Parasitology Research

, 103:51 | Cite as

Trichobilharzia spp. in natural conditions in Annecy Lake, France

  • Damien Jouet
  • Hubert FertéEmail author
  • Jérôme Depaquit
  • Jitka Rudolfová
  • Pierre Latour
  • Damien Zanella
  • Matthieu L. Kaltenbach
  • Nicole Léger
Original Paper


Annecy Lake is a well-known focus of human cercarial dermatitis in France. Identification of the parasites, however, was not performed in the past. Previous studies suspected two species, Trichobilharzia franki and Trichobilharzia regenti, based on the presence of parasites in mallards and/or morphological identification of snails emitting ocellate furcocercariae. Following a standardized molecular approach, we studied snails and furcocercariae and compared their haplotypes with those deposited in GenBank. The selected markers were the second internal transcribed spacer ITS-2 for the snails and ITS-2 and D2 domain of the ribosomal DNA for the parasites. Our results confirm the presence of T. franki and T. regenti and two probable new species that could be potential agents of cercarial dermatitis. All the snails emitting the ocellate furcocercariae belong to the same species identified as Radix peregra (=Radix ovata = Radix balthica). Parasite–host relationships between species of the genus Trichobilharzia and snails of the genus Radix do not seem to be as specific as supposed previously.


Infected Snail Schistosoma Haematobium Tufted Duck Bird Schistosome Cercarial Dermatitis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors thank Monique Boutry, Chantal Grimplet, Emmanuel Liénard, and the technical staff of Syndicat Mixte du Lac d’Annecy (SILA) for their technical assistance and Bernard Pesson for proofreading this manuscript. Financial support for this study was provided by SILA and Office National de la Chasse et de la Faune Sauvage, by the Czech Ministry of Education (Grants No. MSM0021620828 and No. MSM LC06009), and by the Czech Science Foundation (Grant No. 206/07/P092).


  1. Bargues MD, Vigo M, Horák P, Dvořák J, Patzner RA, Pointier JP, Jackiewicz M, Meier-Brook C, Mas Coma S (2001) European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences. Infect Genet Evol 1(2):85–107PubMedCrossRefGoogle Scholar
  2. Bayssade-Dufour C, Martins C, Vuong PN (2001) Histopathologie pulmonaire d’un modèle mammifère et dermatite cercarienne humaine. Med Mal Infect 31:713–722CrossRefGoogle Scholar
  3. Bayssade-Dufour C, Vuong PN, Rene M, Martin-Loehr C, Martins C (2002) Visceral lesions in mammals and birds exposed to agents of human cercarial dermatitis. Bull Soc Pathol Exot 95(4):229–37PubMedGoogle Scholar
  4. Brant SV (2007) The occurrence of the avian schistosome Allobilharzia visceralis Kolářová, Rudolfová, Hampl et Skírnisson, 2006 (Schistosomatidae) in the tundra swan, Cygnus columbianus (Anatidae), from North America. Folia Parasitol 54:99–104PubMedGoogle Scholar
  5. Caumes E, Felder-Moinet S, Couzigou C, Darras-Joly C, Latour P, Léger N (2003) Failure of an ointment based on IR3535 (ethyl butylacetylaminopropionate) to prevent an outbreak of cercarial dermatitis during swimming race across Lake Annecy, France. Ann Trop Med Parasitol 97:157–163PubMedCrossRefGoogle Scholar
  6. Combes C, Albaret J-L, Bartoli P, Bayssade-Dufour C, Deblock S, Durette-Desset M-C, Gabrion C, Jourdane J, Lambert A, Léger N, Maillard C, Matricon M, Nassi H, Prevot G, Richard J, Theron A (1980) Atlas mondial des cercaires. Mem Mus Natl Hist Nat Paris Ser A 115:235Google Scholar
  7. De Gentile L, Picot H, Bourdeau P, Bardet R, Kerjan A, Piriou M, Guennic AL, Bayssade-Dufour C, Chabasse D, Mott KE, Le Guennic A (1996) Cercarial dermatitis in Europe: a new public health problem? Bull World Health Organ 74(2):159–163PubMedGoogle Scholar
  8. Dvořák J, Vaňáčová Š, Hampl V, Flegr J, Horák P (2002) Comparison of European Trichobilharzia species based on ITS-1 and ITS-2 sequences. Parasitology 124(3):307–313PubMedCrossRefGoogle Scholar
  9. Ferté H, Depaquit J, Carré S, Villena I, Léger N (2005) Presence of Trichobilharzia szidati in Lymnaea stagnalis and T. franki in Radix auricularia in northeastern France: molecular evidence. Parasitol Res 95:150–154PubMedCrossRefGoogle Scholar
  10. Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online—a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:W557–W559PubMedCrossRefGoogle Scholar
  11. Horák P, Kolářová L, Adema CM (2002) Biology of the schistosome genus Trichobilharzia. Adv Parasitol 52:155–233PubMedCrossRefGoogle Scholar
  12. Huelsenbeck JP, Ronquist F (2001) Mr Bayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  13. Kock S (2001) Investigations of intermediate host specificity help to elucidate the taxonomic status of Trichobilharzia ocellata (Digenea: Schistosomatidae). Parasitology 123(1):67–70PubMedCrossRefGoogle Scholar
  14. Kolářová L, Horák P, Fajfrlík K (1992) Cercariae of Trichobilharzia szidati Neuhaus, 1952 (Trematoda: Schistosomatidae): the causative agent of cercarial dermatitis in Bohemia and Moravia. Folia Parasitol 39:399–400PubMedGoogle Scholar
  15. Kolářová L, Rudolfová J, Hampl V, Skírnisson K (2006) Allobilharzia visceralis gen. nov., sp. Nov. (Schistosomatidae-Trematoda) from Cygnus Cygnus (L.) (Anatidae). Parasitol Int 55(3):179–86PubMedCrossRefGoogle Scholar
  16. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5(2):150–63PubMedCrossRefGoogle Scholar
  17. Léger N, Martin-Loehr C (1999) La dermatite cercarienne: un désagrément des baignades estivales. Actual Pharm 377:49–50Google Scholar
  18. Lockyer AE, Olson PD, Ostergaard P, Rollinson D, Johnston DA, Attwood SW, Southgate VR, Horák P, Snyder SD, LE TH, Agatsuma T, McManus DP, Carmichael AC, Naem S, Littlewood DT (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126(3):203–24PubMedCrossRefGoogle Scholar
  19. Loy C, Haas W (2001) Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitol Res 87:878–882PubMedCrossRefGoogle Scholar
  20. Mollaret I, Jamieson BG, Adlard RD, Hugall A, Lecointre G, Chombard C, Justine JL (1997) Phylogenetic analysis of the Monogenea and their relationships with Digenea and Eucestoda inferred from 28S rDNA sequences. Mol Biochem Parasitol 90(2):433–8PubMedCrossRefGoogle Scholar
  21. Müller V, Kimmig P (1994) Trichobilharzia franki n. sp. - Die Ursache für Badedermatitiden in südwestdeutschen Baggerseen. Appl Parasitol 34:187–201Google Scholar
  22. Pfenninger M, Cordellier M, Streit B (2006) Comparing the efficacy of morphologic and DNA-based taxonomy in the freshwater gastropod genus Radix (Basommatophora, Pulmonata). BMC Evol Biol 6:100PubMedCrossRefGoogle Scholar
  23. Picard D, Jousson O (2001) Genetic variability among cercariae of the Schistosomatidae (Trematoda: Digenea) causing swimmer’s itch in Europe. Parasite 8:237–242PubMedGoogle Scholar
  24. Posada D, Crandall KA (2001) Selecting the best-fit model of nucleotide substitution. Syst Biol 50:580–601PubMedCrossRefGoogle Scholar
  25. Rudolfová J, Hampl V, Bayssade-Dufour C, Lockyer AE, Littlewood DT, Horák P (2005) Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitol Res 95(2):79–89PubMedCrossRefGoogle Scholar
  26. Rudolfová J, Littlewood DTJ, Sitko J, Horák P (2007) Bird schistosomes of wildfowl in the Czech Republic and Poland. Folia Parasitol 54:88–93PubMedGoogle Scholar
  27. Snyder SD, Loker ES (2000) Evolutionary relationships among the Schistosomatidae (Platyhelminthes: Digenea) and an Asian origin for Schistosoma. J Parasitol 86:283–288PubMedGoogle Scholar
  28. Swofford DL (2002) PAUP*. phylogenetic analysis using parsimony (*and others methods). Version 4. Sinauer, SunderlandGoogle Scholar
  29. Verbrugge LM, Rainey JJ, Reimink RL, Blankespoor HD (2004) Swimmer’s itch: incidence and risk factors. Am J Public Health 94(5):738–741PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Damien Jouet
    • 1
  • Hubert Ferté
    • 1
    Email author
  • Jérôme Depaquit
    • 1
  • Jitka Rudolfová
    • 2
  • Pierre Latour
    • 3
  • Damien Zanella
    • 3
  • Matthieu L. Kaltenbach
    • 4
  • Nicole Léger
    • 5
  1. 1.USC AFSSA « VECPAR », UFR de PharmacieUniversité de Reims Champagne—ArdenneReimsFrance
  2. 2.Faculty of Science, Department of ParasitologyCharles University in PraguePrague 2Czech Republic
  3. 3.SILACran-GevrierFrance
  4. 4.Laboratoire de Pharmacologie, UFR de PharmacieUniversité de Reims Champagne—ArdenneReimsFrance
  5. 5.La Varenne Saint HilaireFrance

Personalised recommendations