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Seasonal variation in tsetse fly apparent density and Trypanosoma spp. infection rate and occurrence of drug-resistant trypanosomes in Lambwe, Kenya

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Abstract

Tsetse flies are major arthropod vectors of trypanosomes that cause debilitating African animal trypanosomiasis. The emergence of drug-resistant trypanosomes is a common problem in sub-Saharan Africa. This study aimed to identify tsetse flies’ seasonal variation in apparent densities and their infection rates and the occurrence of drug-resistant trypanosomes. Tsetse flies were collected from Lambwe, Kenya, during May and September 2021. Genomic DNA was extracted from them, and the ITS1 gene was amplified to detect Trypanosoma infection with subsequent species determination. Transporter genes DMT, E6M6, TbAT/P2, and TcoAde2 were targeted to detect polymorphisms associated with drug-resistance, using sequencing and comparison to drug-sensitive trypanosome species referenced in Genbank. A total of 498 tsetse flies and 29 non-tsetse flies were collected. The apparent density of flies was higher in wet season 6.2 fly per trap per density (FTD) than in the dry season 2.3 FTD (P = 0.001), with n = 386 and n = 141 flies caught in each season, respectively. Male tsetse flies (n = 311) were more numerous than females (n = 187) (P = 0.001). Non-tsetse flies included Tabanids and Stomoxys spp. Overall, Trypanosoma infection rate in tsetse was 5% (25/498) whereby Trypanosoma vivax was 4% (11/25), Trypanosoma congolense 36% (9/25), and Trypanosoma brucei 20% (5/25) (P = 0.186 for the distribution of the species), with infections being higher in females (P = 0.019) and during the wet season (P < 0.001). Numerous polymorphisms and insertions associated with drug resistance were detected in DMT and E6M6 genes in two T. congolense isolates while some isolates lacked these genes. T. brucei lacked TbAT/P2 genes. TcoAde2 sequences in three T. congolense isolates were related to those observed in trypanosomes from cattle blood in our previous study, supporting tsetse fly involvement in transmission in the region. We report Trypanosoma associated with trypanocidal drug-resistance in tsetse flies from Lambwe, Kenya. Female tsetse flies harbored more Trypanosoma infections than males. Tsetse transmission of trypanosomes is common in Lambwe. Risk of trypanosome infection would seem higher in the wet season, when tsetse flies and Trypanosoma infections are more prevalent than during the dry season. More efforts to control animal trypanosome vectors in the region are needed, with particular focus on wet seasons.

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Data availability

Sequence datasets used in this article can be accessed in Genbank.

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Acknowledgements

The authors wish to acknowledge the support of the Kenya Tsetse and Trypanosomiasis Eradication Council (KENTTEC) for their help in carrying out the field activities for this study and thank Dr. Serap Aksoy for providing positive control for Trypansoma DNA.

Funding

Ivy Okello received funding from Partnership for Skills in Applied Sciences, Engineering and Technology-Regional Scholarship Innovative Fund (PASET-RSIF) to pursue this study. GE is supported by the USDA National Institute of Food and Agriculture, Hatch Project VA-160131.

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Authors and Affiliations

  1. Department of Microbiology, Parasitology and Biotechnology, Sokoine University of Agriculture, Chuo Kikuu, P.O. Box 3019, Morogoro, Tanzania

    Ivy Okello, Jahashi Nzalawahe & Eliakunda Mafie

  2. Africa Centre of Excellence for Infectious Diseases of Humans and Animals in Eastern and Southern Africa, SACIDS Foundation for One Health, P.O. Box 3297, Morogoro, Tanzania

    Ivy Okello

  3. Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA, 24061, USA

    Ivy Okello & Gillian Eastwood

  4. The Global Change Center at Virginia Tech, Blacksburg, VA, 24061, USA

    Gillian Eastwood

  5. Center for Emerging, Zoonotic, and Arthropod-borne Pathogens (CeZAP), Virginia Tech, Blacksburg, VA, USA

    Gillian Eastwood

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  1. Ivy Okello
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  2. Jahashi Nzalawahe
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  3. Eliakunda Mafie
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  4. Gillian Eastwood
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Contributions

IO conceptualized the study, acquired the PASET-RSIF scholarship funding, developed the methodology, did the investigation, performed analysis, and did writing of original draft; IO, GE, EM, and JN did the review and editing; GE, EM, and JN provided supervision.

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Correspondence to Ivy Okello.

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Okello, I., Nzalawahe, J., Mafie, E. et al. Seasonal variation in tsetse fly apparent density and Trypanosoma spp. infection rate and occurrence of drug-resistant trypanosomes in Lambwe, Kenya. Parasitol Res 123, 46 (2024). https://doi.org/10.1007/s00436-023-08081-1

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