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Molecular characterization of pathogenic African trypanosomes in biting flies and camels in surra-endemic areas outside the tsetse fly belt in Kenya

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Abstract

African animal trypanosomosis (nagana) is becoming prevalent beyond its traditionally defined geographical boundaries in African tsetse belts. However, knowledge of clinically important trypanosomes and infection rate in non-tsetse hematophagous flies and domestic animals are limited. This study characterized the potential mechanical vectors, their host feeding patterns, and trypanosome infection in them and domestic animals outside the tsetse belt in northern Kenya. Field-trapped flies and blood from camels, cattle, donkeys, goats, and sheep were screened for trypanosome infection by microscopy and polymerase chain reaction (PCR) of the internal transcribed spacer 1 region. Blood-fed specimens were analysed using PCR-HRM and/or sequencing of 16S rRNA gene to identify vertebrate blood-meal host sources. Hippobosca camelina, Stomoxys calcitrans, Tabanus spp., and Pangonia rueppellii were identified as potential vectors of trypanosomes outside the tsetse belt in Marsabit County. The trypanosome species, Trypanosoma vivax, T. evansi, T. brucei, and T. congolense were recovered in biting flies as well as in camels (Camelus dromedarius). The diversity of parasites in the biting flies was similar to that detected in the tsetse fly Glossina pallidipes collected from the tsetse-infested Shimba Hills, in coastal Kenya, suggesting a wide geographic distribution of the trypanosomes in Kenya. The biting flies fed on camels, cattle, goats, and sheep. Furthermore, we identified diverse clinical outcomes based on PCV (anemia), heamorrhagia) associated with infection with disparate Trypanosoma species. Thus, infection of flies and camels by diverse Trypanosoma species could contribute to the complex epidemiology of observed trypanosomosis in camels.

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Data availability

All data generated or analysed in this study are included in the article and as additional files. The newly generated sequences were deposited in the NCBI Nucleotide database under the accession numbers listed in Supplementary table.

Abbreviations

HRM:

High-resolution melting

icipe :

International Centre of Insect Physiology and Ecology

ITS1:

Intergenic transcribed spacer subunit 1

LNA:

Lymph node aspirate

PCV:

Packed Cell Volume

PCR:

Polymerase chain reaction.

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Acknowledgements

We thank Dr Robert Copeland for helping to identify the biting flies and taking photos of the biting flies; Tiberius Marete, David Mbuvi, Peter Muasa and Irene Onyango for technical help; Kimathi Emily and Barbara Kagima, for the study site map; Kelvin Muteru for his help in the bioinformatics; James Kabii for his technical help in the molecular studies, Collins Kigen, JohnMark Makwatta, and Tawich K. Simon for technical help in the parasite survival experiments in S. calcitrans and Caroline Muya for handling the administrative issues. Special thanks go to Daud Tamasot (MCA), Malkash Lolkitarakino and Huka Guyo Qutte, Hussein Haji Abdulahi who facilitated our research at Shurr, Nanyuki and Ngurunit area. We thank Dr Mario Younan for his valuable technical advice on camels. We are grateful for the camel owners of Ngurunit, Nanyuki, and Shurr for their cooperation.

Funding

This work was supported mainly by the IBCARP camel, grant no. DCI-FOOD/2014/ 346–739 by the European Union and funding from Max Planck Institute-icipe partner group to MNG. We also gratefully acknowledge the financial support for this research by the following organisations and agencies: Swedish International Development Cooperation Agency (Sida); the Swiss Agency for Development and Cooperation (SDC); Federal Democratic Republic of Ethiopia; and the Kenyan Government. Joel Bargul was supported whole, or in part, by the Wellcome Trust 107742/Z/15/Z and the UK Foreign, Commonwealth & Development Office, with support from the Developing Excellence in Leadership, Training and Science in Africa (DELTAS Africa) programme. The views expressed herein do not necessarily reflect the official opinion of the donors.

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Authors and Affiliations

  1. International Centre of Insect Physiology and Ecology (Icipe), P.O. Box 30772-00100, Nairobi, Kenya

    Merid N. Getahun, Jandouwe Villinger, Joel L. Bargul, Jackson M. Muema, Abel Orone, John Ngiela, Peter O. Ahuya, Rajinder K. Saini, Baldwyn Torto & Daniel K. Masiga

  2. Department of Biochemistry, Jomo Kenyatta University of Agriculture and Technology, Nairobi, Kenya

    Joel L. Bargul & Jackson M. Muema

  3. Current Address: Pestinix-International Pest & Vector Control Specialists, Nairobi, Kenya

    Rajinder K. Saini

  4. Department of Zoology and Entomology, University of Pretoria, Private Bag X20, Hatfield, 0028, South Africa

    Baldwyn Torto

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  1. Merid N. Getahun
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Contributions

MNG, BT, DM, SR conceptualized and designed the experiments. MNG, JLB, AO, POA, JN, JMM generated experimental data, JV contributed in the molecular part of the study. MNG analysed the data and wrote the manuscript. All authors revised and approved the final manuscript.

Corresponding author

Correspondence to Merid N. Getahun.

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Ethics approval and consent to participate

We collected blood samples within the framework of epidemiological surveillance activities, in accordance to the International Centre of Insect Physiology and Ecology’s Institutional Animal Care and Use Committee (IACUC) guidelines as performed during prophylaxis or diagnostic campaigns (approval number: 495 icipe-IACUC-10/2018.1). Local authorities did not require ethical statements for the research studies. We did the blood sampling of domestic animals with the authorisation of the owner. Herdsmen/women gave their consent for their animal sampling after explaining the objectives of the study. No samples other than those for routine screening and diagnostic procedures were collected. All animals sampled and found positive with trypanosomes were treated using trypanocides.

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42690_2022_896_MOESM1_ESM.tif

Supplementary file1 Figure S1 PCR products were resolved 1% ethidium-bromide stained agarose gel (8V for 1.5 hrs) to check for any contamination. The DNA isolated from whole fly was amplified targeting trypanosomal ITS1 gene. Lane: M 10- bp marker, Bf (reaction buffer), wt (PCR water), TB (T. brucei ILTat 1.4) TV (T. vivax IL 2136), TC (T. congolense savannah (IL3000)), and TE (T. evansi KETRI 2479), F1- F10 DNA sample from H. camelina flies. The absence of PCR product under Bf, and wt show no contamination from extraction buffer (TIF 11846 KB)

42690_2022_896_MOESM2_ESM.tif

Supplementary file2 Figure S2 Number of H. camelina recaptured at the specified distance from pint of release. Number in parenthesis shows percentage of flies recaptured (TIF 5515 KB)

42690_2022_896_MOESM3_ESM.tif

Supplementary file3 Figure S3 (A) PCR products were resolved 1% ethidium-bromide stained agarose gel (8V for 1.5 hrs) to check for trypanosomes in blood and lymph node aspirate. The DNA isolated from blood and lymph node aspirate was amplified targeting trypanosomal ITS1 gene. Lane: M 10- bp marker, -Ve (reaction buffer), TE (T. evansi KETRI 2479) TV (T. vivax IL 2136), TC (T. congolense savannah (IL3000)), and LN_C1, LN_C2, DNA sample from two camel lymph node aspirate, B_C1 and B_C2 DNA from corresponding blood samples from the same camel. The result shows both samples of the lymph node aspirate were positive, while blood samples were negative from the same camel. (B) Five camels blood and lymph node aspirate were analysed, only camel five lymph node aspirate was positive for T.vivax but blood sample from the same camel was negative (TIF 26280 KB)

Supplementary file4 (DOCX 21 KB)

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Getahun, M.N., Villinger, J., Bargul, J.L. et al. Molecular characterization of pathogenic African trypanosomes in biting flies and camels in surra-endemic areas outside the tsetse fly belt in Kenya. Int J Trop Insect Sci 42, 3729–3745 (2022). https://doi.org/10.1007/s42690-022-00896-2

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