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      Snail-Related Contributions from the Schistosomiasis Consortium for Operational Research and Evaluation Program Including Xenomonitoring, Focal Mollusciciding, Biological Control, and Modeling

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          Abstract.

          The Schistosomiasis Consortium for Operational Research and Evaluation (SCORE) was created in 2008 to answer questions of importance to program managers working to reduce the burden of schistosomiasis in Africa. In the past, intermediate host snail monitoring and control was an important part of integrated schistosomiasis control. However, in Africa, efforts to control snails have declined dramatically over the last 30 years. A resurgence of interest in the control of snails has been prompted by the realization, backed by a World Health Assembly resolution (WHA65.21), that mass drug administration alone may be insufficient to achieve schistosomiasis elimination. SCORE has supported work on snail identification and mapping and investigated how xenomonitoring techniques can aid in the identification of infected snails and thereby identify potential transmission areas. Focal mollusciciding with niclosamide was undertaken in Zanzibar and Côte d’Ivoire as a part of elimination studies. Two studies involving biological control of snails were conducted: one explored the association of freshwater riverine prawns and snail hosts in Côte d’Ivoire and the other assessed the current distribution of Procambarus clarkii, the invasive Louisiana red swamp crayfish, in Kenya and its association with snail hosts and schistosomiasis transmission. SCORE also supported modeling studies on the importance of snail control in achieving elimination and a meta-analysis of the impact of molluscicide-based snail control programs on human schistosomiasis prevalence and incidence. SCORE’s snail control studies contributed to increased investment in building capacity, and specimens collected during SCORE research deposited in the Schistosomiasis Collections at the Natural History Museum (SCAN) will provide a valuable resource for the years to come.

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          Most cited references59

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          Comparative genomics of the major parasitic worms

          Parasitic nematodes (roundworms) and platyhelminths (flatworms) cause debilitating chronic infections of humans and animals, decimate crop production and are a major impediment to socioeconomic development. Here we report a broad comparative study of 81 genomes of parasitic and non-parasitic worms. We have identified gene family births and hundreds of expanded gene families at key nodes in the phylogeny that are relevant to parasitism. Examples include gene families that modulate host immune responses, enable parasite migration though host tissues or allow the parasite to feed. We reveal extensive lineage-specific differences in core metabolism and protein families historically targeted for drug development. From an in silico screen, we have identified and prioritized new potential drug targets and compounds for testing. This comparative genomics resource provides a much-needed boost for the research community to understand and combat parasitic worms.
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            Schistosomiasis elimination: lessons from the past guide the future.

            Schistosomiasis is a major neglected tropical disease, with more than 200 million people infected and close to 800 million at risk. The disease burden is estimated to exceed 70 million disability-adjusted life-years. The anthelmintic drug praziquantel is highly effective in killing adult schistosome worms, but it is unable to kill developing schistosomes and so does not prevent reinfection. As a result, current praziquantel-based control programmes in Asia and sub-Saharan Africa are not effective or sustainable in the long term. The control of neglected tropical diseases, including schistosomiasis, is a funding priority for several donor agencies, with over US$350 million committed until 2013. Here we put forward an argument that donor funds would be more effectively spent on the development of a multi-faceted, integrated control programme, which would have a greater and longer lasting effect on disease transmission than the current chemotherapy-based programmes. The development of a transmission-blocking vaccine is also of great importance. A multi-faceted integrated control programme that incorporates a vaccine, even if only partly effective, has the potential to eliminate schistosomiasis. This integrated-approach model has the potential to improve the health of a billion of the world's poorest people and its effect cannot be underestimated. Copyright © 2010 Elsevier Ltd. All rights reserved.
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              Reduced transmission of human schistosomiasis after restoration of a native river prawn that preys on the snail intermediate host.

              Eliminating human parasitic disease often requires interrupting complex transmission pathways. Even when drugs to treat people are available, disease control can be difficult if the parasite can persist in nonhuman hosts. Here, we show that restoration of a natural predator of a parasite's intermediate hosts may enhance drug-based schistosomiasis control. Our study site was the Senegal River Basin, where villagers suffered a massive outbreak and persistent epidemic after the 1986 completion of the Diama Dam. The dam blocked the annual migration of native river prawns (Macrobrachium vollenhoveni) that are voracious predators of the snail intermediate hosts for schistosomiasis. We tested schistosomiasis control by reintroduced river prawns in a before-after-control-impact field experiment that tracked parasitism in snails and people at two matched villages after prawns were stocked at one village's river access point. The abundance of infected snails was 80% lower at that village, presumably because prawn predation reduced the abundance and average life span of latently infected snails. As expected from a reduction in infected snails, human schistosomiasis prevalence was 18 ± 5% lower and egg burden was 50 ± 8% lower at the prawn-stocking village compared with the control village. In a mathematical model of the system, stocking prawns, coupled with infrequent mass drug treatment, eliminates schistosomiasis from high-transmission sites. We conclude that restoring river prawns could be a novel contribution to controlling, or eliminating, schistosomiasis.
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                Author and article information

                Journal
                Am J Trop Med Hyg
                Am. J. Trop. Med. Hyg
                tpmd
                tropmed
                The American Journal of Tropical Medicine and Hygiene
                The American Society of Tropical Medicine and Hygiene
                0002-9637
                1476-1645
                July 2020
                12 May 2020
                12 May 2020
                : 103
                : 1 Suppl
                : 66-79
                Affiliations
                [1 ]Wolfson Wellcome Biomedical Laboratories, Department of Life Sciences, Natural History Museum, London, United Kingdom;
                [2 ]Public Health Laboratory - Ivo de Carneri, Pemba, United Republic of Tanzania;
                [3 ]Unité de Formation et de Recherche Biosciences, Université Félix Houphouët-Boigny, Abidjan, Côte d’Ivoire;
                [4 ]Centre Suisse de Recherches Scientifiques en Côte d’Ivoire, Abidjan, Côte d’Ivoire;
                [5 ]Department of Biology, University of New Mexico, Albuquerque, New Mexico;
                [6 ]Neglected Tropical Disease Unit, Unguja, Ministry of Health, Zanzibar, United Republic of Tanzania;
                [7 ]School of Biosciences, Cardiff University, Cardiff, United Kingdom;
                [8 ]National Institute of Medical Research (NIMR) Mwanza Centre, Mwanza, United Republic of Tanzania;
                [9 ]Réseau International Schistosomoses, Environnement, Aménagement et Lutte (RISEAL-Niger), Niamey, Niger;
                [10 ]Center for Biotechnology Research and Development, Kenya Medical Research Institute (KEMRI), Nairobi, Kenya;
                [11 ]Department of Ecology, Evolution and Marine Biology and Marine Science Institute, University of California, Santa Barbara, California;
                [12 ]Swiss Tropical and Public Health Institute, Basel, Switzerland;
                [13 ]University of Basel, Basel, Switzerland
                Author notes
                [* ]Address correspondence to Fiona Allan, Wolfson Wellcome Biomedical Laboratories, Department of Life Sciences, Natural History Museum, Cromwell Rd., SW7 5BD, London, United Kingdom. E-mail: f.allan@ 123456nhm.ac.uk

                Disclosure: The authors declare that the research summarized herein was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

                Financial support: This study received financial support from the University of Georgia Research Foundation Inc., which is funded by the Bill & Melinda Gates Foundation for the Schistosomiasis Consortium for Operational Research and Evaluation (SCORE) (prime award no. 50816). The WHO donated praziquantel to cover biannual MDA from 2012 to 2017 in Zanzibar, the Schistosomiasis Control Initiative funded the treatment implementation costs, and Bayer S.A.S. donated 3 MT Bayluscide for snail control. F. A. and M. R. were financially supported by the Wellcome Trust (SCAN Project 104958/Z/14/Z). S. K. was financially supported by SCORE sub-award no. RR374-053/4893196 and a direct grant from the Bill & Melinda Gates Foundation (Investment ID: OPP1191423). E. S. L., G. M. M., and B. H. also acknowledge the support from NIH grant R37AI101438.

                Authors’ addresses: Fiona Allan, Bonnie L. Webster, Anouk N Gouvras, Aidan M. Emery, Tom Pennance, Muriel Rabone, and David Rollinson, Wolfson Wellcome Biomedical Laboratories, Department of Life Sciences, Natural History Museum, London, United Kingdom, E-mails: f.allan@ 123456nhm.ac.uk , b.webster@ 123456nhm.ac.uk , anouk.gouvras@ 123456eliminateschisto.org , a.emery@ 123456nhm.ac.uk , t.pennance@ 123456nhm.ac.uk , m.rabone@ 123456nhm.ac.uk , and d.rollinson@ 123456nhm.ac.uk . Shaali Ame, Public Health Laboratory - Ivo de Carneri, Pemba, United Republic of Tanzania, E-mail: shaaliame@ 123456yahoo.com . Yves-Nathan T. Tian-Bi, Nana R. Diakité, Eliezer K. N’Goran, Unité de Formation et de Recherche Biosciences, Université Félix Houphouët-Boigny, Abidjan 22, Côte d’Ivoire, E-mails: nathantianbi@ 123456gmail.com , diaknarose@ 123456yahoo.fr , and eliezerngoran@ 123456yahoo.fr . Bruce V. Hofkin and Eric S. Loker, Department of Biology, University of New Mexico, Albuquerque, New Mexico, E-mails: brunoh@ 123456unm.edu and esloker@ 123456unm.edu . Gerald M. Mkoji, Center for Biotechnology Research and Development, Kenya Medical Research Institute (KEMRI), Nairobi, Kenya, E-mail: gmkoji5@ 123456gmail.com . John P. McLaughlin and Armand M. Kuris, Department of Ecology, Evolution and Marine Biology and Marine Science Institute, University of California, Santa Barbara, CA, E-mails: mclaughlin@ 123456lifesci.ucsb.edu and kuris@ 123456lifesci.ucsb.edu . Safari Kinung’hi, National Institute for Medical Research, Mwanza Research Centre, Mwanza, Tanzania, E-mail: kinunghi_csm@ 123456hotmail.com . Amina Hamidou, Réseau International Schistosomiases, Environnement, Aménagement et Lutte (RISEAL NIGER), Niamey, Niger, E-mail: aminamadou@ 123456yahoo.fr . Stefanie Knopp, Swiss Tropical and Public Health Institute, Basel, Switzerland, E-mail: s.knopp@ 123456swisstph.ch . Fatma M. Kabole, Iddi Simba Khamis, Neglected Tropical Disease Unit, Zanzibar Ministry of Health, Unguja, United Republic of Tanzania, E-mails: fatmaepi@ 123456yahoo.com and mwinsimba@ 123456gmail.com .

                Article
                tpmd190831
                10.4269/ajtmh.19-0831
                7351297
                32400353
                1c15e15a-c89d-4af6-936d-1419b3cccda4
                © The American Society of Tropical Medicine and Hygiene

                This is an open-access article distributed under the terms of the Creative Commons Attribution (CC-BY) License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 06 November 2019
                : 14 February 2020
                Page count
                Pages: 14
                Categories
                Articles

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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