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      Domestic Animal Hosts Strongly Influence Human-Feeding Rates of the Chagas Disease Vector Triatoma infestans in Argentina

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          Abstract

          Background

          The host species composition in a household and their relative availability affect the host-feeding choices of blood-sucking insects and parasite transmission risks. We investigated four hypotheses regarding factors that affect blood-feeding rates, proportion of human-fed bugs (human blood index), and daily human-feeding rates of Triatoma infestans, the main vector of Chagas disease.

          Methods

          A cross-sectional survey collected triatomines in human sleeping quarters (domiciles) of 49 of 270 rural houses in northwestern Argentina. We developed an improved way of estimating the human-feeding rate of domestic T. infestans populations. We fitted generalized linear mixed-effects models to a global model with six explanatory variables (chicken blood index, dog blood index, bug stage, numbers of human residents, bug abundance, and maximum temperature during the night preceding bug catch) and three response variables (daily blood-feeding rate, human blood index, and daily human-feeding rate). Coefficients were estimated via multimodel inference with model averaging.

          Findings

          Median blood-feeding intervals per late-stage bug were 4.1 days, with large variations among households. The main bloodmeal sources were humans (68%), chickens (22%), and dogs (9%). Blood-feeding rates decreased with increases in the chicken blood index. Both the human blood index and daily human-feeding rate decreased substantially with increasing proportions of chicken- or dog-fed bugs, or the presence of chickens indoors. Improved calculations estimated the mean daily human-feeding rate per late-stage bug at 0.231 (95% confidence interval, 0.157–0.305).

          Conclusions and Significance

          Based on the changing availability of chickens in domiciles during spring-summer and the much larger infectivity of dogs compared with humans, we infer that the net effects of chickens in the presence of transmission-competent hosts may be more adequately described by zoopotentiation than by zooprophylaxis. Domestic animals in domiciles profoundly affect the host-feeding choices, human-vector contact rates and parasite transmission predicted by a model based on these estimates.

          Author Summary

          The major vectors of Chagas disease are species of triatomine bugs that have adapted to human sleeping quarters and may feed on domestic animals and humans. There is a striking lack of information on the blood-feeding rates of Triatominae in field conditions, and factors modifying the fraction of bugs that feed on humans have rarely been investigated. Here we tested whether the spring fraction of bugs' feeding contacts with humans would decrease when dogs and chickens are available in human sleeping quarters in a well-defined endemic rural area in northwestern Argentina. On average, late-stage bugs fed every four days in spring and the majority fed on humans. The results demonstrate that both the percentage of human-fed bugs and the daily rate of feeding on humans decreased substantially with increasing proportions of chicken- or dog-fed bugs in the house, or the presence of chickens indoors. Combined with earlier findings on the seasonal dynamics of bug abundance, host-feeding patterns and the relative infectivity of domestic hosts, the net effects of the presence of chickens and dogs in human sleeping quarters is predicted to increase the transmission of T. cruzi in summer when chickens move outdoors.

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          Most cited references45

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          Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm.

          The twin concepts of zooprophylaxis and the dilution effect originated with vector-borne diseases (malaria), were driven forward by studies on Lyme borreliosis and have now developed into the mantra "biodiversity protects against disease". The basic idea is that by diluting the assemblage of transmission-competent hosts with non-competent hosts, the probability of vectors feeding on transmission-competent hosts is reduced and so the abundance of infected vectors is lowered. The same principle has recently been applied to other infectious disease systems--tick-borne, insect-borne, indirectly transmitted via intermediate hosts, directly transmitted. It is claimed that the presence of extra species of various sorts, acting through a variety of distinct mechanisms, causes the prevalence of infectious agents to decrease. Examination of the theoretical and empirical evidence for this hypothesis reveals that it applies only in certain circumstances even amongst tick-borne diseases, and even less often if considering the correct metric--abundance rather than prevalence of infected vectors. Whether dilution or amplification occurs depends more on specific community composition than on biodiversity per se. We warn against raising a straw man, an untenable argument easily dismantled and dismissed. The intrinsic value of protecting biodiversity and ecosystem function outweighs this questionable utilitarian justification.
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            Blood-feeding behaviour of the malarial mosquito Anopheles arabiensis: implications for vector control.

            Feeding behaviour of the malaria vector Anopheles arabiensis Patton (Diptera: Culicidae) was monitored for 12 months (March 2003-February 2004) in the Konso District of southern Ethiopia (5 degrees 15'N, 37 degrees 28'E). More than 45 000 An. arabiensis females were collected by host-baited sampling methods (light-traps, human landing catches, cattle-baited traps) and from resting sites (huts and pit shelters). In the village of Fuchucha, where the ratio of cattle : humans was 0.6 : 1, 51% of outdoor-resting mosquitoes and 66% of those collected indoors had fed on humans, human baits outdoors caught > 2.5 times more mosquitoes than those indoors and the mean catch of mosquitoes from pit shelters was about five times that from huts. Overall, the vast majority of feeding and resting occurred outdoors. In the cattle camps of Konso, where humans slept outdoors close to their cattle, approximately 46% of resting mosquitoes collected outdoors had fed on humans despite the high cattle : human ratio (17 : 1). In both places, relatively high proportions of bloodmeals were mixed cow + human: 22-25% at Fuchucha and 37% in the cattle camps. Anthropophily was also gauged experimentally by comparing the numbers of mosquitoes caught in odour-baited entry traps baited with either human or cattle odour. The human-baited trap caught about five times as many mosquitoes as the cattle-baited one. Notwithstanding the potential pitfalls of using standard sampling devices to analyse mosquito behaviour, the results suggest that the An. arabiensis population is inherently anthropophagic, but this is counterbalanced by exophagic and postprandial exophilic tendencies. Consequently, the population feeds sufficiently on humans to transmit malaria (sporozoite rates: 0.3% for Plasmodium falciparum and 0.5% for P. vivax, by detection of circumsporozoite antigen) but also takes a high proportion of meals from non-human hosts, with 59-91% of resting mosquitoes containing blood from cattle. Hence, classical zooprophylaxis is unlikely to have a significant impact on the malaria vectorial capacity of An. arabiensis in Konso, whereas treating cattle with insecticide might do.
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              The analysis of parasite transmission by bloodsucking insects.

              C. Dye (1992)
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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, USA )
                1935-2727
                1935-2735
                May 2014
                22 May 2014
                28 May 2014
                : 8
                : 5
                : e2894
                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 GMVP LAC JMG MdPF. Analyzed the data: REG MdPF GMVP. Contributed reagents/materials/analysis tools: REG MCC GMVP MdPF UK JEC. Wrote the paper: REG UK JEC.

                Article
                PNTD-D-13-01182
                10.1371/journal.pntd.0002894
                4037315
                24852606
                bcd1df3b-7a7f-4bb0-ba71-41f8959e992d
                Copyright @ 2014

                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
                : 7 August 2013
                : 14 April 2014
                Page count
                Pages: 12
                Funding
                This study was supported by awards from the Agencia Nacional de Promoción Científica y Técnica of Argentina (PICTO-Glaxo 2011-0062 and PICT-2011-2072) to REG; National Institutes of Health/National Science Foundation Ecology of Infectious Disease program award R01 TW05836 funded by the Fogarty International Center and the National Institute of Environmental Health Sciences to UK, REG, and JEC; by the University of Buenos Aires (REG). 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
                Population Ecology
                Population Biology
                Ecology and Environmental Sciences
                Medicine and Health Sciences
                Epidemiology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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