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      The Prawn Macrobrachium vollenhovenii in the Senegal River Basin: Towards Sustainable Restocking of All-Male Populations for Biological Control of Schistosomiasis

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          Abstract

          Early malacological literature suggests that the outbreak of schistosomiasis, a parasitic disease transmitted by aquatic snails, in the Senegal River basin occurred due to ecological changes resulting from the construction of the Diama dam. The common treatment, the drug praziquantel, does not protect from the high risk of re-infection due to human contact with infested water on a daily basis. The construction of the dam interfered with the life cycle of the prawn Macrobrachium vollenhovenii by blocking its access to breeding grounds in the estuary. These prawns were demonstrated to be potential biological control agents, being effective predators of Schistosoma-susceptible snails. Here, we propose a responsible restocking strategy using all-male prawn populations which could provide sustainable disease control. Male prawns reach a larger size and have a lower tendency to migrate than females. We, therefore, expect that periodic restocking of all-male juveniles will decrease the prevalence of schistosomiasis and increase villagers' welfare. In this interdisciplinary study, we examined current prawn abundance along the river basin, complemented with a retrospective questionnaire completed by local fishermen. We revealed the current absence of prawns upriver and thus demonstrated the need for restocking. Since male prawns are suggested to be preferable for bio-control, we laid the molecular foundation for production of all-male M. vollenhovenii through a complete sequencing of the insulin-like androgenic gland-encoding gene (IAG), which is responsible for sexual differentiation in crustaceans. We also conducted bioinformatics and immunohistochemistry analyses to demonstrate the similarity of this sequence to the IAG of another Macrobrachium species in which neo-females are produced and their progeny are 100% males. At least 100 million people at risk of schistosomiasis are residents of areas that experienced water management manipulations. Our suggested non-breeding sustainable model of control—if proven successful—could prevent re-infections and thus prove useful throughout the world.

          Author Summary

          Schistosomiasis is a chronic parasitic disease that infects millions of people, especially in Africa. Schistosomes are transmitted by direct contact with water sources infested by freshwater snails, which are intermediate hosts for the parasite. The cure in humans is a drug, praziquantel, that kills the mature parasites inside the human body. The main problem with controlling the parasite by drug treatment is the high re-infection rate, since individuals are in contact with infected water on a daily basis. To efficiently combat the disease, an integrated management program is needed that includes control of infection in the intermediate host snails. We suggest the use of non-migrating, all-male populations of freshwater prawns that efficiently prey on these snails. Here, we describe the case of the Senegal River basin as an example of human actions (dam construction) that resulted in severe ecosystem changes, including exclusion of the native river prawns and expansion of snails hosting schistosomiasis. We have conducted an interdisciplinary study that documents the reduction of prawn abundance in the Senegal River and lays the molecular foundation for technology to produce all-male prawn populations to be used as part of an integrated disease control program, including both periodic stocking of juvenile prawns and chemotherapy.

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          Most cited references19

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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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            Transmission control for schistosomiasis - why it matters now.

            Current population-based schistosomiasis treatment programs are a first step to reducing the global burden of Schistosoma-related disease; however, they might not dramatically reduce parasite transmission in highly endemic areas. Consequently, the benefits of these programs remain in doubt because recurring low-level reinfection is likely to be associated with subtle but persistent morbidities such as anemia, undernutrition and diminished performance status. The real health benefits of transmission control need to be reconsidered and attention given to more aggressive and, ultimately, more affordable parasite elimination strategies. The next generation of schistosomiasis control can be optimized using new monitoring tools and effective transmission containment.
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              Praziquantel treatment of school children from single and mixed infection foci of intestinal and urogenital schistosomiasis along the Senegal River Basin: monitoring treatment success and re-infection patterns.

              Following major water development schemes in the 1980s, schistosomiasis has become a serious parasitic disease of children living in the Senegal River Basin. Both urogenital (Schistosoma haematobium) and intestinal (Schistosoma mansoni) schistosomiasis can be highly prevalent in school-aged children, with many individuals infected with both parasites. In order to investigate the transmission and re-infection dynamics of both parasite species, single and mixed infection foci at three villages (Nder and Temeye; S. mansoni and S. haematobium foci and Guia; S. haematobium focus) were studied. In each focus infected children were identified and selected for a 12-month study involving two treatments with praziquantel (40mg/kg) three weeks apart at the beginning of the study and again 6 months into the study. Urine and stool samples were examined for schistosome eggs before and at 6 weeks and 6 months after chemotherapy. Prevalence and intensity of infection were recorded for each child at each time point. Before treatment, in all three villages, the prevalence and intensity of infection was extremely high for both S. mansoni (79-100%) and S. haematobium (81-97%). With the first round of chemotherapy sufficient cure rates (CRs) of both species were achieved in all villages (38-96%) with high egg reduction rates (ERRs) (97-99%). The data show that high and rapid re-infection rates occur, especially for S. mansoni, within a six-month period following treatment. Re-infection must be highly linked to ecological and seasonal factors. The persistence of S. mansoni in Nder could raise concern as levels of infection intensity remain high (geometric mean intensity at baseline 653epg changed to 705epg at 12 months) after four rounds of chemotherapy. This phenomenon could be explained by extremely rapid re-infection dynamics or a sub-optimal efficacy of praziquantel against S. mansoni in this village. High intensities in mixed infections may influence disease epidemiology and control warranting further studies. The disease situation in the SRB must be monitored closely and new treatment regimes should be designed and implemented to control schistosomiasis in the school-age population. Copyright © 2012 Elsevier B.V. All rights reserved.
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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
                August 2014
                28 August 2014
                : 8
                : 8
                : e3060
                Affiliations
                [1 ]Department of Life Sciences and the National Institute for Biotechnology in the Negev, Ben-Gurion University, Beer Sheva, Israel
                [2 ]French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institute for Desert Research, Ben-Gurion University, Sede-Boqer, Israel
                [3 ]Department of Biology, Hopkins Marine Station, Stanford University, Palo Alto, California, United States of America
                [4 ]Université Gaston Berger, Saint-Louis, Senegal
                [5 ]University Cheikh Anta Diop, Fann, Dakar, Senegal
                [6 ]Centre de Recherche Biomédicale Espoir Pour La Santé, Sor, Saint-Louis, Senegal
                [7 ]The 20|20 Initiative, Pasadena, California, United States of America
                George Washington University School of Medicine and Health Sciences, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: ASA OR SHS YPWF EDA NJ AS. Performed the experiments: ASA OR YPWF DSF EDA. Analyzed the data: ASA OR SHS YPWF EDA NJ AS. Contributed reagents/materials/analysis tools: ASA OR SHS EDA NJ DZ EH AS. Wrote the paper: ASA OR SHS EH AS.

                Article
                PNTD-D-14-00349
                10.1371/journal.pntd.0003060
                4148216
                25166746
                66b60bc2-5e20-4e58-868a-fa014c42ec9a
                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
                : 27 February 2014
                : 18 June 2014
                Page count
                Pages: 13
                Funding
                We would like to thank the 20/20 Initiative and Project-Crevette for initiating the research and for funding our study and travels to Senegal ( www.projet-crevette.org). We would like to thank Ben-Gurion University of the Negev for funding the molecular study and the Tamar Golan Africa Center ( www.africaafrica.org) for supporting ASA. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Agriculture
                Aquaculture
                Shrimp Farming
                Developmental Biology
                Life Cycles
                Parasitic Life Cycles
                Biotechnology
                Ecology
                Ecosystems
                Coastal Ecosystems
                Freshwater Ecology
                Marine Biology
                Fisheries Science
                Parasitology
                Intestinal Parasites

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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