Accepted Manuscript

Title: A review of coccidiosis in Old World camels

Authors: J.P. Dubey, R.K. Schuster

PII: S0304-4017(18)30297-8
DOI: https://doi.org/10.1016/j.vetpar.2018.08.008
Reference: VETPAR 8733

To appear in: Veterinary Parasitology

Received date: 6-7-2018

Revised date: 20-8-2018
Accepted date: 21-8-2018

Please cite this article as: Dubey JP, Schuster RK, A review of coccidiosis in Old World
camels, Veterinary Parasitology (2018), https://doi.org/10.1016/j.vetpar.2018.08.008

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8-20

A review of coccidiosis in Old World camels

J. P. Dubey1, *Schuster, R.K.2

1
United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural

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Research Center, Animal Parasitic Diseases Laboratory, Beltsville, Maryland, 20705-2350,

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USA.
2
Central Veterinary Research Laboratory, PO Box 597, Dubai, United Arab Emirates

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--------------------

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* Contact for author: J. P. Dubey, USDA-ARS, Beltsville Agricultural Research Center, Animal

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Parasitic Diseases Laboratory, Building 1001, Beltsville, MD, 20705-2350, USA.
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Email --jitender.dubey@ars.usda.gov. Fax 301-504-9022, phone 301-504-8128.
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Highlights
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 Coccidiosis is important as cause of mortality in camels (Camelus dromedarius and C. bactrianus).

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 Eimeria cameli, with the largest oocysts, develops in the lamina propria of the small intestine; only
sexual stages were identified.
 Cystisospora orlovi causes severe coccidiosis of the large intestines of nursing camels; only sexual
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stages are known.

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Abstract

Domesticated Old World camels (Camelus dromedarius and C. bactrianus) are important
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for the economy of several countries in Asia, Africa, and the Arabian Peninsula, and coccidiosis

is important as a cause of mortality in juvenile camels. There is confusion concerning the species

of coccidian parasites in camels and their life cycles. The objective of the present paper is to
review biology of the Eimeria and Cystoisospora species in camels. The following conclusions

were drawn. Although five species of Eimeria; E. cameli, E. rajasthani, E. dromedarii, E.

bactriani, and E. pellerdyi were named from camels, only E. cameli, E. rajasthani, E. dromedarii

have been consistently found in numerous surveys and they are morphologically distinct. We

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consider E. pellerdyi and E. bacterini as species enquirende/ not valid. E. cameli oocysts are

distinctive, dark brown and up to 108 µm long. Its gametogonic stages and oocysts are present in

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the lamina propria of small intestines; only sexual stages have been confirmed. The remaining

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species of Eimeria (E. rajasthani and E. dromedarii) in camels are <40 µm long and their

endogenous stages are unknown. There is one valid species of Cystoisospora, C. orlovi in camels

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and is associated with severe disease in young camels, both pastoral and stall fed camels. Camels

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as young as nine days old can develop severe diarrhea and can die before oocysts are detected in
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feces. Lesions and endogenous stages are confined to the large intestine. The main lesion is
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hemorrhagic, diphtheroid to hemorrhagic colitis-associated with sexual stages; asexual stages are

unknown. Oocysts are rarely excreted by adult camels, and in low numbers. Therefore, infection
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in very young camels remains unexplained.

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Keywords: Camel (Camelus dromedarius; C. bactrianus); Eimeria Cystoisospora;

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Coccidiosis
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1.Introduction
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Domesticated Old World camels are economically important for several countries. They

are used for transport, milk, meat, and camel racing is a big industry in countries of the Arabian

Peninsula. Coccidiosis is an important cause of neonatal diarrhea in livestock, including camels.

There is considerable confusion concerning the species of coccidia and their life cycles in
camels. The objective of this review is to summarize information on all aspects of coccidiosis

(Eimeria and Cystoisospora infections) in camels.

2. History and species of coccidia

Although coccidia were known as pathogens of livestock for more than two centuries,

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Eimeria infections in camels were reported only in 1930’s (Levine and Ivens, 1970). The

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literature on camel coccidia is very confusing. One reason for this confusion is that different

groups of researchers reported on Eimeria infections in camels from different countries at about

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the same time. Henry and Masson (1932 a, b, c) in France reported coccidia in a Camelus

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dromedarius that had died in Alfort, France. They found large-sized protozoa in histological

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sections of ileum that they named Globidium cameli. Reichenow (1952) synonymized
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Globidium with Eimeria and hence the correct name for this parasite became E. cameli (Henry
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and Masson, 1932c) Reichenow, 1952.

Nöller (1932) and Enigk (1934) in Germany reported on coccidian infections in a group of
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20 Bactrian camels (C. bactrianus) that originated from Uralsk (now: Oral, West Kazakhstan)
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brought to Germany by Veterinary Police because they were suspected to have trypanosomosis.
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All camels were eventually euthanized. One of these camels was euthanized three months after

arrival to Berlin. From this camel, Enigk (1934) described endogenous stages of "Globidium
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cameli" which he found mostly in the small intestines starting with duodenum and less in ileum;

only a few stages were found in cecum. Currently, there is general agreement concerning the
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identity of the E. cameli with large-sized oocysts (Table 1).

Most confusion is concerning Eimeria species with small-sized oocysts. Nöller (1932)

found oocysts in three Bactrian camels. The oocysts were about 32 µm long, and 25-27 µm wide

some with micropylar cap and some without it. Unfortunately, he also named the parasite
Eimeria cameli. Enigk (1934) described endogenous stages from one of the three camels from

which Nöller described small sized oocysts. Iwanoff-Gobzem (1934) and Yakimoff (1934) from

the USSR found similar parasites as described by Nöller (1932). Subsequently, Yakimoff and

Matschoulsky (1939) described another new species, Eimeria dromedarii from C. dromedarius

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and differentiated it from spherical oocysts of the parasite described by Nöller (1932). Cygankov

(also spelled Tsygankov, 1950), also from the USSR, said that E. dromedarii was same as the

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parasite reported by Nöller. To reconcile the name E. cameli for two parasites (of Henry and

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Mason, 1932c, and Nöller, 1932), Pellérdy (1965) named the large-sized oocysts as Eimeria

noelleri; this was rejected by Levine and Ivens (1970) and others based on priority of names.

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Because there was no valid name for the parasite described by Nöller (1932), Levine and Ivens

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(1970) created a new species, Eimeria bactriani for the Nöller’s parasite. This parasite has been
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rarely reported from camels.
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Dubey and Pande (1963) described another species, Eimeria rajasthani from C. dromedarius

in India; oocysts of this species were medium-sized (average 35 µm long) –see description later.
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Oocysts with varying sizes have been named as Eimeria pellerdyi by Prasad (1960) from a

camel in London zoo (Prasad, 1960). There are no archived specimens of Eimeria from earlier
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descriptions and there is no way to validate their existence. Additionally, complete life cycles of

Eimeria species in camels are unknown. From a review of literature, it is apparent that only three
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species, E. cameli, E, dromedarii, E. rajasthani are species consistently found in C.

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dromedarius. We consider E. pellerdyi and E. bactriani as non-existent/species enquirende, and

do not discuss them further.

Kasim et al. (1985) and Yagoub (1989) provided detailed morphological descriptions of E.

cameli, E. rajasthani, and E. dromedarii.

 Tsygankov (also spelled Cygankov) (1950) first reported a species of Isospora, Isospora

orlovi from camels in the Almaty region of Kazakhstan but did not mention the host species.

Kinne et al. (2001) confirmed the presence of this Isospora in UAE and reported on its

endogenous stages. Kinne et al. (2002) re-described morphology of I. orlovi. The parasite was

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later transferred to the genus Cystoisospora based on the morphology of oocysts and molecular

characteristics (Morrison et al., 2004; Barta et al., 2005; Bornstein et al., 2008)

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Daruish and Golemansky (1993) found coccidian oocysts in feces of 52 of 112 (46.4%)

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camels from Syria. Isospora oocysts were found in feces of three camels; these oocysts were

reported to be larger in size than C. orlovi oocysts and had Stieda bodies. In retrospect, these

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were most likely contaminants with avian species because C. orlovi oocysts lack Stieda bodies.
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We are also uncertain of the correct identification of Eimeria species in this paper; however, they
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did not find the large-sized E. cameli oocysts—this paper is not discussed further.
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3.Eimeria infections
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Three species of Eimeria are most prevalent (Tables 1-5). Additionally, Abdussalam and
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Rauf (1957) mentioned finding E. cameli-like oocysts in camels from Pakistan in an oral

presentation at a conference; it is mentioned here for completeness. Ryšavŷ (1954) found E.

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cameli oocysts in a C. bactrianus in a zoo in Prague, Czech Republic.

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The following description of oocysts is based on data reported in Tables 1-3.

3.1. Eimeria cameli (Henry and Masson, 1932) Reichenow, 1952

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This species is morphologically distinct from other species of Eimeria of camels (Fig.1).

There is a high variability in size of oocysts, varying from 67-108 µm in length and 57-94 µm in

width (Table 1). The most complete description is provided by Yagoub (1989) who studied
morphology of oocysts from nine camels. Unsporulated oocysts are truncate, ovoid, dark brown

to black. The oocyst wall consists of three layers, a pitted brown outer layer up to 14 µm thick,

the middle layer-1.5 µm thick light yellow to brown, and black 3-4.5 µm thick third layer.

Micropyle is up to 28 µm wide, and 6-9 µm high; micropylar cap is absent. Polar granule and

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oocyst residuum also absent. Sporulation time is up to 25 days. Sporocysts are elongated with

tapering ends, 37.4 x 18.6 (30-40 x 18-20) µm. Stieda bodies and residual bodies are absent.

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Sporozoite size is unknown.

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3.2. Eimeria dromedarii Yakimoff and Matschoulsky, 1939

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Kasim et al. (1985) and Yagoub (1989) provided the most complete description of 270

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oocysts from 24 camels (Table 2). Oocysts are subspherical to ellipsoidal, 23-33 x 19-25 µm;
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most oocysts were ovoidal (Yakimoff and Matschoulsky, 1939). Oocyst wall is 2-3 µm thick,
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smooth with 2 layers, the outer light yellow and the inner brownish green. Oocyst cap is 4-8 µm

wide and 1-3 µm high. Micropyle is absent. Sporocysts are ovoid, 7-11 x 5-9 µm without Stieda
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body and residuum. Sporozoite size is unknown.

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3.3. Eimeria rajasthani (Dubey and Pande, 1963)

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Oocysts are ellipsoidal 34-39 x 25-29 µm with length-width ratio of 1.3-1.4. There is

remarkably loww variability in dimensions of oocysts (Table 3). The oocyst wall is 2-3 µm thick
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with outer layer yellowish green and inner layer light brown. Micropylar end is covered with

dome shaped cap, 4-11 µm wide and 1-3 µm high. Oocyst residuum and polar granule are
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absent. Sporocysts are ovoid, 12-16 x 8-11 µm. Polar granule and oocyst residuum, with an

indistinct Stieda body are present at the narrow end. Sporozoites are curved, approximately 10

µm long.
3.4. Epidemiology

Eimeria infections were widely prevalent in surveys reported from several countries

(Table 4). In general, prevalence was higher in calves than in adult camels. A more detailed

prevalence data is available from the testing of a large numbers of camels at the Central

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Veterinary Research laboratory (CVRL), Dubai, UAE (Table 5). Overall, E. cameli was the most

prevalent species and its prevalence was highest in spring and summer. The other two species, E

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dromedarii and E. rajasthani are less prevalent but consistently present. Der Verdiewr et al.

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(2010) tested weekly feces of calves born to a herd of 30 Bactrian camels in Sweden. Eimeria

spp. Oocysts were excreted between 40 and 90 days of age; one calf excreted most of the

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oocysts. E. cameli oocysts were found in 41 of 67 fecal samples and Eimeria with smaller sized
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oocysts were present in 45 of the 67 samples (der Verdier et al., 2010).
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3.5. Endogenous development of Eimeria spp.

There is uncertainty concerning asexual and sexual stages of Eimeria of camel. Levine
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and Ivens (1970) reviewed the earlier literature. Henry and Masson (1932 a, b, c) first reported
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schizont-like structures, microgamonts, and oocysts in histological sections of a camel that died
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in a zoo in Alfort, France. The schizont-like structures were 350 µm in diameter. The

microgametes were 6 µm long. From the photographs, it is apparent that the oocysts in sections
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were those of E. cameli. Chineme (1980) described schizonts in jejunum of a five-year-old camel

in Nigeria that died of wasting disease. Pinhead-sized whitish-grey foci were seen grossly in
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mucosa. Histologically, the schizont-like structures were 330 x 240 µm in diameter in intestinal

mucosa. Oocysts in sections were 88 x 60 µm and undoubtedly of E. cameli. A more detailed

observation on camel coccidiosis was made on camels in Saudi Arabia by Kawasmeh and

Elbihari (1983) who found E. cameli oocysts in intestinal scrapings in 6 of 30 slaughtered

camels. Large (339 x 309 µm) mature schizonts were detected in crypts of Lieberkühn in

jejunum. A macrogamont-like structure, macrogamonts, and oocysts were identified in

histological sections. The oocysts identified were those of E. cameli and this was the only

species found in 140 (14%) of 960 fecal samples from camel farms they sampled twice weekly

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for 12 months. Ramachandran Iyer et al. (1968) and Narnaware et al. (2017) reported schizonts,

gamonts, and oocysts in duodenum and cecum of camels in India. Enteritis associated with

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endogenous stages of E. cameli-like parasite were found in intestines of camels obtained from

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abattoirs in Iran (Tafti et al., 2001; Borji et al., 2009; Kheirandish et al., 2012).

Hussein et al. (1987) reported on Eimeria infections in camels from farms and at

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abattoirsin Saudi Arabia. Enteric lesions and developmental stages of Eimeria spp. were found
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only in jejunum and ileum. Giant schizonts, micro-and macrogamonts, and oocysts were seen but
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unfortunately not illustrated. “Giant schizonts of all three Eimeria species were seen in jejunum
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and ileum” (Hussein et al., 1987). This is the first mention of endogenous stages of E. rajasthani
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and E. dromedarii in the literature. However, there are no illustrations. This report needs
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confirmation.

Recently, Dubey et al. (2018) described in detail endogenous development of E. cameli in

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naturally infected camels from Dubai, UAE; only sexual stages were found. They illustrated in
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detail microgametogenesis. Based on a review of descriptions of text and illustrations by

previous authors (Henry and Masson 1932a, b, c; Enigk 1934; Ramachandran Iyer et al., 1968;
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Chineme 1980; Kawasmeh and Elbihari 1983; Borji et al. 2009; Kheirandish et al. 2012;

Narnaware et al. 2017). Dubey et al. (2018) concluded that microgamonts were most likely

misidentified as schizonts (Fig.2). Thus, the schizont stage of E. cameli is unknown.

3.6. Clinical disease

 Hussein et al. (1987) reported clinical coccidiosis in camels in Saudi Arabia. Clinical

signs were observed both in animals on the farm and at abattoirs. Young camels (6 months to 2

years old) on farms near Riyadh had signs of diarrhea, dehydration and some died. Ten calves

with severe diarrhea were euthanized and necropsied. Similar signs were observed in 45% of

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camel calves at slaughtered at abattoirs. Most of the calves were excreting Eimeria oocysts.

Adult camels (22%) were excreting oocysts but they were not sick (Hussein et al., 1987).

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Ramachandran Iyer et al. (1968) reported an outbreak of gastro-enteritis in camels in

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Punjab, India affecting hundreds of camels with 1-40% mortality during summer months.

Tissues of one camel euthanized and two dead camels were examined at necropsy. Diarrhea was

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one of the clinical signs and some camels died within a day of onset of clinical signs. Gastro-
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enteritis was the predominant finding and affected abomasum, duodenum, and cecum; jejunum
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and ileum were not examined. Abomasum contained the blood sucking nematode Haemonchus
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longistipes. Endogenous stages (schizonts, gamonts, and oocysts) were detected in duodenum,
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and cecum. The oocysts were large (80 x100 um) and confirmed to the description of E. cameli.
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Mature schizonts were stated to be 900 x 500 µm and reported to contain merozoites. The

authors clearly stated that the role of E. cameli in the disease reported was uncertain. Same
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conclusion applies to a similar case of hemonchosis and E. cameli associated gastroenteritis in a

one-year old camel from India (Narnaware et al., 2017).

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Rangarao and Sharma (1997) noted diarrhea -associated with the presence of E.
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rajasthani oocysts in all eight calves in India.

A coccidiosis-like illness was diagnosed histologically in 27 of 38 camels submitted in

1996 for post mortem examination to the Central Veterinary Research Laboratory (CVRL),

Dubai, UAE (Kinne and Wernery, 1997). Of these 27 camels, illness was severe in 21 and mild
in six. The authors reported: (a) oocysts of Eimeria were not detected in feces but endogenous

stages (gamonts, oocysts) were present in intestines. (b) Most affected camels were young and

racing camels and had excessive amounts of barley in stomach. (c) Severe hemorrhagic enteritis

with eosinophilia of small intestine (mostly jejunum and ileum and rarely duodenum) was

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associated with numerous stages of E. cameli; large intestines were not affected. (d) Some

camels had evidence of enterotoxemia. In view of the experimental evidence with E. cameli in

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camels (see section 4 below) performed at CVRL, the disease observed by Kinne and Wernery

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(1997) was perhaps affected by abnormal high energy rich diet fed to racing camels at that time.

In the past 20 years, such episodes have not been diagnosed at CVRL.

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In conclusion, there is uncertainty concerning the role of Eimeria causing severe enteritis
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in camels because the role of concurrent infections in naturally infected animals has not been
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excluded.
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3.7. Experimental infection of camels with E. cameli oocysts

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Two experiments were performed at CVRL, Dubai. In the first experiment, two 18-month
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old, camels were orally dosed with an unknown number of sporulated oocysts (collected from
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feces of dead camels) and observed for 6 weeks (Kinne and Wernery 1997). Kinne and Wernery

1998). Both camels developed intermittent diarrhea and excreted oocysts after 6 weeks.
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Numerous coccidian stages were found in sections of jejunum and ileum. Whether there were

concurrent infections with other microbes is not clear.

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In the second experiment, 10 camels were inoculated orally with E. cameli 15000 -63000

oocysts and observed for 2 months for oocyst excretion and clinical signs. All inoculated camels

developed patent infections. Overall, the inoculated camels were not severely ill. None of the
camels given 17,000 had clinical signs (Gerlach, 2008). At higher dosage of 63000 oocysts,

lethargy and faintness over two days in one of six camels and a mild diarrhea lasting one day in

two others were noted. Six of these experimentally infected camels were treated with toltrazuril

(Baycox® 5%, 20 mg/kg of body weight) on different days. One animal infected with the high dose

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received treatment six day post infection, one treatment on days six and 12 after infection. Animals in the

low infection group received treatment 22 days after infection. Four camels infected with the high

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infection dose remained as untreated controls. Animals from the low infection group were observed for 63

days, those of the high infection group for 77 days. Prepatent periods ranged from 30 to 37 days

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irrespective of treatment or infection dose. Patent periods ranged from 18 to 38 days in the treated and 32

to 46 days in the untreated animals without appreciable differences. One untreated animal started to

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excrete oocysts 16 days after infection; this was considered an accidental previous infection.
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4. Cystoisospora orlovi infections
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4.1. Morphology
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Unsporulated oocysts are excreted in feces and they are 25-35 µm long (Table 6). They
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are usually ovoid. Sporulation occurs rapidly and some sporulate in host if post mortem is

delayed (Fig 1D). Sporulated oocysts might be slightly larger than unsporulated oocysts.
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Sporocysts are 20 x 15 µm and they contain elongated or ovoid sporozoites. Endogenous

development occurs in the large intestine. Asexual stages are unknown. Microgamonts are big
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and contain hundreds of microgametes. A micropyle, oocyst residuum, and Stieda bodies are

absent.
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4.2 Epidemiology

Cystoisospora-associated infections have been reported from India, Kenya, and United

Arab Emirates (Table 7).

 Cystoisosporosis is a clinical infection of nursing camels from 9-35 days old (Schuster et

al., 2017), but occasionally older calves may also suffer. Oocysts are most commonly detected in

camels with diarrhea and in younger camels. Infections occur both in stall fed as well as pastoral

camels. In a comprehensive investigation of dairy camels, most infections were in winter and

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spring, and most infections were seen in 14-29 day old calves (Schuster et al., 2017).

Many aspects of transmission of C. orlovi infections are unknown. One hypothesis is that

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oocysts sporulate rapidly and calves become infected soon after birth; excretion of oocysts in

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newborn camels is probably the source of infection to other camels. Currently, there is no

evidence for an arrested stage of the parasite in camel tissues or intrauterine or lactogenic

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transmission.
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4.3. Clinical disease
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Affected calves develop diarrhea and dehydration and can die within a short time. The

lesions are confined to large intestine, and consist of diphtheroid to hemorrhagic colitis with
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erosions or elevated areas (Fig. 3). Massive numbers of gamonts and oocysts might be present,
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especially in elevated areas.

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5. Diagnosis of coccidiosis
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Fecal examination and histopathology can aid diagnosis. Of the three common species of

Eimeria in camel feces, E. cameli, E. rajasthani, and E. dromedarii are morphologically

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distinctive (Fig.1). E. cameli oocysts are the largest and the heaviest. It is important to use

sedimentation techniques or flotation solutions higher than 1.3 specific gravity to float E. cameli,

like the diagnosis of E. macusaniensis of South American camelids (Dubey, 2018). Oocysts of E.

rajasthani have a prominent micropylar cap and are larger in size than E. dromedarii (Fig.1).
Eimeria oocysts are excreted unsporulated and sporulation requires more than two days.

Histologically, E. cameli stages are big in size and occur in small intestine, mostly in the ileum

(Fig. 2). Endogenous stages of E. rajasthani and E. dromedarii are unknown.

Oocysts of C. orlovi are often excreted sporulated and they contain two sporocysts,

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compared with four sporocysts in Eimeria species (Fig.1D). in some cases of cystoisosporosis

calves die before oocysts are detectable in feces. C. orlovi stages are found in the large intestine

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(Fig.3). Scrapings of intestinal mucosa can reveal numerous coccidian stages. Histologically,

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there is enteritis with occasional inflammation in submucosa.

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6.Treatment

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Little is known about treatment of coccidiosis in Old World camels. Sulfadimidine given
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as an aquatic suspension orally for 10 days in a dose 30 mg/ kg body weight was used to treat
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dromedary calves (Hussein et al.,1987). Gerlach (2008) attempted to examine the efficacy of

Toltrazuril in experimentally infected dromedaries. Although toltrazuril showed promising high

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serum levels in a pharmacokinetic study it failed to prevent patent infections when given 6, 12 or
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22 day post inoculation.

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Camels are highly susceptible to the adverse effects of ionophoric antibiotics (monensin,

lasalocid or salinomycin) used to control coccidiosis in poultry (Al-Nazawi and Homeida, 2009).
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The toxic effect of these coccidiostats results in degeneration of skeleton muscles.

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Acknowledgements

We would like to thank Drs. Joerg Kinne, Christian Bauer, Camila Cezar, Fernando

Antunes, Andressa Ferreira da Silva, and Oliver Kwok for their help in preparation of this paper.

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Henry, A., Masson, G., 1932b. La coccidiose du dromadaire. Rec. Méd. Vét. Exot. 5, 185-193.

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Kawasmeh, Z.A., Elbihari, S., 1983. Eimeria cameli (Henry and Masson, 1932) Reichenow,
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Kheirandish, R., Nourollahi-Fard, S.R., Faryabi, Z., 2012. Prevalence and pathologic study of
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Eimeria cameli in slaughtered camels. Eurasian J. Vet. Sci. 28, 138-141.
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Mirza, M.Y., Al-Rawas, A.Y., 1976. Coccidia (Protozoa Eimeridiae) from camels (Camelus
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Narnaware, S.D., Kumar, S., Dahiya, S.S., Patil, N.V., 2017. Concurrent infection of coccidiosis
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SC
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Yakhchali, M., Athari, S., 2010. A study on prevalence of Eimeria spp. infection in camels of
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Tabriz region. Arch. Razi Inst. 65, 111-115.
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Yakimoff, W.L., 1934. Zur Frage der Coccidien der Kamele. Arch. Wiss. Prakt. Tierheilk. 68,
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Yakimoff, W.L., Matschoulsky, S.N., 1939. IV. On a new coccidium from camels, Eimeria
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dromedarii n. sp. J. Royal Micro. Soc. 59, 26-29.

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Younan, M., McDonough, S.P., Herbert, D., Saez, J., Kibor, A., 2002. Isospora excretion in
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Legend
Fig.1. Coccidian oocysts from camel. Unstained. (A) Eimeria cameli, unsporulated. Note large
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size and thick wall. (B) Unsporulated E. rajasthani with prominent micropylar cap (arrow). (C)
Unsporulated oocyst of E. dromedarii. (D) Unsporulated (arrowheads) and sporulated oocysts of
Cystoisospora orlovi; oocysts of this coccidian sporulate rapidly and are often sporulated in
A

freshly passed feces. Bar=20 um and applies to all parts.

Fig.2. Histological section of ileum of an adult camel showing sexual stages of Eimeria cameli.
The intestinal lumen is on the top. Hematoxylin and eosin stain. (A) Low magnification showing
microgamonts (mi), macrogamonts (ma), and empty vacuoles (arrows). (B) A very young
gamont, most likely macrogamont (ma), and a young macrogamont (mi). (C) Longitudinally cut
E. cameli oocyst (arrow) enclosed in parasitophorous vacuole (pv). Note, parasitophorous
vacuolar membrane (arrowheads).
Fig.3. Histological section of colon of a young camel showing sexual stages. The intestinal
lumen is on the top. Hematoxylin and eosin stain. (A) Denudation and exudation of intestinal
contents in lumen (arrow). (B) Masses of oocysts (arrows). (C) Unsporulated oocyst (arrow),
sporulated oocyst (arrowhead), and sporozoites (double arrowheads).

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A Figr-1

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A Figr-2

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A Figr-3

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Table 1

Details of of Eimeria camelii oocysts in one-humped camel (Camelus dromedarius); sizes given are in µm

Unsporulated Oocyst Micropyle Sporocysts Remarks Sporulation Country Reference

oocysts wall time [days],
temperature
(oC)
80-100 x 63- 10.4- 10-14 NS Wall 10.4- NS France Henry and
94 15.6 wide 15.6 thick, Masson

PT
thick micropyle 10- (1932a)
14 wide, 2
layers
75 x 95 x 55- Ns NS NS Oocyst wall 5- [10-15], (16- Russia Tsygankov

RI
70 9 thick, 3 20) (1950)
layers.
Sporocysts

SC
40-50 x 14.5-
20 (45 x 18)-
for E.
kazachstanica,

U
now regarded
as E. cameli
67 x 57 (n=1) NS NS NS NS India Dubey and

80-100 x 60- NS 27x 13 NS

N
Wall 3-15 NS India
Pande (1964)
Ramachandran
A
70 thick Iyer et al.
(1968)
M
78-100 x 58- 7-9 10-18 x 2- 30-39 x Pyriform [8], (22-24) Iraq Mirza and Al-
72 (180 from 4 cap 15-20 oocysts, Rawas (1976)
50 camels); (n=100 length-width
average 87 x from 50 ratio 1.1-1.4
D

66 camels)
86-108 x 61- NS 18-28 x Oocyst wall [23-25], Saudi Kawasmeh
86 6-9 with 3 layers, (27) Arabia and Elbihari
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micropyle (1983)
18.5-27.8
78-98 x 64-72 NS 17-26 x 6- 30-40 x From 9 [12-15], (26- Sudan Yagoub
(n=100) 10 18-20 camels—for 30) (1989)
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complete
description
see text
CC

63-81 x 51-61 4.0-8 7-18 39-41 x The dark [8–20] , (24) UAE Gerlach
15-19 colored outer (2008)
wall can be
broken by
light pressure
A

NS=not stated.
A
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M
A
N
U
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 Table 2

Details of Eimeria dromedarii oocysts in one-humped camel (C. dromedarius); sizes given are in µm

Unsporula Avera L/W Microp Sporocy Remarks Sporulati Country Refer

ted oocysts ge ratio yle sts on time, ence
[days],te
mperatu
re
(oC)

PT
23-32 x 27 x NS Cap 6.8- NS Oocysts [15-17], Russia Yakimoff and
20-25 23 8.4 x 2- mostly oval, (10-12) Matschoulsky
3 few (1939)
spherical

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oocyst wall
brown, 0.8-
1.4 thick

SC
26-28 x 27 x 1.19 5-7 x 2- 10-11 x Subspherica NS India Dubey and Pande
21-23 21 - 3 8.5 l to (1964)
(n=100) 1.33 (n=50) spherical,
oocyst wall

U
bilayered,
outer layer
yellowish

24-32 x 28 x 1.1- 4-8 x 2- 8-11 x 6-

greenN
Sporocysts [4], (22- Iraq Mirza and Al-
A
20-23 22 1.3 3 9 (n=150 average 10 x 24) Rawas (1976)
(n=200 micropy from 40 8
M
from 50 lar cap camels)
camels)
24-33 x 29 x 1.17 6-8 x 1- Ovoid, Ellipsoidal NS Saudi Kasim et al.
19-25 23 - 2 7-11 x 6- or spherical, Arabia (1985)
D

(n=120) 1.38 9 (9.8 x bilayered

91.2 7.5) oocyst wall,
8) outer light
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yellow,
inner
brownish
green
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23-33 x 28 x 1.18 4-6 Ovoid, Subspherica [5-7], Sudan Yagoub (1989)

19-24 23 - 7-10 x 5- l to ovoid, 2 (26-30)
(n=150) 1.35 8 (9 x 7) layered
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(1.2 wall, outer

7) pale yellow,
inner dark
green
NS=not stated. L/W=length/width ratio
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Table 3

Details of Eimeria rajasthanii oocysts in one-humped camel (C. dromedarius); sizes given are in µm

Unspor Averag L/W Microp Sporocy Remarks Sporulat Countr Reference

ulated e ratio ylar sts ion time y
oocysts cap [days],
(wide, tempera
high) ture
(oC)

PT
35-39 x 36 x 25 1.30- 8-11 x 14-15 x Oocysts 7 days India Dubey and
25-27 1.44 2-3 8- ellipsoidal, (26-30) Pande (1963,
(n=100) 11(n=50 bilayered, 1964)
) sporozoites 10-14

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x 3-4
34-39 x 36 x 26 1.35- 6-9 x 1- 12-15 x Bilayered oocyst 7-8 (25- Saudi Kasim et al.
25-29 1.41 2.5 9-11 wall, outer layer 28) Arabia (1985)

SC
(n=100) light yellow,
inner layer
brownish green
34-39 x 35 x 26 1.31- 4-7 12-16 x Bilayered oocyst 6-8 (26- Sudan Yagoub

U
26-29 1.36 9-11 wall, outer layer 30) (1989)
(n=100) pale green, inner
layer yellowish

30-40 x 36 x 15 9-12 x 14-15 x

brownN
Ellipsoidal 4-5 India Rangarao and
A
23-29 2-3 8-12 Sharma (1997)
NS=not stated. L/W=length /width ratio
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Table 4

Prevalence of Eimeria species* in Old World camels

Country Region No. % Remarks Reference

positive
sample
d
Bahrain 223 15.2 E. dri, only species reported Abubakr et al.

PT
(2000)
China Inner 321 50.0 E. rai, E. dr, E. cai, E. ba, E. pe. Wei and Wang
Mongolia Samples collected 1982-1987 (1990)

RI
from Bactrian camels
India Rajasthan 45 62.2 E. ra in 28 (62%) Dubey and
E. dr in 20 (44%) Pande (1963,

SC
E. ca in 1 (2.2%) 1964)
No clinical signs, rectal samples
from calves < 10 month-old from 1
farm

U
India Punjab 321 24.0 E. ra in 13 (4%). Gill (1976)
Other species in 64
India Rajasthan 897 25.1 N
E. dri, E. ca, E. pe, E. rai Partani et al.
(1999)
A
Iran Miandoab 33.3 % of Bacterian camels versus Yakhchali and
region 125 12.8 14.3% of dromedarian camels Cheraghi (2007)
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infected. Eimeria species reported:

E. ra 15.6% (only Bactrian camels),
E. ca 11.1%, E. dr 4.4%. Diarrhea in
D

young calves
Iran Mashhad 306 18.6 Samples collected at an abattoir. Borji et al.
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Lesions associated with E. ca (2009)

detected in 29 camels
Iran Tabriz 164 20.7 E. ba 52.4%, E. ca 19.3%, E. pe Yakhchali and
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15.6%, E. dr 12.6% Athari (2010)

Iran Kerman 100 29 Samples collected at an abattoir. Kheirandish et
Lesions associated with E. ca al. (2012)
detected in 29 camels
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Iran Yazad 305 9.5 E. ca 14 (47.5%), E. dr 13 (42.5%), Sazmand et al.

Province E. ba 2 (10.0%) (2012)
Iraq 200 NS 30 samples from northern Iraq Mirza and Al-
A

were negative for oocysts. Of 170 Rawas (1976)

samples from central Iraq, E. ca
was found in 68 (40% and E. dr in
86 (50.65%)
Saudi Hofuf, E. ca oocysts found in 146 of 960 Kawasmeh and
Arabia easten samples of feces collected twice Elbihari (1983)
province 960 14 weekly from an unspecified
 number of camels for 12
consecutive months
Saudi 4 regions 500 41.6 Prevalence reported for 4 different Kasim et al.
Arabia regions in 6 months to 5 years-old (1985)
camels; E. dr 28.4%, E. ra 22.2%, E.
ca
Saudi 5 regions 385 40 E. dr was the most prevalent, Hussein et al.
Arabia followed by E. ra, and the least (1987)

PT
prevalent was E. ca, but relative
figures were not stated. Clinical
signs observed in young camels

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Saudi Gassim 240 12.8 Intestines and feces from camels at Mahmoud et al.
Arabia region an abattoir, 15.7% of 83 adults and (1998)
10.2% of calves infected. In adult

SC
camel E. ca 2.4%, E. ra 7.2%, E. dr
12%. In calves, E. ca 1.3%, E. ra
5.1%, E. dr 6.3%
Sudan 230 17.4 E. ra in 21 (9.1%) Yagoub (1989)

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E. dr in 15 (6.5%)
E. ca in 9 (3.9%)
UAE Dubai 13,301 N
E. ca in 1469 (13%)
E. ra in 578 (6%)
CVRL annual
report (2007)
A
E. dr in452(4%)
Uganda Karamoja 82 11 E. ca 100% Nakayima et al.
M

(2017)
USSR 467 74.4 Eimeria species Tsygankov
(1950)
D
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*E. ba= E. bactriani, E. ca= E. cameli, E. dr= E. dromedarii, E. pe= E. pellerdyi, E. ra= E. rajasthani
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Table 5

Prevalence of Eimeria species in camels in UAEa

Year Number Prevalence (%)

E. cameli E. dromedarii E. rajasthani
2008 12,443 12.9 4.5 2.9

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2009 11.474 14.4 5.6 3.4
2010 3,212 17.5 7.4 4.8
2011 3,174 13.7 2.6 3.6

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2012 3,964 7.7 1.5 1.9
2013 2,718 8.4 3.6 2.6

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2014 4,258 16.6 5.6 4.6
2015 3,182 13.3 5.1 2.9
2016 3,934 11.5 3.0 3.1

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a
Samples were processed at the Central Veterinary Research Laboratory (CVRL), Dubai, and reported by Schuster et
al. (2015)
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Table 6

Morphology of Cystoisospora orlovia

Unsporulated Sporulated Sporocysts Sporozoites Country Reference

Oocysts oocysts
27-35 x 15-20 NS 15-20 x 13-17 7-10 x 4-6 Russia Tsygankov (1950)
NS 25-35 x 17-21 13-15 x 9-11 6-8 x 4-5 India Raisinghani et al. (1987)
27-33 x 20-27 NS 20 x 15 12-14 x 3-4 Dubai Kinne et al. (2002)
(n=10)

PT
NS 28-35 x 18-27 20-23 x 16-19 13-17 x 3-4 Kenya Bornstein et al. (2008)
25-30 x 19-21 27-35 x 17-24 15-22 x 12-19 12-15 x 4-5 Dubai Schuster et al. (2017)
a
Measurements are in µm.

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NS=not stated.

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Table 7

Reports of Cystoisospora orlovi in Old World camels.

Country Region Remarks Reference

Russia Oocysts detected in 10 calves, 10-35 days- old Tsygankov (Cygankov,
1950)
Kenya Lakipia
District C. orlovi-associated diarrhea diagnosed in in four herds. Younan et al. (2002)
Oocysts were seen in 13 calves, 12-30 days old. Two

PT
calves died. Postmortem revealed ulcerative colitis in
one calf with intra-lesional coccidian stages
Kenya Rift Oocysts were detected in feces of 21 of 253 calves. 19 Bornstein et al. (2008)
Valley of 21 calves excreting oocysts had diarrhea. Oocysts

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were not found in healthy calves and in calves older
than 8 weeks of age
India Oocysts found in feces of a 6-month old calf with Raisinghani et al. (1987)

SC
diarrhea
UAE Dubai Outbreak of diarrhea on 2 farms. 22 calves that died Kinne et al. (2001, 2002)
were necropsied. Colitis was found in 8 calves.
Endogenous stages of C. orlovi were detected in large

U
intestine
UAE Dubai Oocysts were found in feces of 72 of 2885 samples from Schuster et al. (2017)
calves, and 13 of 76969 adult camels tested between
N
2005 and 2016 (see epidemiology section)
A
M
D
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A