{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,23]],"date-time":"2026-06-23T02:55:23Z","timestamp":1782183323832,"version":"3.54.5"},"reference-count":52,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2022,6,4]],"date-time":"2022-06-04T00:00:00Z","timestamp":1654300800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Higgins Lake Swimmer\u2019s Itch Organization"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>A novel schistosome from Planorbella snails currently known as avian schistosomatid sp. C (ASC) was recently described as being capable of causing the papules associated with swimmer\u2019s itch. We conducted a paired study with 24 human volunteers, exposing each of their forearms to five drops of water containing cercariae of ASC or Trichobilharzia stagnicolae, and examined the skin for papules 1\u20133 days later. A mixed effects model showed that only the parasite species significantly affected the number of papules, while prior experimental exposure, swimming history, and swimmer\u2019s itch experience did not. The total number of papules produced by the two species were very different: ASC produced a total of 2 papules from the 298 cercariae used, compared to 49 papules from 160 T. stagnicolae cercariae, a difference factor of more than 43X, which was comparable to the odds ratio of 45.5 computed using the statistical model. A well-known agent of swimmer\u2019s itch, T. stagnicolae, is able to penetrate human skin more frequently than ASC, likely meaning that ASC is only a minor cause of swimmer\u2019s itch where T. stagnicolae is present. We also completed limited experiments that compared the cercarial behavior of the two species in vitro and in situ. A known stimulant of schistosome cercarial penetration, \u03b1-linolenic acid, did not stimulate ASC cercariae to initiate penetration-associated behaviors as frequently as T. stagnicolae. However, when placed on esophageal tissue of the known vertebrate host for ASC, Canada goose (Branta canadensis), ASC cercariae were observed penetrating the esophageal epithelium quickly, whereas T. stagnicolae cercariae did not exhibit any penetration behaviors.<\/jats:p>","DOI":"10.3390\/pathogens11060651","type":"journal-article","created":{"date-parts":[[2022,6,4]],"date-time":"2022-06-04T09:42:32Z","timestamp":1654335752000},"page":"651","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["The Tails of Two Avian Schistosomes: Paired Exposure Study Demonstrates Trichobilharzia stagnicolae Penetrates Human Skin More Readily than a Novel Avian Schistosome from Planorbella"],"prefix":"10.3390","volume":"11","author":[{"given":"Nathaniel J.","family":"Anderson","sequence":"first","affiliation":[{"name":"Department of Biology, Calvin University, Grand Rapids, MI 49546, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Curtis L.","family":"Blankespoor","sequence":"additional","affiliation":[{"name":"Science Department, Jackson College, Jackson, MI 49201, USA"},{"name":"University of Michigan Biological Station, Pellston, MI 49769, USA"},{"name":"Swimmer\u2019s Itch Solutions LLC, Adrian, MI 49221, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5660-9227","authenticated-orcid":false,"given":"Randall J.","family":"DeJong","sequence":"additional","affiliation":[{"name":"Department of Biology, Calvin University, Grand Rapids, MI 49546, USA"},{"name":"University of Michigan Biological Station, Pellston, MI 49769, USA"},{"name":"Swimmer\u2019s Itch Solutions LLC, Adrian, MI 49221, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,6,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1001\/jama.1928.02690400023010","article-title":"Schistosome Dermatitis in the United States (Michigan)","volume":"90","author":"Cort","year":"1928","journal-title":"JAMA J. Am. Med. Assoc."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1128\/CMR.00043-14","article-title":"Avian Schistosomes and Outbreaks of Cercarial Dermatitis","volume":"28","author":"Brant","year":"2015","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Loker, E.S., DeJong, R.J., and Brant, S.V. (2022). Scratching the Itch: Updated Perspectives on the Schistosomes Responsible for Swimmer\u2019s Itch Around the World. Pathogens, 11.","DOI":"10.3390\/pathogens11050587"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1186\/s12940-018-0417-7","article-title":"Swimmer\u2019s Itch in Canada: A Look at the Past and a Survey of the Present to Plan for the Future","volume":"17","author":"Gordy","year":"2018","journal-title":"Environ. Health"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1645\/20-74","article-title":"Evidence of a Putative Novel Species of Avian Schistosome Infecting Planorbella trivolvis","volume":"107","author":"McPhail","year":"2021","journal-title":"J. Parasitol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1016\/j.ijppaw.2019.04.006","article-title":"Species-Specific QPCR Assays Allow for High-Resolution Population Assessment of Four Species Avian Schistosome That Cause Swimmer\u2019s Itch in Recreational Lakes","volume":"9","author":"Rudko","year":"2019","journal-title":"Int. J. Parasitol. Parasites Wildl."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1645\/GE-3336.1","article-title":"Ubiquitous Variability in the Prevalence of Trichobilharzia stagnicolae (Schistosomatidae) Infecting Stagnicola emarginata in Three Northern Michigan Lakes","volume":"92","author":"Coady","year":"2006","journal-title":"J. Parasitol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1093\/oxfordjournals.aje.a118225","article-title":"Studies on Schistosome Dermatitis. III. Observations on the Behavior of the Dermatitis-Producing Schistosome Cercariae","volume":"23","author":"Cort","year":"1936","journal-title":"Am. J. Epidemiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1093\/oxfordjournals.aje.a119204","article-title":"Studies on Schistosome Dermatitis: X. Distribution and Epidemiology in Michigan","volume":"47","author":"McMullen","year":"1948","journal-title":"Am. J. Epidemiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"164","DOI":"10.2307\/3273094","article-title":"The Development of the Sporocysts of a Schistosome, Cercaria stagnicolae Talbot, 1936","volume":"29","author":"Cort","year":"1943","journal-title":"J. Parasitol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"725","DOI":"10.4269\/ajtmh.1941.s1-21.725","article-title":"The Distribution and Control of Schistosome Dermatitis in Wisconsin and Michigan","volume":"s1-21","author":"McMullen","year":"1941","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_12","first-page":"134","article-title":"The Penetration Of Dermatitis-Producing Schistosome Cercariae","volume":"49","author":"Olivier","year":"1949","journal-title":"Am. J. Hyg."},{"key":"ref_13","first-page":"290","article-title":"Schistosome Dermatitis, a Sensitization Phenomenon","volume":"49","author":"Olivier","year":"1949","journal-title":"Am. J. Hyg."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3881","DOI":"10.1007\/s00436-018-6095-0","article-title":"Cercarial Dermatitis: A Systematic Follow-up Study of Human Cases with Implications for Diagnostics","volume":"117","year":"2018","journal-title":"Parasitol. Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1007\/s00436-009-1516-8","article-title":"Penetration of Cercariae into the Living Human Skin: Schistosoma mansoni vs. Trichobilharzia szidati","volume":"105","author":"Haas","year":"2009","journal-title":"Parasitol. Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"568","DOI":"10.2307\/3282138","article-title":"Host Identification by Schistosoma japonicum Cercariae","volume":"73","author":"Haas","year":"1987","journal-title":"J. Parasitol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1007\/s00436-007-0807-1","article-title":"Chemical Attractants of Human Skin for Swimming Schistosoma mansoni Cercariae","volume":"102","author":"Haeberlein","year":"2008","journal-title":"Parasitol. Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1007\/BF00925346","article-title":"Characterization of Chemical Stimuli for the Penetration of Schistosoma mansoni Cercariae","volume":"66","author":"Haas","year":"1982","journal-title":"Z. F\u00fcr Parasitenkd."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1007\/s004360050489","article-title":"Invasion of the Vertebrate Skin by Cercariae of Trichobilharzia ocellata: Penetration Processes and Stimulating Host Signals","volume":"84","author":"Haas","year":"1998","journal-title":"Parasitol. Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1007\/s00436-002-0684-6","article-title":"Is There a Potential Danger of swimmer\u2019s Itch in Poland?","volume":"89","year":"2002","journal-title":"Parasitol. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1017\/S0031182000080136","article-title":"Host-Finding in Trichobilharzia ocellata Cercariae: Swimming and Attachment to the Host","volume":"96","author":"Feiler","year":"1988","journal-title":"Parasitology"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1017\/S0031182000080148","article-title":"Trichobilharzia ocellata: Chemical Stimuli of Duck Skin for Cercarial Attachment","volume":"96","author":"Feiler","year":"1988","journal-title":"Parasitology"},{"key":"ref_23","unstructured":"Daniell, D.L. (1978). Biology and Host-Parasite Relationships of Gigantobilharzia huronensis (Trematoda: Schistosomatidae), Iowa State University."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.1139\/z73-148","article-title":"Migration and Development of Trichobilharzia ocellata (Trematoda: Schistosomatidae) in Its Duck Hosts","volume":"51","author":"Bourns","year":"1973","journal-title":"Can. J. Zool."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1163\/002829684X00236","article-title":"Maintenance of the Life Cycle of Trichobilharzia ocellata Via the Duck Anas platyrhynchos and the Pond Snail Lymnaea stagnalis","volume":"34","author":"Meuleman","year":"1983","journal-title":"Neth. J. Zool."},{"key":"ref_26","first-page":"128","article-title":"Studies on Schistosome Dermatitis. IX. The Life Cycles of Three Dermatitis-producing Schistosomes from Birds and a Discussion of the Subfamily Bilharziellinae (Trematoda: Schistosomatidae)","volume":"42","author":"McMullen","year":"1945","journal-title":"Am. J. Hyg."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1007\/BF00928190","article-title":"Finding and Recognition of the Bovine Host by the Cercariae of Schistosoma spindale","volume":"76","author":"Haas","year":"1990","journal-title":"Parasitol. Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4207","DOI":"10.1128\/AEM.00750-15","article-title":"Real-Time PCR and Sequencing Assays for Rapid Detection and Identification of Avian Schistosomes in Environmental Samples","volume":"81","author":"Jothikumar","year":"2015","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1007\/s10393-018-1362-1","article-title":"Use of qPCR-Based Cercariometry to Assess Swimmer\u2019s Itch in Recreational Lakes","volume":"15","author":"Rudko","year":"2018","journal-title":"EcoHealth"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Rudko, S.P., Reimink, R.L., Peter, B., White, J., and Hanington, P.C. (2020). Democratizing Water Monitoring: Implementation of a Community-Based qPCR Monitoring Program for Recreational Water Hazards. PLoS ONE, 15.","DOI":"10.1101\/2020.02.13.947259"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/j.ijpara.2021.11.010","article-title":"Non-Resident Definitive Host Presence Is Sufficient to Sustain Avian Schistosome Populations","volume":"52","author":"Rudko","year":"2022","journal-title":"Int. J. Parasitol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1111\/j.1600-0587.2013.07868.x","article-title":"Evaluating the Role of Regional and Local Processes in Structuring a Larval Trematode Metacommunity of Helisoma trivolvis","volume":"36","author":"Richgels","year":"2013","journal-title":"Ecography"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"289","DOI":"10.2307\/2426001","article-title":"Trematode Prevalence and the Population Dynamics of Freshwater Pond Snails","volume":"120","author":"Brown","year":"1988","journal-title":"Am. Midl. Nat."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1126\/science.53.1367.226","article-title":"Sex in the Trematode Family Schistosomid\u00e6","volume":"53","author":"Cort","year":"1921","journal-title":"Science"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"19","DOI":"10.2307\/3272156","article-title":"A Study of Larval Trematode Infections in Helisoma campanulatum smithii (Baker) in the Douglas Lake Region, Michigan","volume":"25","author":"Cort","year":"1939","journal-title":"J. Parasitol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1017\/S0031182016002547","article-title":"The Distribution of Echinostome Parasites in Ponds and Implications for Larval Anuran Survival","volume":"144","author":"Marino","year":"2017","journal-title":"Parasitol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1654\/4227.1","article-title":"Survey of Seasonal Trematode Infections in Helisoma trivolvis (Gastropoda) from Lentic Ecosystems in New Jersey, U.S.A","volume":"74","author":"Klockars","year":"2007","journal-title":"Comp. Parasitol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"553","DOI":"10.2307\/3282905","article-title":"A Mark-Recapture Study of Trematode Parasitism in Overwintered Helisoma anceps (Pulmonata), with Special Reference to Halipegus occidualis (Hemiuridae)","volume":"75","author":"Goater","year":"1989","journal-title":"J. Parasitol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"246","DOI":"10.2307\/3283091","article-title":"Infra- and Component Community Dynamics in the Pulmonate Snail Helisoma anceps, with Special Emphasis on the Hemiurid Trematode Halipegus occidualis","volume":"77","author":"Williams","year":"1991","journal-title":"J. Parasitol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"540","DOI":"10.2307\/3283157","article-title":"The Component Community Structure of Larval Trematodes in the Pulmonate Snail Helisoma anceps","volume":"77","author":"Fernandez","year":"1991","journal-title":"J. Parasitol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.1645\/GE-1184.1","article-title":"Long-Term Analysis of Charlie\u2019s Pond: Fecundity and Trematode Communities of Helisoma anceps","volume":"93","author":"Negovetich","year":"2007","journal-title":"J. Parasitol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"992","DOI":"10.1645\/GE-1144R.1","article-title":"Environmental Factors Influencing Community Composition of Gastropods and Their Trematode Parasites in Southern Ontario","volume":"93","author":"Koprivnikar","year":"2007","journal-title":"J. Parasitol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1654\/4233.1","article-title":"Seasonal Prevalence of Ribeiroia ondatrae in One Population of Planorbella trivolvis (=Helisoma trivolvis), Including Notes on the Larval Trematode Component Community","volume":"74","author":"Peterson","year":"2007","journal-title":"Comp. Parasitol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"402","DOI":"10.2307\/2420782","article-title":"Life History of Spirorchis elephantis (Cort, 1917), a New Blood Fluke from Chrysemys picta","volume":"25","author":"Wall","year":"1941","journal-title":"Am. Midl. Nat."},{"key":"ref_45","unstructured":"Michigan DNR (2022, April 20). Canada Goose Smart Brochure, Available online: https:\/\/www.michigan.gov\/-\/media\/Project\/Websites\/dnr\/Documents\/WLD\/Goose\/canada_goose_smart_brochure_ada.pdf?rev=bc9f1779ea1740349f8c69bc8d088e99."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"165","DOI":"10.2307\/3284550","article-title":"An Apparatus for Individually Isolating Large Numbers of Snails","volume":"84","author":"Blankespoor","year":"1998","journal-title":"J. Parasitol."},{"key":"ref_47","first-page":"157","article-title":"Prevalence of Larval Trematodes in Helisoma trivolvis (Gastropoda) from a Farm Pond in Northampton County, Pennsylvania with Special Emphasis on Echinostoma trivolvis (Trematoda) Cercariae","volume":"64","author":"Schmidt","year":"1997","journal-title":"J. Helminthol. Soc. Wash."},{"key":"ref_48","unstructured":"Collins, J., Newmark, P., Williams, D., and Bennett, J.B. (2022, April 14). Artificial Pond Water: For the Cultivation of Biomphalaria, Bulinus, and Oncomelania Species. Available online: https:\/\/www.afbr-bri.org\/schistosomiasis\/standard-operating-procedures\/artificial-pond-water\/."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1016\/S0166-6851(97)00176-X","article-title":"Phylogenetic Analysis of the Monogenea and Their Relationships with Digenea and Eucestoda Inferred from 28S rDNA Sequences","volume":"6","author":"Mollaret","year":"1997","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_50","first-page":"294","article-title":"DNA Primers for Amplification of Mitochondrial Cytochrome c Oxidase Subunit I from Diverse Metazoan Invertebrates","volume":"3","author":"Folmer","year":"1994","journal-title":"Mol. Mar. Biol. Biotechnol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"378","DOI":"10.32614\/RJ-2017-066","article-title":"glmmTMB Balances Speed and Flexibility among Packages for Zero-Inflated Generalized Linear Mixed Modeling","volume":"9","author":"Brooks","year":"2017","journal-title":"R J."},{"key":"ref_52","unstructured":"R Core Team (2021). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, R Core Team."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/6\/651\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:24:36Z","timestamp":1760138676000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/6\/651"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,6,4]]},"references-count":52,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2022,6]]}},"alternative-id":["pathogens11060651"],"URL":"https:\/\/doi.org\/10.3390\/pathogens11060651","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,6,4]]}}}