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      Cross-sectional Study of the Burden of Vector-Borne and Soil-Transmitted Polyparasitism in Rural Communities of Coast Province, Kenya

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          Abstract

          Background

          In coastal Kenya, infection of human populations by a variety of parasites often results in co-infection or poly-parasitism. These parasitic infections, separately and in conjunction, are a major cause of chronic clinical and sub-clinical human disease and exert a long-term toll on economic welfare of affected populations. Risk factors for these infections are often shared and overlap in space, resulting in interrelated patterns of transmission that need to be considered at different spatial scales. Integration of novel quantitative tools and qualitative approaches is needed to analyze transmission dynamics and design effective interventions.

          Methodology

          Our study was focused on detecting spatial and demographic patterns of single- and co-infection in six villages in coastal Kenya. Individual and household level data were acquired using cross-sectional, socio-economic, and entomological surveys. Generalized additive models (GAMs and GAMMs) were applied to determine risk factors for infection and co-infections. Spatial analysis techniques were used to detect local clusters of single and multiple infections.

          Principal findings

          Of the 5,713 tested individuals, more than 50% were infected with at least one parasite and nearly 20% showed co-infections. Infections with Schistosoma haematobium (26.0%) and hookworm (21.4%) were most common, as was co-infection by both (6.3%). Single and co-infections shared similar environmental and socio-demographic risk factors. The prevalence of single and multiple infections was heterogeneous among and within communities. Clusters of single and co-infections were detected in each village, often spatially overlapped, and were associated with lower SES and household crowding.

          Conclusion

          Parasitic infections and co-infections are widespread in coastal Kenya, and their distributions are heterogeneous across landscapes, but inter-related. We highlighted how shared risk factors are associated with high prevalence of single infections and can result in spatial clustering of co-infections. Spatial heterogeneity and synergistic risk factors for polyparasitism need to be considered when designing surveillance and intervention strategies.

          Author Summary

          In Coast Province, Kenya, infections with Schistosoma haematobium, Plasmodium spp., filarial nematodes, and geohelminths are common, resulting in high levels of both single infections and polyparasitism. The long-term effect of these infections, separately or in combination, has a major impact on human health and on the economic welfare of affected populations. The transmission dynamics of these parasitic infections can be linked to shared risk factors that often overlap in space. We studied human and environmental factors driving transmission and the resulting spatial pattern of infections in six communities, using cross-sectional, socio-economic and entomological surveys. Single and co-infections were widespread in the communities, and were associated with environmental, demographic and socio-economic risk factors, including distance of community from the coast, sanitation and human age and crowding. The spatial patterns of single and co-infections were heterogeneous among and within communities, with overlapping clusters of single and multiple infections in areas where houses with lower socio-economic status and more crowding were located. The heterogeneities among and within communities can provide important insights when designing surveillance and intervention strategies when planning appropriate surveillance and control strategies targeting polyparasitism.

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          Most cited references65

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          Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis.

          Schistosomiasis is one of the world's most prevalent infections, yet its effect on the global burden of disease is controversial. Published disability-adjusted life-year (DALY) estimates suggest that the average effect of schistosome infection is quite small, although this is disputed. To develop an evidenced-based reassessment of schistosomiasis-related disability, we did a systematic review of data on disability-associated outcomes for all forms of schistosomiasis. We did structured searches using EMBASE, PUBMED, and Cochrane electronic databases. Published bibliographies were manually searched, and unpublished studies were obtained by contacting research groups. Reports were reviewed and abstracted independently by two trained readers. All randomised and observational studies of schistosomiasis morbidity were eligible for inclusion. We calculated pooled estimates of reported disability-related effects using weighted odds ratios for categorical outcomes and standardised mean differences for continuous data. 482 published or unpublished reports (March, 1921, to July, 2002) were screened. Of 135 selected for inclusion, 51 provided data for performance-related symptoms, whereas 109 reported observed measures of disability-linked morbidities. Schistosomiasis was significantly associated with anaemia, chronic pain, diarrhoea, exercise intolerance, and undernutrition. By contrast with WHO estimates of 0.5% disability weight assigned to schistosomiasis, 2-15% disability seems evident in different functional domains of a person with schistosomiasis. This raised estimate, if confirmed in formal patient-preference studies, indicates a need to reassess our priorities for treating this silent pandemic of schistosomiasis.
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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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                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
                July 2014
                24 July 2014
                : 8
                : 7
                : e2992
                Affiliations
                [1 ]Department of Environmental Sciences, Emory University, Atlanta, Georgia, United States of America
                [2 ]Department of Environment and Health Sciences, Technical University of Mombasa, Mombasa, Kenya
                [3 ]Parasitology Department, Liverpool School of Tropical Medicine, Liverpool, United Kingdom
                [4 ]Center for Global Health and Diseases, Case Western Reserve University, Cleveland, Ohio, United States of America
                [5 ]Division of Vector-Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya
                Universidad San Francisco de Quito, Ecuador
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: CHK UK FM. Performed the experiments: FM ALB PLM EMM. Analyzed the data: DB FM UK CHK. Contributed reagents/materials/analysis tools: ALB. Wrote the paper: DB UK CHK FM.

                Article
                PNTD-D-13-01947
                10.1371/journal.pntd.0002992
                4109907
                25057825
                ac8acfa0-a848-489c-9a3d-89eda6b8ca93
                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 December 2013
                : 20 May 2014
                Page count
                Pages: 17
                Funding
                This work was supported by National Institutes of Health Research Grant R01TW008067 funded by the Ecology of Infectious Diseases Program through the Fogarty International Center. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Epidemiology
                Health Care
                Environmental Health
                Socioeconomic Aspects of Health
                Infectious Diseases
                Public and Occupational Health
                Disease Ecology
                Physical Sciences
                Mathematics
                Statistics (Mathematics)

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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