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      Elimination of Schistosomiasis Transmission in Zanzibar: Baseline Findings before the Onset of a Randomized Intervention Trial

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          Abstract

          Background

          Gaining and sustaining control of schistosomiasis and, whenever feasible, achieving local elimination are the year 2020 targets set by the World Health Organization. In Zanzibar, various institutions and stakeholders have joined forces to eliminate urogenital schistosomiasis within 5 years. We report baseline findings before the onset of a randomized intervention trial designed to assess the differential impact of community-based praziquantel administration, snail control, and behavior change interventions.

          Methodology

          In early 2012, a baseline parasitological survey was conducted in ∼20,000 people from 90 communities in Unguja and Pemba. Risk factors for schistosomiasis were assessed by administering a questionnaire to adults. In selected communities, local knowledge about schistosomiasis transmission and prevention was determined in focus group discussions and in-depths interviews. Intermediate host snails were collected and examined for shedding of cercariae.

          Principal Findings

          The baseline Schistosoma haematobium prevalence in school children and adults was 4.3% (range: 0–19.7%) and 2.7% (range: 0–26.5%) in Unguja, and 8.9% (range: 0–31.8%) and 5.5% (range: 0–23.4%) in Pemba, respectively. Heavy infections were detected in 15.1% and 35.6% of the positive school children in Unguja and Pemba, respectively. Males were at higher risk than females (odds ratio (OR): 1.45; 95% confidence interval (CI): 1.03–2.03). Decreasing adult age (OR: 1.04; CI: 1.02–1.06), being born in Pemba (OR: 1.48; CI: 1.02–2.13) or Tanzania (OR: 2.36; CI: 1.16–4.78), and use of freshwater (OR: 2.15; CI: 1.53–3.03) showed higher odds of infection. Community knowledge about schistosomiasis was low. Only few infected Bulinus snails were found.

          Conclusions/Significance

          The relatively low S. haematobium prevalence in Zanzibar is a promising starting point for elimination. However, there is a need to improve community knowledge about disease transmission and prevention. Control measures tailored to the local context, placing particular attention to hot-spot areas, high-risk groups, and individuals, will be necessary if elimination is to be achieved.

          Author Summary

          Schistosomiasis is a chronic and debilitating disease caused by parasitic worms. It negatively impacts on the health and wellbeing of mainly rural dwellers in tropical and sub-tropical countries. The World Health Organization recently put forward an ambitious goal for the year 2020: to control schistosomiasis globally. Interruption of transmission and elimination of schistosomiasis are encouraged whenever resources allow. After careful consideration, the Schistosomiasis Consortium for Operational Research and Evaluation (SCORE) selected the Zanzibar archipelago to learn how best to eliminate schistosomiasis. We report the baseline findings of a 5-year program. Parasitological examination of about 20,000 people on Unguja and Pemba islands revealed a low overall prevalence of Schistosoma haematobium (7%). Nevertheless, hot-spots with high prevalence (>20%) and high-risk groups (males, young adults, people born in Pemba or mainland Tanzania, and people using natural freshwater) were identified. The community knowledge about schistosomiasis transmission and prevention was poor. Few of the collected intermediate host snails shed S. haematobium cercariae. A multi-arm randomized trial is now being implemented to determine the differential impact of mass deworming, snail control, and behavior change interventions. Lessons learned from this schistosomiasis elimination program will be important for other settings.

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          Most cited references 45

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          Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010.

          Measuring disease and injury burden in populations requires a composite metric that captures both premature mortality and the prevalence and severity of ill-health. The 1990 Global Burden of Disease study proposed disability-adjusted life years (DALYs) to measure disease burden. No comprehensive update of disease burden worldwide incorporating a systematic reassessment of disease and injury-specific epidemiology has been done since the 1990 study. We aimed to calculate disease burden worldwide and for 21 regions for 1990, 2005, and 2010 with methods to enable meaningful comparisons over time. We calculated DALYs as the sum of years of life lost (YLLs) and years lived with disability (YLDs). DALYs were calculated for 291 causes, 20 age groups, both sexes, and for 187 countries, and aggregated to regional and global estimates of disease burden for three points in time with strictly comparable definitions and methods. YLLs were calculated from age-sex-country-time-specific estimates of mortality by cause, with death by standardised lost life expectancy at each age. YLDs were calculated as prevalence of 1160 disabling sequelae, by age, sex, and cause, and weighted by new disability weights for each health state. Neither YLLs nor YLDs were age-weighted or discounted. Uncertainty around cause-specific DALYs was calculated incorporating uncertainty in levels of all-cause mortality, cause-specific mortality, prevalence, and disability weights. Global DALYs remained stable from 1990 (2·503 billion) to 2010 (2·490 billion). Crude DALYs per 1000 decreased by 23% (472 per 1000 to 361 per 1000). An important shift has occurred in DALY composition with the contribution of deaths and disability among children (younger than 5 years of age) declining from 41% of global DALYs in 1990 to 25% in 2010. YLLs typically account for about half of disease burden in more developed regions (high-income Asia Pacific, western Europe, high-income North America, and Australasia), rising to over 80% of DALYs in sub-Saharan Africa. In 1990, 47% of DALYs worldwide were from communicable, maternal, neonatal, and nutritional disorders, 43% from non-communicable diseases, and 10% from injuries. By 2010, this had shifted to 35%, 54%, and 11%, respectively. Ischaemic heart disease was the leading cause of DALYs worldwide in 2010 (up from fourth rank in 1990, increasing by 29%), followed by lower respiratory infections (top rank in 1990; 44% decline in DALYs), stroke (fifth in 1990; 19% increase), diarrhoeal diseases (second in 1990; 51% decrease), and HIV/AIDS (33rd in 1990; 351% increase). Major depressive disorder increased from 15th to 11th rank (37% increase) and road injury from 12th to 10th rank (34% increase). Substantial heterogeneity exists in rankings of leading causes of disease burden among regions. Global disease burden has continued to shift away from communicable to non-communicable diseases and from premature death to years lived with disability. In sub-Saharan Africa, however, many communicable, maternal, neonatal, and nutritional disorders remain the dominant causes of disease burden. The rising burden from mental and behavioural disorders, musculoskeletal disorders, and diabetes will impose new challenges on health systems. Regional heterogeneity highlights the importance of understanding local burden of disease and setting goals and targets for the post-2015 agenda taking such patterns into account. Because of improved definitions, methods, and data, these results for 1990 and 2010 supersede all previously published Global Burden of Disease results. Bill & Melinda Gates Foundation. Copyright © 2012 Elsevier Ltd. All rights reserved.
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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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              Schistosomiasis and neglected tropical diseases: towards integrated and sustainable control and a word of caution.

              In May 2001, the World Health Assembly (WHA) passed a resolution which urged member states to attain, by 2010, a minimum target of regularly administering anthelminthic drugs to at least 75% and up to 100% of all school-aged children at risk of morbidity. The refined global strategy for the prevention and control of schistosomiasis and soil-transmitted helminthiasis was issued in the following year and large-scale administration of anthelminthic drugs endorsed as the central feature. This strategy has subsequently been termed 'preventive chemotherapy'. Clearly, the 2001 WHA resolution led the way for concurrently controlling multiple neglected tropical diseases. In this paper, we recall the schistosomiasis situation in Africa in mid-2003. Adhering to strategic guidelines issued by the World Health Organization, we estimate the projected annual treatment needs with praziquantel among the school-aged population and critically discuss these estimates. The important role of geospatial tools for disease risk mapping, surveillance and predictions for resource allocation is emphasised. We clarify that schistosomiasis is only one of many neglected tropical diseases and that considerable uncertainties remain regarding global burden estimates. We examine new control initiatives targeting schistosomiasis and other tropical diseases that are often neglected. The prospect and challenges of integrated control are discussed and the need for combining biomedical, educational and engineering strategies and geospatial tools for sustainable disease control are highlighted. We conclude that, for achieving integrated and sustainable control of neglected tropical diseases, a set of interventions must be tailored to a given endemic setting and fine-tuned over time in response to the changing nature and impact of control. Consequently, besides the environment, the prevailing demographic, health and social systems contexts need to be considered.
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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
                October 2013
                17 October 2013
                : 7
                : 10
                Affiliations
                [1 ]Wolfson Wellcome Biomedical Laboratories, Department of Life Sciences, Natural History Museum, London, United Kingdom
                [2 ]Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland
                [3 ]University of Basel, Basel, Switzerland
                [4 ]Schistosomiasis Consortium for Operational Research and Evaluation, Athens, Georgia, United States of America
                [5 ]Public Health Laboratory - Ivo de Carneri, Pemba, United Republic of Tanzania
                [6 ]Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom
                [7 ]Helminth Control Laboratory Unguja, Ministry of Health, Zanzibar, United Republic of Tanzania
                [8 ]Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Faculty of Medicine, London, United Kingdom
                Centers for Disease Control and Prevention, United States of America
                Author notes

                The molluscicide niclosamide was donated by Bayer for the control of intermediate host snails in Zanzibar. This does not alter our adherence to all PLOS NTDs policies on sharing data and materials.

                Conceived and designed the experiments: SK BP SMAm KAM SMAl ISK FA JU AF DR. Performed the experiments: SK BP SMAm KAM SMAl ISK MR FA AG LB DR. Analyzed the data: SK MR. Contributed reagents/materials/analysis tools: SK BP SMAm KAM SMAl ISK LB AF DR. Wrote the paper: SK BP SMAm KAM SMAl ISK MR FA AG LB AF JU DR.

                Article
                PNTD-D-13-00548
                10.1371/journal.pntd.0002474
                3798599

                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.

                Counts
                Pages: 12
                Funding
                This study received financial support from the University of Georgia Research Foundation Inc., which is funded by the Bill & Melinda Gates Foundation for this SCORE project (prime award no. 50816; sub-award no. RR374-053/4893206). SK is financially supported by sub-award no. RR374-053/4893196. FA and MR are funded by the Wellcome Trust grant WT092749MA “A Biological repository for Schistosomiasis Research” (SCAN project). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article

                Infectious disease & Microbiology

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