History of Trypanosomosis in the One-Humped Camel and Development of its Treatment and Cure, with Special Reference to Sudan
Main Article Content
Abstract
Sudan has one of the largest populations of domestic animals in Africa. One-humped camel (Camelus dromedarius) numbers were estimated at 4.5 million in 2009. Once used extensively for military transport they are still used in the transport role by spatially mobile pastoralist households and are a major source of milk and meat for these people. Trypanosomosis, due to Trypanosoma evansi, generally known as ‘surra’ but as ‘gufar’ in Sudan was first identified in camels in the country in 1902 and is the main cause of disease although T. vivax infections have recently been discovered in parts of Sudan. This protozoan disease is the most important health problem in camels, causing high morbidity and huge production losses. The causal organism, unlike most other trypanosomes, is not transmitted cyclically with tsetse (genus Glossina) flies as the vector but mechanically by biting flies mainly family Tabanidae but also by others of the Muscidae. Identification of the parasite in camel blood was initially by simple microscopic techniques but biotechnology and molecular methods now enable infection to be diagnosed at an earlier stage and with more accuracy. Prophylactic and curative treatments of trypanosomosis are notoriously complicated and uncertain with the situation in camels being exacerbated because of its peculiar physiology. Many trypanocides have been developed over time but the parasite often develops resistance to these drugs. Some drugs are successful, for some time, as both prophylactics and cures but are often accompanied by undesirable side effects. Other drugs used on conventional domestic stock are ineffective in camels or have lower efficacy. Research on diagnosis and treatment of trypanosomosis is continuing but the disease continues to cause production losses to the detriment of national and household incomes and food security.
Keywords:
Trypanosoma evansi, Trypanosoma vivax, Camelus dromedarius, 'surra’, prophylaxis, trypanocides
Article Details
How to Cite
WILSON, R Trevor; DIOLI, Maurizio.
History of Trypanosomosis in the One-Humped Camel and Development of its Treatment and Cure, with Special Reference to Sudan.
Medical Research Archives, [S.l.], v. 9, n. 7, july 2021.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/2513>. Date accessed: 25 apr. 2024.
doi: https://doi.org/10.18103/mra.v9i7.2513.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
FAO. Statistical Yearbook 2020. Food and Agriculture Organization, Rome, Italy. 2020.
2. MARF. Statistical Bulletin for Animal Resources No 19. Information Centre, Ministry of Animal Resources and Fisheries, Khartoum, Sudan. 2009.
3. Wilson, RT. Directors of Veterinary Services in the Anglo-Egyptian Sudan: setting the scene. Vet Hist, 2018; 19(3): 242-259.
4. Wilson, RT. The one-humped camel in the Anglo-Egyptian military campaigns in Sudan, 1885-1926. J Camel Pact Res, 2016; 23(2): 193-205. doi: 10.5958/2277-8934.2016.00034.5.
5. Abdalatif, YAB., Eisa, MO. and Salih AM. Marketing and export system of camels: a case of Gadaref State Sud J Anim Sci, 2013; 15(1): 1-3.
6. Ahmad, ElGA. A short note on camels export from the Sudan: importers conditions and associated practices. Sud J Sci Tech, 2015; 16(3): 11-14.
7. Mossaad, E., Salim, B., Suganuma, K., Musinguzi, P., Hassan, MA., Elamin, EL., Mohammed, GE., Bakhiet, AO., Xuan, X., Satti, RA. and Inoue N. Trypanosoma vivax is the second leading cause of camel trypanosomosis in Sudan after Trypanosoma evansi. Parasites Vectors, 2017; 10(1): 176. doi: 10.1186/s13071-017-2117-5.
8. Röttcher, D., Schillinger, D. and Zweygarth E. Trypanosomiasis in the camel (Camelus dromedarius). Rev Sci Tech, Off Int Epiz, 1987; 6(2): 463-470.
9. Kula Jilo, Nejash Abdela, Golo Dabasa and Makida Elias. Camel trypanosomiasis: a review on past and recent research in Africa and Middle East. American-Eurasian J Sci Res, 2017; 12(1): 13-20. doi: 10.5829/idosi.aejsr.2017.13.20.
10. Evans, G. Report on “surra” disease in the Dera Ismail Khan district. Punjab Government Military Department, Delhi, India. 1880; Report No. 493: 496.
11. Evans, G. On a horse disease in India known as “surra”, probably due to a hæmatozoon. Vet J and Ann Comp Path, 1881; 13(9): 180-200. https://doi.org/10.1016/S2543-3377(17)43154-2.
12. Hoare, CA. Morphological and taxonomic studies on mammalian trypanosomes. VIII. Revision of Trypanosoma evansi. Parasitology, 1956; 46(1-2): 130-172. doi: 10.1017/S0031182000026408.
13. Fetene, E., Leta, S., Regassa, F. and Büscher. P. Global distribution, host range and prevalence of Trypanosoma vivax: a systematic review and meta-analysis. Parasites Vectors 2021; 14(1): 80. doi: 10.1186/s13071-021-04584-x.
14. El Karib, A. Animal trypanosomiasis in Sudan. Sud J Vet Sci Anim Husb, 1961; 2(1): 39-46.
15. Rahman, AH. 2005. Observations on the trypanosomosis problem outside the tsetse belts of Sudan. Rev Sci Tech, OIE, 2005; 24(3): 965-972.
16. Shommein, AM. and Osman, AM. Diseases of camels in the Sudan. Rev Sci Tech, OIE, 1987; 6(2): 481-486. doi: 10.20506/rst.6.2.298.
17. Parsani, HR., Singh, V. and Momin, RR. Common parasitic diseases of camel. Vet World, 2008; 1(10): 317-318.
18. Woo, PT. The haematocrit centrifuge technique for the diagnosis of African trypanosomiasis. Acta Trop, 1970; 27(4): 384-386.
19. Sadek, AlSM. A comparative study on susceptibility, course of parasitemia, and pattern of infection with Trypanosoma evansi between different laboratory animals. Journal of Taibah University for Science, 2020; 14(1): 1302-1307. doi: 10.1080/16583655.2020.1816323.
20. OIE. OIE-listed diseases, infections and infestations in force in 2021. World Organization for Animal Health, Paris, France. 2021. https://www.oie.int/animal-health-in-the-world/oie-listed-diseases-2021/.
21. Balfour, A. Review of some of the recent advances in tropical medicine: hygiene and tropical veterinary science with special reference to their possible bearing on medical, sanitary and veterinary work in the Anglo-Egyptian Sudan (Third report of the Wellcome Research Laboratories at the Gordon Memorial College, Khartoum). Department of Education, Sudan Government, Khartoum, Sudan. 1908.
22. Olver, A. Annual Report 1907. Sudan Veterinary Department, Khartoum., Sudan. 1907
23. Webb, EC. Trypanosomiasis of donkeys and mules in the Anglo-Egyptian Sudan. Some results of transmission experiments and arsenical treatment. J Comp Path Therap, 1915; 28(1): 1-20. https://doi.org/10.1016/S0368-1742(15)80001-0.
24. Droandi I. I1 camello: storia naturale, anatomia, fisiologia, zootecnica, patoloqia (In Italian) [The camel: natural history, anatomy, physiology, performance, pathology]. Istituto Agricolo Coloniale Italiano, Firenze. 1936.
25. Pricolo, A. and Ferraro, G. La trypanosomiasi dell camello (In Italian) [Camel trypanosomiasis in Eritrea]. Clinica Veterinaria, Milano, 1914; 37(22): 941-956.
26. Jack, JAM. Part V The Sudan. In: West JP (ed) A History of the Overseas Veterinary Services Part One. British Veterinary Association, London. 1961; 123-143.
27. Preachily, A. and Ferraro, G. Circa il trypanosome del Camail Della Colonia Eritrea. Coln Vet, 1918; 20-21:.522-524. [In Italian: On camel trypanosomiasis in the Colony of Eritrea]
28. Knowles, RH. The Formol-gel Test as applied to camels affected with Trypanosoma soudanense. J Comp Path Therap, 1924; 37: 37-44. https://doi.org/10.1016/S0368-1742(24)80004-8.
29. Knowles, RH. Treatment of camels affected with Trypanosoma soudanense with “Bayer 205", and further observations on the Formol-gel Test. J Comp Path Therap, 1925; 38: 42-46. https://doi.org/10.1016/S0368-1742(25)80005-5.
30. Knowles, RH. Trypanosomiasis in camels in the Anglo-Egyptian Sudan: diagnosis, chemotherapy, immunity. J Comp Path Therap, 1927; 40: 59-71. https://doi.org/10.1016/S0368-1742(27)80004-4.
31. Cross, HE. The camel and its diseases. Being notes for veterinary surgeons and commandants of camel corps. Bailliere, Tindall and Cox, London. 1917.
32. Tvedt, T. Colonial Technicians: The Sudan Veterinary Service 1898-1956. Thesis. University of Bergen, Bergen, Norway. 1983.
33. Wilson, RT. Directors of Veterinary Services in the Anglo-Egyptian Sudan: William (Bill) Kennedy 9 September 1924-September 1934. J Dairy Vet Anim Res, 2019; 8(3): 115-122. doi: 10.15406jdvar.2019.8.00253.
34. Wilson RT. Directors of Veterinary Services in the Anglo-Egyptian Sudan: Sampson Charles Jenkin Bennett (Assistant Director and Senior Research Officer, 1936-1944) 1925-1944. Anim Husb Dairy Vet Sci, 2019; 3: 1-9 // doi: 10.15761/AHDVS.1000167.
35. Bennett, SCJ and Kenny, PAC. Mercuric Chloride as a diagnostic agent for Trypanosomiasis in camels. J Comp Path Therap, 1928; 41: 341-353. https://doi.org/10.1016/S0368-1742(28)80035-X.
36. Bennett, SCJ. The Mercuric Chloride Test for camel trypanosomiasis. J Comp Path Therap, 1929; 42: 118-126. https://doi.org/10.1016/S0368-1742(29)80016-1.
37. Horgan, ES. and Bennett, SCJ. The Mercuric Chloride Test for trypanosomiasis in camels. Mechanism of the reaction. J Comp Path Therap, 1929; 42: 188-196. https://doi.org/10.1016/S0368-1742(29)80025-2.
38. Cocksedge, TAB. Notes on the practice of Bennett's test for surra in camels combined with use of naganol. J Comp Path Therap, 1934; 47: 64-66. https://doi.org/10.1016/S0368-1742(34)80005-7.
39. Tchernomoretz, L. An experimental study of the “Bennett And Kenny” reaction in guinea-pigs infected with Trypanosoma equiperdum. J Comp Path Therap, 1933; 46: 168-173. https://doi.org/10.1016/S0368-1742(33)80023-3.
40. Bennett, SCJ. Camel trypanosomiasis in the Sudan. Proc Pan-Afr Agric Vet. Conf, Pretoria, 1-17 August 1929, 1929; 10-15.
41. Bennett, SCJ. The control of camel trypanosomiasis. J Comp Path Therap, 1933; 46: 67-77. https://doi.org/10.1016/S0368-1742(33)80012-9.
42. Bennett SCJ. The control of camel trypanosomiasis. J Comp Path Therap, 1933; 46: 174-185. https://doi.org/10.1016/S0368-1742(33)80012-9.
43. Bennett, SCJ. Camel trypanosomiasis control. Annual Report 1935. Veterinary Services Department, Khartoum. 1936; 30-31.
44. Hoare, CA. and Bennett. SCJ. Morphological and taxonomic studies on mammalian trypanosomes: III. Spontaneous occurrence of strains of Trvpanosoma evansi devoid of the kinetonucleus. Parasitol 1937; 29(1): 43-56. https://doi.org/10.1017/S0031182000026196.
45. Hoare, CA. and Bennett, SCJ. Morphological and taxonomic studies on mammalian trypanosomes: VI. Further observations on the absence of the kinetoplast in Trypanosoma evansi. Parasitol, 1938; 30(4): 529-542. https://doi.org/10.1017/S003118200002607X.
46. Wilson, RT. Directors of Veterinary Services in the Anglo-Egyptian Sudan: Joshua Timothy Richard Evans (Director, 1952-1955) 1930-1955. Int J Vet Anim Med. 2019; 2(2): 122(1-8). doi: 10.31021/ijvam.20192122
47. Wilson RT. The incidence and control of livestock diseases in Darfur, Anglo-Egyptian Sudan, during the period of the Condominium 1916-1956. Int J Afr Hist Stud, 1979; 12(1): 162-182. https://doi.org/10.2307/218003.
48. Leach, M. Observations on the treatment of Trypanosoma evansi infection in camels. J Comp Path, 1961; 71: 109-117. https://doi.org/10.1016/S0368-1742(61)80014-3.
49. Homeida, AM., El Amin, EA., Adam, SEI. and Mahmoud, MM. Toxicity of diminazene aceturate (Berenil) to camels. J Comp Path, 1981; 91(3): 355-360. https://doi.org/10.1016/0021-9975(81)90005-0.
50. Elamin, EA., El-Bashir MOA. and Saheed, EMA. Prevalence and infection pattern of T. evansi in camels in mid-eastern Sudan. Trop Anim Hlth Prod, 1998; 30: 107-114. doi: 10.1023/A:1005047801206.
51. Gill, BS. Drug-resistance in Trypanosoma evansi. Trop Anim Hlth Prod, 1971; 3: 195-198. https://doi.org/10.1007/BF02359579.
52. Gill BS. Resistance of Trypanosoma evansi to quinapyramine, suramin, stilbamidine and tryparsamide and analysis of cross-resistance, Trans Royal Soc Trop Med Hyg, 1971; 65(3): 352-357, https://doi.org/10.1016/0035-9203(71)90013-7.
53. Luckins, AS., Boid, R., Rae, P., Mahmoud, MM., El Malik, KH. and Gray, AR. Serodiagnosis of infection with Trypanosoma evansi in camels in the Sudan. Trop Anim Hlth Prod, 1979; 11: 1-12. doi: 10.1007/BF02237757.
54. Boid, R, Mahmoud, MM. and Gray, AR. Changes in the levels of some serum enzymes in dromedary camels affected with Trypanosoma evansi. Res Vet Sci, 1980; 28)3): 336-340. https://doi.org/10.1016/S0034-5288(18)32719-X.
55. Boid, R, el-Amin EA., Mahmoud, MM, and Luckins, AG. Trypanosoma evansi infections and antibodies in goats, sheep and camels in the Sudan. Trop Anim Hlth Prod, 1981; 13: 141-146. doi: 10.1007/BF02237911.
56. Abebe, G., Jones, TW. and Boid, R. Suramin sensitivity of stocks of Trypanosoma evansi isolated in the Sudan. Trop Anim Hlth Prod, 1983; 15: 151-152. https://doi.org/10.1007/BF02239924.
57. Aradaib, IE. and Majid, AA. A simple and rapid method for detection of Trypanosoma evansi in the dromedary camel using a nested polymerase chain reaction. Kinetoplastid Biol Dis, 2006; 5: 2. doi: 10.1186/1475-9292-5-2.
58. Mossaad, E., Salim, B,, Suganuma, K, Hassan, MA., Davaasuren, B., Elamin, EL., Bakhiet, AO., Satti, RA., Xuan, X., Musinguzi, SM. and Inoue, N. Utilization of crude and recombinant ELISAs for serodiagnosis of camel trypanosomosis in Sudan. Vet Parasitol Reg Stud Reports, 2019 Apr; 16: 100278. doi: 10.1016/j.vprsr.2019.100278.
59. Elsaid, HM., Nantulya, VM. and Hilali, M. Diagnosis of Trypanosoma evansi infection among Sudanese camels imported to Egypt using card agglutination test (CATT) and antigen detection latex agglutination test (Suratex). J Protozool Res, 1998; 8: 194-200. https://doi.org/10.32268/jprotozoolres.8.3_194.
60. Rae, PF., Thrusfield, MV., Higgins. A,, Aitken, CG., Jones, TW. and Luckins, AG. Evaluation of enzyme immunoassays in the diagnosis of camel (Camelus dromedarius) trypanosomiasis: a preliminary investigation. Epidemiol Infect, 1989; 102(2): 297-307. doi: 10.1017/s0950268800029976.
61. Abdelgadir, A., Saeed, KMS., Elmalik, K. and Aradaib, IE. Molecular characterisation of drug-resistant Trypanosoma evansi isolated from naturally infected camels in Sudan. J Camel Pract Res, 2009; 16(1): 41-44.
62. Mahmoud, MM. and Gray, AR. Trypanosomiasis due to Trypanosoma evansi (Steel, 1885) Balbiani, 1888. A review of recent research. Trop Anim Hlth Prod, 1980; 12: 35-47. doi: 10.1007/BF02242629.
63. Dia, ML., Diop, C., Aminetou, M., Jacquiet, P. and Thiam, A. Some factors affecting the prevalence of Trypanosoma evansi in camels in Mauritania. Vet Parasitol, 1997; 72(2): 111-120. doi: 10.1016/s0304-4017(97)00054-x.
64 Delafosse, A. and Doutoum, AA. Prevalence of Trypanosoma evansi infection and associated risk factors in camels in eastern Chad. Vet Parasitol, 2004; 119(2-3) :155-164. doi: 10.1016/j.vetpar.2003.11.010.
65. Diall, O., Bajyana Songa, E., Magnus, E., Kouyate, B., Diallo, B., Van Meirvenne, N. and Hamers, R. Evaluation d'un test sérologique d'agglutination directe sur carte dans le diagnostic de la trypanosomes caméline à Trypanosoma evansi Rev Sci Tech, OIE, 1994; 13(3): 793-800.
66. Salah, AA., Robertson, ID. and Mohamed, AS. Prevalence and distribution of Trypanosoma evansi in camels in Somaliland. Trop Anim Hlth Prod, 2019; 51(8): 2371-2377. doi: 10.1007/s11250-019-01947-6.
67. Ali, BH. and Malik, K. Furazolidone efficacy against Trypanosoma evansi infections in mice. Vet Rec, 1983; 113: 454.
68. Ali, BH. and Hassan T. Preliminary pharmacokinetic study of isometamidium chloride (samorin) in camels. Res Vet Sci, 1984; 37(3): 376-377. https://doi.org/10.1016/S0034-5288(18)31888-5.
69. Ali, BH., Hassan, T. and Malik KH, A clinical evaluation of samorin in Trypanosoma evansi infections in Camelus dromedarius. J Vet Pharmacol Therap, 1985; 8: 208-210. doi: 10.1111/j.1365-2885.1985.tb00947.x.
70. Ali, BH. and Hassan, T. Some observations on the toxicosis of isometamidium chloride (samorin) in camels. Vet Hum Toxicol, 1986; 28(5): 424-426.
71. Ali, BH., Hassan, T. and Malik, KH. The efficacy of furazolidone against experimental infections with Trypanosoma evansi in camels and mice: comparisons with quinapyramine and suramin. Rev Elev Med Vet Pays Trop, 1986; 39: 197-201.
72. Ali, BH. A survey of some drugs commonly used in the camel. Vet Res Comm, 1988; 12(1): 67-75. https://doi.org/10.1007/BF00396405.
73. Ali, BH., Oukessou, M. and Bashir, AK. Pharmacokinetic considerations in the camel (Camelus dromedarius): A review. Comp Biochem Physiol, C, Pharmacol Toxicol Endocrinol 1996; 115(1): 1-9. https://doi.org/10.1016/S0742-8413(96)00120-X.
74. Majid AA., Ibtisam, AG. and Salih, DA. Camel research and development in the Sudan. Paper presented at the International Workshop on Camel Research and Development: Formulating a Research Agenda for the Next Decade, 9-12 December 2002, Wad Medani, Sudan. 2002.
75. Rayah, EEl., Kaminsky, R., Schmid, C. and Malik, KHEl. Drug resistance in Sudanese Trypanosoma evansi. Vet Parasitol 1999; 80(4): 281-287. https://doi.org/10.1016/S0304-4017(98)00221-0.
76. Abuessailla, A., Ismail, AA., Agab, H. and Shuaib, YA. Investigation of drug susceptibility in rats experimentally Infected with Trypanosoma evansi isolated from camels in Sudan. Int J Life Sci Sci Res, 2017; 3(4): 1167-1174. doi1 0.21276/ijlssr.2017.3.4.12.
77. Salim, B., Bakheit, MA., Kamau, J. et al. Molecular epidemiology of camel trypanosomiasis based on ITS1 rDNA and RoTat 1.2 VSG gene in the Sudan. Parasites Vectors 2011; 4: 31. https://doi.org/10.1186/1756-3305-4-31.
78. Amer, S., Ryu, O., Tada, C., Fukuda, Y., Inoue, N. and Nakai, Y. Molecular identification and phylogenetic analysis of Trypanosoma evansi from dromedary camels (Camelus dromedarius) in Egypt, a pilot study. Acta Trop 2011; 117(1): 39-46. https://doi.org/10.1016/j.actatropica.2010.09.010.
79. Salim, B., de Meeûs, T., Bakheit, MA., Kamau, J., Nakamura, I. and Sugimoto, C. Population genetics of Trypanosoma evansi from camel in the Sudan. PLoS. Negl Trop Dis, 2011; 5(6), e1196. doi: 10.1371/journal.pntd.0001196.
80. Ali, N., Croof, HIMN. and Abdalla, H. Molecular diagnosis of Trypanosoma evansi infection in Camelus dromedarius from Eastern and Western regions of the Sudan. Emirates J Food Agric, 2011; 23: 320-329.
81. Croof, HIMN., Malelle, I., Brooks, D., Abdella, HS. and Ali. NOM. Molecular Isolation and characterization of Trypanosoma evansi in dromedary camels from different regions of Sudan. Amer J Microbiol Biotech, 2017; 4(6): 67-74.
82. Bala, AIA., Abakar, AD., Mohammed, MS. and Abbas, MA. Prevalence of Trypanosoma evansi in camels in four states of great Butana, Sudan. Int J Zoo Stud, 2018; 3(3): 33-37.
83. Röttcher. D,, Schillinger, D. and Zweigarth E. Trypanosomiasis in the camel (Camelus dromedarius). Rev Sci Tech OIE, 1987; 6(2): 463-470. doi: 10.20506/rst.6.2.301.
84. Kinabo, LDB. and Bogan, JA. The pharmacology of isometamidium. J Vet Pharmacol Therap, 1988; 11(3): 233-245. doi: 10.1111/j.1365-2885.1988.tb00148.x.
85. Musa, MM,, Abdoon, AM., Nasir, BT., Salim, YI., Abdel-Rahman, AY. and Shommein, AM. Efficacy of Cymelarsan in the treatment of natural chronic Trypanosoma evansi infection in camels in the Sudan. Rev Elev Med Vet Pays Trop, 1994; 47(4): 397-400.
86. Bourdichon, AJ. Report on the use of the trypanocidal drug “TRYPAN”. J Protozool Res, 1998; 8(4) : 258-262. https://doi.org/10.32268/jprotozoolres.8.4_258.
87. Giordani, F., Morrison, LJ., Rowan, TG., De Koning, HP. and Barrett, MP. The animal trypanosomiases and their chemotherapy: a review. Parasitology, 2016; 143(14): 1862-1889. doi: 10.1017/s0031182016001268.
88. Mekonnen, G., Mohammed, EF., Kidane, W., Nesibu, A., Yohannes, H., Van Reet, N., Büscher, P. and Birhanu, H. Isometamidium chloride and homidium chloride fail to cure mice infected with Ethiopian Trypanosoma evansi type A and B. PLoS Negl Trop Dis, 2018; 12(9): e0006790. https://doi.org/10.1371/journal.pntd.0006790.
2. MARF. Statistical Bulletin for Animal Resources No 19. Information Centre, Ministry of Animal Resources and Fisheries, Khartoum, Sudan. 2009.
3. Wilson, RT. Directors of Veterinary Services in the Anglo-Egyptian Sudan: setting the scene. Vet Hist, 2018; 19(3): 242-259.
4. Wilson, RT. The one-humped camel in the Anglo-Egyptian military campaigns in Sudan, 1885-1926. J Camel Pact Res, 2016; 23(2): 193-205. doi: 10.5958/2277-8934.2016.00034.5.
5. Abdalatif, YAB., Eisa, MO. and Salih AM. Marketing and export system of camels: a case of Gadaref State Sud J Anim Sci, 2013; 15(1): 1-3.
6. Ahmad, ElGA. A short note on camels export from the Sudan: importers conditions and associated practices. Sud J Sci Tech, 2015; 16(3): 11-14.
7. Mossaad, E., Salim, B., Suganuma, K., Musinguzi, P., Hassan, MA., Elamin, EL., Mohammed, GE., Bakhiet, AO., Xuan, X., Satti, RA. and Inoue N. Trypanosoma vivax is the second leading cause of camel trypanosomosis in Sudan after Trypanosoma evansi. Parasites Vectors, 2017; 10(1): 176. doi: 10.1186/s13071-017-2117-5.
8. Röttcher, D., Schillinger, D. and Zweygarth E. Trypanosomiasis in the camel (Camelus dromedarius). Rev Sci Tech, Off Int Epiz, 1987; 6(2): 463-470.
9. Kula Jilo, Nejash Abdela, Golo Dabasa and Makida Elias. Camel trypanosomiasis: a review on past and recent research in Africa and Middle East. American-Eurasian J Sci Res, 2017; 12(1): 13-20. doi: 10.5829/idosi.aejsr.2017.13.20.
10. Evans, G. Report on “surra” disease in the Dera Ismail Khan district. Punjab Government Military Department, Delhi, India. 1880; Report No. 493: 496.
11. Evans, G. On a horse disease in India known as “surra”, probably due to a hæmatozoon. Vet J and Ann Comp Path, 1881; 13(9): 180-200. https://doi.org/10.1016/S2543-3377(17)43154-2.
12. Hoare, CA. Morphological and taxonomic studies on mammalian trypanosomes. VIII. Revision of Trypanosoma evansi. Parasitology, 1956; 46(1-2): 130-172. doi: 10.1017/S0031182000026408.
13. Fetene, E., Leta, S., Regassa, F. and Büscher. P. Global distribution, host range and prevalence of Trypanosoma vivax: a systematic review and meta-analysis. Parasites Vectors 2021; 14(1): 80. doi: 10.1186/s13071-021-04584-x.
14. El Karib, A. Animal trypanosomiasis in Sudan. Sud J Vet Sci Anim Husb, 1961; 2(1): 39-46.
15. Rahman, AH. 2005. Observations on the trypanosomosis problem outside the tsetse belts of Sudan. Rev Sci Tech, OIE, 2005; 24(3): 965-972.
16. Shommein, AM. and Osman, AM. Diseases of camels in the Sudan. Rev Sci Tech, OIE, 1987; 6(2): 481-486. doi: 10.20506/rst.6.2.298.
17. Parsani, HR., Singh, V. and Momin, RR. Common parasitic diseases of camel. Vet World, 2008; 1(10): 317-318.
18. Woo, PT. The haematocrit centrifuge technique for the diagnosis of African trypanosomiasis. Acta Trop, 1970; 27(4): 384-386.
19. Sadek, AlSM. A comparative study on susceptibility, course of parasitemia, and pattern of infection with Trypanosoma evansi between different laboratory animals. Journal of Taibah University for Science, 2020; 14(1): 1302-1307. doi: 10.1080/16583655.2020.1816323.
20. OIE. OIE-listed diseases, infections and infestations in force in 2021. World Organization for Animal Health, Paris, France. 2021. https://www.oie.int/animal-health-in-the-world/oie-listed-diseases-2021/.
21. Balfour, A. Review of some of the recent advances in tropical medicine: hygiene and tropical veterinary science with special reference to their possible bearing on medical, sanitary and veterinary work in the Anglo-Egyptian Sudan (Third report of the Wellcome Research Laboratories at the Gordon Memorial College, Khartoum). Department of Education, Sudan Government, Khartoum, Sudan. 1908.
22. Olver, A. Annual Report 1907. Sudan Veterinary Department, Khartoum., Sudan. 1907
23. Webb, EC. Trypanosomiasis of donkeys and mules in the Anglo-Egyptian Sudan. Some results of transmission experiments and arsenical treatment. J Comp Path Therap, 1915; 28(1): 1-20. https://doi.org/10.1016/S0368-1742(15)80001-0.
24. Droandi I. I1 camello: storia naturale, anatomia, fisiologia, zootecnica, patoloqia (In Italian) [The camel: natural history, anatomy, physiology, performance, pathology]. Istituto Agricolo Coloniale Italiano, Firenze. 1936.
25. Pricolo, A. and Ferraro, G. La trypanosomiasi dell camello (In Italian) [Camel trypanosomiasis in Eritrea]. Clinica Veterinaria, Milano, 1914; 37(22): 941-956.
26. Jack, JAM. Part V The Sudan. In: West JP (ed) A History of the Overseas Veterinary Services Part One. British Veterinary Association, London. 1961; 123-143.
27. Preachily, A. and Ferraro, G. Circa il trypanosome del Camail Della Colonia Eritrea. Coln Vet, 1918; 20-21:.522-524. [In Italian: On camel trypanosomiasis in the Colony of Eritrea]
28. Knowles, RH. The Formol-gel Test as applied to camels affected with Trypanosoma soudanense. J Comp Path Therap, 1924; 37: 37-44. https://doi.org/10.1016/S0368-1742(24)80004-8.
29. Knowles, RH. Treatment of camels affected with Trypanosoma soudanense with “Bayer 205", and further observations on the Formol-gel Test. J Comp Path Therap, 1925; 38: 42-46. https://doi.org/10.1016/S0368-1742(25)80005-5.
30. Knowles, RH. Trypanosomiasis in camels in the Anglo-Egyptian Sudan: diagnosis, chemotherapy, immunity. J Comp Path Therap, 1927; 40: 59-71. https://doi.org/10.1016/S0368-1742(27)80004-4.
31. Cross, HE. The camel and its diseases. Being notes for veterinary surgeons and commandants of camel corps. Bailliere, Tindall and Cox, London. 1917.
32. Tvedt, T. Colonial Technicians: The Sudan Veterinary Service 1898-1956. Thesis. University of Bergen, Bergen, Norway. 1983.
33. Wilson, RT. Directors of Veterinary Services in the Anglo-Egyptian Sudan: William (Bill) Kennedy 9 September 1924-September 1934. J Dairy Vet Anim Res, 2019; 8(3): 115-122. doi: 10.15406jdvar.2019.8.00253.
34. Wilson RT. Directors of Veterinary Services in the Anglo-Egyptian Sudan: Sampson Charles Jenkin Bennett (Assistant Director and Senior Research Officer, 1936-1944) 1925-1944. Anim Husb Dairy Vet Sci, 2019; 3: 1-9 // doi: 10.15761/AHDVS.1000167.
35. Bennett, SCJ and Kenny, PAC. Mercuric Chloride as a diagnostic agent for Trypanosomiasis in camels. J Comp Path Therap, 1928; 41: 341-353. https://doi.org/10.1016/S0368-1742(28)80035-X.
36. Bennett, SCJ. The Mercuric Chloride Test for camel trypanosomiasis. J Comp Path Therap, 1929; 42: 118-126. https://doi.org/10.1016/S0368-1742(29)80016-1.
37. Horgan, ES. and Bennett, SCJ. The Mercuric Chloride Test for trypanosomiasis in camels. Mechanism of the reaction. J Comp Path Therap, 1929; 42: 188-196. https://doi.org/10.1016/S0368-1742(29)80025-2.
38. Cocksedge, TAB. Notes on the practice of Bennett's test for surra in camels combined with use of naganol. J Comp Path Therap, 1934; 47: 64-66. https://doi.org/10.1016/S0368-1742(34)80005-7.
39. Tchernomoretz, L. An experimental study of the “Bennett And Kenny” reaction in guinea-pigs infected with Trypanosoma equiperdum. J Comp Path Therap, 1933; 46: 168-173. https://doi.org/10.1016/S0368-1742(33)80023-3.
40. Bennett, SCJ. Camel trypanosomiasis in the Sudan. Proc Pan-Afr Agric Vet. Conf, Pretoria, 1-17 August 1929, 1929; 10-15.
41. Bennett, SCJ. The control of camel trypanosomiasis. J Comp Path Therap, 1933; 46: 67-77. https://doi.org/10.1016/S0368-1742(33)80012-9.
42. Bennett SCJ. The control of camel trypanosomiasis. J Comp Path Therap, 1933; 46: 174-185. https://doi.org/10.1016/S0368-1742(33)80012-9.
43. Bennett, SCJ. Camel trypanosomiasis control. Annual Report 1935. Veterinary Services Department, Khartoum. 1936; 30-31.
44. Hoare, CA. and Bennett. SCJ. Morphological and taxonomic studies on mammalian trypanosomes: III. Spontaneous occurrence of strains of Trvpanosoma evansi devoid of the kinetonucleus. Parasitol 1937; 29(1): 43-56. https://doi.org/10.1017/S0031182000026196.
45. Hoare, CA. and Bennett, SCJ. Morphological and taxonomic studies on mammalian trypanosomes: VI. Further observations on the absence of the kinetoplast in Trypanosoma evansi. Parasitol, 1938; 30(4): 529-542. https://doi.org/10.1017/S003118200002607X.
46. Wilson, RT. Directors of Veterinary Services in the Anglo-Egyptian Sudan: Joshua Timothy Richard Evans (Director, 1952-1955) 1930-1955. Int J Vet Anim Med. 2019; 2(2): 122(1-8). doi: 10.31021/ijvam.20192122
47. Wilson RT. The incidence and control of livestock diseases in Darfur, Anglo-Egyptian Sudan, during the period of the Condominium 1916-1956. Int J Afr Hist Stud, 1979; 12(1): 162-182. https://doi.org/10.2307/218003.
48. Leach, M. Observations on the treatment of Trypanosoma evansi infection in camels. J Comp Path, 1961; 71: 109-117. https://doi.org/10.1016/S0368-1742(61)80014-3.
49. Homeida, AM., El Amin, EA., Adam, SEI. and Mahmoud, MM. Toxicity of diminazene aceturate (Berenil) to camels. J Comp Path, 1981; 91(3): 355-360. https://doi.org/10.1016/0021-9975(81)90005-0.
50. Elamin, EA., El-Bashir MOA. and Saheed, EMA. Prevalence and infection pattern of T. evansi in camels in mid-eastern Sudan. Trop Anim Hlth Prod, 1998; 30: 107-114. doi: 10.1023/A:1005047801206.
51. Gill, BS. Drug-resistance in Trypanosoma evansi. Trop Anim Hlth Prod, 1971; 3: 195-198. https://doi.org/10.1007/BF02359579.
52. Gill BS. Resistance of Trypanosoma evansi to quinapyramine, suramin, stilbamidine and tryparsamide and analysis of cross-resistance, Trans Royal Soc Trop Med Hyg, 1971; 65(3): 352-357, https://doi.org/10.1016/0035-9203(71)90013-7.
53. Luckins, AS., Boid, R., Rae, P., Mahmoud, MM., El Malik, KH. and Gray, AR. Serodiagnosis of infection with Trypanosoma evansi in camels in the Sudan. Trop Anim Hlth Prod, 1979; 11: 1-12. doi: 10.1007/BF02237757.
54. Boid, R, Mahmoud, MM. and Gray, AR. Changes in the levels of some serum enzymes in dromedary camels affected with Trypanosoma evansi. Res Vet Sci, 1980; 28)3): 336-340. https://doi.org/10.1016/S0034-5288(18)32719-X.
55. Boid, R, el-Amin EA., Mahmoud, MM, and Luckins, AG. Trypanosoma evansi infections and antibodies in goats, sheep and camels in the Sudan. Trop Anim Hlth Prod, 1981; 13: 141-146. doi: 10.1007/BF02237911.
56. Abebe, G., Jones, TW. and Boid, R. Suramin sensitivity of stocks of Trypanosoma evansi isolated in the Sudan. Trop Anim Hlth Prod, 1983; 15: 151-152. https://doi.org/10.1007/BF02239924.
57. Aradaib, IE. and Majid, AA. A simple and rapid method for detection of Trypanosoma evansi in the dromedary camel using a nested polymerase chain reaction. Kinetoplastid Biol Dis, 2006; 5: 2. doi: 10.1186/1475-9292-5-2.
58. Mossaad, E., Salim, B,, Suganuma, K, Hassan, MA., Davaasuren, B., Elamin, EL., Bakhiet, AO., Satti, RA., Xuan, X., Musinguzi, SM. and Inoue, N. Utilization of crude and recombinant ELISAs for serodiagnosis of camel trypanosomosis in Sudan. Vet Parasitol Reg Stud Reports, 2019 Apr; 16: 100278. doi: 10.1016/j.vprsr.2019.100278.
59. Elsaid, HM., Nantulya, VM. and Hilali, M. Diagnosis of Trypanosoma evansi infection among Sudanese camels imported to Egypt using card agglutination test (CATT) and antigen detection latex agglutination test (Suratex). J Protozool Res, 1998; 8: 194-200. https://doi.org/10.32268/jprotozoolres.8.3_194.
60. Rae, PF., Thrusfield, MV., Higgins. A,, Aitken, CG., Jones, TW. and Luckins, AG. Evaluation of enzyme immunoassays in the diagnosis of camel (Camelus dromedarius) trypanosomiasis: a preliminary investigation. Epidemiol Infect, 1989; 102(2): 297-307. doi: 10.1017/s0950268800029976.
61. Abdelgadir, A., Saeed, KMS., Elmalik, K. and Aradaib, IE. Molecular characterisation of drug-resistant Trypanosoma evansi isolated from naturally infected camels in Sudan. J Camel Pract Res, 2009; 16(1): 41-44.
62. Mahmoud, MM. and Gray, AR. Trypanosomiasis due to Trypanosoma evansi (Steel, 1885) Balbiani, 1888. A review of recent research. Trop Anim Hlth Prod, 1980; 12: 35-47. doi: 10.1007/BF02242629.
63. Dia, ML., Diop, C., Aminetou, M., Jacquiet, P. and Thiam, A. Some factors affecting the prevalence of Trypanosoma evansi in camels in Mauritania. Vet Parasitol, 1997; 72(2): 111-120. doi: 10.1016/s0304-4017(97)00054-x.
64 Delafosse, A. and Doutoum, AA. Prevalence of Trypanosoma evansi infection and associated risk factors in camels in eastern Chad. Vet Parasitol, 2004; 119(2-3) :155-164. doi: 10.1016/j.vetpar.2003.11.010.
65. Diall, O., Bajyana Songa, E., Magnus, E., Kouyate, B., Diallo, B., Van Meirvenne, N. and Hamers, R. Evaluation d'un test sérologique d'agglutination directe sur carte dans le diagnostic de la trypanosomes caméline à Trypanosoma evansi Rev Sci Tech, OIE, 1994; 13(3): 793-800.
66. Salah, AA., Robertson, ID. and Mohamed, AS. Prevalence and distribution of Trypanosoma evansi in camels in Somaliland. Trop Anim Hlth Prod, 2019; 51(8): 2371-2377. doi: 10.1007/s11250-019-01947-6.
67. Ali, BH. and Malik, K. Furazolidone efficacy against Trypanosoma evansi infections in mice. Vet Rec, 1983; 113: 454.
68. Ali, BH. and Hassan T. Preliminary pharmacokinetic study of isometamidium chloride (samorin) in camels. Res Vet Sci, 1984; 37(3): 376-377. https://doi.org/10.1016/S0034-5288(18)31888-5.
69. Ali, BH., Hassan, T. and Malik KH, A clinical evaluation of samorin in Trypanosoma evansi infections in Camelus dromedarius. J Vet Pharmacol Therap, 1985; 8: 208-210. doi: 10.1111/j.1365-2885.1985.tb00947.x.
70. Ali, BH. and Hassan, T. Some observations on the toxicosis of isometamidium chloride (samorin) in camels. Vet Hum Toxicol, 1986; 28(5): 424-426.
71. Ali, BH., Hassan, T. and Malik, KH. The efficacy of furazolidone against experimental infections with Trypanosoma evansi in camels and mice: comparisons with quinapyramine and suramin. Rev Elev Med Vet Pays Trop, 1986; 39: 197-201.
72. Ali, BH. A survey of some drugs commonly used in the camel. Vet Res Comm, 1988; 12(1): 67-75. https://doi.org/10.1007/BF00396405.
73. Ali, BH., Oukessou, M. and Bashir, AK. Pharmacokinetic considerations in the camel (Camelus dromedarius): A review. Comp Biochem Physiol, C, Pharmacol Toxicol Endocrinol 1996; 115(1): 1-9. https://doi.org/10.1016/S0742-8413(96)00120-X.
74. Majid AA., Ibtisam, AG. and Salih, DA. Camel research and development in the Sudan. Paper presented at the International Workshop on Camel Research and Development: Formulating a Research Agenda for the Next Decade, 9-12 December 2002, Wad Medani, Sudan. 2002.
75. Rayah, EEl., Kaminsky, R., Schmid, C. and Malik, KHEl. Drug resistance in Sudanese Trypanosoma evansi. Vet Parasitol 1999; 80(4): 281-287. https://doi.org/10.1016/S0304-4017(98)00221-0.
76. Abuessailla, A., Ismail, AA., Agab, H. and Shuaib, YA. Investigation of drug susceptibility in rats experimentally Infected with Trypanosoma evansi isolated from camels in Sudan. Int J Life Sci Sci Res, 2017; 3(4): 1167-1174. doi1 0.21276/ijlssr.2017.3.4.12.
77. Salim, B., Bakheit, MA., Kamau, J. et al. Molecular epidemiology of camel trypanosomiasis based on ITS1 rDNA and RoTat 1.2 VSG gene in the Sudan. Parasites Vectors 2011; 4: 31. https://doi.org/10.1186/1756-3305-4-31.
78. Amer, S., Ryu, O., Tada, C., Fukuda, Y., Inoue, N. and Nakai, Y. Molecular identification and phylogenetic analysis of Trypanosoma evansi from dromedary camels (Camelus dromedarius) in Egypt, a pilot study. Acta Trop 2011; 117(1): 39-46. https://doi.org/10.1016/j.actatropica.2010.09.010.
79. Salim, B., de Meeûs, T., Bakheit, MA., Kamau, J., Nakamura, I. and Sugimoto, C. Population genetics of Trypanosoma evansi from camel in the Sudan. PLoS. Negl Trop Dis, 2011; 5(6), e1196. doi: 10.1371/journal.pntd.0001196.
80. Ali, N., Croof, HIMN. and Abdalla, H. Molecular diagnosis of Trypanosoma evansi infection in Camelus dromedarius from Eastern and Western regions of the Sudan. Emirates J Food Agric, 2011; 23: 320-329.
81. Croof, HIMN., Malelle, I., Brooks, D., Abdella, HS. and Ali. NOM. Molecular Isolation and characterization of Trypanosoma evansi in dromedary camels from different regions of Sudan. Amer J Microbiol Biotech, 2017; 4(6): 67-74.
82. Bala, AIA., Abakar, AD., Mohammed, MS. and Abbas, MA. Prevalence of Trypanosoma evansi in camels in four states of great Butana, Sudan. Int J Zoo Stud, 2018; 3(3): 33-37.
83. Röttcher. D,, Schillinger, D. and Zweigarth E. Trypanosomiasis in the camel (Camelus dromedarius). Rev Sci Tech OIE, 1987; 6(2): 463-470. doi: 10.20506/rst.6.2.301.
84. Kinabo, LDB. and Bogan, JA. The pharmacology of isometamidium. J Vet Pharmacol Therap, 1988; 11(3): 233-245. doi: 10.1111/j.1365-2885.1988.tb00148.x.
85. Musa, MM,, Abdoon, AM., Nasir, BT., Salim, YI., Abdel-Rahman, AY. and Shommein, AM. Efficacy of Cymelarsan in the treatment of natural chronic Trypanosoma evansi infection in camels in the Sudan. Rev Elev Med Vet Pays Trop, 1994; 47(4): 397-400.
86. Bourdichon, AJ. Report on the use of the trypanocidal drug “TRYPAN”. J Protozool Res, 1998; 8(4) : 258-262. https://doi.org/10.32268/jprotozoolres.8.4_258.
87. Giordani, F., Morrison, LJ., Rowan, TG., De Koning, HP. and Barrett, MP. The animal trypanosomiases and their chemotherapy: a review. Parasitology, 2016; 143(14): 1862-1889. doi: 10.1017/s0031182016001268.
88. Mekonnen, G., Mohammed, EF., Kidane, W., Nesibu, A., Yohannes, H., Van Reet, N., Büscher, P. and Birhanu, H. Isometamidium chloride and homidium chloride fail to cure mice infected with Ethiopian Trypanosoma evansi type A and B. PLoS Negl Trop Dis, 2018; 12(9): e0006790. https://doi.org/10.1371/journal.pntd.0006790.