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Life Science Archives (LSA)

ISSN: 2454-1354
Volume 1; Issue - 3; Year 2015; Page: 166 - 174

Research Article

EFFECT OF HEAVY METAL, NICKEL CHLORIDE ON

HISTOPATHOLOGICAL BIOMARKERS IN GILL, LIVER AND KIDNEY
OF FRESHWATER FISH, Oreochromis mossambicus (PETERS)
M. Muthulingam1*, S. K. Revathi1, P. Ronald Ross1, S. Ravichandran2 and P. Thenmozhi2
1

Department of Zoology, Faculty of Science, Annamalai University, Annamalai Nagar 608 002, Tamil Nadu, India.
2

Centre of Advanced Study in Marine Biology, Annamalai University, Parangipettai - 608 502, Tamil Nadu, India.
3

Department of Zoology, St. Josephs College, Manjakuppam, Cuddalore - 607 001, Tamil Nadu, India.

Abstract
Heavy metals are natural trace components of the aquatic environment, but their levels have
increased due to industrial wastes, geochemical structure, agricultural and mining activities. All these
sources of pollution affect the physiochemical characteristics of the water, sediment and biological
components and thus the quality and quantity of fish stocks. The histological biomarkers are constantly in
use in most studies, as this indicates the overall health of the environment and are important indicators of
pollutants in the environment. The aim of the present study was to assess the histopathological alterations in
gill, liver and kidney of Oreochromis mossambicus was exposed to sub-lethal concentration of nickel
chloride for the period of 30 days. The fish exposed to nickel chloride showed fusion of secondary gill
lamellae, mucous secretion, reduction in length, rupturing of secondary gill lamellae and vacuolization were
observed in the gill, enlargement of hepatocytes, necrosis, ruptured hepatocytes, space formation and
vacuolization were observed in the liver, disintegration of tubules, swelling of glomerulus, tubular necrosis
and vacuolization were observed in kidney of Oreochromis mossambicus. The objective of the present work
was to observe the effect of nickel chloride on histopathological alterations in the gill, liver and kidney of
freshwater fish, Oreochromis mossambicus.
Key words: Histology, nickel chloride, gill, liver,
kidney, Oreochromis mossambicus.

Article History
Received : 30.04.2015
Revised : 07.05.2015
Accepted :10.05.2015
1. Introduction

Pollution of the aquatic environment by

inorganic chemicals has been considered a major
threat to the aquatic organisms including fishes.
The agricultural drainage water containing
pesticides and fertilizers and effluents of industrial
* Corresponding author: M. Muthulingam
Department of Zoology, Faculty of Science, Annamalai
University, Annamalai Nagar 608 002

activities and runoffs in addition to sewage

effluents supply the water bodies and sediment
with huge quantities of inorganic anions and
heavy metals (ECDG, 2002). The most
anthropogenic sources of metals are industrial,
petroleum contamination and sewage disposal
(Santos et al., 2005).
Natural and anthropogenic sources
continuously release heavy metals into aquatic
ecosystem. The heavy metals after reaching to

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M. Muthulingam / Life Science Archives (LSA), Volume 1, Issue 3, Page 166 174, 2015

freshwaters cause serious problem due to their

long
persistence,
bioaccumulation,
biomagnification in the food chain, and toxicity to
the organisms. Fish, being dominant inhibitors of
aquatic environment, are considered as indicators
for heavy metal pollution (Srivastav et al., 2013).
Most environmental problems of concern today
are attributed to the production and release of
toxic chemicals capable of interacting with the
environment and disrupting the ecosystem
(Abumourad et al., 2013).
Lead is a naturally occurring heavy metal
which has been used in various ways including
mining, smelting, refining, gasoline, battery
manufacturing, electrical wiring, soldering,
painting, ceramic glazing, and making of stained
glass. Due to its non-degradable nature, it gets into
the environment and eventually enters the human
and animals blood stream. It is accumulated in
soft tissues such as liver, kidneys, nervous system,
and the brain (Srivastav et al., 2013).
Histopathological changes have been
widely used as biomarkers in the evaluation of the
health of fish exposed to contaminants, both in the
laboratory (Wester and Canton, 1991; Thophon et
al., 2003) and field studies (Hinton et al., 1992;
Schwaiger et al., 1997; Teh et al., 1997). One of
the great advantages of using histopathological
biomarkers in environmental monitoring is that
this category of biomarkers allows examining
specific target organs, including gills, kidney and
liver, that are responsible for vital functions, such
as respiration, excretion and the accumulation and
biotransformation of xenobiotics in the fish
(Gernhofer et al., 2001). Furthermore, the
alterations found in these organs are normally
easier to identify than functional ones (Fanta et al.,
2003), and serve as warning signs of damage to
animal health (Hinton and Laurn, 1990; Camargo
and Martinez, 2007). The present investigation
was to assess the histopathological biomarkers of
gill, liver and kidney of Oreochromis
mossambicus exposed to sub-lethal concentration
of nickel chloride.
2. Materials and Methods
The fish Oreochromis mossambicus having
mean weight 35 - 40 g and length 15 18 cm were

167

collected from PSP fish farm, at Puthur and

acclimatized to laboratory conditions. They were
given the treatment of 0.1% KMNO4 solution and
then kept in plastic pools for acclimatization for a
period of two weeks. They were fed on rice bran
and oil cake daily. The nickel chloride was used in
this study and stock solutions were prepared.
Nickel chloride, LC50 was found out for 96 hrs (37
ppm) (Sprague, 1971) and 1/10th of the LC50 value
was 0.37 ppm taken as sub-lethal concentration for
this study. Forty fish were selected and divided
into 2 groups of 10 each. The first group was
maintained in free from nickel chloride and served
as the control. The 2nd groups were exposed to sub
lethal concentration of nickel chloride, 10 litre
capacity aquaria. The 2nd groups were exposed to
nickel chloride for 30 days respectively. At the
end of each exposure period, the fish were
sacrificed and the required tissues were collected
for
histopathological
examination.
The
histopathological examination in gill, liver and
kidney of Oreochromis mossambicus were
observed by the method of Gurr et al. (1959).
3. Results
Gill Histology
The normal gills of Oreochromis
mossambicus comprised of laterally compressed
leaf like gill filaments (primary gill lamellae)
arranged alternately on either side of the
interbranchial septum. Each primary filament bore
a row of secondary gill lamellae on both sides
perpendicular to its long axis. Primary gill
lamellae comprised of a central core of
cartilaginous rod, lining epithelial cells and blood
vessels whereas secondary lamellae consisted of a
layer of flattened epithelial cells attached to the
basement membrane, contractile pillar cell system
and blood spaces (Plate I; Fig. A).
Gill Histopathology
The fish, Oreochromis mossambicus
when exposed to sub-lethal concentration of
nickel chloride for 30 days showed marked
histopathological changes in their gill. Excessive
secretion of mucous in the intercellular spaces,
fusion of secondary gill lamellae, reduction in
length, swelling of epithelial cells of secondary
lamellae and cytoplasmic vacuolization were

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M. Muthulingam / Life Science Archives (LSA), Volume 1, Issue 3, Page 166 174, 2015

some of the observable changes. The necrotic

changes in the tip regions of the secondary gill
lamellae were noticed on 30 th day (Plate I; Fig.
B).
Liver Histology
The liver of control fish, Oreochromis
mossambicus comprised of a continuous mass of
hepatocytes arranged in irregular cords. The
hepatic cells were large, polygonal in shape with
the nucleus almost centrally placed. Blood
sinusoids were also seen among the hepatocytes
(Plate I; Fig. C).
Liver Histopathology
The structural organization of the liver
appeared disturbed when fish were exposed to 30
days sub-lethal concentration of nickel chloride.
Rupture of hepatocytes and their nuclei, necrosis,
space formation and vacuolization of the tissue
and extension and displacement of nuclei were
some of the observable changes. Additionally,
disintegration of blood sinusoids and central vein
were also observed in the liver tissue (Plate I;
Fig. D).
Kidney Histology
The kidney of normal fish, Oreochromis
mossambicus is made up of tufts of capillaries
forming glomerulus surrounded by Bowman's
capsule. Besides convoluted tubules and
collecting ducts are noticed (Plate I; Fig. E).
Kidney Histopathology
The kidney of sub-lethal concentration of
nickel chloride exposed fish, Oreochromis
mossambicus have shown a marked damage. The
renal tubular cells were vacuolated. Necrosis,
swelling of glomerulus, tubular necrosis and
vacuolization of the cytoplasm are evident. The
tubules became desquamated and have lost their
shape. The tubular epithelium has undergone
degeneration (Plate I; Fig. F).
4. Discussion
Heavy metals in the aquatic environments
have been as a potential threat for aquatic
organism for several decades. Metals are known to
inhibit the several biochemical and physiological

168

mechanisms vital for fish metabolism. The use of

stress indices has been recently proposed to
evaluate the effects of metals on aquatic
organisms
(Atli
and
Canli,
2008).
Histopathological biomarkers have been largely
used in fish to identify and evaluate toxic effects
of exposure to pollutants (Mela et al., 2007).
Histopathology is now recognized as an important
tool to evaluate the effects of contaminants in vital
processes such as growth and reproduction,
detecting early effects in cells, tissues and organs
(Hinton et al., 1992; Adams, 2002).
Gill
In fish the gill is the most important organ
for respiration and osmoregulation and it is the
first organ to which, pollutant comes into contact.
Hence, it is more vulnerable to damage than any
other tissue (Vijayalakshmi and Tilak, 1996). The
fish gill is very sensitive to physical and chemical
alteration of the aquatic medium (Crespo et al.,
1988). Hocutt and Tilney (1985) have described
gill lesions (oedema, epithelial desquamation and
fusion of lamellae) caused by heat. Pollution (acid
stress, un-ionized ammonia, heavy metals,
pesticides, etc.) has been shown to alter chloride
cell structure and induce lamellar epithelium
desquamation
and/or
filament
epithelium
hyperplasia (Sinhaseni and Tesprateed, 1987).
There is a close relationship between gill
morphological alterations and stress (Peters and
Hong 1985) or lack of polyunsaturated fatty acids
in the diet (Bell et al., 1985), and several
infectious agents have been described in
association with proliferative gill diseases and gill
necrosis (Daoust and Ferguson, 1985). Gill
morphology is therefore a good indicator of the
water quality and the general health condition of
cultured fish (Peters et al., 1984).
Gill covers more than sixty percent surface
of the fish and its external location renders the
most vulnerable target organ for the pollutants
(Roberts, 1989). The higher organisms in the food
chain the grater the degree of accumulation.
Fishes are therefore particularly sensitive to
environmental contamination of the water and
pollutants may cause significant impairments of
certain physiological and biochemical processes

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M. Muthulingam / Life Science Archives (LSA), Volume 1, Issue 3, Page 166 174, 2015

which can result in serious tissue damage

(Reichenbach-Klinke, 1972; Straus and Chambers,
1995).
The rupturing of secondary gill lamellae,
excessive secretion of mucous, fusion of secondary
gill lamellae, reduction in length, central core broken
and vacuolization are some of the important
histopathological abnormalities observed in the gill
of Channa punctatus exposed to sub-lethal
concentration of nickel chloride. Similar
histopathological changes have been observed in the
gill of Hill-stream fish exposed to plant toxin
(Chandra Rooj, 1994), in lead exposed estuarine
mullet, Liza parsia (Pandey et al., 1997) and in
DDT exposed estuarine mullet, Liza parsia
(Pandey et al., 1993). Samson Raju et al. (1994)
have observed that Ariel detergent exposure
induced separation of epithelial layer around
respiratory lamellae and atrophy of respiratory
lamellae. They have further reported that
pathological changes in respiratory gill might have
results a shift in metabolic pathway in tissues of
fish under Ariel detergent exposure. The plant
toxin exposed Indian hill stream fish showed
collapsed tips of the swollen gill filaments,
mucous exudation and reduction in the lamellar
spaces (Chandra Rooj, 1994).

169

1975).
In the present investigation the
histopathological changes in gill is evident in the
sub-lethal concentration of nickel chloride
exposed Oreochromis mossambicus.
Liver
The liver has high concentration of
xenobiotic metabolizing enzymes, some of which
activate the toxicants to induce lesions locally (Lu,
1985). Liver is the most important centre for
metabolizing and also for detoxification. Rupture of
hepatocytes and their nuclei, necrosis and
vacuolization of the tissue, extrusion and
displacement of nuclei and disorganization of
sinusoids, space formation and central vein are the
important histopathological abnormalities observed
in the liver of Oreochromis mossambicus exposed
to nickel chloride. Many histopathological studies
indicated that liver is the organ to concentrate more
pesticides (Cough, 1975) and to show greatest damages
or impairment (Prasad and Qureshi, 1994; Gill et al.,
1990). Thilagamani et al. (1990) have suggested
that the severe destruction of hepatic cells and
formation of intercellular spaces could possibly
due to sudden withdrawal and utilization of stored
glycogen from the liver cells to meet the energy
demands during fungicide Cuman L. stress in
Sarotherodon mossambicus. The occurrences of
pycnosis and cytolysis also have been reported
in Cirrhinus mrigala exposed to zinc smelter
effluent (Sharma and Sharma, 1994) and in
Labeo rohita exposed to mercuric chloride
(Jagadeesan, 1994). Narain and Singh (1991)
have observed constriction of the bile duct lumen,
pycnosis of nuclei and loss of glycogen and
extensive degeneration of cytoplasm in
Heteropneustes fossilis exposed to thiodon.

In the present study on Oreochromis

mossambicus the nature of histopathological
changes observed in the gill exposed to sub-lethal
concentration of nickel chloride, lend additional
support to those recorded for Channa punctatus
exposed to sugar mill effluent (Karuppasamy, 1990),
Heteropneustes fossilis exposed to hydrocarbon
and blue gill exposed to alkyl benzene sulfonate
(Lemka and Mount, 1963). Vijayalakshmi and Tilak
(1996) have reported the disorganization of
Rajiv et al. (1995) have reported that the
secondary gill filaments, development of vacuoles,
breaking of the intercellular junction and necrosis
necrosis of nucleus and increased number of
were observed in the liver of Heteropneustes
mucous cells during monocrotophos, fenvalerate
fossilis when exposed to hair dye. In Liza parsia
and monocrotophos-fenvalerate mixture treatment
exposed to mercuric chloride and DDT caused
in Labeo rohita. Severe gill lesions at longer
severe liver damage due to hepatic lesions,
period exposure such as lifting and general necrosis
destruction of cytoplasmic materials,
of gill epithelium were very much evident in this test
levels. These responses can impair gill functions and
could eventually lead to the death of the fish (Eller,
Plate 1: Histology and Histopathology of Gill, Liver and Kidney
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M. Muthulingam / Life Science Archives (LSA), Volume 1, Issue 3, Page 166 174, 2015

170

V
SGL

FSGL
PGL

CC

RSGL

MS

B
RH
SF

V
NC
CV
DCT

PCT

D
SG

BC

G
DT

TN

(A) Gill section taken from control fish showing normal histoarchitectural pattern (XCa 200) and (B)
V
E
Gill section taken from nickel chloride exposure
fish (XCa 200)
F
CC Central core, FSGL Fusion of secondary gill lamellae, MS Mucous secretion, PGL Primary gill lamellae,
EF
RL Reduction in length, RSGL Rupturing of secondary gill lamellae, SGL Secondary gill lamellae and V
Vacuolization
(C) Liver section taken from control fish showing normal histoarchitectural pattern (XCa 200) and
(D) Liver section taken from nickel chloride exposure fish (XCa 200)
CV Central vein, EH Enlargement of hepatocytes, H Hepatocytes, N Nucleus, NC Necrosis, RH Ruptured
hepatocytes, SF Space formation and V Vacuolization
(E) Kidney section taken from control fish showing normal histoarchitectural pattern (XCa 200) and (F)
Kidney section taken from nickel chloride exposure fish (XCa 200)
BC Bowmans capsule, DCT Distal convoluted tubules, DT Disintegration of tubules, G Glomerulus, PCT
Proximal convoluted tubules, SG Swelling of glomerulus, TN Tubular necrosis and V Vacuolization

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M. Muthulingam / Life Science Archives (LSA), Volume 1, Issue 3, Page 166 174, 2015

vacuolization of the hepatocytes and blood

sinusoids exhibited complete disorganization
(Pandey et al., 1997). Since liver is involved in
the detoxification of pesticides Hurtterer et al.
(1969) it is susceptible to a greater degree of
disruption in its structural organization due to toxic
stress.
Degenerative changes in the liver of
Oreochromis mossambicus demonstrated the liver
to be the organ affected most severely in response to
nickel chloride intoxification.
Kidney
Kidney is the excretory organ for the
vertebrates. It is the main route of excretion for
most toxicants and it is a major target organ to
toxic
effects
(Lu,
1985).
Oreochromis
mossambicus when exposed to sub-lethal
concentration of nickel chloride showed structural
damages in the kidney. The important
histopathological abnormalities observed in the
kidney of Oreochromis mossambicus were
disintegration of tubules, vacuolization and
necrosis of kidney tubules.
Similar histopathological changes have
been observed in the kidney of zinc smelter
effluent exposed Cirrhinus mrigala. Sharma and
Sharma (1994) have studied the effect of
industrial pollutants containing mixture of
mercuric chloride, cadmium chloride, phenol and
ammonia, to Channa punctatus. They have
reported the desquamation in epithelial cells of
renal tubules in trunk kidney, vacuolation,
irregular orientation of nuclei and shrinkage of
glomerular tuft and capsules. Jagadeesan (1994)
has observed vacuolization, disintegration of
kidney tubules and necrosis in the fish Labeo
rohita when exposed to mercuric chloride.
Disintegration, vacuolization, necrosis of kidney
tubules have also been noticed in Mystus vittatus
treated with copper (Rajamanickam, 1992). The
foregoing account clearly suggests that the toxic
impact of nickel chloride influences considerable
changes in the histological organization of the gill,
liver and kidney of Oreochromis mossambicus
leading to its functional disruption. In general,
nickel chloride creates manifold disturbances in
the target tissues.

171

Acknowledgement
The authors wish to thank the authorities
of Annamalai University and Dr. N. Indra
Professor and Head, Department of Zoology,
Annamalai University for providing the facilities
to carry out the work.
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