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      Vector competence of sterile male Glossina fuscipes fuscipes for Trypanosoma brucei brucei: implications for the implementation of the sterile insect technique in a sleeping sickness focus in Chad

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          Abstract

          Background

          Human African trypanosomiasis (HAT) is a neglected tropical disease caused by Trypanosoma brucei gambiense transmitted by tsetse flies in sub-Saharan West Africa. In southern Chad the most active and persistent focus is the Mandoul focus, with 98% of the reported human cases, and where African animal trypanosomosis (AAT) is also present. Recently, a control project to eliminate tsetse flies ( Glossina fuscipes fuscipes) in this focus using the sterile insect technique (SIT) was initiated. However, the release of large numbers of sterile males of G. f. fuscipes might result in a potential temporary increase in transmission of trypanosomes since male tsetse flies are also able to transmit the parasite. The objective of this work was therefore to experimentally assess the vector competence of sterile males treated with isometamidium for Trypanosoma brucei brucei.

          Methods

          An experimental infection was set up in the laboratory, mimicking field conditions: the same tsetse species that is present in Mandoul was used. A T. b. brucei strain close to T. b. gambiense was used, and the ability of the sterile male tsetse flies fed on blood with and without a trypanocide to acquire and transmit trypanosomes was measured.

          Results

          Only 2% of the experimentally infected flies developed an immature infection (midgut) while none of the flies developed a metacyclic infection of T. b. brucei in the salivary glands. We did not observe any effect of the trypanocide used (isometamidium chloride at 100 mg/l) on the development of infection in the flies.

          Conclusions

          Our results indicate that sterile males of the tested strain of G. f. fuscipes were unable to cyclically transmit T. b. brucei and might even be refractory to the infection. The data of the research indicate that the risk of cyclical transmission of T. brucei by sterile male G. f. fuscipes of the strain colonized at IAEA for almost 40 years appears to be small.

          Graphical Abstract

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s13071-023-05721-4.

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          Most cited references34

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          TheRCommander: A Basic-Statistics Graphical User Interface toR

          John Fox (2005)
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            Glossina austeni (Diptera: Glossinidae) eradicated on the island of Unguja, Zanzibar, using the sterile insect technique.

            An area-wide integrated tsetse eradication project was initiated in Zanzibar in 1994 by the International Atomic Energy Agency and the governments of Tanzania and Zanzibar, to eradicate Glossina austeni Newstead from Unguja Island (Zanzibar) using the sterile insect technique. Suppression of the tsetse population on Unguja was initiated in 1988 by applying residual pyrethroids as a pour-on formulation to livestock and by the deployment of insecticide impregnated screens in some of the forested areas. This was followed by sequential releases of gamma-sterilized male flies by light aircraft. The flies, packaged in carton release containers, were dispersed twice a week along specific flight lines separated by a distance of 1-2 km. More than 8.5 million sterile male flies were released by air from August 1994 to December 1997. A sterile to indigenous male ratio of >50:1 was obtained in mid-1995 and it increased to >100:1 by the end of 1995. As a consequence the proportion of sampled young females (1-2 ovulations), with an egg in utero in embryonic arrest or an uterus empty as a result of expulsion of a dead embryo, increased from 70% in the last quarter of 1995. In addition, the age structure of the female population became significantly distorted in favor of old flies (> or = 4 ovulations) by the end of 1995. The apparent density of the indigenous fly population declined rapidly in the last quarter of 1995, followed by a population crash in the beginning of 1996. The last trapped indigenous male and female flies were found in weeks 32 and 36, 1996, respectively. Time for 6 fly generations elapsed between the last catch of an indigenous fly and the end of the sterile male releases in December 1997.
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              Trypanosoma brucei: a rapid "matching" method for estimating the host's parasitemia.

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                Author and article information

                Contributors
                mahamatout@ymail.com
                adeline.segard@ird.fr
                rargiles@hotmail.com
                a.g.parker@protonmail.com
                philippe.solano@ird.fr
                A.M.M.Abd-Alla@iaea.org
                J.Bouyer@iaea.org
                sophie.ravel@ird.fr
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                22 March 2023
                22 March 2023
                2023
                : 16
                : 111
                Affiliations
                [1 ]Institut de Recherche en Elevage pour le Développement (IRED), Ndjaména, Chad
                [2 ]GRID grid.121334.6, ISNI 0000 0001 2097 0141, Université de Montpellier, Cirad, IRD, Intertryp, ; Montpellier, France
                [3 ]GRID grid.423769.d, ISNI 0000 0004 7592 2050, Centre International de Recherche-Développement sur l’Elevage en Zone Subhumide (CIRDES), ; Bobo-Dioulasso, Burkina Faso
                [4 ]GRID grid.420221.7, ISNI 0000 0004 0403 8399, Joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency Centre of Nuclear Techniques in Food and Agriculture, , Insect Pest Control Sub-programme, ; A-1400 Vienna, Austria
                [5 ]GRID grid.121334.6, ISNI 0000 0001 2097 0141, Université de Montpellier, Cirad, INRAE, ASTRE, ; Montpellier, France
                Article
                5721
                10.1186/s13071-023-05721-4
                10035118
                36949538
                76d22103-5bbd-4973-8f78-fd2f9a52e86c
                © The Author(s) 2023

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 5 December 2022
                : 1 March 2023
                Funding
                Funded by: IAEA
                Award ID: EVT 1804311
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2023

                Parasitology
                tsetse,isometamidium,trypanocide,trypanosoma brucei gambiense
                Parasitology
                tsetse, isometamidium, trypanocide, trypanosoma brucei gambiense

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