Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-23T17:16:58.150Z Has data issue: false hasContentIssue false
  • English
  • Français

Methodical approaches in the identification of areas with a potential risk of infection by bird schistosomes causing cercarial dermatitis

Published online by Cambridge University Press:  27 January 2010

L. Kolářová ,
P. Horák  and
K. Skírnisson
L. Kolářová*
Affiliation:
Institute of Immunology and Microbiology of the First Faculty of Medicine, Charles University in Prague and General Teaching Hospital, Studničkova 7, 128 00Prague 2, Czech Republic
P. Horák
Affiliation:
Department of Parasitology, Faculty of Science, Charles University in Prague, Prague, Czech Republic
K. Skírnisson
Affiliation:
Institute for Experimental Pathology, University of Iceland, Keldur, Reykjavík, Iceland
*
*Fax: (+420) 224 968 496 E-mail: libuse.kolarova@lf1.cuni.cz
Get access Rights & Permissions [Opens in a new window]

Abstract

Larval stages (cercariae) of schistosomatid flukes represent the causative agents of swimmer's itch (cercarial dermatitis), a waterborne allergic disease. Cercariae of bird schistosomes are the most frequently reported agent. Recent studies on parasite behaviour in mammals showed that infections by cercariae can be linked to more than skin syndromes. Despite the failure of complete development in mammals, bird schistosomes can escape from the skin and migrate transitorily in the hosts. These findings brought novel insights into the fate and potential pathogenic effect of the parasites in non-compatible hosts, including humans. Cercarial dermatitis occurs globally and recently is considered to be re-emerging; however, there are no data on the number of afflicted persons per year. This might be explained by a relatively low interest in human skin infections arising after bathing in fresh water. In addition, the real occurrence of bird schistosomes in the field is known only for a few areas. The paucity of epidemiological/biogeographical data is probably caused by difficulties associated with detection of the parasites in intermediate and definitive hosts. Therefore, based on personal experience and data available in the literature, we have summarized methodological approaches enabling the detection of bird schistosomes in various hosts and environments.

Type
Research Papers
Information
Journal of Helminthology , Volume 84 , Issue 3 , September 2010 , pp. 327 - 335
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aldhoun, J.A., Faltýnková, A., Karvonen, A. & Horák, P. (2009a) Schistosomes in the North: an unique finding from a prosobranch snail using molecular tools. Parasitology International 58, 314–317.CrossRefGoogle ScholarPubMed
Aldhoun, J.A., Kolářová, L., Horák, P. & Skírnisson, K. (2009b) Bird schistosome diversity in Iceland: molecular evidence. Journal of Helminthology 83, 173–180.CrossRefGoogle ScholarPubMed
Allgöwer, R. & Effelsberg, W. (1991) Badedermatitisepidemie im Baggersee – ein Anlaß zur Zustandsanalyse der Gewässers und Vorbereitung einer naturverträglichen Nutzungskonzeption. Das öffentliche Gesundheitswesen 53, 115–156.Google Scholar
Appleton, C.C. (1986) Occurrence of avian Schistosomatidae (Trematoda) in South African birds as determined by a faecal survey. South African Journal of Zoology 21, 60–67.CrossRefGoogle Scholar
Bayssade-Dufour, C., Martins, C. & Vuong, P.N. (2001) Histopathologie d'un modèle mammifère et dermatite cercarienne humaine. Médicine et Maladies Infectieuses 31, 713–722.CrossRefGoogle Scholar
Bei, A.K., Salter, J.P., Lim, K.C. & McKerrow, J.H. (2001) Survey of trematode infections in Spring Lake Regional Park, California, USA. Helminthologia 38, 250.Google Scholar
Blair, D. & Islam, K.S. (1983) The life-cycle and morphology of Trichobilharzia australis n. sp. (Digenea: Schistosomatidae) from the nasal blood vessels of the black duck (Anas superciliosa) in Australia, with a review of the genus Trichobilharzia. Systematic Parasitology 5, 89–117.CrossRefGoogle Scholar
Blažová, K. & Horák, P. (2005) Trichobilharzia regenti: The developmental differences in natural and abnormal hosts. Parasitology International 54, 167–172.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 Parasitologica 54, 99–104.CrossRefGoogle Scholar
Brant, S.V. & Loker, E.S. (2009a) Schistosomes in the southwest United States and their potential for causing cercarial dermatitis or swimmer's itch. Journal of Helmithology 83, 191–198.CrossRefGoogle ScholarPubMed
Brant, S.V. & Loker, E.S. (2009b) Molecular systematics of the avian schistosomes genus Trichobilharzia (Trematoda: Schistosomatidae) in North America. Journal of Parasitology 95, 941–963.CrossRefGoogle ScholarPubMed
Canestri-Trotti, G., Fioravanti, M.L. & Pampliglione, S. (2001) Cercarial dermatitis in Italy. Helminthologia 38, 245.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, 157–163.CrossRefGoogle ScholarPubMed
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. Epidemiology and Infection 120, 305–314.CrossRefGoogle ScholarPubMed
Chanová, M. & Horák, P. (2007) Terminal phase of bird schistosomiasis caused by Trichobilharzia regenti (Schistosomatidae) in ducks (Anas platyrhynchos f. domestica). Folia Parasitologica 54, 105–107.CrossRefGoogle ScholarPubMed
Curtis, L.A. & Hubbard, K.M. (1990) Trematode infections in a gastropod host misrepresented by observing shed cercariae. Journal of Experimental Marine Biology and Ecology 143, 131–137.CrossRefGoogle Scholar
de Gentile, L., Picot, H., Bourdeau, P., Bardet, R., Kerjan, A., Piriou, M., Le Guennic, A., Bayssade-Dufour, C., Chabasse, D. & Mott, K.E. (1996) Le dermatite cercarienne en Europe: un probleme de la santé publique nouveau? Bulletin de l'Organisation Mondiale de la Santé 74, 159–163.Google Scholar
Dvořák, J., Vaňáčová, Š., Hampl, V., Flegr, J. & Horák, P. (2002) Comparison of European Trichobilharzia species based on ITS1 and ITS2 sequences. Parasitology 124, 307–313.CrossRefGoogle ScholarPubMed
Farahnak, A. & Essalat, M. (2003) A study on cercarial dermatitis in Kuzechstan province, south western Iran. BMC Public Health 3, 35.CrossRefGoogle Scholar
Ferté, H., Depaquit, J., Cardo, 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, 150–154.CrossRefGoogle Scholar
Fraser, S.J., Allan, S.J.R., Roworth, M., Smith, H.V. & Holme, S.A. (2009) Cercarial dermatitis in the UK. Clinical and Experimental Dermatology 34, 344–346.CrossRefGoogle ScholarPubMed
Gérard, C. (2004) First occurrence of Schistosomatidae infecting Aplexa hypnorum (Gastropoda, Physidae) in France. Parasite 11, 231–234.CrossRefGoogle ScholarPubMed
Graczyk, T.K. & Shiff, C.J. (2000) Recovery of avian schistosome cercariae from water using penetration stimulant matrix with an unsaturated fatty acid. American Journal of Tropical Medicine and Hygiene 63, 174–177.CrossRefGoogle ScholarPubMed
Haas, W. (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 34, 927–934.Google Scholar
Hertel, J., Hamburger, J., Haberl, B. & Haas, W. (2002) Detection of bird schistosomes in lakes by PCR and filter-hybridization. Experimental Parasitology 101, 57–63.CrossRefGoogle ScholarPubMed
Horák, P. & Kolářová, L. (2000) Survival of bird schistosomes in mammalian lungs. International Journal for Parasitology 30, 65–68.CrossRefGoogle ScholarPubMed
Horák, P., Dvořák, J., Kolářová, L. & Trefil, L. (1999) Trichobilharzia regenti, a pathogen of the avian and mammalian central nervous systems. Parasitology 119, 577–581.CrossRefGoogle ScholarPubMed
Horák, P., Kolářová, L. & Adema, C. (2002) Biology of the schistosome genus Trichobilharzia. Advances in Parasitology 52, 155–233.CrossRefGoogle ScholarPubMed
Horák, P., Mikeš, L., Rudolfová, J. & Kolářová, L. (2008) Penetration of Trichobilharzia cercariae into mammals: dangerous or negligible event? Parasite 15, 299–303.CrossRefGoogle ScholarPubMed
Hörweg, C., Sattmann, H. & Auer, H. (2006) Cercarial dermatitis in Austria: questionnaires as useful tools to estimate risk factors? Wiener klinische Wochenschrift 118, 177–180.CrossRefGoogle ScholarPubMed
Hrádková, K. & Horák, P. (2002) Neurotropic behaviour of Trichobilharzia regenti in duck and mice. Journal of Helminthology 76, 137–141.CrossRefGoogle ScholarPubMed
Jouet, D., Ferté, H., Depaquit, J., Rudolfová, J., Latour, P., Zanella, D., Kaltenbach, M.L. & Léger, N. (2008) Trichobilharzia sp. in natural conditions in Annecy Lake, France. Parasitology Research 103, 51–58.CrossRefGoogle Scholar
Jouet, D., Ferté, H., Hologne, C., Kaltenbach, M.L. & Depaquit, J. (2009) Avian schistosomes in French aquatic birds: a molecular approach. Journal of Helminthology 83, 181–189.CrossRefGoogle ScholarPubMed
Kassai, T. (1999) Veterinary parasitology. Oxford, Butterworth-Heinemann.Google Scholar
Kolářová, L. (2007) Schistosomes causing cercarial dermatitis: a mini-review of current trends in systematics and host specificity and pathogenicity. Folia Parasitologica 54, 81–87.CrossRefGoogle ScholarPubMed
Kolářová, L., Gottwaldová, V., Čechová, D. & Ševcová, M. (1989) The occurrence of cercarial dermatitis in Central Bohemia. Zentralblatt für Hygiene und Umweltmedizin 189, 1–13.Google ScholarPubMed
Kolářová, L., Sýkora, J. & Bah, B.A. (1994) Serodiagnosis of cercarial dermatitis with antigens of Trichobilharzia szidati and Schistosoma mansoni. Central European Journal of Public Health 2, 19–22.Google ScholarPubMed
Kolářová, L., Horák, P. & Čada, F. (2001) Histopathology of the CNS and nasal infections caused by Trichobilharzia regenti in vertebrates. Parasitology Research 87, 644–650.Google ScholarPubMed
Kolářová, L., Skírnisson, K., Rudolfová, J., Jouet, D., Léger, N. & Ferté, H. (2005) Avian schistosomes of the genus Trichobilharzia in Europe. Bulletin of the Scandinavian–Baltic Society for Parasitology 14, 85–86.Google Scholar
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, 179–186.CrossRefGoogle ScholarPubMed
Kouřilová, P. & Kolářová, L. (2002) Variations in immunofluorescent antibody response against Trichobilharzia and Schistosoma antigens in compatible and noncompatible hosts. Parasitology Research 88, 513–521.CrossRefGoogle Scholar
Kouřilová, P., Hogg, K.G., Kolářová, L. & Mountford, A.P. (2004) Cercarial dermatitis caused by bird schistosomes comprises both immediate and late phase cutaneous hypersensitivity reaction. Journal of Immunology 172, 3766–3774.CrossRefGoogle Scholar
Larsen, A.H., Bresciani, J. & Buchmann, K. (2004) Increasing frequency of cercarial dermatitis in higher latitudes. Acta Parasitologica 49, 217–221.Google Scholar
Lawson, J.R. & Wilson, R.A. (1983) The relationship between the age of Schistosoma mansoni cercariae and their ability to penetrate and infect the mammalian host. Parasitology 87, 481–492.CrossRefGoogle ScholarPubMed
Leighton, B.J., Zervos, S. & Webster, J.M. (2000) Ecological factors in schistosome transmission, and an environmentally benign method for controlling snails in a recreational lake with a record of schistosome dermatitis. Parasitology International 49, 9–17.CrossRefGoogle Scholar
Lichtenbergová, L., Kolbeková, P., Kouřilová, P., Kašný, M., Mikeš, L., Haas, H., Schramm, G., Horák, P., Kolářová, L. & Mountford, A.P. (2008) Antibody responses induced by Trichobilharzia regenti antigens in murine and human hosts exhibiting cercarial dermatitis. Parasite Imunology 30, 585–595.CrossRefGoogle ScholarPubMed
Lim, H.-K. & Heyneman, D. (1972) Intramolluscan inter-trematode antagonism: a review of factors influencing the host–parasite system and its possible role in biological control. Advances in Parasitology 10, 191–268.CrossRefGoogle ScholarPubMed
Linder, E., Thors, C. & Jacks, A. (2001) Identification of cercariae causing swimmer's itch: preliminary observations on a skin lipid attachment assay. Helminthologia 38, 245.Google Scholar
Loy, C. & Haas, W. (2001) Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitology Research 87, 878–882.Google Scholar
Mas-Coma, S., Valero, M.A. & Bargues, M.D. (2008) Effect of climate change on animal and zoonotic helminthiases. Revue scientifique et technique 27, 443–457.CrossRefGoogle ScholarPubMed
Mas-Coma, S., Valero, M.A. & Bargues, M.D. (2009) Climate effects on trematodiases, with emphasis on zoonotoc fascioliasis and schistosomiasis. Veterinary Parasitology 163, 264–280.CrossRefGoogle Scholar
McMullen, D.B. & Beaver, P.C. (1945) Studies on schistosome dermatitis. IX. The life cycles of three dermatitis-producing schistosomes from birds and a discussion of the subfamily Bilharziellinae (Trematoda: Schistosomatidae). American Journal of Hygiene 42, 128–154.Google Scholar
Meuleman, E.A., Huyer, A.R. & Mooij, J.H. (1984) Maintenance of the life-cycle of Trichobilharzia ocellata via the duck Anas platyrhynchos and the pond snail Lymnaea stagnalis. Netherlands Journal of Zoology 34, 414–417.CrossRefGoogle Scholar
Moné, H., Mouahid, G. & Morand, S. (1999) The distribution of Schistosoma bovis Sonsino, 1876 in relation to intermediate host mollusk–parasite relationship. Advances in Parasitology 44, 99–138.CrossRefGoogle Scholar
Müller, V. & Kimmig, P. (1994) Trichobilharzia franki n. sp. – die Ursache für Badedermatitiden in südwestdeutschen Baggerseen. Applied Parasitology 35, 12–31.Google Scholar
Neuhaus, W. (1952) Biologie und Entwicklung von Trichobilharzia szidati n. sp. (Trematoda, Schistosomatidae), einem Erreger von Dermatitis beim Menschen. Zeitschrift für Parasitenkunde 15, 203–266.CrossRefGoogle Scholar
Obwaller, A., Sattmann, H., Konecny, R., Hörweg, C., Auer, H. & Aspöck, H. (2001) Cercarial dermatitis in Austria: the recent situation and future aspects. Helminthologia 38, 245.Google Scholar
Podhorský, M., Hůzová, Z., Mikeš, L. & Horák, P. (2009) Cercarial dimensions and surface structures as a tool for species determination of Trichobilharzia spp. Acta Parasitologica 54, 28–36.CrossRefGoogle Scholar
Richard, J. (1971) La chétotaxie des cercaires. Valeur systématique et phylétique. Mémoires du Muséum National d'Histoire Naturelle, Série A, Zoologie 67, 1–179.Google Scholar
Rudolfová, J. (2001) New findings of schistosomes in wildfowl and snails. Helminthologia 38, 248.Google Scholar
Rudolfová, J., Hampl, V., Bayssade-Dufour, C., Lockyer, A.E., Littlewood, D.T.J. & Horák, P. (2005) Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitology Research 95, 79–89.CrossRefGoogle ScholarPubMed
Rudolfová, J., Littlewood, D.T., Sitko, J. & Horák, P. (2007) Bird schistosomes of wildfowl in the Czech Republic and Poland. Folia Parasitologica 54, 88–93.CrossRefGoogle ScholarPubMed
Schets, F.M., Lodder, W.J., van Duynhoven, Y.T.H.P. & de Roda Husman, A.M. (2008) Cercarial dermatitis in the Netherlands caused by Trichobilharzia spp. Journal of Water Health 6, 187–195.CrossRefGoogle ScholarPubMed
Schets, F.M., Lodder, W.J. & De Roda Husman, A.M. (2009) Confirmation of the presence of Trichobilharzia by examination of water samples and snails following reports of cases of cercarail dermatitis. Parasitology 20, 1–7.Google Scholar
Shakarbaev, E.B. & Azimov, D.A. (2001) Trematodes of the family Bilharziellidae in the fauna of Uzbekistan. Helminthologia 38, 248.Google Scholar
Silan, P., Dubois, J.-P. & Halpenny, C. (2001) Contribution to the study of the cercarial dermatitis in the Rhône-Alpes area (France). Helminthologia 38, 245.Google Scholar
Skírnisson, K. & Kolářová, L. (2005) Swimmer's itch in Landmannalaugar, Iceland. The Icelandic Medical Journal 91, 729–736.Google ScholarPubMed
Skírnisson, K., Aldhoun, J.A. & Kolářová, L. (2009) A review on swimmers itch and the occurrence of bird schistosomes in Iceland. Journal of Helminthology 83, 165–171.CrossRefGoogle ScholarPubMed
Špakulová, M., Horák, P. & Müller, V. (1997) The karyotype of Trichobilharzia franki Müller et Kimmig, 1994 (Digenea: Schistosomatidae), a new European schistosome agent of swimmers' itch. Parasite 4, 63–66.CrossRefGoogle Scholar
Špakulová, M., Horák, P. & Dvořák, J. (2001) The karyotype of Trichobilharzia regenti Horák, Kolářová et Dvořák, 1998 (Digenea: Schistosomatidae), a nasal avian schistosome in Central Europe. Parasitology Research 87, 479–483.Google ScholarPubMed
Sturrock, R.F. (1993) The intermediate host and host–parasite relationship. pp. 33–85in Jordan, J., Webbe, G. & Sturrock, R.F. (Eds) Human schistosomiasis. Wallingford, CAB International.Google Scholar
Théron, A. (1986) Cercariometry and the epidemiology of schistosomiasis. Parasitology Today 2, 61–63.CrossRefGoogle ScholarPubMed
Valdovinos, C. & Balboa, C. (2008) Cercarial dermatitis and lake eutrophication in South-central Chile. Epidemiology and Infection 136, 391–394.CrossRefGoogle ScholarPubMed
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, 658–665.CrossRefGoogle ScholarPubMed
Wang, C.R., Chen, J., Zhano, J.P., Chen, A.H., Zhai, Y.Q., Li, L. & Zhu, X.Q. (2008) Orientobilharzia species: neglected zoonotic agents. Acta Tropica 109, 171–175.CrossRefGoogle ScholarPubMed
Wang, C.R., Ni, H.B., Zhai, Y.Q., Chen, A.H., Chen, J. & Zhu, X.Q. (2009) Orientobilharzia turkestanicum is a member of Schistosoma genus based on phylogenetic analysis using ribosomal DNA sequences. Experimental Parasitology 121, 193–197.CrossRefGoogle ScholarPubMed
Webbe, G. (1982) The intermediate host and host–parasite relationships. pp. 16–49in Jordan, P. & Webbe, G. (Eds) Schistosomiasis, epidemiology, treatment and control. London, William Heinemann Medical Books.Google Scholar
Webster, B.L., Rudolfová, J., Horák, P. & Littlewood, D.T. (2007) The complete mitochondrial genome of the bird schistosome Trichobilharzia regenti (Platyhelminthes: Digenea), causative agent of cercarial dermatitis. Journal of Parasitology 96, 553–561.CrossRefGoogle Scholar
Woolhouse, M.E.J. & Dye, C. (2001) Population biology of emerging and re-emerging pathogens. Philosophical Transactions of the Royal Society of London, Series B 356, 981–1106.CrossRefGoogle Scholar
Zbikowska, E. (2001) Bird schistosomes in Lymnaea stagnalis (L.) and Planorbarius corneus (L.) from selected lakes in Poland. Parasitology Research 89, 59–62.Google Scholar