Analyze Diet
Parasites & vectors2015; 8; 212; doi: 10.1186/s13071-015-0818-1

Epidemiology of Trypanosoma evansi and Trypanosoma vivax in domestic animals from selected districts of Tigray and Afar regions, Northern Ethiopia.

Abstract: African animal trypanosomosis, transmitted cyclically by tsetse flies or mechanically by other biting flies, causes serious inflictions to livestock health. This study investigates the extent of non-tsetse transmitted animal trypanosomosis (NTTAT) by Trypanosoma (T.) evansi and T. vivax in domestic animals in the tsetse-free regions of Northern Ethiopia, Afar and Tigray. Methods: A cross sectional study was conducted on 754 dromedary camels, 493 cattle, 264 goats, 181 sheep, 84 donkeys, 25 horses and 10 mules. The microhaematocrit centrifugation technique was used as parasitological test. Plasma was collected for serodiagnosis with CATT/T.evansi and RoTat 1.2 immune trypanolysis (ITL) while buffy coat specimens were collected for molecular diagnosis with T. evansi type A specific RoTat 1.2 PCR, T. evansi type B specific EVAB PCR and T. vivax specific TvPRAC PCR. Results: The parasitological prevalence was 4.7% in Tigray and 2.7% in Afar and significantly higher (z = 2.53, p = 0.011) in cattle (7.3%) than in the other hosts. Seroprevalence in CATT/T.evansi was 24.6% in Tigray and 13.9% in Afar and was significantly higher (z = 9.39, p < 0.001) in cattle (37.3%) than in the other hosts. On the other hand, seroprevalence assessed by ITL was only 1.9% suggesting cross reaction of CATT/T.evansi with T. vivax or other trypanosome infections. Molecular prevalence of T. evansi type A was 8.0% in Tigray and in Afar and varied from 28.0% in horses to 2.2% in sheep. It was also significantly higher (p < 0.001) in camel (11.7%) than in cattle (6.1%), donkey (6%), goat (3.8%), and sheep (2.2%). Four camels were positive for T. evansi type B. Molecular prevalence of T. vivax was 3.0% and was similar in Tigray and Afar. It didn't differ significantly among the host species except that it was not detected in horses and mules. Conclusions: NTTAT caused by T. vivax and T. evansi, is an important threat to animal health in Tigray and Afar. For the first time, we confirm the presence of T. evansi type B in Ethiopian camels. Unexplained results obtained with the current diagnostic tests in bovines warrant particular efforts to isolate and characterise trypanosome strains that circulate in Northern Ethiopia.
Publication Date: 2015-04-09 PubMed ID: 25889702PubMed Central: PMC4403896DOI: 10.1186/s13071-015-0818-1Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research examines the prevalence and epidemiology of non-tsetse transmitted animal trypanosomosis diseases, caused by Trypanosoma evansi and Trypanosoma vivax, in livestock in Northern Ethiopia.

Methods

  • The study was conducted on a variety of domestic animals including camels, cattle, goats, sheep, donkeys, horses, and mules in two northern Ethiopian regions: Tigray and Afar.
  • The researchers collected plasma and buffy coat specimens from a cross-section of 754 camels, 493 cattle, 264 goats, 181 sheep, 84 donkeys, 25 horses, and 10 mules.
  • The microhaematocrit centrifugation technique was applied as a parasitological test.
  • Various diagnostic approaches such as CATT/T.evansi and RoTat 1.2 immune trypanolysis (ITL) were used for serodiagnosis, while T. evansi type A specific RoTat 1.2 PCR, T. evansi type B specific EVAB PCR, and T. vivax specific TvPRAC PCR served for molecular diagnosis.

Results

  • The parasitological prevalence was found to be significantly higher in cattle than the other domestic animals. It was 4.7% in Tigray and 2.7% in Afar, with cattle recording the highest value of 7.3%.
  • The overall seroprevalence in CATT/T.evansi was 24.6% in Tigray and 13.9% in Afar, and again, significantly higher in cattle at 37.3%.
  • The seroprevalence assessed by ITL was lower, at 1.9%, suggesting a cross-reaction of CATT/T.evansi with T. vivax or other trypanosome infections.
  • The molecular prevalence of T. evansi type A was 8.0% in both Tigray and Afar, and varied among the species, with horses recording the highest at 28.0%, and sheep the lowest at 2.2%. It was also higher in camels than in cattle and other animals.
  • Four camels tested positive for T. evansi type B.
  • The molecular prevalence for T. vivax was 3.0%, with no significant differences among the host species, except for its absence in horses and mules.

Conclusions

  • The research concluded that non-tsetse transmitted animal trypanosomosis, caused by T. vivax and T. evansi, is a significant threat to animal health in Northern Ethiopia. This is the first research confirming the presence of T. evansi type B in Ethiopian camels.
  • The study suggests the need for additional research to understand the unexpected results obtained with the current diagnostic tests in bovines, with the goal of isolating and characterising trypanosome strains in Northern Ethiopia.

Cite This Article

APA
Birhanu H, Fikru R, Said M, Kidane W, Gebrehiwot T, Hagos A, Alemu T, Dawit T, Berkvens D, Goddeeris BM, Büscher P. (2015). Epidemiology of Trypanosoma evansi and Trypanosoma vivax in domestic animals from selected districts of Tigray and Afar regions, Northern Ethiopia. Parasit Vectors, 8, 212. https://doi.org/10.1186/s13071-015-0818-1

Publication

ISSN: 1756-3305
NlmUniqueID: 101462774
Country: England
Language: English
Volume: 8
Pages: 212
PII: 212

Researcher Affiliations

Birhanu, Hadush
  • College of Veterinary Medicine, Mekelle University, P. O. Box 2084, Mekelle, Ethiopia. hadushbirhanu@yahoo.com.
  • Department of Biosystems, KU Leuven, Faculty of Bioscience Engineering, Kasteelpark Arenberg 30, B-3001, Leuven, Belgium. hadushbirhanu@yahoo.com.
  • Department of Biomedical Sciences, Institute of Tropical Medicine, Nationalestraat 155, Antwerp, Belgium. hadushbirhanu@yahoo.com.
Fikru, Regassa
  • Department of Biosystems, KU Leuven, Faculty of Bioscience Engineering, Kasteelpark Arenberg 30, B-3001, Leuven, Belgium. fikruregassa@yahoo.com.
  • Department of Biomedical Sciences, Institute of Tropical Medicine, Nationalestraat 155, Antwerp, Belgium. fikruregassa@yahoo.com.
  • College of Veterinary Medicine and Agriculture, Addis Ababa University, P.O. Box 34, Bishoftu, Ethiopia. fikruregassa@yahoo.com.
Said, Mussa
  • Department of Statistics, College of Natural and Computational Sciences, Mekelle University, P.O.Box 231, Mekelle, Ethiopia. mussasaid3226@gmail.com.
Kidane, Weldu
  • College of Veterinary Medicine, Mekelle University, P. O. Box 2084, Mekelle, Ethiopia. kidaneweldu21@yahoo.com.
Gebrehiwot, Tadesse
  • College of Veterinary Medicine, Mekelle University, P. O. Box 2084, Mekelle, Ethiopia. tadessse498@yahoo.com.
Hagos, Ashenafi
  • College of Veterinary Medicine and Agriculture, Addis Ababa University, P.O. Box 34, Bishoftu, Ethiopia. hagos83@yahoo.com.
Alemu, Tola
  • College of Veterinary Medicine and Agriculture, Addis Ababa University, P.O. Box 34, Bishoftu, Ethiopia. alemu.tola@yahoo.com.
Dawit, Tesfaye
  • School of Veterinary Medicine, Hawassa University, P.O. Box 05, Hawassa, Ethiopia. dawit89@yahoo.com.
Berkvens, Dirk
  • Department of Biomedical Sciences, Institute of Tropical Medicine, Nationalestraat 155, Antwerp, Belgium. dberkvens@itg.be.
Goddeeris, Bruno Maria
  • Department of Biosystems, KU Leuven, Faculty of Bioscience Engineering, Kasteelpark Arenberg 30, B-3001, Leuven, Belgium. bruno.goddeeris@kuleuven.be.
Büscher, Philippe
  • Department of Biomedical Sciences, Institute of Tropical Medicine, Nationalestraat 155, Antwerp, Belgium. pbuscher@itg.be.

MeSH Terms

  • Animals
  • Ethiopia / epidemiology
  • Livestock / parasitology
  • Molecular Epidemiology
  • Trypanosoma / classification
  • Trypanosoma / genetics
  • Trypanosomiasis / epidemiology
  • Trypanosomiasis / parasitology
  • Trypanosomiasis / veterinary

References

This article includes 94 references
  1. CSA. Agricultural sample report on livestock and livestock characterstics. Addis Ababa, Ethiopia: 2012:9–22.
  2. MOA. Ethiopia Animal Health Year Book (2009/10). Addis Ababa: Federal Ministry of Agriculture Animal and Plant Health Regulatory Directorate (APHRD). Addis Ababa, Ethiopia: 2010:1–63.
  3. Abebe G. Trypanosomosis in Ethiopia. Ethiop J Biol Sci 2005;4:75–121.
  4. Hoare CA. The Trypanosomes of Mamals. A Zoological Monograph. Oxford, UK: Blackwell Scientific Publications; 1972.
  5. Da Silva AS, Garcia Perez HA, Costa MM, França RT, De Gasperi D, Zanette RA, Amado JA, Lopes ST, Teixeira MM, Monteiro SG. Horses naturally infected by Trypanosoma vivax in southern Brazil.. Parasitol Res 2011 Jan;108(1):23-30.
    doi: 10.1007/s00436-010-2036-2pubmed: 20820805google scholar: lookup
  6. Van den Bossche P. The Development of A New Strategy For The Sustainable Control of Bovine Trypanosomosis In South Africa. Pretoria, South Africa: University of Pretoria; 2000.
  7. Da Silva AS, Pierezan F, Wolkmer P, Costa MM, Oliveiro CB, Tonin AA, Santurio JM, Lopes ST, Monteiro SG. Pathological findings associated with experimental infection by Trypanosoma evansi in cats.. J Comp Pathol 2010 Feb-Apr;142(2-3):170-6.
    doi: 10.1016/j.jcpa.2009.10.020pubmed: 19954795google scholar: lookup
  8. Losos GJ. Infectious Diseases of Tropical Diseases of Domestic Animals. New York: Churchill Livingstone; 1986.
  9. Gutierrez C, Corbera JA, Juste MC, Doreste F, Morales I. An outbreak of abortions and high neonatal mortality associated with Trypanosoma evansi infection in dromedary camels in the Canary Islands.. Vet Parasitol 2005 Jun 10;130(1-2):163-8.
    doi: 10.1016/j.vetpar.2005.02.009pubmed: 15893083google scholar: lookup
  10. Löhr KF, Pholpark S, Siriwan P, Leesirikul N, Srikitjakarn L, Staak C. Trypanosoma evansi infection in buffaloes in North-East Thailand. II. Abortions.. Trop Anim Health Prod 1986 May;18(2):103-8.
    doi: 10.1007/BF02359721pubmed: 3738993google scholar: lookup
  11. Dagnatchew Z. Trypanosomiasis in Ethiopia. Third International Symposium on Veterinary Epidemiology and Economics Arlington, Virginia, USA: Veterinary Medicine Publishing Company; 1982; pp. 467–473.
  12. Abebe G, Yilma J. Trypanosomosis: a threat to cattle production in Ethiopia. Rev Med Vet 1996;147:897–902.
  13. Moloo SK, Gettinby G, Olubayo RO, Kabata JM, Okumu IO. A comparison of African buffalo, N'Dama and Boran cattle as reservoirs of Trypanosoma vivax for different Glossina species.. Parasitology 1993 Apr;106 ( Pt 3):277-82.
    doi: 10.1017/S0031182000075090pubmed: 8098147google scholar: lookup
  14. Osório AL, Madruga CR, Desquesnes M, Soares CO, Ribeiro LR, Costa SC. Trypanosoma (Duttonella) vivax: its biology, epidemiology, pathogenesis, and introduction in the New World--a review.. Mem Inst Oswaldo Cruz 2008 Feb;103(1):1-13.
  15. Mihok S, Maramba O, Munyoki E, Kagoiya J. Mechanical transmission of Trypanosoma spp. by African Stomoxyinae (Diptera: Muscidae).. Trop Med Parasitol 1995 Jun;46(2):103-5.
    pubmed: 8525279
  16. Oluwafemi A, Ilemobade A, Laseined E. The impact of African animal trypanosomosis and tsetse on the livelihood and wellbeing of cattle and their owners in the BICOT study area of Nigeria. Sc Res Essays 2007;2:380–3.
  17. Cortez AP, Ventura RM, Rodrigues AC, Batista JS, Paiva F, Añez N, Machado RZ, Gibson WC, Teixeira MM. The taxonomic and phylogenetic relationships of Trypanosoma vivax from South America and Africa.. Parasitology 2006 Aug;133(Pt 2):159-69.
    doi: 10.1017/S0031182006000254pubmed: 16650339google scholar: lookup
  18. Raina AK, Kumar R, Rajora VS, Sridhar, Singh RP. Oral transmission of Trypanosoma evansi infection in dogs and mice.. Vet Parasitol 1985 Jun;18(1):67-9.
    doi: 10.1016/0304-4017(85)90009-3pubmed: 4049728google scholar: lookup
  19. Sinha PK, Mukherjee GS, Das MS, Lahiri RK. Outbreak of trypanosomiasis evansi amongst tigers and jaguars in the zoological garden, Calcutta.. Indian Vet J 1971 Mar;48(3):306-10.
    pubmed: 5103629
  20. Langridge WP. A tsetse and Trypanosomiasis Survey of Ethiopia. London: Ministry of Overseas Development; 1976.
  21. Desquesnes M, Holzmuller P, Lai DH, Dargantes A, Lun ZR, Jittaplapong S. Trypanosoma evansi and surra: a review and perspectives on origin, history, distribution, taxonomy, morphology, hosts, and pathogenic effects.. Biomed Res Int 2013;2013:194176.
    pmc: PMC3760267pubmed: 24024184doi: 10.1155/2013/194176google scholar: lookup
  22. Desquesnes M, Dargantes A, Lai DH, Lun ZR, Holzmuller P, Jittapalapong S. Trypanosoma evansi and surra: a review and perspectives on transmission, epidemiology and control, impact, and zoonotic aspects.. Biomed Res Int 2013;2013:321237.
    pmc: PMC3789323pubmed: 24151595doi: 10.1155/2013/321237google scholar: lookup
  23. Gutierrez C, Corbera JA, Morales M, Büscher P. Trypanosomosis in goats: current status.. Ann N Y Acad Sci 2006 Oct;1081:300-10.
    doi: 10.1196/annals.1373.040pubmed: 17135529google scholar: lookup
  24. Holland WG, Do TT, Huong NT, Dung NT, Thanh NG, Vercruysse J, Goddeeris BM. The effect of Trypanosoma evansi infection on pig performance and vaccination against classical swine fever.. Vet Parasitol 2003 Feb 13;111(2-3):115-23.
    doi: 10.1016/S0304-4017(02)00363-1pubmed: 12531288google scholar: lookup
  25. Singla LD, Juyal PD, Sharma NS. Immune responses to haemorrhagic septicaemia (HS) vaccination in Trypanosoma evansi infected buffalo-calves.. Trop Anim Health Prod 2010 Apr;42(4):589-95.
    doi: 10.1007/s11250-009-9461-1pubmed: 19784863google scholar: lookup
  26. Holland WG, My LN, Dung TV, Thanh NG, Tam PT, Vercruysse J, Goddeeris BM. The influence of T. evansi infection on the immuno-responsiveness of experimentally infected water buffaloes.. Vet Parasitol 2001 Dec 13;102(3):225-34.
    doi: 10.1016/S0304-4017(01)00534-9pubmed: 11777602google scholar: lookup
  27. Songa EB, Paindavoine P, Wittouck E, Viseshakul N, Muldermans S, Steinert M, Hamers R. Evidence for kinetoplast and nuclear DNA homogeneity in Trypanosoma evansi isolates.. Mol Biochem Parasitol 1990 Dec;43(2):167-79.
    doi: 10.1016/0166-6851(90)90142-9pubmed: 1982554google scholar: lookup
  28. Ou YC, Giroud C, Baltz T. Kinetoplast DNA analysis of four Trypanosoma evansi strains.. Mol Biochem Parasitol 1991 May;46(1):97-102.
    doi: 10.1016/0166-6851(91)90203-Ipubmed: 1677160google scholar: lookup
  29. Lun ZR, Brun R, Gibson W. Kinetoplast DNA and molecular karyotypes of Trypanosoma evansi and Trypanosoma equiperdum from China.. Mol Biochem Parasitol 1992 Feb;50(2):189-96.
    doi: 10.1016/0166-6851(92)90215-6pubmed: 1311051google scholar: lookup
  30. Verloo D, Magnus E, Büscher P. General expression of RoTat 1.2 variable antigen type in Trypanosoma evansi isolates from different origin.. Vet Parasitol 2001 Jun 12;97(3):183-9.
    doi: 10.1016/S0304-4017(01)00412-5pubmed: 11390070google scholar: lookup
  31. Borst P, Fase-Fowler F, Gibson WC. Kinetoplast DNA of Trypanosoma evansi.. Mol Biochem Parasitol 1987 Feb;23(1):31-8.
    doi: 10.1016/0166-6851(87)90184-8pubmed: 3033499google scholar: lookup
  32. Ngaira JM, Olembo NK, Njagi EN, Ngeranwa JJ. The detection of non-RoTat 1.2 Trypanosoma evansi.. Exp Parasitol 2005 May;110(1):30-8.
    doi: 10.1016/j.exppara.2005.01.001pubmed: 15804376google scholar: lookup
  33. Njiru ZK, Constantine CC, Ndung'u JM, Robertson I, Okaye S, Thompson RC, Reid SA. Detection of Trypanosoma evansi in camels using PCR and CATT/T. evansi tests in Kenya.. Vet Parasitol 2004 Oct 5;124(3-4):187-99.
    doi: 10.1016/j.vetpar.2004.06.029pubmed: 15381299google scholar: lookup
  34. Njiru ZK, Constantine CC, Masiga DK, Reid SA, Thompson RC, Gibson WC. Characterization of Trypanosoma evansi type B.. Infect Genet Evol 2006 Jul;6(4):292-300.
    doi: 10.1016/j.meegid.2005.08.002pubmed: 16157514google scholar: lookup
  35. Gibson WC, Wilson AJ, Moloo SK. Characterisation of Trypanosoma (Trypanozoon) evansi from camels in Kenya using isoenzyme electrophoresis.. Res Vet Sci 1983 Jan;34(1):114-8.
    pubmed: 6836172
  36. Bajyana Songa E, Hamers-Casterman C, Hamers R, Pholpark M, Pholpark S, Leidl K, Tangchaitrong S, Chaichanopoonpol I, Vitoorakool C, Thirapatsakum T. The use of the card agglutination test (Testryp CATT) for the detection of T. evansi infection: a comparison with other trypanosomiasis diagnostic tests under field conditions in Thailand.. Ann Soc Belg Med Trop 1987;67(2):137-48.
    pubmed: 3426308
  37. Claes F, Radwanska M, Urakawa T, Majiwa PA, Goddeeris B, Büscher P. Variable Surface Glycoprotein RoTat 1.2 PCR as a specific diagnostic tool for the detection of Trypanosoma evansi infections.. Kinetoplastid Biol Dis 2004 Sep 17;3(1):3.
    doi: 10.1186/1475-9292-3-3pmc: PMC521498pubmed: 15377385google scholar: lookup
  38. Sinshaw A, Abebe G, Desquesnes M, Yoni W. Biting flies and Trypanosoma vivax infection in three highland districts bordering lake Tana, Ethiopia.. Vet Parasitol 2006 Nov 30;142(1-2):35-46.
    doi: 10.1016/j.vetpar.2006.06.032pubmed: 16890359google scholar: lookup
  39. Codjia V, Mulatu W, Majiwa PA, Leak SG, Rowlands GJ, Authié E, d'Ieteren GD, Peregrine AS. Epidemiology of bovine trypanosomiasis in the Ghibe valley, southwest Ethiopia. 3. Occurrence of populations of Trypanosoma congolense resistant to diminazene, isometamidium and homidium.. Acta Trop 1993 Apr;53(2):151-63.
    doi: 10.1016/0001-706X(93)90026-8pubmed: 8098900google scholar: lookup
  40. Rowlands GJ, Mulatu W, Authié E, d'Ieteren GD, Leak SG, Nagda SM, Peregrine AS. Epidemiology of bovine trypanosomiasis in the Ghibe valley, southwest Ethiopia. 2. Factors associated with variations in trypanosome prevalence, incidence of new infections and prevalence of recurrent infections.. Acta Trop 1993 Apr;53(2):135-50.
    doi: 10.1016/0001-706X(93)90025-7pubmed: 8098899google scholar: lookup
  41. Hagos A, Degefa G, Yacob H, Fikru R, Alemu T, Feseha G, Claes F, Goddeeris BM. Seroepidemiological survey of trypanozoon infection in horses in the suspected dourine-infected Bale highlands of the Oromia region, Ethiopia.. Rev Sci Tech 2010 Dec;29(3):649-54.
    pubmed: 21309462doi: 10.20506/rst.29.3.2005google scholar: lookup
  42. Miruk A, Hagos A, Yacob HT, Asnake F, Basu AK. Prevalence of bovine trypanosomosis and trypanocidal drug sensitivity studies on Trypanosoma congolense in Wolyta and Dawero zones of southern Ethiopia.. Vet Parasitol 2008 Mar 25;152(1-2):141-7.
    doi: 10.1016/j.vetpar.2007.12.007pubmed: 18207329google scholar: lookup
  43. Cherenet T, Sani RA, Speybroeck N, Panandam JM, Nadzr S, Van den Bossche P. A comparative longitudinal study of bovine trypanosomiasis in tsetse-free and tsetse-infested zones of the Amhara Region, northwest Ethiopia.. Vet Parasitol 2006 Sep 10;140(3-4):251-8.
    doi: 10.1016/j.vetpar.2006.04.004pubmed: 16675127google scholar: lookup
  44. Fikru R, Goddeeris BM, Delespaux V, Moti Y, Tadesse A, Bekana M, Claes F, De Deken R, Büscher P. Widespread occurrence of Trypanosoma vivax in bovines of tsetse- as well as non-tsetse-infested regions of Ethiopia: a reason for concern?. Vet Parasitol 2012 Dec 21;190(3-4):355-61.
    doi: 10.1016/j.vetpar.2012.07.010pubmed: 22858227google scholar: lookup
  45. Hagos A, Yilkal K, Esayass T, Alemu T, Fikru R, Fesseha G. Parasitological and serological survey on trypanosomosis (surra) in camels in dry and wet areas of Bale Zone, Oromyia Region, Ethiopia. Rev Med Vet 2009;160:569–73.
  46. Aradaib IE, 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 May 20;5:2.
    doi: 10.1186/1475-9292-5-1pmc: PMC1481541pubmed: 16712737google scholar: lookup
  47. Büscher P. Diagnosis of human and animal African trypanosomiasis. In: Black SJ, Seed JR, editors. The African Trypanosomes. Boston: Kluwer Academic Publishers; 2001. pp. 51–63.
  48. Woo PT. The haematocrit centrifuge for the detection of trypanosomes in blood.. Can J Zool 1969 Sep;47(5):921-3.
    doi: 10.1139/z69-150pubmed: 5343381google scholar: lookup
  49. Murray M, Murray PK, McIntyre WI. An improved parasitological technique for the diagnosis of African trypanosomiasis.. Trans R Soc Trop Med Hyg 1977;71(4):325-6.
    doi: 10.1016/0035-9203(77)90110-9pubmed: 563634google scholar: lookup
  50. Lanham SM, Godfrey DG. Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose.. Exp Parasitol 1970 Dec;28(3):521-34.
    doi: 10.1016/0014-4894(70)90120-7pubmed: 4993889google scholar: lookup
  51. Lumsden WH, Kimber CD, Evans DA, Doig SJ. Trypanosoma brucei: Miniature anion-exchange centrifugation technique for detection of low parasitaemias: Adaptation for field use.. Trans R Soc Trop Med Hyg 1979;73(3):312-7.
    doi: 10.1016/0035-9203(79)90092-0pubmed: 473329google scholar: lookup
  52. Zillmann U, Konstantinov SM, Berger MR, Braun R. Improved performance of the anion-exchange centrifugation technique for studies with human infective African trypanosomes.. Acta Trop 1996 Dec 16;62(3):183-7.
    doi: 10.1016/S0001-706X(96)00018-6pubmed: 9025986google scholar: lookup
  53. Büscher P, Mumba Ngoyi D, Kaboré J, Lejon V, Robays J, Jamonneau V, Bebronne N, Van der Veken W, Biéler S. Improved Models of Mini Anion Exchange Centrifugation Technique (mAECT) and Modified Single Centrifugation (MSC) for sleeping sickness diagnosis and staging.. PLoS Negl Trop Dis 2009 Nov 24;3(11):e471.
  54. Konnai S, Mekata H, Mingala CN, Abes NS, Gutierrez CA, Herrera JR, Dargantes AP, Witola WH, Cruz LC, Inoue N, Onuma M, Ohashi K. Development and application of a quantitative real-time PCR for the diagnosis of Surra in water buffaloes.. Infect Genet Evol 2009 Jul;9(4):449-52.
    doi: 10.1016/j.meegid.2009.01.006pubmed: 19460309google scholar: lookup
  55. Desquesnes M, McLaughlin G, Zoungrana A, Dávila AM. Detection and identification of Trypanosoma of African livestock through a single PCR based on internal transcribed spacer 1 of rDNA.. Int J Parasitol 2001 May 1;31(5-6):610-4.
    doi: 10.1016/S0020-7519(01)00161-8pubmed: 11334950google scholar: lookup
  56. Fikru R, Hagos A, Rogé S, Reyna-Bello A, Gonzatti MI, Merga B, Goddeeris BM, Büscher P. A proline racemase based PCR for identification of Trypanosoma vivax in cattle blood.. PLoS One 2014;9(1):e84819.
  57. . Trypanosoma evansi Infection (surra). World Animal Health (OIE) 2012.
  58. Bajyana Songa E, Hamers R. A card agglutination test (CATT) for veterinary use based on an early VAT RoTat 1/2 of Trypanosoma evansi.. Ann Soc Belg Med Trop 1988 Sep;68(3):233-40.
    pubmed: 3223785
  59. Camargo RE, Uzcanga GL, Bubis J. Isolation of two antigens from Trypanosoma evansi that are partially responsible for its cross-reactivity with Trypanosoma vivax.. Vet Parasitol 2004 Aug 13;123(1-2):67-81.
    doi: 10.1016/j.vetpar.2004.01.022pubmed: 15265572google scholar: lookup
  60. Uzcanga GL, Perrone T, Noda JA, Pérez-Pazos J, Medina R, Hoebeke J, Bubis J. Variant surface glycoprotein from Trypanosoma evansi is partially responsible for the cross-reaction between Trypanosoma evansi and Trypanosoma vivax.. Biochemistry 2004 Jan 27;43(3):595-606.
    doi: 10.1021/bi0301946pubmed: 14730963google scholar: lookup
  61. Uzcanga G, Mendoza M, Aso PM, Bubis J. Purification of a 64 kDa antigen from Trypanosoma evansi that exhibits cross-reactivity with Trypanosoma vivax.. Parasitology 2002 Mar;124(Pt 3):287-99.
    doi: 10.1017/S0031182001001214pubmed: 11922430google scholar: lookup
  62. Pillay D, Izotte J, Fikru R, Büscher P, Mucache H, Neves L, Boulangé A, Seck MT, Bouyer J, Napier GB, Chevtzoff C, Coustou V, Baltz T. Trypanosoma vivax GM6 antigen: a candidate antigen for diagnosis of African animal trypanosomosis in cattle.. PLoS One 2013;8(10):e78565.
  63. Tassew W. Economic Analysis and Policy Implications of Farm And Off-Farm Employment: A Case Study In The Tigray Region Of Northern Ethiopia. Wageningen University: Agricultural Economics and Rural Policy Group; 2000.
  64. CSA. Agricultural sample survey. Volume I: Report on area and production of major crops. Addis Ababa, Ethiopia. 2011:1–123.
  65. David HS, Thomas PO. Historical Dictionary of Ethiopia. 2. Maryland, USA: Scarecrow Press; 2013.
  66. Thrusfield M. Veterinary Epidemiology. 3. Edinburgh, UK: Blackwell Publishing; 2007.
  67. Woo PT. Evaluation of the haematocrit centrifuge and other techniques for the field diagnosis of human trypanosomiasis and filariasis.. Acta Trop 1971;28(3):298-303.
    pubmed: 4400769
  68. De Winne K, Büscher P, Luquetti AO, Tavares SB, Oliveira RA, Solari A, Zulantay I, Apt W, Diosque P, Monje Rumi M, Gironès N, Fresno M, Lopez-Velez R, Perez-Molina JA, Monge-Maillo B, Garcia L, Deborggraeve S. The Trypanosoma cruzi satellite DNA OligoC-TesT and Trypanosoma cruzi kinetoplast DNA OligoC-TesT for diagnosis of Chagas disease: a multi-cohort comparative evaluation study.. PLoS Negl Trop Dis 2014;8(1):e2633.
  69. Pyana PP, Ngay Lukusa I, Mumba Ngoyi D, Van Reet N, Kaiser M, Karhemere Bin Shamamba S, Büscher P. Isolation of Trypanosoma brucei gambiense from cured and relapsed sleeping sickness patients and adaptation to laboratory mice.. PLoS Negl Trop Dis 2011 Apr 19;5(4):e1025.
  70. Camara O, Camara M, Lejon V, Ilboudo H, Sakande H, Léno M, Büscher P, Bucheton B, Jamonneau V. Immune trypanolysis test with blood spotted on filter paper for epidemiological surveillance of sleeping sickness.. Trop Med Int Health 2014 Jul;19(7):828-31.
    doi: 10.1111/tmi.12316pubmed: 24750463google scholar: lookup
  71. Herbert WJ, Lumsden WH. Trypanosoma brucei: a rapid "matching" method for estimating the host's parasitemia.. Exp Parasitol 1976 Dec;40(3):427-31.
    doi: 10.1016/0014-4894(76)90110-7pubmed: 976425google scholar: lookup
  72. Aref M, Yasin SM, Bahear W, Ghulam Z, Hastie L, Dennison T, Schauwers W, Büscher P, Deborggraeve S. Canine Trypanosoma evansi infection in Afghanistan.. Vet Parasitol 2013 Nov 8;197(3-4):638-41.
    doi: 10.1016/j.vetpar.2013.07.016pubmed: 23993635google scholar: lookup
  73. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers.. Proc Natl Acad Sci U S A 1989 Aug;86(16):6196-200.
    doi: 10.1073/pnas.86.16.6196pmc: PMC297804pubmed: 2762322google scholar: lookup
  74. StataCorp. Stata: Release 13. Statistical software. College Station. Texas, USA: StataCorp LP; 2013.
  75. Landis JR, Koch GG. The measurement of observer agreement for categorical data.. Biometrics 1977 Mar;33(1):159-74.
    doi: 10.2307/2529310pubmed: 843571google scholar: lookup
  76. Monzón CM, Mancebo OA, Roux JP. Comparison between six parasitological methods for diagnosis of Trypanosoma evansi in the subtropical area of Argentina.. Vet Parasitol 1990 May;36(1-2):141-6.
    doi: 10.1016/0304-4017(90)90102-Hpubmed: 2382382google scholar: lookup
  77. Samson L, Frehiwot M. Prevalence of Small Ruminant Trypanosomosis and Tsetse Fly Challenge In Upper Didessa Valley, Ethiopia. 2010. pp. 215–9.
  78. Tadesse A, Tsegaye B. Bovine trypanosomosis and its vectors in two districts of Bench Maji zone, South Western Ethiopia.. Trop Anim Health Prod 2010 Dec;42(8):1757-62.
    doi: 10.1007/s11250-010-9632-0pubmed: 20577803google scholar: lookup
  79. Kebede N, Fetene T, Animut A. Prevalence of Trypanosomosis of small ruminants in Guangua district of Awi Zone, northwestern Ethiopia.. J Infect Dev Ctries 2009 Apr 30;3(3):245-6.
    doi: 10.3855/jidc.45pubmed: 19759484google scholar: lookup
  80. . Trypanosomosis (tsetse-transmitted). World Animal Health (OIE) 2013.
  81. Salim B, Bakheit MA, Kamau J, Nakamura I, Sugimoto C. Molecular epidemiology of camel trypanosomiasis based on ITS1 rDNA and RoTat 1.2 VSG gene in the Sudan.. Parasit Vectors 2011 Mar 4;4:31.
    doi: 10.1186/1756-3305-4-31pmc: PMC3060148pubmed: 21375725google scholar: lookup
  82. Boid R. Isoenzyme characterisation of 15 stocks of Trypanosoma evansi isolated from camels in the Sudan.. Trop Med Parasitol 1988 Mar;39(1):45-50.
    pubmed: 3291076
  83. Takeet MI, Fagbemi BO, De Donato M, Yakubu A, Rodulfo HE, Peters SO, Wheto M, Imumorin IG. Molecular survey of pathogenic trypanosomes in naturally infected Nigerian cattle.. Res Vet Sci 2013 Jun;94(3):555-61.
    doi: 10.1016/j.rvsc.2012.10.018pubmed: 23245680google scholar: lookup
  84. Gibson W, Pilkington JG, Pemberton JM. Trypanosoma melophagium from the sheep ked Melophagus ovinus on the island of St Kilda.. Parasitology 2010 Oct;137(12):1799-804.
    doi: 10.1017/S0031182010000752pubmed: 20546642google scholar: lookup
  85. Büscher G, Friedhoff KT. The morphology of ovine Trypanosoma melophagium (zoomastigophorea: kinetoplastida).. J Protozool 1984 Feb;31(1):98-101.
  86. Gathuo HK, Nantulya VM, Gardiner PR. Trypanosoma vivax: adaptation of two East African stocks to laboratory rodents.. J Protozool 1987 Feb;34(1):48-53.
  87. D'Archivio S, Medina M, Cosson A, Chamond N, Rotureau B, Minoprio P, Goyard S. Genetic engineering of Trypanosoma (Dutonella) vivax and in vitro differentiation under axenic conditions.. PLoS Negl Trop Dis 2011 Dec;5(12):e1461.
  88. Hilali M, Abdel-Gawad A, Nassar A, Abdel-Wahab A, Magnus E, Büscher P. Evaluation of the card agglutination test (CATT/T. evansi) for detection of Trypanosoma evansi infection in water buffaloes (Bubalus bubalis) in Egypt.. Vet Parasitol 2004 May 7;121(1-2):45-51.
    doi: 10.1016/j.vetpar.2004.02.009pubmed: 15110402google scholar: lookup
  89. Monzon CM, Mancebo OA, Russo AM. Antibody levels by indirect ELISA test in Trypanosoma evansi infected horses following treatment with quinapyramine sulphate.. Vet Parasitol 2003 Jan 20;111(1):59-63.
    doi: 10.1016/S0304-4017(02)00331-Xpubmed: 12523979google scholar: lookup
  90. Büscher P. Diagnosis of African trypanosomiasis. In: Magez S, Radwanska M, editors. Trypanosomes and Trypanosomiasis. Wien: Springer; 2014. pp. 189–216.
  91. Deborggraeve S, Büscher P. Recent progress in molecular diagnosis of sleeping sickness.. Expert Rev Mol Diagn 2012 Sep;12(7):719-30.
    doi: 10.1586/erm.12.72pubmed: 23153239google scholar: lookup
  92. Verloo D, Tibayrenc R, Magnus E, Büscher P, Van Meirvenne N. Performance of serological tests for Trypanosoma evansi infections in camels from Niger. J Protozool Res 1998;8:190–3.
  93. Holland WG, Thanh NG, My LN, Magnus E, Verloo D, Büscher P, Goddeeris B, Vercruysse J. Evaluation of whole fresh blood and dried blood on filter paper discs in serological tests for Trypanosoma evansi in experimentally infected water buffaloes.. Acta Trop 2002 Feb;81(2):159-65.
    doi: 10.1016/S0001-706X(01)00211-Xpubmed: 11801223google scholar: lookup
  94. Van Vlaenderen G. In Search of Cattle Trypanosomiasis in Suriname. Antwerp: Prince Leopold Institute of Tropical Medicine; 1996.

Citations

This article has been cited 32 times.
  1. Behour TS, Abd El Fattah EM. Genotyping of Trypanosoma brucei evansi in Egyptian camels: detection of a different non-RoTat 1.2 Trypanosoma brucei evansi in Egyptian camels. Trop Anim Health Prod 2023 Jul 28;55(4):279.
    doi: 10.1007/s11250-023-03673-6pubmed: 37505344google scholar: lookup
  2. Moh KO, Luka SA, Ndams IS, Lawal IA, Sani D, Obeta SS, Oderinde GP, Dingwoke EJ, Adamude FA, Ubhenin AE, Umar S. Molecular and phylogenetic analysis of a type K1 strain Trypanosoma evansi isolate from Nigerian cattle: An evaluation of the therapeutic effects of compounds from Brassica oleracea on the histopathology of infected wister rats. Biochem Biophys Rep 2023 Mar;33:101424.
    doi: 10.1016/j.bbrep.2023.101424pubmed: 36660764google scholar: lookup
  3. Gebre T, Kapitano B, Beyene D, Alemu D, Beshir A, Worku Z, Kifle T, Selamu A, Debas E, Kalsa A, Asfaw N, Zhao W, Paone M, Cecchi G. The national atlas of tsetse flies and African animal trypanosomosis in Ethiopia. Parasit Vectors 2022 Dec 28;15(1):491.
    doi: 10.1186/s13071-022-05617-9pubmed: 36578020google scholar: lookup
  4. Geerts M, Chen Z, Bebronne N, Savill NJ, Schnaufer A, Büscher P, Van Reet N, Van den Broeck F. Deep kinetoplast genome analyses result in a novel molecular assay for detecting Trypanosoma brucei gambiense-specific minicircles. NAR Genom Bioinform 2022 Dec;4(4):lqac081.
    doi: 10.1093/nargab/lqac081pubmed: 36285287google scholar: lookup
  5. Al-Kharusi A, Elshafie EI, Baqir S, Faraz A, Al-Ansari A, Burger P, Mahgoub O, Al-Kharousi K, Al-Duhli H, Al-Sinani M, Al-Hatali R, Roberts D. Detection of Trypanosoma Infection in Dromedary Camels by Using Different Diagnostic Techniques in Northern Oman. Animals (Basel) 2022 May 25;12(11).
    doi: 10.3390/ani12111348pubmed: 35681813google scholar: lookup
  6. Desquesnes M, Gonzatti M, Sazmand A, Thévenon S, Bossard G, Boulangé A, Gimonneau G, Truc P, Herder S, Ravel S, Sereno D, Jamonneau V, Jittapalapong S, Jacquiet P, Solano P, Berthier D. A review on the diagnosis of animal trypanosomoses. Parasit Vectors 2022 Feb 19;15(1):64.
    doi: 10.1186/s13071-022-05190-1pubmed: 35183235google scholar: lookup
  7. Mersha TT, Mekonnen Wolde B, Shumuye NA, Hailu AB, Mohammed AH, Redda YT, Abera BH, Menghistu HT. Prioritization of neglected tropical zoonotic diseases: A one health perspective from Tigray region, Northern Ethiopia. PLoS One 2021;16(7):e0254071.
    doi: 10.1371/journal.pone.0254071pubmed: 34292951google scholar: lookup
  8. Rafu O, Tulu D, Negera C. Camel Trypanosomosis in Yabelo and Gomole Districts in Ethiopia: Prevalence and Associated Risk Factors Based on Parasitological Examinations. Vet Med (Auckl) 2021;12:87-94.
    doi: 10.2147/VMRR.S288314pubmed: 34007820google scholar: lookup
  9. Aregawi WG, Gutema F, Tesfaye J, Sorsa A, Megersa B, Teshome P, Agga GE, Ashenafi H. Efficacy of diminazene diaceturate and isometamidium chloride hydrochloride for the treatment of Trypanosoma evansi in mice model. J Parasit Dis 2021 Mar;45(1):131-136.
    doi: 10.1007/s12639-020-01289-3pubmed: 33746398google scholar: lookup
  10. Fetene E, Leta S, Regassa F, Büscher P. Global distribution, host range and prevalence of Trypanosoma vivax: a systematic review and meta-analysis. Parasit Vectors 2021 Jan 25;14(1):80.
    doi: 10.1186/s13071-021-04584-xpubmed: 33494807google scholar: lookup
  11. Gerem B, Hamid M, Assefa A. Prevalence and Associated Risk Factors of Trypanosoma evansi in Camels in Ethiopia Based on Parasitological Examinations. Vet Med Int 2020;2020:6172560.
    doi: 10.1155/2020/6172560pubmed: 32908662google scholar: lookup
  12. More S, Bøtner A, Butterworth A, Calistri P, Depner K, Edwards S, Garin-Bastuji B, Good M, Gortázar Schmidt C, Michel V, Miranda MA, Nielsen SS, Raj M, Sihvonen L, Spoolder H, Stegeman JA, Thulke HH, Velarde A, Willeberg P, Winckler C, Baldinelli F, Broglia A, Candiani D, Beltrán Beck B, Kohnle L, Morgado J, Bicout D. Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): Trypanosoma evansi infections (including Surra). EFSA J 2017 Jul;15(7):e04892.
    doi: 10.2903/j.efsa.2017.4892pubmed: 32625557google scholar: lookup
  13. Li Z, Pinto Torres JE, Goossens J, Stijlemans B, Sterckx YG, Magez S. Development of a recombinase polymerase amplification lateral flow assay for the detection of active Trypanosoma evansi infections. PLoS Negl Trop Dis 2020 Feb;14(2):e0008044.
    doi: 10.1371/journal.pntd.0008044pubmed: 32069278google scholar: lookup
  14. Sazmand A, Joachim A, Otranto D. Zoonotic parasites of dromedary camels: so important, so ignored. Parasit Vectors 2019 Dec 27;12(1):610.
    doi: 10.1186/s13071-019-3863-3pubmed: 31881926google scholar: lookup
  15. Boushaki D, Adel A, Dia ML, Büscher P, Madani H, Brihoum BA, Sadaoui H, Bouayed N, Kechemir Issad N. Epidemiological investigations on Trypanosoma evansi infection in dromedary camels in the South of Algeria. Heliyon 2019 Jul;5(7):e02086.
    doi: 10.1016/j.heliyon.2019.e02086pubmed: 31372547google scholar: lookup
  16. Yasine A, Ashenafi H, Geldhof P, Van Brantegem L, Vercauteren G, Bekana M, Tola A, Van Soom A, Duchateau L, Goddeeris B, Govaere J. Histopathological lesions in reproductive organs, distal spinal cord and peripheral nerves of horses naturally infected with Trypanosoma equiperdum. BMC Vet Res 2019 May 28;15(1):175.
    doi: 10.1186/s12917-019-1916-7pubmed: 31138270google scholar: lookup
  17. Büscher P, Gonzatti MI, Hébert L, Inoue N, Pascucci I, Schnaufer A, Suganuma K, Touratier L, Van Reet N. Equine trypanosomosis: enigmas and diagnostic challenges. Parasit Vectors 2019 May 15;12(1):234.
    doi: 10.1186/s13071-019-3484-xpubmed: 31092285google scholar: lookup
  18. Aregawi WG, Agga GE, Abdi RD, Büscher P. Systematic review and meta-analysis on the global distribution, host range, and prevalence of Trypanosoma evansi. Parasit Vectors 2019 Jan 31;12(1):67.
    doi: 10.1186/s13071-019-3311-4pubmed: 30704516google scholar: lookup
  19. Mekonnen G, Mohammed EF, Kidane W, Nesibu A, Yohannes H, Van Reet N, Büscher P, 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 Sep;12(9):e0006790.
    doi: 10.1371/journal.pntd.0006790pubmed: 30208034google scholar: lookup
  20. Degneh E, Shibeshi W, Terefe G, Asres K, Ashenafi H. Bovine trypanosomosis: changes in parasitemia and packed cell volume in dry and wet seasons at Gidami District, Oromia Regional State, western Ethiopia. Acta Vet Scand 2017 Sep 11;59(1):59.
    doi: 10.1186/s13028-017-0327-7pubmed: 28893322google scholar: lookup
  21. Mossaad E, Salim B, Suganuma K, Musinguzi P, Hassan MA, Elamin EA, Mohammed GE, Bakhiet AO, Xuan X, Satti RA, Inoue N. Trypanosoma vivax is the second leading cause of camel trypanosomosis in Sudan after Trypanosoma evansi. Parasit Vectors 2017 Apr 13;10(1):176.
    doi: 10.1186/s13071-017-2117-5pubmed: 28403897google scholar: lookup
  22. Birhanu H, Gebrehiwot T, Goddeeris BM, Büscher P, Van Reet N. New Trypanosoma evansi Type B Isolates from Ethiopian Dromedary Camels. PLoS Negl Trop Dis 2016 Apr;10(4):e0004556.
    doi: 10.1371/journal.pntd.0004556pubmed: 27035661google scholar: lookup
  23. Leta S, Alemayehu G, Seyoum Z, Bezie M. Prevalence of bovine trypanosomosis in Ethiopia: a meta-analysis. Parasit Vectors 2016 Mar 10;9:139.
    doi: 10.1186/s13071-016-1404-xpubmed: 26965590google scholar: lookup
  24. Rodrigues CM, Batista JS, Lima JM, Freitas FJ, Barros IO, Garcia HA, Rodrigues AC, Camargo EP, Teixeira MM. Field and experimental symptomless infections support wandering donkeys as healthy carriers of Trypanosoma vivax in the Brazilian Semiarid, a region of outbreaks of high mortality in cattle and sheep. Parasit Vectors 2015 Oct 28;8:564.
    doi: 10.1186/s13071-015-1169-7pubmed: 26510460google scholar: lookup
  25. Raftery AG, Gummery L, Garcia K, Mohite D, Capewell P, Sutton DGM. Equine trypanosomiasis, a systematic review and meta-analyses: Prevalence, morbidity and mortality. Equine Vet J 2026 Mar;58(2):291-319.
    doi: 10.1111/evj.70101pubmed: 41131780google scholar: lookup
  26. Yudhana A, Illiyin Putri Santosa GA, Wardhana AH, Putra FL, Edila R, Sawitri DH, Praja RN, Kurnianto MA, Rizaldy Tanjung AG, Desquesnes M, Matsubayashi M. Comparative evaluation of three polymerase chain reaction primer sets for accurate molecular detection of Trypanosoma lewisi in wild rodents in Indonesia. Vet World 2025 Aug;18(8):2395-2405.
  27. Firdausy LW, Fikri F, Wicaksono AP, Çalışkan H, Purnama MTE. Prevalence of trypanosomiasis in domesticated animals in Indonesia: A systematic review and meta-analysis. Vet World 2025 May;18(5):1333-1344.
    pubmed: 40584135
  28. Sousa JA, Miranda LM, Coutinho DJB, Costa TF, Costa SP, Freitas ÚS, Costa FB, Machado RZ, Nogueira RMS, Costa APD. Trypanosoma evansi in Brazil: first evidence of infection in equines from Northeast region. Rev Bras Parasitol Vet 2025;34(2):e000125.
    doi: 10.1590/S1984-29612025032pubmed: 40561341google scholar: lookup
  29. Amer MM, Soliman AM, DO T, Hegab AA, El-Kelesh EA, Li Y, Jaroszewski J, Mohanta UK, Xuan X. Parasitological and molecular investigation of Trypanosoma evansi in dromedaries from Greater Cairo, Egypt. J Vet Med Sci 2024 Nov 15;86(11):1177-1184.
    doi: 10.1292/jvms.24-0284pubmed: 39358244google scholar: lookup
  30. Kanchora G, Abebe R. Prevalence of camel trypanosomosis and herders' knowledge, attitude, and practices towards the disease in the pastoral area of southern Ethiopia. BMC Vet Res 2024 Sep 7;20(1):400.
    doi: 10.1186/s12917-024-04250-1pubmed: 39244570google scholar: lookup
  31. Mulat G, Maru M, Tarekegn ZS, Dejene H. A systematic review and meta-analysis on prevalence of bovine trypanosomosis in East Africa. Parasite Epidemiol Control 2024 Aug;26:e00371.
    doi: 10.1016/j.parepi.2024.e00371pubmed: 39184304google scholar: lookup
  32. Chalchisa A, Kumsa B, Gutema Wegi F. Biting Flies and Associated Pathogens in Camels in Amibara District of Afar Region, Ethiopia. Vet Med Int 2024;2024:5407898.
    doi: 10.1155/2024/5407898pubmed: 38234317google scholar: lookup