{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T03:11:40Z","timestamp":1791947500506,"version":"4.3.4"},"update-to":[{"DOI":"10.1371\/journal.pntd.0009175","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,4,5]],"date-time":"2021-04-05T00:00:00Z","timestamp":1617580800000}}],"reference-count":33,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2021,3,24]],"date-time":"2021-03-24T00:00:00Z","timestamp":1616544000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R37AI101438"],"award-info":[{"award-number":["R37AI101438"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R37AI101438"],"award-info":[{"award-number":["R37AI101438"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R37AI101438"],"award-info":[{"award-number":["R37AI101438"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R37AI101438"],"award-info":[{"award-number":["R37AI101438"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R37AI101438"],"award-info":[{"award-number":["R37AI101438"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R37AI101438"],"award-info":[{"award-number":["R37AI101438"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004423","name":"World Health Organization","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100004423","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100004423","name":"World Health Organization","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100004423","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100004423","name":"World Health Organization","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100004423","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100004423","name":"World Health Organization","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100004423","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100004423","name":"World Health Organization","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100004423","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100004423","name":"World Health Organization","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100004423","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosntds.org"],"crossmark-restriction":false},"short-container-title":["PLoS Negl Trop Dis"],"abstract":"<jats:sec id=\"sec001\">\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>\n                      We were tasked by the World Health Organization (WHO) to address the following question: What techniques should be used to diagnose\n                      <jats:italic>Schistosoma<\/jats:italic>\n                      infections in snails and in the water in potential transmission sites? Our goal was to review and evaluate the available literature and provide recommendations and insights for the development of WHO\u2019s Guidelines Development Group for schistosomiasis control and elimination.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec id=\"sec002\">\n                    <jats:title>Methodology<\/jats:title>\n                    <jats:p>We searched several databases using strings of search terms, searched bibliographies of pertinent papers, and contacted investigators who have made contributions to this field. Our search covered from 1970 to Sept 2020. All papers were considered in a PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) framework, and retained papers were grouped by technique and subjected to our GRADE (Grading of Recommendations, Assessment, Development and Evaluations) evidence assessment profile determined in consultation with WHO. We also considered issues of sensitivity, specificity, coverage, cost, robustness, support needs, schistosome species discrimination, and relevant detection limits.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec id=\"sec003\">\n                    <jats:title>Principal findings<\/jats:title>\n                    <jats:p>Our PRISMA process began with the perusal of 949 articles, of which 158 were retained for data extraction and evaluation. We identified 25 different techniques and for each applied a GRADE assessment considering limitations, inconsistency, imprecision, indirectness, and publication bias. We also provide advantages and disadvantages for each category of techniques.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec id=\"sec004\">\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Our GRADE analysis returned an assessment of moderate quality of evidence for environmental DNA (eDNA), qPCR and LAMP (Loop-mediated isothermal amplification). No single ideal diagnostic approach has yet been developed, but considerable recent progress has been made. We note a growing trend to use eDNA techniques to permit more efficient and replicable sampling. qPCR-based protocols for follow-up detection offer a versatile, mature, sensitive, and specific platform for diagnosis though centralized facilities will be required to favor standardization. Droplet digital PCR (ddPCR) can play a complementary role if inhibitors are a concern, or more sensitivity or quantification is needed. Snail collection, followed by shedding, is encouraged to provide specimens for sequence verifications of snails or schistosomes. LAMP or other isothermal detection techniques offer the prospect of less expensive and more distributed network of analysis but may face standardization and verification challenges related to actual sequences amplified.<\/jats:p>\n                    <jats:p>Ability to detect schistosome infections in snails or in the water is needed if control and elimination programs hope to succeed. Any diagnostic techniques used need to be regularly verified by the acquisition of DNA sequences to confirm that the detected targets are of the expected species. Further improvements may be necessary to identify the ideal schistosome or snail sequences to target for amplification. More field testing and standardization will be essential for long-term success.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1371\/journal.pntd.0009175","type":"journal-article","created":{"date-parts":[[2021,3,24]],"date-time":"2021-03-24T13:45:53Z","timestamp":1616593553000},"page":"e0009175","update-policy":"https:\/\/doi.org\/10.1371\/journal.pntd.corrections_policy","source":"Crossref","is-referenced-by-count":39,"title":["Detecting and identifying Schistosoma infections in snails and aquatic habitats: A systematic review"],"prefix":"10.1371","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2934-3827","authenticated-orcid":true,"given":"Bishoy","family":"Kamel","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6250-5555","authenticated-orcid":true,"given":"Martina R.","family":"Laidemitt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5073-3753","authenticated-orcid":true,"given":"Lijun","family":"Lu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5312-9495","authenticated-orcid":true,"given":"Caitlin","family":"Babbitt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4396-9896","authenticated-orcid":true,"given":"Ola Liota","family":"Weinbaum","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gerald M.","family":"Mkoji","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2916-9868","authenticated-orcid":true,"given":"Eric S.","family":"Loker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,3,24]]},"reference":[{"key":"pntd.0009175.ref001","first-page":"601","article-title":"Schistosomiasis and soil-transmitted helminthiases: numbers of people treated in 2018","volume":"94","author":"World Health Organization","year":"2019","journal-title":"Wkly Epidemiol Rec"},{"key":"pntd.0009175.ref002","doi-asserted-by":"crossref","first-page":"2253","DOI":"10.1016\/S0140-6736(13)61949-2","article-title":"Human schistosomiasis","volume":"383","author":"DG Colley","year":"2014","journal-title":"Lancet"},{"key":"pntd.0009175.ref003","doi-asserted-by":"crossref","first-page":"2519","DOI":"10.1056\/NEJMoa1812165","article-title":"Schistosomiasis\u2014assessing progress toward the 2020 and 2025 global goals","volume":"381","author":"AK Deol","year":"2019","journal-title":"N Engl J Med"},{"key":"pntd.0009175.ref004","first-page":"1","article-title":"Schistosomiasis","volume":"4","author":"DP McManus","year":"2018","journal-title":"Nat Rev Dis Prim"},{"key":"pntd.0009175.ref005","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pntd.0008098","article-title":"Cost of interventions to control schistosomiasis: a systematic review of the literature","volume":"14","author":"P Salari","year":"2020","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009175.ref006","doi-asserted-by":"crossref","first-page":"e64","DOI":"10.1016\/S1473-3099(16)30535-7","article-title":"A call to strengthen the global strategy against schistosomiasis and soil-transmitted helminthiasis: the time is now","volume":"17","author":"NC Lo","year":"2017","journal-title":"Lancet Infect Dis"},{"key":"pntd.0009175.ref007","first-page":"19","article-title":"It\u2019s time to dispel the myth of \u201casymptomatic\u201d schistosomiasis","volume":"9","author":"CH King","year":"2015","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009175.ref008","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13071-014-0533-3","article-title":"Field-derived Schistosoma mansoni and Biomphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year","volume":"7","author":"MW Mutuku","year":"2014","journal-title":"Parasites and Vectors"},{"key":"pntd.0009175.ref009","article-title":"Elimination of schistosomiasis","author":"WHO Assembly","year":"2012","journal-title":"WHA65.21"},{"key":"pntd.0009175.ref010","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/s40249-016-0215-9","article-title":"Towards interruption of schistosomiasis transmission in sub-Saharan Africa: developing an appropriate environmental surveillance framework to guide and to support \u2019end game\u2019 interventions","volume":"6","author":"JR Stothard","year":"2017","journal-title":"Infect Dis poverty"},{"key":"pntd.0009175.ref011","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pntd.0003186","article-title":"Sources and distribution of surface water fecal contamination and prevalence of schistosomiasis in a Brazilian village.","volume":"8","author":"R Ponce-Terashima","year":"2014","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009175.ref012","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1186\/1756-3305-7-288","article-title":"Schistosoma haematobium detection in snails by DraI PCR and Sh110\/Sm-Sl PCR: further evidence of the interruption of schistosomiasis transmission in Morocco.","volume":"7","author":"F Amarir","year":"2014","journal-title":"Parasites and Vectors"},{"key":"pntd.0009175.ref013","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1128\/CMR.00137-14","article-title":"Advances in the diagnosis of human schistosomiasis","volume":"28","author":"Gobert GN Weerakoon KGAD","year":"2015","journal-title":"Clin Microbiol Rev"},{"key":"pntd.0009175.ref014","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/j.actatropica.2019.04.030","article-title":"The epidemiological status of schistosomiasis in P. R. China after the World Bank Loan Project, 2002\u20132017","volume":"195","author":"LJ Zhang","year":"2019","journal-title":"Acta Trop"},{"key":"pntd.0009175.ref015","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1136\/bmj.b2535","article-title":"Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement","volume":"339","author":"D Moher","year":"2009","journal-title":"BMJ"},{"key":"pntd.0009175.ref016","article-title":"Jabref reference manager","author":"M Alver","year":"2003"},{"key":"pntd.0009175.ref017","doi-asserted-by":"crossref","first-page":"924","DOI":"10.1136\/bmj.39489.470347.AD","article-title":"GRADE: an emerging consensus on rating quality of evidence and strength of recommendations","volume":"336","author":"GH Guyatt","year":"2008","journal-title":"BMJ"},{"key":"pntd.0009175.ref018","first-page":"1","article-title":"Schistosoma mansoni vector snails in Antigua and Montserrat, with snail-related considerations pertinent to a declaration of elimination of human schistosomiasis","author":"MR Laidemitt","year":"2020","journal-title":"Am J Trop Med Hyg"},{"key":"pntd.0009175.ref019","first-page":"231","article-title":"Mathematical modeling as an aid in understanding transmission and control of Schistosoma japonicum in hilly and mountainous regions of China","volume":"23","author":"RC Spear","year":"2011","journal-title":"Chinese J Schistosomiasis Control"},{"key":"pntd.0009175.ref020","doi-asserted-by":"crossref","first-page":"8931","DOI":"10.1073\/pnas.1815046116","article-title":"Environmental DNA for improved detection and environmental surveillance of schistosomiasis","volume":"116","author":"ME Sengupta","year":"2019","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pntd.0009175.ref021","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.ijid.2018.08.018","article-title":"Usefulness of environmental DNA for detecting Schistosoma mansoni occurrence sites in Madagascar","volume":"76","author":"MO Sato","year":"2018","journal-title":"Int J Infect Dis"},{"key":"pntd.0009175.ref022","first-page":"1","article-title":"Detection of Schistosoma japonicum and Oncomelania hupensis quadrasi environmental DNA and its potential utility to schistosomiasis japonica surveillance in the Philippines","volume":"14","author":"RJC Fornillos","year":"2019","journal-title":"PLoS One"},{"key":"pntd.0009175.ref023","article-title":"Piloting an integrated approach for estimation of environmental risk of Schistosoma haematobium infections in pre-school-aged children and their mothers at Barombi Kotto, Cameroon","volume":"212","author":"MT Eyre","year":"2020","journal-title":"Acta Trop"},{"key":"pntd.0009175.ref024","first-page":"1","article-title":"Schistosoma species detection by environmental DNA assays in African freshwaters","volume":"14","author":"H Alzaylaee","year":"2020","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009175.ref025","article-title":"Pitfalls during in silico prediction of primer specificity for eDNA surveillance","volume":"11","author":"KYK So","year":"2020","journal-title":"Ecosphere"},{"key":"pntd.0009175.ref026","doi-asserted-by":"crossref","DOI":"10.1016\/j.actatropica.2019.105326","article-title":"Report of high prevalence of schistosome infection in Biomphalaria snails from a geographic area with no previous prevalence of human schistosomiasis in Nigeria","volume":"210","author":"OC Okeke","year":"2020","journal-title":"Acta Trop"},{"key":"pntd.0009175.ref027","doi-asserted-by":"crossref","DOI":"10.1016\/j.actatropica.2019.105289","article-title":"Malacological survey to identify transmission sites for intestinal schistosomiasis on Ijinga Island, Mwanza, north-western Tanzania","volume":"203","author":"A Fuss","year":"2020","journal-title":"Acta Trop"},{"key":"pntd.0009175.ref028","doi-asserted-by":"crossref","DOI":"10.1002\/wat2.1491","article-title":"Monitoring schistosomiasis and sanitation interventions\u2014the potential of environmental DNA","volume":"8","author":"TS Champion","year":"2021","journal-title":"WIREs Water"},{"key":"pntd.0009175.ref029","doi-asserted-by":"crossref","first-page":"1401","DOI":"10.1016\/j.ijpara.2007.04.014","article-title":"Making the most of mitochondrial genomes\u2014markers for phylogeny, molecular ecology and barcodes in Schistosoma (Platyhelminthes: Digenea)","volume":"37","author":"MZ Zarowiecki","year":"2007","journal-title":"Int J Parasitol"},{"key":"pntd.0009175.ref030","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pntd.0000422","article-title":"Diagnosing schistosomiasis by detection of cell-free parasite DNA in human plasma","volume":"3","author":"D Wichmann","year":"2009","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009175.ref031","doi-asserted-by":"crossref","DOI":"10.1016\/j.actatropica.2020.105716","article-title":"Comparing PCR techniques against conventional cercarial shedding methods for detecting Schistosoma mansoni infection in Biomphalaria snails","volume":"212","author":"E Joof","year":"2020","journal-title":"Acta Trop"},{"key":"pntd.0009175.ref032","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.molbiopara.2016.11.005","article-title":"WormBase ParaSite \u2212 a comprehensive resource for helminth genomics","volume":"215","author":"KL Howe","year":"2017","journal-title":"Mol Biochem Parasitol"},{"key":"pntd.0009175.ref033","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1890\/14-1530.1","article-title":"Development and application of an eDNA method to detect and quantify a pathogenic parasite in aquatic ecosystems","volume":"25","author":"JR Huver","year":"2015","journal-title":"Ecol Appl"}],"updated-by":[{"DOI":"10.1371\/journal.pntd.0009175","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,4,5]],"date-time":"2021-04-05T00:00:00Z","timestamp":1617580800000}}],"container-title":["PLOS Neglected Tropical Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pntd.0009175","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,4,5]],"date-time":"2021-04-05T13:45:52Z","timestamp":1617630352000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pntd.0009175"}},"subtitle":[],"editor":[{"given":"Ricardo Toshio","family":"Fujiwara","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2021,3,24]]},"references-count":33,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2021,3,24]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pntd.0009175","relation":{},"ISSN":["1935-2735"],"issn-type":[{"value":"1935-2735","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,24]]}}}