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      The prevalence of schistosomiasis in Uganda: A nationally representative population estimate to inform control programs and water and sanitation interventions

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          Abstract

          Background

          To improve schistosomiasis control programs in Uganda, where intestinal schistosomiasis is a widespread public health problem, a country-wide assessment of the disease prevalence among all age ranges is needed. Few studies have aimed to quantify the relationships between disease prevalence and water and sanitation characteristics across Uganda to understand the potential to interrupt disease transmission with an integrated package of interventions.

          Methodology/Principal findings

          A nationally representative survey was undertaken that included a household and individual questionnaire followed by disease testing based on detection of worm antigens (circulating cathodic antigen–CCA), diagnosis and treatment. A comprehensive set of questions was asked of randomly sampled individuals, two years of age and above, to understand their water and sanitation infrastructure, open defecation behaviors, exposure to surface water bodies, and knowledge of schistosomiasis. From a set of 170 randomly sampled, geographically diverse enumeration areas, a total of 9,183 study participants were included. After adjustment with sample weights, the national prevalence of schistosomiasis was 25.6% (95% confidence interval (CI): 22.3, 29.0) with children ages two to four most at risk for the disease with 36.1% infected (95% CI: 30.1, 42.2). The defecation behaviors of an individual were more strongly associated with infection status than the household water and sanitation infrastructure, indicating the importance of incorporating behavior change into community-led total sanitation coverage.

          Conclusions/Significance

          Our results highlight the importance of incorporating monitoring and evaluation data into control programs in Uganda to understand the geographic distribution of schistosomiasis prevalence outside of communities where endemicity is known to be high. The high prevalence of schistosomiasis among the youngest age group, ineligible to receive drug treatment, shows the imperative to develop a child-appropriate drug protocol that can be safely administered to preschool-aged children. Water and sanitation interventions should be considered an essential investment for elimination alongside drug treatment.

          Author summary

          Schistosomiasis is a neglected tropical disease in sub-Saharan Africa that has remained intractable despite efforts to eliminate it through mass drug administration. The transmission cycle is perpetuated when sanitation infrastructure does not adequately capture infected urine or feces and local water bodies, with snail vectors, are contaminated. Schistosomiasis has been linked with stunting and cognitive deficits and there is particular concern for the most vulnerable age group under five years old who are undergoing critical intestinal development but are ineligible to receive drug treatment. Efforts to reduce the disease have focused on children and young adolescents in endemic areas, near water bodies where transmission is known to be high. In Uganda, where fresh water bodies are abundant and intestinal schistosomiasis is endemic, very little is understood about the disease prevalence at a national level. We conducted a large, nationally representative survey and found a national prevalence of 25.6% where the 2–4 year old children had the highest prevalence for schistosomiasis with 36.1% infected. The most significant risk-factor for the disease was an individual’s open defecation behaviors in surface waters. This emphasizes the need to include water and sanitation investments alongside drug treatment and behavior change to control schistosomiasis in Uganda.

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          Most cited references54

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          Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk.

          An estimated 779 million people are at risk of schistosomiasis, of whom 106 million (13.6%) live in irrigation schemes or in close proximity to large dam reservoirs. We identified 58 studies that examined the relation between water resources development projects and schistosomiasis, primarily in African settings. We present a systematic literature review and meta-analysis with the following objectives: (1) to update at-risk populations of schistosomiasis and number of people infected in endemic countries, and (2) to quantify the risk of water resources development and management on schistosomiasis. Using 35 datasets from 24 African studies, our meta-analysis showed pooled random risk ratios of 2.4 and 2.6 for urinary and intestinal schistosomiasis, respectively, among people living adjacent to dam reservoirs. The risk ratio estimate for studies evaluating the effect of irrigation on urinary schistosomiasis was in the range 0.02-7.3 (summary estimate 1.1) and that on intestinal schistosomiasis in the range 0.49-23.0 (summary estimate 4.7). Geographic stratification showed important spatial differences, idiosyncratic to the type of water resources development. We conclude that the development and management of water resources is an important risk factor for schistosomiasis, and hence strategies to mitigate negative effects should become integral parts in the planning, implementation, and operation of future water projects.
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            Prevalence odds ratio or prevalence ratio in the analysis of cross sectional data: what is to be done?

            To review the appropriateness of the prevalence odds ratio (POR) and the prevalence ratio (PR) as effect measures in the analysis of cross sectional data and to evaluate different models for the multivariate estimation of the PR. A system of linear differential equations corresponding to a dynamic model of a cohort with a chronic disease was developed. At any point in time, a cross sectional analysis of the people then in the cohort provided a prevalence based measure of the effect of exposure on disease. This formed the basis for exploring the relations between the POR, the PR, and the incidence rate ratio (IRR). Examples illustrate relations for various IRRs, prevalences, and differential exodus rates. Multivariate point and interval estimation of the PR by logistic regression is illustrated and compared with the results from proportional hazards regression (PH) and generalised linear modelling (GLM). The POR is difficult to interpret without making restrictive assumptions and the POR and PR may lead to different conclusions with regard to confounding and effect modification. The PR is always conservative relative to the IRR and, if PR > 1, the POR is always > PR. In a fixed cohort and with an adverse exposure, the POR is always > or = IRR, but in a dynamic cohort with sufficient underlying follow up the POR may overestimate or underestimate the IRR, depending on the duration of follow up. Logistic regression models provide point and interval estimates of the PR (and POR) but may be intractable in the presence of many covariates. Proportional hazards and generalised linear models provide statistical methods directed specifically at the PR, but the interval estimation in the case of PH is conservative and the GLM procedure may require constrained estimation. The PR is conservative, consistent, and interpretable relative to the IRR and should be used in preference to the POR. Multivariate estimation of the PR should be executed by means of generalised linear models or, conservatively, by proportional hazards regression.
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              Epidemiology and geography of Schistosoma mansoni in Uganda: implications for planning control.

              Intestinal schistosomiasis caused by infection with Schistosoma mansoni is a widespread public health problem in Uganda. Although long known to be endemic, its current distribution within the country requires updating of parasitological data to help guide planned control. We report such data collected between 1998 and 2002 from 201 schools and 68 communities across Uganda. In accordance with epidemiological expectation, prevalence and intensity increased with age, peaking at 10-20 years and thereafter declined moderately with age, whereas intensity declined more rapidly with age, and the prevalence of infection in a school was non-linearly related to the mean intensity of infection. We used geographical information systems to map the distribution of infection and to overlay parasitological data with interpolated environmental surfaces. The derived maps indicate both a widespread occurrence of infection and a marked variability in infection prevalence, with prevalence typically highest near the lakeshore and along large rivers. No transmission occurred at altitudes >1400 m or where total annual rainfall was <900 mm; limits which can help estimate the population at risk of schistosomiasis. The results are discussed in reference to the ecology of infection and provide an epidemiological framework for the design and implementation of control efforts underway in Uganda.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Data curationRole: Project administrationRole: ValidationRole: Writing – review & editing
                Role: Formal analysisRole: SoftwareRole: Visualization
                Role: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisition
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                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
                14 August 2019
                August 2019
                : 13
                : 8
                : e0007617
                Affiliations
                [1 ] Department of Environmental Health and Engineering, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, United States of America
                [2 ] Department of Community Health and Behavioral Sciences, School of Public Health, Makerere University, Kampala, Uganda
                [3 ] Department of Epidemiology and Biostatistics, School of Public Health, Makerere University, Kampala, Uganda
                [4 ] Department of Population, Family and Reproductive Health, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, United States of America
                [5 ] Department of Disease Control and Environmental Health, School of Public Health, College of Health Sciences, Makerere University, Kampala, Uganda
                [6 ] Vector Control Division, Ministry of Health, Kampala, Uganda
                University of Washington, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist. The funds for this project were given in the form of a gift by the Donor through his company MaxMind Inc to the Johns Hopkins University. Scott Radloff has no affliation with either the Donor or the commercial company and therefore has no competing interests.

                Author information
                http://orcid.org/0000-0002-8374-4034
                http://orcid.org/0000-0002-7385-423X
                http://orcid.org/0000-0002-5073-1472
                http://orcid.org/0000-0003-2879-0991
                Article
                PNTD-D-18-01653
                10.1371/journal.pntd.0007617
                6709927
                31412023
                92ccbdbb-cbc1-4b3b-9bb6-5f1228b829db
                © 2019 Exum 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
                : 24 November 2018
                : 9 July 2019
                Page count
                Figures: 3, Tables: 2, Pages: 21
                Funding
                Funded by: Maxmind, Inc
                Award ID: 1607050014
                Award Recipient :
                This work was funded by Maxmind, Inc. Grant/Award No. 1607050014 in partnership with Performance Monitoring and Accountability 2020, the Bill and Melinda Gates Institute for Population and Reproductive Health at the Johns Hopkins School of Public Health and The Osprey Foundation of Maryland. 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
                Parasitic Diseases
                Helminth Infections
                Schistosomiasis
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Schistosomiasis
                People and Places
                Geographical Locations
                Africa
                Uganda
                Medicine and Health Sciences
                Health Care
                Environmental Health
                Sanitation
                Medicine and Health Sciences
                Public and Occupational Health
                Environmental Health
                Sanitation
                Earth Sciences
                Hydrology
                Surface Water
                People and Places
                Population Groupings
                Age Groups
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Schistosoma
                Schistosoma Mansoni
                Medicine and Health Sciences
                Pharmaceutics
                Drug Therapy
                Drug Administration
                Medicine and Health Sciences
                Pharmaceutics
                Drug Therapy
                Custom metadata
                vor-update-to-uncorrected-proof
                2019-08-26
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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