Journal of Zoo and Wildlife Medicine 31(3): 335–338, 2000 Copyright 2000 by American Association of Zoo Veterinarians
A SURVEY OF CAMEL (CAMELUS DROMEDARIUS) DISEASES IN JORDAN Odeh F. Al-Rawashdeh, D.V.M., Ph.D., Falah K. Al-Ani, D.V.M., Ph.D., Labib A. Sharrif, D.V.M., Ph.D., Khaled M. Al-Qudah, D.V.M., Ph.D., Yasin Al-Hami, D.V.M., Ms., and Nicholas Frank, D.V.M. Abstract: Information on incidences of camel (Camelus dromedarius) diseases in Jordan is scarce. In this survey, 369 live and 156 slaughtered camels were examined in four Jordanian geographic regions and the proportion of diseased camels was calculated. Intestinal parasite ova were detected in 98% of camels; one or more species of external parasites were found on the skin of all camels; 33% had nasal myiasis; and hydatid cysts were identified in 44% of the slaughtered animals. Sarcoptic mange (Sarcoptes scabiei var. cameli) and trypanasomiasis, two diseases of economic importance, were also diagnosed in 83% and 33% of the 32 and 257 examined camels, respectively. Rabies virus was detected in eight camels by use of fluorescent antibody examination of brain tissues. Foreign-body accumulation within the first and second stomach compartments was the predominant gastrointestinal disease of slaughtered adult camels (22%). Ten percent of slaughtered camels had bacterial pneumonia, with Pasteurella hemolytica most often isolated (56% of pneumonic lungs). Further investigation into the relationship between parasite burden and health in camels is required to assess the significance of the high prevalence of parasites. Key words: Camel, Camelus dromedarius, epidemiology, diseases, Jordan.
INTRODUCTION
MATERIALS AND METHODS
The domestic camel (Camelus dromedarius) is extremely well adapted to life in the deserts of Jordan, which cover 80% of the country’s land surface. Camels possess a remarkable ability to utilize nutrients from poor-quality vegetation and to survive in hot, dry conditions. The nomadic Bedouin people of Jordan still rely heavily upon them, consuming meat and milk, weaving hair into fabrics, and using them for transport, milling, and lifting water from wells.3,9 There are an estimated 18,000 camels in Jordan,13 and despite their economic, social, and logistical importance, the population size has remained stable in recent years. This lack of population growth may be due to the limited food available, to periodic severe drought, to poor husbandry practices and negligent camel owners, or to suboptimal disease recognition, prevention, and treatment.3 Studies of camel disease in Jordan have focused primarily on parasites,1,7 although serological studies of rickettsial and chlamydial diseases in domestic ruminants have been reported.15 This study assessed the incidence and distribution of diseases within Jordanian camels.
Clinical examinations were performed on 369 camels between April 1996 and February 1998. Of these, 318 were mature (46 males, 272 females), 30 were 1–2-yr-old animals (18 males, 12 females), and 21 were calves ,1 yr (11 males, 10 females). Among the 369 camels under the study, 36 of them were examined postmortem at a slaughterhouse. Also, another 120 slaughtered camels were inspected. Clinical examination data were collected and pooled from four locations, including Al-Badia (cool desert; n 5 230), Al-Ramtha (warm steppe; n 5 36), South Amman (warm temperate; n 5 30), and the Jordan Valley region (warm desert; n 5 73). Herd size ranged between 12–250 camels, with five herds classified as small (12–50 camels), six as medium (51–99 camels), and nine as large (.100 camels). Twenty percent of camels in small herds, 15% in medium herds, and 10% in large herds were sampled using systematic random methodology.14 All camels received a thorough physical examination. Parasitic diseases were diagnosed by direct smear, flotation, and fecal sedimentation (n 5 150). Parasites were identified to the genus level by examining hatched third-stage larvae. Blood samples were taken from 257 of the mature female camels, and Giemsa-stained smears were examined microscopically for the presence of Trypanosoma evansi. Rose Bengal and complement fixation tests were performed on blood samples for detection of antibodies to brucellosis. Dermatologic conditions were evaluated by direct skin examination (n 5 369) and skin scrapings (n 5 32) to identify ectoparasites and fungi. The
From the Faculty of Veterinary Medicine, Jordan University of Science and Technology, P.O. Box 3030, Irbid, Jordan (Al-Rawashdeh, Al-Ani, Sharrif, Al-Qudah, AlHami) and the Department of Veterinary Clinical Sciences, Purdue University, West Lafayette, Indiana 47907, USA (Frank).
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336 Table 1.
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Parasites identified in Jordanian camels.
Parasite species
Haemonchus longistipes Camelostrongylus mentulatus Trichostronglylus probolurus Ascaris spp. Nematodirus dromedarii Cooperia onchophora Moneizia expansa Trichuris ovis Fasciola hepatica Onchocerca fasciata Hylomma dromedari and H. anatolicum Sarcoptes scabiei var. cameli Cephalopina titillator Hydatid cysts Lungs Liver Multiple organs
Camels affected (%)
12 35 56 18 2 10 33 23 2 2 100 83 33 63 24.9 12.1
mammary glands of lactating female camels were examined directly and palpated. Milk samples (n 5 7) were collected and California mastitis testing (CMT) and microbial culture performed. Respiratory tract bacterial flora were assessed by microbial culture of nasal swabs collected at random from 22 camels. A total of 156 camel carcasses were examined postmortem. Lesions were identified, recorded, and examined by histopathology, microbial culture, or parasite identification. RESULTS Intestinal parasitis were found in 98% of the camels. Multiple parasite species were present in 52% of camels, with single-species infections in 48% (Table 1). Trypanosoma evansi was detected in 33% of camels, with the largest percentage of infected animals found within the Jordan Valley region during April–September of each year. Affected camels were anorexic, febrile, weak, and anemic. All of the camels examined in Jordan were infested with a large number of ticks; both Hyalomma dromederi and Hyalomma anatolicum were identified. Mange due to Sarcoptes scabiei var. cameli was diagnosed in 83% of the 32 camels scraped. Affected animals showed alopecia, intense irritation, and anxiety. The percentage of female camels testing positive for Brucella melitensis was low (0.5%). Diseases of the respiratory system included pneumonia, pulmonary congestion, emphysema, and pneumoconiosis. In 16 cases of bacterial pneumonia examined
at necropsy, Pasteurella hemolytica (n 5 9), Actinomyces pyogenes (n 5 3), Escherichia coli (n 5 2), and Streptococcus spp. (n 5 2) were isolated. Hydatid cysts due to Echinococcus granulosus were also identified in lung tissue (44%). Microbial culture of nasal swab samples revealed the same isolates cultured from the pneumonic lungs, with the addition of Staphylococcus spp. and Micrococcus spp. Accumulation of foreign bodies was seen in 22% of the stomachs examined at necropsy. Plastic (65%), rope and leather (23.5%), or all three objects (11.5%) were found within the first or second stomach compartments. Diarrhea was common in calves. Of 21 calves born in December and January, four calves less than 2 wk old died after developing diarrhea, and E. coli was isolated from the intestinal contents. Hepatic abscesses were detected within 1.2% of livers examined at necropsy. Actinomyces pyogenes, Staphylococcus aureus, Streptococcus virdans, and E. coli were isolated. Nervous system diseases included rabies and tetanus. Rabies infection was confirmed by fluorescent antibody testing in eight camels. Observed clinical signs included hyperesthesia, anorexia, profuse salivation, and paralysis. A single case of tetanus was detected in a camel with spasticity and muscle spasms of the jaw after it suffered a deep wound infection. Of the 66 mature female camels examined postmortem, the only reproductive tract abnormalities detected were A. pyogenes metritis in three camels and a single case of an ovarian luteal cyst. Of seven lactating camels examined, four were diagnosed with subclinical mastitis on the basis of CMT results and bacteriologic isolation. Streptococcus spp. was isolated from three glands, and E. coli was isolated from one gland. Staphylococcus aureus was isolated from the milk of one lactating camel with a history of chronic mastitis. Skin diseases found upon examination included alopecia from sarcoptic mange, subcutaneous abscesses, wounds, and dermatophytosis. Abscesses were often due to Corynebacterium pseudotuberculosis infection or chronic wounds. The wounds commonly resulted from foreign-body penetration into footpads (nails, thorns, and sharp stones) or from bite wounds inflicted by adult males during breeding seasons. Dermatophytosis caused by Trichophyton verrucosum was diagnosed in three camels with cutaneous lesions along the neck and thorax. In an isolated group of young camels, generalized encrusted lesions and alopecia were due to Trichophyton schoenleinii. Other diseases observed included suppurative ar-
AL-RAWASHDEH ET AL.—CAMEL DISEASES IN JORDAN
thritis secondary to Cryptococcus neoformans in one animal and fistulous withers infected with S. aureus in two camels. Cutaneous melanoma was seen in one 21-yr-old camel as a firm, raised, grayblack nodule in the skin of the neck area. DISCUSSION The high level of parasitic infestation in this study is similar to that previously reported within other camel populations in the region.7,8,10,18 The same species of gastrointestinal parasites have been described in camels in Iraq and Egypt,6,17 and onchocerciasis (Onchocerca fasciata) has been reported in camels in Saudi Arabia, Iraq, and Egypt.8,10 The high prevalence of ticks (100%) in this study agrees with a previously reported study where Hyalomma, Rhipicephalus, and Amblyomma species were identified.16 Camel nasal flies due to Cephalopina titillator are found in all of the Middle Eastern locations in which camels reside.5,12 The relationship between presence or degree of endoparasitic infestation, as defined by detection of parasite ova in feces, and the degree of health remains difficult to ascertain in camels. Most camels appeared to be in adequate body condition, and diarrhea in adult animals was rare. Further investigation is required to quantitate parasite burden and to assess the significance of parasitic infestation in camels. Sarcoptic mange and trypanosomiasis are two important camel diseases that were detected in the population studied. The economic impact of sarcoptic mange results from the intense anxiety associated with pruritis, causing poor weight gain or weight loss and reduced ability to work. Trypanosomiasis due to Trypanosoma evansi was detected in one third of all camels tested. The chronic debilitating nature of this disease makes it a major health concern for camels, and it is the primary reason for camels being unable to perform their roles in agriculture or transport. Trypanosmiasis infection rates in camels reported from other middle eastern countries include 47% in Iraq, 81% in Egypt, and 74% in Sudan.3,19,20 Interestingly, the proportion of camels positive for brucellosis in Jordan (0.5%) was lower than proportions reported in Chad (26%), Kenya (14%), Saudi Arabia (12%), Iraq (7%), and United Arab Emirates (1.5%).2,4 The reduced level of brucellosis in the Jordanian camel population may reflect the decreased contact of camels from the desert area with sheep and goats. The percentage of camels found with foreign bodies in the compartment 1 and 2 of the stomach (22%) is comparable to results (30.7%) from a previous study conducted in Egypt.11
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Dermatophytosis is not commonly diagnosed in camels. In addition to the two species of ringworm reported here, Trichophyton dankaliense, Trichophyton mentagrophytes, Microsporum canis, and Microsporum gypseum have been reported in camels from Iraq, Egypt, Somalia, and Saudi Arabia.21 Acknowledgment: We thank the Higher Council of Science and Technology for funding this research. Published as contribution 54/97, Jordan Badia Research and Development Program. LITERATURE CITED 1. Abdel-Hafez, S. K., F. M. Al-Yaman, and I. M. Said. 1986. Further studies on prevalence of hydatidosis in slaughtered animals from North Jordan. J. Parasitkde. 72: 89–96. 2. Afzal, M., and M. Sakkin. 1994. Survey of antibodies against various infectious disease agents in racing camels in Abu Dhabi, United Arab Emirates. Revue Sci. Tech. Off. Inter. Epizoo. 13: 787–792. 3. Al-Ani, F. K. 1997. Camel Encyclopedia. Al-Bahga Press, Jordan. 4. Al-Ani, F. K., and M. R. Al-Sharreefi. 1990. Brucellosis in camels in Iraq. J. Basic Appl. Sci. 1: 61–69. 5. Al-Ani, F. K., W. A. Khamas, and K. H. Zenad. 1991. Camel nasal myiasis: clinical, epidemiological and pathological studies in Iraq. Indian J. Anim. Sci. 61: 576– 578. 6. Altaif, K. I. 1974. Helminthes in camels in Iraq. Trop. Anim. Health Prod. 6: 55–57. 7. Al-Yaman, F. M. 1985. Prevalence of hydatidosis in slaughtered animals from North Jordan. Ann. Trop. Med. Parasitol. 79: 501–506. 8. Al-Yousif, M., and H. S. Hussein. 1994. Onchoceriasis in the Arabian camel (Camelus dromedarius) in the central region (Riyadh and Qasim Provinces) of Saudi Arabia. Arab Gulf J. Sci. Res. 12: 361–383. 9. Chatty, D. 1986. From camel to truck: the Bedouin in the modern world. Vantage Press, New York. 10. El-Bihari, S. 1980. Helminthes of the camel: a review. Br. Vet. J. 141: 315–326. 11. Fahmy, L. S., S. El-Zomor, M. B. Mostafa, and A. Hegazy. 1995. An abattoir survey of presence of foreign body in the stomach of the camel (Camelus dromedarius). J. Camel Pract. Res. 2: 139–141. 12. Fatani, A., and M. Hilali. 1994. Prevalence and monthly variations of the second and third instars of Cephalopina titillator (Diptera: Oestridae) infesting camels (Camelus dromedarius) in the eastern province of Saudi Arabia. Vet. Parasitol. 53: 145–151. 13. Food and Agriculture Organization (FAO) Production Yearbook. 1995. The Middle East and North Africa, 41st ed. Europa Publication Limited, England. 14. Martin, S. W., A. H. Meek, and P. Willeberg. 1987. Veterinary Epidemiology—Principles and Methods. Iowa State Univ. Press, Ames, Iowa. Pp. 22–47. 15. Schmatz, H. D., H. Krauss, P. Viertel, A. S. Ismail, and A. A. Hussein. 1978. Serological survey of Rickettsia
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and Chlamydia antibodies in domestic ruminants in Egypt, Somalia and Jordan. Acta Trop. 35: 101–111. 16. Schwartz, H. J., and M. Dioli. 1992. The onehumped camel (Camelus dromedarius) in Eastern Africa. Verlag Josef Margraf Scientific Books, Germany. 17. Selim, M. K., and M. S. Rahman. 1972. Enteric nematodes of camels in Egypt. Egyptian J. Vet. Sci. 9: 75–80. 18. Sharrif, L., K. Al-Qudah, and F. K. Al-Ani. 1996. Prevalence of gastrointestinal parasites in camels in Jordan. J. Camel Pract. Res. 5: 1–4.
19. Soliman, K. N. 1965. Parasites of the Camelus dromedarius in Egypt with special references to it in Sudan. Proc. Egypt. Vet. Med. Assoc. 1965: 385–396. 20. Steward, J. S. 1950. Notes on some parasites of camels (Camelus dromedarius) in the Sudan. Vet. Rec. 62: 835–837. 21. Timawy, A. M., I. Seddik, and M. Atia. 1988. Camel ringworm in upper Egypt. Assiut Vet. Med. J. 20: 54– 59. Received for publication 4 January 1999