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      Quality of Sterile Male Tsetse after Long Distance Transport as Chilled, Irradiated Pupae

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          Abstract

          Background

          Tsetse flies transmit trypanosomes that cause human and African animal trypanosomosis, a debilitating disease of humans (sleeping sickness) and livestock (nagana). An area-wide integrated pest management campaign against Glossina palpalis gambiensis has been implemented in Senegal since 2010 that includes a sterile insect technique (SIT) component. The SIT can only be successful when the sterile males that are destined for release have a flight ability, survival and competitiveness that are as close as possible to that of their wild male counterparts.

          Methodology/Principal Findings

          Tests were developed to assess the quality of G. p. gambiensis males that emerged from pupae that were produced and irradiated in Burkina Faso and Slovakia (irradiation done in Seibersdorf, Austria) and transported weekly under chilled conditions to Dakar, Senegal. For each consignment a sample of 50 pupae was used for a quality control test (QC group). To assess flight ability, the pupae were put in a cylinder filtering emerged flies that were able to escape the cylinder. The survival of these flyers was thereafter monitored under stress conditions (without feeding). Remaining pupae were emerged and released in the target area of the eradication programme (RF group). The following parameter values were obtained for the QC flies: average emergence rate more than 69%, median survival of 6 days, and average flight ability of more than 35%. The quality protocol was a good proxy of fly quality, explaining a large part of the variances of the examined parameters.

          Conclusions/Significance

          The quality protocol described here will allow the accurate monitoring of the quality of shipped sterile male tsetse used in operational eradication programmes in the framework of the Pan-African Tsetse and Trypanosomosis Eradication Campaign.

          Author Summary

          An area-wide integrated pest management campaign against Glossina palpalis gambiensis has been implemented in Senegal since 2010 that includes a sterile insect technique component. The sterile males used for the releases emerged from pupae that were produced and irradiated in Burkina Faso and Slovakia (irradiation done in Seibersdorf, Austria) and transported weekly under chilled conditions to Dakar, Senegal. Tests were developed to assess the quality (flight ability and survival) of sterile males. To assess flight ability, for each consignment a sample of 50 pupae (QC flies) was put in a cylinder filtering emerged flies that were able to escape the cylinder. The survival of these flyers was monitored under stress conditions. Remaining pupae (RF flies) were emerged and released in the target area of the eradication programme. The quality assessment of the QC flies was a good proxy of the quality of the RF flies. The quality protocol described here will allow the accurate monitoring of the quality of shipped sterile tsetse males used in operational eradication programmes.

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          Most cited references21

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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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            Using species distribution models to optimize vector control in the framework of the tsetse eradication campaign in Senegal.

            Tsetse flies are vectors of human and animal trypanosomoses in sub-Saharan Africa and are the target of the Pan African Tsetse and Trypanosomiasis Eradication Campaign (PATTEC). Glossina palpalis gambiensis (Diptera: Glossinidae) is a riverine species that is still present as an isolated metapopulation in the Niayes area of Senegal. It is targeted by a national eradication campaign combining a population reduction phase based on insecticide-treated targets (ITTs) and cattle and an eradication phase based on the sterile insect technique. In this study, we used species distribution models to optimize control operations. We compared the probability of the presence of G. p. gambiensis and habitat suitability using a regularized logistic regression and Maxent, respectively. Both models performed well, with an area under the curve of 0.89 and 0.92, respectively. Only the Maxent model predicted an expert-based classification of landscapes correctly. Maxent predictions were therefore used throughout the eradication campaign in the Niayes to make control operations more efficient in terms of deployment of ITTs, release density of sterile males, and location of monitoring traps used to assess program progress. We discuss how the models' results informed about the particular ecology of tsetse in the target area. Maxent predictions allowed optimizing efficiency and cost within our project, and might be useful for other tsetse control campaigns in the framework of the PATTEC and, more generally, other vector or insect pest control programs.
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              Aiming to eliminate tsetse from Africa.

              The problem of tsetse-transmitted trypanosomiasis occurs only in sub-Saharan Africa, where it represents a major constraint to socio-economic development. The East African form of sleeping sickness, caused by Trypanosoma brucei rhodensiense, is an acute and fatal disease, whereas the West African form, caused by Trypanosoma brucei gambiense, is generally more chronic and debilitating. The African governments have developed a new initiative, known as the Pan African Tsetse and Trypanosomiasis Eradication Campaign, which seeks to employ an area-wide approach and appropriate fly suppression methods to eradicate tsetse from areas of tsetse infestation, at a time, to ultimately create tsetse-free zones.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                12 November 2015
                November 2015
                : 9
                : 11
                : e0004229
                Affiliations
                [1 ]Institut Sénégalais de Recherches Agricoles, Laboratoire National d’Elevage et de Recherches Vétérinaires, Service de Bio-écologie et Pathologies Parasitaires, Hann, Dakar, Sénégal
                [2 ]Pan-African Tsetse and Trypanosomosis Eradication Campaign, Bobo-Dioulasso, Burkina Faso
                [3 ]Centre de Coopération Internationale en Recherche Agronomique pour le Développement, Unité Mixte de Recherche Contrôle des Maladies Animales Exotiques et Emergentes, Campus International de Baillarguet, Montpellier, France
                [4 ]Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1309 ‘Contrôle des Maladies Animales Exotiques et Emergentes’, Montpellier, France
                [5 ]Direction des Services Vétérinaires, Dakar, Sénégal
                [6 ]Insect Pest Control Laboratory, Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture, International Atomic Energy Agency, Vienna, Austria
                [7 ]Centre International de Recherche-Développement sur l’Élevage en Zone Subhumide, Bobo-Dioulasso, Burkina Faso
                [8 ]Institute of Zoology, Section of Molecular and Applied Zoology, Slovak Academy of Sciences, Bratislava, Slovakia
                [9 ]Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), Unité Mixte de Recherche ‘Interactions hôtes-vecteurs-parasites-environnement dans les maladies tropicales négligées dues aux trypanosomatides’, Montpellier, France
                University of Perugia, ITALY
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MTS JB BS MJBV. Performed the experiments: MTS SP MDB AGF TARD JB. Analyzed the data: SP JB GG. Contributed reagents/materials/analysis tools: MTS JB BS MJBV SP GG. Wrote the paper: MTS SP MDB AGF TARD BS MJBV JBR PT IS AGP GNM JB GG.

                Article
                PNTD-D-15-01153
                10.1371/journal.pntd.0004229
                4642948
                26562521
                213fac1a-1a91-42bf-b591-97dc7587abca
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 1 July 2015
                : 22 October 2015
                Page count
                Figures: 3, Tables: 2, Pages: 13
                Funding
                The work presented in this article was supported by the Government of Senegal, the Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture, the Department of Technical Cooperation of the IAEA, the CIRAD (Project “Integrated Vector Management: innovating to improve control and reduce environmental impacts” of Institut Carnot Santé Animale (ICSA) excellence network) and the US State Department. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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