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      The study of trypanosome species circulating in domestic animals in two human African trypanosomiasis foci of Côte d'Ivoire identifies pigs and cattle as potential reservoirs of Trypanosoma brucei gambiense

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          Abstract

          Background

          Important control efforts have led to a significant reduction of the prevalence of human African trypanosomiasis (HAT) in Côte d’Ivoire, but the disease is still present in several foci. The existence of an animal reservoir of Trypanosoma brucei gambiense may explain disease persistence in these foci where animal breeding is an important source of income but where the prevalence of animal African trypanosomiasis (AAT) is unknown. The aim of this study was to identify the trypanosome species circulating in domestic animals in both Bonon and Sinfra HAT endemic foci.

          Methodology/Principal findings

          552 domestic animals (goats, pigs, cattle and sheep) were included. Blood samples were tested for trypanosomes by microscopic observation, species-specific PCR for T. brucei sl, T. congolense, T. vivax and subspecies-specific PCR for T. b. gambiense and T. b. gambiense immune trypanolysis (TL). Infection rates varied significantly between animal species and were by far the highest in pigs (30%). T. brucei s.l was the most prevalent trypanosome species (13.7%) followed by T. congolense. No T. b. gambiense was identified by PCR while high TL positivity rates were observed using T. b. gambiense specific variants (up to 27.6% for pigs in the Bonon focus).

          Conclusion

          This study shows that domestic animals are highly infected by trypanosomes in the studied foci. This was particularly true for pigs, possibly due to a higher exposure of these animals to tsetse flies. Whereas T. brucei s.l. was the most prevalent species, discordant results were obtained between PCR and TL regarding T. b. gambiense identification. It is therefore crucial to develop better tools to study the epidemiological role of potential animal reservoir for T. b. gambiense. Our study illustrates the importance of “one health” approaches to reach HAT elimination and contribute to AAT control in the studied foci.

          Author summary

          In Africa, significant efforts to control human African trypanosomiasis (HAT) over the past three decades have drastically reduced the prevalence of the disease and elimination seems today an achievable goal. However, potential animal reservoirs of Trypanosoma brucei gambiense may compromise this ambitious objective. In the Bonon and Sinfra HAT endemic foci in Côte d’Ivoire, no recent data are available about the prevalence of animal African trypanosomiasis (AAT). The aim of this study was to identify trypanosomes circulating in domestic animals in these two HAT foci using serological, parasitological and molecular tools. We showed that T. brucei s.l. and T. congolense were the most prevalent trypanosome species and that pigs and cattle were the most infected animals. Discordant results were observed between the T. b. gambiense specific molecular and serological tools and the presence of an animal reservoir for T. b. gambiense remains unclear. Nevertheless, improved control strategies can be proposed based on this study to reach HAT elimination and contribute to AAT control in the study areas.

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          Most cited references61

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          microsatellite analyser(MSA): a platform independent analysis tool for large microsatellite data sets

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            Trypanosoma brucei Parasites Occupy and Functionally Adapt to the Adipose Tissue in Mice

            Summary Trypanosoma brucei is an extracellular parasite that causes sleeping sickness. In mammalian hosts, trypanosomes are thought to exist in two major niches: early in infection, they populate the blood; later, they breach the blood-brain barrier. Working with a well-established mouse model, we discovered that adipose tissue constitutes a third major reservoir for T. brucei. Parasites from adipose tissue, here termed adipose tissue forms (ATFs), can replicate and were capable of infecting a naive animal. ATFs were transcriptionally distinct from bloodstream forms, and the genes upregulated included putative fatty acid β-oxidation enzymes. Consistent with this, ATFs were able to utilize exogenous myristate and form β-oxidation intermediates, suggesting that ATF parasites can use fatty acids as an external carbon source. These findings identify the adipose tissue as a niche for T. brucei during its mammalian life cycle and could potentially explain the weight loss associated with sleeping sickness.
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              Epidemiology of human African trypanosomiasis

              Human African trypanosomiasis (HAT), or sleeping sickness, is caused by Trypanosoma brucei gambiense, which is a chronic form of the disease present in western and central Africa, and by Trypanosoma brucei rhodesiense, which is an acute disease located in eastern and southern Africa. The rhodesiense form is a zoonosis, with the occasional infection of humans, but in the gambiense form, the human being is regarded as the main reservoir that plays a key role in the transmission cycle of the disease. The gambiense form currently assumes that 98% of the cases are declared; the Democratic Republic of the Congo is the most affected country, with more than 75% of the gambiense cases declared. The epidemiology of the disease is mediated by the interaction of the parasite (trypanosome) with the vectors (tsetse flies), as well as with the human and animal hosts within a particular environment. Related to these interactions, the disease is confined in spatially limited areas called “foci”, which are located in Sub-Saharan Africa, mainly in remote rural areas. The risk of contracting HAT is, therefore, determined by the possibility of contact of a human being with an infected tsetse fly. Epidemics of HAT were described at the beginning of the 20th century; intensive activities have been set up to confront the disease, and it was under control in the 1960s, with fewer than 5,000 cases reported in the whole continent. The disease resurged at the end of the 1990s, but renewed efforts from endemic countries, cooperation agencies, and nongovernmental organizations led by the World Health Organization succeeded to raise awareness and resources, while reinforcing national programs, reversing the trend of the cases reported, and bringing the disease under control again. In this context, sustainable elimination of the gambiense HAT, defined as the interruption of the transmission of the disease, was considered as a feasible target for 2030. Since rhodesiense HAT is a zoonosis, where the animal reservoir plays a key role, the interruption of the disease’s transmission is not deemed feasible.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: SupervisionRole: Writing – original draft
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: SupervisionRole: Writing – original draft
                Role: Data curationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: Methodology
                Role: Funding acquisitionRole: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: MethodologyRole: Visualization
                Role: Data curationRole: MethodologyRole: Visualization
                Role: Funding acquisitionRole: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: ConceptualizationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: MethodologyRole: ValidationRole: Writing – original draft
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draft
                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
                18 October 2017
                October 2017
                : 11
                : 10
                : e0005993
                Affiliations
                [1 ] Laboratoire des Interactions Hôte-Microorganisme-Environnement et Evolution, Unité de Formation et de Recherche Environnement, Université Jean Lorougnon Guédé, Daloa, Côte d’Ivoire
                [2 ] Unité de recherches sur les bases biologiques de la lutte intégrée, Centre International de Recherche-Développement sur l’Elevage en zone Subhumide, Bobo-Dioulasso, Burkina Faso
                [3 ] Unité de Formation et de Recherche Sciences et Techniques, Université Nazi Boni, Bobo-Dioulasso, Burkina-Faso
                [4 ] Unité de Recherche « Trypanosomoses », Institut Pierre Richet, Bouaké, Côte d’Ivoire
                [5 ] Unité Mixte de Recherche IRD-CIRAD 177, INTERTRYP, Institut de Recherche pour le Développement (IRD), Montpellier, France
                [6 ] Programme National d’Elimination de la Trypanosomose Humaine Africaine, Ministère de la Santé et de l’Hygiène Publique, Abidjan, Côte d’Ivoire
                [7 ] Biomedical Sciences Department, Institute of Tropical Medicine, Antwerp, Belgium
                Institute of Tropical Medicine, BELGIUM
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-8427-0769
                Article
                PNTD-D-17-00414
                10.1371/journal.pntd.0005993
                5662240
                29045405
                963b46f1-1d98-40c8-b0ae-aeb085a43665
                © 2017 N’Djetchi et al

                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
                : 16 April 2017
                : 25 September 2017
                Page count
                Figures: 5, Tables: 3, Pages: 16
                Funding
                This study was funded by Programme d’Appui à l’Enseignement supérieur/Union Economique et Monétaire Ouest Africaine ( http://www.uemoa.int/) to MK. This study also received support from a Word Health Organization (WHO) - Institut de Recherche pour le Développement (IRD) collaborative project to VJ. MK, DK, HI, and JK are supported by the “Jeunes Equipes AIRD” JEAI program (ERHATryp project). 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
                vor-update-to-uncorrected-proof
                2017-10-30
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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