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Trypanosomosis prevalence in natural field-based infection: insights into systematic review and meta-analysis of studies from 1980 to 2018 on The Gambian ruminants with special emphasis on cattle

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Abstract

Consistent quantification of trypanosomes, the parasite responsible for African animal trypanosomosis, is important for effective surveillance, control, and eradication strategies. Here, we used a rigorously predefined protocol to search and select eligible publications that utilized either microscopy, serology, or molecular methods to investigate prevalence of trypanosomosis based on the presence of any of three most common Trypanosoma spp. (T. congolense, T. vivax, and T. brucei) in the field-based naturally grazed Gambian cattle, sheep, and goats. To combine results of studies on cattle through meta-analysis, sensitivity and subgroup analyses were carried out with the random effects model, and prevalence estimates of each study with 95% confidence intervals (CI) were presented with a forest plot. All the eligible studies utilized the buffy coat technique (BCT) to detect trypanosomes in the blood samples, while the more sensitive serological and molecular detection methods are yet to be widely exploited. Heterogeneity among the studies on cattle was moderate (I2 = 55%), and the pooled trypanosomosis prevalence based on the BCT was 5.2% (95% CI: 4.0–6.4). Meanwhile, estimated prevalence varied according to the trypanosome detection methods, study locations, types of publication, year, and length of observations. We could not pool the trypanosomosis prevalence in sheep and goats through meta-analysis due to small number of studies. The prevalence estimates based on the BCT ranged from 3.2 to 8.1% in goats and 2.8 to 10.6% in sheep. Even though there seems to be a slight decrease in trypanosomosis prevalence in cattle in one of the Gambian districts, there was no consistent trend across the years. It is thought that the literature search and formatting procedures presented in this study contribute to doing systematic reviews on the investigated subject and can be adapted for similar cases.

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References

  • Agyemang, K., Dwinger, R.H., Touray, B.N., Jeannin, P., Fofana, D., Grieve, A.S., 1990a. Effects of nutrition on degree of anaemia and liveweight changes in N’Dama cattle infected with trypanosomes. Livestock Production Science 26, 39–51

    Article  Google Scholar 

  • Agyemang, K., Dwinger, R.H., Jeannin, P., Leperre, P., Grieve, A.S., Bah, M.L., Little, D.A., 1990b. Biological and economic impact of trypanosome infections on milk production in N’Dama cattle managed under village conditions in The Gambia. Animal Production 50, 383–389

    Google Scholar 

  • Agyemang, K., Dwinger, R.H., Little, D.A., Leperre, P., Grieve, A.S., 1991. Interaction between physiological status in N’Dama cows and trypanosome infections and its effect on health and productivity of cattle in Gambia. Acta Tropica 50, 91–99

    Article  CAS  Google Scholar 

  • Agyemang, K., Dwinger, R.H., Little, D.A., Rowlands, G.J., 1997. Village N’Dama cattle production in West Africa: Six years of research in The Gambia, (International Livestock Research Institute (Kenya) and International Trypanotolerance Centre (The Gambia)

  • Agyemang, K., Little, D.A., Mattioli, R., Sonko, E., Janneh, L., 1993. Effects of trypanosome inferction and postpartum liveweight change on resumption of reproduction activity in N’Dama cows. Theriogenology 39, 985–95

    Article  CAS  Google Scholar 

  • Barendregt, J.J., Doi, S.A., Lee, Y.Y., Norman, R.E., Vos, T., 2013. Meta-analysis of prevalence. Journal of Epidemiology and Community Health 67, 974–978

    Article  Google Scholar 

  • Bargul, J.L., Jung, J., McOdimba, F.A., Omogo, C.O., Adung’a, V.O., Krüger, T., Masiga, D.K., Engstler, M., 2016. Species-Specific adaptations of trypanosome morphology and motility to the mammalian host. PLOS Pathogens 12, e1005448

    Article  Google Scholar 

  • Batista, J.S., Freitas, C.I.A., da Silva, J.B., Cavalcante, T.V., de Paiva, K.A.R., Lopes, F.C., Lira, R., 2017. Clinical evaluation and reproductive indices of dairy cows naturally infected with Trypanosoma vivax. Semina: Ciências Agrárias, 38, 3031–3038

    Google Scholar 

  • Desquesnes, M., 2016. Compendium of standard diagnostic protocols for animal trypanosomoses of African origin (OIE Reference Laboratory for Animal Trypanosomoses of African origin)

  • Diall, O., Cecchi, G., Wanda, G., Argilés-Herrero, R., Vreysen, M. J. B., Cattoli, G., Viljoen, G.J., Mattioli, R., Bouyer, J., 2017. Developing a Progressive Control Pathway for African Animal Trypanosomosis. Trends in Parasitology 33, 499–509

    Article  Google Scholar 

  • Duffy, C.W., Morrison, L.J., Black, A., Pinchbeck, G.L., Christley, R.M., Schoenefeld, A., Tait, A., Turner, C.M.R., MacLeod, A., 2009. Trypanosoma vivax displays a clonal population structure. International Journal for Parasitology 39, 1475–1483

    Article  CAS  Google Scholar 

  • Duval, S., Tweedie, R., 2000. A nonparametric “Trim and Fill” method of accounting for publication bias in meta-analysis. Journal of the American Statistical Association 95, 89-98

    Google Scholar 

  • Dwinger, R.H., Agyemang, K., Jeannin, P., Grieve, A.S., 1987. Research project on the productivity of N’Dama cattle in Senegambia (Second Annual Report, International Trypanotolerance Centre) [Cited from Agyemang et al., 1990a]

  • Dwinger, R.H, Agyemang, K., Kaufmann, J., Grieve, A.S., Bah, M.L., 1994a. Effects of trypanosome and helminth infections on health and production parameters of village N’Dama cattle in The Gambia. Veterinary Parasitology 54, 353–65

    Article  CAS  Google Scholar 

  • Dwinger, R.H., Agyemang, K., Snow, W.F., Rawlings, P., Leperre, P., Bah, M.L., 1994b. Productivity of trypanotolerant cattle kept under traditional management conditions in the Gambia. Veterinary Quarterly 16, 81–86

    Article  CAS  Google Scholar 

  • Gall, Y., Woitag, T., Bauer, B., Sidibe, I., McDermott, J., Mehlitz, D., Clausen, P-H., 2004. Trypanocidal failure suggested by PCR results in cattle field samples. Acta Tropica 92, 7–16

    Article  CAS  Google Scholar 

  • Giordani, F., Morrison, L.J., Rowan, T.G., De Koning, H.P., Barrett, M.P., 2016. The animal trypanosomiases and their chemotherapy: a review. Parasitology 143, 1862–1889

    Article  Google Scholar 

  • Higgins, J.P.T., Thompson, S.G., 2002. Quantifying heterogeneity in a meta-analysis. Statistics in Medicine 21, 1539–1558

    Article  Google Scholar 

  • Huedo-Medina, T.B., Sánchez-Meca, J., Marín-Martínez, F., Botella, J., 2006. Assessing heterogeneity in meta-analysis: Q statistic or I2 index? Psychological Methods 11, 193–206

    Article  Google Scholar 

  • Israel, H., Richter, R.R., 2011. A guide to understanding meta-analysis. Journal of Orthopaedic & Sports Physical Therapy 41, 496–504

    Article  Google Scholar 

  • ITC, 2011. Assessment of climatic factors on Glossina species distribution, challenge and trypanosome infection in endemic cattle breeds at two PROGEBE sites (Niamina East and Kiang West districts) in The Gambia (Project report, International Trypanotolerance Centre)

  • ITC, 2013. Annual Report of 2013 and Outlook for 2014 (Unpublished report, International Trypanotolerance Centre)

  • ITC, 2014. Annual Report of 2014 and Outlook for 2015 (Unpublished report, International Trypanotolerance Centre)

  • ITC, 2015. Annual Report of 2015 and Outlook for 2016 (Unpublished report, International Trypanotolerance Centre)

  • ITC, 2016. Annual Report of 2016 and Outlook for 2017 (Unpublished report, International Trypanotolerance Centre)

  • ITC, 2017. Annual Report of 2017 and Outlook for 2018 (Unpublished report, International Trypanotolerance Centre)

  • Leperre, P., Dwinger, R.H., Rawlings, P., Janneh, L., Zurcher, G., Faye, J., Maxwell, J., 1992. Etude des paramètres zootechniques de la race Ndama en milieu traditionnel villageois en Gambie. Revue d’élevage et de Médecine Vétérinaire Des Pays Tropicaux 45, 55–62

    Article  Google Scholar 

  • Liberati, A., Altman, D.G., Tetzlaff, J., Mulrow, C., Gøtzsche, P.C., Ioannidis, J.P.A., Clarke, M., Devereaux, P.J., Kleijnen, J., Moher, D., 2009. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339, b2700

    Article  Google Scholar 

  • Majekodunmi, A.O., Fajinmi, A., Dongkum, C., Picozzi, K., Thrusfield, M. V, Welburn, S.C., 2013. A longitudinal survey of African animal trypanosomiasis in domestic cattle on the Jos Plateau, Nigeria: prevalence, distribution and risk factors. Parasites & Vectors 6, 239

    Article  Google Scholar 

  • Mattioli, R.C., Faye, J.A., Jaitner, J., 2001. Estimation of trypanosomal status by the buffy coat technique and an antibody ELISA for assessment of the impact of trypanosomosis on health and productivity of N’Dama cattle in The Gambia. Veterinary Parasitology 95, 25–35

    Article  CAS  Google Scholar 

  • MoA, 2016. National Livestock Census. Ministry of Agriculture. Banjul. pp. 1-32

    Google Scholar 

  • Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., The PRISMA Group, 2009. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Medicine 6, e1000097

    Article  Google Scholar 

  • Morrison, L.J., Vezza, L., Rowan, T., Hope, J.C., 2016. Animal African Trypanosomiasis: Time to Increase Focus on Clinically Relevant Parasite and Host Species. Trends in Parasitology 32, 599–607

    Article  Google Scholar 

  • Murray, M., Murray, P.K., McIntyre, W.I.M., 1977. An improved parasitological technique for the diagnosis of African trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 325–326

    Article  CAS  Google Scholar 

  • Neyeloff, J.L., Fuchs, S.C., Moreira, L.B., 2012. Meta-analyses and Forest plots using a microsoft excel spreadsheet: step-by-step guide focusing on descriptive data analysis. BMC Research Notes 5, 52

    Article  Google Scholar 

  • Odeniran, P.O., Ademola, I.O., 2018. A meta-analysis of the prevalence of African animal trypanosomiasis in Nigeria from 1960 to 2017. Parasites & Vectors 11, 280

    Article  Google Scholar 

  • OIE, 2013. Trypanosomosis (tsetse transmitted): Aetiology, epidemiology, diagnosis, prevention and control (Technical Disease Cards, World Organization for Animal Health)

  • Olaniyan, O.F., 2015. Sustaining N’Dama cattle for the resource-poor farmers in The Gambia. Bulletin of Animal Production and Health in Africa 63, 83–92

    Google Scholar 

  • Olaniyan, O.F., Orunmuyi, M., 2017. Promoting Farmers’ Resilience to Climate Change: An Option of the N’Dama Cattle in West Africa, In: W. Leal Filho, S. Belay, J. Kalangu, W. Menas, P. Munishi, and K. Musiyiwa (eds), Climate Change Adaptation in Africa: Fostering Resilience and Capacity to Adapt, Springer International Publishing, New York City 345–356

    Chapter  Google Scholar 

  • Osaer, S., Goossens, B., Kora, S., Gaye, M., Darboe, L., 1999. Health and productivity of traditionally managed Djallonke sheep and West African dwarf goats under high and moderate trypanosomosis risk. Veterinary Parasitology 82, 101–119

    Article  CAS  Google Scholar 

  • Paris, J., Murray, M., McOdimba, F., 1982. A comparative evaluation of the parasitological techniques currently available for the diagnosis of African trypanosomiasis in cattle. Acta Tropica 39, 307–316

    CAS  PubMed  Google Scholar 

  • Pereira de Almeida, P.J.L., Ndao, M., Goossens, B., Osaer, S., 1998. PCR primer evaluation for the detection of trypanosome DNA in naturally infected goats. Veterinary Parasitology 80, 111–116

    Article  CAS  Google Scholar 

  • Rayaisse, J.B., Tirados, I., Kaba, D., Dewhirst, S.Y., Logan, J.G., Diarrassouba, A., Salou, E., Omolo, M.O., Solano, P., Lehane, M.J., Pickett, J.A., Vale, G.A., Torr, S.J., Esterhuizen, J., 2010. Prospects for the Development of Odour Baits to Control the Tsetse Flies Glossina tachinoides and G. palpalis s.l. PLoS Neglected Tropical Diseases 4, e632

    Article  CAS  Google Scholar 

  • Simukoko, H., Marcotty, T., Phiri, I., Geysen, D., Vercruysse, J., Van den Bossche, P., 2007. The comparative role of cattle, goats and pigs in the epidemiology of livestock trypanosomiasis on the plateau of eastern Zambia. Veterinary Parasitology 147, 231–238

    Article  CAS  Google Scholar 

  • Snow, W.F., Wacher, T.J., Rawlings, P., 1996. Observations on the prevalence of trypanosomosis in small ruminants, equines and cattle in relation to tsetse challenge in The Gambia. Veterinary Parasitology 66, 1–11

    Article  CAS  Google Scholar 

  • Todd, J.L., Wolbach, S.B., 1912. Parasitic Protozoa from the Gambia : Second Report of the Expedition of the Liverpool School of Tropical Medicine to the Gambia, 1911. The Journal of Medical Research 26, 195–218 + Plates X, XI and XII

    CAS  PubMed  PubMed Central  Google Scholar 

  • Toews, L.C., 2017. Compliance of systematic reviews in veterinary journals with Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) literature search reporting guidelines. Journal of the Medical Library Association 105, 233–239

    Article  Google Scholar 

  • Torr, S.J., Prior, A., Wilson, P.J., Schofield, S., 2007. Is there safety in numbers? The effect of cattle herding on biting risk from tsetse flies. Medical and Veterinary Entomology 21, 301–311

    Article  CAS  Google Scholar 

  • Wacher, T.J., Rawlings, P., Snow, W.F., 1993. Cattle migration and stocking densities in relation to tsetse-trypanosomiasis challenge in The Gambia. Annals of Tropical Medicine & Parasitology 87, 517–524

    Article  CAS  Google Scholar 

  • Yorke, W., Blacklock, B., 1911. The Trypanosomes Found in Two Horses Naturally Infected in the Gambia. Annals of Tropical Medicine & Parasitology 5, 413–434

    Article  Google Scholar 

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Acknowledgments

The authors wish to thank the Directorate of Library and Documentation of the Ege University for access to bibliography databases and also the staff of ITC/WALIC for the AAT monitoring survey information.

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Olawale Festus Olaniyan designed the research, extracted and analyzed the data, and drafted the manuscript. Ibrahim Kaya was involved in verification of the analyzed data, results, and texts. Arss Secka was involved in identification of gray literature. All authors contributed to the manuscript, read and approve the final version.

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Correspondence to Olawale Festus Olaniyan.

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Olaniyan, O.F., Kaya, I. & Secka, A. Trypanosomosis prevalence in natural field-based infection: insights into systematic review and meta-analysis of studies from 1980 to 2018 on The Gambian ruminants with special emphasis on cattle. Trop Anim Health Prod 53, 25 (2021). https://doi.org/10.1007/s11250-020-02461-w

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