Abstract
Nasal bird schistosomes can cause bilharziosis in birds and have the potential to cause swimmer’s itch in humans. We determined the prevalence of bird schistosomes in 106 mallards (Anas plathyrhynchos) from 11 water sources in Germany from 2014. Dissections were performed focusing on parasitic infections of the neural system. Infections with Trichobilharzia regenti (Horák et al. 1998) were found in 21% of the birds (n = 22), whereas Bilharziella polonica (Kowalewski 1895) were found between the brain membranes (meninges) and the brain, in the spinal cord or in the intestine of 12% of the mallards (n = 13). No significant influence of sex, age, and body condition between infected and non-infected animals was observed. Our study provides the first description of B. polonica from the neural system of birds and provides an epidemiological understanding of a parasite of human health concern.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2
Baker K (1993) Identification guide to European non-passerines. British trust for ornithology, Thetford
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw. doi:10.18637/jss.v067.i01
Bayssade-Dufour C, Jouet D, Rudolfova J et al (2006) Seasonal morphological variations in bird schistosomes. Parasite 13:205–214. doi:10.1051/parasite/2006133205
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
Cort WW (1928) Schistosome dermatitis in the United States (Michigan). J Am Med Assoc 90:1027–1029
Doster GL, Goater CP (1997) Collection and quantification of avian helminths and protozoa. In: Host-parasite evolution–general principles and avian models. Oxford University Press, Oxford, p 396 ± 418
Haas W, Pietsch U (1991) Migration of Trichobilharzia ocellata schistosomula in the duck and in the abnormal murine host. Parasitol Res 77:642–644. doi:10.1007/BF00931029
Horák P, Dvorák J, Kolárová L, Trefil L (1999) Trichobilharzia regenti, a pathogen of the avian and mammalian central nervous systems. Parasitology 119(Pt 6):577–581
Horák P, Kolárová L (2001) Bird schistosomes: do they die in mammalian skin? Trends Parasitol 17:66–69
Horák P, Kolářová L (2011) Snails, waterfowl and cercarial dermatitis: bird schistosomes. Freshw Biol 56:779–790. doi:10.1111/j.1365-2427.2010.02545.x
Horák P, Kolárová L, Adema CM (2002) Biology of the schistosome genus Trichobilharzia. Adv Parasitol 52:155–233
Horák P, Kolářová L, Dvořák J (1998) Trichobilharzia regenti n. sp. (Schistosomatidae, Bilharziellinae), a new nasal schistosome from Europe. Parasite 5:349–357. doi:10.1051/parasite/1998054349
Jones KE, Patel NG, Levy MA et al (2008) Global trends in emerging infectious diseases. Nature 451:990–993. doi:10.1038/nature06536
Jouet D, Ferté H, Depaquit J et al (2008) Trichobilharzia spp. in natural conditions in Annecy Lake, France. Parasitol Res 103:51–58. doi:10.1007/s00436-008-0926-3
Khalifa R (1972) Studies on schistosomatidae Looss, 1899 (Trematoda) of aquatic birds of Poland. In: I. On the life cycle of Bilharziella polonica Kowalewski, 1895, with a discussion of the subfamily Bilharziellinae Price, 1929. Acta Parasitologica Polonica, p 20:343–365
Kolárová L, Horák P, Cada F (2001) Histopathology of CNS and nasal infections caused by Trichobilharzia regenti in vertebrates. Parasitol Res 87:644–650
Kolárová 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. doi:10.1017/S0022149X09990721
Kolářová L, Skirnisson K, Horák P (1999) Schistosome cercariae as the causative agent of swimmer’s itch in Iceland. J Helminthol 73:215. doi:10.1017/S0022149X99000335
Levine ND, Clark DT, Hanson LE (1956) Encephalitis in a swan due to Dendritobilharzia sp. (Trematoda; schistosomatidae). J Parasitol 42:496. doi:10.2307/3274443
Lichtenbergová L, Kolbeková P, Kourilová P et al (2008) Antibody responses induced by Trichobilharzia regenti antigens in murine and human hosts exhibiting cercarial dermatitis. Parasite Immunol 30:585–595. doi:10.1111/j.1365-3024.2008.01059.x
Lockyer AE, Olson PD, Stergaard P et al (2003) The phylogeny of the schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126:203–224. doi:10.1017/S0031182002002792
Core Team R (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rudolfová J, Littlewood DTJ, Sitko J, Horák P (2007) Bird schistosomes of wildfowl in the Czech Republic and Poland. Folia Parasitol (Praha) 54:88–93
Rudolfová J, Sitko J, Horák P (2002) Nasal schistosomes of wildfowl in the Czech Republic. Parasitol Res 88:1093–1095. doi:10.1007/s00436-002-0634-3
Soldánová M, Selbach C, Kalbe M et al (2013) Swimmer’s itch: etiology, impact, and risk factors in Europe. Trends Parasitol 29:65–74. doi:10.1016/j.pt.2012.12.002
Sonin MD (1985) Key to the determination of trematodes infecting fish eating birds in the Palearctic region I. Publishing House AN SSSR, Moskow
Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197
van der Werf MJ, de Vlas SJ, Brooker S et al (2003) Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 86:125–139. doi:10.1016/S0001-706X(03)00029-9
Wiethoelter AK, Beltrán-Alcrudo D, Kock R, Mor SM (2015) Global trends in infectious diseases at the wildlife–livestock interface. Proc Natl Acad Sci 112:9662–9667. doi:10.1073/pnas.1422741112
Wojcinski ZW, Barker IK, Hunter DB, Lumsden H (1987) An outbreak of schistosomiasis in Atlantic Brant geese, Branta bernicla hrota. J Wildl Dis 23:248–255. doi:10.7589/0090-3558-23.2.248
Acknowledgements
This research was undertaken as part of the Graduate School IMPact-Vector funded by the Senate Competition Committee grant (SAW-2014-SGN-3) of the Leibniz Association. We thank Prof. Petr Horák from the Prague University and his co-workers, especially Jana Bulantová and Roman Leontovyč, for their assistance with the necropsies and genetic methods, all the collaborating hunters, the lab assistants Nina Hartmann, Sophie Ewert, Lisa Giese, Lorena Derezanin, and our supportive colleagues Susanne Auls, Manuela Merling de Chapa, Ines Lesniak, and Mathias Franz.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Prüter, H., Sitko, J. & Krone, O. Having bird schistosomes in mind—the first detection of Bilharziella polonica (Kowalewski 1895) in the bird neural system. Parasitol Res 116, 865–870 (2017). https://doi.org/10.1007/s00436-016-5359-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-016-5359-9