Parasitology Research

, Volume 117, Issue 12, pp 3881–3895 | Cite as

Cercarial dermatitis: a systematic follow-up study of human cases with implications for diagnostics

  • Tomáš Macháček
  • Libuše Turjanicová
  • Jana Bulantová
  • Jiří Hrdý
  • Petr Horák
  • Libor MikešEmail author
Original Paper


Cercarial dermatitis (CD) is an allergic skin disease that rises in consequence of infection by invasive stages (cercariae) of trematodes of the family Schistosomatidae. CD has been considered a re-emerging disease, human cases have been reported from all continents, and tourism-threatening outbreaks occur even in frequented recreational areas. Although the symptoms of CD are generally known, the data on immune response in human patients are sporadic and incomprehensive. In the present study, we attempted to correlate the symptoms, personal history, and time course of CD in human patients with differential cell counts, dynamics of selected cytokines, and dynamics and quality of antibody response. By a systematic follow-up, we obtained a uniquely complex dataset from ten persons accidentally and concurrently infected by the same parasite species in the same locality. The onset of CD was significantly faster, and the symptoms were heavier in participants with a history of CD if compared to naive ones, who, however, also developed some of the symptoms. The repeatedly infected persons had elevated proportion of eosinophils 1 week post exposure (p.e.) and a stronger specific IgG but not IgM response, whereas specific IgE response was not observed. Increased serum levels of IL-4 occurred 1 and 3 week(s) p.e. in all participants. There was high variability in individual immunoblot patterns of IgG response, and no antigen with a universal diagnostic potential was confirmed. The presented analyses suggested that a complex approach can improve the accuracy of the diagnosis of CD, but component data should be interpreted carefully.


Schistosome Trichobilharzia Skin Allergy Immunity Diagnosis 



We thank all participants who agreed to participate in this study. We are also grateful to Mrs. Markéta Leissová, National Reference Laboratory for Tissue Helminthiases, Prague, for the collections of blood samples.


The work on the project was funded by Czech Science Foundation (Grant Nos. 13-29577S and 18-11140S) and by the project “Centre for Research of Pathogenicity and Virulence of Parasites” (no. CZ.02.1.01/0.0/0.0/16_019/0000759) funded by European Regional Development Fund and Ministry of Education, Youth and Sports of the Czech Republic. Charles University institutional support (PROGRES Q43, UNCE 204017, and SVV 244-260432/2017) applied to JB, TM, LT, PH, and LM.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants

This research was performed in accordance with the legislation of the Czech Republic and the European Union. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.The study was approved by the Institutional Review Board of the Charles University, Faculty of Science (approval no. 2017/22). This article does not contain any studies with animals performed by any of the authors.

Informed consent

All human participants involved in the study agreed to provide their data, which are constituent of this paper. Informed consent was obtained from all individual participants included in the study.

Supplementary material

436_2018_6095_MOESM1_ESM.pdf (251 kb)
Online Resource 1 Example of an unfilled questionnaire used for gaining data from individual participants (PDF 250 kb)
436_2018_6095_MOESM2_ESM.pdf (74 kb)
Online Resource 2 Results of personal evaluation of regional symptoms of cercarial dermatitis in individual participants (PDF 73 kb)
436_2018_6095_MOESM3_ESM.pdf (76 kb)
Online Resource 3 Results of personal evaluation of local symptoms of cercarial dermatitis in individual participants (PDF 76 kb)


  1. Aldhoun JA, Podhorský M, Holická M, Horák P (2012) Bird schistosomes in planorbid snails in the Czech Republic. Parasitol Int 61:250–259. CrossRefPubMedGoogle Scholar
  2. Bourke CD, Prendergast CT, Sanin DE, Oulton TE, Hall RJ, Mountford AP (2015) Epidermal keratinocytes initiate wound healing and pro-inflammatory immune responses following percutaneous schistosome infection. Int J Parasitol 45:215–224. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Brackett S (1940) Pathology of schistosome dermatitis. Arch Dermatol Syph 42:410–418. CrossRefGoogle Scholar
  4. Capron M, Capron A (1994) Immunoglobulin E and effector cells in schistosomiasis. Science 264:1876–1877. CrossRefPubMedGoogle Scholar
  5. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chanová M, Vuong S, Horák P (2007) Trichobilharzia szidati: the lung phase of migration within avian and mammalian hosts. Parasitol Res 100:1243–1247. CrossRefPubMedGoogle Scholar
  7. Choi P, Reiser H (1998) IL-4: role in disease and regulation of production. Clin Exp Immunol 113:317–319. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Christiansen AO, Olsen A, Buchmann K, Kania PW, Nejsum P, Vennervald BJ (2016) Molecular diversity of avian schistosomes in Danish freshwater snails. Parasitol Res 115:1027–1037. CrossRefPubMedGoogle Scholar
  9. Cook PC, Aynsley SA, Turner JD, Jenkins GR, Van Rooijen N, Leeto M, Brombacher F, Mountford AP (2011) Multiple helminth infection of the skin causes lymphocyte hypo-responsiveness mediated by Th2 conditioning of dermal myeloid cells. PLoS Pathog 7:e1001323. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dvořák J, Sattmann H, Horák P, Konecny R (1999) Bird schistosomes from freshwater snails in Austria, with some notes on current problems. Mitt Österr Ges Tropenmed Parasitol 21:69–76Google Scholar
  11. Dvořák J, Vaňáčová Š, Hampl V, Flegr J, Horák P (2002) Comparison of European Trichobilharzia species based on ITS1 and ITS2 sequences. Parasitology 124:307–313CrossRefGoogle Scholar
  12. Ganley-Leal LM, Mwinzi PN, Cetre-Sossah CB, Andove J, Hightower AW, Karanja DMS, Colley DG, Secor WE (2006) Correlation between eosinophils and protection against reinfection with Schistosoma mansoni and the effect of human immunodeficiency virus type 1 coinfection in humans. Infect Immun 74:2169–2176. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gieseck RL, Wilson MS, Wynn TA (2018) Type 2 immunity in tissue repair and fibrosis. Nat Rev Immunol 18:62–76. CrossRefPubMedGoogle Scholar
  14. Haas W, Häberlein S (2009) Penetration of cercariae into the living human skin: Schistosoma mansoni vs. Trichobilharzia szidati. Parasitol Res 105:1061–1066. CrossRefPubMedGoogle Scholar
  15. Haas W, van de Roemer A (1998) Invasion of the vertebrate skin by cercariae of Trichobilharzia ocellata: penetration processes and stimulating host signals. Parasitol Res 84:787–795CrossRefGoogle Scholar
  16. Haemmerli U (1953) Schistosomen-Dermatitis am Zürichsee. Dermatologica 107:301–341 (in German)Google Scholar
  17. Hesse M, Piccirillo CA, Belkaid Y, Prufer J, Mentink-Kane M, Leusink M, Cheever AW, Shevach EM, Wynn TA (2004) The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. J Immunol 172:3157–3166. CrossRefPubMedGoogle Scholar
  18. Hoffmann KF, Cheever AW, Wynn TA (2000) IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J Immunol 164:6406–6416. CrossRefPubMedGoogle Scholar
  19. Horák P, Kolářová L (2001) Bird schistosomes - do they die in mammalian skin? Trends Parasitol 17:66–69CrossRefGoogle Scholar
  20. Horák P, Kovář L, Kolářová L, Nebesářová J (1998) Cercaria-schistosomulum surface transformation ofTrichobilharzia szidati and its putative immunological impact. Parasitology 116:139–147CrossRefGoogle Scholar
  21. Horák P, Kolářová L, Adema CM (2002) Biology of the schistosome genus Trichobilharzia. Adv Parasitol 52:155–233CrossRefGoogle Scholar
  22. Horák P, Mikeš L, Rudolfová J, Kolářová L (2008) Penetration of Trichobilharzia cercariae into mammals: dangerous or negligible event? Parasite 15:299–303CrossRefGoogle Scholar
  23. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Jauréguiberry S, Paris L, Caumes E (2010) Acute schistosomiasis, a diagnostic and therapeutic challenge. Clin Microbiol Infect 16:225–231. CrossRefPubMedGoogle Scholar
  25. Jouet D, Ferte H, Depaquit J, Rudolfová J, Latour P, Zanella D, Kaltenbach ML, Leger N (2008) Trichobilharzia spp. in natural conditions in Annecy lake, France. Parasitol Res 103:51–58. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Khalife J, Dunne DW, Richardson BA, Mazza G, Thorne KJ, Capron A, Butterworth AE (1989) Functional role of human IgG subclasses in eosinophil-mediated killing of schistosomula of Schistosoma mansoni. J Immunol 142:4422–4427PubMedGoogle Scholar
  27. Kolářová L, Horák P (1999) Cercarial dermatitis in focus - spectrum of pathogenic agents and their development in non-specific hosts. Klinická mikrobiologie 3:260–267 (in Czech)Google Scholar
  28. Kolářová L, Skírnisson K, Horák P (1999) Schistosome cercariae as the causative agent of swimmer’s itch in Iceland. J Helminthol 73:215–220CrossRefGoogle Scholar
  29. 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. CrossRefGoogle Scholar
  30. Kolářová L, Horák P, Skírnisson K, Marečková H, Doenhoff M (2013) Cercarial dermatitis, a neglected allergic disease. Clin Rev Allergy Immunol 45:63–74. CrossRefGoogle Scholar
  31. Kouřilová P, Kolářová L (2002) Variations in immunofluorescent antibody response against Trichobilharzia and Schistosoma antigens in compatible and incompatible hosts. Parasitol Res 88:513–521. CrossRefPubMedGoogle Scholar
  32. 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 172:3766–3774CrossRefGoogle Scholar
  33. Kovalszki A, Weller PF (2016) Eosinophilia. Primary Care 43:607–617. CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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, 10 pp. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Leontovyč R, Young ND, Korhonen PK, Hall RS, Tan P, Mikeš L, Kašný M, Horák P, Gasser RB (2016) Comparative transcriptomic exploration reveals unique molecular adaptations of neuropathogenic Trichobilharzia to invade and parasitize its avian definitive host. PLoS Negl Trop Dis 10:e0004406, 24 pp. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lichtenberg F, Sher A, Gibbons N, Doughty BL (1976) Eosinophil-enriched inflammatory response to schistosomula in the skin of mice immune to Schistosoma mansoni. Am J Pathol 84:479–500PubMedPubMedCentralGoogle Scholar
  37. Lichtenbergová L, Horák P (2012) Pathogenicity of Trichobilharzia spp. for vertebrates. J Parasitol Res article ID 761968, pp. 9. (Erratum 2013, Article ID 721061)CrossRefGoogle Scholar
  38. Lichtenbergová L, Kolbeková P, Kouřilová P, Kašný M, Mikeš L, Haas H, Schramm G, Horák P, Kolářová L, Mountford AP (2008) Antibody responses induced by Trichobilharzia regenti antigens in murine and human hosts exhibiting cercarial dermatitis. Parasite Immunol 30:585–595. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Ligasová A, Bulantová J, Šebesta O, Kašný M, Koberna K, Mikeš L (2011) Secretory glands in cercaria of the neuropathogenic schistosome Trichobilharzia regenti - ultrastructural characterization, 3-D modelling, volume and pH estimations. Parasit Vectors 4:162, pp 12. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Macfarlane WV (1949) Schistosome dermatitis in New Zealand. Part II. Pathology and immunology of cercarial lesions. Am J Hyg 50:152–167. CrossRefPubMedGoogle Scholar
  41. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Marti H, Hatz C (2017) Eosinophilia and parasites. Ther Umsch 74:297–300. CrossRefPubMedGoogle Scholar
  43. Moore KW, de Waal Malefyt R, Coffman R, O’Garra A (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19:683–765. CrossRefPubMedGoogle Scholar
  44. Olivier L (1949) Schistosome dermatitis, a sensitization phenomenon. Am J Hyg 49:290–302. CrossRefPubMedGoogle Scholar
  45. Olivier L (1953) Observations on the migration of avian schistosomes in mammals previously unexposed to cercariae. J Parasitol 39:237–246CrossRefGoogle Scholar
  46. Pearce EJ, Vasconcelos JP, Brunet LR, Sabin EA (1996) IL-4 in Schistosomiasis. Exp Parasitol 84:295–299. CrossRefPubMedGoogle Scholar
  47. Podhorský M, Hůzová Z, Mikeš L, Horák P (2009) Cercarial dimensions and surface structures as a tool for species determination of Trichobilharzia spp. Acta Parasitol 54:28–36. CrossRefGoogle Scholar
  48. Prendergast CT, Sanin DE, Mountford AP (2016) CD4 T-cell hyporesponsiveness induced by schistosome larvae is not dependent upon eosinophils but may involve connective tissue mast cells. Parasite Immunol 38:81–92. CrossRefPubMedPubMedCentralGoogle Scholar
  49. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL:
  50. Řimnáčová J, Mikeš L, Turjanicová L, Bulantová J, Horák P (2017) Changes in surface glycosylation and glycocalyx shedding in Trichobilharzia regenti (Schistosomatidae) during the transformation of cercaria to schistosomulum. PLoS One 12:e0173217, 20 pp. CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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. CrossRefGoogle Scholar
  52. Selbach C, Soldánová M, Sures B (2016) Estimating the risk of swimmer’s itch in surface waters – a case study from Lake Baldeney, River Ruhr. Int J Hyg Environ Health 219:693–699. CrossRefPubMedGoogle Scholar
  53. Soldánová M, Selbach C, Kalbe M, Kostadinova A, Sures B (2013) Swimmer’s itch: etiology, impact, and risk factors in Europe. Trends Parasitol 29:65–74. CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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, 21 pp. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sridhar J, Deo R (2017) Marine and other aquatic dermatoses. Indian J Dermatol 62:66–78. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Turjanicová L, Mikeš L, Pecková M, Horák P (2015) Antibody response of definitive hosts against antigens of two life stages of the neuropathogenic schistosome Trichobilharzia regenti. Parasit Vectors 8:400, 11 pp. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Vogel H (1930) Hautverӓnderungen durch Cercaria ocellata. Dermatol Wochenschr 90:577–581 (in German)Google Scholar
  58. Weller PF, Spencer LA (2017) Functions of tissue-resident eosinophils. Nat Rev Immunol 17:746–760. CrossRefPubMedGoogle Scholar
  59. Wulff C, Häberlein S, Haas W (2007) Cream formulations protecting against cercarial dermatitis by Trichobilharzia. Parasitol Res 101:91–97. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Parasitology, Faculty of ScienceCharles UniversityPrague 2Czech Republic
  2. 2.Institute of Immunology and Microbiology, First Faculty of MedicineCharles University and General University Hospital in PraguePrague 2Czech Republic

Personalised recommendations