian Pathologists
Fung(I/ infections
Aspergillus
Asperillus spp., primarily A. f11111igat11s , causes CNS disease sec-
ondaiy to pulmonary infections in chickens, turkeys, ducks, quail ,
and several other bird species. Infections in captive birds are es-
pecially common. Lesions occur primarily in the cerebellum and
cerebrum and vary from acute lesions of necrotizing encephalitis
or meningoencephalitis with malacia to chronic lesions of necrosis
and heterophilic granulomas. Necrosis tends to be extensive. Inva-
sion of blood vessels with thrombosis is often seen . Diffuse gliosis
and perivascular lymphocytic cuffing occur in the adjacent neuropil.
Hyphae are 3-5 µm in diameter, branch dichotomously, have paral-
lel sides, and are septate. A. fi1111igat11s typically stains well with
hematoxylin in H&E sections.
Ochroconis gallopava
(formerly Dactylaria gallopava) produces incoordination, torticol-
lis, lateral recumbency, and tremors in chickens, turkeys, and Jap-
anese quail. Grossly, the brain is diffusely reddened with focall y
extensive, demarcated, firm , pale lesions in the cerebellum and cere-
brum less frequently. Multifocal to coalescing areas ofmalacia with
extensive granulomatous inflammation and occasional heterophils
are seen microscopically. Large, often elongated, multinucleated gi-
ant cells that usually have intracellular fungi are numerous . Hyphae
either do not stain or stain poorly in conventional H&E sections.
In histologic sections stained for fungi, hyphae are 1.2-2.4 µm in
diameter, septate, and irregularly branched. Septa tend to be widel y
spaced and may be difficult to identify. Fungal hyphae are naturall y
pigmented (dematiaceous) yellow to pale brown making them easy
to identify in unstained sections.
Encephalitozoon spp.
E11cephalitozoo11, which is currently class ified as fungus in the class
Microsporida, commonly infects a variety of birds based on mo-
lecular studies and has been shown to be vertically transmitted but
it rarely causes disease. Multifocal granulomas with intralesional
Gram-positive organisms morphologically consistent with Micro-
sporidia may be found in the brain of systemically infected birds.
Otherfimgi
Infrequently Penicilli11111 spp., zygomycetes including Mucor and
Rhizopus species, CiJ1ptococc11s, and Candida cause natural or ex-
perimental mycotic encephalitis in birds.
P"msitic infections
Protozoa
Several Apicomplexan protozoa including the hemoprotozoa P!as-
111odiw11 and Leucocylozoon and coccidians Toxop!asma, Sarcocys-
tis, and Neospora cause encephalitis in birds. Infections occur in
free-living birds and hobby or free-range birds kept outdoors; com-
mercial , intensively reared poultry are not affected .
Hemoprotozoa
In passerine birds and penguins with fatal malaria, exo-erytlll'ocytic
meronts develop in endothelial cells and occlude capillaries in th e
brain. Generalized congestion of capillaries is seen. Meronts vary

in size, but are much smaller than those of Leucocytozoon. They
are thin-walled, and contain few to many merozo ites . Birds can die
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when exo-erythrocytic meronts occlude capillaries before parasites
appear in red blood cells. Chickens infected with Plas111odiw11 gal-
linace11111 develop both severe anemia and occlusion of capillaries
in the brain. Mortality can occur from either one and is correlated
w ith the level of parasitemia. Edema, proteinaceous fluid, and mild
gliosis accompany capillary occlusion.
A few species of Leucocytozoon are pathogenic for birds in-
cluding L. simondi in ducks and other waterfowl , L smithi in tur-
keys, L ca11/le1J1i in chickens, and a Le11cocytozoo11 sp. in Nankeen
kestrels. Meronts of some species are very large (megalomeronts) .
As in Plas111odi11111 infections, mortality from Leucocytozoon infec-
tions is mainly due to vascular occlusion by meronts. Megalom-
eronts are capable of occluding larger vessels in the brain causing
infarction and necrosis. Inflammation in the brain may or may not
be associated with megalomeronts. The Leucocytozoon species in
Na nkeen kestrels did not produce megalomeronts but did incite a
vasculocentric granulomatous meningoencephalomyelitis and pro-
liferative arteritis in the brain, spinal cord, and eyes in response to
small intralesional meronts.
Two-host coccidians
Except for some carnivorous birds that are definitive hosts for Sar-
cocystis and also shed sporocysts in their droppings, birds serve
as intermediate hosts while mammals are the definitive hosts for
the coccidians Toxop/asma, Sarcocystis, and Neospora. Birds ac-
cidentally ingest sporulated oocysts or sporocysts shed in the feces
of infected definitive hosts, or ingest prey that has infective tissue
stages. Free-range poulhy and wild birds that forage on the ground
are most likely to ingest infective oocysts or sporocysts. Follow-
ing ingestion, sporozoites are released in the bird's digestive tract
and enter the circulation where they invade host cells and develop
into short-lived stages (free tachyzoities or meronts). Toxoplasma
tachyzoi tes multiple by endodyogeny eventually generating cysts
containing numerous bradyzoites. Merozoites are released and
develop into long-lived meronts that are most common in muscle,
heart, and brain. Cysts and meronts remain viable for the life of
the bird until it is eaten by the definitive host and the life cycle of
the parasite continues. Cysts and meronts that develop in the brain
may cause subclinical or clinical disease characterized by neuro-
logic signs. Canaries develop cataracts and become blind following
infection with Toxop/asma. Severe infections may be fatal. Af-
fected birds are more susceptible to predation by the definitive host.
Protozoa may develop in a broad range of hosts or be restricted to
just one or a few bird species.
Toxoplasma infection in the brain of birds is characterized by
necrosis (malacia), demyelination, neuronal degeneration, gliosis,
lymphocytic encephalitis, and endothelial cell hyperplasia. Enceph-
alitis is most prominent in the brainstem and cerebellar cortex. Nu-
merous tachyzoites are typically seen early in necrotic foci. They
may be difficult to distinguish from cells and cell debris in conven-
tional histologic sections, but are easily identified using immunos-
taining. In advanced infections, there are tissue cysts containing
bradyzoites without associated tissue changes. Cysts stain well with
Nervous System
PAS stain ; tachyzoites stain well with Giemsa stain . Usually, both
tachyzoites and bradyzoites are present in lesions of clinically af-
fected birds.
Species of Sarcocystis causing neurologic disease in birds
include S. neurona, S. falcat11/a, and S. ca/chasi. These species
lack host specificity and infect a variety of birds. In some cases
of neurosarcocystosis, the species of Sarcocystis is not identified.
S. calchas i causes Pigeon Protozoa! Encephalitis, but infects other
species of birds both nan1rally and experimentally. Mortality from
neurologic disease occurs several weeks after mortality associated
with meronts in the lungs and visceral tissues. Lesions consist of
necrosi s, g liosis, and lymphoplasmacytic to lymphohistiocytic me-
ningoencephalitis. Similar lesions occur less frequently in the spi-
nal cord. There may or may not be intralesional protozoa! meronts.
Sarcocystis meronts often have a radial appearance because mero-
zoites bud off of a mother cell by a process called endopolygeny. A
T-cell mediated delayed hypersensitivity has been proposed as the
cause of lesions when there are no cysts.
Neospora is similar to Toxoplasma. Serological and molecu-
lar studies in free-range chickens and other birds indicate Neospora
infection is widespread and relatively common. Chickens and pi-
geons are susceptible to experimental infection following ingestion
of sporulated oocysts from infected canines. Pathology of infected
birds has not been described. Neospora needs to be differentiated
from Toxoplasma and Sarcocystis by immunohistochemishy when
there are intralesional protozoa.
tvfetazoa
Migrating larva of Baylisascaris procyonis cause cerebrospinal ne-
matodiasis in domestic poultry, ratites, gamebirds, Co/11111bifor111es ,
Passeriformes, and Psitlaciformes. The disease occurs when feces
from parasitized raccoons contaminate feeds. Infected birds devel-
op progressive ataxia, paralysis, and torticolli s. There are no gross
lesions. Microscopically, there is liquefactive necrosis, granuloma-
tous migrational tracts, and inflammation in the cerebrum, cerebel-
I
lum, and brain stem. Inflammation consists of a mixture of gitter
cells, lymphocytes, macrophages, giant cells, granulocytes, and
plasma cells with some neovascularization and perivascular cuff-
ing of mixed inflammat01y cells. Larvae may be found within the
inflammatoty lesions or free in the neuropil without inflammatory
cells; most foci of inflammation lack larvae. Migrating larva of
Toxocara cati, a nematode of domestic cats, also produces similar
lesions in the brains of chickens.
In various wild and captive birds in the orders Passeriformes
and Psittac/formes, adult filarioids, especially Chand/ere/la quis-
cali, are located in the ventricles of the brain . Usually, infections
are subclinical, but some compression of periventricular neuropil
and a microfilaremia may be present. In emus, an abnormal host for
the parasite, Chand/ere/la causes verminous encephalitis. Parasites
occur free in the ventricles or in the brain and spinal cord. Either
mild or no inflanunation is associated with parasites in the brain or
spinal cord. However, where there are no parasites, there is mild to
moderate perivascular cuffing, meningitis, and foci of histiocytes
and lymphoplasmacytic cells associated with necrosis. Hemorrhage
is sometimes seen in lesions.
Avian Histopathology (4 th Edition) I 479
 David E. Swayne • H. John Rames • Tahseen Abdul-Aziz • Oscar J. Fletcher
· Neuroangiostrongyliasis is caused by the rat lungworm, Angio-
strongylus cantonensis. Birds become aberrant hosts after ingestion
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of infected intermediate hosts (snails or slugs), or paratenic hosts.
Infections occur in free-living birds in Southeast Asia and Australia,
especially tawny frogmouths (Podarg11s slrigoides), which develop
profound neurological disease following infection. Larvae follow
the same developmental course in birds as they do in rats except
they remain in the brain and spinal cord and do not become adults.
Responses to immature nematodes in the central nervous system
range from no lesions to mild to marked multifocal lymphoplas-
macytic and granulomatous meningitis, encephalitis, or myelitis.
Parasites provoke a granulomatous response when they shed their
sheaths as they molt or when they eventually die.
In ducks, nasal schistosomes, especially Trichobi/harzia re-
genti, enter peripheral nerves shortly after penetrating the skin and
migrate via the spinal cord and brain to the meninges. Often no
inflammation immediately surrounds the parasite, but degeneration,
necrosis, and lymphocytic inflammation are found along migratoty
tracks. In contrast to other schistosomes, nasal schistosomes remain
in the brain and do not enter blood vessels during this phase of their
life cycle. After a period of time in the brain and meninges, para-
sites continue their migration to the veins of the nasal cavity where
they mature.
Eggs of schistosome species infecting visceral vessels, espe-
cially those of Dendritobi/harzia, which resides in atteries rather
than veins, can be accidentally swept into the brain where they
lodge. A granulomatous reaction around the egg may or may not
occur. Schistosome eggs can be recognized by their large size, thick
wall, and presence of an immature miracidium. Sometimes dead
miracidia are seen within the eggs.
Immune-Mediated Diseases
Acute paretic syndrome (peripheral neuropathy, idiopathic
polyneuritis)
A relatively low incidence (0-3 %) of a paralytic disease occurs
I
spontaneously in ce1tain lines of young white leghorn chickens
that usually have a specific major histocompatibility complex type
(B*l9). Acute paretic syndrome is a non-infectious polyradiculitis
that results from cell-mediated immune responses directed at my-
elin. Use of common poul!iy vaccines, other than Marek 's disease
vaccines, can predispose to the disease but do not cause it, presum-
ably via molecular mimic1y. Grossly, cranial and spinal nerves and
their nerve roots are affected. Enlargement of nerves in the sci-
atic plexus tend to be common and prominent. Segments or entire
nerves are enlarged, but not discolored.
Histologically, nerve lesions are similar to Type B Marek's dis-
ease (MD) lesions characterized by separation of nerve fibers by
edema, mild to moderate lymphocytic, lymphohistiocytic, or lym-
phoplasmacytic inflammation, mild perivascular cuffing especially
in ganglia, and demyelination. Mild to moderate microscopic le-
sions may be found in grossly normal nerves. Remyelination occurs
during lesion resolution. Th I lymphocytes initiate the disease while
Th2 lymphocytes predominate when the lesion is resolving. Ab-
sence of tumors or disease-specific lesions in other tissues, inabil-
ity to demonstrate MD Type I or reticuloendotheliosis viruses, and
480 I American Association of Avian Pathologists
negative serology help differentiate this disease from MD and other
tumor virus diseases that may produce similar nerve lesions. Acute
paretic syndrome is useful as an animal model of human inflam-
matory demyelinating diseases including Guillain-Barre syndrome.
Campylobacter-induced paralysis
Following experimental infection of chickens with isolates of Cam-
pylobacter jej11ni from humans with Guillain-BatTe syndrome, a
high percentage of birds developed a paralytic neuropathy. Proin-
flamm atoty cytokines (IFN-y, TNF-a , and IL-6) increased in sciati c
nerves concomitant with increasing inflammatory cells, including
lymphocytes and macrophages in foci and surrounding vessels.
Axonal degeneration and demyelination accompanied the inflam-
mation . Thi lymphocytes predominated when clinical signs devel-
oped, which were replaced by Th2 lymphocytes during the recov-
ery phase. Anti-inflammatory cytokines increased as inflammation
in the sciatic nerves subsided. Antibodies to lipooligosaccharides
in the cell wall of C. jejuni cross-reacted with gangliosides in my-
elin sheaths to activate complement. Production of antibodies was
strain- and host-dependent.
Neoplasia
Central nervous system
Primary astrocytomas in the brain of chickens occur as sporadic
cases or epizootics ("epizootic gliosis"). They are caused by fowl
glioma viruses, which are closely related variants and recombinants
of subgroup A avian leukosis viruses. Tumors are white, usually no
larger than 5 mm, and are most frequent along blood vessels that
have lymphocytic cuffing and the ventricles. Tumors are circum-
scribed and not invasive. Large tumors compress adjacent brain tis-
sue or project into the ventricle. The cerebrum is most often affect-
ed; fewer gliomas occur in the cerebellum and brain stem. Nodular
masses growing in the subcutaneous tissues of the head and neck
of Japanese bantams also are gliomas that are caused by a subtype
A recombinant fowl glioma virus. Microscopically, lesions prog-
ress through three stages: disseminated lymphocytic inflammation,
proliferation of glial cells (gliosis), and formation of glial nodul es
(gliomas). Small gliomas, composed almost entirely of gemi sto-
cytic astrocytes become increasingly sclerotic as they enlarge. Cell s
comprising gliomas are consistent with fibrillary astrocytes. Other
avian leukosis strains may to be able to induce glial tumors in the
CNS. Avian leukosis virus cannot be identified in all tumors.
Rarely, meningiomas have been reported in chickens. Intrace-
rebral injection of the retrovirus avian myeloblastosis virus, espe-
cially in highly susceptible White Leghorn Anya crosses, produces
meningiotheliomatous, fibroblastic, angiomatous, mixed, and an a-
plastic meningiomas.
Teratomas are rare tumors composed of multiple types of ti s-
sues that arise from two (didermic) or three (tridermic) embtyonic
germinal layers. In birds, they have been described from the brain
and spinal cord. A primary teratoma in the cerebrum occu1Ted in a
I-year-old fantail pigeon . The tumor was unencapsulated and com-
posed of adipose, cartilagenous, fibrous, and undifferentiated mes-
enchymal tissues. Epithelial and mesenchymal tissue types were
demonstrated by immunohistochemistry.

Peripheral nervous system
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Tumors of peripheral nerves, including benign and malignant forms
of neurofibromas, perineuriomas, and Schwannomas, are rare in
birds. Differentiation by light microscopy is difficult, but they can
be specifically identified using immunohistochemistry. Tumors
generally occur as nodules associated with nerves or as fusiform
or cylindrical enlargements of nerve roots or ganglia. Tumors may
occ ur as nodules elsewhere. Microscopically, cells are well dif-
fe rentiated , oval to spindle-shaped, and occur in interlacing cords
and bundles. Parallel arrays of spindle cells are characteristic of
Sc hwannoma s. Spindle cells that wrap around axons producing an
" o nion-bulb" appearance are seen in perineuriomas. Sheets of small
round cells with eosinophilic cytoplasm and mitotic figures are less
frequently seen. In chickens, tumors of peripheral nerves are sus-
pected to be associated with avian retroviruses.
Ganglioneuromas caused slowly progressing neurologic dis-
ease in cockatiels. Ganglioneuromas are benign neoplasms that
generally arise from spinal ganglia. Microscopically, they are com-
posed of ganglion cells (neurons), nerves, Schwa1m cells, spindloid
ce lls, and connective tissue.
Neuromas are benign tumors that are not true neoplasms. They
arise in severed peripheral nerves. Nerve damage may result from
trauma, surgical procedures in companion birds, or a management
practice in poultry to control persecution ("cannibalism") in which
the tips of the upper, lower, or both beaks are amputated . Regen-
erati ng nerves become entrapped in connective tissue resulting in a
s lowly enlarging tissue mass. Microscopically, disorganized con-
nective tissue containing numerous small nerves is seen .
Acknowledgement. The assistance of Dr. Isabel Gimeno in writ-
in g the section on Viral Diseases - Herpesviruses is gratefully
acknow Iedged.
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Avian Dis 48 :570-580.
Saggese, A.V. Wettere, and P. Redig. 2005. Pathologic and
immunohistochemical findin gs in goshawks (Accipiter genii/is)
and great horned owls (Bubo virginianus) naturally infected
with West Nile virus. Avian Dis 49:252-259.
Wtinsclunann, A. , N . Timurkaan, A . G. Armien, I. B. Padilla,
A. Glaser, P. T. Redig. 2014. Clinical, pathological, and
immunohistochemical findings in bald eagles (Haliaeetus
/eucocepha/us) and golden eagles (Aquila cl11J1saetos) naturally
infected with West Nile virus. J Vet Diagn In vest 26 :599-609.
Wyrzykowski B., 0. Albaric, S. Moreau, F. Nguyen, R. Fleurance,
S. Belluco, M . Wyers, and M.A. Colle. 2013. Retrospective
study of Jvlycoplas111a ga//iseptic11111 meningoencephalitis in six
turkey flocks in western France . J Comp Pathol 148: 173-177.
Wyrzykowski, B ., 0. Albaric, S. Moreau, F. Nguyen, R. Fleurance,
S. Belluco, M. Wyers, and M. A. Colle. 2013 . Retrospective
study of Mycop/asma ga//iseptic11111 meningoencephalitis in six
turkey flocks in western France . J Comp Pathol 148: 173-177.
Xu, M., S. D. Fitzgerald, H. Zhang, D. M . Karcher, and M.
Heidari. 2012. Vety virulent plus strains of MDV induce
an acute form of transient paral ysis in both susceptible and
resistant chicken lines. Viral ]11111111110125:306-323.
Zhang, Z., F. Wilson, R. Read , L. Pace, and S. Zhang. 2006.
Detection and characterization of naturally acquired West Nile
virus infection in a female wild turkey. J Vet Diagn Invest
18 :204-208.
*For additional references, see Swayne, D. E. 1996. Nervous
system . In C. Riddell, Avian Histopathology, 2 nd Ed. , Am Assoc Avi-
an Pathologists, New Bolton Center, Kennett Square, PA. 183-201 .

Table 1: Revised terminology, followed by classic terminology in parentheses

(httu·//avianbrain orn/atlases html)
A.

C.
Arcopallium
(Archi striatum)

Cerebellum

Ca. Cerebellar arbor vitae

L.

M.

N.
Nucleus prosencephali laterali s
(Lateral forebrain bundle)

Medulla

Nidopallium
(Neostriatum)
nVE. Nuclei vestibulares

Oc. Optic chiasm

Ot. Optic tectum

I
Cp. Cerebellar peduncles nC. Nuclei cerebellaris Pl. Olfactory tubercle & Medial striatum

Ps. Globus pallidus & Lateral striatum

E. Entopallium (Ectostriatum) nl. Nuclei isthmi
(Paleostriatum)
G. Hyperstriatum
nM . Nuclei mesencepha licus Pg. Pineal gland
(General cortex)
H. Hyperpallium & Mesopallium nR. Nucleus ruber
Pc. Posterior commissure
(Hyperstriatum) (Red nucleus)

He. Hippocampus nRe. Nuclei reticulari s V. Ventricle

nT. Substantia nigra

Ht. Hypothalamus
(Nucleus tegmenti)

Avian Histopathology (4' 11 Edition) I 485

 David E. Swayne • H. John Rames • Tahseen Abdul-Aziz • Oscar J. Fletch er
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10.1. Schematic. Chicken. Brain. Schematic of six tra nsverse sections and a sagittal section of the brain of a chi cke n. Revised terminology
is fo llowed by classic terminology in parentheses . (See previous page)

486 I American Association of Avian Pathologists

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10.2. Brain. Normal, sagittal section. One-day-old chicken. 10.4. Medulla. Normal neurons. 8-month-old emu. Normal
Note the relative size of the cerebellum. neurons in an emu from a flock with progressive neurologic disease
(Sanfilippo Syndrome). This bird was not affected. Compare with
I 0-36.

10.3. Cerebellum . Normal. One-day-old chicken. Shown is a
portion of cerebellar folium with external germinal layer, molecular
layer, Purkinje cell layer, and granular cell layer. Scattered darkly
stained Purkinje cells (arrows) are normal.
I
10.5. Brain. Nutritional encephalomalacia. Chicken. Distal
regions of several folia in the cerebellum are necrotic.

Avian Histopathology (4 th Edition) I 487

 David E. Swayne • H. John Bames • Tahseen Abdul-Aziz • Oscar J. Fletcher
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10.6. Brain. Nutritional encephalomalacia. Chicken. Higher 10.8. Brain. Nutritional encephalomalacia. Chicken. Detail of
magnification of a zone of cerebellar necrosis containing multifocal I 0.06 showing fibrin thrombi in small blood vessels, a characteristic
coalescing foci of hemorrhage. lesion of nutritional encephalomalacia.

I
10.7. Brain. Nutritional encephalomalacia. Chicken. Detail 10.9. Brain. Nutritional encephalomalacia. 4-week-old
of I 0.06 showing malacia, acute hemorrhage, and fibrin thrombi broiler breeder male. Marked demyelination of the white matter
occluding small vessels. in the cerebellar arbor vitae.

488 I American Association of Avian Pathologists

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10.10. Brain. Nutritional encephalomalacia. 4-week-old 10.12. Brain. Nutritional encephalomalacia. 4-week-old
broiler breeder male. Lesions consisting of marked vacuolation broiler breeder male. Detail of I 0.11 showing vacuolation of the
of molecular and Purkinje cell layers, necrosis of Purkinje cells, Purkinje cell layer and demyelination of the white matter. Granular
capillary fibrin thrombi, and extravasated red blood cells are in the and molecular layers are not affected.
cerebellum. Necrosis is also present in the granular layer.

10.11. Brain. Nutritional encephalomalacia. 4-week-old 10.13. Cerebellum. Nutritional encephalomalacia, sclerotic
broiler breeder male. Marked vacuolation of the Purkinje cell form. Chicken. Repair of the severely damaged cerebellum in
layer and mild demyelination and perivascular lymphocytic cuffing birds that survive the acute stages of nutritional encephalomalacia
in the white matter. occurs by marked astrocytosis and astrogliosis. Prominent swollen
astrocytes that are randomly arranged fill the molecular layer and
extend into the remaining granular layer. Vessels are not patent. A
single Purkinje cell remains (airnwhead).

Avian Histopathology (4 th Edition) I 489

 David E. Swayne • H. John Barnes • Tahseen Abdul-Aziz • Oscar J. Fletcher
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10.14. Peripheral nerve. Neuropathy. Myelin sheaths are 10.16. Peripheral nerve. Neuropathy. Myelin balls, small
swollen and vacuolated. A cause was not determined in this case, eosinophilic spherical collections ofmyelin debris (box) in vacuoles
but lesions are consistent with ionophore toxicity. referred to as "digestion chambers" are indicative of demyelin ati on.

10.15. Peripheral nerve. Neuropathy. Focal collections of 10.17. Peripheral nerve. Neuropathy. Detail of l 0. I 6 showing
myeloid cells (extramedullary hematopoiesis) are located between myelin balls (box).
swollen and vacuolated nerve fibers.

490 I American Association of Avian Pathologists

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10.18. Sciatic nerve. Peripheral neuropathy. lonophore toxicity.
4-week-old broiler. Vacuoles containing myelin fragments ,
occasionally forming small, spherical masses ("myelin balls") and
increased cellularity are features of peripheral neuropathy. There
is minimal inflammatory response. Several flocks developed acute
lameness. High levels of lasalocid were identified in the feed.
I 0.20. Sciatic nerve. Peripheral neuropathy. lonophore
toxicity. 4-week-old broiler. Increased Schwann cells, often
with a vesicular nucleus, along with evidence of demyelination
characterize the nerve from another affected chicken in these flocks.

I
l 0.19. Sciatic nerve. Peripheral neuropathy. lonophore 10.21. Peripheral nerve. Riboflavin deficiency. Increased
toxicity. 4-week-old broiler. Higher power view of an affected cell ularity is due to proliferation of Schwann cells.
nerve showing changes described above.

Avian Histopathology (4 th Edition) I 491

 Dm1id E. Swayne • H. Jol,11 Bames • Tal,see11 Abdul-Aziz • Oscar J. Fletcl,er
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10.22. Peripheral nerve. Riboflavin deficiency. Detail of I 0.21
showing Schwann cell proliferation and multifocal demyelination.
10.23. Olfactory lobes. Avian vacuolar myelinopathy. Duck.
Bilateral pale areas (arrows) indicate regions of demyelination.
492 I American Association of Avi an Pathologists
10.24. Cerebellum, optic lobes, medulla. Avian vacuolar
myelinopathy. Duck. Bilaterally symmetrical foci of mye lin
loss cause paleness (arrows) in the optic lobes (Cp). Vacuolar
demyelination also diffusely involves the medulla (M). Cerebellum
is unaffected (C).
10.25. Olfactory lobe. Avian vacuolar myelinopathy. Duck.
Numerous vacuoles are characteristic of demyelination in this
olfactory lobe of the cerebrum (A). Higher-power view (B) shows
the variable sized clear vacuoles and absence of any response.
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10.26. Medulla. Avian vacuolar myelinopathy. Duck. Vacuoles 10.28. Thoracolumbar spinal cord. Spondylolisthesis. 55-day-
are prominent in the white matter of the medulla (A). Higher-power old broiler. Ventral deviation of the cranial free thoracic vertebra
view (B) shows vacuoles in a myelinated tract and absence of both articulation thrusts the caudal vertebral articulation dorsally, which
neuronal changes and reactive responses. compresses the spinal cord causing paresis and paralysis.

10.27. Thoracolumbar spinal cord. Chondrodystrophy. 4-week-
old male turkey. Marked deformity and fusion of the free thoracic
vertebra (T6) with the notarium and synsacrum. A1ycoplasma iowae
is often associated with this lesion in turkeys. Lameness results
from stenosis of the vertebral canal and compression of the spinal
cord .
10.29. Thoracolumbar spinal cord. Spondylitis. 55-day-old
broiler. Lame bird from same flock as above. There is necrosis
and inflammation of the free thoracic vertebra and adjacent vertebra
in the notarium. Compression of the overlying spinal cord leads
to lameness and paralysis. Bacteria causing spondylitis include
Staphylococcus, Enterococcus, and Escherichia.

Avian Histopathology (4 th Edition) I 493

 D"vid E. Sw"yne • H. John B"mes • T"hseen Abdul-Aziz • Osc"r J. Fletcher
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10.30. Brain. Lipofuscin. Emu . Neurons contain granular gray- 10.32. Cerebellum. Lysosomal storage disease. Hawaiian goose.
black pigment consistent with lipofuscin . Small vacuo les of variable size are scattered in the cerebellum .

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stain. Detail of 10.32 shows vacuoles in white matter of cerebellum and
small pale-staining, coa lescing vacuoles expanding neurons in the
cerebellar nucleus.

494 I American Association of Avian Pathologists

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10.34. Cerebellum. Lysosomal storage disease. Hawaiian goose.
Detail of 10.33 shows distension of neurons due to accumulation of
complex lipids in the cytoplasm.
10.36. Mid brain. Sanfilippo Syndrome (Mucopolysaccharidosis
IHB). 8-month-old emu. Neurons are swo llen with pale, finel y,
vesiculated cytoplasm and aggregat ion ofN issl substance around th e
nucleus. Changes in these neurons are typica l of a lysosomal storage
disease. In this di sease, heparan is the product that accumulates in
the lysoso mes. Disease was confirmed by genotyping.

I
10.35. Medulla. Lysosomal storage disease. Hawaiian goose. 10.37. Midbrain. Sanfilippo syndrome (mucopolysaccharidosis
Neurons (boxes) in medulla have accumulated lipid in the cytoplasm IIIB). 8-month-old emu. Cytoplasmic staining with PAS is weakly
that is ca using cell enlargement and distention. positive. (I111age courtesy of L. Borst)

Avian Histopathology (4 th Edition) I 495

 Da11id E. Swayne • H. John Bames • Tahseen Abdul-Aziz • Oscar J. Fletcher
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10.38. Midbrain. Sanfilippo syndrome (mucopolysaccharidosis 10.40. Brain. Hydrocephalus and cerebellar hypoplasia. One-
TUB). 8-month-old emu. Cytoplasmic staining with a myelin day-old chicken. Subgross view shows the expanded ventricul ar
stain, Luxol-fast blue, is also weakly positive. (Image courtesy of space (hydrocephalus) in an optic lobe and small , deformed
L. Borst) . cerebellum (hypoplasia).

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10.39. Brain. Normal and cerebellar hypoplasia. One-day-old 10.41. Brain. Hydrocephalus. One-day-old chicken. Detail of
chickens. Cerebellum is small (hypoplasia, top) and malformed. I 0.40 showing the expanded ventricular space in the optic lobe.
Compare with normal cerebellum (bottom). Cerebellar hypoplasia
has been associated with parvovirus infection.

496 I American Association of Avian Pathologists


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10.42. Brain. Cerebellar hypoplasia. One-day-old chicken.
Size and shape of cerebellar folia are variable.
10.43. Brain. Cerebellar hypoplasia. One-day-old chicken.
Purkinje cells are mixed within a hypoplastic granular cell layer.
Isolated Purkinje cells are in the white matter of the cerebellar arbor
vitae.
Nervous System
10.44. Brain. Cerebellar hypoplasia. One-day-old chicken.
Detail of 10.43 showing disorganization of Purkinje cells and
hypoplasia of the granular cell layer.
I
10.45. Cerebellum. Marek's disease. 18-week-old chicken. At
this low power, cellularity is increased in the cerebellar nucleus
(box) and smaller perivascular lymphocytic cuffs (arrows) are
prominent.
Avian Histopathology (4'h Edition) I 497
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10.46. Cerebellum. Marek's disease. 18-week-old Chicken. 10.48. Cerebrum. Marek's disease. 18-week-old chicken. Detail
Detail of boxed region in 10.45 shows heterogenous lymphocytic of region within box in I 0.47 shows heterogenous lymphocytes
cells around blood vessels with nearly obliterated lumens. forming several layers around a blood vessel.

10.47. Cerebrum. Marek's disease. 18-week-old chicken. 10.49. Medulla. Marek's disease. 2-month-old chicken.
Blood vessels have perivascular cuffs with heterogenous Perivascular cuffing by heterogenous lymphocytes is prominent.
lymphocytes. Angiocentric localization of lymphocytes with little Note the lack of neuronal involvement.
to no involvement of the intervening neuropil is characteristic of
Marek's disease.

498 I American Association of Avian Pathologists

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10.50. Cerebrum. Marek's disease. 6-month-old backyard 10.52. Cerebrum. Marek's disease. Adult backyard chicken.
chicken. Higher-power view showing marked infiltration of Detail of I 0.51 showing extensive, multiple layers of lymphocytes
lymphocytes around a blood vessel. Neurons are not affected. expanding from a perivascular location into the neuropil.

I
10.51. Cerebrum. Marek's disease. Adult backyard chicken. 10.53. Cerebrum. Marek's disease. Adult backyard chicken.
Nearly the entire cerebrum is replaced by neoplastic lymphocytes. Detail of I 0.52 shows a large perivascular collection of lymphocytes
This is a rare case ofa Marek's disease lymphoid tumor in the brain. infiltrating the neuropil.

Avian Histopathology (4 th Edition) I 499

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chicken. Marked lymphocytic meningoencephalitis occurred in
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10.56. Sciatic nerve. Normal. Chicken . Normal sciatic nerve;
compare with nerves that have Marek 's disease lesions in figures
this pullet with Marek's disease. Lesions were present in other 10.57- 10.63.
organs but not in the sciatic nerves.

I
10.55. Cerebellum. Marek's disease. 4-monthold female 10.57. Sciatic nerve. Marek's disease. 7-month-old backyard
WLH chicken. Same bird as I 0.54. Cells are CD3-positive chicken. Disruption of the nerve tissu e by lymphocytic infiltrates.
T-lymphocytes. T-lymphocytes are transformed in Marek 's disease.

500 I American Association of Avian Pathologi sts

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10.58. Sciatic nerve. Marek's disease. One-year-old backyard 10.60. Sciatic nerve. Marek's disease. Chicken. Diffuse
chicken. Disruption of the nerve tissue by lymphocytic infiltrates. infiltration by neoplastic lymphocytes is typical of Type A Marek's
disease nerve lesions.

I
10.59. Sciatic nerve. Marek's disease. 6-month-old backyard 10.61. Sciatic nerve. Marek's disease. Chicken. Type B Marek 's
chicken. Detail of J 0.58 showing diffuse and marked infiltration disease nerve lesions have fewer infiltrating lymphocytes than Type
and disruption of sciatic nerve with heterogenous lymphocytes. A lesions. (Image provided by Isabel Gimeno).

Avian Histopathology (4 th Edition) I 501

 David E. Swayne • H. John Rames • Tahseen Abdul-Aziz • Oscar J. Fletcher
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10.62. Sciatic nerve. Marek's disease. Chicken. Type B lesions 10.64. Neuroganglia. Marek's disease. One-year-old backyard
include cell necrosis and edema with demyelination. (Image rooster. Ganglia around the adrenal gland are markedly infiltrated
provided by Isabel Gimeno). with lymphocytes.

I
10.63. Sciatic nerve. Marek's disease. 10-week-old 10.65. Neuroganglia. Marek's disease. One-year-old backya rd
backyard chicken. Type B nerve lesion is characterized by mild rooster. Ganglia around the pancreas are markedly infiltrated with
lymphoplasmacytic infiltration, edema, and demyelination. lymphocytes.

502 I American Association of Avian Pathologists

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10.66. Neuroganglion. Marek's disease. One-year-old backyard 10.68. Sciatic nerve. Peripheral neuropathy. Table-egg layer.
rooster. Neuroganglion between the inner and outer muscular Lymphocytic neuritis with demyelination resembles mild nerve
layers of the proventriculus (myenteric ganglion) is infiltrated with lesions ofMarek's disease.
lymphocytes.

10.67. Visceral nerve. Marek's disease. One-year-old 10.69. Sciatic nerve. Peripheral neuropathy. Table-egg layer.
rooster. Nerve in the intestinal serosa is markedly infiltrated with Detail of 10.68 shows demyelination (box) with a few ly1i1phocytes
lymphocytes. Lymphocytic infiltrates also involve the serosa. infiltrating the nerve.

Avian Histopathology (4 th Edition) I 503

 David E. Swayne • H. John Bames • Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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10.70. Sciatic nerve. Peripheral neuropathy. Table-egg layer.
Detail of a peripheral neuropathy lesion showing plasma cells (box)
in the nerve.
10.72. Cerebrum. Aviadenovirus infection. Parrotlet. Walls
of small to medium arteries are thickened because of large, finel y
granular eosinophilic inclusion bodies in the nuclei of endothelial
cells. Fibrinoid degeneration and swelling of smooth muscle nuclei
in the muscular tunic are present. (Glass slide courtesy of H. L.
Shivaprasad).

I
10. 71. Cerebrum. Aviadenovirus infection. Parrotlet. 10.73. Cerebrum. Aviadenovirus infection. Parrotlet.
Multifocal necrosis and prominent blood vessels are seen. (Glass Longitudinal section of a blood vessel showing large inclusion
slide courtesy ofH. L. Shivaprasad). bodies that narrow the lumen and obstruct blood flow. (Glass slide
courtesy of H. L. Shivaprasad).

504 J American Association of Avian Pathologists

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10.74. Cerebrum. Aviadenovirus infection. Parrotlet. Positive 10. 76. Cerebellum. Avian encephalomyelitis. 2.5-week-old
immunostaining of inclusions in endothelial cells is seen using broiler. Peri vascular cuffing is prominent and degenerating neurons
an antibody to aviadenov.irus. (Glass slide courtesy of H L. with central chromatolysis are characteristic of AE.
Shivaprasad. !1111111111ostaining by J. S. Guy).

10. 75. Cerebellum. Avian encephalomyelitis. 2.5-week-old 10.77. Cerebellum. Avian encephalomyelitis. 2.5-week-old
broiler. Lymphocytic cell accumulation is prominent in the broiler. Detail of 10.76 shows central chromatolysis and gliosis.
cerebellar nucleus.

Avian Histopathology (4 th Edition) I 505

 David E. Swayne • H. Jol,11 Bames • Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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10.78. Spinal cord. Avian encephalomyelitis. 2.5-week-old 10.80. Spinal cord. Avian encephalomyelitis. 2.5-week-old
broiler. Increased cellularity is bilateral and confined to the gray broiler. Detail of I 0.79 showing central chromatolysis and gliosi s.
matter of the spinal cord.

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broiler. Gliosis and degenerating neurons are characteristic of AE. broiler. Detail of 10.80 showing central clu-omatolysis.
Central chromatolysis of neurons is a diagnostic feature.

506 I American Association of Avian Pathologists

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10.82. Dorsal root ganglion. Avian encephalomyelitis. 10.84. Brain. Eastern equine encephalomyelitis. Macaw.
2.5-week-old broiler. Multiple variably sized lymphocytic foci are Multiple blood vessels have vasculitis and prominent cuffing by
in a dorsal root ganglion. lymphohistiocytic cells.

10.83. Dorsal root ganglion. Avian encephalomyelitis. 2.5-week- 10.85. Brain. Eastern equine encephalomyelitis. Macaw. Detail
old chicken. Detail of 10.82 shows a large focus of lymphocytes of I 0.84 showing lymphohistiocytic encephalitis.
within a dorsal root ganglion.

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 David E. Swayne • H. Jol,11 Bames • Tal,see11 Abdul-Aziz • Oscar J. Fletcl,er
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10.86. Brain. Eastern equine encephalomyelitis. Macaw. 10.88. Ganglion, Pericardium. Eastern equine
Some neurons contain vacuoles and are degenerating; there is no encepha lomyelitis. Macaw. Neurons are swollen and degenerating
sate IIitosis. and there is increased cellularity in the ganglion .

I
10.87. Brain. Eastern equine encephalomyelitis. Macaw. 10.89. Ganglion, Pericardium. Eastern equine
Eastern equine encephalomyelitis viral antigen in neurons is encephalomyelitis. Macaw. Detail of 10.88 shows degenerating
demonstrated by immunohistochemistty. neurons and scattered lymphoid cell infiltration. Eastern equine
encepha litis viral antigen was demonstrated in these neurons by
immunohistochemistry.

508 I American Association of Avian Pathologists

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10.90. Cerebrum. West Nile virus infection. Adult male red- 10.92. Visceral nerve. Proventriculus. Avian bornavirus
shouldered hawk. Considering the severity of clinical disease infection. African gray parrot. Visceral nerve in the serosa of the
and mo1tality, lesions are .relatively mild. There is lymphocytic proventriculus has increased cellularity (box) due to infiltration by
vasculitis and perivascular cuffing affecting this vessel. Vacuoles lymphocytes.
around vessels and cells have been caused by decomposition.

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10.91. Cerebrum. West Nile virus (WNV) infection. Adnlt 10.93. Visceral nerve. Proventriculus. Avian bornavirus
male red-shouldered hawk. Affinity of WNV virus for neurons infection. African gray parrot. Detail of lesion m I 0.92 shows
is apparent when tissue sections are immunostained with anti-WNV lymphocytes infiltrating a visceral nerve.
antibody. Punctate positive staining is diffuse in the neuropil, but
cells other than neurons show little to no staining.

Avian Histopathology (4th Edition) I 509

 David E. Swayne • H. John Bames • Tahsee11 Abdul-Aziz • Oscar J. Fletcher

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10.94. Brain. Lymphocytic encephalitis. Avian bornavirus 10.96. Meninges. Cerebellum. Sal111011ella ariw 11ae infection.
infection. African gray parrot. There is perivascular cuffing by 2-week-old turkey. Heterophilic infiltration has ex panded th e
lymphohistiocytic cells. meninges.

10.95. Spinal cord. Avian bornavirus infection. Cockatoo. In
addition to lymphocytic inflammation of the plexuses of peripheral
nerve, lesions occur in the gray matter of the CNS of some birds. A
diffuse poliomyelitis can be seen in this bird.
10.97. Meninges. Cerebellum. Sal111011ella ariwnae infectio n.
2-week-old turkey. Heterophils and lymphohistiocytic cells are
major components of the inflanunation in the meninges. In contra st
to ORT meningitis ( 10.106), inflammatory cells extend into the
underl y ing brain ti ssue.

510 I America n Association of Avian Pathologists

 Nervous System
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10.98. Cerebellum. Colibacillosis. 7-week-old turkey. Meninges 10.100. CerebelJum. Colibacillosis. 7-week-old turkey. Detail
are increased in thickness because of extensive fibrinoheterophilic of 10.99 shows necrosis with fibrinoheterophilic exudate and
meningitis. Necrosis is extensive in the molecular layer. numerous intralesional bacteria.

10.99. Cerebellum. Colibacillosis. 7-week-old turkey. Detail 10.101. Cerebrum. Colibacillosis. 7-week-old turkey. Severe
of 10.98 shows necrosis in the meninges and molecular layer of the fibrinoheterophilic meningitis expands the meninges.
cerebellum. Bacterial colonies are visible.

Avian Histopathology (4'" Edition) I 511

 DaJ1id E. Swayne • H. Jol,11 Bames • Tal,seen Abdul-Aziz • Oscar J. Fletcl,er
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10.102. Cerebrum. Colibacillosis. 7-week-old turkey. 10.104. Cerebrum. Pse11do111om1s aer11gi11osa. 5-day-old
Lymphohistiocytic perivascular cuffing in the cerebral cortex. broiler breeder. Detail of 10.103 shows numerous intralesional
bacteria within the necrotic area.

I
10.103. Cerebrum. Pse11do111011as aer11gi11osa. 5-day-old 10.105. Cerebrum. Pse11do111011as aeruginosa. 5-day-old
broiler breeder. Large area of necrosis (malacia) with a well- broiler breeder. Giemsa stain shows numerous intralesional
defined margin is located in the cerebrum. bacterial colonies and individual bacteria (arrow).

512 I American Association of Avian Pathologists


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10.106. Meninges. Cerebrum. Omithobacteri11111
rhinotracheale (ORT). 5-week-old broiler. Heterophils and
edema expand the meninges. Lesion is not ORT-specific, but does
indicate a bacterial infection. Isolation and identification of the
specific agent is required for a specific diagnosis .
10.107. Medulla. Infectious encephalomalacia. Enterococcus
llirae. Chicken. Large circumscribed focus ofmalacia nearly spans
the medulla. Lesion is an infarct that resulted from tlu-ombosis
caused by E. hirae. There are early vascular changes and thrombi in
vessels but only minimal inflammation.
Nervous System
10.108. Medulla. Infectious encephalomalacia. Enterococcus
hirae. Chicken. Fibrin thrombi occlude and expand a vessel. No
bacteria are evident. Early vascular changes are evident. Changes
in the neuropil most likely resulted from decomposition.
10.109. Medulla. Infectious encephalomalacia. Enterococcus
llirae. Chicken. There are no blood cells in this vessel, but there
is an accumulation of mononuclear cells. Endothelial cells are
swollen.
Avian Histopathology (4 th Edition) I 513
 Dm,id E. Swayne • H. John Barnes • Tahseen Abdul-Aziz • Oscar J. Fletcher

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10.110.Medulla. Infectious encephalomalacia. Enterococcus 10.112.Brain. Enceplwlitozaon hellem infection. Yellow-headed
hime. Chicken. Fibrin thrombus stained with Gram 's stain reveals Amazon Parrot. Focal nodular encephalitis is shown.
several Gram-positive cocci. E. hime was isolated from the chicks.

10.111. Brain. Mycobacterial infection. 5-year-old golden
manakin. Pale staining histiocytic cells comprise the blood vessel
cuff (A). An acid-fast stain (B) is positive. Granulomatous lesions
containing acid-fast bacteria were found in other tissues from this
bird.
10.113.Brain. Enceplwlitozoon hellem infection. Yellow-headed
Amazon parrot. Detail of 10.112 showing a nodule composed of
histiocytic cells. Histiocytic nodules were found in other organs,
including kidney, in this bird. Organism can be demonstrated with
a Gram stain.

514 I American Association of Avian Pathologists

 Nervous System
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10.114. Cerebellum. Aspergillosis. 4-week-old turkey. 10.116.Cerebellum. Aspergillosis. 4-week-old turkey. Septate,
Meningitis is extensive and inflammation with necrosis extends into dichotomous branching hyphae are typical of A5pe1gil/11s sp. In
the molecular, Purkinje cell, and granular cell layers. contrast with other fungi , Aspe1gi//11s often stains with H&E.

I
10.115.Cerebellum. Aspergillosis. 4-week-old turkey. Detail of 10.117.Cerebellum. Ochroconosis. 2-week-old turkey. Extensive
I 0.114 showing extensive malacia and inflammation. meningoencephalitis, malacia, and hemorrhage are caused by
Ochroconis ga/lopava .

Avian Histopathology (4 th Edition) I 515

 David E. Swayne • H. John Ba m es • Taltseen Abdul-A ziz • Oscar J. Fletch er
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10.118.Cerebellum. Ochroconosis. 2-week-old turkey. 10.120. Brain. Avian malaria. Robin. Focalareasofhemorrhage
Lymphohistiocytic perivascul ar cuffing and numerous are adjacent to vessels that have meronts of Plasmodium relic/11111 in
multinucleated giant cell s are characteristic features. endothe lial cells.

I
10.119.Cerebellum. Ochroconosis. 2-week-old turkey. Fungi
are difficult to identify in H&E stained sections, but are numerous
when Gomori's methenamine sil ver stai n is used.
10.121. Brain. Avian malaria. Robin. Meronts in endothe li al
cells of some vessels are not associated w ith hemorrhage. Meronts
are consistent w ith Plasmodiw11. P re/icll1111 was identified in blood
smears.

516 I Ameri can Association of Avian Patholog ists


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10.122. Brain. Toxoplasmosis. Adult backyard chicken.
Necrotic blood vessel contains tlu·ombocytes and e1ytlu·ocytes.
Tachyzoites oftoxoplasma (arrows) are scattered within the necrotic
neuropil.
10.123. Brain. Toxoplasmosis. Adult backyard chicken.
Cyst containing bradyzoites (box) and numerous free tachyzoites
(arrows) are within the necrotic region of the brain.
Nervous System
10.124. Brain. Toxoplasmosis. Adult backyard chicken.
Immunoperoxidase stain specific for Toxop/asllla antigen reveals
numerous organisms.
I
10.125. Brain. Neurosarcocystosis, Sarcocystis calchasi.
Dove. Meronts develop in endothelial cells and often have a radial
appearance because merozoites bud off of a mother cell by a process
called endopolygeny. (Image courtesy of H. L. Shivaprasad).
Avian Histopathology (4 th Edition) I 517
 Dm•hl E. Swayne • H. John Bames • Tahseen Abdul-Aziz • Oscar J. Fletcher

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10.126. Cerebrum. Verminous encephalitis, Clumdlerella 10.128. Brain. Glioma. Adult backyard chicken. Deta il of
quiscali. Emu. Normally a filarioid parasite in the latera l ventricl es 10.127.
of indi ge nou s passerine birds, the orga nism causes lesio ns in the
brain and spi nal cord when unnatural hosts, such as emus, are
infec ted. (Image courtesy of J. lv1. Law).

I
10.127. Brain. Glioma. Adult backyard chicken. Large ma ss
with irregular margi ns is located in the cerebellar nucleus. Certain
strains of avian leukosis virus called avian glio ma viruses cause
epizootic g li osis.
10.129. Cervical mass. Ganglioneuroma. Adult male African
gray parrot. Heterogenous islands of neoplastic cells are separated
by fib rovascular trabeculae.

5 18 I American Association of Av ian Pathologists

 Nervous System
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10.130. Cervical mass. Ganglioneuroma. Adult male African 10.132. Skin. Schwannoma. Adult cockatiel. Nodular,
gray parrot. Detail of I 0.129. Islands contain a loose fibrillar cutaneous, well-demarcated mass is composed of a uniform
stroma and large polygonal ganglion cells consistent with nervous population of differentiated spindle cells arranged in parallel arrays
tissue. characteristic of a Schwannoma.

10.131. Cervical mass. Ganglioneuroma. Adult male

African gray parrot. Immunostaining with NSE (neuron-specific
enolase) identifies the large polygonal cells as ganglion cells.
Ganglioneuromas are characterized by the presence of differentiated
ganglion cells.

Avian Histopathology (4 th Edition) I 519

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CHAPTER
Eye and Ear
H. L. Shivaprasad
Eye
Introduction, Anatomy, and Histology
Bird's eyes are the finest ocular organs in the animal kingdom
being capable of constellation recognition for stellar orientation
and navigation. They have high resolving power for perception of
movements and are endowed with excellent visual acuity. Bird 's
eyes display the basic pattern of organization found in vertebrates
but have incorporated many adaptations for improved and en-
hanced visual ability. Bird's eyes are capable of color discrimi-
nation and pattern recognition, and they provide vision in bright
and dim light, under-water accommodation, sun orientation, and
ultraviolet light perception. Some birds can, through their vision,
discriminate whether a fruit is ripe or not, distinguish male or a
female , and find their prey by locating the prey's territory when
marked by urine. The avian eye, especially of chicks, has been
extensively used in basic vision research, including studies on ac-
commodation, myopia, glaucoma (light induced), certain genetic
diseases, teratology, toxicities, wound healing, and developmen-
tal pathology.
Only salient features of avian eye anatomy will be given here;
readers are advised to see references at the end of the chapter. Com-
pared to the mammalian eye, the avian eye is large and in a few
birds the combined weight of the eyes is greater than the weight of
the brain. Avian eyes are located in a large orbit that is laterally di-
rected. The lacrimal bone, interorbital septum, orbitosphenoid, and
parsorbitalis of the orbital bone form its bony limits. There is a gap
in the orbital ring, which is bridged by the !iga111entu111 mandibu!are
!ong11111. Eyes can be flat, globose, or tubular.
Fibrous tunic
The fibrous tunic forms the outermost layer of the eye. It con-
sists of the sclera, scleral ossicles, and cornea. Ca1iilage is present
in the sclera. Sciera! ossicles are a group of 10 to 18 bones that
form a complete ring of overlapping plates near the junction with
the cornea. The cornea is a refractive component made of densely
packed collagen fibrils embedded in a ground substance. The an-
terior surface of the cornea is covered by few-cell-thick stratified
squamous epithelium that rests on a prominent basement membrane
(Bowman's membrane). Posteriorly, a layer of low cuboidal epithe-
lium called the corneal endothelium covers the inner surface of the
cornea. A thick basal lamina (Descemet's membrane) separates the
endothelium from the corneal stroma.
11
Vascular tunic (uvea)
The vascular tunic or uvea forms the middle layer of the eye and
consists of the choroid, iris, and ciliary body. The iris contains stri-
ated muscle. The color of the iris is due to fat and the pigment that
it contains. The ciliary body also contains striated muscle and car-
ries numerous folds, the cilia1y processes. The pectinate ligament,
an extensive trabecular elastic fiber network is better developed in
avian species than in mammals. The choroid is the black-pigmented
layer and it lines the greater pari of the eyeball. It has several layers
and carries large blood vessels and a dense capillary network.
Nervous tunic
The retina is similar to other vertebrates in organization and strati-
fication but, compared to mammals, it is thicker in birds and lacks
blood vessels. It has ten distinct layers . The pecten is a unique
vascular strncture in birds that projects from the retina into the vit-
reous at the point of exit of the optic nerves. Most avian species
have a pleated type ofpecten that is composed almost exclusively of
capillaries and extra-vascular pigmented stromal cells. The primary
function of the pecten appears to be nutritional; it provides nutrients
to the avascular retina through the vitreous body. The lens is trans-
parent, biconvex, and has an annular pad. A fluid-filled cleft lies
between the annular pad and the body of the lens. The vitreous body
composed of a gelatinous transparent material fills the space behind
the lens and the ciliaiy body. Optic nerves are well developed and
enter the eyes at the ventroposterior aspect of the globe.
Extra-ocular anatomy
Birds have upper and lower eyelids that can be feathered in most
species but are non-feathered in parrots, pigeons, ostriches, rheas,
and Passeriformes. The lower eyelid has an oval, flat mass of con-
nective tissue in the dermis called the tarsal plate. Birds have a
third eyelid (nictitating membrane), a conjunctiva[ fold that origi-
nates from the medial canthus of the eye. Conjunctiva I associated
lymphoid tissue (CALT) is present most prominently between the
fissures and longitudinal folds of the lower eyelid. Harderian gland
or gland of the nictitating membrane is irregular and situated in the
medial side. In the interstitium of the Harderian gland are large
numbers of plasma cells that produce antibody. The lacrimal gland
is located in the ventrotemporal part of the orbit (in the external can-
thus) and is covered by conjunctiva. A nasal or salt gland is present
in the orbit dorsomedially to the eyeball. It is well developed in
marine birds and excretes hypertonic salt solution. Six oculomo-
Avian Histopathology {4°' Edition) I 521
 H. L. Shivaprasad
tor muscles are in the exterior of the eyeball. After fixation in 10%
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formalin solution, the eyes of birds have to be decalcified with a
decalcifying solution (due to the presence of the scleral ossicles)
before processing. Eyes then should be hardened for 24 hours each
in a graded series of alcohols (50-100%) before trimming and final
processing.
Diseases
Birds' eyes are subject to various diseases, both infectious and
noninfectious. These include anomalies, infectious diseases, nutri-
tional, toxic, neoplastic, and miscellaneous diseases or conditions of
unknown cause.
Developme11ta/ and ftereditmy
Various anomalies have been described in birds, especially poul-
try. These include 'monsters' such as cyclopia or trip le eyes, buph-
thalmia, microphthalmia, optic nerve hypopl asia, cataracts, corneal
edema, and corneal ectasia. Genetics and incubation factors such as
suboptimal temperature, humidity, or failure of turning mechanisms
in the incubator can contribute to these conditions. Various known
genetic diseases, primarily in chickens, include microphthalmia, ret-
inal dysplasia in various breeds of chickens, delayed amelanosis in
the Smyth chicken, partial retinal dysplasia and degeneration, blind-
ness and enlarged globe, retinopathy, multiple malformations of the
eye in the creeper chicken, hereditary blindness (Eli) in the White
Leghorn chicken (WLH), keratoconus ("Pop-Eye") in WLH, hyper-
plastic lens epithelium, coloboma of the iris, blindness due to cata-
racts evident at hatching in chickens, cataracts evident at various
ages in different breeds of chickens, and multiple ocular anomalies
in pigmented WLH chickens. Most of these conditions are prob-
ably inherited as autosomal recessives, and in the pigmented WLH
the condition is influenced by sex-linked genes. Similarly, there are
conditions such as ring retina, scleral ectasia, glaucoma, and cata-
racts in mutant Japanese quail, secondary angle-closure glaucoma
in Slate turkeys, and changes in the ganglionic cells of the retina
associated with mucopolysaccharidosis type III B in emus. Retinal
dysplasia also has been described in falcons and Tippler pigeons.
The earliest light microscopic changes seen in retinal dys-
plasia in chickens is degeneration of photoreceptors that progress
to retinal detachment, hypertrophy of retinal pigmented epithelial
I (RPE) cells, folding ofRPE, disorganization and degeneration of the
retina, and rosette formation. In chronic cases, fibrosis with replace-
ment of connective tissue in the vitreous that can undergo cartilage
and osseous metaplasia occur.
Nutritio11a/ diseases
Ocular diseases caused by nutritional deficiencies such as vitamin
A, vitamin E, pantothenic acid, biotin, zinc, and tyrosine have been
described. Microscopic changes due to vitamin A deficiency in-
clude atrophy, degeneration, and proliferation of the epithelium of
the conjunctiva and cornea and changes in the rod and cone pho-
toreceptors. Other changes such as squamous metaplasia of the
nasolacrimal duct with keratin formation can also occur. Second-
ary bacterial infections can result in severe fibrinoheterophilic con-
junctivitis and, occasionally, keratitis. Blepharoconjunctivitis due
522 I American Association of Avian Pathologists
to deficiency of pantothenic acid and biotin have been described in
chickens. Lesions due to vitamin E deficiency have been primaril y
experimental in nature. Lesions such as keratoconus, cataract, and
marked degeneration of the lens that progressed to severe liquefac-
tion have been described . Other changes include hyperplasia oflens
epithelium, mineralization of corneal stroma, and retinal folding.
Toxicities
Ocular conditions due to toxicities in birds are rare except for those
caused by ammonia toxicity in poultry. The prima1y lesion due to
ammonia toxicity in chickens is keratoconjunctivitis. Lesions are
characterized by necrosis of the epithelium, ulceration and infiltra-
tion of heterophils into the epithelium, corneal edema, and inflam-
mation of the corneal substantial propria . Often there is a band of
precipitated calcium in the center of the cornea where the epithelium
is missing. There can be secondary involvement of the anterior uvea
characterized by infiltration of the iris and ciliary body with hetero -
phils and lymphocytes, especially in chronic cases. Lesions can be
complicated with secondary bacterial infections.
Photosensitization due to certain plants such as spring parsley
(A111111i 111aj11s, A. visnaga) results in lesions that are primarily kerato -
conjunctivitis characterized by edema of the eyelids and nictitating
membrane, erythema, corneal opacification, and ankyloblepharon in
chronic stages. Ammeline, which is an S-triazine compound, causes
blindness in baby chicks characterized by edema, degeneration, de-
struction of photoreceptor cells, and retinal detachment. Fonno-
guanamine causes similar lesions to those of ammeline in chicks.
Mi scellaneous toxicities include glycine, which causes enlargement
of the eyeballs due to increased si ze of the vitreous, sodium toxicit y
which causes conjunctivitis and lens opacity in clucks, congestion
of the nictitating membrane, and dilation of the pupil from nicotine
disulfide toxicity in chickens, rapid eye blinking from dichlorodi -
phenyltrichloroethane (DDT poisoning), cataracts in chicks from
dinitrophenol, and keratitis in pheasants from phenothiazine toxici -
ties. Severe keratoconjunctivitis in chickens can be caused by sulfi.tr
toxicity. Colchicine can cause necrosis of ganglion cells and exces-
sive ocular growth when given to chicks.
Infections
Infectious diseases are probably the most common diseases affect-
ing the eyes of birds. This is because the intraocular route is an
important mode of transmission for these diseases. Poultry raised in
confinement provides close contact that facilitates transfer of agents
via the intraocular route.
Viral infections
Conjunctivitis is a common feature in many diseases caused by
viruses including herpesviruses (infectious la1yngotracheitis [ILT)
virus in chickens, duck viral enteritis virus, psittacine and finch
herpesviruses), Newcastle disease virus, avian influenza virus, in-
fectious bronchitis virus, metapneumovirus, poxvirus, and aviad-
enovirus. Conjunctivitis associated with circoviruses occurs in psit-
tacines and pigeons.
Conjunctivitis in chickens caused by !LT can range from mild
lymphocytic or lymphoplasmacytic inflammation with syncytia

fo rmation that may contain intranuclear inclusions to necrosis of
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the epithelium and hemorrhage. The latter lesions resemble those
caused by exotic Newcastle disease virus and highly pathogenic
av ian influenza virus. In chickens, infectious bronchitis virus pri-
marily causes lymphoplasmacytic inflammation of the conjunctiva.
Frequently, lymphoplasmacytic iridocyclitis can be seen in addition
to viral conjunctivitis.
Lesions in the conjunctiva due to poxvirus infection are char-
acterized by hypertrophy and proliferation of conjunctiva! epithelial
cells, many of which contain eosinophilic intracytoplasmic inclu-
sions. Occasionally, pox lesions extend onto the cornea. It should
be pointed out that many of the viral diseases are commonly com-
plicated by secondaty bacterial infections resulting in heterophilic
conjunctivitis, keratitis, iritis, cyclitis, and ophthalmitis.
Marek's disease is a common and complex disease primar-
ily of chickens caused by a herpesvirus. Ocular lesions associated
with Marek's disease have been well studied in chickens. Lesions
range from irregular pupils due to inflammation of the iris to a grey
iris resulting from infiltration of neoplastic lymphocytes. In ad-
vanced stages, lymphoma can involve other parts of the eye includ-
ing the sclera. Other changes such as corneal edema, inflammation
with occasional eosinophilic intranuclear inclusions in mononu-
clear cells of the cornea and retinal ganglia cells, and cataractous
changes have been described in Marek's disease caused by very
virulent virus strains.
Among exotic birds (e.g., Gouldian finches) , herpesvirus
causes proliferative conjunctivitis with hypertrophied, karyome-
galic epithelial cells that contain basophilic intranuclear inclusion
bodies. Polyomavirus in psittacines can cause lymphoplasmacytic
conjunctivitis and iridocyclitis with characteristic faint staining,
amphophilic intranuclear inclusions in the mononuclear inflamma-
tory cells.
Bacterial infections
Ocular lesions caused by bacteria are common in birds either as
primary infections or as a manifestation of septicemia. Secondary
complications of primary viral infections are common. Bacterial
diseases include colibacillosis, salmonellosis, especially Salmonella
arizonae in turkey poults, fowl cholera caused by Pasteurella 111ul-
tocida, mycoplasmosis especially M gal/isepticu111, bordetello-
sis caused by B. aviu111, infectious coryza caused by Avibacteri11111
(Haemophilus) paragalli11ar11111 , and ornithosis caused by Chla-
mydia psittaci. Other bacterial diseases include those caused by
Riemerel/a anatipestifer, Mycobacteri11111 spp., Staphylococcus spp.,
Streptococcus spp. , Pse11do111011as aeruginosa, and E1J1sipelothrix
rhusiopathiae. Lesions caused by most of the above bacteria are
characterized by fibrinoheterophilic inflammation of the conjunctiva
with keratitis and ophthalmitis. Pseudomonas aeruginosa infection
frequently results in corneal perforation. Ophthalmitis associated
with a large number of gram-negative bacteria due to S. arizonae is
common in turkey poults that have no lesions in the conjunctiva or
the cornea. Lesions due to Mycoplasma gal/iseptic11111 in chickens,
turkeys, and house finches are primarily lymphoplasmacytic in na-
ture. Elementaty bodies in the cytoplasm of macrophages may be
seen when conjunctivitis is caused by C. psittaci.
Eye mu/ Ear
Fungal infections
Fungal diseases such as aspergillosi s, ochroconosis (formerly dac-
tylariosis), candidiasis, and favus due to /v!icrosporu111 gal/inae are
common in domestic poultry. Aspergillosis is primarily caused by
Aspergil/11s.f11111igat11s, but can also be caused by A. flavus. Young
turkey poults and chicks are most susceptible. Microscopic lesions in
the acute stages consist offibrinoheterophilic inflammation that may
be associated with necrosis of conjunctiva! epithelium. In chronic
stages, lesions progress to heterophilic granulomatous inflamma-
tion . lntraocular structures, especially the pecten can be severely af-
fected, but the vitreous is also often severely involved. Lesions due
to aspergillosis can range from fibrinoheterophilic to heterophilic
granulomatous inflammation involving the anterior chamber, poste-
rior chamber, vitreous, pecten, ciliary body, iris, retina, and cornea.
Numerous septate branching hyphae with parallel sides and mea-
suring 5 to 7 ~Lm are usually present within the exudate, and even
in the sclera and lens. Mycotic keratitis, mycotic blepharitis and
dermatitis have been reported in a Blue-fronted Amazon parrot and
Falcon hybrid, respectively. Lesions of ochroconosis are less fre-
quent in turkeys but are similar to those ofaspergillosis. Giant cells
tend to be numerous and contain hyphae of Ochroconis gal/opava.
The natural pale brown color of fungal hyphae can be identified in
unstained histologic sections. Candida albicans infection produces
corneal edema and infiltration of the nictitating membrane, cornea,
and iris with heterophils and lymphocytes that are associated with
the organism 's characteristic pseudomycelia and blastospores. /v!i-
crosporum gal/inae infection (favus) causes blepharitis character-
ized by acanthosis, hyperkeratosis, degeneration and necrosis of the
epidermis, and infiltration with a mixed population of inflammatory
cells in the dermis. Superficial epidermis and feather follicles may
contain fungal hyphae, which are slender, 2 to 5 µm in diameter,
septate and branching. Granulomatous iridocyclitis has occurred in
chickens experimentally infected with Histoplasma caps11latu111 and
in pigeons experimentally infected with C1J1ptococc11s 11eo.for111ans.
Pamsitic infections
Parasitic infections associated with ocular diseases in birds are lim-
ited to protozoa such as (e.g. , Toxoplasma, C!Jptosporidi11111 , Leuco-
cytozoon), a few helminths (e.g., 0Jyspirura), and a few trematodes.
I
Toxoplasmosis in chickens is characterized by severe necrosis of the
optic nerve and inflammation, sometimes associated with giant cells
and cysts of Toxoplasma gone/ii and free tachyzoites. Lymphoplas-
macytic inflammation associated with similar cysts in various parts
of the eye including the iris, ciliary body, choroid, retina, pecten,
optic nerve, and periocular structures including the connective tis-
sue and muscles are recorded. lridocyclitis and cataracts have also
been reported. Similar lesions can also be seen in canaries affected
by toxoplasmosis.
Mild to moderate heterophilic conjunctivitis associated with
cryptosporidiosis has been described in several species of birds.
Microscopic lesions range from mild infiltration of heterophils and
lymphocytes in the subconjunctiva to marked hyperplasia and hy-
pettrophy of the epithelium with inflammation involving the epi-
thelium and lamina propria. Numerous basophilic staining, small
spherical bodies measuring 3 to 5 ~Lm in diameter are seen on the
Avian Histopathology (4 th Edition) I 523
 H. L. Shi11apmsad
surface of the conjunctiva! epithelium. Megaloschizonts of Le11-
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cocylozoo11 simondi that are as large as 25 µm in diameter and may
or may not be associated with inflammation have been described
in various structures of the eye. This is a sporadic disease seen in
North American waterfowl, most commonly during the fall season .
Keratoconjunctivitis caused by the microsporidian Encephalitozoon
hel/em has been reported in an Umbrella cockatoo. Other conditions
such as blepharoconjunctivitis due to Plas111odi11111 /ophurae, cysts
of Sarcocystisfa/ca/11/a in the ocular muscle ofpsittacines, myositis
in periocular muscles associated with Hae111oprote11s /oph ortyx spe-
cies in quail have also been reported.
Among helminths, nematodes of the genus 0 ,\)'5pi/'llra can in-
fect the eyes of more than I 00 species of wi Id and domestic birds,
ca using mild to severe conjunctivitis leading to heterophilic ophthal-
mitis and blindness. Thelazia species have also been described in
the eyes of birds. Trematodes of the family Philophthalmidae have
been found in the eyes resulting in conjunctivitis of various species
of birds including chickens, peafowl, ducks, geese, and ostriches.
Miscellaneous Ocular Conditions
Catarncts
Cataracts due to various etiologic agents have been de scribed in a
variety of birds, and were associated with ocular inflammation from
viral di seases, nutritional deficiencies, heredity, old age, and cata-
racts of unknown causes. Cataracts in poultry, secondary to avian
encephalomyelitis virus, Newcastle disease virus, Marek's disease,
aspergillosis, toxoplasmosi s, and other diseases can occur. These le-
sions can range from mild degeneration of lens fibers , epithelial hy-
perplasia, formation of bladder cells, and liquefaction in advanced
stages. In some cases, inflammation, sometimes with multinucle-
ated giant cells can also be seen. Cataracts have been described in
quail associated with senility and in chickens with retinal dysplasia .
Cataracts associated with retinal changes and optic nerve hypopla-
sia was observed in commercial turkey poults at one day of age.
Some of the turkey poults under 12 weeks of age revealed smaller
optic nerves. Microscopically all lens regions were affected and
the changes were characterized by vacuolation of epithelial cells,
presence of balloon cells, nuclear retention, and liquefaction. In the
retina, there was marked depletion in the inner plexiform laye r, gan-
I
glion cells, and optic nerve fiber layers. A hereditary basis appeared
most likely. Cataracts have also been described in ostriches, wood
quail, canaries, and other birds.
Other conditions
A number of miscellaneous ocular conditions including blepharo-
conjunctivitis or keratoconjunctivitis in turkeys, cll.l'onic endophthal-
mitis in chickens, granulomatous chorioretinitis and buphthalmia of
unknown ca use have been described. Blepharoconjunctivitis is an
enzootic di sease of the eyelids of turkey breeders that is charac-
teri zed by ocular discharge, swelling and ulceration of the eyelid,
caseo us exudate in the conjunctiva, corneal necrosis, rupture, Jens
opacity, and blindness. This condition occurs primarily during the
co lder seasons. The cause of thi s condition is not known, but vita-
min A deficiency, infectious agents, and the environment have been
considered poss ible pred isposing factors.
524 I American Association of Avian Pathologists
Chronic endophthalmitis among immature broiler breeder
chickens is characteri zed by gray opacity of the papillary region,
cataract formation, retinal thickening and detachment, and shrunken
vitreous. The globes are firm and filled with granulation tissue; yel-
low gelatinous and atrophied optic nerves are found in severely af-
fected globes. Chronic inflammation is found in all portions of the
uvea, pecten, lens, vitreous, retina, and optic nerve.
Turkey blindness syndrome characterized by chorioretinitis
and buphthalmus was reproduced by exposing them to continuous
a11ificial light for 6 weeks. The most consistent lesions were cho-
roiditis with thickening of the choroid, edema, fibro sis, and inflam-
mation . Retinas were detached. Another condition, termed ophthal-
mopathy has been rep011ed in a 22-week-old broiler-breeder flock
characterized by retinal degeneration and detachment, and early cat-
aract formation . This condition was attributed to a combination of
low-intensity light and relatively short period of exposure (6 hours a
day for IO weeks in dark housing).
lntraocular ossification is a common condition in chickens
and turkeys that is probably a sequel of chronic endophthalmitis or
neoplasia. In the rd chicken, ossification is associated with reti-
nal disorganization and appears to require retinal pigment epithe-
lium. Eye notch syndrome or ulcerative blepharoconjunctivitis is a
widespread ocular lesion of egg-type laying chickens of unknown
etiology. Subretinal fluid , degeneration of the vitreous body, sepa-
ration of the retina and the junction of the RPE and photoreceptors,
adhesions between the detached tissue, pecten and lens, cystoid de-
fects in the retina and giant cell granulomas containing cholesterol
clefts in the vitreous have been associated with retinal detachment
in pheasants. Uveitis of undetermined cause has been described in
broiler-breeders. Lesions consisted of swelling of the periorbital
tissue and conjunctiva as well as corneal opacification. In addition
to uveitis, retinas of several eyes were elevated from the basement
membrane by exudates composed of fibrin, heterophils, lympho-
cytes, and a few macrophages.
Bilateral dermoid characterized by formation of skin on the
cornea has been recorded in different species of birds.
Neoplasia
Neoplasms of the eye, other than Marek's disease lymphoma in
chickens, are rare. Orbital lymphosarcoma associated with re-
ticuloendotheliosis virus has been repo1ted in a peafowl. Rare tu -
mors such as retinoblastoma have been described in a 38-day-old
White Leghorn hen with a firm reddish mass extending from the
ocular fundus towards the ciliary body and lens. Other tumors in-
clude hemangioma in a pullet, melanoma in an adult chicken, uveal
malignant melanoma in a duck, two cases of rhabdomyosarcom a,
myelogenous sarcoma in a mature chicken, and an undifferentiated
sarcoma, which involved not only the globe, but also the spleen and
liver. A neurofibrosarcoma involving the vitreous in a mature White
Leghorn chicken has also been described . lntraocular adenocarci-
noma and retrobulbar rhabdomyosarcoma in budgerigars, a mali g-
nant intraocular teratoid medulloepithelioma in a cockatiel, and a
papilloma of the eyelid associated with papillomavirus in an Afri can
Grey parrot have been described.

Ear
VetBooks.ir
Introduction, Anatomy, and Histology
Hearing, after vision, is the second most important sense in birds .
B irds use hearing for social interaction, warning and locating prey.
Songbirds have the most complex audito1y communication signals .
The hunting owl has the best acuity in acoustically locating a target
in a tlU'ee-dimensional space. Birds, like other vertebrates, have
ex ternal, middle and internal ears but do not have external sound-
collecting structures, as these would be aerodynamically disadvan-
tageous .
External ear
External ears are located ventral and caudal to the eye and are cov-
ered by auricular feathers. The external ear is a continuation of the
skin, lined by epidermis, and contains glands that secrete waxy ma-
terial (cerumen). The number of glands in the external ear of birds is
not known but up to 25 have been counted. There is lymphoid tissue
associated with the glands .. The tympanic membrane is convex in
birds and separates the external ear from the middle ear.
Middle ear
The middle ear is an air filled funnel-shaped cavity that is lined by
cuboidal epithelium connecting to the orophmynx via the Eusta-
chian tube. The middle ear contains a single rod-like ossicle called
the columella, which is similar to the stapes in mammals. It is com-
posed of bone and cartilage and forms a direct connection between
the tympanic membrane and perilymph of the inner ear.
/ 11ner ear
The inner ear is composed of bony and membranous labyrinths, the
vestibule, and the cochlea. The bony labyrinth encloses the membra-
nous labyrinth that is surrounded by perilymph and contains endo-
lymph. The membranous labyrinth contains the semicircular canals,
utriculus, and saccule. These in turn contain sensory areas of thick-
ened epithelium, maculae, crests, and papillae. The vestibular or-
gan responsible for equilibrium contains receptors sensitive to head
movements and structures that include the utriculus, sacculus, and
lagena where otoliths are located. The cochlear organ is responsible
for hearing and contains the cochlear duct filled with endolymph. It
also contains sensoty epithelium and basilar papilla that consist of
ciliated hair cells and supporting cells. Branches of the eighth cranial
nerve (vestibulocochlear nerve) go to the vestibule and cochlea.
Diseases
Diseases involving the ear have not received extensive study and are
not well characterized. The avian ear, primarily the chicken ear, has
been used as a model to study conditions such as toxicities, hair cell
regeneration, effects of sound and noise, and a few genetic diseases.
Similar to mammals, birds ' ears can be injured due to a variety of
infectious and parasitic agents as well as non-infectious agents in-
cluding toxic, nutritional, plant material, and miscellaneous entities .
Diseases of the extem al ear
Among diseases of the external, middle, and il1ller ears of the birds,
diseases of the external ear are most common. The external ear is
Eye and Ear
the continuation of the skin; as such it is prone to injury by various
etiologic agents that cause lesions including hyperkeratosis, acan-
thos is, ulceration, and inflammation. Glands in the external ears
can undergo atrophy, hypertrophy, and vacuolation of cells, as well
as inflammation and occasional squamous metaplasia . Occluded
external ear openings can be seen in young macaws, especially mili-
tary macaws. Mild to severe inflammation of the external ear due to
bacteria such as E. coli, Pse11do111011as aeruginosa, Staphy lococcus
aureus, Pasteurella 11111/tocida, Pmteus 111irabilis, and Entemcoccus
sp ., has been observed in domestic chickens. Similar lesions as-
sociated with bacteria have also been observed in a variety of birds
including psittacines, pigeons, doves , ducks, pheasants, mocking-
birds, turaco, and finches . Otitis externa and otitis media due to
1Ylycobacteri11111 sp. has been identified in a Cordon Bleu finch.
Among viruses, fowl pox in chickens is probably one of the
most common causes of otitis externa. Intranuclear inclusion bodies
of herpesvirus have been observed in epidermal cells of the exter-
nal ear in pigeons and a Ring-neck dove. It is probable that other
viruses such as polyomaviruses and circoviruses that infect the skin
can also infect the external ears.
Hyperkeratosis and inflammation of the external ear associated
with yeast forms of Candida spp. including C. glabrata have been
identified in various species of birds. 1Ylicrospor11111 gallinae, which
causes favus in chickens, can also infect the external ear. Certain
mites, such as Jvlegninia gingly11111ra have been associated with oc-
clusion of the external meatus and otitis externa in chickens. Mites
of an undetermined species have also been observed associated with
otitis externa in psittacines. Mites of Knemidocoptes sp . in psit-
tacines can cause otitis externa, probably as an extension from the
skin of the face. Granulomatous otitis in a gyrfalcon was diagnosed
with severe otitis associated with remnants of fly larvae. One of
the most common causes of otitis within various species of birds is
a foreign body, such as plant material or dust, which can be present
with or without bacteria.
Squamous metaplasia of the glands of the external ear associ-
ated with generalized lesions of vitamin A deficiency has been ob-
served in turkeys, ostriches, and psittacines. Tumors such as fibro-
mas, or lymphomas arising near the ear can occlude the external ear.
Trauma of the external ears is common in game chickens involved
I
in ' cock fighting ' .
Diseases of the middle ear
Neurological signs such as head tilt (torticollis) can be a manifesta-
tion of middle or inner ear infection. Most middle ear infections re-
sult from bacteria gaining access through the Eustachian tube from
the oropharynx, or rarely as an extension from an external ear infec-
tion. Diseases of the oropha1ynx can also lead to middle ear infec-
tions, but it is ve1y rare to see middle ear infections as an extension
from the inner ear. Lesions in the middle ear can range from mild
to severe fibrinoheterophilic, lymphoplasmacytic, or granulomatous
inflammation with infiltration of giant cells. One of the most com-
mon diseases associated with otitis media in gallinaceous birds such
as chickens and turkeys is fowl cholera, caused by Pasteurella 11111/-
tocida. Lesions can extend into the surrounding air spaces of the
cranium. Inflammation of the cranial bone around the middle ear
Avian Histopathology (4 th Edition) I 525
 H. L. Shivaprasad
due to Pse11do111onas aeruginosa has been reported in young African
VetBooks.ir
Grey parrots that had cl inical sig ns of opisthotonus and malposition-
ing of the head. Mycop/asma gallisepticwn ca n cause lymph oplas-
macytic otitis media in turkeys.
Among viruses, poxvirus in canaries and herpesvirus in psit-
tac ines have been associated with otitis media. Inflammation of the
air spaces within the cranial bones associated with or without bac-
teria is co mmon in birds. Sometimes thi s inflanunation can be as-
sociated with middle ear infec tion s. Often the inflammation within
the air spaces is associated with xanthoma fo rmation, especially in
clu·onic stages with the presence of typic al cholesterol cleft s and
mononuclear inflammato1y cells mi xed w ith multinucleated giant
cells. Hemorrhage, especially in the middl e ears, is a finding in
birds, but the cause is unknown.
Diseases of the inner ear
Diseases of the inner ear are rare in birds. They are primaril y mani-
fested as neurological signs and must be differentiated from those
caused by les ions in the brain. The complex structure of the inner
ear, as well as the difficulty of accessing the inner ear in live birds
makes it difficult to evaluate.
One of the geneti c defects of the inner ea r described in birds
is d ysgenesis of the hair cell s on the basilar papilla in Be lg ian
Waterslager ca narie s . Abnormal otoliths are assoc iated co nge ni-
tal neuro logic disea ses in chickens and turkeys called " congeni-
tal loco".
Some of the most co mmon viral di seases that cause oti ti s in-
terna are avian paramyxov irus 1 (APMV-1) in pigeons and av ian
paramyxov irus 3 (APMV-3) in psittacines and passerines, such as
finches and canaries. Otitis interna due to polyomav irus infect ion
has been observed in lovebirds. Lesions were primarily lympho-
plasmacytic in nature. Intranuclear inc lusions can be observed in
the epithelial cells of the cochlea with APMV-3 and in the e pithelial
and monon uclear inflammatory cells with polyomavirus. Lympho-
plasmacytic inflammation of the vestibulocochlear nerve and the
ganglia has also been seen in such diseases as Marek 's disease in
chickens, bornavirus infecti o n (proventricul ar dil atation di sease) in
psittacines, and avian encephalomyelitis vi ru s in chickens.
Fibrinoheterophilic otitis interna associated with intrales ional
bacteria was observed in turkeys and was caused by Sa /111011ella
I
arizo11ae. These birds also had severe meningoencephalitis and in-
flamm ation of the vestibul ocochlear nerve, suggesting that the prob-
able mode of transmission was through the e ig hth cra ni al nerve.
Other such examples of otiti s interna due to bacteria include Rie-
m erella ana fip estifer infection in Pekin ducks, E. co li infection in
Pekin ducks, Salmonella typhim11ri11m va r. Copenhagen in squa bs,
Flavobacterium in pigeons, and unknown bacteria in a male Black-
Masked lovebird. Ne uriti s and ga nglionitis of the vestibulocochlear
nerve due to Pasteurella multocida was di agnosed in a Blue and
Gold macaw that had meningitis.
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toxicosis in newly hatched chicks. Vet Pathol 31 :619 .
Rigdon , R.H ., T. M. Ferguson, and J. R. Couch. 1959.
Spontaneous cataracts in turkeys . Am J Vet Res 20:961-965.
Romanoff, A. L. 1972. Pathogenesis of the Avian Emb1J'O. John
Wiley & Sons: New York.
Salter, D. W. , W. S. Payne, D . T. Ramsey, M. Blair, and J. A.
Render. 1997. A new inherited ocular anomaly in pigmented
White Leghorn chickens. J Vet Diag n in vest 9:407-409.
Sanger, V. L., E. N. Moore, and N. A. Frank. 1960.
Blepharoconjunctivitis in turkeys. Poul/ Sci 39:482-487.
Schmidt, R . E. , D. R. Reavill, and D. N. Phalen. 2003. Pathology
o_f Pet and AvialJ' Birds. Iowa State Press: Ames, IA. pp. 197-
212
Seifried, 0. 1931. Histopathology of infectious laryngotracheitis in
chickens. J fap Med 56:817-826.
Shivaprasad, H . L. Avian Ear - Anatomy and Diseases (Masters
class). Proc. Assoc Avian Vet. pp. 127-133.
Shivaprasad, H. L. 1999. Poultry ophthalmology. In: K. N. Gelatt
(ed.). VeterinalJ' Ophthal111ology. Lippincott, Williams and
Wilkins: Philadelphia, PA. pp. 1177-1207.
Shivaprasad, H. L. 1993. Diseases of the nervous system in pet
birds; a revi ew and report of diseases rarely documented. Proc.
Assoc Avian Vet. pp. 213-222.
Shivaprasad, H. L. , P. Cortes, and R. Crespo. 2006. Otitis inferna
(labyrinthitis) associated with Salmonella enterica arizonae in
turkey poults. Avian Dis 50: 135-138.
Shivaprasad, H. L. and R . Korbel. Blindness due to retinal
dysplasia in broiler chicks. Avian Dis 47:469-473.
Smith, T. W., D . M. Albert, N. Robinson, B. W. Calnek, and 0.
Schwabe. I 974. Ocular manifestations of Marek's disease.
Invest Ophthal111ol 13:586-592.
Smyth, J. R. J. 1989. The Smyth chicken: a model for autoimmun e
amelanosis. Crit Rev Poul/ Biol 2: 1-19.
Smyth, J . R . J., R. E. Boissy, and K. V. Fite. 1981. The DAM
chicken: a mode l for spontaneous postnatal cutaneous and
ocular amelanosis. J H eredity 72: 150-156.
Sola, S. C., M. Castagnaro, and K. M. Cheng. 1997. Histological
changes caused by the re mutation in chickens. J Comp Pathol
116:329-338.
Somes, R. G. J., K. M. Cheng, D. E. Brenon, and R . D. Crawford.
1990. Mutations and major variants of other body systems
in chickens: mutations involving the eye. In R. D. Crawford
(ed.). PoulflJ' Breeding and Genetics. Elsevier, Amsterdam pp.
281-291.
Spalatin, J. , R. P. Hanson, and T. D. Jones. 1973. Edema of the
eyelid and face of chickens exposed to the viscerotropic type of
Newcastle disease virus. Avian Dis 17:623-628.

Stoc kard , C . R. l 914. The artificial production of eye abnormalities
in the chick embryo. Anal. Rec 8:33-41.
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Suwa , T. , S. Ando, N . Hashimoto, and C . ltakura . 1990. Pathology
of experimental chlamydiosis in chicks. Jpn J Vet Sci 52:275-
283.
Swayne, D. E. 1996. Eye and ear. In C. Riddell (ed.) Avian
Histopathofogy. AAAP. Kennett Square, Philadelphia, PA. pp.
203-210.
Takatsuji, K. , H. Ito, M . Watanabe, M. Ikushima, and A.
Nakamura. l 984. Histopathological changes of the retina and
optic nerve in the albino mutant quail (Cot11rnixjapo11ica). J
Co111p Pathof 94:387-404.
Trenchi , H. l 960. Ingestion of A111111i visnaga seeds and
photosensitization-the cause of vesicular dermatitis in fowls.
Avian Dis 4:275-280 .
Ulshafer, R. J. 1985. Avian modefs o,fhereditary retina!
degeneration. Retinal degeneration: experimental and clinical
studies. Alan R. Liss: New York, NY. pp. 321-337 .
Ulshafer, R. J. , C . Allen, W.W. Dawson, and E. D. Wolf. 1984.
Hereditary retinal degeneration in the Rhode Island Red
chicken. l. Histology and ERG . Exp Eye Res 39: 125-135.
Eye and Ear
Wight, P. A. L. 1965. Histopathology of a chronic endophthalmitis
of the domestic fowl. J Co111p Pathof 75 :353-361.
Wight, P.A. L. and J. G. Carr. 1965. Dominant microphthalmia in
the fowl. J Pathof Bacteriof 89:681-689.
Williams, M. C. and W. Binns. 1968. Experimental
photosensitization by spring parsley (Cy111opter11s watsonii) in
chickens . Am} Vet Res 29:lll-115.
Wilson, H. , J. E. Graham, and B. Ritchie. 2000. Otitis externa in a
group of neonatal psittacine birds. Proc. Assoc Avian Vet. pp.
197-198.
Wilson, S. C. 1994. Investigation of suspected mycobacteriosis in a
group of tropical birds at the Topeka zoological park. Proc Am
Assoc Zoo Vet.
Wolf, E. D. 1982. An inherited retinal abnormality in Rhode Island
Red chickens . In: R. M. Clayton, B. Haywood, H . W. Reading
and A . Wright (eds.) . Probfe111s of Nom1af and Geneticaffy
Abnormaf Retinas. Academic Press: London. pp. 249-252.
Worthen, D. M. and C . Moscovici. 1972. Viral-induced ocular
tumors in chicks. Invest. Ophthafmof I I: 122-125 .
Wright, G. W. and J. F. Frank. 1957. Ocular lesions in chickens
caused by anunonia fumes. Can J Comp Med 21 :225-227.
Avian Histopathology (4 th Edition) I 529
 H. L. Shivaprasad
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\ II

11
\

' )

11.1. Eye. Normal cornea. Chicken. The refractive component
is composed of the following zones: the multilayered anterior
epithelium, the anterior limiting membrane, Bowman's layer (lacks
stroma cells), substantia propria, posterior limiting membrane, and
the single layer posterior epithelium.
11.3. Eye. Normal iris. Chicken. Single layer of epithelial cells
covers the anteri or surface of the iris and the posterior is covered by
2 to 7 layers of pigmented epithelium. Muscle fibers within the iris
are striated.

I ~ ·

11.2. Eye. Normal scleral ossicles. Chicken. This group of 11.4. Eye. Norma l iris. African grey parrot. Pigment is in th e
bones forms a complete ring of overlapping plates in the anterior cytoplasm of lip id-laden cells.
part of the globe. Because of the scleral ossicles, most bird 's eyes
need decalcification before processing.

530 I American Association of Avian Patho logists

 Eye and Ear
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11.5. Eye. Normal lens. Chicken. The lens is transparent and
bi-convex. The amrnlar pad (AP) surrounds the equator of the lens
like a belt. There is a fluid-filled cleft located between the annular
pad and the body of the lens. C. Cornea; I. Iris.
11.7. Eye. Normal pecten. Chicken. The pecten is unique
to birds. Shown is the pleated type projecting from the retina to
the vitreous and consisting almost exclusively of capillaries,
extravascular pigment, and stromal cells. Its prima1y fimction is to
provide nutrition to the retina.

I'
!
-
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11.6. Eye. Normal retina. Chicken. The avian retina is similar

to other vertebrates in its general organization. It is avascular
11.8. Eye. Retinal dysplasia. 7-day-old chicken. Retinal
dysplasia is characterized in this case by degeneration of photo-
I
in birds. Layers shown are: N. nerve fiber layer; G. ganglion receptor cells.
cell layer; IP. inner plexiform layer; IN. inner nuclear layer; OP.
outer plexiform layer; ON. outer nuclear layer; R. layer of rods
and cones; E. Pigmented epithelium . The inner and the external
limiting membranes are difficult to visualize and are not labeled.

Avian Histopathology (4'" Edition) I 531

 H. L. Shil'(tprasad
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11.9. Retinal dysplasia. 14-day-old chicken. Retinal dysplasia
in this case is characterized by loss of photo-receptors and by rosette
formations.
I 11.10. Eye. Retinal dysplasia. 24-week-old broiler breeder
chicken. Severe retina l dysplasi a in this case is characterized by
complete loss of photo-receptors, fibrosis of the retinal pigment
epithelium, and rosette formations.
532 [ American Association of Av ian Pathologists
11.11 . Conjunctiva and third eyelid. Vitamin A deficiency.
3-to-4-week-old turkey. Severe squamous metaplasia is in th e
conjunctiva and the third eyelid.
11.12. Eye. Corneal erosion caused by ammonia. 26-day-old
broiler. Area in the center of the cornea is devoid of epithelium.
The exposed basement membrane is thickened and contains minera l.
The corneal epithelium at the border of the erosion is detached from
the underlying basement membra ne. (Image and legend courtesy of
Tahseen Abdul-Aziz) .

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,,.
, Cor,n~ stroma
., /
r
11 .13. Eye. Corneal erosion caused by ammonia. 26-day-old
broiler. Calcific band keratopathy and corneal erosion. An area in
the cornea is devoid of comeal epithelium (corneal erosion). The
basement membrane (arrow) is thickened and basophilic (bluish)
due to deposition of calcium. (Image and legend courtesy of
Tahseen Abdul-Aziz).
Corneal stroma
11.14. Eye. Corneal erosion caused by ammonia. 26-day-old
broiler. Von Kossa stain shows the deposition of calcium (black
material) in the basement membrane. The arrow indicates corneal
epithelium detached from the basement membrane at the margin
of the eroded area. (Image and legend courtesy of Tahseen Abdul-
Aziz).
Eye and Ear
Lens
11.15. Eye. Corneal erosion caused by ammonia. 6-week-old
broiler. The center of the cornea has collapsed. The upper part of
the corneal stroma has been replaced by loose fibrous tissue covered
with irregular corneal epithelium. Often blood vessels, which are
not normally present in the cornea, can be seen in these lesions.
This lesion is indicative of a chronic repair process. (Image and
legend courtesy of Tahseen Abdul-Aziz).
11.16. Conjunctivitis. Infectious laryngotracheitis. Chicken.
Severe inflammation is accompanied by syncytia formation. Some
I
syncytial cells contain intranuclear inclusion bodies characteristic
of infectious laiyngotracheitis virus ( Gal/id he1pesvims I) .
Avian Histopathology (4 th Edition) I 533
 H. L. Shivapmsad
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11.17. Conjunctivitis. Infectious laryngotracheitis and fowl 11.19. Conjunctivitis, Exotic Newcastle disease. Game chicken.
pox. 24-week-old white leghorn chicken. Note the intranuclear Severe necrohemorrhagic inflammation in the conjunctiva.
inclusion bodies due to ILT virus and the intracytoplasmic
eosinophilic inclusion bodies of pox virus. Occasional cells contain
both intranuclear and intracytoplasmic inclusion bodies.

11.18. Conjunctivitis. Pox. Pheasant. Severe proliferative 11.20. Iridocyclitis. Polyomavirus infection. Psittacine. Note
conjunctivitis is characterized by hypertrophied and hyperplastic the characteristic intranuclear inclusion bodies of polyomav irus in
epithelial cells containing eosi nophilic intracytoplasmic inclusion the mononuclear cells.
bodies.

534 I American Association of Avian Pathologists

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11.21. Proliferative conjunctivitis. Herpesvirus infection. 11.23. Eye. Vitreous. Sa/111011el/a typhi11111ri11111 infection.
Gouldian finch. Proliferative conjunctivitis 1s severe with Pigeon. Granulomatous inflammation is severe.
karyomegalic cells containing typical herpesvirus intranuclear
inclusions.

•' '. '

11.22. Eye. Vitreous. Escherichia coli infection. Chicken. 11.24. Eye. Vitreous. Sa/111011ella ariza11ae. Turkey poult.
Severe granulomatous inflammation in the vitreous. Fibrinoheterophilic inflammation is severe.

Avian Histopathology (4' h Edition) I 535

 H. L. S!,i)!(tpmsad
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11 .25. Conjunctivitis, Mycopfrtsm" galliseptic11111 infection. 11.27. Vitreous. Aspergillosis. Turkey poult. Fibrinoheterophili c
Pheasant. Lymphopl asmacyti c inflammation with lymphoid inflammati on is severe.
nodule form ati on is characteri sti c of mycoplas mal infecti ons.

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11.26. Eye. Sciera and optic nerve. Vasculitis and neuritis. 11.28. Eye. Vitreous. Aspergillosis. Turkey poult. Funga l
Mycop/(ls111a synoviae infection. Turkey. Vasculitis and optic hyphae are shown.
neuritis are severe.

536 I Ameri ca n Assoc iati on of Av ian Patho logists

 Eye and Ear
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11.29. Optic nerve. Neuritis. Toxoplasmosis. Chicken. Severe 11.31. Eye. Pecten. Le11cocytozoo11 simondi infection. Duck.
necrotizing optic neuritis is associated with a large number of This higher magnification of 11.30 shows megaloschizonts of
tachyzoites and a few cysts that are scattered throughout the lesion. Leucocytozoon simondi in the optic nerve and the choroid.

11.30. Eye. Pecten. Le11cocytozoo11 simondi infection. Duck.

Megaloschizonts are characteristic of Leucocytozoon simondi.
11.32. Lymphoma. Marek's disease. Chicken. The sclera and
choroid are infiltrated with neoplastic lymphocytes.
I

Avian Histopathology (4 th Edition) I 537

 H. L. Shivaprasad
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11.33. Eye. Lymphoma. Marek's disease. Chicken. The cornea 11.35. Eye. Retina and optic nerve. Marek's disease. Chicken.
is infiltrated by neoplastic lymphocytes (A) that are shown at higher Neoplastic lymphocytes are infiltrating the pecten and optic nerve.
magnification in B. A diffuse infiltration of lymphocytes in the iris
and ciliary body is shown in C. See D for a higher magnification.

I 11.34. Eye. Pecten. Lymphoma. Marek's disease. Chicken.

Neoplastic lymphocytes are infiltrating the pecten.
11.36. Eye. Retina and optic nerve. Marek's disease. Chicken.
Neoplastic lymphocytes are infiltrating the pecten and optic nerve.
Insert shows intranuclear inclusions in retinal ganglion cells at
higher magnification .

538 I American Association of Avian Pathologists

 Eye and Ear
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11.37. Eye. Myelocytoma (avian leukosis subgroup J Virus). 11.39. Eye. Lens. Cataract. 16-week-old white leghorn
Broiler breeder Chicken. Neoplastic myeloid cells are invading chicken. Cataract formation is probably secondary to avian
the anterior uvea encephalomyelitis virus infection.

11.38. Eye. Choroid. Melanoma. 25-year-old scarlet macaw.

Neoplastic melanocytes are invading choroid.
11.40. Eye. Lens. Cataract. 26-week-old broiler breeder
Chicken. Severe cataract formation. The cause is unknown in this
I
case.

Avian Histopathology (4 th Edition) I 539

 H. L. Shil'aprasad
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11.41. Vitreous. lntraocular ossification. Adult chicken. 11.43. Ear. Normal. Chicken. Glands of the external ear are
lntraocular ossification includes bone formation and bone marrow. shown with two prominent lymphoid nodules that are considered
lntraocular ossification could be clue to genetics or a consequence of normal.
severe clu-onic inflammation.

I Chicken. Showing external ear (E) with

glands, middle ear (M), and the inner ear composed of cochlea
11.44. Ear. Normal. Chicken. Glands of the external ear are
composed of epithelial cells with vacuolated cytoplasm.
(C), vestibule (V), and semicircular canals (SC). Also note
vestibulocochlear nerve (VC) and tympanic membrane (T).

540 I American Association of Avian Pathologists


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11.45. External Ear. Vitamin A deficiency. Turkey pouit.
Severe squamous metaplasia due to vitamin A deficiency is in a
gland of the external ear.
11.46. Ear. Otitis externa. Escherichia coli infection. Adult
layer breeder Chicken. Exudate is in the external ear. Note the
inflammation in the superficial layers of the external ear.
Eye and Ear
11.47. Ear. Otitis externa. Bacterial and foreign body. Turkey
poult. External ear shows severe otitis externa with ulceration and
inflammation associated with bacteria and plant material in the
superficial layer.
11.48. Ear. Otitis media. Riemerella anatipestifer infection.
Duckling. Subgross image of the ears shows bilateral otitis media.
I
Riemerella analipestifer was isolated from internal organs.
Avian Histopathology (4 th Edition) I 541
 H. L. Shil'apmsad
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11.49. Ear. Otitis media. Escl,ericl,ia coli. Young broiler. Severe 11.51. Ear. Otitis media. Mycop/asma gallisepticum infection
fibrinoheterophilic exudate is in the middle ear and osteomyelitis is 12-week-old turkey. Severe lymphoplasmacytic inflammation
severe. Note that the inner ear is not affected. characterizes this case of otitis media due to Mycoplas111a
gall iseptic11111.

I 11.50. Ear. Otitis media. Pasteurella 11111/tocida infection. 11.52. Ear. Otitis interna. Sa/111011ella arizonae infection .
Broiler breeder chicken. Otitis media is severe. Turkey poult. Subgross of ears shows severe otitis interna (closed
arrow) on the right, normal inner ear on the left (open arrow). E.
external ears. M. middle ears.

542 I American Association of Avian Patholog ists

 Eye and Ear
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5()_;_0 1:16i·- ;
...,.
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11.53. Ear. Otitis interna. Sal111011ella Arizo11ae infection. 11.55. Vestibulocochlear nerve. Marek's disease. Adult
Turkey poult. Higher magnification of the region at the closed chicken. Infiltration of lymphocytes due to Marek's disease is in
arrow in 11.52 shows severe otitis interna with destruction of the the vestibulocochlear nerve.
normal architecture of the cochlea and vestibule. The bird had
severe meningoencephalitis associated with bacteria from which
Salmonella arizo11ae was isolated.

11.54. Ear. Otitis interna. Sal111onella Arizo11ae infection.

Turkey poult. Higher magnification of 11 .53 shows severe otitis
I
interna with bacterial colonies and multinucleated giant cells at the
periphery.

Avian Histopathology (4 th Edition) I 543

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CHAPTER
Endocrine System
Tahseen Abdul-Aziz • Oscar J. Fletcher
Pancreas
Anatomy and Histology
The pancreas is an elongated, white to light-pink gland in the mes-
entery between the descending and ascending limbs of the duo-
denal loop. In some avian species, it almost completely occupies
the space within the loop. In most avian species, the pancreas has
three lobes, ventral, dorsal, and splenic. The splenic lobe is a small,
narrow strip that extends from the head of the pancreas toward the
spleen. Two pancreatic ducts from the ventral lobe and one duct
from the dorsal lobe open into the distal end of the ascending limb
of the duodenum, close to the openings of the bile ducts. A thin
connective tissue capsule covers the surface of the pancreas. Due to
the lack of interlobular com1ective tissue septa, the lobular pattern is
not as prominent in birds as it is in mammals . The pancreas is com-
posed of two histologically and fonctionally distinct components,
the exocrine and endocrine pancreas. The exocrine pancreas, which
secretes digestive enzymes, is composed oftubuloacinar glands and
intralobular ducts. In routine histological sections, these glandular
epithelial cells appear generally pyramidal or triangular in shape,
and may be arranged around a central lumen. Nuclei are spherical
and located near the base of the cells. The apical cytoplasm is filled
with coarse eosinophilic granules, which are the precursors to pan-
creatic enzymes. Intralobular ducts of va1ying sizes may be seen.
Smaller ducts are lined with flattened epithelium, while larger ducts
are lined with cuboidal epithelium. The main branches of the pan-
creatic ducts are lined by columnar epithelial cells and have a thick
subepithelial layer of fibrous connective tissue and smooth muscle.
The exocrine pancreas secretes enzymes that degrade lipids, pro-
teins, carbohydrates, and amino acids. Enzymes are transpmted into
the lumen of the duodenum via the pancreatic ducts. The proteolytic
enzymes trypsin and chymotrypsin, and the lipolytic enzyme phos-
pholipase, are formed and secreted in an inactive form (as enzyme
precursor molecules) to prevent digestion of the cells in which they
are synthesized. The inactive molecules of the enzymes are acti-
vated in the lumen of the intestine.
The endocrine pancreas is composed of roughly spherical or ir-
regularly shaped microscopic collections of secretory cells scattered
among the exocrine glandular tissue termed islets of Langerhans.
They are not uniformly distributed in the tlll'ee lobes, being more
numerous and larger in the splenic lobe. Also there are generally
more islets in the anterior third of the pancreas than in the other
regions . Major cell types in the islets are designated as alpha, beta,
12
and delta cells . Alpha cells, which secrete glucagon, are columnar
in shape and are the largest of the three cell types. Beta cells, which
secrete insulin, are smaller than Alpha cells and are round to polygo-
nal in shape. Delta cells, which secrete somatostatin, are smaller
than alpha and beta cells. Three types of islets have been described
in birds, alpha , beta and mixed based on the relative numbers of the
major cell types. Alpha islets are comprised predominately of alpha
cells with a few delta cells. Beta islets contain predominantly beta
cells with a few delta cells . Mixed islets contain both alpha and
beta cells in variable proportions with a few delta cells . Alpha islets
are usually large, irregular in shape, and have a faintly eosinophilic
appearance. Beta islets are generally smaller than alpha islets and
appear as faintly basophilic, roughly round compact groups of cells.
Delta cells are scattered single or small groups of cells at the periph-
e1y of the islets. lmmunohistochemical staining for their secreto1y
products readily identifies the different cell types.
Non-Specific Lesions
Depletion of zymogen granules and shrinkage, degeneration, vacu-
olation, and apoptosis of acinar cells are non-specific lesions. Star-
vation, anorexia, malnutrition, and vitamin deficiencies alone or in
combination can cause these changes. Additionally, these changes
are also commonly seen in emaciated birds with neoplasia, severe
parasitism, or other chronic debilitating diseases (e.g. , mycobacte-
riosis). In some cases, acini around islets appear normal with their
cells filled with zymogen granules, while acinar cells in other areas
are pattially or completely depleted of zymogen granules. For un-
known reasons, acini around islets are the last to be affected.
An increase in the amount and density of the interstitial con-
nective tissues with compression atrophy of acini characterizes the
chronic phases of inflammation in the pancreas. Typically, bands
I
of mature fibrous tissue separate small lobules of acinar tissues.
Mononuclear inflammatory cells may be present in the fibrous tis-
sue. In the most severe cases of fibrosis (pancreatic sclerosis), only
blood vessels, pancreatic ducts, occasional pancreatic islets, and
small groups of isolated acini remain.
Non-Infectious Conditions
Cytoplasmic vacuolation of acinar cells with many vacuoles con-
taining spherical, amorphous eosinophilic masses are early lesions
seen in selenium deficiency. Later, acinar cells undergo atrophy, the
acinar lumen becomes dilated, and fibroblasts appear in the intersti-
tial spaces. In chronic cases, there is marked fibrosis that contains
Avian Histopathology (4 th Edition) I 545
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
indi vidual ducts with dilated lumens and severely shrunken lining
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cells, the cytoplasm of which is hard ly di scernible.
Widespread, severe apoptosis and loss of normal pancreatic
structure occurs in severe cases of zinc toxicity. Apoptotic cells ap-
pear as acidophilic bodies containing fragmented pyknotic nuclei .
In chronic zinc toxicity, variable degrees of fibrosis separate acini
and disrupt the normal architecture of the pancreas. Regeneration
is characterized by misshapen, di sorga ni zed ductular structures
separated by bands of fibrous ti ssue. Ducts are lined by epithelium
co nta ining mitotic figure s. The ductul ar structures likel y represent
regenerating acini. The identity of cells of origin in acinar regen-
erati on is uncertain. This spectrum is not specific for zinc toxicity,
but indicative of acute or chroni c damage to the pancreas; toxicity
should be considered in any differential di agnosis.
Diffuse coagulative necrosis of the pancreas is characteris-
tic of acute pancreatic necrosis. Necrotic tissue appears acellular
with finely granular necrotic debris. This lesion is seen in psitta-
c ine birds, particularly Quaker parakeets. Parakeets on a hi gh-fa t
diet that are obese are most likely to be affected. Usually an en-
tire pancreatic lobe is invo lved . Areas of hemorrhage and necrosis
of the mesenteric fat are common. The diffuse, severe necrosis is
most likely caused by activation oftrypsinogen to trypsin within the
pancreas, leading to subsequent activat ion of other proteases which
digest the pancreatic tissue. However, the triggering event for tryp-
sinogen activation is not known.
Marked macrovesicular vacuolation of beta cells, with or with-
out multifocal lymphocytic infiltrate, cluonic lymphocyti c pancre-
atiti s, or islet cell carcinoma has been found in cases of diabetes
mellitus in budgerigars, touca ns, Africa n grey parrots, red-tailed
hawks, Emperor penguins, cockatiels, and blue and gold macaws .
The presence of a homogenous or fibrillar eosi nopbilic mate-
rial that efface s and replaces exocrine and endocrine cells is char-
acteristic of amyloidosis. In severe cases, only individual or sma ll
gro ups of disorganized acini separated by amyloid are present. Cells
in the remaining acini appear small but may still contain zymogen
granules. Pancreatic islets may beco me hardl y recognizable due to
extensive amyloid deposition.
Infections
Viral infections
Partial or complete depl etion of zymogen gra nules, cytoplas mi c
vacuolation, and sometimes necrosis of individual cells are early
lesions seen in pancreatic acinar ce ll s of broiler chi ckens with infec-
tious runting-stunting syndrom e. Eosi nophilic byaline inclusions
may be seen in the cytoplasmic vacuoles. The lumens of so me ac ini
are dilated and lined by cuboidal to flattened epithelium. There
are foci of lymphocytes, macrophages, and a few granulocytes. In
older chickens, atrophy of ac ini with marked interstitial and capsu-
lar fibrosis may be found. Fibrosis tends to obliterate much of the
exocrine tissue, and several lobes may contain only small, distotted
ac inar-like structures and small branching ductules embedded in fi-
brous tissue. Acini immediately peripheral to the pancreatic islets
are usually spared. Lymphoid cells are present in the fibrous stroma,
and there are lymphoid germinal ce nters. Lesions are sometimes
fo und in intralobular ducts, with some ducts showing epithelia l
546 I American Association of Av ian Pathologists
degeneration and necros is, va ri able numbers of degenerate and ne-
crotic cells in the lumen, and infiltration of the wall by lymphocytes,
ma crophages, and few gra nul ocytes. Some ducts may be dilated
and lined by flattened or cuboidal epithelium.
Scattered variably s ized foc i of necrosis with large, deeply
basophilic intranuclear inclusio n bodies in acinar cells are lesions
seen in some cases of av iadenoviral infection (inc lusion bod y
hepatiti s) in chicks. Massive necrosis of exocrine pancreas can be
caused by adenovirus in fect ion in young (<7day) chi cks. In Guin-
ea fowl , adenov irus can ca use severe pancreatitis without liver le-
sions. There is necros is of pancrea tic tissue of vary ing degrees
and severity and heterop hil s and macrophages may be assoc iated
with some necroti c foci. Large, basophilic inclusion bodies typi-
ca l of adenovirus inclusions fill the enl arge d nuclei of degenerat-
ing acinar cells.
In chicks affected with av ian encephalomyelitis, small foc i of
lymphoid cell infiltration occur in the pancreas and small encapsu-
lated reactive follicles co mposed of large, lymphoblast-like cell s are
occasionally found .
Multifocal areas of ac inar cell degeneration and necrosis w it h
variable infiltrates of lym phocytes characteri ze pancreatic lesions
in pigeons infected with paramyxovirus type 1. In severe cases,
ac ini are lost and replaced by fibrous tissue, with large number of
lymphocytes.
Necrosis of varying extent and severity in the pancrea ti c pa-
renchyma is common in birds th at die from natural or experimental
infect ion with hi ghl y pathogenic av ian influenza viruses. Multifo-
ca l areas of necrosis of exocrine cells and mixed inflammatory cel l
infiltrations may be features fo und in so me avian species dying of
natural infection with West N ile virus.
In parrots that di e of Pacheco 's di sease, a genera lized vira l
infect ion ca used by herpesvi ru s, the pancreas may contain foci of
degeneration and necrosis of acinar tissues, with intranuclear inclu-
sion bodies in ac inar and ductal epi the lial cells. Few syncytia l cells
containing intranuclear inclusions are seen in some cases.
Acinar cells with enlarged nu clei· (karyomegaly) co ntaining
intranuclear inclusion bodies of polyomavirus, with no ev idence of
necrosis or inflammatio n, are found in the pancreas of nestling par-
rots dying of generalized polyomav irus infection .
Multi focal areas of ac inar cell degeneration and necrosis w ith
infiltration of variable numbers of heterophils and inflammatory
mononuclear cells can be found in the pancreas of turkey poults
affected with turkey viral hepatitis. Later, as the necrosis resolves,
the lesions become densely infil trated with lymphocytes and macro-
phages. Syncytial cells occasionally are seen.
Bacterial infections
Multifocal to diffuse infiltration of macrophages that are occasio n-
all y accompanied by small foci of necrosis are features of subac ut e
to chronic cases of chl amydi osis ca used by Chlamydia psittaci. In-
terstiti al fibrosis may be present in clU"onic cases.
Although not as frequently involved as other organs such as
the li ver, intestines, spleen, serosa, and lungs, the pancreas can be
infected with Jvfycobacteri11111 aviu111. Individual clusters of ma c-
rophages with cytoplasmic ac id-fast bacteri a are more likely in th e

pancreas than larger histiocytic or caseous granulomas. Lesions of
M. avi11111 in the pancreas are usually relatively mild.
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Neoplasia
Pancreatic duct adenomas and adenocarcinomas are the most im-
portant pancreatic tumors in birds. Pancreatic duct adenoma is
characterized by marked intraductal proliferation that may be papil-
lary, with dilation of the lumen and extensive periductal fibrosis that
compresses adjacent acini. In pancreatic duct adenocarcinoma, the
panc,reatic parenchyma is effaced and replaced by numerous lob-
ules of neoplastic ductular structures lined by columnar epithelium
and surrounded by abundant fibrous connective tissue stroma. Pet
birds with pancreatic duct adenoma/carcinoma may concurrently
have ductular neoplasms in the liver and/or internal papillomatous
lesions. Without histochemical staining, it may be difficult to de-
termine whether the tumor in the liver is of bile duct or pancreatic
duct origin . In chickens, the pancreas is a common site for intra-
coelomic metastasis of ovarian and oviductal carcinoma. A mor-
phological distinction bern:een ovarian, oviductal, and pancreatic
duct carcinomas may be difficult to determine when all 3 organs
are involved. Neoplasms of pancreatic islet cells are very rare in
birds. This neoplasm consists of groups of a uniform population of
poorly differentiated, densely packed epithelial cells that infiltrate
and replace the surrounding pancreatic parenchyma. Thin connec-
tive tissue septa separate the groups of cells. Neoplastic cells have
indistinct cell membranes; fine granular, eosinophilic cytoplasm;
and round to oval, eccentric, hyperclu-omatic nuclei. The pancreas
is one the organs that may be involved in lymphoid tumors, (lym-
phoid leukosis or Marek's disease) in chickens.
Thyroid Glands
Anatomy and Histology
Birds have a pair of thyroid glands located in the thoracic inlet
at the base of the neck. The thyroid glands are small, deep red
to reddish-brown structures closely related to the medial side of
the jugular veins just anterior to the angle formed by the subcla-
vian and common carotid arteries. There are variations in the
dimensions and shape of the glands among avian species. Dur-
ing necropsy, the gland must be distinguished from neighboring
syringeal and tracheal muscle, and thymus, which have a similar
color. Careful dissection is necessary to locate and remove the
glands in small birds. Color of the glands distinguishes them
from adjacent thymic lobes. Histologically, thyroid glands are
composed of closely packed, roughly spherical to polyhedral
follicles delineated and separated by thin strands of interstitial
fibrous tissue with a capsule of fibrous tissue. Follicles are lined
by a single layer of epithelial cells and contain an eosinophilic,
homogenous material that is the protein gel constituting the thy-
roid colloid. The size of the follicles, shape of the lining epithe-
lium, and eosinophilic staining intensity of the colloid depend
on the activity of the gland. In active glands, as in young birds,
follicles are small , contain small amounts of palely stained col-
loid, and are lined by cuboidal to low columnar epithelium. In
adult birds, the follicles are large, distended by deeply stained
E11docri11e System
colloid, and lined by flattened epithelial cells. Occasionally, in-
trafollicular corpora amylacea occur as an incidental finding in
older birds. Calcitonin-secreting cells (C cells) are absent in the
avian thyroids, except in pigeons.
Goiter
Goiter refers to a non-neoplastic enlargement of the thyroid glands.
Goiter has been reported in different species of birds, but is particu-
larly common in budgerigars, which seem sensitive to iodine defi-
ciency. High incidence of goiter has also been reported in macaws,
patticularly blue and gold macaws. The primary cause of goiter is
iodine deficiency, but goitrogenic substances of plant origin should
be considered as potential causes.
In birds, goiter can be broadly classified into two types: hy-
perplastic and colloid. These two types are stages of the same
disease process and not separate disease conditions. Grossly,
both types are characterized by varying degrees of bilateral en-
largement of the thyroids . Follicular hyperplasia (hyperplastic
goiter) is an early lesion of iodine deficiency, which results from
increased thyroid-stimulating hormone (TSH), secreted from the
pituitary gland. Increased TSH secretion occurs in response to low
levels of thyroid hormone due to iodine deficiency. Hyperplastic
goiter is characterized histologically by numerous, irregularly-
shaped, closely packed, small follicles lined with cuboidal to low
columnar epithelium. The follicles have small or no lumens with
little or no colloid. In some cases, follicles with persistent lumens
are lined with hyperplastic epithelial cells that occasionally form
small papillary projections. Colloid goiter develops during the
resolution phase of the hyperplastic lesions when the level ofTSH
hormone in the blood is reduced. In colloid goiter, follicles are
large, filled with pale-staining, vacuolated colloid, and lined by
flattened epithelium. In the early stages, large follicles may be still
lined by cuboidal to columnar cells.
In advanced cases, a mixhtre of lesions is seen in the glands .
Many follicles are dilated and lined with hypertrophic and hyper-
plastic epithelium that form multiple layers of cells and intraluminal
papillary projections. Dilated follic les contain lightly eosinophilic,
vacuolated colloid, and the cytoplasm of follicular epithelial cells
have vacuoles. Other dilated follicles contain blood, hemosiderin-
laden macrophages, foamy macrophages, fibrin, sloughed epithelial
cells, and some colloid-like material. There may be subcapsular
hemorrhage. Hemosiderin granules may also be present in the
cytoplasm of follicular epithelial cells. Groups of variably sized
I
and shaped follicles lined by columnar epithelium with collapsed
lumens that lack colloid are also seen. Such lesions must be dif-
ferentiated from adenoma, which is solitary and surrounded by a
fibrous capsule.
Lymphocytic Thyroiditis
Disruptions of thyroid architechtre by intense lymphocytic infiltrates
that surround, separate, and occasionally efface thyroid follicles ,
with formation of lymphoid follicles are features of lymphocytic
thyroiditis. There is an increase in the interfollicular connective tis-
sue with variable degrees of distortion of remaining follicles and
degeneration of follicular epithelium.
Avian Histopathology (4 th Edition) I 547
 Tal,see11 Abdul-Aziz • Oscar J. Fletcher
Follicular Cysts
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Single or multiple follicular cysts are seen occasionally. Cysts are
lined with normal flattened epithelium, and contain colloid. The
cause and significance of thyroid follicular cysts are unknown.
Neoplasia
Follicular adenoma (solitary adenomatous nodule) is the most
common neoplasm in pet birds and other avian species. Follicular
adenoma is solitary and surrounded by a fibrous capsule of varying
thickness. The tumor usually is composed of follicles of varying
size (microfollicular or macrofollicular). Microfollicular adeno-
mas consist of small follicles lined by cuboidal to low columnar
epithelial cells that contain little or no colloid. Macrofollicular
adenomas are composed of follicles that are distended with colloid
and lined by flattened follicular cells. The presence of a fibrous
capsule and compression of adjacent thyroid parenchyma in ad-
enomas differentiate them from circumscribed nodular hyperpla-
sia. Other patterns of thyroid adenoma that are recognized less
frequently are cystic adenoma and papillary adenoma. Thyroid
carcinoma consists of neoplastic cells that form cyst-like struc-
tures (cystadenocarcinoma), papillary structures, (papillary ad-
enocarcinoma), and/or trabeculae, nests, or solid sheets of cells
separated by a fibrous tissue stroma. Neoplastic cells may invade
the capsule and surrounding tissues.
Parathyroid Glands
Anatomy and Histology
The parathyroid glands are bilateral and lie close to or are attached
to the posterior pole of each thyroid gland. They are minute, oval,
and yellowish-brown to brownish-red structures embedded in con-
nective tissue stroma. Normal parathyroid glands may be difficult to
find grossly due to their small size. Histologically, a well-developed
connective tissue capsule surrounds the glands. The parenchyma is
composed of anastomosing cords of cells. Each cord is surrounded
by a small amount of connective tissue stroma containing numerous
blood capillaries. Cross sections of cords appear as irregular groups
of cells surrounded by connective tissue. Cords are composed of a
single cell-type, the chief cells that have basophilic, finely granular
cytoplasm, and round- to oval-shaped nuclei with prominent single
or double nucleoli.
Hyperparathyroidism (Parathyroid
Hyperplasia)
I
Hyperparathyroidism is the most important pathological condition
of the parathyroid gland in birds. Primary hyperparathyroidism ,
usually due to parathyroid gland adenoma has not been docu-
mented in birds. Secondary hyperparathyroidism, occurring in
response to hypocalcemia can be classified into two major entities:
nutritional hyperparathyroidism and renal hyperparathyroidism.
Both result in hyperplasia of the chief cells and gross enlargement
of the parathyroid glands. Secondary renal hyperparathyroidism ,
associated with chronic renal disease, has not been documented in
birds. Nutritional hyperparathyroidism is associated with chronic
rickets caused by dietary deficiencies of vitamin 0 3 or calcium, di-
548 I American Association of Avian Pathologists
etary excess of phosphorous, or low calcium to phosphorous ratio
in the feed. Regardless of the cause, prolonged hypocalcemia tri g-
gers hypertrophy and hyperplasia of chief cells. Histologicall y,
the overall mass of the chief cells is increased because of hyper-
trophy and hyperplasia. The cord arrangement of the cells is pre-
served. A type of hyperplasia termed " water-clear hyperplasia" is
sometimes seen, in which hyperplastic cells have abundant, clear
cytoplasm. Hypertrophy and cytoplasmic vacuolization of chief
cells, without hyperplasia, is an indication of increased glandular
activity. Fibrous osteodystrophy usually is seen in birds with hy-
perparathyroidism.
Adrenal Glands
Anatomy and Histology
Each of the paired adrenal glands lies at the anterior end of the
anterior division of the kidneys, just behind the lungs. They are
yellowish or light brown, irregularly oval to triangular, and closely
related to or covere_d by the gonads in males and females . Large
nerves and sympathetic ganglia surround the glands. Histologically,
a capsule of connective tissue containing blood vessels, nerves, and
ganglia surrounds each gland. Avian adrenal glands do not have
distinct cortical and medullary zones, but rather cords and groups
of cortical (interrenal) and medullary (chromaffin) cells intermingle
throughout the gland . Groups of cortical cells consist of solid cords
of cells, which appear as columns in longitudinal sections and as
groups of radially arranged, round to polygonal cells in cross sec-
tions. These cells have strongly eosinophilic, granular, microvesic-
ular (finely vacuolated) cytoplasm. Numerous cytoplasmic vesicles
indicate the presence of lipid droplets in the cytoplasm. Medulla1y
cells occur as irregular strands or groups of large, round to polygo-
nal cells with a distinctly basophilic cytoplasm, which distinguishes
them from cortical cells. The proportions and distribution of corti-
cal and medullaiy cells vary considerably among species as well as
between individuals of the same species. Cortical cells produce the
steroid hormones, corticosterone, and aldosterone. Medullary cells
produce epinephrine and norepinephrine.
Non-Infectious Conditions
Swelling and vacuolar degeneration of the cortical cells may be
an indication of prolonged uncompensated stress. A condition of
unknown etiology called " idiopathic adrenal degeneration" is seen
in some African grey parrots that die suddenly. Microscopically,
there is a diffuse, marked swelling and vacuolation of cortical cells.
Although no other gross and microscopic lesions may be found in
birds with such adrenal lesions, it is uncertain whether those birds
die from adrenal failure. Marked macrovesicular fatty vacuolation
of the cytoplasm of cortical cells is seen in African gray parrots with
hepatic lipidosis and arterial atherosclerosis. Granular lipofuscin
pigment can markedly accumulate in the cytoplasm of cortical cells.
Mineralization and amyloidosis may be found in the adrenal glands.
Viral Infections
Multifocal areas of necrosis that involve both cortical and medul-
lary cells are caused by infection with highly pathogenic influen-

za viruses in chickens. Mild, subacute to chronic inflammation
of the adrenal gland and/or peri-adrenal neuroganglia is found
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in so me avian species dying from natural infection with West
N il e virus. Polyomavirus inclusions may be seen in enlarged
nuclei of medullary cells . Diffuse or multifocal infiltration of
lymphocytes and fewer plasma cells throughout the parenchyma
are lesions in the adrenal glands of psittacine birds affected with
prove ntricular dilatation disea se. A characteristic lesion in this
sy ndrome is lymphocytic infiltration in the neuroganglia and,
occas ionall y, connective tissues around the glands. Infiltrates
of heterogenous lymphocytes occur in adrenal glands and sur-
ro unding ganglia of chickens that have Marek's disease. The
ex tensive nervous tissue surrounding the adrenal glands, as well
as the glands themselves, makes this an excellent site to examine
for lesions of Marek ' s disease.
Neoplasia
Neoplasms of adrenal glands are rare in birds, and include adeno-
mas, carcinomas, and pheoc:hromocytomas. Adrenal glands may be
a site of metastasis of tumors that originate in other organs. Adrenal
glands may be enlarged, and completely replaced by scirrhous car-
cinoma of ovarian or pancreatic origin. Lesions of lymphosarcoma
occur in Marek's disease; the adrenal gland may be focally infil-
trated or totally effaced by neoplastic lymphoid cells.
Pituitary Gland (Hypophysis)
Anatomy and Histology
The pituitary gland is a small structure located in a depression on
the floor of the sphenoid bone, which forms the greater part of
the floor of the cranial cavity. It lies beneath the diencephalon,
immediately posterior to the optic chiasma, and it is intimately
connected to the hypothalamus . In birds, the gland is divided
into two distinct parts, the adenohypophysis and the neurohy-
pophys is. The adenohypophysis is further divided into the pars
distal is and the pars tuberalis. The pars distal is consists of in-
terconnected cords and follicles of cells surrounded by capillary
sinuses. Many of the cord and follicular structures have central
lumens filled with colloid. The pars tubera/is consists of cords
of cells and a few small colloid-filled acini. Cells of the ad-
enohypophysis secrete several glycoprotein or polypeptide hor-
mones that control other glands . These hormones include follicle
stimulating hormone (FSH), luteini zing hormone (LH), thyroid
stimulating hormone (TSH), growth hormone, prolactin, adre-
nocorticotrophic hormone (ACTH), and melanocyte-stimulating
hormone. The neurohypophysis consists of an internal layer of
ependymal cells (ependymal layer), a middle layer (fiber layer)
of large bundles of coarse unmyelinated axons from neurons in
the hypothalamus, and an external layer (palisade layer) of nu-
merous ependymal and glial cell processes . Variable numbers of
glial cells, which are structurally similar to ependymal cells, are
present within the fiber layer or in the area between it and the
pali sade layer. Small granules of neurosecretory substance are
scattered throughout the middle layer. Vasotocin, functionally
equivalent to mammalian antidiuretic hormone (vasopressin),
Endocrine System
and mesotocin, functionally equivalent to oxytocin, are the hor-
mones sec reted by the hypothalamus . These hormones migrate
down nerve fiber tracts into the neurohypophysis where they are
either stored or released directly into the blood.
Lesions
The pituitary gland should be collected for histopathology from
birds with a clinical history, clinical signs, or gross lesions of blind-
ness, unilateral or bilateral exophthalmia, hyperglycemia, polyuria
and polydipsia, convulsion, obesity, stupor, feather dystrophy, or
abnormal pigmentation. Tumors are the most common lesions that
occur in the pituitary glands of pet birds, pa11icularly budgerigars.
Pituitary gland adenomas are well-delineated tumors composed of
a fairly uniform population of cuboidal to polygonal cells having
a faintly eosinophilic cytoplasm. Tumor cells are arranged in lob-
ules separated by a fibrovascular stroma. Pituitary gland adeno-
carcinomas are composed of sheets of cells of variable sizes with
faintly eosinophilic to colorless cytoplasm that may contain a few
eosinophilic or basophilic granules. The nuclei are round and hy-
perchromatic. A characteristic feature of pituitary gland carcinomas
is the presence of numerous giant cells with large, hyperchromatic,
bizarre nuclei. Pituita1y gland carcinoma is an invasive tumor that
should be suspected when a retrobulbar tissue mass causes bulging
of the eye (exophthalmia).
Additional Readings
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J. Cardona. 1992. Avian paramyxovirus type l infections in
racing pigeons in California. I. Clinical signs, pathology, and
serology. Avian Dis 36:463-468.
Candeletta, S. C., B. L. Homer, M. M. Garner, and R . Isaza.
1993 . Diabetes mellitus associated with chronic lymphocytic
pancreatitis in an African grey parrot (Psittacus erithacus
erithacus). J Assoc Avian Vet 7:39-43.
Capua I. , R. E. Gough, P. Scaramozz ino, R. Lelli , and A. Gatti.
I 994. Isolation of an adenovirus from an ostrich (Struthio
came/us) causing pancreatitis in experimentally infected guinea
fowl (Numida meleagris). Avian Dis 38:642-646.
Carpenter, J W. , G.A. Andrews, and W. N . Beyer. 2004. Zinc
toxicosis in a free-flying trumpeter swan (Cygnus buccinator).
J Wild/ Dis 40:769-774.
Charlton, B. R . and A. A. Bickford. l 995. Gross and histologic
lesions of adenovirus group I in guinea fowl. J Vet Diagn
Invest 7:552~554.
I
Cornelissen, H . and A . Verhofstad. 1999. Adrenal neoplasia
in a scarlet macaw (Ara macao) with clinical signs of
hyperadrenocorticism . J Avian Med S111g 13:92-97.
Curtis-Valasco, M. 1992. Pituitary adenoma in a cockatiel
(Nymphicus hollandicus) J Assoc Avian Vet 6:21-22.
Goodwin, M.A., K. S. Latimer, R. S. Resurreccion, P. G. Miller,
and R. P. Campagnoli. 1996. DNA in situ hybridization for
the rapid diagnosis of massive necrotizing avian adenovirus
hepatitis and pancreatitis in chicks. Avian Dis 40:828-83 I.
Graham, D. L. 1994. Acute pancreatic necrosis in a Quaker
parakeet (Jvfyiopsitta monachus). Proc Assoc Avian Vet 87-88.
Avian Histopathology (4 th Edition) I 549
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
Graham D . L. and G. W. Heyer. 1992. Diseases of the exocrine
VetBooks.ir
pancreas in pet, exotic and wild birds: a pathologist's
perspective. Proc Assoc Avian Vet pp. 190- 193.
Guy, J. S. 2013. Turkey viral hepatitis. In: D.E. Swayne el al. (eds).
Diseases ofPo11lflJ1, 13th ed. Wiley-Blackwell Press: Ames, Iowa.
482-485; 507.
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L. Nolan . 1997. Metastatic pheochromocytoma in a parakeet.
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Hodges, R . D. 1974. The Histology of the Fowl. Academic Press,
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Hodges, R. D. 1981. Endocrine glands. In Form and Function in
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NY, Academic Press pp. 149-234.
Hooper, P.T., G.W. Russell , P.W. Selleck, and W.L. Stanislawek.
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the virulence of some avian influenza viruses and their
pathogenicity for various organs. Avian Dis. 39:458-464.
Jones, Y. L. and D. E. Swayne. 2004. Comparative pathobiology
of low and high pathogenicity H7N3 Chilean avian influen za
viruses in chickens. Avian Dis 48: 119-128.
Klein, P. N., A. E. Castro, C. U. Meteyer, B. Reynolds, J.
A. Swa11zman-Andert; G. Cooper, R. P. Chin, and H . L.
Shivaprasad. 1991. Experimental transmission of turkey viral
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Latimer, K. S. and C . B . Greenacre. 1995. Adrenal carcinoma in
a budgerigar (Me/opsillarns 11nd11/a111s) . J Avian Med Surg
9:141-143.
Phalen, D. N ., M . Falcon, and E. K. Tomaszewski. 2007.
Endocrine pancreatic insufficiency secondary to chronic
herpesvirus pancreatitis in a cockatiel (Nymphicus
ho//andicus). J Avian Med Surg 21: 140- 145.
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fronted macaw (Ara severa). J Avian Med Swg 19:297- 302.
Quesenberry, K. E. 1986. Pancreatic atrophy in a blue and gold
macaw. J Am Vet Med Assoc 189: 1107-1108.
Reece, R.L. and J.A. Frazier. 1990. Infectious stunting syndrome
of chickens in Great Britain: field and experimental studies.
Avian Patho/ 19:723-758 .
Reece, R. L. , P. T. Hooper, S. H. Tate, V. D. Beddome, W. M.
Frosyth, P. C. Scott, and D . A. Barr. 1984. Field, clinical and
pathological observations of a run ting and stunting syndrome
I
in broilers . Vet Rec 115:483-485.
550 I American Association of Avian Pathologists
Ritchey, J. W. , L. A. Degernes, and T. T. Brown, Jr. 1997. Exocrine
pancreatic insufficiency in a yellow-naped Amazon (Amazona
ochrocepha/a) with pancreatic adenocarcinoma. Vet Path
34:55-57.
Ryan, C. P., E. J. Walder, and E. B. Howard. 1982. Diabetes
mellitus and islet cell carcinoma in a parakeet. J Am An Hosp
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Thyroid cystadenocarcinoma in a saker falcon (Falco cherrng).
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(Nymphirns ho//andicus ). Avian Dis 32: 169-172.
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birds. J Avian Med Sw g 16: 111-114.
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chromophobe pituitary tumor. Cancer Res 14:237-245 .
Shivaprasad . H. L. 1990. An outbreak ofhll'key viral hepatitis in
California turkey flocks. Proc 39th Wes/em Poul! Dis Conj,
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Sileo, L. , W. N . Beyer, and R. Mateo. 2004 . Pancreatitis in wild
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6:92 .
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12.1. Pancreas. Normal. 3-week-old broiler. Pancreatic 12.3. Pancreas, splenic lobe. 2-day-old chick. The pancreatic
exocrine tissue bas arrangement of glandular acini. Each acinus is islets in the splenic lobe are numerous and larger than those in the
made up of cells surrounding a minute central lumen that represents ventral or dorsal lobe.
the terminal end of pancreatic duct. The acinar cells are roughly
triangular in shape and have deeply basophilic cytoplasm and large,
round nuclei . The apical cytoplasm is filled with coarse, eosinophilic
granules (zymogen granules).

12.2. Pancreas. Normal. Intralobular duct. 14-week-old

turkey. Large pancreatic duct is lined by low columnar epithelial
cells sheathed by fibrous connective tissue. The pink material in the
lumen is pancreatic secretion.
12.4. Pancreas. Alpha pancreatic islet. 4.5-week-old chicken.
The alpha islet is comprised oflarge alpha cells, which are columnar
and have abundant eosinophilic cytoplasm. The cells secrete the
hormone glucagon.
I
Avian Histopathology (4 th Edition) I 551
 Tahsee11 Abdul-Aziz • Oscar J. Fletcher
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12.5. Pancreas. Beta pancreatic islet. 4.5-week-old chicken.
The beta islet is comprised of beta cells, which are small and round
to polygonal in shape. The cells secrete the hormone insulin. The
magnification is the same as 12.4.
12.7. Pancreas. Depletion of zymogen granules. 27-day-old
turkey. Group of ac ini w ith cells devoid of zymogen granules
are adj acent to acini wi th cells fill ed with eosinophilic zymogen
gra nul es. This pattern of normal ac ini alternating with zymogen-
depleted ac ini is fo und commonl y. This change is frequent in cases
of malnutrition.

I 12.6. Pancreas. 14-day-old broiler. The cytoplasm of the aci ni

inunediately around an islet is packed with zymogen gra nul es,
g iving the area deeply eosi nophilic appearance. The zymogen
gra nul es in the cytoplasm of other acini are less dense. This pattern
is com mon ly seen in the pancreas of chi ckens.
12.8. Pancreas. Depletion of zymogen granules. 3-week-old
turkey. Acinar cells are shrunken and almost completely devoid of
zymogen granules. The bird was small in size for its age and was
infecte d with Cochloso111a anatis.

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12.9. Pancreas. Depletion of zymogen granules. 3-week-old 12.11. Pancreas. Apoptosis. 39-day-old turkey. Higher-
quail. The acinar cells are almost completely depleted ofzymogen power view of 12.10 shows apoptotic acinar cells within vacuoles
granules. There is an apparent loss of acinar arrangement. (apoptotic vacuoles). The pink areas are zymogen granules that
remain in some surrounding acinar cells .

12.10. Pancreas. Apoptosis. 39-day-old turkey. Acinar cells

are severely depleted of zymogen granules, and there is widespread
apoptosis . Apoptotic cells appear as round, deeply basophilic bodies
within vacuoles (apoptotic vacuoles). This is a non-specific lesion
that may be found in birds with other disease conditions.
12.12. Pancreas. Atrophy. 18-day-old broiler. Acinar cells
lack zymogen granules and have ductular appearance rather than
glandular structures. Increased interstitial connective tissue with
some fibrosis is shown at a higher magnification in B. Bird was
from a flock with poor growth/uniformity and intestinal lesions
consistent with runting-stunting syndrome.
I
Avian Histopathology (4 th Edition) I 553
 Tal,seen Abdul-Aziz • Oscar J. Fletcl,er
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12.13. Pancreas. Atrophy. IO-month-old backyard chicken.
Low-power view shows severe atrophy of lobes of the pancreas.
There is marked thickening of the capsule.
12.15. Pancreas. Atrophy. 10-month-old backyard chicken.
Higher-power view of an area in 12. 14 demonstrates the replacement
ofacini by ductular structures separated by sparse amount of fibrou s
stroma. Note the small group of spared aci nar cells wi th zymogen
granul es in the lower right corner. T he identi ty of cells of ori gi n in
these ductular structures is uncerta in. It is also uncertain whether
these ductules represent regenerating aci ni .

I 12.14. Pancreas. Atrophy. IO-month-old backyard chicken.

Higher-power view of 12.13 shows loss of pancreatic acini and
replacement by ductular structures. There are two small collections
of spared pancreatic cells with zy mogen granules. Note th e
thickened capsule on the surface.
12.16. Pancreas. Atrophy. 10-month-old backyard chicken .
High-power view of area in 12. 15 shows the ductular structures and
th e lining cells, with interstitial fibrous stroma.

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12.17. Pancreas. Regenerating acini. 4-year-old backyard 12.19. Pancreas. Regional fibrosis. Over 3-year-old turkey.
chicken. Acini are replaced by ductular structures separated by Severe collagenous fibrosis of area in the pancreas. Only small
fibrous tissue. groups of atrophic acinar cells remain. This was an incidental
finding .

12.18. Pancreas. Regenerating acini. 4-year-old backyard

chicken. Higher-power view of area in 12.17. The acini are replaced
by irregularly shaped ductular structures separated by fibrous tissue
stroma. The origin of the cells that form these ductules is uncertain.
lt is also unce1tain whether these ductules represent regenerating
acini . This lesion is not etiology- or disease-specific but overall
12.20. Pancreas. Amyloid deposition. Swan. Amorphous
eosinophilic material (amyloid) effaces and replaces most of the
acini. The remaining acinar cells are individualized, shrunken and
lack acinar arrangement. The cytoplasm of many acinar cells is still
filled with zymogen granules, which give the cells the eosinophilic
appearance.
I
indicative of damage to the pancreas.

Avian Histopathology (4th Edition) I 555

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12.21. Pancreas. Amyloidosis. 3.5-year-old goose. Effacement 12.23. Pancreas. Acute pancreatic necrosis. 4-year-old Quaker
and replacement of a pancreatic islet by eosinophilic, amorphous parakeet. Section of pancreatic lobe shows severe necrosis of most
material consistent with amyloid. The bird had amyloid deposition of the pancreatic tissue. An area of the exocrine tissue appears viable
in other organs mad tissues. but has hemorrhages. Note the absence of inflammatory response.

I 12.22. Pancreas. Acute pancreatic necrosis. Quaker parakeet.

Lobes of the pancreas adjacent to the intestine are amorphous,
eosinophilic, and devoid of viable pancreatic tissue.
12.24. Pancreas. Acute pancreatic necrosis. 4-year-old Quaker
parakeet. Necrosis of the pancreatic tissue and the fat around it.
Note the few remaining basophilic-stained acini. The pathogenesis
of acute pancreatic necrosis is thought to be autodigestive process.
Proteolytic enzymes digest pancreatic tissue and damage blood
vessels resulting in hemorrhage and edema. Lipolytic enzymes also
cause necrosis of the fat around the pancreas.

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12.25. Pancreas. Acute pancreatic necrosis. 7-year-old African
gray parrot. Most of the pancreatic tissue is destroyed and replaced
by acellular eosinophilic material with hemorrhage. Only small
group of acini is spared.
12.26. Pancreas. Acute pancreatic necrosis. 7-year-old African
gray parrot. Another area of the same pancreas in 12.25 shows
destruction of pancreatic tissues and replacement by acellular
eosinophilic debris. Note the hemorrhages in the area.
Endocrine System
12.27. Pancreas. Copper toxicity. 13-week-old turkey breeder
replacement hen. Illustrated is one of multiple foci of coagulative
necrosis with mild hemorrhage in the pancreas. Copper toxicity in
the flock was due to feeding diet with copper level of 2000-2500
parts per million.
12.28. Pancreas. Copper toxicity. 13-week-old turkey breeder
replacement hen. Higher-power view demonstrates the coagulative
necrosis of acinar cells and extravasated e1ytlu·ocytes. I
Avian Histopathology (4 th Edition) I 557
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12.29. Pancreas. Adenovirus infection. 11-day-old broiler.
Large area of necrosis is characterized by loss of the pancreatic
tissue and replacement by cytoplasmic and nuclear debris.
12.31. Pancreas. Adenovirus infection. 2-week-old-old broiler.
Focal area of necrosis with some heterophilic infiltration involving
acinar tissue. Several acinar cells around the lesion contain large,
deeply basophilic, intranuclear inclusion bodies that are typical of
adenovirus inclusions. This bird had inclusion body hepatitis.

I 12.30. Pancreas. Adenovirus infection. 11-day-old broiler. This

high-power of view of area in 12.29 show several dark nuclei that are
enlarged and filled with basophilic inclusion bodies characteristic of
adenovirus infection.
12.32. Pancreas. Adenovirus infection. 23-day-old broiler.
Focal area of necrosis is characterized by replacement of pancreatic
tissues by eosinophilic debris. Intranuclear inclusion bodies are
present in the lesion.

558 I American Association of Avian Pathologists


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12.33. Pancreas. Adenovirus infection. 13-day-old-broiler.
Focal area of necrosis involving acinar tissue, with infiltration of
few heterophils. Large, deeply basophilic, intranuclear inclusion
bodies typical of adenovirus inclusions are present in acinar cells
around the necrotic lesion. This bird had inclusion body hepatitis.
12.34. Pancreas. Adenovirus infection. 23-day-old-old broiler.
Focal area of necrosis involving acinar tissues. Cells with large,
deeply basophilic, intranuclear inclusions that are typical of
adenovirus inclusions bodies were identified in the lesion. This bird
had inclusion body hepatitis.
E11docri11e System
12.35. Pancreas. Turkey viral hepatitis. 4-week-old turkey.
Multifocal, irregularly shaped areas of necrosis with infiltration
of small numbers of heterophils. The bird had liver lesions most
suggestive of turkey viral hepatitis.
12.36. Pancreas. Avian paramyxovirus type-1 infection.
Pigeon. Pancreatic tissue is disrupted by dense lymphocytic
infiltrates. Affected pigeons were displaying neurologic signs, and
tracheal swab was positive by PCR for avian paramyxovirus-1.
I
Avian Histopathology (4 th Edition) I 559
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12.37. Pancreas. Avian paramyxovirus type-1 infection.
Pigeon. Regionally extensive and severe disruption of pancreatic
tissue by dense lymphocytic infiltrates. Affected pigeons were
displaying neurologic signs, and tracheal swab was positive for
avian paramyxovirus-1 by PCR test.
I 12.38. Pancreas. Avian paramyxovirus-1 infection.
Area of severe necrosis of acinar cells.
Pigeon.
560 I American Association of Avian Pathologists
12.39. Pancreas - Avian paramyxovirus-1 infection. Pigeon.
Small focal area of necrosis is composed predominantly of necrotic
and apoptotic acinar cells. The bird was displaying neurologic
signs, and tracheal swab was positive for avian paramyxovi1ys- l
by PCR test.
12.40. Pancreas. Avian paramyxovirus-1 infection. Pigeon.
Area of severe disruption of the acini due to necrosis of acinar cells,
with light infiltration of inflammatory cells.
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12.41. Pancreas. Avian paramyxovirus-1. Pigeon. Area of 12.43. Pancreas. Avian encephalomyelitis. 15-day-old broiler.
necrosis of acinar cells with infiltration of mononuclear inflammatory Higher-power view of lymphoid infiltrates involving acinar tissues.
cells and few heterophils. .

12.42. Pancreas. Avian encephalomyelitis. 15-day-old broiler.

Multifocal areas of infiltration of acinar tissue by lymphoid cells.
The bird had brain lesions characteristic of avian encephalomyelitis,
and the causative virus was isolated from affected birds.
12.44. Pancreas. Avian encephalomyelitis. 15-day-old broiler.
Large encapsulated reactive lymphoid follicle (germinal center) in
the acinar tissue. The follicle is composed of large lymphoblast-like
cells, with many apoptotic cells.
I
Avian Histopathology (4 th Edition) I 561
 Tahseen Abdul-Aziz • Oscar J. Fletcher
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12.45. Pancreas. Avian encephalomyelitis. 15-day-old 12.47. Pancreas. Intraductal trematode. Screech owl. Higher-
broiler. Well-demarcated reactive lymphoid follicle composed of power view of 12.46 shows section of trematode within dilated
lymphoblast-like cells in the acinar tissue. The follicle is surrounded intralobular pancreatic duct.
by a ve1y thin fibrous capsule.

I 12.46. Pancreas. Intraductal trematode. Screech owl. Section

of trematode is within the lumen of distended interlobular pancreatic
duct.
12.48. Pancreas. Marek's disease. 5-month-old backyard
chicken. Area in the pancreas is effaced and replaced by a dense
population of pleomorphic lymphoid cells.

562 I American Association of Avian Pathologists


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12.49. Pancreas. Marek's disease. 5-month-old backyard
chicken. Another area in the same section of 12.48 Shows
effacement of most of th.e pancreatic acini in by pleomorphic
lymphoid cells.
12.50. Pancreas. Marek's disease. 5-month-old backyard
chicken. Same pancreas section as 12.49. Higher-power view
of demonstrates the pleomorphic population of lymphoid cells.
Several mitotic figures are present.
Endocrine System
12.51. Pancreas. Marek's disease. 5-month-old backyard
chicken. Same pancreas section as 12.49. Immunohistochemical
staining for CD3 shows that the vast majority of the lymphoid
cells are CD3-positive, indicating T-cell lymphoma. Only a few
lymphoid cells were positive for PAX5 , which is a B-lymphocyte
marker.
12.52. Pancreas. Adenoarcinoma of ovarian origin. 3-year-old
backyard chicken. Focal carcinomatous lesion in the pancreas.
The bird had ovarian adenocarcinoma. Carcinoma of the ovary
almost always involves the pancreas.
I
Avian Histopathology (4 th Edition) I 563
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12.53. Pancreas. Adenocarcinoma of ovarian origin. 3-year-
old backyard chicken. Large area in the pancreas is replaced by
carcinoma. The bird had very extensive coelomic carcinomatosis
involving the mesentery, pancreas, serosal surface of the intestine
and proventriculus and gizzard, peritoneal septa, and visceral
ligaments.
12.55. Pancreas. Adenocarcinoma of ovarian ongm. 3-year-
old backyard. Neoplastic embolus fills the lumen of a blood vessel
in the pancreas of this chicken with ovarian adenocarcinoma. This
is an unusual lesion, as metastasis of the ovarian adenocarcinoma to
the pancreas usually occurs by intracoelomic implantation.

I 12.54. Pancreas. Adenocarcinoma of ovarian origin. 3-year-

old backyard. Higher-power view of the ovarian adenocarcinoma
in 12.53.
12.56. Thyroid gland. Normal. 8-week-old chicken. This figure
illustrates the close anatomical relationship between the thymus,
thyroid gland, and parathyroid gland .

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12.57. Thyroid gland. Normal. 15-week-old turkey breeder
replacement hen. Illustrated is the close anatomical relationship of
the thyroid gland to the thy1pus.
12.59. Thyroid gland. Normal, quiescent. LS-year-old
backyard chicken. Higher-power view. Thyroid follicles are filled
with colloid and lined by flattened epithelial cells. Note the blood
capillaries within the scant interfollicular connective tissue stroma.
These follicles are considered quiescent (inactive) follicles.

I
If
•I I

12.58. Thyroid gland. Normal. 1.5-year-old chicken. Thyroid

follicles are large, lined with flattened epithelium, and filled with
eosinophilic colloid. Interfollicular connective tissue is scant and
contains blood capillaries.
12.60. Thyroid gland. Normal, active. 15-day-old chicken.
Thyroid follicles are round, smaller in size compared to those
in 12.59, lined with low cuboidal epithelial cells, and filled with
eosinophilic colloid. These follicles are considered active.
I
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12.61. Thyroid gland. Normal, active. 14-day-old turkey. The
thyroid follicles are lined by cuboidal epithelial cells with large
nuclei and blebs on the apical surface. The colloid is ve1y thin
and vacuolated. This appearance is characteristic of active thyroid
gland.
12.63. Thyroid gland. Follicular atrophy. 20-day-old-broiler.
Thyroid follicles are small and lined by low cuboidal epithelial
cells. Many follicles are devoid of colloid and appear as nests of
cells without lumen.

I 12.62. Thyroid gland. FoJlicular atrophy. 20-day-old broiler.

Thyroid follicles are small and many of them appear totally
collapsed.
12.64. Thyroid gland. Focal foJJicular atrophy. 5-year-old
backyard chicken. There is atrophy of group thyroid follicles.

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12.65. Thyroid gland. Focal follicular atrophy. 5-year-old
backyard chicken. Higher-power view of atrophic follicles in
12.64. Some follicles haye small or barely discernible lumens,
while others lack lumens and appear as small clusters of cells. This
was incidental finding in backyard chicken.
12.66. Thyroid. Amyloidosis. Duck with mycobacteriosis.
Deposition of amorphous eosinophilic material (amyloid) causes
expansion of the interfollicular spaces.
Endocrine System
12.67. Thyroid gland. Follicular cyst. Chukar partridge.
Follicle is dilated, lined by flattened epithelial cells, and filled with
colloid.
12.68. Thyroid gland. Non-cancerous cyst. One-year-old
chukar partridge. Large colloid-filled cystic space replaces most
of the thyroid follicles. Thin rim of normal, non-adenomatous
thyroid tissue (follicles) surrounds the cystic space.
I
Avian Histopathology (4 th Edition) I 567
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12.69. Thyroid gland. Follicular cyst. 65-week-old broiler
breeder male. Large cyst lined by flattened epithelial cells is
located beneath the capsule of this thyroid gland. There is some
compression of adjacent thyroid tissue.
12.71. Thyroid gland. Follicular cyst. 5-year-old backyard
chicken. Higher-power view of area in 12.70 showing the clefts
in the colloid, the single layer of follicular epithelial cell lining th e
cyst, and the interstitial lymphocytic infiltrate in the surrounding
thyroid tissue.

I 12.70. Thyroid gland. Follicular cyst. 5-year-old backyard

chicken. Large cyst is filled with colloid and lined by a single
layer of well-differentiated follicular epithelium. Acicular shaped
clefts (possibly of cholesterol) are in the colloid of the cyst. The
surrounding thyroid tissue contains interstitial lymphocytic infiltrate.
12.72. Thyroid gland. Lymphocytic thyroiditis. 65-week-old
broiler breeder male. Multiple nodular to diffuse collections of
lymphocytes are replacing follicles.

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12.73. Thyroid gland. Lymphocytic thyroiditis. 65-week-old
broiler breeder male. Higher-power view of an area in 12.72
showing the replacement o,f normal thyroid tissue by lymphocytes.
There is small area of papillary hyperplasia in the wall of follicle
(arrow). Within the box is follicle containing heterophils.
12.74. Lymphocytic thyroiditis. 65-week-old broiler breeder
male. Expansion of interfollicular tissue and effacement and
compression of follicles ofby dense lymphocytic infiltrate. Papillary
projection into the lumen of follicle is shown (arrow). These lesions
were not associated with clinical signs of disease.
Endocrine System
12.75. Thyroid gland. Papillary hyperplasia. 65-week-old
broiler breeder male. Proliferation of glandular epithelium results
in papillary projection (airnw) into the colloid-filled gland. Insert
shows the orderly arranged epithelial cells.
12. 76. Thyroid gland. Papillary hyperplasia. 65-week-old
broiler breeder male. Adenomatous changes are in several
follicles, with more extensive cellular proliferation replacing
colloid. An affected follicle is enlarged, contains blood, and
compresses adjacent thyroid tissue. This was an incidental finding
not associated with evidence of clinical disease in the chicken.
I
Differentiation between hyperplasia and adenoma is difficult.
Avian Histopathology (4 th Edition) I 569
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12.77. Thyroid gland. Papillary hyperplasia. 65-week- old 12.79. Thyroid gland. Follicular hyperplasia (hyperplastic
broiler breeder male. Higher-power view of area in 12.76 goiter). Pigeon. Higher-power view showing the papillary
illustrates the adenomatous changes in follicles and the relatively projections in the lumen of one follicle. Illustrated also are the
orderly arrangement of epithelial cells. cuboidal and low colunmar epithelial cells lining the follicles.

I 12.78. Thyroid gland. Follicular hyperplasia (hyperplastic

goiter). Pigeon. Numerous follicles are lined by cuboidal or low
columnar epithelial cells and lack colloid. Follicular lumens are
obliterated in some follicles. Note the papillary projection in the
lumen of one follicle.
12.80. Thyroid gland. Colloid goiter. 6-year-old backyard
chicken. Scanning view of the left and right thyroid gland
demonstrating the size of the glands. Grossly, both thyroid glands
were markedly enlarged, measuring about 16 x 12 111111 .

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12.81. Thyroid gland. Colloid goiter. 6-year-old backyard 12.83. Thyroid gland. Colloid goiter. 6-year-old backyard
chicken. The goiterous glands consist of many variably sized and chicken. The follicles are lined with flattened or low cuboidal
shaped follicles filled with ,colloid. epithelium.

12.82. Thyroid gland. Colloid goiter. 6-year-old backyard

chicken. Higher-power view of an area in 12.81.
12.84. Thyroid gland. Colloid goiter. 6-year-old backyard
chicken. Higher-power view to show the low cuboidal and flattened
epithelium lining follicles . I
Avian Histopathology (4 th Edition) I 571
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12.85. Thyroid gland. Colloid goiter. 6-year-old backyard
chicken. Focal area of follicular hyperplasia . Follicles are small
and the lining epithelium is hyperplastic. Foci of follicular cell
hyperplasia may be seen in thyroid glands with colloid goiter.
12.87. Thyroid gland. Goiter. Budgerigar. Thyroid follicles are
markedly distended and contain colloid-like material, fibrin , red
blood cells, and hemosiderin-laden macrophages. Note the papilla1y
projection in the lumen of a dilated follicle (see 12.90 for higher-
power view of the papillary projection). (Glass slide courtesy of
Panayiotis Lo11kopo11los).

I 12.86. Thyroid gland. Mixed goiter (hyperplastic and colloid

goiter). Adult dove. Proliferation of the follicular epithelium
results in obliteration of some follicular lumens. Some follicles
show small lumen with or without colloid. Other follicles are
dilated, irregularly shaped, lined by cuboidal or flattened epithelium,
and filled with thyroid colloid.
12.88. Thyroid gland. Goiter. Budgerigar. Dilated follicle
contains e1ytluocytes, fibrin, and hemosiderin-laden macrophages.
(Glass slide co urtesy of Panayiotis Lo11kopo11los).

572 I American Association of Avian Pathologists

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12.89. Thyroid gland. Goiter. Budgerigar. Numerous 12.91. Thyroid gland. Goiter. Budgerigar. Sheet ofhyperplasti c
hemosiderin-laden macrophages and some erythrocytes are in fo llicular epithelial cells with numerous hemosiderin-laden cells
the lumen of dilated follic,le. (Glass slide courtesy of Panay iotis projects into the lumen of the follicle. Proteinaceous material, some
Loukopoulos). erythrocytes, and hemosiderin-laden cells are in the lumen. (Glass
slide courtesy of Panayiotis Loukopoulos).

,..
.... .. . .
· , . : ... It

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12.90. Thyroid gland. Goiter. Budgerigar. Simple papillary
projection extends from the inner surface of the a dilated follicle into
the lumen. The projection has fibrous stalk, sheet of hyperplastic
follicular epithelium, and hemosiderin-laden macrophages. There
is some proteinaceous material. (Glass slide courtesy of Panayiotis
Loukopoulos) .
12.92. Thyroid gland. Goiter. Budgerigar. Higher-power view
of the papillary projection in 12.91 demonstrating the sheet of
hyperplastic follicular epithelial cells that projects into the follicular
lumen. Note the numerous hemosiderin-laden cells. (Glass slide
courtesy of Panayiotis Loukopoulos).
I
Avian Histopathology (4 th Edition) I 573
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12.93. Thyroid gland. Adenoma. 7-week-old cockatiel. The
normal thyroid architecture is distorted due to marked proliferation
of follicular epithelium that appears columnar and shows evidence
of papillary growth. Remaining follicles contain vacuolated colloid.
12.95. Thyroid gland. Lymphoid leukosis. Backyard chicken.
There is focal area of dense infiltrate of monomorphic population of
large cells morphologically consistent with lymphoblasts. Several
mitotic figures are recognized among the lymphoid cell population .
The birds had lymphoid leukosis tumors in other tissues.

I 12.94. Thyroid gland. Adenoma. 7-week-old cockatiel. Another

area of the same thyroid in 12.93 showing the compression of
thyroid follicles at the periphery of the adenoma. Large numbers of
hemosiderin-laden macrophages are at the margin of the neoplasm
and some are within the lumen of dilated follicle.
12.96. Parathyroid gland. Normal. 40-day-old Broiler.
Illustrated are two parathyroid glands and their close relationship to
the thyroid gland. The parathyroid glands are embedded in adipose
tissue. Note the thin strand of fibrous tissue between the two glands.

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12.97. Parathyroid gland. Normal. 3-year-old backyard 12.99. Parathyroid gland. Normal. 30-week-old broiler breeder
chicken. Illustrated is the close anatomical relationship between hen. Higher-power view of nonnal parathyroid gland showing
the parathyroid and the thyroid glands. The parathyroid gland is cords of chief cells separated by the delicate vascular interstitial
well encapsulated by fibrous tissue. connective tissue.

12.98. Parathyroid gland. Normal. 30-week-old broiler breeder

hen. Cords of cells (chief cells) are separated by thin strands of
fibrous tissues containing numerous blood capillaries.
12.100. Parathyroid gland. Normal. 40-day-old broiler. Cords
of cells (chief cells) are separated by small amounts of fibrous tissue
containing numerous blood capillaries. Note the fibrous capsule on
the surface of the gland.
I
Avian Histopathology (4 th Edition) I 575
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12.101. Parathyroid gland. Hyperplasia. 4-week-old broiler
breeder male. Marked hypertrophy and hyperplasia of the chief
cells, with more or less preservation of the cord arrangement of the
cells. Grossly, both parathyroid glands looked enlarged. This bird
was affected with rickets.
12.103. Parathyroid gland. Hyperplasia. 4-week-old broiler
breeder pullet. Hypertrophy and hyperplasia of the chief cells are
evident. There is variation in the size ofnuclei. Note the vacuolation
of some cells.

I 12.102. Parathyroid gland. Hyperplasia. 12-week-old

backyard chicken. Hypertrophy and hyperplasia of the chief
cells are the key histological features of parathyroid hyperplasia.
Note that the cord-like arrangement of the cells is still somewhat
recogni zable. Grossly, both parathyroid glands were enlarged. This
bird was affected with osteomalacia.
12.104. Parathyroid gland. Hypertrophy. 3-year-old duck.
The chief cells are enlarged and have markedly vacuolar cytoplasm
and enlarged nuclei. Chief cell hypertrophy indicates increase in
the gland activity.

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12.105. Parathyroid gland. Hypertrophy. 3-year-old duck.
Higher-power view demonstrating the hype11rophic chief cells with
markedly vacuolar cytopla~m and enlarged nuclei that show some
pleomorphism.
12.106. Parathyroid gland. Cystic adenoma. 27-week-
old broiler breeder. Cyst with papillary projections occupies
a relatively large pat1 of this parathyroid gland. The smaller
cyst and adjacent cells outlined by the box are shown at a higher
magnification in the insert.
E11docri11e System
12.107. Parathyroid gland. Water-clear varia nt adenoma.
12-year-old parrot. Parathyroid tissue is replaced by a
circumscribed, thin-capsulated nodule composed of cells with clear-
appearing cytoplasm. Rim of compressed parathyroid tissue is seen
on the left side of the nodule, just beneath the thyroid gland.
12.108. Parathyroid gland. Water-clear variant adenoma.
12-yearold parrot. Higher-power view of area in 12.107. The
cells have severely vacuolated cytoplasm and are arranged in nests
separated by delicate fibrovascular stroma.
I
Avian Histopathology (4 th Edition) I 577
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12.109. Parathyroid gland. Water-clear variant adenoma.
12-year-old parrot. Higher-power view of area in 12.108. The
cytoplasm of the cells is severely vacuolated and shows only fine
eosinophilic strands. The nuclei are dark and small and show
minimal pleomorphism.
12.111.Adrenal gland. Lipofuscinosis. Duck. The cytoplasm of
co11ical cells is filled with brown, finely granular lipofuscin pigment.
The pigment was negative for iron with the Prussian blue stain.

I 12.110.Adrenal gland. Normal. 9-week-old chicken. Cortical and

medullary tissues are intermingled. The cortical tissue is composed
of groups of co11ical (interrenal) cells with eosinophilic, granular,
finely vacuolated, lipid-containing cytoplasm. The medullary tissue
consists of groups and strands of medullary ( chromaffin) cells that
have distinctly basophilic cytoplasm.
12.112.Adrenal gland. Lipofuscinosis. Duck. The granular
lipofuscin pigment in the cytoplasm of cortical cells stains brownish
purple with PAS stain.

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12.113.Adrenal gland. Fatty vacuolation. 15-year-old African
gray parrot. Microvesicular and macrovesicular vacuolation of the
cortical cells. Note that th~ medullary cells are not vacuolated.
12.114.Adrenal gland. Fatty vacuolation. 15-year-old African
gray parrot. Microvesicular and macrovesicular vacuolation of
the cortical cells. The cytoplasmic vacuoles are morphologically
consistent with lipid vacuoles (fatty vacuolation). The bird had
hepatic lipidosis and severe atherosclerosis of the great arteries of
the heart. Note that the medullary cells are not vacuolated.
Endocrine System
12.115.Adrenal gland. Fatty vacuolation. 15-year-old African
gray parrot. Higher-power view showing the macrovesicular and
microvesicular fatty vacuolation of cortical cells.
12.116.Adrenal gland. Amyloidosis. Duck with mycobacteriosis.
Amorphous, eosinophilic material (amyloid) replaces adrenal
tissue. Many of the remaining cortical and medullary cells are in
small groups and appear disrupted.
Avian Histopathology W' Edition) I 579
 Tahseen Abdul-Aziz • Oscar J. Fletcher
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12.117.Adrenal gland. Marek's disease. infiltration ofmedullary
areas with pleomorphic lymphoid cells. This bird had lymphoid cell
infiltrates in other organs and tissues.
12.119.Pituitary gland. Carcinoma. Cockatiel. This is a section
of tumor in the orbit that caused bilateral exophthalmia . The tumor
consists of lobules of fairly uniform cells separated by thin strands
of connective tissue stroma. The cells appear round to polygonal
in shape with scant cytoplasm and large, round nucleus with single
prominent nucleolus.

I 12.118.Pituitary gland. Normal. Turkey. Illustrated is the

location of the pituitaiy gland in the floor of the cranial cavity and its
close association to the brain being just beneath the diencephalon.
The insert shows higher magnification of the cord-like arrangement
of cells.
12.120. Pituitary gland. Carcinoma. Cockatiel. Higher-power
view showing giant cells with large, bizarre, deeply basophilic
nuclei.

580 I American Association of Avian Pathologists

VetBooks.ir
CHAPTER
Reproductive System
H . John Barnes • Oscar J. Fletcher • Tahseen Abdul-Aziz
The normal histology of reproductive tissues varies considerably
depending on the age of the bird, season of the year, and light cycle
to which the bird is exposed. In egg laying females, daily changes
result from follicles that develop and mature, ovulation, follicu-
lar atresia, cyclical discharge and replenishment of albumen, and
production of the shell and its membrane by glands in the oviduc-
tal mucosa. To interpret pathology of the reproductive system, it
is essential to be familiar with the range in variation that occurs
in the normal histology of the reproductive organs . Both normal
physiologic cycles and disease processes can initiate degenerative
changes, referred to as atresia, atrophy, regression, or involution,
that are indistinguishable microscopically. Accurate interpretation
of degenerative changes requires know ledge of the overall status of
the bird and its health. Some normal processes result in changes
that could be interpreted as pathologic. During ovulation, bleeding
can occur if small vessels in the follicular wall are ruptured, and it
is common to find heterophils and later, foamy macrophages in the
post-ovulatory follicle . This normal "physiologic" inflammation
should not be interpreted as oophoritis or folliculitis in the absence
of more definitive lesions.
Male Reproductive Tract
Anatomy and Histology
Paired testes, typically unequal in size and shape, are located inter-
nally on either side of the midline near the cranial divisions of the
kidney and caudal to the lungs. Seminiferous tubules from each
testis connect with tubules in the epididymis located dorsally and
medially, where spermatozoa are stored and undergo maturation.
The ductus deferens continues from the epididymal duct in a tight
zigzag pattern parallel to the ureter along the surface of the kidney to
enter the cloaca. Additional sperm storage is provided by the ductus
deferens. There are no accessory sex glands . Only a few types of
birds have a well-developed (intromittent) phallus (e.g. , waterfowl,
ratites, etc .) that extends from the vent during copulation, otherwise
the phallus is merely a protuberance in the proctodeum on the ven-
tral margin of the vent. Tumescence of the phallus during copula-
tion results from rapid filling of lymph channels within the organ.
Microscopically, avian testes consist of a thin, but tough, fi-
brovascular covering (tunica a/buginea) , and numerous convoluted,
interconnected seminiferous tubules. Avian testes lack septa and a
111ediastin11m testis. In the immature testis, seminiferous tubules are
13
small, widely separated by interstitial tissue, and lined by a single
layer of spermatogonia and Sertoli (sustentacular) cells. Spermato-
genesis progressively develops as the bird ages. By sexual maturity,
seminiferous tubules have markedly increased in size and are lined
by columns of cells that have initiated production of spermatozoa
( spermatogenesis ).
From the basement membrane to the lumen of the seminifer-
ous tubules, spermatogenic columns consist of spermatogonia, pri-
mary spermatocytes, secondary spermatocytes, early spermatids,
and late spermatids. Mitotic figures may be numerous among the
more immature cells. Cells decrease in size and increase in staining
as they differentiate to form spermatozoa. Recognition of specific
cell types may not be possible, but a gradient of cells from the basal
germinal layer to the lumen should be apparent. Sertoli cells are in-
terspersed between the columns of spermatogenic cells. They can
be identified by their larger, pale-staining, vesicular nucleus with
prominent nucleolus, and abundant cytoplasm that streams toward
the lumen. Groups of late spermatids, attached by their heads to
Sertoli cells, appear as tufts on the epithelial surface. These Se11oli
cell/ late spermatid complexes are where maturation of late sperma-
tids to spermatozoa occurs. Spermatozoa are present in the lumen,
but their numbers are variable among tubules and they may not
be numerous even in a fully fertile male. Paradoxically, retention
of late spermatids and spermatozoa by Sertoli cells leads to high
numbers in the seminiferous tubules, which results in a reduction
in the number and concentration of spermatozoa in semen, and low
fertility in roosters .
Spermatozoa produced in the seminiferdus tubules of the
testis pass through the following structures to reach the cloaca:
straight tubules of the testis, rete testis that bridges the testis and
epididymis, efferent ducts, connecting ducts, and epididymal duct
within the epididymis, ductus deferens, and ejaculatory duct.
Each of these passageways has a characteristic structure and can
be recognized histologically. Straight tubules are within the testis,
lack spermatogenic cells, and are lined by Sertoli cells. Channels
I
within the rete testis lie between the testis and epididymis, external
to the tunica albuginea. They are large and lined with a simple
squamous to cuboidal epithelium. Within the epididymis, the epi-
thelium of efferent ducts is arranged in folds and consists of simple
cuboidal to columnar non-ciliated cells with focal areas of ciliated
pseudostratified epithelium. Non-ciliated epithelial cells of the
efferent ducts are capable of phagocytizing spermatozoa (spermi-
ophagy) and other particulates. Variable numbers of macrophages
Avian Histopathology (4' h Edition) I 581
 H. John Ba mes • Oscar J. Fletcher • Tahseen Abdul-Aziz
commonly found in the rete testis and efferent ducts are capable
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of retrograde movement into the seminiferous tubules where they
remove cells sloughed during degeneration. Efferent duct epithe-
lial cells often contain a light brown pigment. Connecting ducts
and the epididymal duct are lined with a secretory pseudostrati-
fied columnar epithelium. There are sparse cilia in the connecting
ducts and a lack of cilia in the epididymal duct. Size also helps
distinguish the different ducts within the epididymis; connecting
ducts are the smallest, the epididymal duct is the largest, and ef-
ferent ducts are variable. Epididymal ducts are filled with mature
spermatozoa in normal adult males. Blind (aberrant) ductules also
are present in the epididymis and may extend into the adjacent
adrenal gland. The ductus deferens continues from the epididymal
duct and has a similar histologic appearance - pseudostratified,
non-ciliated epithelium and numerous spermatozoa in the lumen.
It enlarges, and is surrounded by smooth muscle that increases in
thickness along its length . The ejaculatory duct extends from the
ductus deferens, through the cloaca! wall , and opens on a small,
conical papilla in the urodeum of the cloaca. Occlusion at any
point in the tubular system, either internally by blockage or exter-
nally by compression, leads to stasis and formation of semen-filled
tubular dilations (spermatoceles). If the stasis is prolonged or se-
vere, a sperm granuloma may result.
In mature functional testes, interstitial tissue is thin, barely sep-
arating the seminiferous tubules. Infrequently, individual or small
groups of interstitial (Leydig) cells can be identified in the intersti-
tium, usually where tubules come together and interstitial space is
greater. They are flattened to angular cells with a granular orange-
red cytoplasm on H&E staining. The cytoplasm may be vacuolated.
Interstitial cells are readily apparent in immature testes in which
the seminiferous tubules have not sta11ed to expand . Small foci of
granulocytic cells, probably extramedulla1y hematopoietic cells, are
occasionally seen in the interstitium of immature testes. In mature
testes, occasional small lymphoid foci are located in the intersti-
tium. Even though they are conunonly seen, they are likely abnor-
mal as there is no known physiologic purpose for such cells in this
location. The testis-blood barrier makes the testis an immunologi-
cally privileged tissue. More than a few small interstitial lymphoid
foci shotdp be interpreted as i11terstitial lyniphocytic orchitis, espe-
cially if there are concurrent changes in adjacent seminiferous tu-
bules. Variable amounts of melanin in the testes occur in the tunica
albuginea and interstitial tissues ofmelanistic birds (e.g., cockatoos,
silkie chickens) that have pigmented skin. The testes, especially on
the left side, are intimately associated with the adrenal glands. It is
normal to find adrenal tissue within the testis.
Degeneration
I
Testicular degeneration (atrophy, regression, involution) is charac-
teri zed by a decrease in the size of the testes . When the condition
is advanced, the testes are small, firm , and yellow. Both testes
tend to be involved, but the degree of atrophy may not be equal or
uniform . The epididymis is also affected, but the change is not as
apparent, resulting in it appearing larger than expected relative to
the small testis. If the testis is pigmented, the color intensifies as
atrophy progresses.
582 I American Association of Avian Pathologists
Microscopically, seminiferous tubules decrease in size and
there is a relative increase in interstitial tissue. Absolute inter-
stitial fibrosis occurs in advanced lesions. Germinal epithelium
of the seminiferous tubules is disorganized, spermatogenic col-
umns are no longer evident, and sloughing of degenerating and
necrotic spermatogenic cells results in increased cells, including
macrophages (spermiophages), within the seminiferous tubules.
Spermatozoa and spermatids undergo degeneration, necrosis, and
may be engulfed by phagocytic cells. Spermatidic giant cells with
condensed pyknotic or fragmented nuclei can be seen, and are a
hallmark of testicular degeneration. As the process continues,
sloughed cells are removed, leaving only the basal germinal layer
composed of Sertoli cells and spermatogonia. In extreme cases,
only cuboidal to columnar Sertoli cells line the tubules. Spermato-
zoa are no longer present in seminiferous tubules, but usually can
be found in the tubules of the epididymis mixed with degenerating
or necrotic spermatogenic cells, spermiophages, and spermatidic
giant cells from the testis. Pigmented cells also are commonly
found within the epididymal tubules . Similar pigmented cells are
located in the tubular epithelium; possibly the ones in the lumen
are cells that have sloughed as part of the degenerative process.
Regressive changes occurring in the testis are mirrored in the epi-
didymis. Inflammatory changes in either the testis or epididymis
are not a feature of degeneration.
Testicular and epididymal atrophy can have a multitude of
causes. It may result from normal seasonal involution or be an indi-
rect result of any adverse or debilitating condition, e.g. , starvation,
chronic infections, malnutrition, etc. Specific causes of testicular
degeneration include vitamin E deficiency and toxicities e.g. , lead,
cadmium, selenium, mycotoxins, etc. Even in these cases, the pos-
sibility that the systemic effects of the toxicity contributed more to
testicular degeneration than a direct toxic effect cannot be entirely
excluded. Several insecticides, herbicides, endocrine disrupters or
mimics, estrogenic and other environmental chemicals cause testic-
ular degeneration, especially in quail, which are frequently used as
the avian target species for toxicity testing. Surgical removal of the
pituitary gland, ligation of the bile duct, vasoligation, incomplete
castration, and hypothyroidism are experimental methods that result
in testicular degeneration.
Cystic testicular degeneration occurs in young birds because
of excess salt intake, furazolidone toxicity, or phosphorus de-
ficiency (unpublished), and is characterized by greatly enlarged
testes that have extensive fluid accumulation in the seminiferous
tubules. Enlargement of the heart is also seen in salt and fura -
zolidone toxicity. Both testes are variably affected. Microscopi-
cally, immature seminiferous tubules are distended with fluid but
are otherwise normal. As tubules continue to expand with fluid ,
the epithelium becomes flattened and there is a relative decrease in
interstitial tissue. lfthe cause is removed, the testes return to nor-
mal size by the time of sexual maturity, but focal areas of abnor-
mal dilated tubules persist and are found microscopically. Simple
cysts also can occur in the testes of adult birds, but they are not
common. They develop within seminiferous tubul es, have a con-
nective tissue capsule, are lined by a simple squamous to cuboidal

epithelium, and compress adjacent tissue causing atrophy. Mul-
tiple cysts are common in affected testes.
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Orchitis and Epididymitis
Bacterial orchitis is intratubular and occurs sporadically in adult
males. One or both testes may be affected. Inflammation of the
epididymis typically accompanies orchitis (epididymo-orchitis).
Affected testes are enlarged, firm , discolored, and have an irregu-
lar shape, vascular pattern, and areas of discoloration. Extensive
necrosis of seminiferous tubules and exudation are apparent on
cut surface. Salmonella, E. coli, Pasteurella, Gallibacterium, and
Staphylococcus are recognized causes of bacterial orchitis in birds.
Infection may result from ascending infection via the ductus defer-
ens, analogous to salpingitis in females, hematogenously as part ofa
systemic infection, or by extension from lesions in adjacent tissues,
especially air sacs that invest the testes.
Microscopically, the tubular architecture of the testis is pre-
served but there is extensive necrosis of seminiferous epithelium,
with fibrinoheteropbilic infiltration of the affected tubules and
adjacent interstitium. Ma~rophages and giant cells increase with
time. Intralesional bacterial colonies are numerous. Granuloma-
tous orchitis is caused by mycobacteria and can be recognized by
characteristic histiocytic granulomas. It occurs in companion and
free-living birds, but has not been reported in poultry.
Orchitis and epididymitis are among the lesions of systemic
Chlamydia infections in turkeys and companion birds. Affected
tubules are filled with eosinophilic exudate composed of fibrin, ne-
crotic epithelial cells, and inflammato1y cells. Testicular lesions are
useful in distinguishing chlamydiosis from mycoplasmosis, which
appears otherwise similar. Ruptured testicular blood vessels fre-
quently caused death of experimentally infected turkeys.
Interstitial lymphocytic orchitis, degeneration of seminiferous
epithelium, and atrophy occur in the testes of ducks following infec-
tion with Tembusu virus, a Flavivirus.
Epididymal Lithiasis
Epididymal lithiasis is characterized by calculi in the efferent
ducts of the epididymis, atrophy of seminiferous tubules, and lym-
phoid infiltration in the interstitial tissues of the epididymis. It is
common and a significant cause of decreased fertility in roosters
as they age. Only roosters are affected -- calculi have not been
found in epididymides from turkeys, quail, pigeons, ducks, or 21
species of free-living birds . Initially, aggregates of spermatozoa,
cell debris, and macrophages occlude the lumen of efferent ducts
in the epididymis and the duct epithelium becomes vacuolated.
Intraluminal masses continue to expand and undergo mineraliza-
tion, ducts become cystic, and the epithelium is compressed and
may undergo focal erosion. Lymphoid infiltrates containing small
numbers of plasma cells and macrophages develop in the intersti-
tial tissues, especially around tubules in which the epithelium has
been compromised and the luminal mass has come in direct con-
tact with interstitial tissues. Over time, testicular atrophy and de-
generation of the spermatogenic epithelium in some of the testicu-
lar seminiferous tubules occur. The cause of epididymal lithiasis
is unknown. An association with prepubertal infection with infec-
Reproducthie System
tious bronchitis virus, including vaccine strains, has been shown ,
but spontaneous cases in the absence of infection with the virus
also occur, albeit less frequently. Current information suggests
expression of proteins needed to reabsorb calcium from the effer-
ent ducts is deficient.
Goose Venereal Disease
The relatively large intromittent phallus and adjacent cloaca of the
gander becomes severely inflamed in goose venereal disease. Acute
inflammation of the cloaca! mucosa and phallus begins as a small
erosion at the tip or base of the phallus, followed by an enlarging area
of ulceration and necrosis. In severe cases, the process spreads to
involve the entire phallus and adjacent tissues, and there is necrosis
and gangrene that may lead to loss of the tip of the phallus. Affected
flocks experience increased mortality and decreased fertility. Micro-
scopically, acute inflammatory changes are followed by ulceration
and infiltrates composed of heterophils, mononuclear cells, macro-
phages, giant cells, and heterophilic granulomas. Intralesional Can-
dida and bacteria may be present. The cause of goose venereal dis-
ease is uncertain, but Neisseria, Mycoplasma, Candida, and a variety
of other bacteria have been isolated from the lesions. Subsequent
traumatic myiasis caused by Woh/fahrtia can be a complication.
Neoplasia
Tumors in the testes are uncommon to rare. However, neoplasms
that may be found include Marek's disease, lymphoid leukosis, my-
eloid leukosis, seminomas, teratomas, Sertoli cell tumors, and inter-
stitial cell tumors. Marek's disease, lymphoid leukosis, and myeloid
leukosis can be recognized by interstitial infiltrates of a population
of pleomorphic lymphocytes, uniform population of large lympho-
blasts, or immature granulocytes, respectively. Seminiferous tu-
bules are usually intact but compressed and atrophic. Diffuse to
focal tumors are present in a variety of other tissues.
Seminomas and teratomas arise from the germinal epithelium
ofseminiferous tubules and are classified as germ cell tumors. Typi-
cally, they are benign, but malignant forms with metastases to other
organs occur. Seminomas are usually unilateral, rarely bilateral.
Affected testes are diffusely enlarged, have a thick capsule, and dif-
fer little from a nonnal testis in color and consistency. The contra-
lateral testis is usually normal. Well differentiated seminomas have
a recognizable tubular pattern reminiscent of a normal testis, but
large round to polyhedral cells with eosinophilic cytoplasm and a
prominent, round, often eccentric, nucleus with a prominent nucleo-
lus, replace the germinal epithelium. Normal and abnormal mitotic
figures are common and bizarre multinucleated cells are occasion-
ally seen. Cells in poorly differentiated or malignant seminomas are
similar but occur as sheets or clusters separated by a fine connec-
tive tissue stroma. Invasion of adjacent tissues or distant metastases
are features of malignant seminomas. Teratomas are recognized
microscopically by the presence of a complex variety of otherwise
normal tissues that arise from more than one primordial germ layer.
They are rare. Grossly, they tend to be large, nodular, have a thick
capsule, and contain multiple cysts. Teratomas have been induced
experimentally by injecting actively sperm-producing testes with
I
cadmium, copper, or zinc.
Avian Histopathology (4 th Edition) J 583
 H. Joh11 Bames • Oscar J. Fletcher • Tahsee11 Abdul-Aziz
Sertoli cell tumors and interstitial cell tumors are sex cord/go-
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nadostromal tumors of the testis. Sertoli cell tumors are usually
unilateral, lobulated, gray white to white, and firm. Atrophy of the
contralateral testis frequently occurs. Tubules within a discrete en-
capsulated tumor lined with fairly uniform cuboidal to columnar
cells and separated by thin to dense fibrovascular stroma, are seen
microscopically. Within tubules, cells are usually elongated, ori-
ented perpendicular to the basement membrane, and have a basal
nucleus and abundant eosinophilic cytoplasm that may be finely
vacuolated. Diffuse sheets without a tubular architecture are seen in
some tumors. Se1toli cell tumors also can develop in the epididymis
and ovary. Se1toli cell nodules (adenomas) are seen occasionally
in the testes and epididymides of egg-laying roosters. They are cir-
cumscribed clusters of tubules lined by well-differentiated Sertoli
cells surrounded by a fibrous capsule. In the testis, they are usually
compressed and found adjacent to the tunica albuginea. Interstitial
cells are angular and have an orange-red cytoplasm that may be vac-
uolated. Occasionally they are seen as small clusters associated with
other testicular tumors. Interstitial cell tumors have been reported
in companion birds, but not in poultry.
Female Reproductive Tract
Introduction
Compared to the female reproductive tract of mammals, the re-
productive tract of most female birds, including poult1y, is much
reduced, consisting of just a single left ovary, oviduct, and short
muscular vagina. Birds occasionally have paired ovaries, but even
when present; the right ovaiy may not actually be functional. Birds
rarely have paired oviducts. Fu nctioning of the reproductive tracts
of mammals and birds is also profoundly different. Internal devel-
opment of the mammalian emb1yo/fetus requires a constant nurtur-
ing environment, while external development of the avian emb1yo
requires everything the embryo needs to be provided within the egg.
This includes maternally derived antibodies (IgG), which are trans-
ferred from the circulation of the hen to the yolk of the developing
oocyte in the ovaiy. Thus, the avian reproductive tract is predomi-
nantl y secreto1y, which explains the extensive glandular structure of
the oviduct mucosa. Another distinct difference between repf·oduc-
tion in birds and mammals is the female bird is the heterogametic
sex, whereas the male is the heterogametic sex in mammals. Avian
female gametes possess either a Z or W sex chromosome, which,
when combined with the Z clu·omosome contributed by the male,
results in either male (ZZ) or female (ZW) chicks. Among birds,
the default sex is male.
Ovary Anatomy and Histology
I
The ovary is adjacent to the cranial division of the left kidney where
it is suspended from the dorsal body wall by the mesovarium. A
portion of the left adrenal gland and associated ovarian and adrenal
sympathetic ganglia are commonly embedded in the base (hilus) of
the ovary. Flattened to cuboidal epithelial cells cover the surface of
the ovary and represent an area of specialized peritoneum ca lled the
ovarian surface epithelium . The surface epithelium rests on a thin
layer of connective tissue, the t1111ica albuginea. A distinct medulla
584 I American Association of Avian Pathologists
and cortex are only discernible in the juvenile ovary. Primary oo-
cytes and stromal cells comprise the cortex, which covers the me-
dulla except at the base of the ova1y. Clusters of granulocytes in
areas of extra-medullary hematopoiesis occur occasionally in the
cortex. Bands of connective tissue and smooth muscle, blood ves-
sels, and nerves make up the medulla. Growth of the ova1y with
progressive folding of the cortex slowly progresses until sexual
maturity approaches, at which point the maturation process rapidly
accelerates.
At sexual maturity, individual oocytes acquire yolk from sub-
stances produced in the liver, and follicles progressively enlarge
over a period of 5-6 days to form a hi erarchy of incrementally sized
follicles destined to be ovulated. Follicles develop within a richly
innervated fibrovascular stalk (pedicle) that extends from the ovary.
A fluid-filled follicular antrum does not develop in avian follicles.
Ovulation occurs along the stigma, a poorly vascularized zone in
the follicle wall. Progressive folding that has been occurring in the
cortex during development, possible expansion of the medulla into
the cortex, and development of large follicles on stalks blur the ear-
lier distinction between the medulla and co1tex to the point they
are no longer distinctly recognizable. It has been proposed that the
more peripheral area of the mature avian ovary where oocytes are
present and developing (co1tex) be called the parenchymatous zone,
and the more central area composed of connective tissue, smooth
muscle, nerves, and numerous, often thick- walled vessels (medulla)
be called the vascular zone.
Normal follicles of differing size and development, atretic
follicles, post-ovulato1y follicles in different stages, and previous
ovulation sites are normal structures that are present in the paren-
chyma of a mature ovary. Additionally, ovarian surface epithelial
hyperplasia, stromal cell hyperplasia, foci of foamy cells containing
lipid, cholesterol clefts in atretic follicles, hemosiderin-laden mac-
rophages, and clusters of granulocytes may be seen . In the vascular
zone, smooth muscle hyperplasia, small leiomyomas, and degen-
erative changes in the walls of large muscular aiteries, including
mineralization and atherosclerosis, frequently occur in older hens.
Wolffian duct remnants (rete ovarii, epoophoron) consisting of a
small collection of different tubules lined with either larger ciliated
epithelium or smaller non-ciliated cuboidal epithelium are occa-
sionally seen near the hilus. In the male, they would have developed
into the epididymis and rete testis respectively. They should not be
confused with neoplasia. A few small lymphoid foci in either zone
are normal, whereas large foci, diffuse infiltrates, or numerous foci
of lymphocytes are indicative of disease. Melanin, which can be
extensive and blacken the ova1y, is present in melanistic birds .
Follicles are spherical and contain the oocyte centrally. Ma-
ture oocytes of birds represent the largest cells among animals. The
relatively large oocyte nucleus, which subsequently becomes the
germinal disc, may or may not be visible depending on the plane of
section. Yolk is homogenous, finely granular, and pink staining with
H&E stain. Free cells other than the oocyte are not found within the
normal follicle. Shortly before ovulation, the prima1y oocyte under-
goes the first meiotic division to form the first polar body and sec-
ondary oocyte. Divisio n to form the second polar body and ovum
occurs in the infundibulum of the oviduct at the time offertilization.

Several layers comprise the follicle wall. Immediately adja-
cent to the oocyte cell membrane (vitelline membrane), is the thin,
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brightly eosinophilic, acellular perivitelline membrane . External to
the perivitelline membrane is the granulosa cell layer (follicular epi-
thelium), which is composed of a single layer of cuboidal cells in
small and large follicles and a pseudostratified columnar cell layer
in intermediate sized follicles. Granulosa cells rest on a prominent
basement membrane, which separates them from the theca interna.
Surrounding the granulosa cell layer are the thinner, more compact
theca interna, and the thicker, less dense theca externa. There is no
distinct separation between the internal and external theca. Both
thecal layers are composed of fibrous tissue, collagen, elastic fibers ,
and smooth muscle cells, and are richly vascularized and innervat-
ed. Cells of the theca intema are compressed and spindle shaped.
Spherical, oval, or elongated nests of endocrine thecal interstitial
cells, sometimes referred to as thecal glands, are located within the
thecal layers. Interstitial cells are large, variably shaped, and have
an eccentric round to oval nucleus and pale finely vacuolated cy-
toplasm . Groups of interstitial cells also occur in the parenchymal
stroma and vascular zone of the ovary. Controversy exists about
the functional similarities of interstitial cells in different parts of the
ovaty, but morphologically they are the same.
Following release of the oocyte, the post-ovulatoty follicle
contracts causing the wall to thicken, and the cavity fills with granu-
losa and thecal cells that accumulate lipid and develop a vacuolated
cytoplasm. Fibrovascular tissue rapidly fills the space and regres-
sion is complete within a few weeks; only a small mass of scar tissue
rematns. No co1p11s !11te11111 develops in the post-ovulat01y follicle
of birds.
Oviduct Anatomy and Histology
The oviduct is a single, open-ended tubular organ that extends from
the level of the ovary to connect with the urodeum of the cloaca.
Before production of the first egg, an occluding membrane (hy-
men) separates the vagina from the urodeum. Normally only the
left oviduct is functional. In mature female birds that are producing
eggs, the oviduct is large and occupies most of the left side of the
body cavity. Its size is greatly reduced in adult female birds that
are not producing eggs, but it still has the general appearance of a
developed oviduct. In juvenile birds, the itmnature oviduct runs
parallel to the left ureter on the surface of the kidney, is thin-walled,
and barely recognizable grossly. The oviduct serves as the site for
oocyte maturation and fertilization, secretion of egg contents, other
than yolk, that are essential for embryo development, formation of
the egg, and ovipositioning.
Five parts of the oviduct - infundibulum, magnum, isthmus,
shell gland, and vagina - are distinguished by their different struc-
ture and function (Table 1). Overall, the architecture of the oviduct
is similar to that of other tubular organs. The peritoneum provides
the serosal surface. Ligaments containing well-developed smooth
muscle, connective tissue, elastic fibers, vessels, and nerves extend
from the dorsal and ventral margins of the oviduct as the dorsal and
ventral mesosalpinx. These suspend the oviduct from the dorsal
body wall, maintain it in a contracted state, and may aid in moving
the developing egg along the oviduct. A muscle layer composed
Reproductive System
of smooth muscle arranged in inner circular and outer longitudinal
layers extends the length of the oviduct. In the upper infundibulum,
the muscle layer is incomplete, while it is thickest in the wall of the
vagina. There is no submucosa or muscularis mucosa, but a distinct
connective tissue layer separates the muscle layers from the mucosa.
The oviduct mucosa is folded and consists of a lining epitheli-
um and lamina propria. Simple glands or gland-like structures may
occur at the base of folds . They have cuboidal to columnar non-
ciliated epithelium. At the shell gland/vaginal junction and, less fre-
quently the infundibulum, these glands maintain viable spermatozoa
for an extended period and are referred to as sperm host glands. Cil-
iated cells, with interspersed secretoty cells that stain intensely with
PAS and Alcian blue, comprise the epithelium. The epithelium is
usually pseudostratified columnar, but can be simple. Beginning in
the lower infimdibulum, tubular glands progressively increase until
they fill the lamina propria in much of the remainder of the oviduct.
They are most numerous in the lamina propria of the magnum, but
are absent in the upper infundibulum, clear zone between the mag-
mun and isthmus, and vagina. Short ducts extend from the tubular
glands and open onto the epithelial surface . Microscopically, duct
openings appear as small pits in the epithelial surface .
Glandular epithelial cells of the magnum undergo secret01y,
regenerating, and resting phases that cotTelate with egg formation.
In the secreto1y phase, the cytoplasm of glandular epithelial cells is
distended with coarse, eosinophilic to basophilic granules, which
are so numerous that they compress the nucleus making it appear
pyknotic. Trichrome stain is useful for demonstrating differences
among granules. Glandular lumina are no longer visible because of
enlargement of the epithelial cells and albumen secretion. Follow-
ing discharge of the albumen with passage of the yolk, cells enter
the regenerating stage. They are now cuboidal with a round, vesicu-
lar nucleus and are largely devoid of cytoplasmic granules. Glands
have regained a distinct lumen. Cells in the resting stage are inter-
mediate between those in the regenerating and secretory phases. In
the regressed oviduct, mucosa! glands are much reduced and cells
are in a quiescent state without production of cytoplasmic albumin
granules.
Not all glandular cells discharge their contents with the pas-
sage of evety developing egg. It is common to find areas of cells in
both regenerating and secretory phases adjoining each other in the
magnal glands. Focal areas of glandular hyperplasia are common in
older hens. In these, the glands are convoluted and lined with cuboi-
dal cells that have large, basophilic nuclei and few to no cytoplasmic
granules. They blend imperceptibly with adjacent normal tissue.
Hyperplastic foci need to be differentiated from adenomas, which
also occur frequently in the magnum of older hens (see Neoplasia) .
Oviductal cysts, formed by involutions of the mucosa and lined by
I
ciliated epithelium, are filled with proteinaceous fluid or laminated
layers of inspissated secretions. They are often located in the mu-
cosa of the magnum of older hens. A mild granulomatous reaction
results if the cyst contents contact interstitial tissues. Infrequent
small lymphoid foci in the lamina propria are normal.
A "jelly-roll" procedure is an excellent method for examin-
ing the oviduct microscopically. In this procedure, the oviduct is
opened along its length, cut it into two or 3 pieces depending on the
Avian Histopathology (4 th Edition) I 585
 H. John Barnes • Oscar J. Fletcher • Tahseen Abdul-Aziz

Table 1: Characteristics of the parts of the avian oviduct.

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Oviduct Part Fuuction Structurn

Infundibulum - Oocyte capture Funnel shape.
Upper (Fimbria) Oocyte maturation Thin wall lacking glands with scattered bundles of smooth muscle.
Fertilization Mast cells numerous.
Low mucosa! folds or ridges.
Simple ciliated columnar epithelium; secretory epit helia l cells not present; short cilia.
lnfundibulum - Chalaza formation Tubular shape.
Lower (Neck) Secretion of thick Thicker wall with scattered tubular glands in lamina propria near magnum; muscle forms incom-
albumin plete longitudinal layer.
Sperm storage Higher mucosa! folds; secondary and tertiary folds; simple glands present at base of fo lds (glan-
dular grooves).
Mast cells numerous.
Simple ciliated columnar epithe lium, numerous secretory epithelial cells; short cilia.
Magnum Secretion of thin Longest part of oviduct; cranial and caudal parts.
albumin Well developed longitudinal and circular muscle layers.
Thick mucosa with long, tall, wide oblique folds; secondary folds .
Lamina propria packed with tubular glands containing eosinophilic cytop lasmic ovalbumin gran-
ules; regenerating, secretory, and resting phases.
Pseudostratified ciliated columnar epithelium.
Approximately equa l ciliated columnar and secretory epithelial cells; tall cilia.
Adenomas and adenocarcinomas most frequent in the magnum.
Isthmus Formation of shell mem- Shorter and more narrow than magnum.
branes Separated from magnum by clear zone devoid of tubular glands.
Initiation of shell Long, narrow longitudinal folds ; secondary folds.
formation Better developed muscle layers, espec ially longitudinal.
Tubular glands in lamina propria less numerous; pale staining ce ll s secrete keratin rich protein
fibers; cyclical changes not evident.
"Red region" near shell gland where initial shell formation occurs.
Approximately equal ciliated pseudostratified columnar and
secretory epithe lial cells; tall cilia.

Shell Gland Plumping of egg Short, wide, globose part of oviduct.

Shell formation Relatively thin wall and mucosa.
completed Well developed muscle layers, especially longitudinal.
Shell pigmentation Numerous short, narrow longitudinal, leaf like folds; secondary folds present.
Tubular glands in lamina propria less numerous; pale staining cells produce both protein and min-
era l rich secretions; cyclical changes not evident.
Ciliated pseudostratified columnar and secretory epithelia l cells;
intermediate cilia.

Vagina Sperm storage Short, narrow, folded part of oviduct.

Expulsion of egg
(ovipositioning)
Thick muscle layer, especially circular.
Tall , narrow longitudinal folds; secondary folds numerous .
Ciliated pseudostratified columnar and secretory epithelial cells; short cilia.
No secretory tubular glands in lamina propria.
Shell gland/vaginal sphincter and sperm host glands.
Occlusive membrane at cloaca prior to first ovulation.

size of the oviduct, and the pieces are rolled up with the mucosa! tions before sexual maturity that permanently damage the imma-
surface on the inside. Rolls should be made in one direction to pre- ture oviduct. Disturbances of growth include oviductal hypoplasia ,
serve the orientation of the oviduct so that the inner cut is the begin- cysts, and vestigial remnants of the right reproductive tract.

I
ning and the outer cut is the ending of that particular piece of the
oviduct. The rolls are placed into fixative and trimmed to produce a
continuous spiral, which will permit the entire length of the oviduct
to be examined microscopically when slides are prepared.
Disturbances of Growth
Abnormal development of the fema le reproductive tract usually af-
fects the oviduct and may have a genetic cause or result from infec-
Certain strains of infectious bronchitis virus (IBV) have a tro-
pism for the oviduct. Infection of young female chicks can result in
segmental occlusion or hypoplasia of the oviduct when they reach
adulthood; the ovary is unaffected. Age at time of exposure, ma-
ternal antibody titers, and virus strain influence the degree of ovi-
ductal damage. Lack of oviduct patency results in decreased egg
production. Microscopically, obliteration of the oviduct lumen,
loss of surface epithelium, and lymphoplasmacytic infiltration of

586 I American Association of Avian Pathologists


the lamina propria with progressive increase in germinal centers
is seen in the juvenile oviduct. In the adult hen following early
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IBV infection, varying degrees of oviductal hypoplasia, especially
of the upper isthmus and lower magnum, and focal oviductal cysts
resulting from lack of patency can occur. Microscopic lesions are
similar, but less pronounced, than those in immature birds. Numer-
ous lymphoid nodules persist in affected hens. QX type strains of
infectious bronchitis vims produce cystic oviducts, which result in
false-layers at maturity. Lack of mucosa! development, flattening of
mucosa! folds, and occasional mononuclear cell infiltrates beneath
the epithelium or serosa are seen microscopically.
Simple or multilocular cysts occur in the ovary and ligaments
of the oviduct. Large cysts on the margin of the fimbria (infundibu-
lar cysts) interfere with its fimction and predispose to misovulation.
Infundibular cysts are lined by cuboidal ciliated epithelium similar
in appearance to that lining the oviduct. Infundibular cysts need to
be differentiated from cystadenomas that occur at this same location.
Cystadenomas are more cellular and have an irregular epithelium in
multiple layers. Infrequent,ly, infundibular cysts and cystadenomas
occur within the lumen of the infundibulum. Cystic oviducts caused
by Chlamydia psittaci occur in laying flocks with poor egg produc-
tion, but microscopic lesions have not been described.
Right ovmJ' and oviduct
Development of the right ovary and oviduct is arrested during em-
bryonic development; however, it is common to find variably sized
cystic vestiges of the right oviduct in laying hens. They attach to the
cloaca, but usually are not patent. Microscopically, remnants of the
right oviduct may be thin-walled and lined with a simple ciliated cu-
boidal epithelium, or have a narrow mucosa with variable numbers
of secretoty tubular glands like those in the normal magnum. In-
flammation and neoplasia can affect cystic right oviducts, but this is
much less common than the left oviduct. Developed right oviducts
in poult1y are always abnormal, and are usually smaller than the
left oviduct, but do not differ from the left oviduct microscopically.
Trip/oidy
In chickens, paired oviducts are seen in triploid hens, which also
have ari ·ovotestis. Cells of triploid birds are larger thah those of
normal diploid hens and have three nucleoli- one for each set of
chromosomes. In triploid birds, the left gonad is an ovotestis where-
as the right gonad is a testis. Ovotestes are composed of va1ying
amounts of normal ovarian and testicular tissue. As the bird ma-
tures, testicular tissue usually develops to the point that tubules are
lined with spermatogenic cells, while ovarian tissue remains sup-
pressed in a juvenile state. Lack of ovarian tissue development in
ovotestes helps distinguish them from sex cord-stromal tumors that
have an appearance of testicular tissue, as these tumors occur in
developed ovaries and there is no spermatogenesis.
Degeneration
In most birds, regression (degeneration, involution, atrophy) of the
ovary and oviduct is a normal phenomenon that occurs at the end of
egg laying. However, in domestic poultry, it may occur during egg
laying because of stressors, including environmental factors, nutri-
Reproductil'e System
tional changes, tox1c1hes (mycotoxins, heavy metals), infectious
diseases, or hormonal manipulations (experimental), that cause an
abrupt cessation of ovulation.
Follicular atresia
Follicular atresia is a prominent feature of ovarian regression. Fol-
licular atresia (degeneration) may be physiologic or pathologic.
Regardless of cause, two types of follicular atresia occur - oblitera-
tive or invasion atresia, and cystic or bursting atresia. Obliterative
atresia is most common and affects small follicles that have little or
no yolk. Cells from the follicle wall, either granulosa cells or cells
from the theca intema, enter the follicle and destroy the oocyte;
eventually filling the follicle with invading cells. It occurs through-
out the bird 's life and is the primary means by which the number of
oocytes is reduced. Obliterative atresia is commonly seen in both
juvenile and adult ovaries, and, unless extensive or accompanied by
other changes in the ovary, it should be considered a normal physi-
ologic process.
Cystic atresia
Cystic atresia occurs in ovaries of mature birds in active production
and must be distinguished from inflammation (oophoritis). Larger,
hierarchal follicles undergo cystic atresia when there are excess ma-
turing follicles (e.g. , super-ovulation), pedicle torsion, abrupt ces-
sation of reproduction at the end of a reproductive cycle, or the hen
becomes acutely ill and is incapable of continuing reproduction. If
the cause of atresia is due to excess follicles, follicles of any size
may be atretic and usually only a single follicle is affected. Torsion
of the follicle pedicle is another cause of individual follicular atre-
sia. Initially, yolk within these follicles is thin and watery, but has a
green to brown color due to blood pigments. Eventually the follicle
contents sluink and inspissate to form a firm discolored nodule at
the end of a pedicle. When there is an abrupt cessation of produc-
tion, atresia of the largest follicle occurs first, followed by atresia of
the next largest follicle and so on until all of the hierarchal follicles
undergo atresia. Initially, the normally viscous, deep yellow yolk
becomes watery and light yellow. Instead of being spherical and
turgid, the follicle becomes flaccid and wrinkled . The thin watery
yolk enters the thecal layers of the follicle, either by seepage through
the granulosa cell layer or rnpture of the granulosa cell layer, where
it either is captured in vascular channels or passes tlu·ough the wall
of the follicle into the body cavity. Eventually the follicle shrinks
until only a small mass of lipid-laden cells surrounded by a ring of
dense colll1ective tissue remains. Sometimes cholesterol clefts or
aggregates of macrophages containing hemosiderin are present in
advanced atretic follicles.
Inflammation
Inflammation involving the ovary (oophoritis), oviduct (salpingi-
tis), or vagina (vaginitis) in birds can be caused by a number of
infectious agents (Table 2). "Metritis" is an inappropriate term to
describe inflammation of the shell gland, as the shell gland is not a
homologue of the mammalian uterus. Often more than one repro-
I
ductive organ is affected, e.g., oophoritis-salpingitis. Inflammation
Avian Histopathology (4 th Edition) I 587
 H. John Barnes • Oscar J. Fletcher • Tahseen Abdul-Aziz

Table 2. Known or suspected causes of inflammatory lesions in the reproductive tract.

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Viruses Bacteria Other

Alphaviruses Acti11obacil/11s spp. Fungi & Toxins
Eastern equine encephalitis virus Aero111011as l,ydropl,i/a Avibacteri11111 Aspergillus fumigatus
Highlands J virus gal/i11aru111 Zeara lenone
Adenoviruses Bacteroides spp. Protozoa
Quail bronchitis and related viruses C!,/a111ydia psillaci Tetratrichomonas
Egg-drop syndrome virus Citrobac/er spp. Toxoplasma
Avian influenza virus E111erococc11s faeca/is Helmin//,s
Avian metapneumovirus Escl,ericl,ia coli Ascaridia
Herpesviruses Gallibac/eri11111 analis Prosthogonimus
Marek's disease virus Klebsiella spp.
Duck virus enteritis lisleria 111011ocyloge11es
Pacheco's virus (Psittacines) Moraxella spp.
Hemorrhagic enteritis (Storks) A1ycobac/eri11111 avi11111
Infectious bronchitis virus Mycoplas111a
Newcastle disease virus M. gallisepticum
Tembusu virus (Ducks) M. spp. (Geese)
Turkey meningoencephalitis virus M . synov iae
Turkey pox On1i//,obac/eri11111 rl,i110/racl,eale
Pas/eurella 11111/tocida
Pro/eus 111irabilis
Pse11do111011as spp.
Rie111erel/a anatipes/ifer
Sa/111011ella
S. enteriditis
S. ga llinarum
S. heidelberg
S. pullorum
S. typhimurium
S!ap!,y/ococcus aureus
S!replococcus Group C
S. equi subsp. zooepide111ic11s

of adjacent tissues such as the cloaca in cases of vaginitis, and peri-
toneum when there is inflammation of the oviduct (salpingoperito-
nitis) is common. The reproductive tract can become infected via
an ascending infection from the cloaca, hematogenously in systemic
diseases, or by spread from adjacent tissues. Salpingitis in young
birds is usually associated with airsacculitis involving the left ab-
dominal air sac. In hens, egg binding is often initiates salpingitis.
Oophoritis, salpingitis, and peritonitis can result in incorporation of
the agent into the egg, resulting in possible vertical transmission of
the causative agent to the progeny of the infected hen or possible
foodborne illness from consumption of contaminated eggs.
Ooplwritis
Oophoritis most frequently results from bacterial infections includ-
ing Sa/111one/la p11/lorw11, S. ga/linarum, S. enteriditis, Escherichia
coli, or less commonly, other bacteria. Both normal and abnormal
fo llicles in the same ovaty are generally seen; affected follicles are
firm, miss hapen, discolored, or hemorrhagic. Inflammatory cells
neum has the appearance of yolk, and the term "yolk peritonitis"
has been frequently used, but this is incorrect as infec ti ous peritoni-
tis is completely different from yolk peritonitis (see Degeneration).
Grossly, copious caseating exudate that often is malodorous, helps
distinguish infectious peritonitis from the relatively mild, diffuse
serositis that characterizes yolk peritonitis. Experimentally, yolk
facilitates the virulence of avian pathogenic E. coli. Demonstration
of bacteria, either by culture or microscopically, serves to confirm
infectious peritonitis.
Microscopically, lesions of oophoritis are similar to those in
other tissues caused by Gram-negative bacteria, and depend on the
duration and degree of infection and viru lence of the organism. Ini-
tially, hyperemia, accompanied by increasing accumu lation of serous
proteinaceous fluid and fibrin, expands the stromal tissue separating
structures within the ovary; fo llicles are not yet affected and bacterial
colonies may or may not be visible. Subsequently, there is necrosis,
exudate becomes fibrinoheterophilic, follicular walls are affected,
and exudate extends into the yo lk. Bacterial colonies are often nu-

I within a follic le are indicat ive of folliculiti s. Peritonitis often ac-

companies oophoritis. When peritonitis is also present, the ova1y
may be covered with exudate that fills the spaces around follicles
embedding the ovaty in a mass of exudate. Differentiating peri-
tonitis from oophoritis in such cases is not always easy, requiring
microscopic identification of inflammation within the ovary rather
merous, proliferating in the nutrient rich environment provided by
the inflammato1y exudate and yolk. Yolk undergoes caseation as
it becomes mixed with exudate within the follicle. Lymphocytes,
plasma cells, and macrophages increase in the ovaty; macrophages
isolate affected areas and the lesion transitions into heterophilic gran-
ulomatous inflammation. Fibrosis is seen in advanced lesions. Dif-
than just on its surface. In such cases, exudate within the perito- fuse infiltrates of epithel ioid macrophages or multifocal gra nulomas

588 I American Association of Avian Pathologists


with numerous intracytoplasmic acid-fast bacteria occur in myco-
bacterial oophoritis. Lymphocytic inflammation with genninal cen-
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ters characterizes mycoplasmal infections . Serofibrinous to fibrinous
inflammation, without bacterial colonies, is seen in chlamydiosis.
Viral infections typically result in abrupt ovarian regression
with cystic atresia of follicles and concurrent acute yolk peritonitis .
Hemorrhages are seen grossly in virulent viral infections including
Newcastle disease, highly pathogenic avian influenza, and duck
virus enteritis . Experimental infection of gallinaceous birds with
highly pathogenic HSN l avian influenza virus resulted in minimal
necrosis and inflammation of the medullary stroma and cells of the
thecal layer in some of the birds. Histologic lesions in chickens
infected with high pathogenic avian influenza consisted of hemor-
rhage, heterophils, and cell debris in the wall of follicles, bursting
atresia, and yolk in the body cavity. Viral matrix inclusions in ovar-
ian smooth muscle may be seen in chickens with avian leukosis vi-
rus associated tumors, but the ovary is otherwise normal. Ovarian
hemorrhage, follicular atresia and rupture, ovarian regression, and
peritonitis occur in ducks i,nfected with Tembusu virus. Syncytial
cells with intranuclear inclusions typical of herpesvirus infections
can occur in the ovaries ofpsittacines with Pacheco 's disease.
Salpingitis
Salpingitis is usually the reason for egg production drops, poor egg-
shell quality, and decreased internal quality that occur in infectious
diseases. Eggs without a shell or with an abnormal shape, wrinkles
and folds in the shell, or thin, watery albumen indicate damage to the
oviduct. Respirato1y viruses often affect egg production suggesting
a common affinity for both respirato1y and reproductive tracts.
Gross lesions in viral salpingitis consist of edema, hyperemia,
hemorrhage, and pale, turbid, creamy or gelatinous exudate within
the oviduct lumen. They differ markedly from the massive, firm
exudates that develop within the oviduct in bacterial infections . Mi-
croscopic changes include patchy deciliation, degenerative changes,
or necrosis in mucosa[ epithelium, along with distention of tubular
secretory glands and glandular epithelial degeneration. There is
edema and infiltration of lymphocytes, mononuclear cells, plasma
cells, and heterophils in the lamina propria. Fibrosis and permanent
oviductal damage are possible outcomes. Necrosis and hemorrhage
may occur with more virulent virus infections. Intravenous inocula-
tion of influenza virus caused lymphocytic infiltration, and necrosis
and atrophy of glandular epithelium in the oviduct of laying chick-
ens . Similarly, heterophil infiltration and lymphoid hyperplasia
characterized lesions in the oviduct of hens infected with Newcastle
disease virus . Usually, viral antigens are readily demonstrated by
inununostaining even if the oviduct appears minimally affected or
normal. Inclusion bodies may be seen in adenoviral and herpesviral
infections. In some viral infections, only specific areas of the ovi-
duct are affected. Lesions in hens with egg drop syndrome, caused
by an atadenovirus (formerly type 3 avian adenovirus), are mainly
in the shell gland. Degeneration and desquamation of epithelial
cells that may contain intranuclear inclusion bodies, hyperplasia of
epithelium, atrophy of tubular secretory glands, and infiltration of
the lamina propria by lymphocytes, plasma cells, macrophages, and
heterophils are seen.
Reproductive System
Bacterial salpingitis tends to be more exudative than salpin-
gitis caused by viruses. Large masses, composed of inflammato1y
exudate, yolks, and oviduct secretions, progressively accumulate in
concentric layers within the oviduct lumen of mature birds, eventu-
ally thinning the oviduct wall and causing impaction. Sometimes
a fully formed egg will be found within the mass suggesting that
salpingitis either started as binding of the egg or the egg became
lodged in the oviduct because of a localized area of inflammation.
Almost invariably, when there is salpingitis there is concurrent peri-
tonitis, which is referred to as salpingoperitonitis. Whether perito-
nitis is a sequel to salpingitis or vice versa is unknown, but either
direction of spread is possible because the infimdibulum opens di-
rectly into the body cavity. Masses within the oviduct, up to the size
of an egg, can be regurgitated into the abdominal cavity by reverse
peristalsis. The oviductal origin of these caseated masses can be
confirmed by revealing the typical concentric layering of oviductal
masses on cut section. Masses from the oviduct may also be found
within the abdominal cavity if the oviduct ruptures, but this is very
rare in poultry. Mostly the masses are so large that they persist for
long periods within the oviduct until ovulation ceases, which slows
further enlargement of the mass. Extension from yolk sac or air
sac infections may cause salpingitis in immature birds. The oviduct
is distended by caseous fibrinoheterophilic exudate, which persists
until maturity, when it is passed just before egg production.
Microscopically, pink proteinaceous material arranged in lay-
ers fills the oviduct lumen. Cells are not a significant component
of the exudate . Bacterial colonies are generally numerous within
the luminal mass and have the characteristic appearance and Gram
staining reaction of the causative organism. The mucosa is com-
pressed by the expanding luminal mass, and the tubular secret01y
glands in the lamina propria are separated from each other by edema
and fibrin. Heterophils are present, often seen migrating through
the mucosa! epithelium, but usually they are not numerous. Ne-
crosis is infrequent and the process generally does not progress to
heterophilic granulomatous inflanunation or a chronic stage with fi-
brosis. The relatively mild microscopic changes in the oviduct mu-
cosa are in sharp contrast to the massive gross lesions, but most of
the material obstructing the oviduct has come from ovulations and
secretions, not inflammation. Salpiilgitis caused -by mycoplasthas
and ureaplasmas is characterized by lymphocytic to lymphoplas-
macytic infiltration of the lamina propria, often with perivascular
localization, and numerous lymphoid nodules and germinal centers.
A similar lymphocytic infiltration in the oviduct of unknown cause,
not associated with mycoplasmal infection, has been reported in an
infertility syndrome of turkey hens .
Vaginitis
I
Vaginitis occurs in young females at the onset of egg production
because of infection of traumatized tissues by organisms in the clo-
aca. It is often accompanied by cloacitis. Trauma results from pas-
sage of eggs through the immature vagina, or from insemination of
young turkey hens. In geese, vaginitis occurs as a venereal disease
of unce11ain etiology. Swelling, inflammation, mucosa! necrosis
with ulceration and pseudomembranes, and caseous plugs are seen
grossly. Egg binding results from constriction of the vaginal lumen.
Avian Histopathology (4 th Edition) I 589
 H. John Barnes • Oscar J. Fletcher • Tahseen Abdul-Aziz
Microscopically, there is marked fibrinous, fibrinoheterophilic, or
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heterophilic inflammation, and edema. Hyperemia and granuloma-
tous responses are present in deeper tissues of the vaginal wall. In
severe cases, the mucosa! surface is ulcerated and covered by a case-
ous necrotic diphtheritic membrane. Bacterial colonies with char-
acteristics of the causative organism are numerous . E1J1sipelothrix
and E. coli have been identified as causes of vaginitis in turkeys.
Vaginitis with typical pox lesions occurred in turkeys when the vi-
rus was accidentally transferred from infected to uninfected hens by
insemination.
Peritonitis. Yolk Peritonitis
Free yolk in the body cavity provokes a mild, diffuse serositis (yolk
peritonitis). Prominent, irregular tags of tissue frequently seen on
the serosal surfaces of the duodenum and pancreas of older hens are
the cumulative result of multiple bouts of yolk peritonitis. Lesions
typically have foci oflymphocytes, foamy macrophages, and hemo-
siderin. Yolk may be present if the lesion has developed recently.
Free yolk in the body cavity from cystic atresia is wate1y and pale
yellow, which distinguishes it from thick, viscous, yellow yolk that
came from one or more follicles that ruptured during handling or
at necropsy. Infectious peritonitis in which exudate resembles co-
agulated yolk needs to be distinguished from yolk peritonitis (see
Salpingitis).
Microscopically, the earliest changes in cystic atresia are sepa-
ration of the oocyte cell membrane from the granulosa cell layer
and theca interna from the basement membrane of the granulosa
cell layer. Hemorrhagic atretic follicles resulting from a separation
of the granulosa cell layer and theca interna are characteristic of
vitamin A deficiency. The yolk of the oocyte develops an altered
appearance and contains free cells and numerous basophilic yolk
globules. The granulosa cell layer ruptures, although this is infre-
quently seen in single sections of large follicles undergoing atresia.
Thickening and infolding of the granulosa cell layer into the cavity
created by the degenerating oocyte are seen. Later, phagocytic cells
increase in the affected follicle, acquire lipid, and become foamy
macrophages. Eventually, fibrosis of the follicle occurs and it con-
tracts into a small mass of connective tissue. While the granulosa
cell layer ruptures, the follicle wall remains intact, a feature that
helps distinguish cystic atretic follicles from postovulato1y follicles .
Cystic atresia can be differentiated from inflammation (oophoritis)
by the lack of inflammato1y cells.
Paralleling the regressive changes in the ovary are similar
changes in the oviduct, which markedly decreases in size. The basic
architecture of the oviduct remains unchanged, but the layers de-
crease in size more closely resembling those of the juvenile oviduct.
Tubular secreto1y glands in the lamina propria decrease in number
I
and size reflecting their inactivity. Secretory granules are no longer
evident in glandular epithelium, which assumes the characteristics
seen in glands that are in the regenerating phase. Inflammatory cells
are not a feature of oviductal regression.
Misov11/atio11
Misovulation occurs when a follicle ruptures and the ovum is not
captured by the infundibulum . It falls free into the intestinal com-
590 I American Association of Avian Pathologists
pa11ment of the peritoneum. It may rupture and provoke a serositis
as described above, but, more often it remains intact and gravitates
to the dependent (caudal-ventral abdomen) area of the body cav-
ity where it lodges against the body wall. Adhesions develop and
the ovum becomes encapsulated creating a focal chronic peritonitis.
Over time, the ovum is reduced to a caseous mass that may contain
cholesterol clefts and foamy macrophages. A collapsed, convoluted,
bright eosinophilic vitelline membrane is occasionally seen in the
lesion. Inflammation is generally lymphocytic and mild unless the
lesion becomes infected, which causes extensive fibrinoheterophilic
inflammation with numerous intralesional bacterial colonies. Miso-
vulated ova need to be differentiated from retained yolk, which is
located in Meckel 's diverticulum, and yolk sacs that are unabsorbed
emb1yonic yolk. These are frequently seen as small spherical to
oval green to brown-yellow masses that are free in the body cavity.
Neoplasia
Several different types of tumors can be found in the female repro-
ductive tract, but most are uncommon to rare (Table 3). Neoplasms
that occur with some frequency in the ovary include the viral tu-
mors (Marek's disease, lymphoid leukosis, myeloid leukosis, and
reticuloendotheliosis), sex cord/gonadostromal tumors (granulosa
cell tumors, ovarian Sertoli cell tumors), germ cell tumors (dysger-
minomas), and adenocarcinomas. In the oviduct, adenomas and
adenocarcinomas are common, primarily in the magnum, and cyst-
adenomas occur infrequently in the infundibulum. Leiomyomas are
the most frequently occurring neoplasm in the female reproductive
tract, and are found in the ovary, smooth muscle layers of the ovi-
duct, and free margin of the ventral mesosalpinx. Other than ad-
enocarcinomas shared between the ova1y and oviduct, metastasis of
tumors to the avian ovary or oviduct is rare . Except for the viral tu-
mors and leiomyomas, other mesenchymal tumors (fibromas, fibro-
sarcomas, myxomas, myxosarcomas, malignant melanomas, etc.)
are much less common than epithelial tumors. Leiomyomas and
ovarian adenocarcinomas provide good animal models for studying
fibroids and ovarian cancer, respectively, .in women.
Lymphoma, caused by Marek's disease virus, is the most com-
mon tumor of immature ovaries. Marek's disease, lymphoid leu-
kosis, and myeloid leukosis in the adult ova1y can be recognized
by proliferative infiltrates of heterogenous lymphocytes, large lym-
phoblasts, or immature granulocytes, respectively. Cell infiltrates
widely expand or replace the ovarian stroma. Follicles are initially
spared but may finally be compressed and degenerate. Cells com-
prising tumors caused by reticuloendotheliosis virus can be pleo-
morphic lymphoid cells, monomorphic immature lymphoblasts, or
large histiocytic (reticulum) cells. Differentiating reticuloendothe-
liosis from Marek 's disease and lymphoid leukosis usually requires
virus identification as the gross and microscopic lesions can be in-
distinguishable among these lymphoid tumors. Lesions of the viral
tumor diseases are not confined to the ovary; focal to diffuse tumors
are present in liver, spleen, kidney, and a variety of other tissues
depending on the type of tumor. Viral tumor lesions rarely occur in
the oviduct even though the magnum is the primary source for avian
leukosis viruses that cause emb1yo infection and ve11ical transmis-
sion. The minimal lymphoid and hemopoietic tissue in the oviduct
 Reprod11ctiJ1e System

may provide an explanation for why lesions of vira l tumors do not produce hormones, but this feature is inconsistent and not usefu l for
occur there more frequently. classification.
VetBooks.ir

Sex cord/gonadostromal tumors
Among sex cord/gonadostromal tumors, granulosa cell tumors are
more frequent than ovarian Se1toli cell tumors. Classification of
tumors with intermediate characteristics is difficult. They are often
referred to as " mixed" sex cord/go nadostromal tumors or just go-
nadal tumors. Arrhenoma and arrh enoblastoma are terms that are
also used to describe tumors in the ovary, which have the same or
similar morphology as testicular tissue, and cause virilism. Whether
virilism results from excess androgens produced by the tumor or
from a defici ency of estrogens is unknown . Thecal tumors are rare
in poultry, but it is common for gra nulosa cell tumors to have a
thecal cell component, which is why the term gra nulosa-thecal cell
tumor is often used. Sex cord/go nadostromal tumors are usually
beni gn and confined to the ovary, but around 10-20% of cases are
malignant and spread to other organs. Often they develop in an
ova-testis or the rudimentary right ovary following damage or re-
moval of the left ovary. S~x cord/gonadostroma l tumors frequently
Granulosa cell tumors are often cysti c with necrosis and hem-
orrhage. The overall architecture and cells making up the tumor are
hi ghl y variable, even within the same tumor. Usually there are solid
or cystic spherical to elongated clusters of cells that are separated
by fine delicate connective tissue. Cystic structures have multiple
layers of tumor cells that surround an open central area and palisade
along the inner septa! wall giving it a rudimentary, follicl e-like ap-
pearance. Rosettes, whorled gyriform formations, or an irregular
cribiform architecture in which a single layer of cuboidal tumor
cells lines the surfaces of prominent stromal connective tissue are
present in some tumors. Call-Ex ner bodies, which are seen in mam-
malian gra nulosa cell tumors, are not a feature of avian granulosa
cell tumors. Tumor cells range from uniform cuboidal cells with
moderate pale cytoplasm and a central deeply stained nucleus to
larger, irregular spherical or polyhedral cells with finely granular
eosi nophilic cytoplasm and a central, ves icular nucleus. The latter
cells have an epithelioid appearance and individual or small nests of
these cell s are often invested by a thin, eosinophilic membrane. Mi-

Table 3. Classification and characteristics of avian female reproductive tract tumors.

A. Epithelial Tumors - epithelial cells, A 2.2.1 Albuminous D. l .2Monomorphic, B-lymphocytes -

cytokerati11 positive, usually ovalb11111i11
positive
A. I Well-differentiated, expanding, non-
invasive, often polypoid in ov iduct -
Adenoma
A. I. I Glandular epithelium, albumin
granules, non-ciliated epithelial
cells - Oviductal adenoma
A. I. I. I Numerous oviductal
adenomas -
Adenomatosis
A. l .2 Ciliated epithelium, located in
infundibulum - Infundibul ar
cystadeno111a
A.2 Invasive, proliferating, multiple
organs affected - Adenocarcinoma
Arcli itecture - Tubular, Cystic,
Papillary, Solid, Lobular, Mixed
Differentiation:
Grade I: Well-differentiated - mitosis
rare to absent, defined pattern
Grade 2: Mitosis rare to occasional,
architectural pleomorphism but
tubular pattern present,
minimal to moderate
(oviductal ce ll type)
adenoca rcinoma
A 2.2.2 Adenocarcinoma
with squamous
differentiation
A.3 Metastatic tumor from other primary
site - pancreas, intestine, kidney, li ver,
other
B. Sex Cord/Go11ados/romal Tumors
B. l Follicular pattern, indi vidual and
small groups of large cell s, fine stroma
- Granulosa cell tumor
B.1.1 Benign: well differenti ated,
localized or multifocal in ovary
B. I .2Ma lignant : poorly differentiated,
multiple tissues affected
B.2 Tubules containing Sertoli and/or
seminiferous cell s - Sex-cord Tumor
B.2.1 Ovarian Sertoli cell tumor
C. Germ Cell Tumors
C. l Multiple ti ssue types without defined
organization - Teratoma
C.2 Sheets or cords of large, round to
angular cells resembling primitive
Lymphoid leukosis
D.2 Immature myeloid cells - Myeloid
leukosis
E. Mesenchymal Tumors
E. 1 Well-d ifferentiated smooth muscle
ce ll s - Leiomyoma
Ventral mesosalpinx margin
Tunica muscularis of oviduct or
intestine, ti.mica media of large
arteri es
Ovarian medulla
E.2 Poorly differentiated, proliferating
s111ooth 111uscle cell s, mitotic figures,
tissue invasion - Leio111yosarco111a
E.3 Well-differentiated fibrocytes,
co ll agen production - Fibroma
E.4 Poorly differentiated, proliferating
fibroblasts , ti ssue invasion, collagen
production - Fibrosarcoma
E.5 Blood-filled capillary or cavernous
spaces lined by endothelial cells -
Hemangiosarco111a
E.6 Multipl e mesenchymal cell types -
Mixed mesenchymal tumor

ce llular dysplasia
Grade 3: Mitosis co111mon, cellular
pleomorphism, often in sheets,
anaplasia
A.2. 1Cytoplas111ic granules, usua lly
ovalbumin positive, oviduct -
Oviductal adenocarcinoma
A 2.20vary- Ovarian
adenocarcinoma
germ cells - Dysgerminoma (female F. Other Tumors
counterpart of male sem inoma)
F. l
D. Hemopoietic Tumors - stro111al i11filtratio11
a11d replaceme111 by 11eoplaslic blood cells
D. I Ly111phosarcoma
D.1.1 Pleomorphic, T-lymphocytes, F.2
may affect immature females -
Marek's disease
I
Well differentiated leiomyoma
with < 10% ofti.unor composed of
embedded neop last ic epithelium -
Leiomyocarcinoma
Epithelial and connective tissues
with primitive renal differentiation -
Nephroblastoma

Avian Histopathology (4th Edition) I 591

 H. Jol,11 Ba mes • Oscar J. Fletcher • Tahseen Abdul-Aziz

totic figures are rare. Thecal areas are composed of large angular to than ovarian adenocarcinomas. If tumors are present in both organs,
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fusiform cells with pale, vacuolated cytoplasm and large, open pale it is not possible to determine their origin or spread. It is unknown if
nuclei . Marked cytoplasmic vacuolation of thecal cells indicates reproductive tract adenocarcinomas arise at a single site and spread
luteinization. Ovarian Sertoli cell tumors have a tubular structure to other tissues by metastasis, or if they arise simultaneously in
and the same microscopic appearance as Sertoli cell tumors in the multiple sites (synchronous or multicentric origin). When only one
testis (see Male Reproductive Tract: Neoplasia). organ is affected, the type of adenocarcinoma can be determined by
careful examination of both the ovary and oviduct to confirm that
Germ cell tumors the tumor is only present in one of the tissues. Although the repro-
Among germ cell tumors in the ova1y, dysgerminomas, the female ductive tumors in chickens are an excellent animal model, attempts
homologue of male seminomas, are rare. Well-differentiated dys- to classify reproductive tumors in chickens as the same tumors in
germinomas have a tubular pattern resembling seminiferous tu- women is unjustified. For example, the term "endometrioid tumor"
bules. Cells are large, round to polyhedral, with scant eosinophilic hardly seems possible when birds do not have a uterus. Similarly,
cytoplasm and a large prominent, round , often eccentric nucleus the term "serous" is inappropriate as the tumor cells do not contain
with a prominent nucleolus. Mitotic figures can usually be found , or secrete fluid. They produce albumin and should be called albu-
and occasionally there are multinucleated syncytial cells. In less minous adenocarcinomas.
differentiated tumors, the tubular pattern is not as evident. Ovarian Hens with advanced reproductive tract adenocarcinomas have
teratomas are very rare, but have the same microscopic characteris- moderate to marked ascites, weight loss, metastatic tumors in the
tics as those in other tissues. liver and lungs, and generalized serosal tumors involving the intesti-
nal peritoneal cavity (carcinomatosis). Distribution of tumors with-
Epithelial tumors
in the body cavity depends on which communications exist between
Adenomas in the oviduct and adenocarcinomas in the ovary and ovi-
the different peritoneal compartments. Ovarian adenocarcinomas
duct are frequently found in older egg-laying chickens. Their oc-
are firm to hard, multilobular, irregular, solid or pedunculated, and
currence increases with age. Other birds, including broiler breeder
light tan to cream colored frequently having a "cauliflower-like" ap-
chickens and turkeys, may be affected, but the rate of occurrence
pearance. Affected ovaries may have only a single or a few small
is lower. Oviductal tumors are usually located in the magnum, but
tumor nodules among normal follicles, or be completely involved
may also be rarely found in the infundibulum and shell gland.
with no active follicles. Tumors are commonly accompanied by
Adenomas are round to oval, soft, sessile masses or peduncu-
small cysts on the ovarian surface. Cystadenocarcinomas composed
lated polyps, up to 1 cm in si ze, that are the color of the oviduct
of numerous small to large cysts that replace the ova1y and may fill
mucosa and have a smooth surface. Larger masses with an irregular
the body cavity are a morphologic variant that occurs in about 5%
surface or different colored areas are more likely to be adenocarcino-
of affected birds. Hens often remain in production even with very
mas. In contrast to adenomas, adenocarcinomas are usually firmly
large tumors.
embedded in the oviduct mucosa. Adenomas should be considered
Adenocarcinomas in the oviduct occur as thickened, firm areas
pre-malignant, as a progression from hyperplasia to adenoma to ad-
with irregular lobular or nodular patterns within the oviduct wall.
enocarcinoma can often be recognized in affected hens. Adenoma-
Tumors may bulge into the body cavity or lumen of the oviduct.
tosis describes the presence of numerous adenomas in the magnal
Oviductal obstruction is possible if the tumors are vety large. Me-
mucosa. Adenomas do not occur in the ovary.
tastasis occurs by both implantation of tumor cells on serosal sur-
Microscopically, oviductal adenomas are composed of well-
faces and vascular spread. Even small oviductal adenocarcinomas
differentiated albuminous glands that are in a secretmy or resting
are capable of metastasis. Secondary tumor growth involving the
phase. Orientation of glands within an adenoma is more irregu-
pancreas and duodenum ts often extensive' becau~e of their location
lar compared to that in the mucosa. The margin of an adenoma is
just ventral to the reproductive tract, which may result in intestinal
distinct, which provides a contrast between normal glands in the
obstruction from tumor tissue encircling and constricting the intes-
mucosa and glands in the tumor, but they are not encapsulated. The
tine.
expansive nature of adenomas compresses adjacent tissues in the
Microscopically, adenocarcinomas in the ova1y and oviduct
lamina propria and causes bulging of the surface epithelium. There
are similar. The basic pattern is lobules or nodules comprised of
is no invasion of adjacent tissues, especially the wall of the ovi-
glandular acini or short tubules and spherules lined with a secretory,
duct, which serves to distinguish adenomas from adenocarcinomas .
simple, cuboidal, or low columnar epithelium. The lumen of tu-
Differentiating adenomas from hyperplastic foci can be more prob-
bules and spherules often contains eosinophilic proteinaceous fluid.
lematic. In general, hyperplastic foci are smaller, glands are more

I
Some tumors have a predominantly papilla1y or cystic architecture.
nmmally oriented, hyperplastic foci lack distinct margins, and they
Oviductal adenocarcinomas invade the wall of the oviduct. Large
transition with adjacent normal mucosa! glands.
tumors are transmural and protrude from the serosal surface. They
Adenocarcinomas occur simultaneously in the ovary and ovi-
rarely breach the mucosa! epithelium. Tumors in the ovary either
duct more frequently than in either organ alone. Approximately 20
occur as small surface nodules or replace stromal tissue in the par-
- 25% of affected hens have a tumor in either the ova1y or oviduct
enchymatous and vascular zones. Follicles are spared, but variably
while the remaining 50 - 60% have tumors in both organs. Col-
si zed tumor nodules are frequently located in perifollicular spaces
lectively, oviductal adenocarcinomas tend to occur more frequently
consistent with lymphatics.

592 I American Association of Avian Pathologists


Tumors vary greatly in their morphology depending largely
on the reproductive status of the birds . Most tumors are well dif-
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ferentiated (Grade 1). Cells in these tumors are similar to those in
normal magnal albuminous glands, differing only in greater nuclear
variability. If the hen is reproductively active, there will be eosino-
philic granules in the cytoplasm. Mitotic figures are rarely present.
Less differentiated adenocarcinomas (Grade 2) still have recogniz-
able tubules and spherules, but these are irregular or poorly formed
and lined by cells that lack uniformity, often showing crowding or
piling along the basement membrane. Cytoplasmic granules are
limited to focal areas and secretory material is minimal to absent in
many tubules. The number of mitotic figures is variable, but usu-
ally are not numerous. Poorly differentiated tumors (Grade 3) are
rare. They are composed of highly pleomorphic, anaplastic cells,
devoid of cytoplasmic granules, in sheets or barely recognizable
acini, tubules, or spherules. Nuclei vary in size and mitotic figures
are usually numerous. Infrequently tumors will have a squamous
differentiation. Tumors within the same bird often exhibit varying
degrees of differentiation . . The amount of interstitial fibrovascular
tissue and smooth muscle bundles is variable, but can be substantial
in some tumors. The latter is referred to as scirrhous, desmoplastic,
or sclerosing tumors . The amount of connective tissue and smooth
muscle does not correlate with degree of differentiation. Tumors on
the surface of the ovary are less likely to be scirrhous.
Oval bum in is an excellent marker for reproductive tract adeno-
carcinomas, but cannot be relied on to discriminate between ovarian
and oviductal tumors. Previously, it was believed that ovalbumin,
which is usually present in cells of both ovarian and oviductal ad-
enocarcinomas, proved the tumors were of oviductal origin. This is
incorrect, as adenocarcinomas restricted to the ovary also produce
ovalbumin. The amount of ovalbumin within the cytoplasm of tu-
mor cells depends on the reproductive state of the hen. Tumor cells
in terminally ill, cachectic hens may produce little or no ovalbumin.
Recently, HER2/neu was identified in most tumors restricted to the
oviduct while it was absent from tumors found only in the ova1y
Leiomyoma
Leiomyomas are benign smooth muscle tumors that develop in the
free margin of the ventral mesosalpinx, or arise from smooth muscle
in the muscle layeis of the oviduct, tunica 1iledia of large arteries,
mesovarium, or muscle bundles in the vascular zone of the ovary.
They are hormonally responsive and among the most common tu-
mors of the reproductive tracts of egg-laying hens. Leiomyomas
within the ovary are small and difficult to distinguish from bundles
ofhyperplastic smooth muscle. An oval to spherical shape that com-
presses adjacent tissues helps to differentiate them from normal tis-
sue. Leiomyomas that arise from the oviduct muscle layers are often
multiple, round to oval, smooth, firm, translucent, white to pale gray,
up to 2 cm, and have a characteristic shiny surface. Rarely, a few
tumors can also be found outside of the oviduct in the mesente1y or
along the wall of the lower intestine. Leiomyomas in the mesosal-
pinx are solita1y and up to 5 cm. Numerous varicose veins radiate
from some of these tumors. Microscopically, tumor nodules consist
of bundles of muscle fibers with large nuclei and rare mitoses sepa-
rated by variable amounts of fibrous tissue. A peculiar tumor that
Reproductive System
appears to be a typical leiomyoma, but has embedded carcinomatous
epithelial tissue that accounts for less than 10% of the tumor, occurs
infrequently. Currently, these are being called leiomyocarcinomas,
and are considered to represent a type of collision tumor.
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of oviduct lesions in immature chickens following exposure to
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Crinion, R. A. P., R. A. Ball, and M. S. Hofstad. 1971.
Abnormalities in laying chickens fqllowing exposure to
infectious bronchitis vims at one day old. Avian Dis 15:42-48.
Dobos-Kovacs, M., G. Czifra, Jr., Z. Varga, and L. Stipkovits .
1987. Mass outbreak of vaginitis in geese in their first year of
lay. Magyar Al/atorvosok Lapja 42:541-545.
Domermuth, C.H. , W. B. Gross, and R. T. Dubose.1967.
Mycoplasmal salpingitis of chickens and turkeys. Avian Dis
11 :393-398.
Fitzgerald, S. D. and C. J. Cardona. 1993. True hermaphrodites in a
flock of Cochin bantams. Avian Dis 37:912-916.
Fredrickson, T. N. 1987. Qvarian tumors of the hen. Environ
Health Perspec f 73 :35-51.
Gazdzinski , P. and H. J. Barnes. 2004. Venereal colibacillosis
(acute vaginitis) in turkey breeder hens. Avian Dis 48:681-685.
Gilbe1t, A. B. 1979. Female genital organs. In Form and Function
in Birds, Vol. 1, A. S. King and J. McClelland (eds). Academic
Press, London, pp. 237-360.
Giles, J. R., H. L. Shivaprasad, and P.A. Johnson. 2004. Ovarian
tumor expression of an oviductal protein in the hen: a model
for human serous ovarian adenocarcinoma. Gyneco/ Onco/
95:530-533 .
Gupta, S. K. , A. B. Gilbert, and M. A. Walker. 1988. Histological
study of follicular atresia in the ovary of the domestic hen
(Gallus do111esficus). J Reprod Fertil 82:219-225.
Johnson, A. L. 1996. The avian ovarian hierarchy: a balance
between follicle differentiation and atresia. Pou/t Avian Biol
Rev7:99-ll0.
Johnson, P.A. and J. R. Giles. 2013. The hen as a model of ovarian
cancer. Nat Rev Cancer 13 :432-436.
Jordan, F. T. W, N. J. Williams, A. Wattret, and T. Jones. (2005).
Observations on salpingitis, peritonitis and salpingoperitonitis
in a layer breeder flock. Vet Rec 157:573-577.
Kajigaya, H., M. Kamemura, N . Tanahara, A. Ohta, H. Suzuki,
M . Sugiyama, and M. !soda. 1987. The influence of celomic
membranes and a tunnel between celomic cavities on cancer
metastasis in poultry. Avian Dis 31 : 176-186.
Madekurozwa, M. C. and W. H. Kimaro. 2006. A morphological
and immunohistochemical study of healthy and atretic follicles
in the ovary of the sexually immature ostrich (Struthio
came/us). Anaf Hist E111b1J10/ 35:253 -25 8.
Mickley, K ., M. Buote, M. Kiupel, J. Graham, and C. Orcutt. 2009.
Ovarian hemangiosarcoma in an orange-winged Amazon parrot
(Amazona a111azonica). J Avian Med Surg 23:29-35.
Reproductive System
Moore, C. B. and T. D. Siopes. 2004. Spontaneous ovarian
adenocarcinoma in the domestic turkey breeder hen (Meleagris
gal/opavo): effects ofphotoperiod and melatonin. N ew-a
Endocrino / Leff 25:94-10 I.
Nad, P. , P. Massanyi, M. Skalicka, B. Korenekova, V. Cigankova,
and V. Almasiova. 2007 . The effect of cadmium in combination
with zinc and selenium on ovarian structure in Japanese quails .
J En viron Sci Hlth [A} 42 :2017-2022.
Nakamura, K., T. Higashi, M. Yamada, K. Imai, and Y. Yamamoto.
2007. Basophilic intracytoplasmic viral matrix inclusions
distributed widely in layer hens affected with avian-leukosis-
virus-associated tumours . Avian Pathol 36:53-58.
Nakatani, H. , K. Nakamura, Y. Yamamoto, M. Yamada,
and Y. Yamamoto. 2005. Epidemiology, pathology, and
immunohistochemistry of layer hens naturally affected with
HSN I highly pathogenic avian influenza in Japan. Avian Dis
49:436-441.
Parshad, R. K . 1997. Follicular atresia in the avian ova1y. Indian J
fap Biol 35:685-695 .
Perkins, L. E. and D. E. Swayne. 2001. Pathobiology of A/chicken/
Hong Kong/220/97 (HSN I) avian influenza virus in seven
gallinaceous species. Vet Pathol 38: 149-164.
Pors, S.E. , R.H. Olsen, and J.P. Christensen.2014. Variations in
virulence of avian pathogenic Escherichia coli demonstrated
by the use of a new in vivo infection model. Vet Atlicrobio/
170:368-374.
Ramis, A., J. Tarres, D. Fondevila, and L. Ferrer. 1996.
Immunocytochemical study of the pathogenesis of Pacheco 's
parrot disease in budgerigars. Vet Microbial 52:49-61.
Rhoades, K. R. 1971. Mycoplas111a 111eleagridis infection: reproductive
tract lesions in mature turkeys. Avian Dis 15:722-729.
Sae Silva, M, D. R. Rissi, M . Pantin-Jackwood, and D. E. Swayne
DE. 2013 . High-pathogenicity avian influenza virus in the
reproductive tract of chickens. Vet Patho/ 50:956-560.
Shivaprasad, H. L. 2000. Fowl typhoid and pullorum disease. Rev
Sci Tech 19:405-424.
Smyth, J. A., M.A. Platten, and J.B. Mcferran. 1988. A study of
the pathogenesis of egg drop syndrome in laying hens. Avian
Patho/ 17:653 -666.
Stipkovits, L., P. A. Brown, R. Glavits, and R. J. Julian. 1983. The
possible role ofureaplasma in a continuous infertility problem
in turkeys. Avian Dis 27 :513-523.
Wu, L., J. Liu, P. Chen, Y. Jiang, L. Ding, Y. Lin, Q. Li, X. He, Q.
Chen, and H. Chen. 2014. The sequential tissue distribution
of duck Tembusu virus in adult ducks. Bio111ed Res Int
2014 :703930.
Xu, B., W. Dong, C. Yu, Z. He, Y. Lv, Y. Sun, X. Feng, N. Li, L.
I
F. Lee, and M. X . Li. 2004 . Occurrence of avian leukosis virus
subgroup J in commercial layer flocks in China. Avian Patho/
33:13-17.
Zhang, F. , S. Li, J. Yang, W. Pang, L. Yang, and C. He. 2008.
Isolations and characterization of Chlamydia psittaci isolated
from laying hens with cystic oviducts. Avian Dis 52:74-78 .
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13.1. Testis. Normal. Adult rooster. Convoluted, 13.3. Testis. Normal. 4-day-old chicken. Immature
interconnecting seminiferous tubules lined by a spermatogenic seminiferous tubules are small, lack a lumen, lined by a single
epithelium are separated by a thin fibrovascular stroma. There is no layer of spermatogonia and Sertoli cells, and separated by a cellular
lobular structure or mediastinum testis as seen in manunalian testes. interstitium. lnm1ature testes are similar to mature testes in non-
breeding adult male birds (compare with 13.5).

13.2. Testis. Normal. Adult rooster. Epithelium ofseminiferous 13.4. Testis. Early regression. Adult pigeon. Epithelium 1s
tubules is composed of spermatogenic and Sertoli cells arranged disorganized and the normal spermatogenic columns are no longer
in columns . Sertoli cells are capped by tufts of late spermatids recognizable. Numerous spermatidic giant cells in the lumen are

I
attached by their heads. A few mature spermatozoa are in the a hallmark of regression. Testicular regression indicates an end
lumen. It is normal to see only limited numbers of spermatozoa of reproduction and may result from physiologic or pathologic
within seminiferous tubules. Spermatogonia form the basal layer. processes. Similar sloughed cells and spermatidic giant cells are
Se1toli cells have large vesicular nuclei and with prominent nucleoli also present in the epididymal tubules.
(arrowhead). Other cells including spermatocytes and spermatids
can be differentiated by their decreasing size.

596 I American Association of Avian Pathologists


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13.5. Testis. Advanced regression. Adult American kestrel.
When regression is complete, the testis resembles an immature
testis (compare with 13)). Seminiferous tubules are small,
interstitium is cellular, and spermatogenic cells are no longer
present leaving only a single layer of cells. Age and reproductive
state of the bird are helpful in distinguishing an immature testis from
advanced regression. Microscopically, a few residual cells from the
spermatogenic epithelium and a few spermatozoa often remain in
the seminiferous and epididymal tubules and ductus deferens .
13.6. Testis. Melanin. Adult cockatoo. Gonads (testes, ovaries)
of some types of birds are normally pigmented. In this testis, there
are degenerative changes in the epithelium of the seminiferous
tubules that are inte1111ediate between those shown in 13.4 and 13.5.
Cells in the interstitium and ti.mica albuginea contain large amounts
of melanin. Insert. Detail of dense melanin in interstitial tissues but
not seminiferous ti.1bules.
Reproductive System
13.7. Testis. Cystic. 3-week-old chicken. Experimental
phosphorus deficiency. A. Markedly distended immature
seminiferous tubules form a cribiform pattern at low magnification.
B. Lining epithelium is flattened. If the cause is removed, the
testis will return to normal or near normal before sexual maturity.
Although sodium and furazolidone toxicity are known causes of
cystic testes, these young broiler breeders were on an experimental
diet deficient in phosphorus.
13.8. Testis. Sperm retention, early. Adult rooster. Usually,
only a few isolated spermatozoa are present in the seminiferous
tubules. In this tubule, a tangled mass of spermatozoa mixed with
I
sloughed necrotic cells is located within the lumen. Late spermatids
are irregular and disrupted along much of the epithelial surface
except for an area above the mass. Only a few tubules such as this
one were present in an otherwise normal testis. More severe or
extensive lesions are associated with decreased fetiility.
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13.9. Testis - Sperm retention, advanced. 62-week-old
rooster. In advanced lesions, retention of spermatozoa affects most
seminiferous tubules and there is degeneration of the spermatogenic
epithelium. Impaction of tubules results from the large masses
of necrotic cells and spermatozoa. Contact between the necrotic
mass and interstitium may occur in some tubules as the tubular
wall breaks down, which results in an interstitial lymphocytic or
granulomatous orchitis.
13.10. Testis. Sperm retention, advanced. 68-week-old tom
turkey. Multifocal interstitial orchitis is apparent at low power in
this section of testis from a tom turkey at the end of its first breeding
I
cycle. Fertility in this flock was low. Seminiferous tubules close to
the epididymis are most affected (box). The epididymis shows only
minimal changes . Infection with turkey herpesvirus was associated
with the lesion.
598 I American Association of Avian Pathologists
13.11. Testis. Sperm retention, advanced. 68-week-old tom
turkey. Detail of 13.10 showing masses of necrotic cells and
spermatozoa that occlude many seminiferous tubules. Where
tubular walls have been breached, there is hyperemia and extensive
infiltration oflymphocytes and macrophages. Giant cells are present
in some lesions but are not seen in this image.
13.12. Testis. Orchitis. 62-week-old broiler breeder. Multicentric,
intratubular, heterophilic granulomatous orchitis affected one testis.
There is degeneration and necrosis of seminiferous epithelium and
intratubular caseous exudate with numerous intralesional bacterial
colonies. Less affected tubules contain proteinaceous fluid and
fibrin. Fibrin, early fibroplasia , and collagenous connective tissue
infiltrated by heterophils, lymphocytes, plasma cells, macrophages,
and multinucleated giant cells are present in the interstitial
tissue. Insert. Exudate and bacterial colonies are surrounded by
multinucleated giant cells.

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13.13. Testis. Orchitis. 62-week-old broiler breeder. Detail of
13 .12 showing caseous exudate composed of fibrin , degenerated
spermatozoa, necrotic hete,rophils , epithelial debris, macrophages,
and botryoid bacterial colonies filling the lumen of a seminiferous
n1bule. Exudate is covered by multinucleated giant cells and
surrounded by a broader outer zone of macrophages. Inse1t.
Intralesional colonies, which stain dark purple with Gram's
stain, are numerous within lesions in the seminiferous tubules.
Staphylococcus aureus was isolated.
13.14. Testis. Epididymo-Orchitis. 28-week-old broiler breeder.
Acute intratubular fibrinoheterophilic epididymo-orcb.itis affected
both testes and epididymides. A. Multicentric, coalescing acute
inflammatoty and necrotic lesions affect the seminiferous n1bules.
B, C. Lumina of affected n1bules are filled with fibrin , degenerated
spermatozoa, heterophils, epithelial debris, macrophages, and numerous
colonies of rod-shaped bacteria. The interstitium is expanded by
fibrin , inunantre granulation tissue, and collagenous connective tissue
infiltrated by heterophils, lymphocytes, plasma cells, and macrophages.
D. Tubules in the epididymis are filled with fibrin, degenerated
spermatozoa, heterophils, epithelial debris, macrophages, and bacterial
colonies. Bacteria stained negative with Gram's stain. Escherichia coli
was isolated.
Reproducti11e System
13.15. Testis/Epididymis. Normal. Adult rooster. Spermatozoa
produced in the seminiferous tubules (ST) of the testis pass through
straight tubules in the testis (not present in this figure) into the
rete testis (RT), efferent ducts (ED), connecting ducts (CD), and
epididymal ducts (EpD) of the epididymis to reach the ductus
deferens. Spermatozoa are visible in the connecting and epididymal
ducts. Transition between the rete testis and an efferent duct can be
seen (*). The thin connective tissue layer that separates the testis
from the epididymis is the nmica albuginea (arrowheads).
13.16. Epididymis. Normal. Adult Rooster. Tubules of the
epididymis include efferent ducts (ED), connecting ducts (CD),
and epididymal ducts (EpD) . Location, size, and lining epithelium
I
distinguish the different types of ducts. Spermatozoa are visible
in some of the connecting ducts and epididymal ducts. Normally
tubules in the epididymis of a reproductively active male bird have
only a few free cells in the lumen.
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13.17. Epididymis. Normal. Adult rooster. A. Rete testis external
to the ti.mica albuginea in the connective tissue between the testis and
epididymis is lined with a flattened simple squamous epithelium. B.
Efferent ducts are relatively large, convoluted, and lined by tall colunrnar
mixed ciliated and non-ciliated epithelium. C. Transition between
rete testis and efferent duct. D. Connecting ducts are small, lined
by a sparsely ciliated, pseudostratified epithelium, and often contain
spermatozoa. Epididymal ducts are much larger and contain abundant
spennatozoa in the reproductively active male bird. An efferent duct on
the left, connecting ducts in the center, and an epididymal duct on the
right can be seen.
13.18. Epididymis. Normal. Adult Rooster. Presence of one
or a few lymphoid foci in the interstitium of the epididymis of a
conventional bird in the absence oft1.1bular changes or other lesions
I
should be considered normal and not interstitial lymphocytic
epididymitis.
600 I American Association of Avian Pathologists
13.19. Epididymis. Lithiasis. 62-week-old rooster. An efferent
duct is dilated and contains a proteinaceous mass, spermatozoa, and
a calculus. The calcu lus has been shattered in processing. Other
ducts have spermatozoa and increased free cells. A calculus in an
early stage of formation can be seen in the distended duct in the
upper right. Lymphocytes are modestly increased in the interstitium.
Epididymal lithiasis is increased in roosters from flocks with low
fertility, and, in some cases, has been assoc iated with infectious
bronchitis virus infection.
13.20. Ductus deferens. Normal. Adult rooster. The zigzag
pattern, large size, and numerous spermatozoa in the lumen are
identifying features of the ductus deferens. The wall is composed
of smooth muscle and connective tissue.

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13.21. Ductus deferens. Normal. Adult rooster. Detail of 13.20.
The ductus deferens is a continuation of the epididymal ducts. Both
are lined by a similar n9n-ciliated, pseudostratified epithelium
and both have numerous spermatozoa in the lumen during active
reproduction.
13 .22. Epididymis. Sertoli cell nodule. 62-week-old rooster.
Sertoli cell nodules occur as small well-differentiated discrete
nodules within an otherwise normal testis or epididymis. Nodules
are composed of tubules lined by a single layer of elongated cells
with a basal nucleus and vacuolated feathery apical cytoplasm.
Cells in nodules need to be differentiated from Se1ioli cell tumors.
Insert. Detail of a tubule.
Reproductive System
13.23. Epididymis. Sertoli cell nodule. 62-week-old rooster.
Another example of a Sertoli cell nodule within the epididymis
is seen here. Compared to 13 .22, the cytoplasm of these cells is
finely vacuolated and cell borders are more distinct. The tubular
pattern and basal orientation of elongated cells are still evident. An
efferent duct is invested within the margin of the tumor, but this is
not interpreted as evidence of neoplasia. Inse1t. Detail of a tubule .
13.24. Testis. Malignant seminoma. 9-year-old budgerigar. One
testis was markedly enlarged. A. Intensely stained neoplastic tubules
replace the normal seminiferous tubules, but the general architecture
I
of the testis is still apparent. B, C. At higher magnification, the
epithelium of tubules is comprised of multiple layers of variably sized,
round to polyhedral, intensely staining cells with a large round nucleus
containing a conspicuous nucleolus. In well-differentiated tumors,
the similarity to normal seminiferous tubules is readily recognized.
Mitoses may be common along with bizarre multinucleated cells. D.
Malignancy of this tumor is indicated by the numerous individual and
small clusters of tumor cells in the air spaces of a pneumatic ve1iebra
and adjacent tissues.
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13.25. Ovary. Normal. Adult hen. Primary (smaller) and
secondaiy (larger) follicles are located in folds on the surface.
Tertiary follicles (not shown here) develop within fibrovascular
stalks. In the adult ovary, the term parenchymatous zone (PZ)
has been proposed for the surface layer, which corresponds to the
cortex in the juvenile ovaty (compare with 13.33, 13.34). The
parenchymatous zone covers the centrally located vascular zone
(VZ) (medulla in the juvenile ovary) except at the hilus.
13.26. Ovary. Normal. Adult Hen. Follicular atresia may
be physiologic or pathologic. Larger follicles that contain yolk
undergo cystic (bursting) atresia (A) while smaller follicles undergo
I
obliterative (invasion) atresia (a). Compare atretic follicles with
normal larger (N) and smaller follicles. Ovulation sites (ov) can be
distinguished from advanced atretic follicles by a peripheral ring of
dense connective tissue.
602 I American Association of Avian Pathologists
13.27. Ovary, follicle. Normal. 4-year-old hen. The follicular
wall surrounding the ovum consists of a thin, hyaline perivitelline
membrane (PYM) between the ovum and granulosa cell layer (GC),
theca interna (TI), and theca externa (TE). Fine feathery structures
extending perpendicular to the PYM into the ovum form the zona
radiata. The GC can vaiy from one to several cells thick depending
on the maturity of the follicle. A mitotic figure is present(*).
13.28. Ovary, follicle. Cystic (Bursting) Atresia. 4-year-old
hen. Architecture of the follicular wall is disrupted and a partial
rupture extends through the granulosa cell layer and theca interna
(compare with 13.27). Mononuclear cells with extensive foamy
cytoplasm and scattered granulocytes are present. This example of
' physiologic ' inflammation should not be interpreted as oophoritis
or folliculitis (see 13.35, 13.36). Yolk from cystic atresia often
escapes into the body cavity causing a diffuse serositis commonly
referred to as ' yolk peritonitis ' (see 13.71 , 13.72).

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13.29. Ovary, follicle. Obliterative (Invasion) Atresia. 4-year-
old hen. Two small follicles, the one on the right is normal while
the one on the left is und~rgoing obi iterative atresia. The atretic
ovum is shrinking, granulosa cells have rounded up, and, along with
cells that migrate from the theca interna, they eventually invade and
destroy the ovum. Clear structures in the theca interna surrounding
the atretic follicle are thecal glands. They appear prominent and
increased in number, but are also present around the unaffected
follicle albeit compressed by the normal ovum.
13.30. Ovary, follicle. Ovulation site. Adult cockatiel. A post-
ovulatory follicle is filled with fibrin and cells including those from
the granulosa cell layer (center). A cross section of the fibrovascular
stalk is located at the base of the post-ovulatoty follicle and smaller
older ovulation sites, now filled with luteinized (vacuolated) cells,
are just above and to the right of the recently ovulated follicle.
Reproductil'e System
13.31. Ovary, follicle. Ovulation site. 4-year-old hen. Walls of
the post-ovulato1y follicle have collapsed and the cavity previously
occupied by the ovum is filled with luteinized, lipid-laden cells. No
true corpus luteum is formed. The stigma where the follicle ruptured
can be seen (upper left). Eventually the follicular wall transitions
into dense connective tissue that surrounds a residual collection of
vacuolated cells and the ovulation site persists for an extended time.
13.32. Ovary, follicle. Obliterative (invasion) atresia,
epoiiphoron, Wolffian duct remnant. 9-week-old broiler
breeder. Obliterative atresia of small follicles occurs in the juvenile
ovary as seen here (a). Along the surface of the ova1y is a well-
developed epoophoron (ep), which in the male would develop into
the epididymis. At higher magnification, tubules can be identified
that correspond to the different tubules in the epididymis (see I 3.16,
13.17). A remnant of the Wolffian duct (wd) that would develop into
the ductus deferens in the male is also present.
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13.33. Ovary, juvenile. Normal. 20-day-old broiler. A distinct
outer cortex and inner medulla can be identified in the juvenile
ovary. Development of folds on the surface, which has begun at this
age, and other changes cause the distinction between the cortex and
medulla in the adult ovary to be lost.
13.34. Ovary, juvenile. Normal. 20-day-old broiler. Detail
13.33 showing the distinct cortex and medulla in the juvenile ovary.
The specialized ovarian surface epithelium can be seen at this
I
magnification as a layer of cuboidal cells on the surface of the ova1y.
604 I American Association of Avian Pathologists
13.35. Ovary, follicle. Atresia (A) vs. Folliculitis (oophoritis)
(B). 32-week-old broiler breeder hen. A. Advanced cystic atresia
is characterized by breakdown of yolk and yolk spherules, loss of
definition of the perivitelline membrane, and marked vacuolar
degeneration of the granulosa cell layer. B. In folliculitis , the ovum
has disintegrated and filled with proteinaceous fluid, perivitelline
membrane is indistinct, granulosa cells have been replaced by a
radial palisade of macrophages and giant cells, and the follicle wall
is markedly expanded by free yolk and proteinaceous fluid. Often
bacterial colonies can be seen, but they are not visible in this image.
13.36. Ovary, follicle. Folliculitis [oophoritis]. 44-week-old
turkey breeder hen. The ovum has partially collapsed because
of cystic degeneration of the yolk, which has led to folding and
thickening of the perivitelline membrane. Granulosa cells have been
replaced by masses of necrotic inflammato1y cells, macrophages,
and giant cells. The theca interna is edematous. Numerous bacterial
colonies are located in the folds of the perivitelline membrane.

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13.37. Ovary. Granulomatous oophoritis, mycobacteriosis.
6-year-old golden-headed manakin. Follicles are widely
separated by numerous ~1acrophages and giant cells that have
replaced the stroma. Nuclei are eccentric, often pressed against
the cell membrane, and cytoplasm is finely granular and slightly
basophilic. The crescent arrangement of nuclei in multinucleated
cells is characteristic of Langhans giant cells. (Case courtesy of
A. van Wet/ere)
13.38. Ovary. Granulomatous oophoritis, mycobacteriosis.
6-year-old golden-headed manakin. An acid-fast stain of 13.37
reveals numerous intracellular acid-fast positive bacteria typical of
Jyfycobacterium spp . (Case courtesy ofA. van Wet/ere).
Reproductive System
13.39. Oviduct, fimbria. Normal. Adult laying hen. The fimbria
is pa11 of the infondibulum and forms the most distal pa11 of the
oviduct. Immediately adjacent to the ovary, but not connected to
it, the infundibulum receives the 0V11m following OV1tlation and is
the site of fe11ilization . It is identified by a thin wall containing
incomplete muscle layers and absence of mucosa! glands. Inse11.
Mucosa is covered with a low cuboidal epithelium with short cilia
and no secretory epithelial cells.
13.40. Oviduct, infundibulum. Normal. Adult laying hen. As
the infundibulum approaches the magnum, the wall thickens, muscle
layers become better defined, mucosa increases in height, there are
I
mucosa[ folds, and simple glands are at the base of mucosa[ folds.
Mucosa[ glands are still lacking until near the junction with the
magnum.
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13.41. Oviduct, magnum. Normal. Adult laying hen. The 13.43. Oviduct, shell gland. Normal. Adult laying hen. Mucosa!
magnum is the largest part of the oviduct and the piece most often folds in the shell gland are relatively short and narrow. Mucosa!
taken for microscopic examination . The mucosa is thick and glands are pale staining. Muscle layers are well developed . Insert.
composed of broad folds packed with albuminous glands that are Detail of mucosa showing epithelium and mucosa! glands.
covered by a simple to pseudostratified columnar ciliated secreto1y
epithelium. Mucosa[ glands in this section are in the resting phase
and are in the process of re-accumulating cytoplasmic granules
following discharge of albumin with the passing of a developing
egg. More commonly, glandular cells are in the secretory phase,
which can be seen in 13.51 and 123.67.

13.42. Oviduct, isthmus. Normal. Adult laying hen. Mucosa! 13 .44. Oviduct, vagina. Normal. Adult laying hen. Mucosa!
folds in the istlunus are long, narrow, and oriented longitudinally. folds in the vagina are tall and narrow. Glands are present in the
Mucosa[ glands are less numerous than in the magnum, pale base of seconda1y folds . Muscle layers are thicker in the vagina

I
staining, and lack the brightly eosinophilic albuminous granules of than in any other part of the oviduct. Insert. Detail of mucosa (box)
the magnal glands. Insert. Mucosa is covered with a pseudostratified showing epithelium and lack of secretory mucosa! glands.
epithelium composed of a mix of secretory and non-secretory cells
with tall cilia.

606 I American Association of Avian Pathologists


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13.45. Oviduct, vagina. Sperm host glands. 31-week-old
broiler breeder. Sperm host glands are characteristic of the avian
oviduct. They are most 1~umerous at the junction of the vagina
and shell gland and infrequent in the infundibulum. At the base
of mucosa! folds, the epithelium changes from a pseudostratified
ciliated to a simple columnar non-ciliated epithelium with basally
oriented nuclei. ln this section, there are both empty glands and
ones containing spermatozoa. Spermatozoa are adhering to the
surface epithelium and migrating down a mucosa! fold toward the
gland at the base (center) .
13.46. Oviduct, magnum. Advanced regression. 12-year-
old wood duck. The hyperchromatic ductal epithelium indicates
the oviduct had been functional , but has undergone almost total
regression. Albuminous glands lack any evidence of activity. (Case
courtesy of D,: C. Johnson)
Reproductive System
13.47. Oviduct, magnum. Aviadenovirus infection (quail
bronchitis). 7-month-old bobwhite quail. Multifocal necrosis
affects glandular epithelial cells. Nuclei are obscured by large
diffuse basophilic inclusion bodies characteristic of aviadenovirus
infections. Secreto1y albuminous granules in the glandular cells
indicate the bird was in production. Insert. Detail of intranuclear
inclusion bodies .
13.48. Oviduct, magnum. Aviadenovirus infection (quail
bronchitis). 7-month-old bobwhite quail. Necrosis is diffuse
and more severe in the shell gland than in the magnum. Inclusions
I
are numerous. If eggs were being produced, they would likely lack
a shell. Infection with aviadenovirus occurs most frequently m
juvenile quail. lnse1t. Detail of intranuclear inclusion bodies.
Avian Histopathology (4 th Edition) I 607
 H. John Ba mes • Oscar J. Fletcher • Tahseen Abdul-Aziz
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13.49. Oviduct, magnum. Psittacine herpesvirus infection
(Pacheco's disease). Adult Amazon parrot. There is necrosis of
the mucosa) epithelium and necrotic debris in the lumen. Several
multinucleated viral syncytial cells with intranuclear inclusions are
in the remaining epithelium. Glandular epithelium is inactive and is
not involved in the viral infection. Infection of the oviduct was part
of a systemic disease with lesions in many tissues. Insert. Detail of
the intranuclear inclusion bodies in viral syncytial cells.
13.50. Oviduct, magnum. Bacterial salpingitis. 106-week-old
hen. Granulocytes have accumulated beneath the epithelium and
are migrating through the epithelium into the lumen. Epithelium is
I
hypersecreto1y, which has resulted in a thick layer of proteinaceous
material accumulating in the lumen. This acute lesion is relatively
mild. Much of the material that comprises the large masses seen
grossly in the oviduct comes from the products of reproduction and
not inflammation.
608 I American Association of Avian Pathologists
13.51. Oviduct, magnum. Bacterial salpingitis. 106-week-old
hen. Another field from the same hen as 13.50. A bacterial colony
is trapped within the proteinaceous material in the lumen (left) and
a mass of exudate containing necrotic cells is undergoing caseation
(right). The hen is in active production. Glandular cells are in the
secreto1y phase. Albumen that is being secreted will add to the
luminal contents.
13.52. Ovary. Marek's disease. 7-month-old hobby hen. In this
immature ovaiy, sparse follicles are widely separated because of
lymphoid tissue that has replaced most of the ovarian stroma. Two
remaining follicles are undergoing degeneration and necrosis (*), a
process completely different from atresia .

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13.53. Ovary. Marek's disease. 7-month-old hobby hen. At
higher magnification of the ovaiy in I 3 .52, a normal small follicle
is surrounded by a confluent ,infiltrate of lymphoid cells. Lymphoid
cells do not show the variability typically seen in Marek 's disease.
However, the characteristic heterogeneity of lymphocytes was
present in other areas of the ovary and the hen had lesions in
many tissues, including those of the central and peripheral nervous
systems.
13.54. Myeloid leukosis. Adult broiler breeder. Sheets of well-
differentiated myeloid cells expand and replace the ovarian stroma.
Small foci of granulocytes that often occur in the ovary are readily
differentiated from myeloid tumors. Myeloid leukosis lesions were
also present in several other tissues including bone, and the flock
was known to be positive for avian leukosis virus - serotype J.
Reproductil'e System
13.55. Ovary. Myeloblastosis. Adult broiler breeder. In the
same ovary as 13.54, masses of extremely large, deeply basophilic
blast cells are located in the walls of a few follicles . Large, pale
pink, hyaline granules visible in the cytoplasm of several cells
identify them as myeloblasts.
13.56. Ovary. Sertoli cell tumor. 4-year-old hen. Tubules
lined by narrow, radially arranged elongated cells that have a basal
nucleus and thin, wispy apical cytoplasm characterize this well-
I
differentiated ovarian Sertoli cell tumor. Less differentiated tumors
also occur that may be difficult to classify. Inse1t. Detail of tubules
lined by well-defined Sertoli cells.
Avian Histopathology (4 th Edition) I 609
 H. John Ba mes • Oscar J. Fletcher • Tahseen Abdul-Aziz
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13.57. Ovary. Gonadal tumor. 20-week-old broiler breeder.
These tumors occur in young females approaching sexual maturity
that show precocious development, and adults that never come
into production. They are characterized by long, parallel cords,
often two cells wide that lack a lumen and are separated by a well-
developed connective tissue stroma. Note the multinucleated cell
in the extreme lower right. The term gonadal tumor is being used
because the histogenesis of these tumors is unknown.
13.58. Ovary. Gonadal tumor. 20-week-od broiler breeder.
Same ovary as 13 .57. Architecture of the tumor is variable but
the same general pattern is seen here. Rows of tall columnar cells
I
with sub-apical nuclei form the cords in the upper left whereas the
more frequent rounded to cuboidal cells in a more irregular jumbled
pattern form the cords in the lower right.
610 I American Association of Avian Pathologists
13.59. Ovary. Gonadal tumor. 20-week-old broiler breeder.
Ovary from a different bird in the same flock with the same clinical
presentation. Cords of tumor cells are still evident even though
they are less distinct in thi s ovary compared to the previous one.
Rows of small cells with dark nuclei (left of center) are suggestive
of granulosa cells.
13.60. Ovary. Adenocarcinoma. 4-year-old hen. Small nodules
stud the surface of the ovary with the largest one at the hilus (arrow).
An adrenal gland (*) is adjacent to the large tumor. Although
not evident at this magnification, the small tumor nodules are
associated with follicles (see 13.61). Localization of small tumors
on the surface without tumor in the vascular zone suggests this
is a metastatic adenocarcinoma from the oviduct, but an accurate
classification of the tumor source depends on knowing the status of
the oviduct.

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13.61. Ovary. Adenocarcinoma. 4-year-old hen.
Adenocarcinomas often develop in perifollicular spaces where
they partially or complete,ly surround the ovum. As long as the
granulosa cell layer is intact, ova are spared and not invaded by an
adenocarcinoma. The dilated perifollicular space contains protein-
rich fluid but not cells suggesting it may be a lymphatic.
13.62. Ovary. Adenocarcinoma. 4-year-old hen. An early
adenocarcinoma is developing in the wall of a follicle . Inse1t. At
higher magnification, ovalbumin secretion in a small tumor (box) is
seen. Ovalbumin is secreted if the hen is in production. Ovalbumin
is an excellent marker of reproductive tract adenocarcinomas, but
cannot differentiate primary ovarian and oviductal cancers, as both
produce ovalbumin.
Reproductive System
13.63. Ovary. Adenocarcinoma, well-differentiated (grade 1).
4-year-old hen. Most adenocarcinomas of the reproductive tract
(ovarian, oviductal) are well differentiated and readily identified.
Well-differentiated adenocarcinomas are composed of glandular
structures that conform to the albuminous glands of the magnum.
Cells comprising the glands are uniform, have basal nuclei that
are vesicular and vaiy little in shape and size, and may or may not
have brightly eosinophilic cytoplasmic granules depending on the
reproductive state of the hen. Mitotic figures are ve1y rare to absent.
13.64. Peritoneum. Reproductive tract adenocarcinoma,
intermediate differentiation (grade 2). 4-year hen. Interstitial
fibrovascular tissue and smooth muscle account for the scirrhous
I
nature of this metastatic peritoneal tumor. Tubules and glandular
structures are still evident but not distinct, which defines the degree
of differentiation of this tumor as intermediate. Mitotic figures
may be present, but are not numerous (not visible in this section
at this magnification). This tumor is classified as a reproductive
tract adenocarcinoma because it was not possible to determine if the
primary tumor was ovarian or oviductal.
Avian Histopathology (4 th Edition) I 611
 H. John Barnes • Oscar J. Fletcher • Tahsee11 Abdul-Aziz
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13.65. Peritoneum. Ovarian adenocarcinoma, poorly
differentiated (grade 3). 4-year-old hen. Glandular architecture
is barely recognizable. Cells are highly anaplastic and there are
numerous mitotic figures. Tumors of this type are rare. Most
ovarian and oviductal adenocarcinomas are well-differentiated
Grade 1 tumors.
13.66. Oviduct, magnum. Adenocarcinoma. Adenocarcinoma.
106-week-old hen. Adenomas and adenocarcinomas occur most
frequently in the magnum. Several tumors are present in the muscle
I
layers and mucosa. Larger tumors have displaced the glands in the
lamina propria of the mucosa . They frequently extend tlu-ough the
serosa, but rarely, breach the epithelial lining. A concurrent bacterial
salpingitis is responsible for the excess protein in the lumen (see
13.50, 13.51).
612 I American Association of Avian Pathologists
13.67. Oviduct, magnum. Adenocarcinoma. 106-week-old hen.
Oviductal adenocarcinomas are indistinguishable histologically
from ovarian adenocarcinomas (compare with 13 .63). They are
usually well differentiated. Normal magnal glands are located in
the upper right. Glandular cells are in the secreto1y phase, which
is mirrored in the tumor cells. Tissue invasion and metastasis
distinguish adenocarcinomas from adenomas, which are not
invasive and do not spread .
13.68. Oviduct, magnum. Adenocarcinoma. 106-week-old
hen. Even though the oviductal adenocarcinoma in this bird is well
differentiated, it is still highly malignant. Several tumor emboli are
in vessels consistent with lymphatics in the submucosa and muscle
layer. Direct implantation of tumor cells on serosal membranes
has previously been considered the method of metastasis for these
tumors, but there is increasing evidence that vascular dissemination,
probably via lymphatics, is also important.

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13.69. Mesovarium. Leiomyoma. 4-year-old hen. Leiomyomas
are benign smooth muscle tumors that are commonly found in
the reproductive tracts of.older laying hens. They are composed
of interwoven bundles and masses of well-differentiated smooth
muscle. Although leiomyomas have been described most often in
the margin of the ventral mesosalpinx, they can develop from smooth
muscle anywhere in the reproductive tract and, less infrequently,
the digestive tract. This one developed from smooth muscle in the
mesovanum .
13.70. Mesovarium. Leiomyoma. 4-year-old hen. Detail
of 13.69. Tumor cells are elongated and have an elongated oval
nucleus ( circular in cross section) . Often they are more spindle-
shaped than in this tumor. Leiomyomas lack cross-striations,
mitotic figures are rare to absent, the tumor compresses but does not
invade or replace adjacent tissue, and they do not metastasize. Size
is the only criterion for differentiating smooth muscle hyperplasia
from a leiomyoma .
Reproductive System
13.71. Pancreas, peritoneum. Diffuse serositis (yolk peritonitis).
106-week-old hen. Repeated release of fluid yolk into the intestinal
peritoneal cavity from cystic atresia of large follicles results in
diffuse serositis (peritonitis). Serositis is most pronounced on the
surface of the duodenum and pancreas because they lie directly
beneath the ovary. The peritoneum, which forms the serosa
covering organs in the body cavity, becomes thickened and covered
by irregular tissue fronds. Gross lesions can resemble metastatic
adenocarcinoma, but microscopic examination readily distinguishes
serositis from tumors.
13. 72. Pancreas, peritoneum. Diffuse serositis (yolk peritonitis).
106-week-old hen. Detail of 13 .71. Lipid filled macrophages
with fewer lymphocytes and granulocytes make up the cellular
I
component of the fronds. Connective tissue and small blood vessels
are increased along the surface of the affected organ. Occasionally
yolk spherules (seen here as bright eosinophilic masses) are seen
if there has been recent atresia of large follicles. Occasionally
granulomas or cholesterol clefts are present within the lesions.
Free yolk on the serosal surface, without inflammatory changes, is
usually an artifact.
Avian Histopathology (41h Edition) I 613
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CHAPTER
Integumentary System
H. L. Shivaprasad • H. John Barnes
Introduction
The avian integument forms the external layer of the body and is
composed of skin, feathers, and other structures. Functions of the
avian integument include flight, diving, sensory perception, mating,
social rank, temperature control to an extent, resistance to various
irritants and infectious agents, etc. Skin and feathers are unique
structures with many adaptations. Feathers are unique to birds and
are a prominent feature of avian anatomy. Other structures within
the avian integument include beak, nails, comb, wattle, snood, ear-
lobes, cere, shields (coots, gallinules), knob (goose), casque (cas-
sowaries, hornbills), helmet (guinea fowl) , modified combs such as
plumage (crests, bristles), scales (shank and feet), webbing of feet
(waterfowl), footpads, and glands (uropygial gland near the tail and
glands in the external ear) . Skin, beak, nails, and feathers are pres-
ent in all birds. These vary in pigmentation, shape, texture, func-
tion, location, and number.
Normal avian skin is remarkably resistant to disease. Howev-
er, various factors such as poor management, environment, genetics,
disease agents, and malnutrition can cause integumentaiy diseases.
Integumentary diseases can be prima1y or secondary to systemic
diseases or diseases of a specific organ including the liver, pancreas,
kidneys, gastrointestinal tract, hemopoietic system, endocrine sys-
tem, etc. However, malnutrition probably plays a bigger role in avi-
an integumentary diseases and as such, diseases of the skin caused
by malnutrition are probably under diagnosed. ln addition, diseases
of the avian integument have not received extensive investigation,
nor are they well characterized due to a variety of reasons. Certain
diseases of economic significance, such as cellulitis, avian keratoac-
anthoma (squamous cell carcinoma), and Marek's disease in broiler
chickens, and to a lesser extent, tumors in pet and exotic birds have
received more study.
Avian skin can be biopsied for evaluation. However, the thin-
ness of avian skin makes it difficult to prevent rolling and contrac-
tion of skin biopsy specimens during collection and fixation. A
modified skin biopsy technique for obtaining avian skin has been
described. In this technique, non-translucent self-adhesive tape
("Scotch tape") was attached to skin biopsy sites before obtaining
skin biopsies using a standard skin biopsy punch instrument. This
tape technique did not produce any appreciable artifacts and ensured
flat fixation of the biopsy specimen.
For proper evaluation, a paired biopsy of skin and feathers
needs to be obtained from affected and unaffected sites on the same
bird and fixed in IO % neutral buffered formalin . However, care
14
should be taken to immerse the skin as well as the feathers in forma-
lin completely either by covering the surface of the formalin with a
paper towel or gauze. Otherwise, feathers have a tendency to float
and may not fix properly. It is possible for fungi to grow in poorly
fixed feathers and give misleading results.
Anatomy
Avian skin is made up of primarily two main layers: epidermis and
dermis. The thickness of the skin in birds varies depending on the
part of the body. In parts where there are feathers, skin may be
only 3 or 4 cell layers thick, whereas parts of the feet where there is
no feathering can be many layers thick. Invaginations of the skin
form feather follicles but there are no glands associated with the fol-
licles . The only glands present in the avian skin are the uropygial
or preen gland (not present in all species), glands of the external ear
(ceruminous glands), and glands around the vent. The entire skin is
lipogenic and serves the same function as sebaceous glands in mam-
mals. Small bundles of smooth muscle, the erector feather muscles,
attach to the feather follicles, and control raising, lowering, and ro-
tating feathers. Herbst corpuscles (pressure receptors) are present in
the dermis adjacent to feathers , especially on the face.
Epidermis
Epidermis over most parts of the body is ext remely thin; usually 3
to 5 cells thick, but is much thicker over the unfeathered parts of the
legs and face . The epidermis is composed of two main layers. The
stratum corneum (cornified layer) forms the outer layer, while the
inner layer is the stratum germinativum (germinal layer). Three lay-
ers comprise the stratum ger111inativu111, but they are poorly defined
in histologic sections. From the dermis, they are the stratum ba-
sa/e (basal layer), stra/11111 spinosum (prickle cell layer), and stmtum
transitivum (transitional layer). The transitional layer is equivalent
to the stratum granulos11111 of mammals, but keratohyalin granules
are not obvious in sections stained with hematoxylin and eosin. The
cornified layer is composed of sheets of keratinized, anuclear, flat
cells that form lamellae, separated by lipids. It is thickest in the
scales on the legs and plantar surface of the feet. Avian keratino-
cytes are unique in that they produce lipids.
Scales, claws, and beaks have a structure similar to that of the
thick epidermis of the feet, but the keratin components are harder due
I
to thicker layers of keratinized cells in the presence of free and kera-
tin-bound calcium salts. The epidermis of the comb is similar to that
of thick skin while the dermis is composed of a superficial vascular
Avian Histopathology (4 th Edition) I 615
 H. L. Shivapmsad • H. John Bames
layer, a wide intermediate layer, and a thick collagen layer. When the
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comb and wattle are red, the superficial dermis contains large sinus
cavities immediately below the epidermis. A sternal bursa is located
in the subcutis over the anterior ventral aspect of the keel bone in
chickens and turkeys. The lining of the bursa is composed of a typi-
cal synovial membrane, thrown into folds at the edges, which is lined
by cuboidal or squamous cells towards the edges.
Feathers
For the arrangement, types, development, growth, structure, and
microscopic appearance of feathers, see the description by Lucas
and Stettenheim (1972) . Feather a1Tangements are described asap-
terium , pterylae, ptery losis, and ptilosis. The feather is composed of
a shaft, vane, and an after feather. Pulp is the mesodermal compo-
nent of the growing feather consisting of vascu lar connective tissue.
Pulp regresses as the feather grows and is absent in mature feathers.
About 10 feather types are recognized : contour feathers, coverts,
remiges, rectrices, down feathers, powder downs, semiplumes, bris-
tles, semibristles, and piloplumes.
Invaginations of the embryonic epidermis form the feather fol-
licles and feather growth occurs in cycles. Regenerating feathers
grow upward from a dermal papillae pushing the old feather out, or
replacing a feather that has been plucked. In the resting phase, the
feather is held in the follic le by tension exerted on the follicle by the
erector feather muscles and keratin bridges between the follicular
and feather epidermis .
There are two basic components of the feather, the outer epider-
mis, and the inner pulp. The epidermis differentiates into barbed ridges,
rachis, and hyporachis as it grows longitudinally. It also develops later-
ally from a basal layer to a keratinized layer, which becomes the feather
sheath. The follic le epidermis develops laterally to form a stratified
squamous keratinizing epidermis but it develops towards the feather so
that the two keratinized smfaces are opposed to each other, but eventu-
ally separate towards the neck of the follicle. The pulp develops with in
the epidermis and is covered distally by the pulp cap. As the feather
grows longitudinally, the pulp regresses by degeneration and resorption
of the connective tissue. Degenerative changes in the pulp inunediately
below the pulp caps can be quite marked. Necrosis, edema, hemor-
rhage, and acute inflamn1ation are normal, but any form of inflamma-
tion deeper in the pulp is abnormal. The keratinized pulp cap remains,
the new distal end of the pulp is re-epithelialized and the process is
repeated. Many pulp caps disintegrate as they are exposed, but others
remain and are sti ll visible in the calamus (qu ill). The calamus becomes
completely keratinized when longitudinal growth is completed. Cell
division occurs mostly at the base of the feather where germ and basal
cells first differentiate as they move upward. Accordingly, the distal
and peripheral pat1s of the growing feather are more fully developed
than the proximal and central pai1s. The tips of the barbs (and the ra-
chis, if any), are formed before the bases and, in feathers with a rachis,
the barbs at the distal end are formed before those at the proximal end.
Paradoxically, although the proximal and central pat1s of the grow ing
I
feather are younger and less folly developed than the more distal pat1s,
they represent the latest stage in the histo1y of the feather as a whole.
This sequence must be kept in mind when studying factors that affect
the appearance of the feather as a whole.
616 I American Association of Avian Pathologists
Skin and feather colors
Color is due to pigment, structural conditions, and combinations
of these according to Lucas and Stettenheim. The pigments are
melanin, keratinoids, and porphyrins. Melanin is produced by me-
lanocytes, which migrate into the epidermis during development.
Melanin is very prominent in silky chickens and cockatoos, which
is responsible for their black skin.
Response to Injury
Similar to mammals, avian skin can undergo various changes in-
cluding acanthosis, acantho lysis, hyperkeratosis, parakeratosis, dys-
keratosis, hypertrophy, hyperplasia, hydropic (ballooning) degen-
eration, spongiosis, macule, papule, pustule, degeneration, necrosis,
ulceration, various forms of inflammation, neoplasia, fo llicu lar
dysplasia, vasculitis, and hypersensitivity. However, certain dis-
eases or conditions such as hypersensitivity dermatitis, vasculitis,
and autoimmune skin disease have not been well described and are
probably rare.
lnflammatmy reactions in the avian skin, pat1icularly in chick-
ens have been studied using various irritants (turpentine), infectious
agents (Staphy/ococc11s) , non-infectious but immunogenic agents
such as Freund's complete adjuvant, and relatively immunologically
inert particulates e.g., talc. It appears that the qualitative nature of
the reaction is the same, irrespective of the stimulus. Experimen-
tally induced type III hypersensitivity such as an At1hus reaction has
been described in chicken skin.
Genetic Disorders
Inherited ski n abnormalities including avian ichthyosis, scleroder-
ma, and autoimmune vitiligo in the Smyth line chicken, albinism,
and others occur in chickens. Avian ichthyosis occurs as an auto-
somal recessive trait in chickens. The disease is characterized by
thickened irregular patches of skin with stiff, wiry, down feathers,
and a greasy exudate. Histologically, the epiderm is is up to four
times normal thickness due to acanthosis and hyperkeratosis.
Scleroderma is an inherited spontaneous autoimmune disease
in a line of White Leghorn chickens. Affected chicks are normal at
hatching, but by 1 to 2 weeks of age, 90% of birds develop erythe-
ma, edema, necrosis, subsequent loss of the comb, and joint swell-
ing. From 4 to 6 weeks, lesions appear in the skin on the back of
the neck and in the esophagus, small intestine, lung, kidney, heart,
and testes. Grossly, the skin swells, loses feathers , and becomes in-
durated. Histologically, mononuclear cells infiltrate all layers of the
dermis, subcutis, and underlying muscles and there is marked vas-
cular proliferation and intense collagen deposition. Thickening of
the muscular wall and intimal proliferation occlude small arterio les
cause ischemia, which leads to sloughing of the comb and digits.
A mutant line of chickens, the DAM (Delayed Amelanosis)
line, which subsequently became known as the Smyth chicken, was
described in 1981. Amelanotic chickens have a high incidence of
spontaneous postnatal cutaneous amelanosis and blindness. The
Smyth line of chickens is a useful animal model for studying vitiligo
in humans. Immunologic studies in these chickens have suggested
that an autoimmune reaction is associated with the changes in the

skin and eye. Further, it has been suggested that cell mediated im-
munity plays a more important role than humoral immunity.
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Complete albinism due to a recessive autosomal gene and im-
perfect albinism due to a single sex-linked recessive gene occurs in
chickens and turkeys. Birds with albinism also lack pigment in the
retinal epithelium, which causes them to be blind. A genetic defect
also may cause white plumage in zebra finches.
An unusual skin disorder characterized by dermolytic, blister-
ing, skin peeling, and loss of feathers occurs in ostriches. Histo-
pathology and electron microscopy of the skin show subepidermal
bulla secondaiy to splitting of the sublaminar densa. Based on epi-
demiology, clinical, and pathologic findings, it is genetically related
to dermolytic mechanobullous disease.
A lethal mutation in domestic fowl characterized by absence of
an upper beak and eyelids is associated with an autosomal recessive
gene having complete penetrance.
A developmental disorder, ' feather cysts ' commonly occur in
canaries, especially the Norwich strain, and other species of birds.
Occasionally, older broil~r breeders that have lost most of their
feathers during the production cycle have feather cysts. Cysts are
caused by dysplastic feather and feather follicle growth. They can
be single or multiple and are present as hard yellow lumps within,
and projecting from the skin. Cysts are lined by stratified squamous
epithelium, which in places often has the characteristic ofa develop-
ing feather epidermis in that barb ridges and even keratinized struc-
tures resemble pulp caps.
Nutritional Disorders
Lesions in the skin and feathers have been described primarily in
poultry species due to deficiency of biotin, pantothenic acid, folic
acid, nicotinic acid, zinc, manganese, tryptophan, vitamin A, Vita-
min E, protein, and amino acids.
Skin lesions of biotin deficiency occur at the commissure of
the beak (rictus) and on the plantar surface of the feet. Histologi-
cally, there is epidermal hyperplasia, papillary growth, acanthosis,
and hyperkeratosis on the foot and sides of the toe. Cells of the
stratum spinos11111 enlarged nuclei with prominent nucleoli and in-
creased mitotic figures . There is increased vascularity and dermal
vessels are engorged. This is followed by erosions, ulcerations, and
inflammation.
Hyperkeratosis and parakeratosis accompanied by heterophil
infiltration and mild dermal edema are associated with pantothenic
acid deficiency in chickens. The birds have gross lesions of thicken-
ing and fissuring of the skin of the rictus of the beak, eyelids, toes,
tarsus, and metatarsus. Epidermal hyperplasia with areas of marked
hyperkeratosis and parakeratosis of feather follicles and adjacent
non-follicular skin is associated with pantothenic acid deficiency in
quail. Focal dermatitis is also seen.
Focal hemorrhage and necrosis on the beak developed in broil-
er chicks fed diets deficient in tryptophan. The lesion of the maxil-
lary rhamphotheca was located on the culmen between the nares and
appeared as a crusty or scab-like area on gross examination. The
main histological observations of the beak lesions were epidermal
erosion and ulceration. In individual histologic sections, the bed of
the ulcer was filled with fibrin, red blood cells, and a few scattered
l11teg11111e11fa,y System
heterophils. Inflammation was occasionally observed at the dermal-
epidermal junction.
Experimental zinc deficiency has been studied in various spe-
cies of birds including chickens, turkeys, pheasants, Japanese quail,
and ducks. The basic skin lesions consist ofhyperkeratosis and ac-
anthosis in various parts of the body, including feet and rictus of the
beak. Hyperkeratosis can also involve feather follicles with atrophy
of follicles and feathers or failure of feather development. Follicles
are eventually replaced by fibrous tissue. In ducks, the lesion occurs
deep in prickle cells adjacent to the basal layer of the epidermis.
Basal cells enlarge and resemble prickle cells and mitotic figures
are increased in the deep prickle cell layers rather than in the basal
layers. Spongiosis of the epidermis and ballooning degeneration,
dyskeratosis, acantholysis of individual keratinocytes, and bullae
that contain acantholytic cells and heterophils are seen. Heterophils
may be present diffusely throughout the epidermis. Erosion of the
epithelium is associated with formation of superficial crusts contain-
ing secondary bacteria and inflammation in the dermis.
A condition called ' clubbed down ' in broilers is associated with
zinc, and possibly, manganese deficiency. The disease is charac-
terized by short, abnormal down feathers that have a characteristic
bilaterally symmetrical distribution. Histopathology of the skin in
2-day-old embryo reveals a lack of mitotic figures in the stratum
inten11edi11111 , ballooning degeneration, and necrosis of basilar cells
in the stratum spinos11111. Barb ridges are disorganized as feathers
develop and the feather shaft is thick. At hatching, feathers contain
an abnormally large amount of pulp. Endothelial proliferation, en-
dothelial degeneration, perivascular edema, hemorrhage and fibro-
sis, and infiltration of heterophils and mononuclear inflammatory
cells in the pulp and perifollicular dermis may occur.
Hyperkeratosis of the epidermis and feather follicles occurs in
poultry that are deficient in vitamin A. Exudative diathesis charac-
teri zed by accumulation of green, brown, or red fluid under the skin
is a classic lesion of vitamin E and selenium deficiency in chickens.
Exudative diathesis needs to be distinguished from subcutaneous
edema, which is clear to pale yellow, and caused by hypoprotein-
emia in newly hatched birds exposed to excess humidity during in-
cubation. Nickel deficiency has been associated with altered shank
skin pigmentation associated with a decrease in yellow lipochrome
pigments in chicks. Footpad dermatitis has been associated with
methionine deficiency in turkey poults. Many amino acid deficien-
cies or imbalances have been described as causing abnormal feath-
ers but histopathologic descriptions are lacking.
Toxicities
Skin and feather lesions in birds due to toxicities are not well de-
scribed or well understood. Mycotoxins such as T-2 toxin and di-
acetoxyscirpenol of F11sari11111 sp. have a radiomimetic effect and
produce lesions in feathers as well as in other organs. Lesions con-
sist of necrosis of cells in the epidermal collar, rachis, and barbed
ridges of the feathers . Necrosis of cells of the stratum germinati-
v11111 of the neck of the feather follicles also occurs. Degenerative
changes in growing feather quills, followed by hemorrhage into
the feather pulp, occurred in chickens and Japanese quail fed diets
containing excess vitamin A, but microscopic lesions have not been
Avian Histopathology (4 th Edition) I 617
 H. L. Shivapmsad • H. John Rames
described. Feather malformations including retarded growth and
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curved feathers were induced by exposing 10 to 12 day chick em-
bryos to cadmium chloride.
Selenium toxicity in various species of birds including aquatic
birds has an effect on various organs, including feathers. Gross le-
sions consist of bilaterally symmetrical alopecia of the scalp and
dorsal cervical midline, broken or lost digital nails, and necrosis of
the tip of the beak. Histologic lesions in digital and maxillary nails
included single cell to full thickness necrosis of keratinocytes and
multifocal parakeratosis of the stratum corne11111. Lesions in feath-
ers included mild necrosis of the epidermal collar, inflammation of
feather pulp, and follicular keratosis. Deformed beaks and abnor-
mal eyes were observed in pheasant chicks hatched from pheasant
breeders suffering from selenium toxicosis.
Furocoumarins are well known photosensitizers that are most
prevalent in the parsley fami ly. Various avian species: duck lings,
geese, turkeys, and chickens show signs of photosensitivity when
exposed to sunlight after ingesting weeds or seeds containing pho-
toactive compounds in A111111i 111aj11s, A. visnaga, and Cymopterus
watsonii. With some variation between species, lesions consist of
fluid-filled vesicles and scab formation on the beak and feet, and he-
matoma formation and sloughing of tissue debris. This is followed
by loss of feathers in the periorbital region and other areas of the
head. Chronic changes consist of deformities of the beak and feet.
Histopathologic lesions are unknown. Seeds of C. longipes also
cause similar lesions, including multiple lesions on the comb, legs,
and keratoconjunctivitis.
Dry gangrene of the toes, comb, associated with sloughing of
the tissues can occur due to ergotism. Histological lesions consist of
epidermal necrosis and vascular necrosis in the dermis.
Concanavalin A induced cutaneous reaction in the chicken is
characterized by increased vascular permeability, marked accumu-
lation of basophils, and perivascular aggregations of lymphocytes.
Other changes include acanthosis, hypertrophy, and hyperplasia of
vascular endothelium. Cyclophosphamide interferes with feather
growth and barb development in chickens resembling 'nakanuke'
feathering . Experimental injection of chick embryos with retinoic
acid between 10 and 12 days of incubation induces feather forma-
tion on the scales of the dorsal and ventral surfaces of the feet. De-
layed type skin reactions to oxazolone can be induced in chickens
sensitized 7 days prior to challenge.
Thyroxine plays an important role in feather growth and de-
ve lopment. Hypothyroidism causes abnormal feathers, which are
elongated with loss ofbarbules that resemble immature down feath-
ers. In the ' obese strain' of chickens that develop autoimmune thy-
roiditis, feathers have a lacy or silky appearance. Increased levels
of thyroxine in the diet induced molt in chickens between 7 and 13
days after feeding. Similarly, low salt and increased zinc can also
induce molt in chickens.
Infections
Viral i11fectio11s
I A number of viruses cause lesions in the skin and feathers in birds.
Certain viruses, such as avian poxvirus, have a predilection for epi-
thelial cells and others such as circovirus, which causes beak and
618 I American Association of Avian Pathologists
feather disease in psittacines and other birds, has a predilection for
primarily feathers. Alpha herpesvirus in chickens, wh ich causes
Marek's disease, multiplies in the feather follicle epithelium.
Avian pox
Avian pox is a slow-spreading viral disease of chickens, turkeys,
quail , pigeons, canaries, raptors, psittacines, and numerous wild
birds . The etiology is poxvirus of the genus Avipox . Many
strains of the virus are recognized including fowl pox, turkey
pox, pigeon pox, canary pox , etc. Pox on the skin is commonly
called the dry form of pox . Generally, lesions occur in unfeath-
ered areas of the skin but occasionally feathered parts of the body
may be involved. Papilloma-like and tumor- like lesions due to
pox virus occur on the head, legs, feet , and toes of raptors , canar-
ies, crows, ostriches, peafowl, pheasants, flamingoes , etc. Mi-
croscopically, lesions are characterized by marked hypertrophy
and hyperplasia of epidermal cells, many of which undergo bal-
looning (hydropic) degeneration and often contain intracytoplas-
mic eosinophilic inclusion bodies called Bollinger bodies . Inclu-
sions can be large and compress the nucleus to the side. Often
they contain vacuoles due to their high lipid content. Fat stains
are a useful aid for identifying pox inclusion bodies. The com-
bination of epithelial cell hyperplasia, ballooning degeneration,
and intracytoplasmic eosinophilic inclusion bodies is diagnostic
for avian poxvirus infection .
Marek's disease virus
Lesions due to Marek's disease virus (MDV), an alpha herpesvirus,
occur in most organs. Lesions in the skin are primarily associated
with feather follicles where viral replication takes place. The virus
infects the cells of the follicular epidermis, the dermis adjacent to the
affected epidermis, and feather pulp. The earliest lesion is the ap-
pearance of intranuclear inclusion bodies in cells of the transitional
zone and stratum corneum of the follicular epidermis of the feather
follicle . Syncytial cells are not a feature of MDV infection. Inclu-
sions are eosinophilic to amphophilic and can be large and fill the
nucleus, with margination of chromatin. In feather pulp, lesions can
range from lymphoid cell infiltrates to lymphoma formation . How-
ever, the most frequent lesions in Marek's disease of the skin occur
in the dermis. They begin as aggregates of small lymphocytes in the
dermis adjacent to affected feather follicle epidermis. The number
and size of lymphoid aggregates increase with post-exposure time
and eventually coalesce. Lymphocytes are seen behveen vessels of
the follicular vascular bed, between and replacing erector feather
muscles, in feather follicle epidermis, and interfollicular connective
tissue, fat, and nerves. Neoplastic transformation occurs in some of
these sites as the larger aggregates contain more neoplastic medium
and large lymphocytes and blast cells. Neoplastic lymphoid cells
gradually replace dermal structures and cause atrophy of feather fol-
licles and skin epidermis.
Several other avian herpesviruses, including infectious la-
ryngotracheitis virus of chickens, psittacine herpesviruses, pigeon
herpesvirus, finch herpesvirus, raptor herpesvirus causes blepharo-
conjunctivitis characterized by presence of intranuclear inclusion
bodies in the conjunctiva! epithelium and inflammation . Cloacal

papillomas and papillomas of the crop and feet in psittacines have
been associated with herpesvirus-like and herpesvirus sequences in
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psittacines, but no cause and effect relationship has been demon-
strated between the virus and papillomas.
Highly pathogenic avian influenza virus and Newcastle disease
virus can cause lesions on the comb, face, wattles, eyelids, neck, and
shanks characterized by acute multifocal to severe diffuse necrotiz-
ing dermal inflanm1ation, edema, hemorrhage, and focal epidermal
vesicles in the wattles. Other lesions including diffuse congestion
and petechiation of the skin, edema of the face and eyelids, and
microvesicles, hemorrhagic ulcers, and bullae on the combs can oc-
cur. In some birds, vasculitis in the dermis is a prominent feature.
Both Newcastle disease and highly pathogenic avian influenza virus
cause pterylitis characterized by mononuclear cell infiltration within
the pulp cavity with presence of viral antigen in the cells lining the
follicular epithelium as well as the mononuclear inflammatory cells.
Similar lesions have also been seen in the feathers of pigeons due
to pigeon paramyxovirus-1 and in various species of birds including
corvids and psittacines du,e to West Nile Virus infection.
Circovimses
Various circoviruses affect a variety of species of birds, but the most
common and significant disease is psittacine beak and feather dis-
ease (PBFD). PBFD is a viral disease of many species ofpsittacines
characterized by chronic feather and beak dystrophy. Microscopic
changes are in the epidermal collar, developing rachis, barb ridges
of growing feathers, feather pulp, and occasionally feather follicle
epidermis and dermis . Lesions are not normally seen in the interfol-
licular epidermis of the skin. The basic lesion is epidermal cell ne-
crosis, which varies from being focal and involving only a few cells
to more extensive lesions with cleft formation and separation of the
epidermis from the pulp. The basal layer often appears disordered
due to hyperplasia. Macrophages with conspicuous purple intracy-
toplasmic inclusion bodies of variable size and number per cell may
be present in the epidermis and pulp. These inclusions are often
called botryoid or morula inclusions. Changes within the pulp can
range from mild to severe inflammation characterized by infiltra-
tion of heterophils, lymphocytes, plasma cells, and less frequently,
multinucleated giant cells. Pulp lesions in PDFD need to be differ-
entiated from physioiogic necrosis and inflammation that occurs as
the feather grows. Occasionally, distinct intranuclear eosinophilic
inclusion bodies are seen in the epidermal cells of both the feathers
and skin. Lesions of the beak are most common in cockatoos and
are necrosis of epidermal cells and accumulation of macrophages
with purple intracytoplasmic granules in and below the epidermis.
Necrosis results in separation of the cornified layers, fluid accumu-
lation, and often infiltration by inflammatory cells . Chronic inflam-
mation is common.
Poly o11,avin1ses
Polyomaviruses cause a generalized disease called Budgerigar
Fledgling disease (BFD), often with significant feather abnormalities
in psittacine birds and occasionally in finches. Lesions due to BFD
occur in many organs, including skin, feather follicles, feathers, and
uropygial gland. Microscopically, nuclei of affected epidermal cells
I11teg11111e11tm:1• System
are enlarged (karyomegalic) and basophilic and have a clear center
containing faintly basophilic material with marginated clu·omatin.
Affected cells often undergo cytoplasmic vacuolar (ballooning) de-
generation and occasional dyskeratosis. Cytoplasmic distention with
basophilic globules and acanthosis and hyperkeratosis may be seen.
Dermal and epidermal hemorrhage is also conunon.
Papil/omaviruses
Papillomaviruses have been associated with papillomas on the feet,
rictus, and face of passerine birds. Papilloma and proliferative skin
lesions, as well as hyperplastic epithelium with large nuclei but no
distinct inclusion bodies, occurred in an African Grey parrot. Papil-
lomavirus has been demonstrated in a papilloma of the eyelid in an
African Grey parrot and from the skin of feet in wild bird species
(chaffinch), Fringilla coelebs. The nonneoplastic proliferative dis-
ease in chaffinches is called 'tassel foot ' .
Other viruses
Other viruses that cause skin and feather abnormalities include
chicken infectious anemia virus (gyrovirus) associated with blue
wing disease (severe gangrenous dermatitis involving the ends of
the wings), hemorrhagic enteritis virus (siadenovirus) associated
with subcutaneous hemorrhages in turkeys and abnormal feathers
in psittacines, and enteric viruses, (e.g. , astrovirus, rotavirus, coro-
navirus) associated with poult enteritis complex that cause poor
feathering and skin pigmentation in turkey poults. Other diseases
of the avian integument associated with viruses include infectious
atrophy of the beak due to parvovirus in ducklings and calicivirus
causing vesicular lesions on the webbing between the toes of white
tern chicks.
Retroviruses of the leukosis-sarcoma group cause fibromas , fi-
brosarcomas, myxofibrosarcomas, and hemangiomas in the skin of
chickens. Fibromas are firm , white, and composed of interwoven
bundles of dense or loosely arranged fibroblasts and collagen fibers .
Occasionally they may contain cartilage and bone. Fibrosarcomas
can locally infiltrate and may metastasize to various organs includ-
ing liver, kidney, heart, pancreas, and intestine. Hemangiomas oc-
cur as single or multiple nodules, several millimeters in diameter in
the skin. They may be composed of obvious, but thin-walled, ir-
regularly shaped, blood vessels or less well differentiated masses of
endothelial-like cells in thin, irregular clefts. The overlying dermis
may be edematous and hemorrhagic. Another virus of the leukosis-
sarcoma group causes Rous sarcoma (transmissible myxosarcoma).
A disease similar to lymphoid leukosis in turkeys, chickens,
geese, ducks, quail, and pheasants results from reticuloendothe-
liosis virus (REV, retrovirus) infection. REV also causes pox-like
lesions composed of neoplastic lymphocytes in the dermis on the
head of turkeys. REV virus has been associated with a feather-
I
ing abnormality ('nakanuke') of young chickens characterized by
increased transparency of the calamus and rachis, loss of proximal
barbs, and sparseness of the vane in primary and secondary flight
feathers. Histopathology reveals necrosis of individual or clusters
of cells in germinative layers of epidermis of the rachis and barb
ridges. Cells in the barb ridges are disordered and mild inflamma-
tion is seen in the pulp.
Avian Histopathology (4'" Edition) I 619
 H. L. Shivapmsad • H. John Eames
Bacterial infections
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Bacterial infections in the skin tend to be similar, characterized by
fibrinoheterophilic inflammation with or without intralesional bac-
teria. Depending on the stage of infection, lesions can have mul-
tinucleated giant cells surrounding a coagulum of fibrin, necrotic
debris, and degranulating heterophils (heterophilic granulomas).
Swollen-head syndrome in chickens is a facial cellulitis, usu-
ally due to E. coli, that is secondary to either pneumovirus or coro-
navirus infection or exposure to high levels of aerial ammonia. The
disease is characterized by hyperemia of conjunctiva, subcutaneous
edema, and caseous exudate in the subcutis of the skin of the head.
Histologically, there is edema, heterophil infiltration, and lymphoid
hyperplasia. Pasteure!la 11111ltocida can also cause similar lesions
in turkeys.
Cellulitis is a condition commonly seen in broiler chickens
and, less frequently, turkeys at processing that is characterized by
extensive lesions in the subcutaneous tissue. Cellulitis usually fol-
lows wounds, especially scratches, but also can result from navel
infections early in life. Exudate gravitates to dependent areas of the
body resulting in lesions in the legs, groin, and hips. Lesions else-
where, including breast, abdomen, and back, may occur, but are less
frequent. Lesions are associated with bacteria; most often£. coli is
isolated. Microscopically, lesions are characterized by fibrinohet-
erophilic inflammation in the dermis with edema associated with
intralesional Gram-negative bacteria. Lesions can be extensive and
extend into the epidermis and underlying muscle.
Inflammation of the wattles similar to cellulitis with resultant
swelling in chickens is a characteristic lesion of Paste11re!la 11111lto-
cida infection (fowl cholera). Similar lesions can occur with Staph-
y lococcus and£. coli infections. Staphy lococcus dermatitis occurs
occasionally in birds and may involve feather follicles in addition
to the skin.
Acute exudative dermatitis, particularly in the head and neck,
has been described in broiler chickens. Subcutaneous tissues are
swollen and contain serosanguinous exudate from which pure cul-
tures of Staphylococcus a11re11s can be isolated. In addition, out-
breaks of acute vesicular dermatitis of the comb, wattles, face, feet,
and shanks from which staphylococci and Paste11re!la sp. are isolat-
ed affects egg-laying chickens. Lesions include necrosis of epide'r-
mal cells, epithelial hyperplasia, hyperemia, vesicle formation in the
epidermis, and hemorrhages with fibrin tluombi in the underlying
dermis of the comb. Similar lesions are seen in septicemia.
Gangrenous dermatitis of chickens and turkeys is caused by
infection with either Clostridi11111 septicum or Staphylococcus a11-
re11s, alone or in combination . Clostridium pe,ji-ingens type A,
and £. coli, Proteus sp., Enterococc11s faecalis, and Bacillus sp.
have also been isolated from these lesions. The disease occurs
most commonly in broiler chickens, particularly those that have
no maternal antibody to infectious bursa] disease virus or chicken
infectious anemia virus. Wound infections may also occur. Le-
sions consist of black, purple, or dark green discoloration of the
I
skin and serosanguinous, sometimes emphysematous, exudation
into the subcutis of any area of skin, but particularly the wing tips,
thighs, and abdomen. Feathers fall out or are easily removed. His-
tologically, there is necrosis of the skin, accumulation of fluid , and
620 I American Association of Avian Pathologists
erythrocytes in the subcutis and necrosis of the underlying mus-
cle. Red cells tend to be lysed and there is a lack of heterophils.
Large, elongated Gram-positive rods or Gram-positive cocci are
seen in the lesion. Gangrenous dermatitis, secondary to a primary
infection of reticuloendotheliosis virus also has been described.
Bacteria such as Pse11do111onas aeruginosa and £1:vsipelothrix rlw-
siopathiae have been associated with severe dermatitis in broiler
chickens, and turkeys.
Enlargement of the sternal bursa, commonly called 'breast blis-
ters ' is a common occurrence, especially in heavy male turkeys, but
also can occur in heavy broiler chickens. Most of the time, the en-
largement of the bursa is due to chronic irritation. In such instances,
there is accumulation of fluid with proliferation of synovial cells,
subsynovial fibrosis, and a few inflammatory cells in the lumen.
In pet and exotic birds, mycobacteriosis clue to Mycobacteri11111
avi11111, M. genavense, or occasionally Iv!. tuberculosis can cause
granulomatous dermatitis characterized by infiltration of macro-
phages and a few giant cells in the subcutis. Macrophages and giant
cells usually contain numerous acid-fast bacteria in their cytoplasm.
Fungal infections
Inflammation of the skin can result from infection with a variety
of fungi including Candida albicans, C. glabrata, Aspergi!l11s spp.,
Rhodotorula spp. , Microspon1111 gallinae, Penici//i11111 cyc/opi11111,
lvfalassezia spp., Geotrichum candidum, etc. Thickened, yellow-
ish brown skin associated with Rhodotorula 11111cilagi11osa and R.
gl11tinis occurs in broiler chickens. Histologically, focal , multifocal ,
or diffuse areas of ulceration or acute inflammation in the dermis are
seen . Infections with Aspe1gi!l11s spp. or M11cor spp. cause thick,
scaly skin due to acanthosis and hyperkeratosis. Necrosis of epider-
mal cells, infiltration of the dermis with heterophils, intraepiclermal
vesicles that contain heterophils, and acute heterophilic dermatitis
may be present. Fungal hyphae are present in the cornified lay-
ers. Candida albicans causes dermatitis on the back of chickens
and combs of broiler breeders. Microscopic changes consist of epi-
dermal necrosis and inflammation. Yeas( forms and pseudohyphae
are present in cornified areas and necrotic tissues. Candida glabrata
is a common fungus associated with hyperkeratosis of the epider-
mis and feather follicles in various species of birds. Combined C.
albicans and A. flavus infection has been associated with n~dular
granulomatous dermatitis in chickens.
Favus in chickens due to Microsporum gal/inae is rare in com-
mercial chickens but affects hobby chickens in small flocks . Histo-
logic lesions include hyperkeratosis of the epidermis with invasion
of the stratum corneum by fungal mycelia, acanthosis, acantholysis,
and hydropic degeneration of cells in the stratum spinosum. The
underlying dermis is infiltrated by mononuclear inflammatory cells
and contains lymphoid foci. Fungi can also be seen in feather fol-
licles associated with hyperkeratosis. Feather damage characterized
by changes in the rachis and pulp cavity has been associated with
eight different orders of fungi in wild turkeys. Geotrichum candi-
d11111 was isolated from the skin of three flamingoes , which were
suffering from extensive necrosis, and inflammation of the skin
of the webs and legs. Abundant mycelium and arthrospores were
demonstrated in the altered dermis and epidermis of the flamingoes.

Fungi of Jvfalassezia spp. have been demonstrated on the skin of
psittacine birds with feather destructive behavior. Penicil/i11111 cy-
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clopi11111 caused a localized infection of the beak in a macaw that
was characterized by focal destruction of the corneal layer in the
upper zone of the beak. Similarly, severe destruction of both lower
and upper beaks associated with A ..fwnigatus occurs in psittacines.
Cutaneous pythiosis caused by Pythi11111 insidios11111 affected the
skin of a nestling White-faced ibis. Gross lesions included multi fo-
cal ulcerations of the skin over the wings, neck, head, and limbs.
Histopathology revealed intense, necrotizing, eosinophilic, granu-
lomatous inflanunation associated with large, hyaline, and pauci-
septate hyphae.
Parasitic infestations
Most parasites that cause skin lesions in birds are mites; lice, fleas,
ticks, and other biting or stinging artlu·opods are less likely. Other
parasites, such as the trematode, Collyric11/11111.faba is found in cysts
in the subcutaneous tissues of free-living birds. Pelecifus spp., are
filarids that occur in the subcutaneous tissues of the legs and neck of
several species of birds including pigeons and owls. Other filarids
include Aviose1pe11s, Ornithofilaria, Si11gl?filaria, and Splendido-
.filaria. Microfilaria in the subcutaneous tissue of various species
of birds are usually associated with minimal or no inflammation.
Exo-erytlu·ocytic meronts ofhemosporidia may be found within the
endothelium of dermal vessels, including feather pulp, and occlude
the vessels causing necrosis of the overlying epidermis and ulcer-
ative dermatitis.
Numerous species of mites infest most, if not all, species of
birds. Mites include feather mites, quill mites, subcutaneous mites,
etc. They reproduce on or in the host or in the nest and feed on
blood, tissue fluid, skin, feather lipids, debris, keratin, fungi, al-
gae, or other mites. Mites may spend their entire life cycle on the
bird or live in the bird 's environment, intermittingly feeding on the
bird. They are transmitted directly from bird to bird. Some of the
important mites of the integument are Dem,anyss11s gallinae (red
mite), Omithonyssus sylviam111 (northern fowl mite), Kne111idocop-
fes 11111/ans (scaly leg and scaly face mites), La111inosioptes cysti-
cola (subcutaneous mite), which mainly infest poultry species, and
Knemidocoptes pilae, also called scaly leg and scaly face mites that
primarily affect psittacines. Numerous other mites have been identi-
fied and described in various species of birds, but their significance
is unknown.
In general, lesions caused by mites consist of severe hyper-
keratosis, hyperplasia of the epidermis, acanthosis, and occasion-
ally, inflammation of the dermis with accumulation ofheterophils
and vesiculation in the germinal layers. Atrophy of epidermis
around mites may occur. Knemidocoptes lesions occur on any un-
feathered parts of the skin and are characterized by typical raised
yellowish honeycombed encrustations on the cere, beak, face ,
eyelids, ("scaly face") and less commonly on the legs, digits, and
vent of psittacine birds and on the legs and feet ("scaly leg") of
gallinaceous and passerine birds. Northern fowl mites, Ornitho-
nyssus sylviaru111 commonly infest the feathers around the vent of
chickens, causing severe black discoloration of the feathers and
dermatitis. Subcutaneous mites are seen in various species of
J11teg11me11tmJ1 System
birds and appear as small grains of rice, white to crea m in color.
Mites are often surrounded by connective tissue or, if old, they
are calcified.
Dermatitis due to ectoparasites such as larvae of trombiculid
mites (chiggers), and various species of birds appear as non-pruritic,
edematous swellings of the skin of the legs, dorsal to the hocks, and
in some cases abdominal thoracic skin. Microscopically, lesions
consist of severe subcutaneous edema, areas of intense acute inflam-
mation, perivascular accumulation of lymphocytes, and in cluonic
stages, severe fibrosis. The areas of acute inflammation are associ-
ated with the attachment of larvae. At the point of attaclunent, there
is necrosis of epidermis, deposition of amorphous, eosinophilic ma-
terial, infiltration of heterophils, and necrosis of blood vessel walls.
The mites are often enclosed within ski n due to swelling of the skin
around the mite . Quill mites of Syringophilus sp. and Dennogly-
phus sp. are commonly seen within the calamus of feathers but ex-
cept for breakage of feathers, they do not cause significant lesions.
Histologic responses due to lice, fleas, and tick infestations of
the skin and feathers are minimal. The chicken body louse, Jvfe-
nacanth11s stra111ine11s, and the shaft louse, Menopon gallinae are
ectoparasites of older commercial chickens in layer and breeder
flocks as well as in backyard chickens. Female lice glue their eggs
(nits) to host feathers . These eggs are usually attached to the in-
side of the most distal portion of the calamus or most proximal
portion of the rachis .
Fleas are rare in commercial chickens, but they do occur in
backyard flocks. The stick tight flea, Echidnophaga gallinacea, also
known as the tropical hen flea and the chicken flea , can cause der-
matitis with severe lymphoplasmacytic inflanunation in the dermis
with visible embedded flea mouth parts. Fowl ticks, such as A,gas
persicus are rare pests of commercial poultly. Dermatopathology
due to ticks is not known, but ticks are known to feed on blood, and
can cause anemia. In addition, ticks transmit various bacterial and
rickettsial diseases.
Stings from the imported red fire ant (Solenopsis invicta) de-
bilitate birds, reduce their reproductive ability, and cause mortality
in young birds . Circular pale foci mainly on the feet and legs are
seen grossly. Similar lesions may be found in the oropharynx if the
bird is eating the ants. Microscopically,.the initi11l. le.s ion consists of
congestion and edema. Subsequently, focal necrosis characterized
by tissue lysis that extends tluough the epidermis into the dermis is
seen. Margins of the lesion are well delineated . Few, if any inflam-
matory cells are present. The lytic lesion may expand slightly in the
dermis giving it a "flask-shape".
Miscellaneous Conditions
Fayoumi chickens develop feather amelanosis due to spontaneous
lymphocytic thyroiditis. Histologically, barbed ridges and barbule
cells of many contour feathers lack pigment or have abnormal pig-
ment clumping. Melanocyte abnormalities such as irregularities in
cell shape and bulbous swelling with thick and sho1t dendrites are
I
seen. In the pulp cavity, there is marked infiltration of lymphocytes
and macrophages, especially around blood vessels. Dermal and
adipose melanization due to melanocytes in the abdominal wall can
cause downgrading of broiler chickens at processing.
Avian Histopathology (4 th Edition) I 621
 H. L. ShiV(ljJl'(IS(ld • H. John B(lmes
A skin and feather disease of unknown etiology is described in
VetBooks.ir
female silver spangled Hamburg and silver Sebright bantam chick-
ens. In the silver spangled Hamburg bantams, feathers on the ven-
tral neck and the first 5 secondary wing feathers have bent shafts
which eventually break in half, leaving an area of broken feathers .
Only the shafts of the feathers are damaged. Clinical signs are most
severe in young birds in which the entire ventral neck and breast
is affected. Microscopic lesions include mononuclear perivascular
dermatitis and perifolliculitis. The silver Sebright bantams develop
ba ldness under the earlobes or broken feathers on the back.
Granulomatous dermatitis most commonly affects Peach-faced
lovebirds. Histologically, skin nodules are composed of lympho-
cytes, macrophages, epithelioid cells, and multinucleated giant cells
around feather follicles and blood vessels within the deep dermis.
Endothelial cells of vessels within the aggregates are both hyper-
trophic and hyperplastic; some granulomas appear to be surrounded
by a fine connective tissue capsule. The epidermis overlying the
inflammatory exudates is acanthotic. Lesions within the feathers
and feather follicle epithelium are typical for psittacine beak and
feather disease.
Granulomatous inflammation of the dermis is conunon in poul-
tty due to faulty vaccination or vaccines contaminated with bacteria .
Often, these vaccines contain oil , which can elicit a foreign body
reaction. In most cases, the white vaccine emulsion is seen grossly
within the dermis and subcutaneous tissues. Accumulation of ho-
mogenous eosinophilic material in the dermis of waterfowl char-
acteristic of amyloid has been observed. Dermatitis of the hip and
thigh in broilers, also called scabby-hip, and scratches on the back
of broiler chickens have been described and are probably related to
stocking density and mobility of the birds.
Feather loss or destructive behavior (persecution) and self-
mutilation of the skin are common problems in confined birds par-
ticularly chickens and psittacines. A number of causes have been
proposed such as mycotic, bacterial, viral, parasitic, hypersensitiv-
ity, hormonal, hepatic, pancreatic, psychogenic, as well as genetics.
Lesions can range from mild exudative epidermitis to marked acan-
thosis, necrosis of the epidermis, ulceration, and extensive fibrino-
heterophilic dermatitis. Lymphocytes, occasional plasma cells, and
histiocytes with fibrosis and granulation tissue are found depending
on the stage and severity,of the condition. It should be pointed out
that feather picking-and cannibalism are separate phenomena. Can-
nibalism may be divided into vent picking and cannibalism affecting
other parts of the body. Feather picking in chickens has been related
to behavior and various developmental traits attributed to genetics.
Normally a single feather is associated with a feather follicle.
In polyfolliculosis, up to six feathers that may be in different stages
of maturation emerge from a single follicle. In young birds short,
twisted tail feathers are seen. In older birds, feathers emerge from
nodular thickenings and tend to be short and thick with retained
feather sheaths. Inflammation is uncommon, but is associated with
pruriti s (psittacine pruritic polyfolliculitis, PPPF) when present.
I
Small psittacines (lovebirds, cockatiels, budgerigars) are mostly af-
fected; lesions are usually on the neck, thigh, and tail.
Dry gangrene of the toes, legs, and comb, associated with
sloughing of the tissues can occur due to frostbite.
622 I American Association of Avian Pathologists
Encapsulated calcium deposits in the skin (calcinosis circum-
scripta) that can be associated with granulomatous inflammation are
rarely seen in birds. Urate deposits may extend into subcutaneous
tissues over joints in birds with articular gout.
Neoplasia
Neoplasia due to viral diseases such as Marek's disease, lymphoid
leukosis, and reticuloendotheliosis has been described above (See
Viral diseases). However, there are numerous neoplasms of un-
lmown cause. Neoplasms in the avian integument have been report-
ed from various species of birds, but is most common in psittacines,
particularly budgerigars, and chickens.
Avian keratoacanthoma (formerly termed dermal sq uamous
cell carcinoma), is found in the skin of broiler chickens during pro-
cessing, which results in the affected carcass being condemned . The
tumor primarily affects the dermis. Lesions occur most commonly
in feather tracts on the back and sides. Lesions appear as single
to multiple craterous ulcers from a few 111111 in diameter to large
irregular coalescing lesions. Histologically, they are proliferative
outgrowths of feather follicle epithelium, cysts that originate from
dysplastic feather follicle epithelium, or hyperplastic feather fol-
licles that contain hyperkeratotic feathers. Ulcers are lined by epi-
thelium and filled with keratin, bacteria, sloughed epithelial cells,
and inflammatory cells. Cytokeratin profiles of tumor cells suggest
the tumors originate from feather follicle epithelium.
Squamous cell carcinomas occur in older birds. Tumors may
develop anywhere in the integument, including the legs and uropy-
gial gland. They also occur in the upper digestive tract. Tumors
are usually locally invasive, slow growing, and ulcerated. Histo-
logically, squamous cell carcinomas tend to be fairly well differenti-
ated composed of variably sized epithelial cells that often produce
whorls of cells with central keratinization ("keratin pearls"). Inva-
sion of the dermis is the most common manifestation of malignancy.
Soft tissue tumors such as fibromas, fibrosarcomas, myxomas,
myxosarcomas, hemangiomas, and hemangiosarcomas can occur in
the skin of chickens. Avian leukosis - sarcoma group viruses prob-
ably induce these tumors. Hemangiomas in the skin can occur as
single or multiple nodules, several millimeters in diameter. They
bleed easily and may be composed of thin-walled irregularly shaped
blood vessels or less well differenti ated endothelial-like cells with
thin, irregular clefts. Hemangiopericytomas in the subcutaneous tis-
sues are uncommon. They are composed of uniform spindle-shaped
cells with a fusiform nucleus, diffuse cluomatin and abundant cyto-
plasm, but indistinct cell borders are arranged concentrically around
small blood vessels.
Feather folliculomas of various species of birds including
chickens, turkeys, canaries (Norwich canaries), and owls, have been
described. Histologically, they consist of multiple cystic structures
with central lumens containing keratin debris and feather remnants.
They are lined by cuboidal to squamous epithelial cells with abrupt
keratinization and areas of disorganized feather follicle epithelium.
Adenoma and adenocarcinoma of the uropygial gland in chickens
as well as various other species of birds have been descri bed. Li-
pomas are not common in chickens but are conunon in psittacine
birds, particularly budgerigars. Often, they occur in the abdominal

and sternal skin and may be multiple. The tumors are composed
of typical adipocytes and may be encapsulated. Degenerative and
VetBooks.ir
inflammatory changes within the tumors are common and may re-
semble a xanthoma. Melanoma and mast cell tumors occurring in
the skin have also been described in various species of birds. Mast
cell tumors are composed of round to oval cells having distinct cy-
toplasmic metaclu·omatic granules and hyperclu·omatic nuclei with
a prominent chromatin ring. Mast cell tumors can metastasize to the
lungs. Neuromas appearing as firm pale yellow nodules have been
described at the tips of the beak following partial beak amputation
in chickens.
Tumors of the skin and soft tissues described in various species
of birds other than chickens include fibroma , myxofibroma, vascu-
lar hamartoma, hemangiolipoma, myelolipoma, papillomas, kera-
toacanthoma, pte1yloepithelioma (avian equivalent of mammalian
trichoepithelioma), basal cell carcinoma, squamous cell carcinoma,
fibrosarcoma , liposarcoma, and round cell sarcoma.
Xanthoma is a nonneoplastic mass that occurs in the subcutis
of various species of birds .including psittacines and chickens. It is
composed of cholesterol clefts, multinucleated giant cells, macro-
phages, and lymphocytes.
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Severe pododermatitis in broiler breeder hens housed on
pressure-treated slats. Avian Dis 38: 172-176.
Saunders, J. R. and A. A. Bickford. 1965. Clostridial infections in
growing chickens. Avian Dis 9:317-326.
Saunders, N. C. and G. K. Saunders. 1991. Malignant melanoma
in a budgerigar (Jvfelopsittacus undulatus). Avian Dis 35:999-
1000.
Sawyer, R.H. and L. W. Knapp. 2003. Avian skin development and
the evolutionaiy origin of feathers . J Exp Zoo! (Mo! Dev Evol)
298:57-72 .
Schulz, T. A., J. S. Stewart, and M. E. Fowler. 1989.
Knemidokoptes mutans (Acari: Knemidocoptidae) in a great-
horned owl (Bubo virginianus) . J Wild! Dis 25:430-432.
Sentfes-Cue, C. G. , B. R. Charlton, P. Woolcock, A. A. Bickford,
G. Cooper, and M. Bland. Atypical distribution of fowl pox
lesions in broilers. Avian Dis 54:1316- 1318.
Shlosberg, A. and M. N . Egyed. 1978. Photosensitization in
ducklings induced by seeds of Cymopterus watsonii and C.
longipes. Avian Dis 22 :576-582.
Sinha, B. K. , J. L. Vegad, and R. P. Awadhiya. 1987. Pathology of
concanavalin A-induced cutaneous reaction in the chicken. Res
Vet Sci 42:365-372 .
Smyth, J. R. J., R. E. Boissy, and K. V. Fite. 1981. The DAM
chicktfo: A model fo_r ~pontaneous postnatal cutaneous and
ocular amelanosis. J Hered 72: 150-156.
Sola S. C. , B. Borello B, and M. Castagnaro M. 1997. Occurrence
of cutaneous haemangiomas in chickens: Morphological
aspects. Avian Pathol 26:501-510.
I 626 I American Association of Avian Pathologists
Spalding, M. G., W. J. Wrenn, S. T. Schwikert, and J. A. Schmidt.
1997. Dermatitis in young Florida sandhill cranes ( Grus
canadensis pratensis) due to infestation by the chigger,
Blankaartia sinna11w1J1i. J Parasitol 83 :768-771 .
Spearman, R. I. C. and J. A. Hardy. 1985 . Integument. In: A. S.
King and J. McLelland (eds). Form and Function in Birds, Vol.
3. Academic Press: London. pp. 1-56.
Steinberg, H ., J. A. Pare, and J. Paul-Murphy. 2006 . A dermal
vascular hamaiioma in a sun conure (Aratinga solstitialis) . J
Avian Med Surg 20: 161-166.
Stettenheim, P.R. 2000. The integumentaty morphology of modern
birds -- an overview. Ame,: Zoo!. 40:461-477.
Swayne, D. E. and S. E. Weisbrode. 1990. Cutaneous mast cell
tumor in a great horned owl (Bubo vilginianus) . Vet Pathol
27: 124-126.
Tripathy, D. N . and W. M . Reed. 2013. Pox . In: D.E. Swayne el
al. (eds). Diseases of Po11lt1J', 13th ed. Wiley-Blackwell Press:
Ames, Iowa. 333-349.
Weinstock, D., M. T. Correa, D . V. Rives, and D . P. Wages . 1995.
Histopathology and epidemiology of condemnations due to
squamous cell carcinoma in broiler chickens in North Carolina.
Avian Dis 39:676-686.
Wellehan, J. F., Jr., C. B. Greenacre, G. J. Fleming, M. D. Stelter,
A. L. Childress, and S. P Terrell. 2009. Siadenovirns infection
in two psittacine bird species . Avian Pathol 38:413-417.
Wheeldon, E. B. and M. R. J. Culbertson.1982. Feather folliculoma
in the canaty (Serinus canarius). Vet Pathol 19:204-206.
Wight, P.A. L. and W. A. Dewar. 1976. The histopathology of zinc
deficiency in ducks. J Pathol 120:183-191.
Willoughby, D. H. , A. A. Bickford, G. L. Cooper, and B. R.
Charlton. 1996. Periodic recurrence of gangrenous dermatitis
associated with Clostridium septicwn in a broiler chicken
operation. J Vet Diagn Invest 8:259-261.
Yamamoto, Y. , K . Nakamura, M . Okamatsu, and M. Mase. 2008.
Avian Influenza (HSN I) replication in feathers of domestic
waterfowl. Eme,ging Infect Dis 14: 149-151.
Yu, M. , P. Wu, R. B. Widelitz, and C.-M. Chuong. 2002. The
morphogenesis of feathers. Nature 420 :308-312.
Zavala, G., B. Lucio-Matiinez, S. Cheng, and T. Barbosa . 2006.
Sarcomas and myelocytomas induced by a retrovirus related
to myeloblastosis-associated virus type l in white leghorn egg
layer chickens. Avian Dis 50:201-208.
Zhang, Y. and A. C. Gilliam. 2002. Animal models for
scleroderma : An update. Cul'/" Rheumatol Rep 4: 150-162.

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14.1. Skin. Normal. Chicken. Shown are the epidermis (E),
dermis (D), part offeather follicles (FF) and a Herbst corpuscle (H)
next to the follicle.
14.2. Footpad. Normal. Chicken. Note the thick epidermis (E)
with large amounts of surface keratin (K). D. Dermis.
I11teg11111e11f<11J 1 System
14.3. Skin and feather follicle. Normal. Chicken. Normal
feather follicle is prominent. The central pulp (P) is surrounded by
the pulp epithelium (PE). The feather sheath (FS) and epidermis of
the feather follicle (EF) are shown. A portion of the skin epithelium
is in the upper left corner of the image.
14.4. Skin and feather follicle. Normal. Chicken. Shown are
the epithelium (E), dermis (D), epidermis of the feather follicle
(arrow), feather sheath (FS), barbs (B), pulp epithelium (PE), and
pulp (P).
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14.5. Skin. Epidermal inclusion cysts. Adult blue and gold 14.7. Skin. Dermal granuloma. Lovebird. Dermal granuloma
macaw. Two epidermal inclusion cysts in the dermis are shown. is composed ofmultinucleated giant cells associated with barbs and
Note the relatively thin epidermis. barbules from a disintegrating feather.

14.6. Preen gland. Inflammation. 6-week-old broiler breeder
chicken. This preen gland (A) has area of inflammation (arrow).
A relative ly normal area (*) is shown at higher magnification in B.
The area of inflammation is shown at higher magnification in C and
D. This bird had ulcers of the skin, probably due to cannibalism.
14.8. Dermal granuloma. Lovebird. Higher magnification of
14.7 shows the multinucleated giant cells associated with barbules
of a feather.

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14.9. Skin, Neck region. Granulomatous cellulitis, oil emulsion

vaccine reaction. Turkey. Severe granulomatous cellulitis is
associated with oil emulsi,on vaccine. Note the empty spaces which
14.11. Skin. Turkey pox. Turkey. Cutaneous pox is characterized
represent the lipid in the vaccine that dissolved in the processing of
by severe hypertrophy and hyperplasia (acanthosis) of the epidermal
tissue.
cells associated with intracytoplasmic inclusions of poxvirus. Note
the ballooning degeneration of the cells with inclusion bodies.

14.10. Skin. Turkey pox. Turkey. Severe hyperplasia

(acanthosis) and hypertrophy of epithelial cells are associated
with intracytoplasmic inclusions of poxvirus in the feather follicle
14.12. Skin. Feather. Psittacine beak and feather disease.
epithelium . Note the severe inflanunation around the feather follicle.
Moluccan cockatoo. Acute multifocal necrosis of the feather
follicle epithelium is associated with a few bottyoid inclusion bodies
(arrow) of circovirus. Note the epidermal collar and dermal papilla .
Insert is a higher magnification of the area below the arrow and
shows a bottyoid inclusion and necrotic follicular epithelial cells.

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14.13. Skin. Feather. Psittacine beak and feather disease.
Moluccan cockatoo. Severe inflammation in the pulp cavity is
associated with botryoid inclusions in the mononuclear cells and a
few intranuclear inclusion bodies in the feather follicle epithelium.
Insert is a higher magnification of the cells with intranuclear
inclusion bodies.
14.15. Skin. Feather. Psittacine beak and feather disease.
Moluccan cockatoo. Severe inflammation in the pulp cavity
includes multinucleated giant cells associated with a few botryoid
inclusion bodies.

14.14. Skin . Feather. Psittacine beak and feather disease. 14.16. Skin. Feather. Psittacine beak and feather disease.
Moluccan cockatoo. Basophilic globular and botryoid inclusion Budgerigar. Basophilic globular inclusions characteristic of
bodies in the macrophages in the pulp cavity are characteristic of circovirus are in macrophages within the pulp cavity.
circovirus infection.

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14.17. Skin. Feather follicle. Polyomavirus. Juvenile lovebird. 14.19. Skin. Feather follicle. Polyomavirus infection. Juvenile
Numerous karyomegalic cells in the feather follicle, barbs, and lovebird. Mononuclear cells in the pulp contain basophilic
barbules contain intranucl~ar inclusion bodies of polyomavirus. intranuclear inclusion bodies of polyomavirus.
Also note the lymphoplasmacytic inflammation in the pulp.

14.18. Skin. Feather Follicle. Polyomavirus infection. 14.20. Skin. Polyomavirus. Juvenile blue and gold macaw.
Budgerigar. Follicular epithelium contains numerous karyomegalic Severe subcutaneous hemorrhage is associated with polyomavirus
cells with basophilic and some eosinophilic intranuclear inclusion infection.
bodies of polyomavirus.

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14.21. Skin. Feather Follicle. West Nile virus infection. 14.23. Skin. Gangrenous dermatitis. C/ostridi11111 pe1fri11ge11s
Canary. lmmunohistochemistry shows West Nile virus antigen 111 infection. Broiler. Large number of Gram positive rods of
the cytoplasm of mononuclear cells of the pulp. Clostridi11111 sp. are shown in this gram stain.

14.22. Skin. Gangrenous dermatitis. Clostridi11111 pe1fi'i11ge11s 14.24. Skin. Fibrinoheterophilic cellulitis, Escherichia coli
infection. 4-week-old broiler. A. Necrosis is diffuse involving infection. Broiler. Fibrinoheterophilic cellulitis is diffuse and
epithelium (NE) and dermis with extension into subcutaneous fat. severe. Note the prominent eosinophilic band of necrotic cellular
Bacteria are numerous(* *). B shows a higher magnification of the debris.
necrotic epithelium (NE) and dermis. C is a higher magnification
of the subcutaneous region (**) showing numerous bacteria and
D shows necrosis that extends into skeletal muscle. Note lys is of

I
erythrocytes and the variable-sized spaces that indicate accumulation
of gas.

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14.25. Skin. Fibrinoheterophilic cellulitis. Escherichia coli

infection. Broiler. This higher magnification of 14.24 shows
severe fibrinoheterophilic i_nflammation with intralesional bacteria.

14.27. Snood. Cellulitis. Pasteurella 11111/tocida infection.

Turkey. Severe fibrinoheterophilic cellulitis and vascular
thrombosis are shown.

14.28. 14.28. Skin. Feather follicle. Folliculitis. Staphylococcus

14.26. Wattle. Cellulitis. Pasteurella 11111/tocida infection. aureus infection. Broiler. Folliculitis with intralesional bacteria
Broiler breeder chicken. Severe cellulitis and edema are shown. and perifolliculitis are shown .

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14.29. Skin. Mycobacteriosis. Parrot. Granuloma in the dermis 14.31. Skin. Mycobacteriosis. Parrot. Numerous acid-
is composed of multinucleated giant cells and macrophages. fast bacteria are revealed in the cytoplasm of macrophages and
multinucleated giant cells by this acid-fast stain .

14.30. Skin. Mycobacteriosis. Parrot. Higher magnification of 14.32. Skin. Feather follicle. Favus (Microspomm galli11ae
14.29 shows multinucleated giant cells and foamy macrophages infection). Adult chicken. Dermatophytes are numerous in this
containing faintly staining basophilic organisms in the cytoplasm. feather follicle.

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14.35. Skin. Feather follicle. Favus (Microspor11111 galli11ae

14.33. Skin. Feather follicle. Favus (Microspornm galli11ae infection). Adult Chicken. Numerous PAS positive dermatophytes
infection). Adult chicken. PAS satin. Numerous PAS-positive of Microsporum ga!linae are demonstrated (PAS stain).
dermatophytes of Microsporwn ga!linae are in this feather follicle
from the face.

14.34. Skin. Feather follicle. Favus (Microspor11111 gallinae 14.36. Skin. Hyperkeratosis, Candida glabrata infection.
infection), Adult Chicken. Dermatophytes are numerous in the Chicken. Severe hyperkeratosis is associated with numerous yeasts
superficial layer of the skin. Hyperkeratosis also is shown. of Candida glabrata. Note the severe hyperkeratosis and numerous
yeasts of Candida glabrata.

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14.37. Hyperkeratosis. Candida glabrata infection. Chicken. 14.39. Skin. Feather. Dermatophytes. Canary. Few
This is higher magnification of l 0.36. dermatophytes of unknown species are in this feather follicle .

..,,....,, :-

_...J§..,.,_,

' , ..··...-y,. "

'\:

14.38. Skin. Hyperkeratosis. Candida glabrata infection. 14.40. Skin. Feather. Pediculosis. Adult chicken . Numerous
Chicken. PAS stain reveals yeasts of Candida glabrata. eggs of lice are shown.

I 636 / American Association of Avian Pathologists

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14.41. Skin. Feather. Pediculosis. Adult chicken. Adult chicken,

lice eggs containing parasites in various stages of development.

14.43. Skin (Leg). Scaly leg mites (Knemidocoptes 11111ta11s).

Adult chicken. Severe acanthosis, hyperkeratosis and focal
ulceration of the epidermis are associated with scaly leg mites.

14.42. Skin (Leg). Scaly leg mites (Knemidocoptes 11111tans). 14.44. Skin. Feather. Quill mites. Budgerigar. Quill mites are
Adult chicken. Severe acanthosis and hyperkeratosis of the in the pulp cavity of several feathers.
epidermis are associated with scaly leg mites.

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14.45. Skin. Feather. Quill mites. Budgerigar. Three quill mites 14.47. Skin. Feather. Quill mite. Plum head parakeet. Two
are in the pulp cavity. quill mites are in the pulp cavity.

14.46. Skin. Feather. Quill mite. Plum head parakeet. Quill 14.48. Skin. Xanthoma. Hooded parakeet. The dermis
mite is in a feather. contains numerous macrophages, lymphocytes, and occasional
multinucleated giant cells. Cholesterol clefts also are shown.

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14.49. Skin. Keratoacanthoma (Dermal squamous cell 14.51. Skin, feather follicle. Marek's disease. Chicken.
carcinoma). Broiler, Processing Age. Crater-like depression Numerous intranuclear inclusion bodies and mild degeneration and
with raised edges char~cteristic of keratoacanthoma (dermal necrosis of the feather follicle epithelial cells are shown.
squamous cell carcinoma) is shown (A). Note the loss of surface
epithelium that is common following processing. The edges of the
lesion contain nests of epithelial cells with keratin accumulation
(pearls) (B). C is a higher magnification of B. D shows a cluster of
squamous epithelial cells with keratin accumulation.

14.50. Skin, feather follicle. Marek's disease. Chicken. 14.52. Skin. Marek's disease. Chicken. Neoplastic lymphocytes
Degeneration, necrosis, and intranuclear inclusion bodies are in this are infiltrating the dermis.
feather follicle epithelium. Also note the neoplastic lymphocytes at
the periphery.

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Index
A lesion in air sac, 266
Acute pancreatic necrosis, 546, 556, 557
Adenovirus infection, brain, 504, 505
Adrenal glands, 548, 578
amyloidosis, 579
anatomy and histology, 548
. fatty vacuolation, 579 ·
lipofuscinosis, 578
Marek's disease, 58
neoplasia, 549
non-infectious conditions, 548
normal, 578
viral infections, 548
Aflatoxicosis
glomerulopathy, 424, 425, 440, 450, 451
liver lesion, 357, 376-379
Air sac nematode Cyathsto111a sp ., 268
Air sac, neoplasms, 268, 269
Air sac, respiratory mite, 267
Airsacculitis caused by
adenovirus (in quail), 261
E. coli, 263-265
infectious alryngotracheitis virus, 260
infectious bronchitis virus, 262, 263
lvfycoplasma synoviae, 266
Ammonia,
damage to airways, 196, 197
ocular lesion, 522, 532, 533
trachea lesion, 215
Amyloidosis/amyloid deposits
in adrenal gland, 579
in blood vessels, 145, 187, 188
in kidney, 424, 439
in liver, 356, 374, 375
in pancreas, 555, 556
in spleen, 19, 54-57, 187
in thyroid gland, 567
Arsenic toxicity, liver lesion, 357, 379, 378
Ascaridia
in intestine, 276, 342, 343
in liver, 359, 411-413
Note: Numbers in boldface indicate figures.
Aspergil/11s sp. and aspergillosis
lesion in blood vessels, 14 7, 191
lesion in brain, 478, 515
lesion in eye, 523, 536
lesion in heart, 177
lesion in lung, 191 , 249, 250, 251
lesion in proventriculus, 306
lesion in trachea, 225
Atherosclerosis, 145, 182-187
Atoxoplas111a infection
liver lesion, 359, 410
spleen lesion, 21 , 67
Attaching-effacing E.coli, cecum, 275 , 323, 324
Avian encephalomyelitis
cataract and, 524, 539
lesion in central nervous system, 474, 505-507
lesion in myocardium, 145, 159, 160
Avian lymph node, 33, 34
Avian vacuolar myelinopathy, 471 , 492, 493
B
Bile ductular hyperplasia, 356, 364
Blood vessels
adenovirus inclusions, 190
amyloid deposition, 145, 187, 188
atherosclerosis, 145, 182-187
bacterial vasculitis, 190
embolism, 147
fibrinoid necrosis, 187
fibromuscular dysplasia, 145
hamangisarcoma, 194
histology, 143
intimal hyperplasia, 182
intraendothelial organisms, 191
Marek's disease, 193, 194
medial hyperplasia, 180, 181
mineral deposition, 179, 180
mycotic vasculitis, 191
schistosomiasis, 146, 192, 193
thrombosis, 147, 188-190
Avian Histopathology (4 1h Edition) I 641
 Index
Blood vessels (continued)
VetBooks.ir
Toxoplasma infection, 190
vasculitis, 14 7
Bone/joints
arthritis/synovitis, 78, 102-104
articular gout, 77, 105
chondrodystrophy, 75
degenerative joint disease, 77
dyschondroplasia, 75 , 96, 97
fracture and fracture repair,76, 91-94
histology, 73, 82-86
medullary bone, 74, 83 , 86
Mycoplasa synoviae infection, 103 , 104
neoplasia, 78
osteochondrosis, 75, 94, 95, 97-99
osteomyelitis, 76, 77t, 100-102
osteopetrosis, 78 105, 106
polyostotic hyperostosis, 47
response to injury, 76
rickets, 74, 86-93
spondylolisthesis, 75
tenosynovitis, 78
urate deposition, 105
Brachyspira infection, 275, 328
Brain, bacterial infections, 476
E.coli infection (colibacillosis), 511, 512
Enterococcus hirae infection, 513
Omithobacteri11111 rhinotmcheale infection, 513
Pse11do111011as aeruginosa infection, 512
Salmonella arizonae infection, 510
Bronchus-associated lymphoid tissue, 17, 30
Bursa ofFabricius, 17
adenovirus inclusion bodies, 41
atrophy, 35, 36, 37
chicken infectious anemia, 20, 41
circovirus infection in pigeon, 20, 42, 43
Clostridiwn perfi'ingens infection, 44, 45
OJ1ptospordi11111 infection, 21, 46
Eimeria developmental stages, 21 , 46
heterophilic granuloma, 44
histology, 24, 25
Histomonas infection, 21 , 46, 47
infectious bursa! disease, 20, 37-41
lymphoid leukosis, 21 , 48
Marek's disease, 21, 47, 48
polyomavirus infection, 20, 44
642 / American Association of Avian Pathologists
C
Candidiasis
of esophagus and crop, 272, 292, 297-299
of eye, 523
of gizzard, 273 , 314, 315
of oral cavity, 286
ofskin, 620,635,636
Capillaria infection
in esophagus, 272, 293, 294
in intestine, 341, 342
in crop, 272, 300, 301
Cecal tonsils, 17, 31
Cecum
attaching-effacing E. coli, 275, 323, 324
Bmchy:,pim infection, 328
coccidiosis, pheasant, 3 37
coccidisois, turkey, 433-436
Eimeria tene/la infection, 433-436
Hetemkis gallinarum infection 343, 344
Histomoniasis, 338, 339
salmonellosis, 327
Tetmtrichomonas infection, 339
Cerebellar hypoplasia, 468, 496, 497
Chand/ere/la quiscali infection of brain, 518
Chicken infectious anemia
bone marrow lesion of , 13, 14
bursa ofFabricius lesion of, 41
inclusion bodies in small intestine, 51
Pancytopenia and, St, 6
thymus lesion of, 49-51
Chlamy dia and chlamydiosis
epicarditis, 168
kidney lesion, 456-458
liver lesion, 404-405
orchitis and epididymitis, 583
pancreas lesion, 546
pericardium lesion, 146
Cholangiocholecystitis caused by C/ostridi11111 pe1fringens, 399
Cholangiohepatitis, 358, 397-399
Cholecystitis, 358, 401-402
caused by Campylobacter, 401 , 402
caused by C/ostridi11111 pe,fringens, 400
caused by Pseudomonas aeruginosa, 401
Circovirus infection
beak and feather disease, 618, 619
bursa of Fabricius lesion of, 20, 42 , 43
conjunctivitis associated with, 522
external ears, 525
skin, feather, 629, 630
Cloaca, 276
cloacitis, 276, 348, 349
Cloacotaenia mega/ops infection, 349
papilloma, 276, 353 , 354
Cloaca! papilloma, 276, 353, 354
 Index

Coccidiosis, intestinal
cecal coccidiosis, pheasant, 336, 337
E
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Ei111eria acerv11/i11a, 275 , 329, 330 Ear, 525-529

Eimeria maxim, 275, 331 , 332 anatomy, and histology, 525, 540
Ei111eria 111eleagri111itis, 232, 333 diseases of external ears, 525
Eimeria necatrix, 275, 330, 331 diseases of inner ear, 526
Eimeria tenel/a, 275 , 333-336 diseases of middle ear, 525
in pigeon, 333 lesions in, 541-543
Cochlosoa111a anatis and cochlosomiasis, 276, 339, 340 Eastern equine encephalitis (EEE) virus infection
Copper toxicity and hemorrhagic enterocolitis,
gizzard lesion of, 311 and hepatic necrosis, 358
kidney lesion of, 449, 450 and myocardium lesion, 146
!iv.e r lesion of, 380, 381 of the nervous system, 475, 507, 508
pancreas lesion of, 457 Ectopic lymphoid tissues, 17
proventriculus lesion of, 302, 303 Eimeria ace11111/ina, 275, 329, 330
Cronic active hepatitis, 370-371 Eimeria gnlis, 276
Crop Eimeria 111axi111, 275 , 331, 332
capillariasis, 300, 301 Ei111eria 111eleagri111itis, 232, 333
epithelial thickening, 29~ Ei111eria necatrix, 275 , 330, 331
fenbendazole toxicity, 296 Ei111eria tenella
mycosis, 297-299 in bursa of Fabricius, 21 , 46
physiological hyperplasia, 295 in cecum, 275, 333-336
proventricular dilatation disease, 296, 297 Ei111eria reichenowi, 276
Sa/111011ella typhi11111ri11111 , finches, 297 Eimeria truncata, 426, 459
CiJ1ptosporidi11111 infection Encephalitozoon he//em/microsporidiosis
of bursa ofFabricius, 21 , 45, 46 brain lesion, 478, 514
of infrorbital sinus, 213 intestine lesion, 276
of kidney, 426 kidney lesion, 426, 457, 458
of small intestine, 23 7, 238 liver lesion, 358 , 405- 7
of trachea, 225, 226 Endocardial fibroelastosis , 144, 157, 158
Cyathostoma nematode Endocrine system, 545
in air sacs, 268 Endogenous lipid pneumonia, 235
in trachea, 227 Enterococcus-associated enteritis, 324, 325
Cystic atresia, ovary, 587, 602 Erythrophagocytosis
and hemolytic anemia, 6
in spleen, 19, 53
Esophageal tonsil, 31
D E11bactri11111 tortuosum infection, liver, 400-401
Deep p·ectoral n1,yopathy, 109, 121-123 Eye, 521-524
Duck viral enteritis lesions anatomy, and histology, 521 , 530, 531
in esophagus, 290 aspergillosis, 536
in liver, 389 avian leukosis subgroup j virus, 539
in spleen, 58 bacterial infections, 523
Ductus deferens, normal, 600, 601 cataract, 524, 539
Ductular reaction, liver, 365 choroid, 539
Dust granulomas in lung, 229, 230 circovirns infections, 522
Dust particles and lungs, 197, 230 Conjunctivitis
Dyschondroplasia, 75 , 96-97 in Newcastle disease, 534
Dysgerminoma, 592 in laryngotracheitis, 533, 534
in pox, 534
conjunctivitis, 533, 534, 536
corneal erosion caused by ammonia, 532, 533
developmental and hereditary, 522
Escherichia coli infection, 535
exotic Newcastle disease, 534

Note: Numbers in boldface indicate figures. Avian Histopathology (4' h Edition) I 643
 Index

Eye, (continued) Germ cell tumor, ova1y, 592

VetBooks.ir

Gizzard
extra-ocular anatomy, 521
adenovirus infection, quail, 311 , 312
fungal infections, 523
avian encephalomyelitis lesion, 312, 313
herpesvirus infection, 535
bacterial infections, 271
infectious laryngotracheitis and fowl pox, 534
candidiasis, 273, 314, 315
infectious laryngotracheitis, 522,533, 534
Chei/ospirura sp . infection, 316
intraocular ossification, 540
copper toxicity, 311
/eucocyfozoon si111011di infection, 537
erosion ofkoilin layer, 310, 311
lymphoma, 537, 538
Hadje/ia tr1111cfafa infection, 316, 317
Marek's disease, 537, 538
nematode infection , turkey, 316
melanoma, 539
parasitic infections, 271
miscellaneous Ocular Conditions, 524
proventricular dilatation disease lesion, 313, 314
Mycoplas111a ga//iseptic11111 infection, 536
toxicities and deficiencies, 272
myelocytoma, 539
viral infections, 271
neoplasia, 524
vitamin E/selenium deficiency, 309
nervous tunic, 521
Gi zzard erosion, 272, 273 , 310, 311
neuritis, 537
Glomerulopathies, 424
nutritional diseases, 522
Glioma, 480, 518
other conditions, 524
Glyocogen storage disease
parasitic infections, 523
lesion in myocardium, 156, 157
pecten, 537, 538
lesion in skeletal muscles, 11 0
polyomavirus infection, 534
Granulosa cell tumor, 591
pox,534
Gut-associated lymphoid tissues, 17
proliferative conjunctivitis, 535
retina and optic nerve, 538
retinal dysplasia, 531, 532
Sa/111011ella arizonae infection, 535
Sa/111011e//a typhi111uri11111 infection, 535
H
Hadje/ia tnmcata, 316, 317
toxicities, 522
Harderian glands, 17, 34, 35
toxoplasmosis, 537
Hassall 's corpuscles, 18, 25, 26
vascular tunic (uvea), 521
Head-associated lymphoid tissue, 17
vasculitis and neuritis, 53
Heart
viral infections, 522
anatomy and histology, 143, 150-153
vitamin A deficiency, 532
avian encephalomyelitis, 160, 161
avian influenza, 159, 160
bacterial infections, 146
F calcium deposits, 153
cardiomyopathies, 144
Fatty liver/fatty vacuolation, 356, 368
cardiomyopathy, 154-156
Female reproductive tumors, 591 t
endocardial fibroelastosis, 144, 157, 158
Fenbendazole toxicity, 296, 318
epicarditis, 165-170
Fibrinoid necrosis, 21 , 59, 61-63, 147, 187
e1ysipelas, 170-171
Fibromuscular dysplasia, arterial, 145
extramedulla1y hematopoiesis, 152
intimal hyperplasia, 182
fatty infiltration, 153
medial hyperplasia, 180, 181
fungal infections, 146
Follicular atresia, ovary, 587, 602
glycogenosis, 156, 157
ionophore toxicity, 159
lipofuscin pigment, 145
G listeriosis, 172, 173
Ganglioneuroma, 481 , 518, 519 Marek 's disease, 178, 179
Gangrenous dermatitis mycotic myocarditis, 176, 177
muscle lesion, 111 , 126, 127 myocardial scarring, 145, 155, 156
skin lesion, 621, 632 parasitic infections, 146
polyomavirus, 164, 165

644 I American Association of Avian Pathologists

 Index

Heart (continued) Histomoniasis

bursa of Fabricius lesion, 46, 47
proventrucular dilatation disease, 164
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cecal lesion, 276, 338, 339

Purkinje cells, 152
kidney lesion, 426
reovirus, 161-163
liver lesion, 359, 407-409
. round-heart disease, turkey, 154
Hypoxia, liver lesion, 372
sarcocysts, 178
subendocardial fat, 152
toxicities, 145
urate deposition, 145, 154
valvular endocardiosis, 145
I
Inclusion body hepatitis
vegetative valvular endocarditis, 175, 176
kidney lesion, 424, 440, 442
viral infections, 145
liver lesion, 357 , 381-383
Hemic system, 1-16
pancreas lesion, 546, 558, 559
anemia, 4, St
Infectious bursa! disease, 20, 37-41
bone marrow hyperplasia, 6, 14
Infectious bronchitis
bone marrow inflammation, 7
air sac lesion, 262, 263
bone marrow, 4, 12
eye lesion, 522, 523
erythroblastosis, 9
kidney lesion, 425, 426, 451-453
erythrocytes, 2
oviduct lesion, 586, 587, 588t
erythrophagocytosis, 19
trachea lesion, 197, 216, 217
extramedulla1y hematopoiesis, l , 12
urolithiasis lesion, 583 , 600
granular leukocytes, 2
Infectious laiyngotracheitis lesion in
granulomatous inflammation, 7, 15
air sacs, 260
hematopoiseis, 1
esophagus, 271 , 289
hemic cells, 2
conjunctiva, 522, 533, 534
hemoglobinuria, 13
nasal chambers and sinuses, 208
hemolytic anemia, 5
respirato1y tissues, 197
hemorrahgic anemia, 5
lung, 238, 239
inflammation, 7, 7t, 13, 14
trachea, 218- 220
intravascular hemolysis, 13
Inhalant toxicity, 232, 233
leukocytosis, 15
Integument, 615
myeloblastomas/myeloblastosis 9, 16
anatomy, 615
myelocytomas/myeloid leukosis, 9, 15
bacterial infections, 620
myeloid leukosis, 15
cellulitis, 633
myelopathic anemia, 6
circovirus infections, 618 , 619,629, 630
neoplasia, 9
dermal granuloma, 628
nongranular leukocytes, 3
dermatophytes, 636
other types of anemia, 6
epidermal inclusion cysts, 628
pancytopenia, 6, 13, 14
favus, 634, 635
pigments, 7
fibrinoheterophilic cellulitis, 632, 633
thrombocytes, 2
folliculitis, 633
Hemosiderin pigment
fungal infections, 620
in bone marrow, 7
gangrenous dermatitis, 632
in kidney, 424, 436
genetic disorders, 616
in liver, 356,366
granulomatous cellulitis, 629
in spleen, 19
hyperkeratosis, 635, 636
Hepatic fibrosis and fatty vacuolation/steatosis, 369
inflammation, 628
Hepatic hemosiderosis, 356, 366
keratoacanthoma, 621 , 639
Hepatic lipidosis in turkeys, 357, 373-374
Marek's disease, 639
Herpesvirus infections, liver, 387-390
miscellaneous conditions, 621
Heterakis isolonche, 276, 344, 345
mycobacteriosis, 634
neoplasia, 622
normal, 627
nutritional disorders, 6 l 7

Note: Numbers in boldface indicate figures. Avian Histopathology (4 1h Edition) I 645

 Index

Integument, (continued) Kidney (continued)

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parasitic infestations, 621 hemangiosarcoma, metastatic, 468

pediculosis, 636, 637 hemoglobin casts, 437
polyomavirus infection, 631 hemoglobin droplets, 437
psittacine beak and feather disease, 6 I 8, 619, 629, 630 hemosiderin pigment, 424, 436
quill mites, 637, 638 herpesvirus infection in pigeons, 426, 454
response to injury, 616 infectious bronchitis virus infection, 426, 451-453
scaly leg mites, 637 lead toxicity, 449
toxicities, 617 Leucocytozoon infection, 460
turkey pox, 629 lymphoid leukosis, 467,468
viral infections, 618 lymphosarcoma, 468
West Nile virus infection, 632 Marek's disease lesion, 466-467
xanthoma, 638 mineral deposits, 424
Infraorbital sinus and middle nasal chamber membranoproliferative glomerulopathy, 424
infectious laryngotracheitis lesion, 208 membranous glomerulopathy, 424, 440
pox lesion, 209 mesangioproliferative glomerulopathy, 424, 441 , 442
bacterial infection, 210 metazoal infections, 426
Mycoplas111 gallisepticu111 infection , 211-213 myelocytomatosis, 468
C1yptosporidiu111 infection, 213 necrogranulomatous nephritis, 456
Ionophore toxicity neoplasia, 426
muscle lesion 19, 123, 124 nephroblastoma, 426, 463-466
myocardium lesion, 159 nephrosis vs. neplu-itis, 425
peripheral nerve lesion, 490, 491 oxalate nephropathy, 439
Iron storage disease, 356, 367 Paramyxovirus-1 infection in pigeons, 426, 453, 454
Paratanaisia spp. infection, 426, 461
Pigments, 424
polyomavirus infection, 426, 454
K proliferative glomerulopathy, 424
Ketamine/xyline toxicity, 471 protozoa! infections, 426
Kidney renal coccidiosis, 458, 459
aflatoxicosis, 450, 451 renal gout, 446, 447
amyloid deposit, 424, 439 renal trematodiasis, 426, 461
anatomy and histology, 423 , 429-434 Sarcocystis infection, 426, 459, 460
avian nephritis virus, 426 toxicities, 425
baby chick neplu-opathy, 424, 443-445 tubular adenoma, 462, 463
bacterial infection, 426 tubular epithelial hyperplasia, 435
bacterial septicemia, 456 urate deposition, 424, 425 , 443, 445-447, 449
bile cast, 437 urate nephropathy, 445, 446
bile pigment, 424, 436, 437 urate tophus, 447
calcium deposits, 438 ureteritis, 448
Chlamy dia infection, 456, 457 urolithiasis, 425, 447, 448
Clu-onic renal disease, 448, 449 viral infections, 425
copper toxicity, 449, 450 viral intranuclear inclusion bodies, 455
dehydration/water deprivation, 445-446 Knemidocoptes mu/ans, 621 , 637
Eimeria truncata infection, 458, 459
Encephalitozoo11 infection, 426, 457, 458
extramedullaiy hematopoiesis in, 435
fungal infections, 426 L
glomerular bacterial embolus, 455 Lead toxicity, 471
glomerular calcinosis, 438 Leucocytozoon and leucocytozoonosis
glomernlar fibrin microtlu-ombi , 455 infection and hemolytic anemia, 6
g lomerular lipidosis, 443 infection of brain, 479
g lomerular sclerosis, 442 infection of eye, 523 , 537
glomerulopathies, 424 lesion in liver, 359

646 I American Association of Avian Pathologists

 Index

Leucocytozoon and leucocytozoonosis (continued) Li ver (continued)

meronts in kidney, 460 iatrogenic granulomas, 357
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meronts in lung, 199, 253 inclusion body hepatitis, 381 , 382

meronts in muscles, 111 intrahepatic cholangiocarcinoma, 419, 420
Lipofuscin pigment / lipofuscinosis intravasc ular fibrin thrombus, 393
in adrenal glands, 548, 578 iron storage disease, 356, 367
in cardiac myocytes, 145, 153 ischemia/hypoxia lesion, 372
in neurons, 472, 494 Kupffer cell hypertrophy and hyperplasia, 356
Lipogranuloma, liver, 365 Kupffer cell micronodule, 356, 364
Listeria monocytogenes infection lipogranulomas, 365
lesion in central nervous system, 477 lymphoid leukosis, 417
lesion in heart, 172, 173 lymphoid leukosis lesion, 359, 417
Liver malignant melanoma, 421
adenoma or microhamai1oma of bile ductules, 419 Marek's disease lesion, 359, 414-416
aflatoxicosis, 376-379 Marek 's disease, 414-417
amyloidosis, 356, 374, 375 metastatic adenocarcinoma, 419
arsenic toxicity, 357,379,380 metastatic carcinoma, 419
Ascaridia aberrant migration, 411-413 metazoal infections, 359
ascites lesion, 356, 373, 376 microsporidiosis, 405-407
atoxoplasmosis, 410 mycobacteriosis, 402, 403
bacterail infections, 358 mycotic hepatitis, 407
bile ductular hyperplasia, 356, 364, 365 myelocytomatosis, 359, 418
chlamydiosis, 404, 405 myeloid leucosis, 418
cholangiocholecystitis caused by Clostridi11111 pe1fri11ge11s, 399 myeloproliferative disease, 418
cholangiohepatitis caused by Clostridium pe1:fringe11s, 398, 399 neoplasia, 359
cholangiohepatitis, 397, 398 histology, 355, 362, 363
cholangitis caused by Clostridium pe1fringens, 398, 400 Pasteurella 11111/tocida infection, 394
cholecystitis caused by Campylobacter, 401 , 402 pasteurellosis, 394
cholecystitis caused by Pseudomonas, 401 polyomavirus infection, 385, 387
cholngiocarcinoma, 420 protozoa! infections, 359
chronic-active hepatitis, 370, 371 reaction to oil-emulsion vaccine, 375, 374
Clostridi11111 pe1ji'inge11s, 398 Reovirus-vaccine lesion, 384, 385
congestive heart failure lesion, 3 73 Salmonella enteritidis infection, 394, 395
copper toxicity, 380, 381 Salmonella typhi111uriw11 infection, 397
duck viral enteritis, 389 Salmonella typhim11riw11 infection, finches, 397
Encephalitozoon hellem, 358, 405-407 sample collection, 355
erysipelas lesion, 395, 396 sarcocystosis, 359, 410, 411
extramedullaiy hematopoiesis, 363 schistosomiasis, 414
fatty liver/fatty vacuolation, 356, 368, 369 sinusoidal fibrin thrombi, 392
fatty-liver hemorrahgic syndrome, 357 toxicities, 357
fungal infections, 358 toxoplasmosis, 409
granuloma caused by filamentou s bacteria, 400, 401 turkey viral hepatitis, 357, 383,384
hemangiosa rcoma, 421 ulcerative enteritis, 397
hemosiderosis, 356, 366, 367 urate deposition, 356, 374
hepatic lipidosis in turkeys, 357,373,374 viral infection, 357
hepatic serositis, 391 , 392 Liver lesions and bacterial infections,
herpesvirus infection, cockatoo, 389, 390 coliseptisemia, 391-393
herpesvirus infection, hawk, 388, 389 erysipelas, 395, 396
herpesvirus infection, parrot, 390 Pasteurella multocida infection, 394
herpesvirus infection, pigeon, 387, 388 Salmonella enteritidis infection, 394,395
histology, 355, 362, 363 Salmonella typhi11111ri11111 infection, 397
histomoniasis, 359 407-409 ulcerative enteritis, 397
histomonias is, 407-409
hypoxic injuty, 356,372

Note: Numbers in boldface indicate figures. Avian Histopathology (4 th Edition) I 647

 I11tlex

Lung Marek's disease lesion (continued)

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bacterial infections, 240-246

in ovary, 608, 609
cartilaginous nodules in, 228
in pancreas, 562, 563
dust granuloma and pneumoconiosis, 229, 230
in proventriculus, 350
food aspiration, 233, 234
in skeletal muscle, 112, 129
infectious laryngotracheitis lesion, 238, 239
in spleen, 67, 68
inhalant toxicity, 232
in vestibulocochlear nerve, 542
lesion caused by /'v/ycoplas111a synoviae, 240, 248
lesion lung, 256, 257
Leucocytozoon infection, 253
Meckel's dive1ticulum, 17
Marek 's disease, 256, 257
Methyl mercmy toxicity, 471
metastatic melanoma, 259
Mite, respirato1y infection
metastatic ovarian carcinoma, 258
Cy todites 1111d11s, 199, 255
metastatic squamous cell carcinoma, 258
Sternostoma tracheacolu111 , 199, 226, 254, 267
mineral deposition/pulmonary calcinosis, 230-231
Mural lymph nodes, 19
mycobacteriosis, 246, 247
Muscle, 107
mycotic infection, 249-251
atrophy, 116
nocardiosis, 247, 248
avian encephalomyelitis lesion , 126
primary adenocarcinoma, 256
bacterial infections, 111
proliferative response, 236, 237
bacterial myositis, 127, 128
quail bronchitis lesion, 239
chronic myositis with minerali zation, 121
repiratory mite Cy todites 1111d11s, 254
deep pectoral myopathy, I 09
repiratory mite Sternostoma tracheaco/11111 , 254
degenerative myopathy, I 08
Sarcocystis infection, 252 exertional (capture) myopathy, I 08
Toxoplasma infection, 253 fungal infections, 111
Lung lesion and bacterial infection with
gangrenous dermatitis, 126, 127
E. coli, 241 , 243
glycogen storage diseases, 110
Ornithobacteri11111 rhinotracheale, 243, 244 granulomatous myositis, 110
Pasterella 11111/ocida, 240, 241 , 245 green muscle disease, I 09
Lymphocytic myositis, 117
hereditary muscular dystrophy, I 08
Lymphoid depletion, 19
histology, 107, 116, 118, 120-124
Lymphoid hyperplasia, 19
hype1thermia, 109
Lymphoid leukosis
injection site injmy, 110
lesion in liver,359, 417
ionophore toxicosis, 123, 124
lesion in bursa of Fabricius, 48
lymphocytic myositis, 117
lesion in kidney, 467, 468
Marek 's disease, 129
lesion in spleen, 69, 70
metazoal infections, 111
lesion in thyroid gland, 574
muscle hemorrhage, 110
lymphoid tissue neoplasia, 21
mycotic myositis, 127, 128
Lysosomal storage disease, 472
myopathies of uncertain etiology, 110
neuronal lesion is Hawiian swan, 494, 495
myopathy, 118, 121-123
Sanfilippo syndrome (mucopolysaccharide III), 495, 496
narasin toxicosis, 123
neoplasia, 112
neurogenic atrophy, 116, 117

M nutritional myopathy, 108

oil-emulsion vaccine injection site, 124, 125
Marek's disease lesion
protozoa! infections, 111
in adrenal gland, 580
rhabdomyosarcoma, 129
in blood vessels, 193 , 194
sarcocyst, 111 , 128
in bursa ofFabricius, 47, 48
toxic myopathies, 109
in eye, 523 , 537, 538
viral infections, 111
in heart, 178, 179
wooden breast, 119, 120
in integument, 618, 639
Mycobacteriosis lesion in
in kidney, 466, 467
bone marrow, 7, 77
in liver, 414-417
esophagus, 291
in nervous system, 473 , 497-503

648 I American Association of Avian Pathologists


Mycobacteriosis lesion in (continued)
heart, 146
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liver, 358, 15, 402, 403
lung, 246,247
ovary, 605
pancreas, 546
skin, 620
small intestine, 327, 328
spleen, 21 , 63-65
lvfycoplasma galliseptic11111 infection, 198
brain lesion (in turkeys) in, 478
conjunctivitis in, 523 , 536
otitis media (in turkeys) in, 526, 542
rhinitis and sinusitis in, 211-213
tracheitis in, 223-224
lv!ycoplas111a synoviae
airsacculitis caused by, 266
eye lesion caused by, 536
infection of joint synovium, 78, 103, 104
lung lesion caused by, 240, 248
meningeal vessel lesion caused by, 478
tenosynovitis caused by, 113 , 141, 142
Myeloproliferative disease, 418
Muscle atrophy, 116, 117
Muscular dystrophy, 108
Mycotic hepatitis, 407
Mycotic infection of lung, 249-251
Mycotic myocarditis, 176, 177
Myelocytomatosis/myelocytom/myeloid leukosis
eye, 539
hematopoietic cell neoplasia, 9, 15
kidney, 426, 468
liver, 359, 418
Myocardium, bacterial infections, 170-175
Myopathy, 118, 120, 121
deep pectoral, I 09
degenerative, I 08
exertional, 108
of uncertain etiology, 110
toxic, 109
N lysosomal storage diseases, 472, 494-496
Necrotic enteritis, 325, 326
Nervous system, 469
acute paretic syndrome, 480
adenoviruses, 474
alphaviruses, 475
aspergillus, 478, 515
aviadenovirus infection, 504, 505
avian bornavirus infection, 509, 510
avian encephalomyelitis, 505-507
avian leukosis viruses, 476
Note: Numbers in boldface indicate figures .
Index
Nervous system, (continued)
avian malaria, 516
avian vacuo Jar myelinopathy, 4 71 , 492, 493
bacterial infections, 476
bacterial thrombosis, 478
bagaza virus, 475
bornaviruses, 476
buggy creek virus, 475
b-vitamin deficiencies, 470
campylobacter-induced paralysis, 480
central nervous system, 480
cerebellar hypoplasia, 496, 497
ceroid and lipofuscin, 472
chondrodystrophy, 493
colibacillosis, 511 , 512
coliform bacteria (enterobacteriaceae), 477
degeneration and necrosis, 470
developmental conditions, 473
Eastern quine encephalomyelitis virus, 475 , 507, 508
Encephalitozoon hellem infection, 478, 514
feed additives, 4 71
flaviviruses, 475
fungal infections, 478
ganglioneuroma, 518, 519
glioma, 518
hemoprotozoa, 478
herpesviruses, 473
histology, 469, 487
hydrocephalus and cerebellar hypoplasia, 496
hydrocephalus, 496
idiopathic polyneuritis, 480
immune-mediated diseases, 480
infections, 473
infectious encephalomalacia, 513, 514
ionophore toxicity, 491
Israel turkey meningoencephalitis virus, 475
ketamine/xylazine, 471
lead, 471
lipofuscin, 494
Listeria monocytogenes, 477
louping ill virus, 476
lymphocytic encephalitis, 510
lymphoproliferative disease, 476
Marek's disease, 497-503
metabolic diseases, 472
metazoa, 4 79
methyl mercury, 471
Mycobacterium infection, 478, 514
Mycoplasma spp. infection, 478
neoplasia, 480
nutritional deficienc ies, 4 70
nutritional encephalomalacia, 470, 487-489
Ochroconis gallopava, 478, 515,516
Avian Histopathology (4 th Edition) I 649
 J11dex

Nervous system, (continued)

0
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organic arsenicals, 471 Obliterative atresia, ova1y, 603

organophosphates, 4 71 Ochroconis gallopava and ocluoconosis
Ornithobacteri11111 rhinotmcheale, 477 , 513 infection of brain, 478 , 515, 516
orthomyxoviruses, 474 infection of eye, 523
other bacteria, 478 infection of lung, 198
other fungi, 478 Oil-emulsion vaccine injection
paramyxoviruses, 475 granulomatous lesion in skin, 622, 629
parasitic infections, 478 granulomatous tenosynovitis, 113
Pasteurella 11111/tocida, 477 iatrogenic granulomas in liver, 357
peripheral nervous system, 481 muscle injury, 110, 124, 125
peripheral neuropathy, 490-492, 503 , 504 reaction to vaccine, liver, 375, 376
picornaviruses, 474 Organic arsenicals toxicity, 4 71
polyomaviruses, 474 Organophosphates toxicity, 4 71
protozoa, 4 78 Osteochondrosis, 75, 94, 95 , 97-99
Pse11do111011as infection ,477, 512 Ovary
reoviruses, 4 76 adenocarcinoma, 592, 610, 611
reticuloendotheliosis, 476 anatomy and histology, 585 , 586t, 602-604
retroviruses, 476 cystic atresia, 587, 602
riboflavin deficiency, 491 , 492 disturbance of growth, 586
Rie111erella analipest/fer infection, 477 follicular atresia, 587, 602
Sa/111onella arizonae infection, 510 germ cell tumor, 592
Sanfilippo syndrome, 495, 496 gonadal tumor, 610
sarcocystosis, 479, 517 granulomatous oophoritis, 605
schwannoma, 519 granulosa cell tumor, 591
Senna (=cassia) occidentalis, 471 inflammation, 587 , 588t
sitiawan virus, 476 Marek's disease, 608, 609
sodium chloride, 471 misovulation, 590
spinal cord injmy, 472 multilocular cysts, 587
spondylitis, 472, 493 mycobacteriosis, 605
spondylolisthesis, 472, 493 myeloblastosis, 609
Streptococcus infection, 477 myeloid leukosis, 609
tembusu virus, 476 neoplasia, 590, 591 t
terminology, 485t obliterative atresia, 603
toxicities, 471 oophoritis, 588 , 604
toxoplasmosis, 517 regression, 587
trauma, 472 right oviduct, 587
two-host coccidians, 479 Sertoli cell tumor, 609
usutu virus, 476 sexcord/gonadostromal tumor, 591
verminous encephalitis, 518 vaginitis, 589
viral infections, 473 Osteomyelitis, 76, 100-102
vitamin a deficiency, 470 Oviduct
vitamin e/selenium deficiency, 470 adenocarcinoma, 592, 612
West Nile virus, 475 , 509 adenomas, 592
Western equine encephalitis (EEE) virus, 475 adenovirus infection, 607
Nocardiosis, lung, 247, 248 anatomy and histology, 585 , 586t, 605-607
Nutritional encephalomalacia, 470, 487-489 bacterial salpingitis, 608
cystic right oviducts, 588
disturbance of growth, 586
herpesvirus infection, 608
infectious bronchitis virus infection, 586, 587
inflammation, 587, 588t
leiomyoma, 593 , 613
multilocular cysts, 587

650 [ American Association of Avian Pathologists

 Index

Oviduct (continued) Peripheral neuropathy, 490-491

immune-mediated, 480
neoplasia, 590, 591 t
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in lead toxicity, 471

regression, 587, 607
in organic arsenicals toxicity, 4 71
saplingitis, 589
in Senna accident a/is toxicity, 4 71
vaginitis, 589
organophosphate-induced, 4 71
Peyer 's patches, 17
Pituitary gland, 549, 580
p anatomy and histology, 549
carcinoma, 580
Pancreas, 545
lesions, 549
acute pancreatic necrosis, 556, 557
Plas111odi11111 infection of brain, 478, 516
adenoarcinoma of ovarian origin, 563 , 564
Pneumoconiosis, 229, 230
adenovirus infection, 558, 559
Polyomavirus infection
Alpha pancreatic islet, 551
of adrenal glands, 549
amyloid deposition, 555
of feather follicles, 631
amyloidosis, 556
of kidney, 426, 454
anatomy and histology, 545 , 551 , 552
ofliver, 357 , 385-387
apoptosis, 553
and otitis interna, 526
atrophy, 553, 554
Pox, cutaneous, 618, 629
avian encephalomyelitis, 561, 562
Pox, diphtheritic
avian paramyxovirus-1 infection, 546, 559-561
lesion in infraorbital sinus, 209
bacterial infections, 546
lesion in trachea, la1ynx, 221 , 222
Beta pancreatic islet, 552
lesion in oral cavity, 383-385
copper toxicity, 557
lesion in esophagus, 287, 288
depletion ofzymogen granules, 552, 553
Proventricular dilatation disease (avian bornavirus infection)
infections, 546
adrenal gland lesion of, 549
intraductal trematode, 562
crop lesion of, 296, 297
intralobular duct, 551
gizzard lesion of, 313,314
Marek's disease, 562, 563
heart lesion of, 146, 163, 165
neoplasia, 547
nervous system lesion of, 476, 510
non-infectious conditions, 545
proventriculus lesion of, 305, 509
non-specific lesions, 545
small intestine lesion of, 322
regenerating acini, 555
vestibulotracheal nerve lesion of, 526
regional fibrosis , 555
Proventriculus
splenic lobe, 551
avian encephalomyelitis, 304
turkey viral hepatitis, 559
copper toxicity, 302, 303
viral infections, 546
Dispha,J,nx nasuta infection, 309
Paramyxovirus infection of nervous system, 475
Macrorhabdus ornithogaster infection, 306-308
Paramyxovirus-1 infection in pigeons,
Marek's disease, 350
lesion in kidney, 453, 454
mucosa! carcinoma, 351 , 352
lesion in pancreas, 546, 559, 561
mycotic proventriculitis, 305, 306
lesion in nervous system, 475
necrohemorrahgic proventriculitis, 301, 302
Paratanaisia (trematode) in kidneys, 426, 461
pasteurellosis lesion, 305
Parathyroid Glands, 548
proventricular dilatation disease, 305
anatomy and histology, 548, 574, 575
Tetrameres infection, 308, 309
cystic adenoma, 577
transmissible viral proventriculitis, 304
hyperparathyroidism, 548
hyperplasia, 548, 576
hypertrophy, 576, 577
water-clear variant adenoma, 577, 578
Parathyroid gland hyperplasia, 548, 576
Parathyroid gland hypertrophy, 576, 577

Note: Numbers in boldface indicate figures. Avian Histopathology (4'h Edition) I 651
 Index

Small intestine (continued)

Q
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Quail bronchitis, coccidisosis, chickens, 329-332

respiratory infection, 197 Coch/osama anatis, 339,340
lesion in air sacs, 261 cryptosporidiosis, 276, 337, 338
lesion in lung, 239 Davainea prog!ottina, 346
lesion in oviduct, 607 Eimeria acervu!ian infection, 329, 330
lesion in trachea, 220, 221 Eimeria maxima infection, 331 , 332
Eimeria necatrix infection, 330, 331
Enterococcus-associated enteritis, 275 324, 325
fenbendazole toxicity, 318
R hemangiosarcoma, metastatic, 352
Rai/lietina echinobothrida, 346, 347 hemorrhagic enterit is of turkeys, 274,321,322
Reovirus infection and Heterakis iso!onche infection, 344, 345
artlu·itis, 78, 132-140 histology, 273
liver lesion, reovirus vaccine 384-385 histopathological evaluation, 273
myocardium lesions, 161-163 mycobacteriosis, 327, 328
tenosynovitis, 113 necrotic eneteritis, 325, 326
Respiratory system anatomy and histology, 195 parasitic infections, 275
Rickets, 74, 86-93 poult enteritis complex, 320
Runting-stunting syndrome proventricular dilatation disease lesion, 322
intestine lesion, 274, 321 Rallietina echinobothrida infection, 346, 347
pancreas lesion 546 reproductive tract carcinoma, metastastic, 354
runting-stunting syndrome, 321
schistosomiasis, 347
Spiro1111c!e11s/spironeucleosis, 340, 341
s ulcerative enteritis, 326
villous atrophy, 274
Sarcocystis infection
of heatt, 146, 178 viral enteritis, 319
of kidney, 426, 459, 460 viral inclusion bodies in enterocytes, 274
of liver, 359, 410, 411 vira l infections, 274
of lung, 199, 252 Spironuc!eus/spironucleosis, 276, 340, 341
of nervous system, 489, 479, 517 Spleen, 18
of skeletal muscles, 111 , 128 amyloidosis, 19, 54-57, 187
of spleen , 21 , 66 atoxop lasmosis, 67
Scaly leg mite, 621 , 637 chlamydiosis lesion, 65, 66
Schistosomiasis colisepticemia, 58, 59
blood vesse ls lesion of, 146, 192, 193 erysipelas lesion, 60-62
intestine lesion of, 347 e1ytlu-ophagocytosis, 19, 53
liver lesion of, 414 germinal centers, 19, 29, 30
Secondary lymphoid tissues, 17 hemorrahgic enteritis, 57, 58
Seminoma, 583, 601 histology, 18, 26-28
Senna accidenta/is toxicity, 471 lipidosis, 52
Sex cord/gonadostromal tumor, 591 lymphoid hyperplasia, 19
Shwannoma, 481,518 lymphoid leukosis, 21, 69, 70
Small intestine Marek's disease, 21 , 67, 68
adenovirus inclusion bodies, 319, 320 metastatic reproductive tract adenocarcinoma, 71
Ascaridia, 342, 343 mycobacteriosis, 63-65
attaching-effacing E. coli, 275, 323, 324 neoplasia, 21
bacterial infections, 275 polyomavirus infection, 58, 59
Capillaria, 341 , 342 protozoa! infection, 21
catarrhal enteritis, 274 pseudomonas aeruginosa infection, 60
cestodes, 345-347 reactive lymphoid fo llicles, 28-30
coccidiosis, pigeon, 333 reactive spleen, 19, 28
coccidiosis, turkeys, 432, 433 reticular cell hyperplasia, 52

652 I American Association of Avian Pathologists

 Index

Spleen, (continued) Thyroid glands, (continued)

reticuloendotheliosis, 21, 70 mixed goiter, 572
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sarcocystis infection, 21 , 66 neoplasia, 548

ulcerative enteritis lesion, 63 non-cancerous cyst, 567
urate deposition, 20, 54 papillary hyperplasia, 569, 570
urate tophi, 54 Toxic myopathies, 109
Toxoplasma and toxoplasmosis
infection of brain, 479, 517
infection of eye, 523 , 537
T lesion in artery wall, 190
Tendons, 112, 130, 131 lesion in liver, 359, 409
bacterial infections, 112 lesion in lung, 253
bacterial tenosynovitis, 131, 132 lesion in spleen, 21 , 67
Mycoplas111a sy noviae infection, 141 , 142 Trachea
mycoplasmal infections, l 13 adenovirus infection in quail, 220, 221
reovirus tenosynovitis, 132-140 ammonia-induced injury, 214, 215
ruptured tendon, 140, 141 aspergillosis, 225
tenosynovitis, 112 Bordetella avi11111 infection, 222 , 223
urate deposition, 112 , C, yptosporidi11111 infection, 225, 226
vaccine-associated granulomatous tenosynovitis, l 13 diphtheritic pox lesion, 221 , 222
viral infections, 113 epithelial hyperplasia, 216
Testis/epididymis infectious bronchitis lesion, 216, 217
anatomy and histology, 581 infectious laryngotracheitis lesion, 218-220
cystic testis, 582, 597 /v!ycoplasma galliseptic11111 infection, 223, 224
degeneration, 582 respiratory mite, 226
epididymal lithaiasis, 583 , 600 tracheal worm (swan), 227
epididymis, normal, 599, 600 Tetratrichomonas infection, cecum, 339
goose viral disease, 583 Trematode in pancreas, 562
neoplasia, 583 Tricho111011as infection, 272, 291, 192
orchitis and epididymitis, 583 , 598 , 599 Triploidy, 587
regression, 696, 597 Turkey viral hepatitis
seminoma, 583 , 601 liver lesion, 357 , 383,384
Sertoli cell nodule, epididymis, 601 pancreas lesion, 546, 559
sperm retention, 597, 589
testis, histology 596
Tibial dyschondroplasia, 96-97
Thymus, 18 u
atrophy, 20, 48, 49 Ulcer~tive enteritis, 326
chicken infectious anemia lesion, 20, 49-51 Urate deposit
hassall 's corpuscle, 25, 26 in heart, 145, 154
histology, 18, 25, 26 in joint, 105
Thyroid glands, 547 in kidney, 424, 425, 443 , 445-447, 449
adenoma, 574 in liver, 356, 374
amyloidosis, 567 in muscle/tendon, 112
anatomy and histology, 54 7, 564-566 in spleen, 20, 54
colloid goiter, 570-572 Ureteritis, 448
focal follicular atrophy, 566, 567
follicular atrophy, 566
follicular cysts, 548, 567, 568
follicular hyperplasia, 570 V
goiter, 547 , 570-573 Vegetative valvular endocarditis, 146, 175-176
hyperplastic goiter, 570 Verminous encephalitis 518
lymphocytic thyroiditis, 547, 568, 569
lymphoid leucosis, 574

Note: Numbers in boldface indicate figures. Avian Histopathology (4' h Edition) I 653
 Index

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White striping in muscle, I 08

West Nile virus infection
adrenal gland lesion, 549
brain and spinal cord lesion, 475, 509
muscle lesion, 111
myocardium lesion, 146
pancreas lesion, 546
virus antigen in feather follicles, 632
Wooden breast, 108,119, 120

X
Xanothoma, 623 , 638

654 I American Association of Avian Pathologists

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