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Avian schistosomes in French aquatic birds: a molecular approach

Published online by Cambridge University Press:  01 June 2009

D. Jouet*
Affiliation:
JE 2533 – USC AFSSA ‘VECPAR’, UFR de Pharmacie, Université de Reims Champagne – Ardenne, 51 rue Cognacq-Jay, 51096Reims, France
H. Ferté
Affiliation:
JE 2533 – USC AFSSA ‘VECPAR’, UFR de Pharmacie, Université de Reims Champagne – Ardenne, 51 rue Cognacq-Jay, 51096Reims, France
C. Hologne
Affiliation:
JE 2533 – USC AFSSA ‘VECPAR’, UFR de Pharmacie, Université de Reims Champagne – Ardenne, 51 rue Cognacq-Jay, 51096Reims, France
M.L. Kaltenbach
Affiliation:
Laboratoire de Pharmacologie, UFR de Pharmacie, Université de Reims Champagne – Ardenne, 51 rue Cognacq-Jay, 51096Reims, France
J. Depaquit
Affiliation:
JE 2533 – USC AFSSA ‘VECPAR’, UFR de Pharmacie, Université de Reims Champagne – Ardenne, 51 rue Cognacq-Jay, 51096Reims, France
*
*Fax: +33 326 913 569, E-mail: damienjouet@hotmail.com

Abstract

The prevalence of human cercarial dermatitis (HCD) caused by bird schistosomes appears to be increasing in France, in light of the impact of tourism combined with high densities of wild aquatic hosts in freshwater areas. The present work expands our knowledge of schistosome systematics by including samples of bird schistosomes collected from their natural hosts in France. Heads (318) and viscera (81) of aquatic birds belonging to 16 species from five orders, collecting during the hunting seasons or found dead, were autopsied for nasal and visceral schistosomes. Eggs and/or adults were analysed by molecular methods using the D2 domain and the second internal transcribed spacer (ITS-2) region of rDNA to determine species. Even if nasal eggs were polymorphic according to the host, all haplotypes were similar to that of Trichobilharzia regenti. Marked diversity of visceral species was observed. Final hosts under natural conditions were reported. For the first time, Trichobilharzia franki is reported in its natural bird hosts, Anas platyrhynchos, Anas crecca, Aythya fuligula and Cygnus olor. We also identified T. szidati in A. crecca and Anas clypeata. Bilharziella polonica was found in six species of aquatic birds, including Grus grus. This finding is the first record of bird schistosomes in this aquatic bird. Three new taxa of visceral schistosomes in Anser anser are strongly suspected according to their haplotypes. Futhermore, a new haplotype of visceral schistosomes isolated in Cygnus olor and similar to Allobilharzia visceralis was identified.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2009

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References

Bayssade-Dufour, C., Martins, C. & Vuong, P.N. (2001) Histopathologie pulmonaire d'un modèle mammifère et dermatite cercarienne humaine. Médecine et Maladies Infectieuses 31, 713722.CrossRefGoogle Scholar
Bayssade-Dufour, C., Vuong, P.N., René, M., Martin-Loehr, C. & Martins, C. (2002) Lésions viscérales de mammifères et oiseaux, exposés aux agents de dermatite cercarienne humaine. Bulletin de la Société de Pathologie Exotique (1990) 95, 229237.Google Scholar
Bayssade-Dufour, C., Jouet, D., Rudolfová, J., Horák, P. & Ferté, H. (2006) Seasonal morphological variations in bird schistosomes. Parasite 13, 205214.CrossRefGoogle ScholarPubMed
Brant, S.V. (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 Parasitologia (Praha) 54, 99104.CrossRefGoogle Scholar
Brant, S.V., Morgan, J.A., Mkoji, G.M., Snyder, S.D., Rajapakse, R.P. & Loker, E.S. (2006) An approach to revealing blood fluke life cycles, taxonomy, and diversity: provision of key reference data including DNA sequence from single life cycle stages. Journal of Parasitology 92, 7788.CrossRefGoogle ScholarPubMed
Brumpt, E. (1931) Prurit et dermatites produites chez les nageurs par des cercaires de mollusques d'eau douce. Comptes Rendus de l'Académie des Sciences de Paris 193, 253255.Google Scholar
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 races across Lake Annecy, France. Annals of Tropical Medicine and Parasitology 97, 157163.CrossRefGoogle ScholarPubMed
de Gentile, L., Picot, H., Bourdeau, P., Bardet, R., Kerjan, A., Piriou, M., Guennic, A.L., Bayssade-Dufour, C., Chabasse, D., Mott, K.E. & Le Guennic, A. (1996) Cercarial dermatitis in Europe: a new public health problem? Bulletin of the World Health Organization 74, 159163.Google ScholarPubMed
Desportes, C. (1945) La dermatite des nageurs. Annales de Parasitologie 20, 263278.Google Scholar
Dönges, J. (1965) Schistosomatiden-Cercarien Süddeutschlands. Ein beitrag zur Kenntnis dermatitiserregender Trematodenlarven. Zeitschrift fur Tropenmedicin und Parasitologie 16, 305321.Google Scholar
Dvořák, J., Vancova, S., Hampl, V., Flegr, J. & Horák, P. (2002) Comparison of European Trichobilharzia species based on ITS1 and ITS2 sequences. Parasitology 124, 307313.CrossRefGoogle ScholarPubMed
Eklu-Natey, D.T., Al-Khudri, M., Gauthey, D., Dubois, J.P., Wüest, J., Vaucher, C. & Huggel, H. (1985) Epidemiologie de la dermatite des baigneurs et morphologie de Trichobilharzia cf. ocellata dans le lac Léman. Revue Suisse de Zoologie 92, 939953.CrossRefGoogle Scholar
Fain, A. (1955a) Une nouvelle bilharziose des oiseaux: la trichobilharziose nasale. Remarque sur l'importance des Schistosomes d'oiseaux en pathologie humaine. Note préliminaire. Annales de la Société Belge de Médecine Tropicale 35, 323327.Google Scholar
Fain, A. (1955b) Recherche sur les Schistosomes d'oiseaux au Ruanda-Urundi (Congo belge). Découverte d'une nouvelle bilharzie aviaire: la Trichobilharzie nasale, et description de Schistosomes nouveaux. Note préliminaire. Revue Zoologique de Botanique Africaines 51, 373387.Google Scholar
Fain, A. (1956a) Les Schistosomes d'oiseaux du genre Trichobilharzia Skrjabin et Zakharow, 1920 au Ruanda-Urundi. Revue de Zoologie et Botanique Africaines 54, 147178.Google Scholar
Fain, A. (1956b) Nasal trichobilharziasis: a new avian schistosomiasis. Nature 177, 389.CrossRefGoogle ScholarPubMed
Fain, A. (1959) Un nouveau schistosome du genre Trichobilharzia dans les fosses nasales du Canard nain. Revue de Zoologie et Botanique Africaines 60, 227232.Google Scholar
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. Parasitology Research 95, 150154.CrossRefGoogle Scholar
Gay, P., Bayssade-Dufour, C., Grenouillet, F., Bourezane, Y. & Dubois, J.P. (1999) Etude expérimentale de dermatites cercariennes provoquées par Trichobilharzia en France. Médecine et Maladies Infectieuses 29, 629637.CrossRefGoogle Scholar
Gottschalk, C. & Prange, H. (2002) Parasiten des Grauen Kranichs Grus grus (L.) in Europa. Berliner und Münchener Tierärztliche Wochenschrift 115, 203206.Google Scholar
Guindon, S., Lethiec, F., Duroux, P. & Gascuel, O. (2005) PHYML Online – a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Research 33 (Web Derver issue), W557W559.CrossRefGoogle ScholarPubMed
Haas, W. & Pietsch, U. (1991) Migration of Trichobilharzia ocellata schistosomula in the duck and in the abnormal murine host. Parasitology Research 77, 642644.CrossRefGoogle ScholarPubMed
Horák, P. & Kolářová, L. (2000) Survival of bird schistosomes in mammalian lungs. International Journal of Parasitology 30, 6568.CrossRefGoogle ScholarPubMed
Horák, P. & Kolářová, L. (2001) Bird schistosomes: do they die in mammalian skin? Trends of Parasitology 17, 6669.CrossRefGoogle ScholarPubMed
Horák, P., Kolářová, L. & Dvořák, J. (1998) Trichobilharzia regenti n. sp. (Schistosomatidae, Bilharziellinae), a new nasal schistosome from Europe. Parasite 5, 349357.CrossRefGoogle Scholar
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755.CrossRefGoogle ScholarPubMed
Jouet, D., Ferté, H., Depaquit, J., Rudolfová, J., Latour, P., Zaniella, D., Kaltenbach, M.L. & Léger, N. (2008) Trichobilharzia spp. in natural conditions in Annecy Lake, France. Parasitology Research 103, 5158.CrossRefGoogle ScholarPubMed
Kolářová, L., Gottwaldova, V., Cechova, D. & Sevcova, M. (1989) The occurrence of cercarial dermatitis in Central Bohemia. International Journal of Hygiene and Environmental Medicine 189, 113.Google ScholarPubMed
Kolářová, L., Horák, P. & Fajfrlik, K. (1992) Cercariae of Trichobilharzia szidati Neuhaus, 1952 (Trematoda: Schistosomatidae): the causative agent of cercarial dermatitis in Bohemia and Moravia. Folia Parasitologia 39, 399400.Google Scholar
Kolářová, L., Horák, P. & Sitko, J. (1997) Cercarial dermatitis in focus: Schistosomes in the Czech Republic. Helminthologia 34, 127139.Google Scholar
Kolářová, L., Skírnisson, K. & Horák, P. (1999) Schistosome cercariae as the causative agent of swimmer's itch in Iceland. Journal of Helminthology 73, 215220.CrossRefGoogle ScholarPubMed
Kolářová, L., Rudolfová, J., Hampl, V. & Skírnisson, K. (2006) Allobilharzia visceralis gen. nov. sp. nov. (Schistosomatidae-Trematoda) from Cygnus cygnus (L.) (Anatidae). Parasitology International 55, 179186.CrossRefGoogle ScholarPubMed
Kumar, S., Tamura, K. & Neï, M. (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150163.CrossRefGoogle ScholarPubMed
Léger, N. & Martin-Loehr, C. (1999) La dermatite cercarienne: un désagrément des baignades estivales. Actualités Pharmarceutiques 377, 4950.Google Scholar
Lévine, N.D., Clark, D.T. & Hanon, L.E. (1956) Encephalitis in a swan due to Dendritobilharzia sp. (Trematoda; Schistosomatidae). Journal of Parasitology 42, 496500.CrossRefGoogle Scholar
Littlewood, D.T. & Johnston, D.A. (1995) Molecular phylogenetics of the four Schistosoma species groups determined with partial 28S ribosomal RNA gene sequences. Parasitology 111, 167175.CrossRefGoogle ScholarPubMed
Lockyer, A.E., Olson, P.D., Ostergaard, P., Rollinson, D., Johnston, D.A., Attwood, S.W., Southgate, V.R., Horák, P., Snyder, S.D., Le, T.H., Agatsuma, T., McManus, D.P., Carmichael, A.C., Naem, S. & Littlewood, D.T. (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126, 203224.CrossRefGoogle ScholarPubMed
Loker, E.S. & Brant, S.V. (2006) Diversification, dioecy and dimorphism in schistosomes. Trends of Parasitology 22, 521528.CrossRefGoogle ScholarPubMed
Mollaret, I., Jamieson, B.G., Adlard, R.D., Hugall, A., Lecointre, G., Chombard, C. & Justine, J.L. (1997) Phylogenetic analysis of the Monogenea and their relationships with Digenea and Eucestoda inferred from 28S rDNA sequences. Molecular and Biochemical Parasitology 90, 433438.CrossRefGoogle ScholarPubMed
Müller, V. & Kimmig, P. (1994) Trichobilharzia franki n. sp. – Die Ursache für Badedermatitiden in südwestdeutschen Baggerseen. Applied Parasitology 34, 187201.Google Scholar
Neuhaus, W. (1952) Biologie und Entwicklung von Trichobilharzia szidati n. sp. (Trematoda, Schistosomatidae). Einem Erreger von Dermatitis beim Menschen. Zeitschrift für Parasitenkunde (Berlin, Germany) 15, 203266.CrossRefGoogle Scholar
Olson, P.D., Cribb, T.H., Tkach, V.V., Bray, R.A. & Lttlewood, D.T. (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal of Parasitology 33, 733755.CrossRefGoogle ScholarPubMed
Palmer, D. & Ossent, P. (1984) Nasal schistosomiasis in Mute Swans in Switzerland. Revue Suisse de Zoologie 91, 709715.CrossRefGoogle Scholar
Posada, D. & Crandall, K.A. (2001) Selecting the best-fit model of nucleotide substitution. Systematic Biology 50, 580601.CrossRefGoogle ScholarPubMed
Rudolfová, J., Sitko, J. & Horák, P. (2002) Nasal schistosomes of wildfowl in the Czech Republic. Parasitology Research 88, 10931095.CrossRefGoogle ScholarPubMed
Rudolfová, J., Hampl, V., Bayssade-Dufour, C., Lockyer, A.E., Littlewood, D.T. & Horák, P. (2005) Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitology Research 95, 7989.CrossRefGoogle ScholarPubMed
Rudolfová, J., Littlewood, D.T., Sitko, J. & Horák, P. (2007) Bird schistosomes of wildfowl in the Czech Republic and Poland. Folia Parasitologia (Praha) 54, 8893.CrossRefGoogle ScholarPubMed
Simon-Martin, F. & Simon-Vicente, F. (1999) The life cycle of Trichobilharzia salmanticensis n. sp. (Digenea: Schistosomatidae), related to cases of human dermatitis. Research and Reviews in Parasitology 59, 12.Google Scholar
Skírnisson, K. & Kolářová, L. (2008) Diversity of bird Schistosomes in anseriform birds in Iceland based on egg measurements and egg morphology. Parasitology Research 103, 4350.CrossRefGoogle ScholarPubMed
Snyder, S.D. (2004) Phylogeny and paraphyly among tetrapod blood flukes (Digenea: Schistosomatidae and Spirorchiidae). International Journal of Parasitology 34, 13851392.CrossRefGoogle ScholarPubMed
Snyder, S.D. & Loker, E.S. (2000) Evolutionary relationships among the Schistosomatidae (Platyhelminthes:Digenea) and an Asian origin for Schistosoma. Journal of Parasitology 86, 283288.CrossRefGoogle Scholar
Szidat, L. (1930) Uber Hautinfektionen bei Bluttrematoden insbesondere bei Bilharziella polonica Kow. Archiv für Dermatologie und Syphilis 160, 304308.CrossRefGoogle Scholar
van Bolhuis, G.H., Rijks, J.M., Dorrestein, G.M., Rudolfová, J., van Dijk, M. & Kuiken, T. (2004) Obliterative endophlebitis in mute swans (Cygnus olor) caused by Trichobilharzia sp. (Digenea: Schistosomatidae) infection. Veterinary Pathology 41, 658665.CrossRefGoogle ScholarPubMed
van den Broek, E. (1965) Some recent cases of avian schistosomiasis and schistosome dermatitits in the Netherlands. Tropical and Geographical Medicine 17, 229235.Google Scholar
Wilson, R.B., New, J.C. & Scholtens, R.G. (1982) Granulomatous encephalitis caused by schistosomiasis in swans. Journal of the American Veterinary Medical Association 181, 13861387.Google ScholarPubMed
Wojcinski, Z.W., Barker, I.K., Hunter, D.B. & Lumsden, H. (1987) An outbreak of schistosomiasis in Atlantic brent geese, Branta bernicola hrota. Journal of Wildlife Diseases 23, 248255.CrossRefGoogle Scholar
Zbikowska, E. (2003) Is there a potential danger of ‘swimmer's itch’ in Poland? Parasitology Research 89, 5962.Google Scholar
Zbikowska, E. (2004) Infection of snails with bird schistosomes and the threat of swimmer's itch in selected Polish lakes. Parasitology Research 92, 3035.CrossRefGoogle ScholarPubMed
Zbikowska, E., Franckiewicz Grygon, B. & Wojcik, A.R. (2001) The case of dermatitis in the human as a result of the influence of the cercaria of the bird schistosome. Wiadomosci Parazytologiczne 47, 427431.Google ScholarPubMed