STUDIES ON SOME ENDOPARASITES OF CAMELS IN THE SOUTHEASTERN AREA OF EGYPT

SCVMJ, XIII (1) 2008 81 STUDIES ON SOME ENDOPARASITES OF CAMELS IN THE SOUTHEASTERN AREA OF EGYPT **Mona A. Mahmoud ; *Amin, M.M.;*Youssef, R.R.;**El-Kattan, A.;**Azza S. A. Goda and**t.r. Abou El-Naga. *Department of Internal Medicine and Infectious Diseases Fac. Of Vet. Med. Cairo Univ. **Animal Health Department, Desert Research Center. ABSTRACT In the present study, a total of 261 camels (185 local and76 imported) from Halaieb, Shalateen and Abu-Ramad, were subjected to parasitological examination for determination of the prevalence of gastrointestinal nematodes and blood parasites. 41.08% of local and 51.3% of imported camels were found infested with nematodes. Trichostrongylus was the prevalent one in both local (20%) and imported camels (36.84%). The other recovered nematodes were Nematodiru, Trichuris and Strongyloid The blood parasites, Trypanosoma evansi and Theileria were recorded in 79.4 and 75% of local and imported camels respectively. Mixed infection of blood parasites and gastrointestinal nematodes were also found. Spring showed the highest infection rate of both blood parasites and gastrointestinal nematodes in the study area. In conclusion, Trypanosoma evansi, Theileria species and gastrointestinal nematodes constitute large problems affecting camel health and productivity especially during rainy seasons (Winter and Spring). In brief, the data obtained proved that imported camels play an important role in the epizootology of parasitic infection of camels. INTRODUCTION Camels play an important socio-economic role within the pastoral and agricultural system in the dry and semidry zones of Asia and Africa. The survival of millions of human being is dependent on the camel in such areas. For meat, milk and hair production and still an important mean of drought and transportation for large sectors of pastoral societies (El Sawalhy et al., 1996). In 1998, the total number of camels in Egypt was 135 thousands camels representing 1.1, 0.9 and 0.7% from the total number of camels in Arabian countries, Africa and in the world respect-

82 Mona A. Mahmoud et al., ively (Anon, 2000). More than 42 thousands of camels inhabit El- Shalateen area and the total number of imported camels from Sudan to Egypt through El Shalateen Veterinary quarantine was 91.299 camels in 2001 (Mahran, 2004). Camels in Egypt annually produce about 20.8, 2.3, 0.62 and 0.09 thousand tons of consumable milk, meat, hides and fibers respectively (Wardeh, 1992). Due to the few number of camels raised in Egypt, it is essential to import camels from other countries as Sudan, Somalia, Djibouti and Kenya, thus the occurrence of exotic diseases at any time could be expected and also the free movements of camels throughout the borders leads to the transmission and spreading of diseases (Abd El-Aziz, 1996). The area of the present study (Halaieb, Shalateen and Abo-Ramad triangle, Red Sea Governorate, Egypt) representing the South Eastern border of Egypt and considered the major point of entry of the imported camel from Sudan and other African countries into Egypt. The main objective of this work is to investigate some of endoparasites affecting local and imported camels in the study area. MATERIAL & METHODS Study Area: This region forms a triangular area reach about 18000 km 2, its base is about 300 km, begins at Halaieb (Lateral line 23º North, Long 36º 45ˉ) and end at Shalateen (Lateral line 23º 20ˉ, Long 36º 10ˉ) (El-Shaer, 1999). Animals: A total number of 261 dromedary camels (185 local Rashidi and 76 imported from Sudan) during the period from August 2003 till September 2004, were randomly involved in this study. They were represented various ages (3 8 years) of both sexes. Samples: 1- Faecal samples: A total of 261 faecal samples were examined using concentration floatation technique according to (Soulsby, 1982) for oviscopical examination of gastrointestinal nematodes. 2- Blood samples: Two blood samples for each camel were collected from the jugular vein of 261 camels; the first blood sample was evacuated in 5ml EDTA containing vaccutainer for blood smears, the second used for serum collection to be used latterly in serological examination. Detection of blood parasites using stained smears technique according to (Coles, 1986). 3- Clinical examination: Camels were thoroughly examined according to the methods described by (Higgins, 1986). 4- Serological examination: Indirect Enzyme Linked Immuno Sorbent Assay (ELISA):

SCVMJ, XIII (1) 2008 83 Antigens: Crude antigen of Trypanosoma evansi was supplied by the Molecular Biology Unit, Faculty of Vet. Medicine, Cairo University, Egypt. (ELISA) for determination of antibodies of Trypanosoma evansi in camel sera was done according to (Zweygarth et al., 1986 and El Sawalhy and Ebeid, 1994). RESULTS Infected camels with blood and gastrointestinal parasites showed signs of illness including, loss of body weight, edema, decreased animal production. The overall prevalence rates for gastrointestinal nematodes was 41.08and 51.3% for local and imported camels respectively, while the seasonal prevalence rates were 40.9, 52.2, 34.6 and 50% in Summer, Autumn, Winter and Spring respectively,(tables 1,2 and 3). In local camels, (Table 1), the most prevalent was Trichostrongylus (20%) followed by Nematodirus (12.9%) then Trichuris (1.62%) and Strongyloid (0.54%). In imported camels, Trichostrongylus was recorded in 36.84% of examined camels followed by Trichuris (5.26%) (Table 2). Mixed infestations were recorded in 5.9%, and 9.2% of local and imported camels respectively. The highest rate of mixed infestation was found in Spring (13.7%) followed by Autumn (8.9%). Trichostrongylus was found in all mixed infestation with other species. (Table 3). The prevalence of blood parasites (T. evansi and Theleria ) was presented in Tables (4 and 5). The overall infection rate of local camels was 79.4%. The highest prevalence 94.5% was recorded in spring. In imported camels, the overall prevalence was 75% with highest in winter (100%). Mixed infection with gastrointestinal nematodes and T. evansi was recorded in 7.5 and 14.4% of local and imported camels respectively (Table 7). Table (8) showed that, 63.1% of tested camels' sera showed antibodies against T. evansi while the rate of infection was 51.9% using stained blood smears. DISCUSSION The conditions under which camels are usually kept are not conducive to parasite transmission but surprisingly large numbers of helminthes are known to occur in the camel (El- Behari, 1985). Internal parasites constitute an important disease problem that affect the health and productivity of camel and is often more sound in areas and in certain seasons of the year (Majid et al., 1997). It was necessary, in our study, to investigate the most prevalent parasites infesting camels.

84 Mona A. Mahmoud et al., The clinical signs (signs of illness including, loss of body weight, edema, decreased animal production) appeared on examined animals were like that recorded by Mourad and El- Sherif, (2002). The overall prevalence rate of gastrointestinal nematodes infestation was 41.1 and 51.31% in local and imported camels respectively, a relatively similar rate was obtained by Awad, (1996) who recorded 52.0% in Egypt and (Anwar and Khan 1998) recorded 42% in Pakistan, while higher and lower rates were reported by Sharrif et al., (1998) 84% in Jordan, El-Salahy et al., (2000) 60% in Egypt and Kumar et al., (2001) 37.8% in India. Mourad and El- Sherif, (2002) in Egypt found that, Trichostrongylus was the most prevalent one recorded in 20 and 36.84% of local and imported camels respectively. These findings were in agreement with Awad, (1996) and Magzoub et al., (1997).This might be a result of adaptation and higher resistance of Trichostrongylus larvae to the hot dry climatic and other environmental conditions (El-Salahy et al., 2000). Mixed infestation was reported with a prevalence of 5.9 and 9.2% in local and imported camels respectively. Mixed infestation with 2 or 3 parasites in the same camel was common (El-Molla et al., 1981; Magzoub et al., 1997 and Sharrif et al., 1998). Regarding the seasonal variations, it is well known that the prevalence of gastrointestinal helminthes may vary widely from region to other as well as during the various seasons within the same region (El-Behari, 1985). Similar finding was obtained in this study. The rate of infestation was peaked during autumn (52.2%) followed by spring (50%). while the lowest one was observed during Winter (34.6%). Similar results had been recorded by Awad (1996) who reported an infection rate 67% in autumn and 51.1% in spring. In fact, helminthes infestation is precipitated by the sever stress brought on by the long migratory trip in which the camels are subjected to in the early rainy season (early weeks of autumn). During this time, camels are also weak and have poor nutritional status besides unsuitable climatic condition in autumn which favor the maintenance and development of larval stages, while Winter is not drastically affect the survival of different stages of parasites (Awad, 1996, and Agab and Abbas, 2001). In the present study, the total prevalence of blood parasites using stained blood smear examination was 9.4% in local camels and 75% in imported camels. The prevalence rate of Trypanosoma evansi was 23.7 and

SCVMJ, XIII (1) 2008 85 27.6% in local and imported camels respectively, while Theileria was 76.7 and 67.1% of local and imported camels respectively. Mixed infestation with the both blood parasites was recorded in 21.08, and 19.73% of local and imported camels respectively. The variations of rates of Trypanosoma evansi which were recorded in Egypt, either higher rates Mahran, 2004 (11.5%), and Baraka et al. 2005 (26.6%), or lower rates of same Fayed et al., 1984 (3.7%) Laila et al., 2001 (4.1%). In our opinion, these variations may be attributed to nature of the study area, climatic condition and animal influences. Serologically, 63.4% of the examined camels were proved to harbor T. evansi antibodies with sensitivity and specificity 90.4% and 65% respectively. This finding was in agreement with that of (Awad, 1996) 55.9% and Shahardar et al., (2004) 62.2% In our opinion, the high infection rate observed in this serological study proved that trypanosomiasis is prevalent in the study area although the test couldn't discriminate between past or current infection. In addition, the stained blood smears can't able to detect the chronic cases with very low parasitaemia. Theileria was also recorded in high infection rate in the present study (91.3%), this may be attributed to abundance of the vectors as hard ticks (Hayaloma dermodrii). Lower rate was recorded by different authors Abou-Elnga et al., (2004) 44.8% and Mahran, (2004) (6.4%). Spring was the most favorable season for blood parasites infection during which the prevalence rate of Trypanosoma evansi and Theileria was 7.9 and 91.3% respectively. These results were in agreement with that reported by Gruvel and Balis, (1965) who found that, the infection with Trypanosoma evansi had a seasonal variation towards the end of rainy season and in the early dry season when the biting insects are more abundent. Also Higgins, (1983) noticed that, Surra was a seasonal and regional disease in Arabian region and Saeed et al., (2002) found that, the infection rate of Trypanosomiasis was higher during the period extending from November to May, as well as Mahran, (2004) found that, Theileriosis was most prevalent during Spring. From the above findings, it could be concluded that, blood parasites including Trypanosome evansi and Theileria species and gastrointestinal nematodes constitute the large problems affecting camel health and productivity, especially during rainy seasons (Winter and Spring). In brief, the data obtained proved that, imported camels play an important role in the epizootology of parasitic diseases of camels. Our final recommendation is to replace the Veterinary quarantine from El-Shalateen city to the border line between Egypt and Sudan in order to give the chance for applying the restricted control measures when any epizootic suspected to be occurring.

86 Mona A. Mahmoud et al., Season Table (1): Seasonal dynamics of gastrointestinal nematodes infesting local camels in Halaieb,Shalateen and Abo-Ramad triangle. Number of examined camels Nemato- dirus Single infestation Trichuris Strongyloid Mixed infestations Total infestation (single+mixed) No. % No. % No. % No. % No. % No. % Summer 37 12 32.43 0 0 0 0 0 0 1 2.70 13 35.13 Autumn 52 2 3.84 20 38.46 2 3.84 0 0 5 9.61 29 55.76 Winter 59 9 15.25 6 10.16 1 1.69 1 1.69 1 1.69 18 30.50 Spring 37 1 2.70 11 29.72 0 0 0 0 4 10.81 16 43.24 Total 185 24 12.97 37 20 3 1.62 1 0.54 11 5.94 76 41.08 No. = Number. Season Table (2): Seasonal dynamics of gastrointestinal nematodes infest imported camels in Halaieb, Shalateen and Abo-Ramad triangle. Number of examined camels Trichostrongylus Nematodirus Single infestation Trich- ostrongylus Trichuris Strongyloid Mixed infestations Total infestation (single+mixed) No. % No. % No. % No. % No. % No. % Summer 24 0 0 11 45.83 1 4.16 0 0 0 0 12 50 Autumn 15 0 0 5 33.33 0 0 0 0 1 6.66 6 40 Winter 16 0 0 5 31.25 1 6.25 0 0 2 12.5 8 50 Spring 21 0 0 7 33.33 2 9.52 0 0 4 19.04 13 61. 90 Total 76 0 0 28 36.84 4 5.26 0 0 7 9.21 39 51.31 No. = Number.

SCVMJ, XIII (1) 2008 87 Table (3): Seasonal dynamics of gastrointestinal nematodes infesting local and imported camels in Halaieb, Shalateen and Abo-Ramad triangle. Season Number of examined camels Nemato- dirus Single infestation Trichostron- gylus Trichuris Strongyloid Mixed infestations Total infestation (single+mixed) No. % No. % No. % No. % No. % No. % Summer 61 12 19.67 11 18.03 1 1.63 0 0 1 1.63 25 40.98 Autumn 67 2 2.98 25 37.31 2 2.98 0 0 6 8.95 35 52.23 Winter 75 9 12 11 14.66 2 2.66 1 1.33 3 4 26 34.66 Spring 58 1 1.72 18 31.03 2 3.44 0 0 8 13.79 29 50 Total 261 24 9.19 65 24.90 7 2.68 1 0.38 18 6.89 115 44.06 No. = Number Table (4): Seasonal dynamics of blood parasites infesting local camels using stained blood smears examination. Season Single infestation Total Number Mixed Trypano- Theileria infestation of examined infestations soma evansi Spp. single+mixed camels No. % No. % No. % No. % Summer 37 1 2.70 19 51.35 3 8.10 23 62.16 Autumn 52 0 0 31 59.61 7 13.46 38 73.07 Winter 59 3 5.08 32 54.23 16 27.11 51 86.44 Spring 37 1 2.70 21 56.75 13 35.13 35 94.59 Total 185 5 2.70 103 55.67 39 21.08 147 79.45 NO. = Number of positive.

88 Mona A. Mahmoud et al., Table (5): Seasonal dynamics of blood parasites infesting imported camels using stained blood smears examination. Season Number of examined camels Single infestation Total Trypano- Mixed infestation Theileria soma infestations (single+mix Spp. evansi ed) No. % No. % No. % No. % Summer 24 1 4.16 14 58.33 3 12.5 18 75 Autumn 15 2 13.33 1 6.66 0 0 3 20 Winter 16 2 12.5 9 56.25 5 31.25 16 100 Spring 21 1 4.76 12 57.14 7 33.33 20 95.23 Total 76 6 7.89 36 47.36 15 19.73 57 75 NO. = Number of positive. Table (6): Seasonal dynamics of blood parasites infesting local and imported camels using stained blood smears examination. Single infestation Season Number Trypano- Mixed Total infestation Theileria Of examined soma infestations (single+mixed) Spp. Camels evansi No. % No. % No. % No. % Summer 61 2 3.27 33 54.09 6 9.83 41 67.21 Autumn 67 2 2.98 32 47.76 7 10.44 41 61.19 Winter 75 5 6.66 41 54.66 21 28 67 89.33 Spring 58 2 3.44 33 56.89 20 34.48 55 94.82 Total 261 11 4.21 139 53.25 54 20.68 204 78.16 NO. = Number of positive.

SCVMJ, XIII (1) 2008 89 Table (7): Mixed infestation with gastrointestinal nematodes (GIN) and Trypanosoma evansi among camels. Item Number Mixed infestation with of examined GIN. and Trypanosoma evansi camels NO. % Local 185 14 7.56 Imported 76 11 14.47 Total 261 25 9.57 GIN = gastrointestinal nematodes NO. = Number of positive. Table (8): Comparative results between stained blood smears and indirect ELISA for diagnosis of Trypanosona evansi in camels. ELISA Item Stained blood smears (parasitological method) Total positive negative positive 57 21 78 negative 6 39 45 Total 63 60 123 REFERENCES Abdel-Aziz, A. A. (1996): Studies of some diseases of exotic camels. M. V. Sc. Thesis, Faculity of Vet. Med., Cairo University, Egypt. Abou-Elnga, T. R.; Abd El-Baky, S. M. and Mahran, K.A. (2004): Some studies on Theileriosis of camels associated with rate and control to camel ticks species (Hyalomma Family: Ixodidae) in Egypt. Proc. of 3rd International Conference on Animal Production and Health North Sinai, 297-312. Agab, H. and Abbas, B. (2001): Epidemiological studies on camel diseases in Eastern Sudan. Camel Newsletter, (18): 31-43. Anon (2000): Camels in Sudan. CARDN/ ACSAD/ Camel/ p69.

90 Mona A. Mahmoud et al., Sharrif, L. A. Al-Ani, F. K.; andal- Rawashdeh, O. F.; (1998): Camels diseases in Jordon. Proceedings of The Third Annual Meeting for Animal Production Under Arid Conditions, United Arab Emirates University, 2: 77-92. Anwar, A. H. and Khan, M. N. (1998): Parasitic founa of camel in Pakistan. Proceedings of The Third Annual Meeting for Animal Production Under Arid conditions, United Arab Emirates University, 2: 69-76. Awad, H. (1996): Studies on parasitic infection in camels. Ph. D. Thesis, Faculty of Vet. Med. Cairo University, Egypt. Baraka, T. A.; Abdou, T. A.; and Abou-Elnga, R. (2005): Clinical and laboratory studies of rumen performance and blood hemato-biochemical status in Trypanosome infected camels. 4 th Int. Sci. Conf. April 2005, 1-14. Coles, E. H. (1986) : Veterinary Clinical pathology, 4 th Ed. Sounders Comp. Philadelphia, London, Toronto. Schmidt. El-Behari, S. (1985): Helminthiasis of camels. British Vet. J., 141 : 315-326. El-Molla, A. and Fahmy, F. (1981): Trials with some anthelmintics against gastrointestinal nematodes in camels. Zagazig Vet. Journal, IV : 24-30. El-Salahy, M.; Monib, M. and Arafa, M. I. (2000): Prasitological studies of some gastrointestinal parasites of camels in Assiut governorate with special reference to zoonotic nematodes. Assiut Vet. Med. J., 43 (87) : 280-294. El-Sawalhy, A. A. and Ebeid, M. A. (1994): Evaluation of different methods of diagnosis for Camel Trypanosomiasis Beni-Suef. Vet. Med. Res. IV (I/I) : 70-79. El-Sawalhy, A. A.; Montaser, A. M. and Rizk, L. G. (1996) :Proceedings of the 4 th sci. cong. Vet. Med. J. Giza, 44 (2) : 323-329. El-Shaer, H. (1999): Characterization of camel breed in Shlateen- Halaieb triangle in Southern Egypt. ( ARDN/ ACSAD/ Camel / P 67). Fayed, A. A.; Arab, R. M.; and Abozeid, A. A. (1984): Studies on some diagnostic aids and chemotherapeutic druges of camels trypanosomiasis. Vet. Med. J., 32 (3) : 219-227. Gruvel, J. and Balis, J. (1965): Trypanosoma evansi infection in camels in Chad Republic. Principle vectors Revue. Eler. Med. Vet. Pays. Top. 18: 435-449. Higgins, A. J. (1983): Observation on the diseases of the Arabian camel (Camelus dromedarius) and their

SCVMJ, XIII (1) 2008 91 control.a review. Vet. Bull., 53 (12): 1089-1097. Higgins, A. J. (1986): The camel in health and disease. Baillere, Tindall, London, Philadelphia Toronto. Kumar, R.; Sena, D. S.; Mal, G. and Sahani, M. S. (2001): Epizootiological, Haemato-biochemical and therapeutic studies on gastrointestinal nematodosis in Indian dromedary camel. International Conference of Reproduction and Production of Camelids, Al-Ain,United Arab Emirates, p.15. Laila, S. Ahmed; Allawy, T. A. and Mohamed, A. A. M. (2001) : Some epidemiological aspects of camel trypanosomiasis in Upper Egypt. International Conference on Reproduction and Production of Camelids, Al-Ain, United Arab Emirates, p. 14. Magzoub, M.; Omer, O. H.; and Haroun, E. M. (1997): Gastrointestinal parasites of dromedary camels in Gassim region, Saudi Arabia. Ind. Vet. J., 74: 373-376. Mahran, O. M. (2004): Some studies on blood parasites in camels (Camelus dromedarius) at Shalateen city, Red Sea Governorate. Assuit Vet. Med. J., 50 (102) : 172-184. Majid, A. A.; Yagoub, I. A. and Ibtisam, A. G. (1997): Internal parasites of camels in central Sudan State. ACSAD/ CARDN. The annual technical report, p. 99. Mourad, S, D. and EL-Sherif, A. M. (2002): Epizootiological study on the relation between Imported camels from Sudan and some parasitic diseases in Egypt. 10 th Sci. Cong. 2002 Fac. Vet. Med. Assuit Univ. Egypt. 321-331. Saeed, E. M.; El-Amin, E. A. and El-Bashir, M. O. (2002) : Investigation of cameline Trypano-somiasis in Mid-Eastern Sudan using Ag ELISA conjunction with parasitological examination. Deutscher Tropentag, Witzenhausen. Proc. of Challenges to Organic Farming and Sustainable Land Use in the Tropics and Subtropics. Shahardar, R. A.; Mishra, A. K. and Rao, J. R. (2004): Detection of antibodies against Trypano-soma evansi in dromedary camels by ELISA using solubilized antigens. Ind. J. of Animal Science, 74 (1): 3-6. Sharrif, L.; Al-Rawashdeh, O. M.; Al-Qudah, K. M. and Al-Ani, F. K. (1998):Prevalence of gastrointestinal helminthes, hydatid cysts and nasal myiasis in camels in Jordan. Proceeding of The Third Annual Meeting for Animal Production Under Arid Conditions, United Arab Emirates University, 2 : 108-114.

92 Mona A. Mahmoud et al., Soulsby, E. J. L. (1982): Helminth, arthropods and protozoa of domesticated animals. 7 th Ed. The English language book society. Balliere, Tindall and Cassel. London. Wardeh, M.F. (1992): The importance of the dromedary camel in the Arab countries. ACSAD, Camel Newsletter, (9): 15-19. Zweygarth, E.; Sabawa, C. and Rottcher, D. (1986): An enzyme-lin-ked immunosorbent assay for the detection of antibodies to T.bruci and T. evansi in Camelus dromdarus using peroxidase-conjugated protein A. Tropical Med. and Para., (37): 105-106. الملخص العربى اجريت هذة الدراسة على 162 جمال )281 جمل محلي و 66 جمل مستورد( فىى مطقةىة المثلىال حاليى والشالتين وأبو رماد, وقد تم اجراء فحوص لقفيليات الدم وقفيليىات امماىاءعلى هىذة الجمىال, فوجىد أن طسبة االصابة بالقفيليات الداخليىة فىى الجمىال المحليىة %82,18 و الجمىال المسىتوردة 12,15 %. وتىم التوصل الى أن جطس التريكوسىتروطجيلس كىان مىن أكثىر القفيليىات اصىابة فىى كىال مىن الجمىال المحليىة بطسىىبة %11 والجمىىال المسىىتوردة بطسىىبة %56,88, يليهىىا االصىىابة بكىىال مىىن الطيمىىاتوديرس وجىىطس تركيوريس ثم جطس ستروطجيلويد.وأوضىحت الدراسىة الىى أن االصىابة بتريباطوسىوما ايفىاطلاي والثيليريىا كاطت بطسبة 8,,%6 فى الجمال المحلية و 61 % فى الجمال المستوردة. كما وجدت اصابات ملدوجة من قفيليات الدم وقفيليات االمااء. واثبتت الدراسة أن اعلى مادل لالصابة كان فى موسم الربيى وذلى فىى مطقةىىة البحىال. والخالصىىة أن كىىال مىىن التريباطوسىوما ايفىاطلاي والثيليريىا وقفيليىات االماىاء تسىب مشاكل صحية واطتاجية كثيرة للجمال فى هذة المطاقق وخاصة فىى موسىمى الشىتاء والربيى. وقىد اثبتىت الدراسة أن الجمال المستوردة تلا دورا هاما فى طةل الادوي للجمال المحلية.