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Key Source Habitats and Potential Dispersal of Triatoma infestans Populations in Northwestern Argentina: Implications for Vector Control

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      Abstract

      BackgroundTriatoma infestans —the principal vector of the infection that causes Chagas disease— defies elimination efforts in the Gran Chaco region. This study identifies the types of human-made or -used structures that are key sources of these bugs in the initial stages of house reinfestation after an insecticide spraying campaign.Methodology and Principal FindingsWe measured demographic and blood-feeding parameters at two geographic scales in 11 rural communities in Figueroa, northwest Argentina. Of 1,297 sites searched in spring, 279 (21.5%) were infested. Bug abundance per site and female fecundity differed significantly among habitat types (ecotopes) and were highly aggregated. Domiciles (human sleeping quarters) had maximum infestation prevalence (38.7%), human-feeding bugs and total egg production, with submaximal values for other demographic and blood-feeding attributes. Taken collectively peridomestic sites were three times more often infested than domiciles. Chicken coops had greater bug abundance, blood-feeding rates, engorgement status, and female fecundity than pig and goat corrals. The host-feeding patterns were spatially structured yet there was strong evidence of active dispersal of late-stage bugs between ecotopes. Two flight indices predicted that female fliers were more likely to originate from kitchens and domiciles, rejecting our initial hypothesis that goat and pig corrals would dominate.Conclusions and SignificanceChicken coops and domiciles were key source habitats fueling rapid house reinfestation. Focusing control efforts on ecotopes with human-fed bugs (domiciles, storerooms, goat corrals) would neither eliminate the substantial contributions to bug population growth from kitchens, chicken coops, and pig corrals nor stop dispersal of adult female bugs from kitchens. Rather, comprehensive control of the linked network of ecotopes is required to prevent feeding on humans, bug population growth, and bug dispersal simultaneously. Our study illustrates a demographic approach that may be applied to other regions and triatomine species for the design of innovative, improved vector control strategies.

      Author Summary

      The major vectors of Chagas disease are species of triatomine bugs adapted to human sleeping quarters and peridomestic annexes where they feed on humans and domestic or synanthropic mammals or birds. Knowledge of the demography and nutritional status of Triatominae in real-life settings is still fragmentary, and this affects our ability to prevent or reduce house reinfestation after insecticide spraying. In addition to showing where the bugs are likely to live (occupancy and density information), our observations and analysis of flight dispersal provide insights into where bugs are likely to originate. Data on nymphal and adult sex ratios, nutritional status, and female fecundity point to the key ecotopes and sites driving the population growth of the bugs and fueling house reinfestation. Focusing control efforts on the three ecotopes (human sleeping quarters, storerooms, and goat corrals) that housed reactive, human-fed bugs would neither eliminate the substantial contributions to bug population growth from kitchens, chicken coops, and pig corrals nor stop dispersal of adult female bugs from kitchens. Rather, comprehensive control of the linked network of ecotopes in a typical house compound and community is required to prevent feeding on humans, bug population growth, and bug dispersal simultaneously.

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      Most cited references 57

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      Sustainable vector control and management of Chagas disease in the Gran Chaco, Argentina.

      Chagas disease remains a serious obstacle to health and economic development in Latin America, especially for the rural poor. We report the long-term effects of interventions in rural villages in northern Argentina during 1984-2006. Two community-wide campaigns of residual insecticide spraying immediately and strongly reduced domestic infestation and infection with Trypanosoma cruzi in Triatoma infestans bugs and dogs and more gradually reduced the seroprevalence of children <15 years of age. Because no effective surveillance and control actions followed the first campaign in 1985, transmission resurged in 2-3 years. Renewed interventions in 1992 followed by sustained, supervised, community-based vector control largely suppressed the reestablishment of domestic bug colonies and finally led to the interruption of local human T. cruzi transmission. Human incidence of infection was nearly an order of magnitude higher in peripheral rural areas under pulsed, unsupervised, community-based interventions, where human transmission became apparent in 2000. The sustained, supervised, community-based strategy nearly interrupted domestic transmission to dogs but did not eliminate T. infestans despite the absence of pyrethroid-insecticide resistance. T. infestans persisted in part because of the lack of major changes in housing construction and quality. Sustained community participation grew out of establishing a trusted relationship with the affected communities and the local schools. The process included health promotion and community mobilization, motivation, and supervision in close cooperation with locally nominated leaders.
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        Vital statistics of Triatominae (Hemiptera: Reduviidae) under laboratory conditions. I. Triatoma infestans Klug.

         J Rabinovich (1972)
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          Effectiveness of residual spraying of peridomestic ecotopes with deltamethrin and permethrin on Triatoma infestans in rural western Argentina: a district-wide randomized trial.

          To compare the effectiveness of a single residual spraying of pyrethroids on the occurrence and abundance of Triatoma infestans in peridomestic ecotopes in rural La Rioja. A total of 667 (32.8%) peridomestic sites positive for T. infestans in May 1999 were randomly assigned to treatment within each village, sprayed in December 1999, and reinspected in December 2000. Treatments included 2.5% suspension concentrate (SC) deltamethrin in water at 25 mg active ingredient (a.i.)/m(2) applied with: (a) manual compression sprayers (standard treatment) or (b) power sprayers; (c) 1.5% emulsifiable concentrate (EC) deltamethrin at 25 mg a.i./m(2); and (d) 10% EC cis-permethrin at 170 mg a.i./m(2). EC pyrethroids were diluted in soybean oil and applied with power sprayers. All habitations were sprayed with the standard treatment. The prevalence of T. infestans 1-year post-spraying was significantly lower in sites treated with SC deltamethrin applied with manual (24%) or power sprayers (31%) than in sites treated with EC deltamethrin (40%) or EC permethrin (53%). The relative odds of infestation and catch of T. infestans 1-year post-spraying significantly increased with the use of EC pyrethroids, the abundance of bugs per site before spraying, total surface, and host numbers. All insecticides had poor residual effects on wooden posts. Most of the infestations probably originated from triatomines that survived exposure to insecticides at each site. Despite the standard treatment proving to be the most effective, the current tactics and procedures fail to eliminate peridomestic populations of T. infestans in semiarid rural areas and need to be revised.
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            Author and article information

            Affiliations
            [1 ]Laboratory of Eco-Epidemiology, Department of Ecology, Genetics and Evolution, Universidad de Buenos Aires-IEGEBA (CONICET-UBA), Buenos Aires, Argentina
            [2 ]Department of Environmental Studies, Emory University, Atlanta, Georgia, United States of America
            [3 ]Laboratory of Populations, Rockefeller and Columbia Universities, New York, New York, United States of America
            Universidad Autónoma de Yucatán, Mexico
            Author notes

            The authors have declared that no competing interests exist.

            Conceived and designed the experiments: REG MCC LAC GMVP JEC. Performed the experiments: MCC MdPF GMVP LAC JMG. Analyzed the data: REG MdPF GMVP UK JEC. Contributed reagents/materials/analysis tools: REG MCC GMVP MdPF JMG UK JEC. Wrote the paper: REG JEC.

            Contributors
            Role: Editor
            Journal
            PLoS Negl Trop Dis
            PLoS Negl Trop Dis
            plos
            plosntds
            PLoS Neglected Tropical Diseases
            Public Library of Science (San Francisco, USA )
            1935-2727
            1935-2735
            October 2014
            9 October 2014
            : 8
            : 10
            25299653
            4191936
            PNTD-D-14-00653
            10.1371/journal.pntd.0003238
            (Editor)

            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.

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            Pages: 15
            Funding
            This study was supported by awards from the National Institutes of Health/National Science Foundation Ecology of Infectious Disease program award R01TW05836 funded by the Fogarty International Center and the National Institute of Environmental Health Sciences to UK, REG and JEC, Agencia Nacional de Promoción Científica y Tecnológica (PICT and PICTO-Glaxo), and the University of Buenos Aires to REG. REG and MCC are members of CONICET Researcher's Career. JEC acknowledges with thanks the support of U.S. National Science Foundation grants EF-1038337 and DMS-1225529. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
            Categories
            Research Article
            Biology and Life Sciences
            Ecology and Environmental Sciences
            Medicine and Health Sciences
            Custom metadata
            The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.

            Infectious disease & Microbiology

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