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      Water, Sanitation, Hygiene, and Soil-Transmitted Helminth Infection: A Systematic Review and Meta-Analysis

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          Abstract

          In a systematic review and meta-analysis, Eric Strunz and colleagues examine whether improvements in water, sanitation, and hygiene (WASH) practices are associated with reduced risk of infections with soil-transmitted helminths.

          Please see later in the article for the Editors' Summary

          Abstract

          Background

          Preventive chemotherapy represents a powerful but short-term control strategy for soil-transmitted helminthiasis. Since humans are often re-infected rapidly, long-term solutions require improvements in water, sanitation, and hygiene (WASH). The purpose of this study was to quantitatively summarize the relationship between WASH access or practices and soil-transmitted helminth (STH) infection.

          Methods and Findings

          We conducted a systematic review and meta-analysis to examine the associations of improved WASH on infection with STH ( Ascaris lumbricoides, Trichuris trichiura, hookworm [ Ancylostoma duodenale and Necator americanus], and Strongyloides stercoralis). PubMed, Embase, Web of Science, and LILACS were searched from inception to October 28, 2013 with no language restrictions. Studies were eligible for inclusion if they provided an estimate for the effect of WASH access or practices on STH infection. We assessed the quality of published studies with the Grades of Recommendation, Assessment, Development and Evaluation (GRADE) approach. A total of 94 studies met our eligibility criteria; five were randomized controlled trials, whilst most others were cross-sectional studies. We used random-effects meta-analyses and analyzed only adjusted estimates to help account for heterogeneity and potential confounding respectively.

          Use of treated water was associated with lower odds of STH infection (odds ratio [OR] 0.46, 95% CI 0.36–0.60). Piped water access was associated with lower odds of A. lumbricoides (OR 0.40, 95% CI 0.39–0.41) and T. trichiura infection (OR 0.57, 95% CI 0.45–0.72), but not any STH infection (OR 0.93, 95% CI 0.28–3.11). Access to sanitation was associated with decreased likelihood of infection with any STH (OR 0.66, 95% CI 0.57–0.76), T. trichiura (OR 0.61, 95% CI 0.50–0.74), and A. lumbricoides (OR 0.62, 95% CI 0.44–0.88), but not with hookworm infection (OR 0.80, 95% CI 0.61–1.06). Wearing shoes was associated with reduced odds of hookworm infection (OR 0.29, 95% CI 0.18–0.47) and infection with any STH (OR 0.30, 95% CI 0.11–0.83). Handwashing, both before eating (OR 0.38, 95% CI 0.26–0.55) and after defecating (OR 0.45, 95% CI 0.35–0.58), was associated with lower odds of A. lumbricoides infection. Soap use or availability was significantly associated with lower infection with any STH (OR 0.53, 95% CI 0.29–0.98), as was handwashing after defecation (OR 0.47, 95% CI 0.24–0.90).

          Observational evidence constituted the majority of included literature, which limits any attempt to make causal inferences. Due to underlying heterogeneity across observational studies, the meta-analysis results reflect an average of many potentially distinct effects, not an average of one specific exposure-outcome relationship.

          Conclusions

          WASH access and practices are generally associated with reduced odds of STH infection. Pooled estimates from all meta-analyses, except for two, indicated at least a 33% reduction in odds of infection associated with individual WASH practices or access. Although most WASH interventions for STH have focused on sanitation, access to water and hygiene also appear to significantly reduce odds of infection. Overall quality of evidence was low due to the preponderance of observational studies, though recent randomized controlled trials have further underscored the benefit of handwashing interventions. Limited use of the Joint Monitoring Program's standardized water and sanitation definitions in the literature restricted efforts to generalize across studies. While further research is warranted to determine the magnitude of benefit from WASH interventions for STH control, these results call for multi-sectoral, integrated intervention packages that are tailored to social-ecological contexts.

          Please see later in the article for the Editors' Summary

          Editors' Summary

          Background

          Worldwide, more than a billion people are infected with soil-transmitted helminths (STHs), parasitic worms that live in the human intestine (gut). These intestinal worms, including roundworm, hookworm, and whipworm, mainly occur in tropical and subtropical regions and are most common in developing countries, where personal hygiene is poor, there is insufficient access to clean water, and sanitation (disposal of human feces and urine) is inadequate or absent. STHs colonize the human intestine and their eggs are shed in feces and enter the soil. Humans ingest the eggs, either by touching contaminated ground or eating unwashed fruit and vegetables grown in such soil. Hookworm may enter the body by burrowing through the skin, most commonly when bare-footed individuals walk on infected soil. Repeated infection with STHs leads to a heavy parasite infestation of the gut, causing chronic diarrhea, intestinal bleeding, and abdominal pain. In addition the parasites compete with their human host for nutrients, leading to malnutrition, anemia, and, in heavily infected children, stunting of physical growth and slowing of mental development.

          Why Was This Study Done?

          While STH infections can be treated in the short-term with deworming medication, rapid re-infection is common, therefore a more comprehensive program of improved water, sanitation, and hygiene (WASH) is needed. WASH strategies include improvements in water access (e.g., water quality, water quantity, and distance to water), sanitation access (e.g., access to improved latrines, latrine maintenance, and fecal sludge management), and hygiene practices (e.g., handwashing before eating and/or after defecation, water treatment, soap use, wearing shoes, and water storage practices). WASH strategies have been shown to be effective for reducing rates of diarrhea and other neglected tropical diseases, such as trachoma; however, there is limited evidence linking specific WASH access or practices to STH infection rates. In this systematic review and meta-analysis, the researchers investigate whether WASH access or practices lower the risk of STH infections. A systematic review uses predefined criteria to identify all the research on a given topic; a meta-analysis is a statistical method that combines the results of several studies.

          What Did the Researchers Do and Find?

          The researchers identified 94 studies that included measurements of the relationship between WASH access and practices with one or more types of STHs. Meta-analyses of the data from 35 of these studies indicated that overall people with access to WASH strategies or practices were about half as likely to be infected with any STH. Specifically, a lower odds of infection with any STH was observed for those people who use treated water (odd ratio [OR] of 0.46), have access to sanitation (OR of 0.66), wear shoes (OR of 0.30), and use soap or have soap availability (OR of 0.53) compared to those without access to these practices or strategies. In addition, infection with roundworm was less than half as likely in those who practiced handwashing both before eating and after defecating than those who did not practice handwashing (OR of 0.38 and 0.45, respectively).

          What Do These Findings Mean?

          The studies included in this systematic review and meta-analysis have several shortcomings. For example, most were cross-sectional surveys—studies that examined the effect of WASH strategies on STH infections in a population at a single time point. Given this study design, people with access to WASH strategies may have shared other characteristics that were actually responsible for the observed reductions in the risk of STH infections. Consequently, the overall quality of the included studies was low and there was some evidence for publication bias (studies showing a positive association are more likely to be published than those that do not). Nevertheless, these findings confirm that WASH access and practices provide an effective control measure for STH. Controlling STHs in developing countries would have a huge positive impact on the physical and mental health of the population, especially children, therefore there should be more emphasis on expanding access to WASH as part of development guidelines and targets, in addition to short-term preventative chemotherapy currently used.

          Additional Information

          Please access these websites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.1001620.

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          Most cited references 129

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          Water, sanitation and hygiene for the prevention of diarrhoea

          Background Ever since John Snow’s intervention on the Broad St pump, the effect of water quality, hygiene and sanitation in preventing diarrhoea deaths has always been debated. The evidence identified in previous reviews is of variable quality, and mostly relates to morbidity rather than mortality. Methods We drew on three systematic reviews, two of them for the Cochrane Collaboration, focussed on the effect of handwashing with soap on diarrhoea, of water quality improvement and of excreta disposal, respectively. The estimated effect on diarrhoea mortality was determined by applying the rules adopted for this supplement, where appropriate. Results The striking effect of handwashing with soap is consistent across various study designs and pathogens, though it depends on access to water. The effect of water treatment appears similarly large, but is not found in few blinded studies, suggesting that it may be partly due to the placebo effect. There is very little rigorous evidence for the health benefit of sanitation; four intervention studies were eventually identified, though they were all quasi-randomized, had morbidity as the outcome, and were in Chinese. Conclusion We propose diarrhoea risk reductions of 48, 17 and 36%, associated respectively, with handwashing with soap, improved water quality and excreta disposal as the estimates of effect for the LiST model. Most of the evidence is of poor quality. More trials are needed, but the evidence is nonetheless strong enough to support the provision of water supply, sanitation and hygiene for all.
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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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              When can odds ratios mislead?

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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Med
                PLoS Med
                PLoS
                plosmed
                PLoS Medicine
                Public Library of Science (San Francisco, USA )
                1549-1277
                1549-1676
                March 2014
                25 March 2014
                : 11
                : 3
                Affiliations
                [1 ]Children Without Worms, The Task Force for Global Health, Decatur, Georgia, United States of America
                [2 ]Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, Georgia, United States of America
                [3 ]International Trachoma Initiative, The Task Force for Global Health, Decatur, Georgia, United States of America
                [4 ]Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland
                [5 ]University of Basel, Basel, Switzerland
                University of Otago, New Zealand
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: ECS DGA MES SO MCF. Performed the experiments: ECS DGA MCF. Analyzed the data: ECS. Contributed reagents/materials/analysis tools: ECS MES. Wrote the first draft of the manuscript: ECS DGA MCF. Contributed to the writing of the manuscript: ECS DGA MES SO JU MCF. ICMJE criteria for authorship read and met: ECS DGA MES SO JU MCF. Agree with manuscript results and conclusions: ECS DGA MES SO JU MCF.

                Article
                PMEDICINE-D-13-02702
                10.1371/journal.pmed.1001620
                3965411

                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.

                Page count
                Pages: 38
                Funding
                M.C.F. was funded in part by UK aid from the Department for International Development (DFID) as part of the SHARE Research Programme (www.SHAREResearch.org). However, the views expressed do not necessarily reflect the Department's official policies. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Physical Sciences
                Mathematics
                Statistics (Mathematics)
                Confidence Intervals
                Medicine and Health Sciences
                Epidemiology
                Infectious Disease Epidemiology
                Public and Occupational Health
                Global Health
                Infectious Diseases
                Parasitic Diseases
                Helminth Infections
                Soil-Transmitted Helminthiases
                Ascariasis
                Hookworm Diseases
                Strongyloidiasis
                Trichuriasis

                Medicine

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