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      The Role of Human Movement in the Transmission of Vector-Borne Pathogens

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          Abstract

          Background

          Human movement is a key behavioral factor in many vector-borne disease systems because it influences exposure to vectors and thus the transmission of pathogens. Human movement transcends spatial and temporal scales with different influences on disease dynamics. Here we develop a conceptual model to evaluate the importance of variation in exposure due to individual human movements for pathogen transmission, focusing on mosquito-borne dengue virus.

          Methodology and Principal Findings

          We develop a model showing that the relevance of human movement at a particular scale depends on vector behavior. Focusing on the day-biting Aedes aegypti, we illustrate how vector biting behavior combined with fine-scale movements of individual humans engaged in their regular daily routine can influence transmission. Using a simple example, we estimate a transmission rate ( R 0 ) of 1.3 when exposure is assumed to occur only in the home versus 3.75 when exposure at multiple locations—e.g., market, friend's—due to movement is considered. Movement also influences for which sites and individuals risk is greatest. For the example considered, intriguingly, our model predicts little correspondence between vector abundance in a site and estimated R 0 for that site when movement is considered. This illustrates the importance of human movement for understanding and predicting the dynamics of a disease like dengue. To encourage investigation of human movement and disease, we review methods currently available to study human movement and, based on our experience studying dengue in Peru, discuss several important questions to address when designing a study.

          Conclusions/Significance

          Human movement is a critical, understudied behavioral component underlying the transmission dynamics of many vector-borne pathogens. Understanding movement will facilitate identification of key individuals and sites in the transmission of pathogens such as dengue, which then may provide targets for surveillance, intervention, and improved disease prevention.

          Author Summary

          Vector-borne diseases constitute a largely neglected and enormous burden on public health in many resource-challenged environments, demanding efficient control strategies that could be developed through improved understanding of pathogen transmission. Human movement—which determines exposure to vectors—is a key behavioral component of vector-borne disease epidemiology that is poorly understood. We develop a conceptual framework to organize past studies by the scale of movement and then examine movements at fine-scale—i.e., people going through their regular, daily routine—that determine exposure to insect vectors for their role in the dynamics of pathogen transmission. We develop a model to quantify risk of vector contact across locations people visit, with emphasis on mosquito-borne dengue virus in the Amazonian city of Iquitos, Peru. An example scenario illustrates how movement generates variation in exposure risk across individuals, how transmission rates within sites can be increased, and that risk within sites is not solely determined by vector density, as is commonly assumed. Our analysis illustrates the importance of human movement for pathogen transmission, yet little is known—especially for populations most at risk to vector-borne diseases (e.g., dengue, leishmaniasis, etc.). We outline several important considerations for designing epidemiological studies to encourage investigation of individual human movement, based on experience studying dengue.

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          Most cited references 31

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          Heterogeneities in the transmission of infectious agents: implications for the design of control programs.

          From an analysis of the distributions of measures of transmission rates among hosts, we identify an empirical relationship suggesting that, typically, 20% of the host population contributes at least 80% of the net transmission potential, as measured by the basic reproduction number, R0. This is an example of a statistical pattern known as the 20/80 rule. The rule applies to a variety of disease systems, including vector-borne parasites and sexually transmitted pathogens. The rule implies that control programs targeted at the "core" 20% group are potentially highly effective and, conversely, that programs that fail to reach all of this group will be much less effective than expected in reducing levels of infection in the population as a whole.
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            Dispersal of the dengue vector Aedes aegypti within and between rural communities.

            Knowledge of mosquito dispersal is critical for vector-borne disease control and prevention strategies and for understanding population structure and pathogen dissemination. We determined Aedes aegypti flight range and dispersal patterns from 21 mark-release-recapture experiments conducted over 11 years (1991-2002) in Puerto Rico and Thailand. Dispersal was compared by release location, sex, age, season, and village. For all experiments, the majority of mosquitoes were collected from their release house or adjacent house. Inter-village movement was detected rarely, with a few mosquitoes moving a maximum of 512 meters from one Thai village to the next. Average dispersal distances were similar for males and females and females released indoors versus outdoors. The movement of Ae. aegypti was not influenced by season or age, but differed by village. Results demonstrate that adult Ae. aegypti disperse relatively short distances, suggesting that people rather than mosquitoes are the primary mode of dengue virus dissemination within and among communities.
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              Characteristics of the spatial pattern of the dengue vector, Aedes aegypti, in Iquitos, Peru.

              We determine the spatial pattern of Aedes aegypti and the containers in which they develop in two neighborhoods of the Amazonian city of Iquitos, Peru. Four variables were examined: adult Ae. aegypti, pupae, containers positive for larvae or pupae, and all water-holding containers. Adults clustered strongly within houses and weakly to a distance of 30 meters beyond the household; clustering was not detected beyond 10 meters for positive containers or pupae. Over short periods of time restricted flight range and frequent blood-feeding behavior of Ae. aegypti appear to be underlying factors in the clustering patterns of human dengue infections. Permanent, consistently infested containers (key premises) were not major producers of Ae. aegypti, indicating that larvaciding strategies by themselves may be less effective than reduction of mosquito development sites by source reduction and education campaigns. We conclude that entomologic risk of human dengue infection should be assessed at the household level at frequent time intervals.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                July 2009
                21 July 2009
                : 3
                : 7
                Affiliations
                [1 ]Entomology, University of California, Davis, California, United States of America
                [2 ]Department of Environmental Studies, Emory University, Atlanta, Georgia, United States of America
                [3 ]Tulane University, New Orleans, Louisiana, United States of America
                [4 ]United States Naval Medical Research Center Detachment, Lima and Iquitos, Peru
                [5 ]Graduate School of Public Health, San Diego State University, San Diego, California, United States of America
                Mahidol University, Thailand
                Author notes

                Conceived and designed the experiments: STS ACM GMVP VPS TJK UK JPE TWS. Performed the experiments: STS. Analyzed the data: STS. Contributed reagents/materials/analysis tools: STS. Wrote the paper: STS. Edited the manuscript: ACM GMVP VPS UK JPE TWS. Approved the manuscript: TJK.

                Article
                09-PNTD-RA-0185R1
                10.1371/journal.pntd.0000481
                2710008
                19621090
                This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
                Page count
                Pages: 9
                Categories
                Research Article
                Ecology/Behavioral Ecology
                Ecology/Spatial and Landscape Ecology
                Infectious Diseases
                Infectious Diseases/Epidemiology and Control of Infectious Diseases
                Infectious Diseases/Neglected Tropical Diseases
                Infectious Diseases/Protozoal Infections
                Infectious Diseases/Tropical and Travel-Associated Diseases
                Infectious Diseases/Viral Infections
                Public Health and Epidemiology/Social and Behavioral Determinants of Health

                Infectious disease & Microbiology

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