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      Global Assessment of Schistosomiasis Control Over the Past Century Shows Targeting the Snail Intermediate Host Works Best

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          Abstract

          Background

          Despite control efforts, human schistosomiasis remains prevalent throughout Africa, Asia, and South America. The global schistosomiasis burden has changed little since the new anthelmintic drug, praziquantel, promised widespread control.

          Methodology

          We evaluated large-scale schistosomiasis control attempts over the past century and across the globe by identifying factors that predict control program success: snail control (e.g., molluscicides or biological control), mass drug administrations (MDA) with praziquantel, or a combined strategy using both. For data, we compiled historical information on control tactics and their quantitative outcomes for all 83 countries and territories in which: (i) schistosomiasis was allegedly endemic during the 20 th century, and (ii) schistosomiasis remains endemic, or (iii) schistosomiasis has been "eliminated," or is "no longer endemic," or transmission has been interrupted.

          Principal Findings

          Widespread snail control reduced prevalence by 92 ± 5% (N = 19) vs. 37 ± 7% (N = 29) for programs using little or no snail control. In addition, ecological, economic, and political factors contributed to schistosomiasis elimination. For instance, snail control was most common and widespread in wealthier countries and when control began earlier in the 20 th century.

          Conclusions/Significance

          Snail control has been the most effective way to reduce schistosomiasis prevalence. Despite evidence that snail control leads to long-term disease reduction and elimination, most current schistosomiasis control efforts emphasize MDA using praziquantel over snail control. Combining drug-based control programs with affordable snail control seems the best strategy for eliminating schistosomiasis.

          Author Summary

          Schistosomiasis is a parasitic disease infecting more than 250 million people worldwide, with almost 800 million at risk. Over the past century, nations undertook schistosomiasis control programs, with outcomes varying from little effect to elimination. The biggest hope for elimination began about 40 years ago with the discovery of the antischistosomal drug praziquantel, after which snail control was seen as old fashioned. Here, we review control program outcomes over the past 100 years across all major schistosomiasis endemic zones, including Africa, Asia, and the Americas. We screened for differences in long-term schistosomiasis reductions among countries and found the most successful programs focused on transmission control (most often snail control, with or without engineering interventions), sometimes in tandem with praziquantel. Although praziquantel has important human-health benefits, our results suggest old-fashioned snail control has been the key to schistosomiasis elimination.

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          Most cited references31

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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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            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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              Sex- and stage-related sensitivity of Schistosoma mansoni to in vivo and in vitro praziquantel treatment.

              The efficacy of praziquantel against a Puerto Rican strain of Schistosoma mansoni was assessed using both in vivo and in vitro approach. The drug effective dose (50%) in the infected mouse model was about 30 times higher when determined against 28-day-old infections than against 7-week-old parasites. Single-sex female infections were also largely refractory to treatment and single-sex male infections moderately refractory, in comparison with bisexual infections. The in vitro approach consisted of overnight exposure of parasite cultures to various drug concentrations, followed by several days of culture in drug-free medium. In vitro results confirmed in vivo data and allowed for the observation of schistosome morphological phenomena after praziquantel exposure. Early worm contraction was observed in all cases, even after exposure to sub-lethal concentrations of praziquantel or upon exposure of the largely refractory 28-day-old schistosomes. In these instances, however, worms resumed movements and normal shape upon drug removal and were able to survive. The inference of these observations on the clinical use of praziquantel and on its mechanism of action is discussed.
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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, CA USA )
                1935-2727
                1935-2735
                21 July 2016
                July 2016
                : 10
                : 7
                : e0004794
                Affiliations
                [1 ]Hopkins Marine Station, Stanford University, Pacific Grove, California, United States of America
                [2 ]Marine Science Institute, and Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, California, United States of America
                [3 ]Michigan Society of Fellows, University of Michigan, Ann Arbor, Michigan, United States of America
                [4 ]Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, United States of America
                [5 ]Children's National Health System, Washington, D.C., United States of America
                [6 ]The George Washington University, Washington, D.C., United States of America
                [7 ]Biomedical Research Institute, Rockville, Maryland, United States of America
                [8 ]Western Ecological Research Center, U.S. Geological Survey, Santa Barbara, California, United States of America
                [9 ]Department of Bioengineering, Stanford University, Stanford, California, United States of America
                Center for Discovery and Innovation in Parasitic Diseases, UNITED STATES
                Author notes

                The authors have declared no competing interests exist.

                Conceived and designed the experiments: SHS GADL CLW MHH. Performed the experiments: SHS IJJ SJS ML. Analyzed the data: SHS GADL CLW KDL CR. Wrote the paper: SHS GADL CLW SJS AMK KDL ML IJJ MHH.

                Author information
                http://orcid.org/0000-0001-5419-788X
                http://orcid.org/0000-0002-9650-2691
                Article
                PNTD-D-15-01236
                10.1371/journal.pntd.0004794
                4956325
                27441556
                78ecac25-1ae1-495c-8c35-362798698fce

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 16 July 2015
                : 31 May 2016
                Page count
                Figures: 8, Tables: 3, Pages: 19
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100005492, Stanford University;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100005492, Stanford University;
                Award ID: 61093292
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000865, Bill and Melinda Gates Foundation;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: DK087895
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R01TW010286
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 1414102
                Award Recipient :
                All funding sources: a grant by the Woods Institute’s Environmental Ventures Projects at Stanford University https://woods.stanford.edu, the Stanford Institute for Innovation in Developing Economies https://seed.stanford.edu/ through the Global Development and Poverty Initiative http://fsi.stanford.edu/docs/global-development-and-poverty-gdp, the Bill and Melinda Gates Foundation http://www.gatesfoundation.org, National Institutes of Health grant DK087895 and grant 1R01TW010286 http://www.nih.gov, and National Science Foundation Coupled Natural and Human Systems grant 1414102 http://www.nsf.gov. All grants provided partial salary support for SHS, IJJ, SJS, ML, MHH, AMK, and GADL. 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
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Molluscs
                Gastropods
                Snails
                Medicine and Health Sciences
                Infectious Diseases
                Infectious Disease Control
                Engineering and Technology
                Engineering and Technology
                Control Engineering
                Medicine and Health Sciences
                Pharmaceutics
                Drug Therapy
                Medicine and Health Sciences
                Health Care
                Environmental Health
                Sanitation
                Medicine and Health Sciences
                Public and Occupational Health
                Environmental Health
                Sanitation
                Medicine and Health Sciences
                Oncology
                Cancer Treatment
                Chemotherapy
                Medicine and Health Sciences
                Clinical Medicine
                Clinical Oncology
                Chemotherapy
                Medicine and Health Sciences
                Oncology
                Clinical Oncology
                Chemotherapy
                Medicine and Health Sciences
                Pharmaceutics
                Drug Therapy
                Chemotherapy
                Custom metadata
                Data, including schistosomiasis-control fact sheets for the countries and territories assessed, are available at the purl website hosted on Stanford University library servers for public access: https://purl.stanford.edu/yt060bn1019.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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