Molecular Diagnosis of Subclinical African Trypanosoma vivax Infection and Association with Physiological Indices and Serum Metabolites in Extensively Managed Goats in the Tropics

Timothy M. Sanni, Gbolabo O. Onasanya, Mufliat A. Adefenwa, Abdulmojeed Yakubu, Christian O. N. Ikeobi, Olufunmilayo A. Adebambo, Adewale O. Talabi, Michael O. Ozoje, Mathew Wheto, Michael I. Takeet, Sunday O. Peters, Marcos De Donato, Bolaji N. Thomas, Ikhide G. Imumorin

.
Department of Animal Science, Cornell University, Ithaca, USA.

DOI: 10.4236/ojvm.2013.31007                

Abstract

Trypanosomosis remains a major challenge to livestock production in much of tropical Sub-Saharan Africa, while diagnosis and treatment still depend on inefficient parasitological techniques. Endemic infections depend on animal reservoirs with subclinical parasitemia. We report molecular diagnosis of subclinical Trypanosoma vivax (T. vivax) infection using polymerase chain reaction (PCR) for the first time in Nigerian goats and associate parasite presence with gross physiological traits and serum metabolites in extensively managed Nigerian goats. PCR was used to amplify a 400 bp DNA fragment of the parasite genome in 205 goats across three geographical zones of the country. Results showed a high subclinical infection rate (SCIR) of 71.7% in the total goats examined. Overall SCIRs of 71%, 75.9% and 55.6% were recorded in West African Dwarf, Red Sokoto and Sahel goats respectively, while geographical SCIRs were 71.2% (Southwest), 75% (Northwest) and 70% (Northeast). T. vivax presence had significant (P < 0.05) effect on respiratory rate and is associated with higher creatinine levels in sera. Logistic regression analyses with Hosmer-Lemeshow goodness-of-fit showed that respiratory rate is the most important predictive trait for the presence of T. vivax infection (P < 0.05). Goats appear to be a viable reservoir for T. vivax infection of other livestock. Molecular diagnosis of subclinical trypanosomosis using PCR could be useful for large scale epidemiological studies, early diagnosis of subclinical infection and treatment of the disease in extensively managed tropical goats.

Keywords

Molecular Diagnosis; Trypanosoma vivax; Serum Metabolites; Physiological Indices; Nigeria; Goats

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	A. Mugisha, A. Mcleod, R. Percy and E. Kyewalabye, “Socio-Economic Factors Influencing Control of Vector- Borne Diseases in the Pastoralist System of South Western Uganda,” Tropical Animal Health and Production, Vol. 40, No. 1, 2008, pp. 287-297. doi:10.1007/s11250-011-9943-9
[2]	T. T. Desta, W. Ayalew and P. B. Hedge, “Farmers’ Perceptions on Trypanosomosis and Trypanotolerance Character of the Taurine Sheko,” Tropical Animal Health and Production, Vol. 44, No. 3, 2012, pp. 609-616. doi:10.1007/s11250-011-9943-9
[3]	D. Tesfaye, N. Speybroeck, R. De Deken and E. Thys, “Economic Burden of Bovine Trypanosomosis in Three Villages of Metekel Zone, Northwest Ethiopia,” Tropical Animal Health and Production, Vol. 44, No. 4, 2011, pp. 873-879. doi:10.1007/s11250-011-9981-3
[4]	P. R. Torgerson and C. N. L. Macpherson, “The Socioeconomic Burden of Parasitic Zoonoses: Global Trends,” Veterinary Parasitology, Vol. 182, No. 1, 2011, pp. 79-95. doi:10.1016/j.vetpar.2011.07.017
[5]	P. Van den Bossche and R. De Deken, “Seasonal Variations in the Distribution and Abundance of the Tsetse Fly, Glossina morsitans in Eastern Zambia,” Medical and Veterinary Entomology, Vol. 16, No. 1, 2002, pp. 170-176. doi:10.1046/j.1365-2915.2002.00360.x
[6]	P. J. Hotez and A. Kamath, “Neglected Tropical Diseases in Sub-Saharan Africa: Review of their Prevalence, Distribution and Disease Burden,” PLoS Neglected Tropical Diseases, Vol. 3, No. 8, 2009, p. e412. doi:10.1371/journal.pntd.0000412
[7]	M. C. Ezeani, H. Okoro, V. O. Anosa, C. C. Onyenekwe, S. C. Meludu, C. E. Dioka and C. C. Azikiwe, “Immunodiagnosis of Bovine Trypanosomosis in Anambra and Imo States, Nigeria, Using Enzymes Linked Immunosorbent Assay: Zoonotic Implication to Human Health,” Journal of Vector Borne Diseases, Vol. 45, No. 1, 2008, pp. 292-300.
[8]	I. Malele, L. Craske, C. Knight, V. Ferris, Z. K. Njiru, P. Hamilton, L. Stella, M. Lehane and W. C. Gibson, “The Use of Specific and Generic Primers to Identify Trypanosome Infections of Wild Tsetse Flies in Tanzania by PCR,” Infection Genetics and Evolution, Vol. 3, No. 1, 2003, pp. 271-279. doi:10.1016/S1567-1348(03)00090-X
[9]	G. Z. Lin, F. Y. Zheng, J. Z. Zhou, X. W. Gong, G. H. Wang, X. H. Cao and C. Q. Qiu, “Loop-Mediated Isothermal Amplification Assay Targeting the OMP25 Gene for Rapid Detection of Brucella Spp,” Molecular and Cellular Probes, Vol. 23, No. 1, 2011, pp. 126-129. doi:10.1016/j.mcp.2011.01.001
[10]	S. M. Thumbi, F. A. McOdimba, R. O. Mosi and J. O. Junga, “Comparative Evaluation of Three PCR Base Diagnostic Assays for the Detection of Pathogenic Trypanosomes in Cattle Blood,” Parasites and Vectors, Vol. 1, No. 1, 2008, p. 46. doi:10.1186/1756-3305-1-46
[11]	Z. K. Njiru, C. C. Constantine, S. Guya, J. Crowther, J. M. Kiragu, R. C. Thompson and A. M. Dávila, “The Use of ITS1 rDNA PCR in Detecting Pathogenic African Trypanosomes,” Parasitology Research, Vol. 95, No. 2005, pp. 186-192.
[12]	D. K. Masiga, A. J. Smyth, P. Hayes, T. J. Bromidge and W. C. Gibson, “Sensitive Detection of Trypanosomes in Tsetse Flies by DNA Amplification,” International Journal for Parasitology, Vol. 22, No. 1, 1992, pp. 909-918. doi:10.1016/0020-7519(92)90047-O
[13]	R. A. Masake, P. A. Majiwa, S. K. Moloo, J. M. Makau, J. T. Njuguna, M. Maina, J. Kabata, O. K. ole-MoiYoi and V. M. Nantulya, “Sensitive and Specific Detection of Trypanosoma vivax Using the Polymerase Chain Reaction,” Experimental Parasitology, Vol. 85, No. 2, 1997, pp. 193-205. doi:10.1006/expr.1996.4124
[14]	Z. K. Njiru, J. O. Ouma, R. Bateta, S. E. Njeru, K. Ndungu, P. K. Gitonga, S. Guya and R. Traub, “Loop-Mediated Isothermal Amplification Test for Trypanosoma vivax Based on Satellite Repeat DNA,” Veterinary Parasitology, Vol. 180, No. 1, 2011, pp. 358-362. doi:10.1016/j.vetpar.2011.03.021
[15]	B. S. Oladimeji, O. A. Osinowo, J. P. Alawa and J. O. Hambolu, “Estimation of Average Values for Pulse Rate, Respiratory Rate and Rectal Temperature and Development of Heat Stress Index for Adult Yankassa Sheep,” Bulletin of Animal Health and Production, Vol. 44, No. 1, 1996, pp. 105-107.
[16]	N. C. Jain, “Schalman’s Veterinary Haematology,” 4th Edition, Lea and Babings, Philadelphia, 1986, pp. 208- 224.
[17]	“SAS Users Guide: Statistics Ver. 9.1,” Statistical Analysis System Inc., Cary, 2009.
[18]	D. W. Hosmer and S. Lemeshow, “Applied Survival Analysis: Regression Modeling of Time to Event Data,” 2nd Edition, John Wiley and Sons Inc., New York, 2008.
[19]	S. Mekuria and F. Gadissa, “Survey on Bovine Trypanosomosis and Its Vector in Metekel and Awi Zones of Northwest Ethiopia,” Acta Tropica, Vol. 117, No. 1, 2011, pp. 146-151. doi:10.1016/j.actatropica.2010.11.009
[20]	A. Cox, A. Tilley, F. McOdimba, J. Fyfe, M. Eisler, G. Hide and S. Welburn, “A PCR Based Assay for Detection and Differentiation of African Trypanosome Species in Blood,” Experimental Parasitology, Vol. 111, No. 1, 2005, pp. 24-29. doi:10.1016/j.exppara.2005.03.014
[21]	J. L. Gonzales, A. Loza and E. Chacon, “Sensitivity of Different Trypanosoma vivax Specific Primers for the Diagnosis of Livestock Trypanosomosis Using Different DNA Extraction Methods,” Veterinary Parasitology, Vol. 136, No. 1, 2006, pp. 119-126. doi:10.1016/j.vetpar.2005.10.024
[22]	F. J. Li, B. Robin, R. B. Gasser, D. H. Lai, F. Claes, X. Q. Zhu and Z. R. Lun, “PCR Approach for the Detection of Trypanosoma brucei and T. equiperdum and Their Differentiation from T. evansi Based on Maxicircle Kinetoplast DNA,” Molecular Cellular Probe, Vol. 21, No. 1, 2007, pp. 1-7. doi:10.1016/j.mcp.2006.03.009
[23]	G. J. N. Galiza, H. A. Garcia, A. C. O. Assis, D. M. Oliveira, L. A. Pimentel, A. F. M. Dantas, S. V. D. Simoes, M. M. G. Teixeira and F. Riet-Correa, “High Mortality and Lesions of the Central Nervous System in Trypanosomosis by Trypanosoma vivax in Brazilian Hair Sheep,” Veterinary Parasitology, Vol. 182, No. 1, 2011, pp. 359-363. doi:10.1016/j.vetpar.2011.05.016
[24]	M. T. Tejedor-Junco, M. Gonzalez, N. F. Rodriguez, J. A. Corbera and C. Gutierrez, “Comparison Between Micro- Hematocrit Centrifugation Technique and Polymerase Chain Reaction (PCR) to Detect Trypanosoma evansi in Experimentally Inoculated Goats,” Small Ruminant Research, Vol. 96, No. 2011, 2011, pp. 70-72.
[25]	C. C. Ohaeri, “Prevalence of Trypanosomiasis in Ruminants in Parts of Abia State, Nigeria,” Journal of Animal and Veterinary Advances, Vol. 9, No. 18, 2010, pp. 2422- 2426.
[26]	H. Dinka and G. Abebe, “Small Ruminants Trypanosomosis in the Southwest of Ethiopia,” Small Ruminant Research, Vol. 57, No. 1, 2005, pp. 239-243. doi:10.1016/j.smallrumres.2004.07.008
[27]	D. K. Masiga, G. Okech, P. Irungu, J. Ouma, S. Wekesa, B. Ouma, S. O. Guya and J. M. Ndung’u, “Growth and Mortality in Sheep and Goats under High Tsetse Challenge in Kenya,” Tropical Animal Health and Production, Vol. 34, No. 1, 2002, pp. 489-501. doi:10.1023/A:1021241220575
[28]	J. O. Daramola and A. A. Adeloye, “Physiological Adaptation to the Humid Tropics with Special Reference to the West African Dwarf (WAD) Goat,” Tropical Animal Health and Production, Vol. 41, No. 1, 2009, pp. 1005- 1016. doi:10.1007/s11250-008-9267-6
[29]	G. K. Dayo, Z. Bengaly, S. Messad, B. Bucheton, I. Sidibe, B. Cene, G. Cuny and S. Thevenon, “Prevalence and Incidence of Bovine Trypanosomosis in an AgroPastoral Area of Southwestern Burkina Faso,” Research in Veterinary Science, Vol. 88, No. 1, 2010, pp. 470-477. doi:10.1016/j.rvsc.2009.10.010
[30]	S. J. Migchelsen, P. Buscher, A. I. M. Hoepelman, H. D. F. H. Schallig and E. R. Adams, “Human African Trypanosomiasis: A Review of Non-Endemic Cases in the Past 20 Years,” International Journal of Infectious Diseases, Vol. 15, No. 8, 2011, pp. 517-524. doi:10.1016/j.ijid.2011.03.018
[31]	G. L. Pinchbeck, L. J. Morrison, A. Tait, J. Langford, L. Meehan, S. Jallow, A. Jallow and R. M. Christley, “Trypanosomosis in the Gambia: Prevalence in Working Horses and Donkeys Detected by Whole Genome Amplification and PCR, and Evidence for Interactions between Trypanosome Species,” BMC Veterinary Research, Vol. 4, 2008, p. 7.
[32]	I. F. M. Marai, A. A. El-Darawany, A. Fadiel and M. A. M. Abdel-Hafez, “Physiological Traits as Affected by Heat Stress in Sheep—A Review,” Small Ruminant Research, Vol. 71, No. 1, 2007, pp. 1-12. doi:10.1016/j.smallrumres.2006.10.003
[33]	E. H. von Borell, “The Biology of Stress and Its Application to Livestock Housing and Transportation Assessment,” Journal of Animal Science, Vol. 79, No. 2001, 2001, pp. 260-267.
[34]	S. Sadeghian, M. R. M. Dezfouli, G. A. Kojouri, T. T. Bazargani and A. Tavasoli, “Pasteurella multocida Pneumonic Infection in Goat: Hematological, Biochemical, Clinical and Pathological Studies,” Small Ruminant Research, Vol. 100, No. 1, 2011, pp. 189-194. doi:10.1016/j.smallrumres.2011.07.006
[35]	A. O. Fajinmi, J. N. Abenga, F. A. G. Lawani, J. C. A. Ukah, E. C. D. Ikemereh and P. U. Nwabuko, “An Outbreak and Observations on Trypanosomiasis in Friesian Cattle at Sabon-Birni, Kaduna State of Nigeria,” African Journal of Clinical and Experimental Microbiology, Vol. 7, No. 1, 2006, pp. 28-34.
[36]	C. C. Ohaeri and M. C. Eluwa, “Abnormal Biochemical and Haematological Indices in Trypanosomiasis as a Threat to Herd Production,” Veterinary Parasitology, Vol. 177, No. 1, 2011, pp. 199-202. doi:10.1016/j.vetpar.2011.02.002
[37]	M. W. Verstegen, D., Zwart, W. van der, B. O. Hel Brouwer and T, Wensing, “Effect of Trypanosoma vivax Infection on Energy and Nitrogen Metabolism of West African Dwarf Goats,” Journal of Animal Science, Vol. 69, No. 4, 1991, pp. 1667-1677.
[38]	A. O. Ogunsanmi, S. O. Akpavie and V. O. Anosa, “Serum Biochemical Changes in West African Dwarf Sheep Experimentally Infected With Trypanosoma brucei,” Revue D’élevage et de Médecine Vétérinaire des Pays Tropicaux, Vol. 47, No. 2, 1994, pp. 195-200.
[39]	I. O. Igbokwe and A. Mohammed, “Some Plasma Biochemical Changes in Experimental Trypanosoma brucei Infection of Sokoto Red Goats,” Revue D’élevage et de Médecine Vétérinaire des Pays Tropicaux, Vol. 45, No. 3-4, 1992, pp. 287-90.
[40]	S. Osaer, O. O. Akinbamijo and B. Goossens, “Some Biochemical Changes Following Trypanosoma congolense Infection in Djallonké Ewe Lambs and Breeding Ewes Fed on Two Levels of Nutrition,” Acta Tropica, Vol. 75, No. 2, 2000, pp. 229-241. doi:10.1016/S0001-706X(00)00060-7
[41]	J. W. West, “Nutritional Strategies for Managing the Heat Stress in Dairy Cow,” Animal Science Journal, Vol. 77, No. 1, 1999, pp. 21-35.
[42]	I. S. Butswat, S. T. Mbap and G. A. Ayibantoye, “Heat Tolerance of Sheep in Bauchi Nigeria,” Tropical Agriculture (Trinidad), Vol. 77, No. 1, 2000, pp. 265-268.