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A review of coccidiosis in Old World camels
Accepted Manuscript Title: A review of coccidiosis in Old World camels Authors: J.P. Dubey, R.K. Schuster PII: DOI: Reference:
S0304-4017(18)30297-8 https://doi.org/10.1016/j.vetpar.2018.08.008 VETPAR 8733
To appear in:
Veterinary Parasitology
Received date: Revised date: Accepted date:
6-7-2018 20-8-2018 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 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
8-20 A review of coccidiosis in Old World camels J. P. Dubey1, *Schuster, R.K.2 United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural
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Research Center, Animal Parasitic Diseases Laboratory, Beltsville, Maryland, 20705-2350, USA. 2
Central Veterinary Research Laboratory, PO Box 597, Dubai, United Arab Emirates
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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 [email protected]. Fax 301-504-9022, phone 301-504-8128.
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Coccidiosis is important as cause of mortality in camels (Camelus dromedarius and C. bactrianus). 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 stages are known.
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Highlights
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Abstract
Domesticated Old World camels (Camelus dromedarius and C. bactrianus) are important
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
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have been consistently found in numerous surveys and they are morphologically distinct. We 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 the lamina propria of small intestines; only sexual stages have been confirmed. The remaining species of Eimeria (E. rajasthani and E. dromedarii) in camels are <40 µm long and their
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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 hemorrhagic, diphtheroid to hemorrhagic colitis-associated with sexual stages; asexual stages are
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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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Coccidiosis
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Keywords: Camel (Camelus dromedarius; C. bactrianus); Eimeria Cystoisospora;
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1.Introduction
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
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Although coccidia were known as pathogens of livestock for more than two centuries, Eimeria infections in camels were reported only in 1930’s (Levine and Ivens, 1970). The
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 and Masson, 1932c) Reichenow, 1952.
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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. All camels were eventually euthanized. One of these camels was euthanized three months after
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arrival to Berlin. From this camel, Enigk (1934) described endogenous stages of "Globidium cameli" which he found mostly in the small intestines starting with duodenum and less in ileum;
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only a few stages were found in cecum. Currently, there is general agreement concerning the 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
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Matschoulsky (1939) described another new species, Eimeria dromedarii from C. dromedarius 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 parasite reported by Nöller. To reconcile the name E. cameli for two parasites (of Henry and Mason, 1932c, and Nöller, 1932), Pellérdy (1965) named the large-sized oocysts as Eimeria
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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.
Dubey and Pande (1963) described another species, Eimeria rajasthani from C. dromedarius
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in India; oocysts of this species were medium-sized (average 35 µm long) –see description later. Oocysts with varying sizes have been named as Eimeria pellerdyi by Prasad (1960) from a
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camel in London zoo (Prasad, 1960). There are no archived specimens of Eimeria from earlier descriptions and there is no way to validate their existence. Additionally, complete life cycles of
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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. 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
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endogenous stages. Kinne et al. (2002) re-described morphology of I. orlovi. The parasite was 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)
Daruish and Golemansky (1993) found coccidian oocysts in feces of 52 of 112 (46.4%)
camels from Syria. Isospora oocysts were found in feces of three camels; these oocysts were
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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 Rauf (1957) mentioned finding E. cameli-like oocysts in camels from Pakistan in an oral
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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. The following description of oocysts is based on data reported in Tables 1-3.
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3.1. Eimeria cameli (Henry and Masson, 1932) Reichenow, 1952 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.
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Micropyle is up to 28 µm wide, and 6-9 µm high; micropylar cap is absent. Polar granule and 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. 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, smooth with 2 layers, the outer light yellow and the inner brownish green. Oocyst cap is 4-8 µm
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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) Oocysts are ellipsoidal 34-39 x 25-29 µm with length-width ratio of 1.3-1.4. There is
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remarkably loww variability in dimensions of oocysts (Table 3). The oocyst wall is 2-3 µm thick with outer layer yellowish green and inner layer light brown. Micropylar end is covered with
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dome shaped cap, 4-11 µm wide and 1-3 µm high. Oocyst residuum and polar granule are 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
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prevalence data is available from the testing of a large numbers of camels at the Central 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 dromedarii and E. rajasthani are less prevalent but consistently present. Der Verdiewr et al.
(2010) tested weekly feces of calves born to a herd of 30 Bactrian camels in Sweden. Eimeria
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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). 3.5. Endogenous development of Eimeria spp.
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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 in a zoo in Alfort, France. The schizont-like structures were 350 µm in diameter. The
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microgametes were 6 µm long. From the photographs, it is apparent that the oocysts in sections were those of E. cameli. Chineme (1980) described schizonts in jejunum of a five-year-old camel
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in Nigeria that died of wasting disease. Pinhead-sized whitish-grey foci were seen grossly in 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
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species found in 140 (14%) of 960 fecal samples from camel farms they sampled twice weekly 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
endogenous stages of E. cameli-like parasite were found in intestines of camels obtained from abattoirs in Iran (Tafti et al., 2001; Borji et al., 2009; Kheirandish et al., 2012).
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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
confirmation.
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and E. dromedarii in the literature. However, there are no illustrations. This report needs
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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 detail microgametogenesis. Based on a review of descriptions of text and illustrations by
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previous authors (Henry and Masson 1932a, b, c; Enigk 1934; Ramachandran Iyer et al., 1968; 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
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with severe diarrhea were euthanized and necropsied. Similar signs were observed in 45% of 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).
Ramachandran Iyer et al. (1968) reported an outbreak of gastro-enteritis in camels in Punjab, India affecting hundreds of camels with 1-40% mortality during summer months.
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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. Mature schizonts were stated to be 900 x 500 µm and reported to contain merozoites. The
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authors clearly stated that the role of E. cameli in the disease reported was uncertain. Same conclusion applies to a similar case of hemonchosis and E. cameli associated gastroenteritis in a
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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.
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
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with eosinophilia of small intestine (mostly jejunum and ileum and rarely duodenum) was 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
camels (see section 4 below) performed at CVRL, the disease observed by Kinne and Wernery
(1997) was perhaps affected by abnormal high energy rich diet fed to racing camels at that time.
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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 feces of dead camels) and observed for 6 weeks (Kinne and Wernery 1997). Kinne and Wernery
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1998). Both camels developed intermittent diarrhea and excreted oocysts after 6 weeks. Numerous coccidian stages were found in sections of jejunum and ileum. Whether there were
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concurrent infections with other microbes is not clear. 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
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(Baycox® 5%, 20 mg/kg of body weight) on different days. One animal infected with the high dose 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
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
irrespective of treatment or infection dose. Patent periods ranged from 18 to 38 days in the treated and 32
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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 are usually ovoid. Sporulation occurs rapidly and some sporulate in host if post mortem is
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delayed (Fig 1D). Sporulated oocysts might be slightly larger than unsporulated oocysts. Sporocysts are 20 x 15 µm and they contain elongated or ovoid sporozoites. Endogenous
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development occurs in the large intestine. Asexual stages are unknown. Microgamonts are big and contain hundreds of microgametes. A micropyle, oocyst residuum, and Stieda bodies are
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absent.
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
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camels. In a comprehensive investigation of dairy camels, most infections were in winter and 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 oocysts sporulate rapidly and calves become infected soon after birth; excretion of oocysts in newborn camels is probably the source of infection to other camels. Currently, there is no
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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
Affected calves develop diarrhea and dehydration and can die within a short time. The
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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 Fecal examination and histopathology can aid diagnosis. Of the three common species of
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Eimeria in camel feces, E. cameli, E. rajasthani, and E. dromedarii are morphologically 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.
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Oocysts of C. orlovi are often excreted sporulated and they contain two sporocysts, 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 (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 dromedary calves (Hussein et al.,1987). Gerlach (2008) attempted to examine the efficacy of
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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.
Camels are highly susceptible to the adverse effects of ionophoric antibiotics (monensin,
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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. 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. References
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Iwanoff-Gobzem, P.S., 1934. Die Kokzidiose der Kamele. Zeitschr. Infektionskr. Haust. 46, 1-4.
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Kheirandish, R., Nourollahi-Fard, S.R., Faryabi, Z., 2012. Prevalence and pathologic study of Eimeria cameli in slaughtered camels. Eurasian J. Vet. Sci. 28, 138-141.
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Kinne, J., Wernery, U., 1997. Severe outbreak of camel coccidiosis in the United Arab Emirates. J. Camel Pract. Res. 4, 261-265.
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Kinne, J., Wernery, U., 1998. Pathological studies on camel coccidiosis in the United Arab Emirates. Proceedings of the Third Annual Meeting for Animal Production Under Arid Conditions. 1, 131-142.
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Kinne, J., Ali, M., Wernery, U., 2001. Camel coccidiosis caused by Isospora orlovi in the United Arab Emirates. Emir. J. Agric. Sci. 13, 62-65.
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Kinne, J., Ali, M., Wernery, U., Dubey, J.P., 2002. Clinical large intestinal coccidiosis in camels (Camelus dromedarius) in the United Arab Emirates: description of lesions, endogenous stages, and redescription of Isospora orlovi, Tsygankov, 1950 oocysts. J. Parasitol. 88, 548-552.
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Levine N.D., and Ivens, V., 1970. The Coccidian Parasites (Protozoa, Sporozoa) of Ruminants. University of Illinois Press. Illinois Biological Monographs no. 44. 1-278. Mahmoud, O., Haroun, E.M., Magzoub, M., Sulman, A., 1998. Coccidial infection in camels of Gassim region, Central Saudi Arabia. J. Camel Pract. Res. 5, 257-260. Mirza, M.Y., Al-Rawas, A.Y., 1976. Coccidia (Protozoa Eimeridiae) from camels (Camelus dromedarius) in Iraq. Bull. Biol. Res. Center, Baghdad. 7, 24-31.
Morrison, D.A., Bornstein, S., Thebo, P., Wernery, U., Kinne, J., Mattsson, J.G., 2004. The current status of the small subunit rRNA phylogeny of the coccidia (Sporozoa). Int. J. Parasitol. 34, 501-514.
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Nakayima, J., Kabasa, W., Aleper, D., Okidi, D., 2017. Prevalence of endo-parasites in donkeys and camels in Karamoja sub-region, North-eastern Uganda. J. Vet. Med. Anim. Health. 9, 11-15. Narnaware, S.D., Kumar, S., Dahiya, S.S., Patil, N.V., 2017. Concurrent infection of coccidiosis and haemonchosis in a dromedary camel calf from Rajasthan, India. J Camel Pract. Res. 24, 225-228. Nöller, W., 1932. Ueber Coccidien beim Kamel (Eimeria cameli n. sp.). Sitzungsberichte. Gesellsch. Naturf. Fr. Berlin. 1932, 417-418.
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Partani, A.K., Kumar, D., Manohar, G.S., 1999. Prevalence of Eimeria infection in camels (Camelus dromedarius) at Bikaner (Rajasthan). J. Camel Pract. Res. 6, 69-71.
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Pellérdy, L.P., 1965. Coccidia and coccidiosis.514-516. Pub. House Hung. Acad. Sci., Budapest
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Prasad, H., 1960. Studies on the coccidia of some mammals of the families Bovidae, Cervidae and Camelidae. Zeits. Parasitenkunde. 20, 390-400.
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Raisinghani, P.M., Manohar, G.S., Yadav, J.S., 1987. Isospora infection in the Indian camel Camelus dromedarius. Indian J. Parasitol. 11, 93-94.
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Ramachandran Iyer, P.K., Ramachandran, S., Joshi, T.P., 1968. An outbreak of haemorrhagic gastro-enteritis in camels (Camelus dromedarius). Ann. Parasitol. Hum. Comp. 43, 5-14.
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Rangarao, G.S.C., Sharma, R.L., 1997. Intestinal coccidiosis due to Eimeria rajasthani in camel (Camelus dromedarius). Indian Vet. J. 74, 427-428.
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Reichenow, E. (1952). Grundriss der Protozoologie für Arzte and Tierärzte. Third edition. Barth, Leipzig. 1-102.
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Ryšavý, B., 1954. Prispevek k poznani kokcidii nasich i dovezenych obratlovcu. Cesk. Parasitol. 1, 131-143.
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Sazmand, A., Hamidinejat, H., Hekmatimoghaddam, S., Asadollahi, Z., Mirabdollahi, S., 2012. Eimeria infection in camels (Camelus dromedarius) in Yazd province, central Iran. Trop. Biomed. 29, 77-80. Schuster, R.K., Sivakumar, S, Kinne, J. (2015): Parasites in camels in the United Arab Emirates. International Conference dedicated to the 95th anniversary of the cathederes Parasitology and Veterinary Hygiene. Moscow 11-13 Nov. 2015.
Schuster, R.K., Sivakumar, S., Nagy, P., Juhasz, J., Ismail, A., Kinne, J., 2017. Cystoisospora orlovi (Eimeriorina: Sarcocystidae) - a little known coccidian of the Old World camelids. J. Camel Pract. Res. 24, 117-122.
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Tafti, A.K., Maleki, M., Oryan, A., 2001. Pathological study of intestines and mesenteric lymph nodes of camels (Camelus dromedarius) slaughtered in Iran. J. Camel Pract. Res. 8, 209213. Tsygankov, A.A., 1950. To revision of species composition of camel coccidia. Investiya of the Acad. Sci. Kazakh SSP. 8, 174-185. Wei, J., Wang, Z., 1990. Survey of Eimeria sp. in Bactrian camels in Inner Mongolia. Chinese Vet. J. 16, 23-24 (in Chinese).
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Yagoub, I.A., 1989. Coccidiosis in Sudanese camels (Camelus dromedarius): 1--First record and description of Eimeria spp. harboured by camels in the eastern region of Sudan. J. Protozool. 36, 422-423.
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Yakhchali, M., Cheraghi, E., 2007. Eimeriosis in Bactrian and Dromedary camels in the Miandoab Region, Iran. Acta Vet. (Beograd). 57, 545-552.
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Yakhchali, M., Athari, S., 2010. A study on prevalence of Eimeria spp. infection in camels of Tabriz region. Arch. Razi Inst. 65, 111-115. Yakimoff, W.L., 1934. Zur Frage der Coccidien der Kamele. Arch. Wiss. Prakt. Tierheilk. 68, 134-137.
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Yakimoff, W.L., Matschoulsky, S.N., 1939. IV. On a new coccidium from camels, Eimeria 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 scouring camel calves (Camelus dromedarius). Vet. Rec. 151, 548-549.
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Legend Fig.1. Coccidian oocysts from camel. Unstained. (A) Eimeria cameli, unsporulated. Note large 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 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).
A
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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).
D
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CC
A
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U
N
A
M
Figr-1
D
TE
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CC
A
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U
N
A
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Figr-2
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CC
A
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A
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Figr-3
Table 1 Details of of Eimeria camelii oocysts in one-humped camel (Camelus dromedarius); sizes given are in µm Oocyst wall
Micropyle
Sporocysts
Remarks
80-100 x 6394
10.415.6 thick
10-14 wide
NS
75 x 95 x 5570
Ns
NS
NS
Wall 10.415.6 thick, micropyle 1014 wide, 2 layers Oocyst wall 59 thick, 3 layers. Sporocysts 40-50 x 14.520 (45 x 18)for E. kazachstanica, now regarded as E. cameli
67 x 57 (n=1)
NS
NS
NS
80-100 x 6070
NS
27x 13
NS
78-100 x 5872 (180 from 50 camels); average 87 x 66 86-108 x 6186
7-9
10-18 x 24 cap
30-39 x 15-20 (n=100 from 50 camels)
NS
18-28 x 6-9
78-98 x 64-72 (n=100)
NS
NS=not stated.
4.0-8
Henry and Masson (1932a)
[10-15], (1620)
NS
India
Pyriform oocysts, length-width ratio 1.1-1.4
[8], (22-24)
Iraq
Dubey and Pande (1964) Ramachandran Iyer et al. (1968) Mirza and AlRawas (1976)
Oocyst wall with 3 layers, micropyle 18.5-27.8 From 9 camels—for complete description see text The dark colored outer wall can be broken by light pressure
[23-25], (27)
Saudi Arabia
Kawasmeh and Elbihari (1983)
[12-15], (2630)
Sudan
Yagoub (1989)
[8–20] , (24)
UAE
Gerlach (2008)
U
India
N
39-41 x 15-19
France
NS
A
7-18
Reference
Tsygankov (1950)
M
D
TE
30-40 x 18-20
Country
Russia
Wall 3-15 thick
17-26 x 610
EP
CC
A
63-81 x 51-61
Sporulation time [days], temperature (oC) NS
SC RI PT
Unsporulated oocysts
D
TE
EP
CC
A
SC RI PT
U
N
A
M
Table 2 Details of Eimeria dromedarii oocysts in one-humped camel (C. dromedarius); sizes given are in µm L/W ratio
Microp yle
Sporocy sts
Remarks
23-32 x 20-25
27 x 23
NS
Cap 6.88.4 x 23
NS
26-28 x 21-23 (n=100)
27 x 21
1.19 1.33
5-7 x 23
10-11 x 8.5 (n=50)
24-32 x 20-23 (n=200 from 50 camels) 24-33 x 19-25 (n=120)
28 x 22
1.11.3
4-8 x 23 micropy lar cap
8-11 x 69 (n=150 from 40 camels)
Oocysts mostly oval, few spherical oocyst wall brown, 0.81.4 thick Subspherica l to spherical, oocyst wall bilayered, outer layer yellowish green Sporocysts average 10 x 8
29 x 23
1.17 1.38 91.2 8)
6-8 x 12
Ovoid, 7-11 x 69 (9.8 x 7.5)
Sporulati on time, [days],te mperatu re (oC) [15-17], (10-12)
Country
Refer ence
Russia
Yakimoff and Matschoulsky (1939)
NS
India
Dubey and Pande (1964)
[4], (2224)
Iraq
Mirza and AlRawas (1976)
NS
Saudi Arabia
Kasim et al. (1985)
[5-7], (26-30)
Sudan
Yagoub (1989)
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Avera ge
A
NS=not stated. L/W=length/width ratio
1.18 1.35 (1.2 7)
4-6
A
M
D
TE EP 28 x 23
CC
23-33 x 19-24 (n=150)
N
U
Unsporula ted oocysts
Ovoid, 7-10 x 58 (9 x 7)
Ellipsoidal or spherical, bilayered oocyst wall, outer light yellow, inner brownish green Subspherica l to ovoid, 2 layered wall, outer pale yellow, inner dark green
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CC
A
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N
A
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Table 3 Details of Eimeria rajasthanii oocysts in one-humped camel (C. dromedarius); sizes given are in µm L/W ratio
Microp ylar cap (wide, high)
Sporocy sts
Remarks
35-39 x 25-27 (n=100)
36 x 25
1.301.44
8-11 x 2-3
14-15 x 811(n=50 )
34-39 x 25-29 (n=100)
36 x 26
1.351.41
6-9 x 12.5
12-15 x 9-11
34-39 x 26-29 (n=100)
35 x 26
1.311.36
4-7
12-16 x 9-11
9-12 x 2-3
14-15 x 8-12
Oocysts ellipsoidal, bilayered, sporozoites 10-14 x 3-4 Bilayered oocyst wall, outer layer light yellow, inner layer brownish green Bilayered oocyst wall, outer layer pale green, inner layer yellowish brown Ellipsoidal
A
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D
N
A
M
30-40 x 36 x 15 23-29 NS=not stated. L/W=length /width ratio
Sporulat ion time [days], tempera ture (oC) 7 days (26-30)
Countr y
Reference
India
Dubey and Pande (1963, 1964)
7-8 (2528)
Saudi Arabia
Kasim et al. (1985)
6-8 (2630)
Sudan
Yagoub (1989)
4-5
India
Rangarao and Sharma (1997)
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Averag e
U
Unspor ulated oocysts
Table 4 Prevalence of Eimeria species* in Old World camels Reference
sample d 223
15.2
E. dri, only species reported
E. rai, E. dr, E. cai, E. ba, E. pe. Samples collected 1982-1987 from Bactrian camels E. ra in 28 (62%) E. dr in 20 (44%) E. ca in 1 (2.2%) No clinical signs, rectal samples from calves < 10 month-old from 1 farm E. ra in 13 (4%). Other species in 64 E. dri, E. ca, E. pe, E. rai
Abubakr et al. (2000) Wei and Wang (1990)
Inner Mongolia
321
50.0
India
Rajasthan
45
62.2
India
Punjab
321
24.0
India
Rajasthan
897
25.1
Iran
Miandoab region
125
12.8
Iran
Mashhad
306
Iran
Tabriz
164
20.7
100
29
305
9.5
200
NS
Iran
Yazad Province
A
Iraq
Saudi Arabia
D 18.6
TE
EP Kerman
CC
Iran
Hofuf, easten province
960
33.3 % of Bacterian camels versus 14.3% of dromedarian camels infected. Eimeria species reported: E. ra 15.6% (only Bactrian camels), E. ca 11.1%, E. dr 4.4%. Diarrhea in young calves Samples collected at an abattoir. Lesions associated with E. ca detected in 29 camels E. ba 52.4%, E. ca 19.3%, E. pe 15.6%, E. dr 12.6% Samples collected at an abattoir. Lesions associated with E. ca detected in 29 camels E. ca 14 (47.5%), E. dr 13 (42.5%), E. ba 2 (10.0%) 30 samples from northern Iraq were negative for oocysts. Of 170 samples from central Iraq, E. ca was found in 68 (40% and E. dr in 86 (50.65%) E. ca oocysts found in 146 of 960 samples of feces collected twice weekly from an unspecified
M
China
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Bahrain
% Remarks positive
U
No.
N
Region
A
Country
14
Dubey and Pande (1963, 1964)
Gill (1976) Partani et al. (1999) Yakhchali and Cheraghi (2007)
Borji et al. (2009) Yakhchali and Athari (2010) Kheirandish et al. (2012) Sazmand et al. (2012) Mirza and AlRawas (1976)
Kawasmeh and Elbihari (1983)
41.6
Saudi Arabia
5 regions
385
40
Saudi Arabia
Gassim region
240
12.8
230
17.4
Sudan
Dubai
13,301
Uganda
Karamoja
82
11
467
74.4
TE
M
D
USSR
A
UAE
Kasim et al. (1985)
Hussein et al. (1987)
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500
U
4 regions
N
Saudi Arabia
number of camels for 12 consecutive months Prevalence reported for 4 different regions in 6 months to 5 years-old camels; E. dr 28.4%, E. ra 22.2%, E. ca E. dr was the most prevalent, followed by E. ra, and the least prevalent was E. ca, but relative figures were not stated. Clinical signs observed in young camels Intestines and feces from camels at an abattoir, 15.7% of 83 adults and 10.2% of calves infected. In adult 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% E. ra in 21 (9.1%) E. dr in 15 (6.5%) E. ca in 9 (3.9%) E. ca in 1469 (13%) E. ra in 578 (6%) E. dr in452(4%) E. ca 100% Eimeria species
Mahmoud et al. (1998)
Yagoub (1989)
CVRL annual report (2007) Nakayima et al. (2017) Tsygankov (1950)
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*E. ba= E. bactriani, E. ca= E. cameli, E. dr= E. dromedarii, E. pe= E. pellerdyi, E. ra= E. rajasthani
Table 5 Prevalence of Eimeria species in camels in UAEa
Prevalence (%)
Number E. cameli
E. dromedarii
12,443
12.9
2009
11.474
14.4
2010
3,212
17.5
2011
3,174
13.7
2012
3,964
7.7
2013
2,718
8.4
2014
4,258
16.6
2015
3,182
13.3
2016
3,934
11.5
4.5
2.9
5.6
3.4
7.4
4.8
2.6
3.6
1.5
1.9
3.6
2.6
5.6
4.6
5.1
2.9
3.0
3.1
a
TE
D
M
A
N
U
2008
E. rajasthani
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Year
Samples were processed at the Central Veterinary Research Laboratory (CVRL), Dubai, and reported by Schuster et
A
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al. (2015)
Table 6 Morphology of Cystoisospora orlovia Sporulated oocysts NS 25-35 x 17-21 NS
NS 28-35 x 18-27 25-30 x 19-21 27-35 x 17-24 a Measurements are in µm.
Sporocysts
Sporozoites
Country
Reference
15-20 x 13-17 13-15 x 9-11 20 x 15 (n=10) 20-23 x 16-19 15-22 x 12-19
7-10 x 4-6 6-8 x 4-5 12-14 x 3-4
Russia India Dubai
Tsygankov (1950) Raisinghani et al. (1987) Kinne et al. (2002)
13-17 x 3-4 12-15 x 4-5
Kenya Dubai
A
CC
EP
TE
D
M
A
N
U
NS=not stated.
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Unsporulated Oocysts 27-35 x 15-20 NS 27-33 x 20-27
Bornstein et al. (2008) Schuster et al. (2017)
Table 7 Reports of Cystoisospora orlovi in Old World camels.
Kenya
Lakipia District
Kenya
Rift Valley
India Dubai
UAE
Dubai
Reference Tsygankov (Cygankov, 1950)
C. orlovi-associated diarrhea diagnosed in in four herds. Oocysts were seen in 13 calves, 12-30 days old. Two calves died. Postmortem revealed ulcerative colitis in one calf with intra-lesional coccidian stages Oocysts were detected in feces of 21 of 253 calves. 19 of 21 calves excreting oocysts had diarrhea. Oocysts were not found in healthy calves and in calves older than 8 weeks of age Oocysts found in feces of a 6-month old calf with diarrhea Outbreak of diarrhea on 2 farms. 22 calves that died were necropsied. Colitis was found in 8 calves. Endogenous stages of C. orlovi were detected in large intestine Oocysts were found in feces of 72 of 2885 samples from calves, and 13 of 76969 adult camels tested between 2005 and 2016 (see epidemiology section)
Younan et al. (2002)
A
CC
EP
TE
D
M
A
N
UAE
Remarks Oocysts detected in 10 calves, 10-35 days- old
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Region
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Country Russia
Bornstein et al. (2008)
Raisinghani et al. (1987) Kinne et al. (2001, 2002)
Schuster et al. (2017)
S0304-4017(18)30297-8 https://doi.org/10.1016/j.vetpar.2018.08.008 VETPAR 8733
To appear in:
Veterinary Parasitology
Received date: Revised date: Accepted date:
6-7-2018 20-8-2018 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 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
8-20 A review of coccidiosis in Old World camels J. P. Dubey1, *Schuster, R.K.2 United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural
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1
Research Center, Animal Parasitic Diseases Laboratory, Beltsville, Maryland, 20705-2350, USA. 2
Central Veterinary Research Laboratory, PO Box 597, Dubai, United Arab Emirates
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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 [email protected]. Fax 301-504-9022, phone 301-504-8128.
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Coccidiosis is important as cause of mortality in camels (Camelus dromedarius and C. bactrianus). 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 stages are known.
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Highlights
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Abstract
Domesticated Old World camels (Camelus dromedarius and C. bactrianus) are important
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
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have been consistently found in numerous surveys and they are morphologically distinct. We 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 the lamina propria of small intestines; only sexual stages have been confirmed. The remaining species of Eimeria (E. rajasthani and E. dromedarii) in camels are <40 µm long and their
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endogenous stages are unknown. There is one valid species of Cystoisospora, C. orlovi in camels
N
and is associated with severe disease in young camels, both pastoral and stall fed camels. Camels
A
as young as nine days old can develop severe diarrhea and can die before oocysts are detected in
M
feces. Lesions and endogenous stages are confined to the large intestine. The main lesion is hemorrhagic, diphtheroid to hemorrhagic colitis-associated with sexual stages; asexual stages are
D
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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Coccidiosis
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Keywords: Camel (Camelus dromedarius; C. bactrianus); Eimeria Cystoisospora;
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1.Introduction
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
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Although coccidia were known as pathogens of livestock for more than two centuries, Eimeria infections in camels were reported only in 1930’s (Levine and Ivens, 1970). The
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
N
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 and Masson, 1932c) Reichenow, 1952.
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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. All camels were eventually euthanized. One of these camels was euthanized three months after
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arrival to Berlin. From this camel, Enigk (1934) described endogenous stages of "Globidium cameli" which he found mostly in the small intestines starting with duodenum and less in ileum;
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only a few stages were found in cecum. Currently, there is general agreement concerning the 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
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Matschoulsky (1939) described another new species, Eimeria dromedarii from C. dromedarius 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 parasite reported by Nöller. To reconcile the name E. cameli for two parasites (of Henry and Mason, 1932c, and Nöller, 1932), Pellérdy (1965) named the large-sized oocysts as Eimeria
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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.
Dubey and Pande (1963) described another species, Eimeria rajasthani from C. dromedarius
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in India; oocysts of this species were medium-sized (average 35 µm long) –see description later. Oocysts with varying sizes have been named as Eimeria pellerdyi by Prasad (1960) from a
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camel in London zoo (Prasad, 1960). There are no archived specimens of Eimeria from earlier descriptions and there is no way to validate their existence. Additionally, complete life cycles of
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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. 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
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endogenous stages. Kinne et al. (2002) re-described morphology of I. orlovi. The parasite was 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)
Daruish and Golemansky (1993) found coccidian oocysts in feces of 52 of 112 (46.4%)
camels from Syria. Isospora oocysts were found in feces of three camels; these oocysts were
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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 Rauf (1957) mentioned finding E. cameli-like oocysts in camels from Pakistan in an oral
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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. The following description of oocysts is based on data reported in Tables 1-3.
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3.1. Eimeria cameli (Henry and Masson, 1932) Reichenow, 1952 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.
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Micropyle is up to 28 µm wide, and 6-9 µm high; micropylar cap is absent. Polar granule and 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. 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, smooth with 2 layers, the outer light yellow and the inner brownish green. Oocyst cap is 4-8 µm
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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) Oocysts are ellipsoidal 34-39 x 25-29 µm with length-width ratio of 1.3-1.4. There is
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remarkably loww variability in dimensions of oocysts (Table 3). The oocyst wall is 2-3 µm thick with outer layer yellowish green and inner layer light brown. Micropylar end is covered with
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dome shaped cap, 4-11 µm wide and 1-3 µm high. Oocyst residuum and polar granule are 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
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prevalence data is available from the testing of a large numbers of camels at the Central 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 dromedarii and E. rajasthani are less prevalent but consistently present. Der Verdiewr et al.
(2010) tested weekly feces of calves born to a herd of 30 Bactrian camels in Sweden. Eimeria
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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). 3.5. Endogenous development of Eimeria spp.
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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 in a zoo in Alfort, France. The schizont-like structures were 350 µm in diameter. The
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microgametes were 6 µm long. From the photographs, it is apparent that the oocysts in sections were those of E. cameli. Chineme (1980) described schizonts in jejunum of a five-year-old camel
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in Nigeria that died of wasting disease. Pinhead-sized whitish-grey foci were seen grossly in 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
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species found in 140 (14%) of 960 fecal samples from camel farms they sampled twice weekly 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
endogenous stages of E. cameli-like parasite were found in intestines of camels obtained from abattoirs in Iran (Tafti et al., 2001; Borji et al., 2009; Kheirandish et al., 2012).
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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
confirmation.
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and E. dromedarii in the literature. However, there are no illustrations. This report needs
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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 detail microgametogenesis. Based on a review of descriptions of text and illustrations by
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previous authors (Henry and Masson 1932a, b, c; Enigk 1934; Ramachandran Iyer et al., 1968; 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
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with severe diarrhea were euthanized and necropsied. Similar signs were observed in 45% of 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).
Ramachandran Iyer et al. (1968) reported an outbreak of gastro-enteritis in camels in Punjab, India affecting hundreds of camels with 1-40% mortality during summer months.
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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. Mature schizonts were stated to be 900 x 500 µm and reported to contain merozoites. The
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authors clearly stated that the role of E. cameli in the disease reported was uncertain. Same conclusion applies to a similar case of hemonchosis and E. cameli associated gastroenteritis in a
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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.
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
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with eosinophilia of small intestine (mostly jejunum and ileum and rarely duodenum) was 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
camels (see section 4 below) performed at CVRL, the disease observed by Kinne and Wernery
(1997) was perhaps affected by abnormal high energy rich diet fed to racing camels at that time.
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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 feces of dead camels) and observed for 6 weeks (Kinne and Wernery 1997). Kinne and Wernery
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1998). Both camels developed intermittent diarrhea and excreted oocysts after 6 weeks. Numerous coccidian stages were found in sections of jejunum and ileum. Whether there were
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concurrent infections with other microbes is not clear. 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
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(Baycox® 5%, 20 mg/kg of body weight) on different days. One animal infected with the high dose 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
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
irrespective of treatment or infection dose. Patent periods ranged from 18 to 38 days in the treated and 32
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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 are usually ovoid. Sporulation occurs rapidly and some sporulate in host if post mortem is
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delayed (Fig 1D). Sporulated oocysts might be slightly larger than unsporulated oocysts. Sporocysts are 20 x 15 µm and they contain elongated or ovoid sporozoites. Endogenous
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development occurs in the large intestine. Asexual stages are unknown. Microgamonts are big and contain hundreds of microgametes. A micropyle, oocyst residuum, and Stieda bodies are
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absent.
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
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camels. In a comprehensive investigation of dairy camels, most infections were in winter and 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 oocysts sporulate rapidly and calves become infected soon after birth; excretion of oocysts in newborn camels is probably the source of infection to other camels. Currently, there is no
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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
Affected calves develop diarrhea and dehydration and can die within a short time. The
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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 Fecal examination and histopathology can aid diagnosis. Of the three common species of
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Eimeria in camel feces, E. cameli, E. rajasthani, and E. dromedarii are morphologically 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.
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Oocysts of C. orlovi are often excreted sporulated and they contain two sporocysts, 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 (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 dromedary calves (Hussein et al.,1987). Gerlach (2008) attempted to examine the efficacy of
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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.
Camels are highly susceptible to the adverse effects of ionophoric antibiotics (monensin,
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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. 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. References
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Morrison, D.A., Bornstein, S., Thebo, P., Wernery, U., Kinne, J., Mattsson, J.G., 2004. The current status of the small subunit rRNA phylogeny of the coccidia (Sporozoa). Int. J. Parasitol. 34, 501-514.
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Partani, A.K., Kumar, D., Manohar, G.S., 1999. Prevalence of Eimeria infection in camels (Camelus dromedarius) at Bikaner (Rajasthan). J. Camel Pract. Res. 6, 69-71.
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Prasad, H., 1960. Studies on the coccidia of some mammals of the families Bovidae, Cervidae and Camelidae. Zeits. Parasitenkunde. 20, 390-400.
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Raisinghani, P.M., Manohar, G.S., Yadav, J.S., 1987. Isospora infection in the Indian camel Camelus dromedarius. Indian J. Parasitol. 11, 93-94.
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Ramachandran Iyer, P.K., Ramachandran, S., Joshi, T.P., 1968. An outbreak of haemorrhagic gastro-enteritis in camels (Camelus dromedarius). Ann. Parasitol. Hum. Comp. 43, 5-14.
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Reichenow, E. (1952). Grundriss der Protozoologie für Arzte and Tierärzte. Third edition. Barth, Leipzig. 1-102.
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Ryšavý, B., 1954. Prispevek k poznani kokcidii nasich i dovezenych obratlovcu. Cesk. Parasitol. 1, 131-143.
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Sazmand, A., Hamidinejat, H., Hekmatimoghaddam, S., Asadollahi, Z., Mirabdollahi, S., 2012. Eimeria infection in camels (Camelus dromedarius) in Yazd province, central Iran. Trop. Biomed. 29, 77-80. Schuster, R.K., Sivakumar, S, Kinne, J. (2015): Parasites in camels in the United Arab Emirates. International Conference dedicated to the 95th anniversary of the cathederes Parasitology and Veterinary Hygiene. Moscow 11-13 Nov. 2015.
Schuster, R.K., Sivakumar, S., Nagy, P., Juhasz, J., Ismail, A., Kinne, J., 2017. Cystoisospora orlovi (Eimeriorina: Sarcocystidae) - a little known coccidian of the Old World camelids. J. Camel Pract. Res. 24, 117-122.
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Tafti, A.K., Maleki, M., Oryan, A., 2001. Pathological study of intestines and mesenteric lymph nodes of camels (Camelus dromedarius) slaughtered in Iran. J. Camel Pract. Res. 8, 209213. Tsygankov, A.A., 1950. To revision of species composition of camel coccidia. Investiya of the Acad. Sci. Kazakh SSP. 8, 174-185. Wei, J., Wang, Z., 1990. Survey of Eimeria sp. in Bactrian camels in Inner Mongolia. Chinese Vet. J. 16, 23-24 (in Chinese).
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Yagoub, I.A., 1989. Coccidiosis in Sudanese camels (Camelus dromedarius): 1--First record and description of Eimeria spp. harboured by camels in the eastern region of Sudan. J. Protozool. 36, 422-423.
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Yakhchali, M., Cheraghi, E., 2007. Eimeriosis in Bactrian and Dromedary camels in the Miandoab Region, Iran. Acta Vet. (Beograd). 57, 545-552.
M
A
Yakhchali, M., Athari, S., 2010. A study on prevalence of Eimeria spp. infection in camels of Tabriz region. Arch. Razi Inst. 65, 111-115. Yakimoff, W.L., 1934. Zur Frage der Coccidien der Kamele. Arch. Wiss. Prakt. Tierheilk. 68, 134-137.
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Yakimoff, W.L., Matschoulsky, S.N., 1939. IV. On a new coccidium from camels, Eimeria 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 scouring camel calves (Camelus dromedarius). Vet. Rec. 151, 548-549.
A
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Legend Fig.1. Coccidian oocysts from camel. Unstained. (A) Eimeria cameli, unsporulated. Note large 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 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).
A
CC
EP
TE
D
M
A
N
U
SC RI PT
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).
D
TE
EP
CC
A
SC RI PT
U
N
A
M
Figr-1
D
TE
EP
CC
A
SC RI PT
U
N
A
M
Figr-2
D
TE
EP
CC
A
SC RI PT
U
N
A
M
Figr-3
Table 1 Details of of Eimeria camelii oocysts in one-humped camel (Camelus dromedarius); sizes given are in µm Oocyst wall
Micropyle
Sporocysts
Remarks
80-100 x 6394
10.415.6 thick
10-14 wide
NS
75 x 95 x 5570
Ns
NS
NS
Wall 10.415.6 thick, micropyle 1014 wide, 2 layers Oocyst wall 59 thick, 3 layers. Sporocysts 40-50 x 14.520 (45 x 18)for E. kazachstanica, now regarded as E. cameli
67 x 57 (n=1)
NS
NS
NS
80-100 x 6070
NS
27x 13
NS
78-100 x 5872 (180 from 50 camels); average 87 x 66 86-108 x 6186
7-9
10-18 x 24 cap
30-39 x 15-20 (n=100 from 50 camels)
NS
18-28 x 6-9
78-98 x 64-72 (n=100)
NS
NS=not stated.
4.0-8
Henry and Masson (1932a)
[10-15], (1620)
NS
India
Pyriform oocysts, length-width ratio 1.1-1.4
[8], (22-24)
Iraq
Dubey and Pande (1964) Ramachandran Iyer et al. (1968) Mirza and AlRawas (1976)
Oocyst wall with 3 layers, micropyle 18.5-27.8 From 9 camels—for complete description see text The dark colored outer wall can be broken by light pressure
[23-25], (27)
Saudi Arabia
Kawasmeh and Elbihari (1983)
[12-15], (2630)
Sudan
Yagoub (1989)
[8–20] , (24)
UAE
Gerlach (2008)
U
India
N
39-41 x 15-19
France
NS
A
7-18
Reference
Tsygankov (1950)
M
D
TE
30-40 x 18-20
Country
Russia
Wall 3-15 thick
17-26 x 610
EP
CC
A
63-81 x 51-61
Sporulation time [days], temperature (oC) NS
SC RI PT
Unsporulated oocysts
D
TE
EP
CC
A
SC RI PT
U
N
A
M
Table 2 Details of Eimeria dromedarii oocysts in one-humped camel (C. dromedarius); sizes given are in µm L/W ratio
Microp yle
Sporocy sts
Remarks
23-32 x 20-25
27 x 23
NS
Cap 6.88.4 x 23
NS
26-28 x 21-23 (n=100)
27 x 21
1.19 1.33
5-7 x 23
10-11 x 8.5 (n=50)
24-32 x 20-23 (n=200 from 50 camels) 24-33 x 19-25 (n=120)
28 x 22
1.11.3
4-8 x 23 micropy lar cap
8-11 x 69 (n=150 from 40 camels)
Oocysts mostly oval, few spherical oocyst wall brown, 0.81.4 thick Subspherica l to spherical, oocyst wall bilayered, outer layer yellowish green Sporocysts average 10 x 8
29 x 23
1.17 1.38 91.2 8)
6-8 x 12
Ovoid, 7-11 x 69 (9.8 x 7.5)
Sporulati on time, [days],te mperatu re (oC) [15-17], (10-12)
Country
Refer ence
Russia
Yakimoff and Matschoulsky (1939)
NS
India
Dubey and Pande (1964)
[4], (2224)
Iraq
Mirza and AlRawas (1976)
NS
Saudi Arabia
Kasim et al. (1985)
[5-7], (26-30)
Sudan
Yagoub (1989)
SC RI PT
Avera ge
A
NS=not stated. L/W=length/width ratio
1.18 1.35 (1.2 7)
4-6
A
M
D
TE EP 28 x 23
CC
23-33 x 19-24 (n=150)
N
U
Unsporula ted oocysts
Ovoid, 7-10 x 58 (9 x 7)
Ellipsoidal or spherical, bilayered oocyst wall, outer light yellow, inner brownish green Subspherica l to ovoid, 2 layered wall, outer pale yellow, inner dark green
D
TE
EP
CC
A
SC RI PT
U
N
A
M
Table 3 Details of Eimeria rajasthanii oocysts in one-humped camel (C. dromedarius); sizes given are in µm L/W ratio
Microp ylar cap (wide, high)
Sporocy sts
Remarks
35-39 x 25-27 (n=100)
36 x 25
1.301.44
8-11 x 2-3
14-15 x 811(n=50 )
34-39 x 25-29 (n=100)
36 x 26
1.351.41
6-9 x 12.5
12-15 x 9-11
34-39 x 26-29 (n=100)
35 x 26
1.311.36
4-7
12-16 x 9-11
9-12 x 2-3
14-15 x 8-12
Oocysts ellipsoidal, bilayered, sporozoites 10-14 x 3-4 Bilayered oocyst wall, outer layer light yellow, inner layer brownish green Bilayered oocyst wall, outer layer pale green, inner layer yellowish brown Ellipsoidal
A
CC
EP
TE
D
N
A
M
30-40 x 36 x 15 23-29 NS=not stated. L/W=length /width ratio
Sporulat ion time [days], tempera ture (oC) 7 days (26-30)
Countr y
Reference
India
Dubey and Pande (1963, 1964)
7-8 (2528)
Saudi Arabia
Kasim et al. (1985)
6-8 (2630)
Sudan
Yagoub (1989)
4-5
India
Rangarao and Sharma (1997)
SC RI PT
Averag e
U
Unspor ulated oocysts
Table 4 Prevalence of Eimeria species* in Old World camels Reference
sample d 223
15.2
E. dri, only species reported
E. rai, E. dr, E. cai, E. ba, E. pe. Samples collected 1982-1987 from Bactrian camels E. ra in 28 (62%) E. dr in 20 (44%) E. ca in 1 (2.2%) No clinical signs, rectal samples from calves < 10 month-old from 1 farm E. ra in 13 (4%). Other species in 64 E. dri, E. ca, E. pe, E. rai
Abubakr et al. (2000) Wei and Wang (1990)
Inner Mongolia
321
50.0
India
Rajasthan
45
62.2
India
Punjab
321
24.0
India
Rajasthan
897
25.1
Iran
Miandoab region
125
12.8
Iran
Mashhad
306
Iran
Tabriz
164
20.7
100
29
305
9.5
200
NS
Iran
Yazad Province
A
Iraq
Saudi Arabia
D 18.6
TE
EP Kerman
CC
Iran
Hofuf, easten province
960
33.3 % of Bacterian camels versus 14.3% of dromedarian camels infected. Eimeria species reported: E. ra 15.6% (only Bactrian camels), E. ca 11.1%, E. dr 4.4%. Diarrhea in young calves Samples collected at an abattoir. Lesions associated with E. ca detected in 29 camels E. ba 52.4%, E. ca 19.3%, E. pe 15.6%, E. dr 12.6% Samples collected at an abattoir. Lesions associated with E. ca detected in 29 camels E. ca 14 (47.5%), E. dr 13 (42.5%), E. ba 2 (10.0%) 30 samples from northern Iraq were negative for oocysts. Of 170 samples from central Iraq, E. ca was found in 68 (40% and E. dr in 86 (50.65%) E. ca oocysts found in 146 of 960 samples of feces collected twice weekly from an unspecified
M
China
SC RI PT
Bahrain
% Remarks positive
U
No.
N
Region
A
Country
14
Dubey and Pande (1963, 1964)
Gill (1976) Partani et al. (1999) Yakhchali and Cheraghi (2007)
Borji et al. (2009) Yakhchali and Athari (2010) Kheirandish et al. (2012) Sazmand et al. (2012) Mirza and AlRawas (1976)
Kawasmeh and Elbihari (1983)
41.6
Saudi Arabia
5 regions
385
40
Saudi Arabia
Gassim region
240
12.8
230
17.4
Sudan
Dubai
13,301
Uganda
Karamoja
82
11
467
74.4
TE
M
D
USSR
A
UAE
Kasim et al. (1985)
Hussein et al. (1987)
SC RI PT
500
U
4 regions
N
Saudi Arabia
number of camels for 12 consecutive months Prevalence reported for 4 different regions in 6 months to 5 years-old camels; E. dr 28.4%, E. ra 22.2%, E. ca E. dr was the most prevalent, followed by E. ra, and the least prevalent was E. ca, but relative figures were not stated. Clinical signs observed in young camels Intestines and feces from camels at an abattoir, 15.7% of 83 adults and 10.2% of calves infected. In adult 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% E. ra in 21 (9.1%) E. dr in 15 (6.5%) E. ca in 9 (3.9%) E. ca in 1469 (13%) E. ra in 578 (6%) E. dr in452(4%) E. ca 100% Eimeria species
Mahmoud et al. (1998)
Yagoub (1989)
CVRL annual report (2007) Nakayima et al. (2017) Tsygankov (1950)
A
CC
EP
*E. ba= E. bactriani, E. ca= E. cameli, E. dr= E. dromedarii, E. pe= E. pellerdyi, E. ra= E. rajasthani
Table 5 Prevalence of Eimeria species in camels in UAEa
Prevalence (%)
Number E. cameli
E. dromedarii
12,443
12.9
2009
11.474
14.4
2010
3,212
17.5
2011
3,174
13.7
2012
3,964
7.7
2013
2,718
8.4
2014
4,258
16.6
2015
3,182
13.3
2016
3,934
11.5
4.5
2.9
5.6
3.4
7.4
4.8
2.6
3.6
1.5
1.9
3.6
2.6
5.6
4.6
5.1
2.9
3.0
3.1
a
TE
D
M
A
N
U
2008
E. rajasthani
SC RI PT
Year
Samples were processed at the Central Veterinary Research Laboratory (CVRL), Dubai, and reported by Schuster et
A
CC
EP
al. (2015)
Table 6 Morphology of Cystoisospora orlovia Sporulated oocysts NS 25-35 x 17-21 NS
NS 28-35 x 18-27 25-30 x 19-21 27-35 x 17-24 a Measurements are in µm.
Sporocysts
Sporozoites
Country
Reference
15-20 x 13-17 13-15 x 9-11 20 x 15 (n=10) 20-23 x 16-19 15-22 x 12-19
7-10 x 4-6 6-8 x 4-5 12-14 x 3-4
Russia India Dubai
Tsygankov (1950) Raisinghani et al. (1987) Kinne et al. (2002)
13-17 x 3-4 12-15 x 4-5
Kenya Dubai
A
CC
EP
TE
D
M
A
N
U
NS=not stated.
SC RI PT
Unsporulated Oocysts 27-35 x 15-20 NS 27-33 x 20-27
Bornstein et al. (2008) Schuster et al. (2017)
Table 7 Reports of Cystoisospora orlovi in Old World camels.
Kenya
Lakipia District
Kenya
Rift Valley
India Dubai
UAE
Dubai
Reference Tsygankov (Cygankov, 1950)
C. orlovi-associated diarrhea diagnosed in in four herds. Oocysts were seen in 13 calves, 12-30 days old. Two calves died. Postmortem revealed ulcerative colitis in one calf with intra-lesional coccidian stages Oocysts were detected in feces of 21 of 253 calves. 19 of 21 calves excreting oocysts had diarrhea. Oocysts were not found in healthy calves and in calves older than 8 weeks of age Oocysts found in feces of a 6-month old calf with diarrhea Outbreak of diarrhea on 2 farms. 22 calves that died were necropsied. Colitis was found in 8 calves. Endogenous stages of C. orlovi were detected in large intestine Oocysts were found in feces of 72 of 2885 samples from calves, and 13 of 76969 adult camels tested between 2005 and 2016 (see epidemiology section)
Younan et al. (2002)
A
CC
EP
TE
D
M
A
N
UAE
Remarks Oocysts detected in 10 calves, 10-35 days- old
SC RI PT
Region
U
Country Russia
Bornstein et al. (2008)
Raisinghani et al. (1987) Kinne et al. (2001, 2002)
Schuster et al. (2017)