Abstract
Human cercarial dermatitis is a parasitic disease that causes an allergic reaction in the skin (swimmer’s itch) as a consequence of contact with cercariae of bird schistosomes present in water, mainly of the genus Trichobilharzia Skrjabin et Zakarow, 1920. The main objective of the study was to confirm the presence of the zoonotic disease agent following reports of human infections in recreational water in Slovakia. We identified two species of freshwater snails at Košice Lake, Radix auricularia (Linnaeus, 1758) and Physa acuta (Draparnaud, 1805). Trematode infections were observed only in R. auricularia. Of the 62 snails collected, 11 (17.7%) were infected with 5 different species of larval stages of trematodes. The blood fluke Trichobilharzia franki was found in 2 (3.2%) of the examined snails. The present record provides the first evidence that T. franki from the pulmonate snail R. auricularia represents a source of human cercarial dermatitis in recreational water in Slovakia. Our finding complements the easternmost records of both swimmer’s itch and the confirmed occurrence of a bird schistosome in a waterbody in Europe. The present work suggests that the health risks associated with trichobilharziasis need to be further studied by detailed monitoring of the occurrence of the major causative agent of human cercarial dermatitis, T. franki.
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References
Aldhoun JA, Podhorský M, Holická M, Horák P (2012) Bird schistosomes in planorbid snails in the Czech Republic. Parasitol Int 61:250–259. https://doi.org/10.1016/j.parint.2011.10.006
Balůsek J, Vojtek J (1973) Contribution to the knowledge of our cercariae. Folia Fac Sci Nat Univ Purkyn Brun 14:3–119 (In Czech)
Brant SV, Loker ES (2013) Discovery-based studies of schistosome diversity stimulate new hypotheses about parasite biology. Trends Parasitol 29:449–459. https://doi.org/10.1016/j.pt.2013.06.004
Caron Y, Cabaraux A, Marechal F, Losson B (2017) Swimmer’s itch in Belgium: first recorded outbreaks, molecular identification of the parasite species and intermediate hosts. Vector Borne Zoonotic Dis 17:190–194. https://doi.org/10.1089/vbz.2016.2034
Chamot E, Toscani L, Rougemont A (1998) Public health importance and risk factors for cercarial dermatitis associated with swimming in Lake Leman at Geneva, Switzerland. Epidemiol Infect 120:305–314. https://doi.org/10.1017/s0950268898008826
Chrisanfova GG, Lopatkin AA, Mishchenkov VA, Kheidorova EE, Dorozhenkova TE, Zhukova TV, Ryskova AP, Semyenova SK (2009) Genetic variability of bird schistosomes (class Trematoda, family Schistosomatidae) of Naroch Lake: identification of a new species in the Trichobilharzia ocellata group. Dokl Biochem Biophys 428:268–272. https://doi.org/10.1134/s1607672909050123
Cichy A, Faltýnková A, Żbikowska E (2011) Cercariae (Trematoda, Digenea) in European freshwater snails – a checklist of records from over one hundred years. Folia Malacol 19:165–189. https://doi.org/10.2478/v10125-011-0023-6
De Liberato C, Berrilli F, Bossù T, Magliano A, Montalbano Di Filippo M, Di Cave D, Sigismondi M, Cannavacciuolo A, Scaramozzino P (2019) Outbreak of swimmer’s itch in Central Italy: description, causative agent and preventive measures. Zoonoses Public Health 66:377–381. https://doi.org/10.1111/zph.12570
Dillon RT (2004) The ecology of freshwater molluscs. Cambridge University Press, Cambridge 509 pp.
Faltýnková A, Haas W (2006) Larval trematodes in freshwater molluscs from the Elbe to Danube rivers (Southeast Germany): before and today. Parasitol Res 99:572–582. https://doi.org/10.1007/s00436-006-0197-9
Faltýnková A, Literák I (2002) Cercariae of trematodes from Bythinella austriaca (Frauenfeld, 1857) agg. (Gastropoda, Prosobranchia). Acta Parasitol 47:196–204
Faltýnková A, Našincová V, Kablásková L (2007) Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gatropoda, Pulmonata) in Central Europe: a survey of species and key to their identification. Parasite 14:39–51. https://doi.org/10.1051/parasite/2007141039
Faltýnková A, Našincová V, Kablásková L (2008) Larval trematodes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in Central Europe: a survey of species and key to their identification. Syst Parasitol 69:155–178. https://doi.org/10.1007/s11230-007-9127-1
Faltýnková A, Sures B, Kostadinova A (2016) Biodiversity of trematodes in their intermediate mollusc and fish hosts in the freshwater ecosystems of Europe. Syst Parasitol 93:283–293. https://doi.org/10.1007/s11230-016-9627-y
Farkaš J (1976) On the problems of cercarial dermatitis. Česk Dermatol 51:248–254 (in Slovak)
Gordy MA, Cobb TP, Hanington PC (2018) Swimmer’s itch in Canada: a look at the past and survey of the present to plan for the future. Environ Health 17:73. https://doi.org/10.1186/s12940-018-0417-7
Grimes JET, Croll D, Harrison WE, Utzinger J, Freeman MC, Templeton MR (2015) The roles of water, sanitation and hygiene in reducing schistosomiasis: a review. Parasit Vectors 8:156. https://doi.org/10.1186/s13071-015-0766-9
Horák P, Mikeš L, Lichtenbergová L, Skála V, Soldánová M, Brant SV (2015) Avian schistosomes and outbreaks of cercarial dermatitis. Clin Microbiol Rev 28:165–190. https://doi.org/10.1128/CMR.00043-14
Horsák M, Juřičková L, Picka J (2013) Molluscs of the Czech and Slovak Republics (Měkkýši České a Slovenské republiky). Kabourek, Zlín, 264 pp. (in Czech and English)
Huňová K, Kašný M, Hampl V, Leontovyč R, Kuběna A, Mikeš L, Horák P (2012) Radix spp.: identification of trematode intermediate hosts in the Czech Republic. Acta Parasitol 57:273–284. https://doi.org/10.2478/s11686-012-0040-7
Jouet D, Ferté H, Depaquit J, Rudolfová J, Latour P, Zanella D, Kaltenbach ML, Léger N (2008) Trichobilharzia spp. in natural conditions in Annecy Lake, France. Parasitol Res 103:51–58. https://doi.org/10.1007/s00436-008-0926-3
Jouet D, Ferté H, Holognel C, Kaltenbach ML, Depaquit J (2009) Avian schistosomes in French aquatic birds. J Helminthol 83:181–189. https://doi.org/10.1017/S0022149X09311712
Jouet D, Skírnisson K, Kolářová L, Ferté H (2010) Molecular diversity of Trichobilharzia franki in two intermediate hosts (Radix auricularia and Radix peregra): a complex of species. Infect Genet Evol 10:1218–1227. https://doi.org/10.1016/j.meegid.2010.08.001
Kock S (2001) Investigations of intermediate host specificity help to elucidate the taxonomic status of Trichobilharzia ocellata (Digenea: Schistosomatidae). Parasitology 123:67–70. https://doi.org/10.1017/s0031182001008101
Kolářová L, Horák P, Skírnisson K (2010) Methodical approaches in the identification of areas with a potential risk of infection by bird schistosomes causing cercarial dermatitis. J Helminthol 84:327–335. https://doi.org/10.1017/S0022149X09990721
Kolářová L, Horák P, Skírnisson K, Marečková H, Doenhoff M (2012) Cercarial dermatitis, a neglected allergic disease. Clin Rev Allergy Immunol 45:63–74. https://doi.org/10.1007/s12016-012-8334-y
Kouřilová P, Hogg KG, Kolářová L, Mountford AP (2004) Cercarial dermatitis caused by bird schistosomes comprises both immediate and late phase cutaneous hypersensitivity reactions. J Immunol 172:3766–3774. https://doi.org/10.4049/jimmunol.172.6.3766
Lawton SP, Lim RM, Dukes JP, Cook RT, Walker AJ, Kirk RS (2014) Identification of a major causative agent of human cercarial dermatitis, Trichobilharzia franki (Müller and Kimmig 1994), in southern England and its evolutionary relationships with other European populations. Parasit Vectors 7:277. https://doi.org/10.1186/1756-3305-7-277
Leighton BJ, Nervos S, Webster JM (2000) Ecological factors in schistosome transmission, and an environmentally benign method for controlling snails in a recreational lake with a record of schistosome dermatitis. Parasitol Int 49:9–17. https://doi.org/10.1016/s1383-5769(99)00034-3
Macháček T, Turjanicová L, Bulantová J, Hrdý J, Horák P, Mikeš L (2018) Cercarial dermatitis: a systematic follow-up study of human cases with implications for diagnostics. Parasitol Res 117:3881–3895. https://doi.org/10.1007/s00436-018-6095-0
Marszewska A, Cichy A, Heese T, Żbikowska E (2016) The real threat of swimmers’ itch in anthropogenic recreational water body of the Polish Lowland. Parasitol Res 115:3049–3056. https://doi.org/10.1007/s00436-016-5060-z
Marszewska A, Strzala T, Cichy A, Dąbrowska GB, Żbikowska E (2018) Agents of swimmer’s itch – dangerous minority in the Digenea invasion of Lymnaeidae in water bodies and the first report of Trichobilharzia regenti in Poland. Parasitol Res 117:3695–3704. https://doi.org/10.1007/s00436-018-6068-3
Murár B (1973) Finding of developmental stages of Echinoparyphium recurvatum (Trematoda, Echinostomatidae) in Planorbis planorbis. Biológia (Bratislava) 28:689–634. (In Slovak)
Nesterenko SV, Malko NJ (2007) Dynamics of human allergic dermatites caused by schistosomes in the Mjadel district (1995-2006). In: Problems of cercarial dermatitis in the Naroch district. Scientific seminar. Medisont, Minsk, pp 202–207
Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132:143–151. https://doi.org/10.1017/S0031182005008693
Rizevsky SV, Cherviakovsky EM, Kurchenko VP (2011) Molecular taxonomic identification of Schistosomatidae from Naroch Lake and Polonevichi Lake in Belarus. Biochem Syst Ecol 39:14–21. https://doi.org/10.1016/j.bse.2010.12.014
Sckrabulis JP, Flory AR, Raffel TR (2020) Direct onshore wind predicts daily swimmer’s itch (avian schistosome) incidence at a Michigan beach. Parasitology 22:1–10. https://doi.org/10.1017/S0031182020000074
Skála V, Černíková A, Jindrová Z, Kašný M, Vostrý M, Walker AJ, Horák P (2014) Influence of Trichobilharzia regenti (Digenea: Schistosomatidae) on the defence activity of Radix lagotis (Lymnaeidae) haemocytes. PLoS One 9:e111696. https://doi.org/10.1371/journal.pone.0111696
Skírnisson K, Kolářová L (2008) Diversity of bird schistosomes in anseriform birds in Iceland based on egg measurements and egg morphology. Parasitol Res 103:43–50. https://doi.org/10.1007/s00436-008-0925-4
Skírnisson K, Aldhoun JA, Kolářová L (2009) A review on swimmer’s itch and the occurrence of bird schistosomes in Iceland. J Helminthol 83:165–171. https://doi.org/10.1017/S0022149X09336408
Soldánová M, Selbach C, Kalbe M, Kostadinova A, Sures B (2013) Swimmer’s itch: etiology, impact, and risk factors in Europe. Trends Parasitol 29:2–74. https://doi.org/10.1016/j.pt.2012.12.002
Soldánová M, Selbach C, Sures B (2016) The early worm catches the bird? Productivity and patterns of Trichobilharzia szidati cercarial emission from Lymnaea stagnalis. PLoS One 11:e0149678. https://doi.org/10.1371/journal.pone.0149678
Soleng S, Mehl R (2011) Geographical distribution of cercarial dermatitis in Norway. J Helminthol 85:345–352. https://doi.org/10.1016/j.pt.2012.12.002
Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J (2006) Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6:411–425. https://doi.org/10.1016/S1473-3099(06)70521-7
Valdovinos C, Balboa C (2008) Cercarial dermatitis and lake eutrophication in south-Central Chile. Epidemiol Infect 136:391–394. https://doi.org/10.1017/S0950268807008734
Verbrugge LM, Rainey JJ, Reimink RL, Blankespoor HD (2004) Prospective study of swimmer’s itch incidence and severity. J Parasitol 90:697–704. https://doi.org/10.1645/GE-237R
Żbikowska E (2004) Infection of snails with bird schistosomes and the threat of swimmer’s itch in selected Polish lakes. Parasitol Res 92:30–35. https://doi.org/10.1007/s00436-003-0997-0
Żbikowska E (2005) Do larvae of Trichobilharzia szidati and Echinostoma revolutum generate behavioral fever in Lymnaea stagnalis individuals? Parasitol Res 97:68–72. https://doi.org/10.1007/s00436-005-1394-7
Żbikowska E (2007) Digenea species in chosen populations of freshwater snails in northern and central part of Poland. Wiad Parazytol 53:301–308
Żbikowska E, Marszewska A (2018) Thermal preference of bird schistosome snail hosts increase the risk of swimmer’s itch. J Therm Biol 78:22–26. https://doi.org/10.1016/j.jtherbio.2018.08.023
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We thank the two anonymous reviewers for their helpful suggestions.
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The present study was supported by the bilateral project of the Slovak Academy of Sciences (SAS-MOST JRP 2016/7), Grant Agency VEGA (No. 2/0126/20) and the Czech Science Foundation (17-20936Y).
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Gulyás, K., Soldánová, M., Orosová, M. et al. Confirmation of the presence of zoonotic Trichobilharzia franki following a human cercarial dermatitis outbreak in recreational water in Slovakia. Parasitol Res 119, 2531–2537 (2020). https://doi.org/10.1007/s00436-020-06751-y
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DOI: https://doi.org/10.1007/s00436-020-06751-y