The avian schistosome Trichobilharzia franki in mice: Migration, pathogenicity, and the host immune response
Status PubMed-not-MEDLINE Jazyk angličtina Země Nizozemsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
41017965
PubMed Central
PMC12466281
DOI
10.1016/j.fawpar.2025.e00289
PII: S2405-6766(25)00036-8
Knihovny.cz E-zdroje
- Klíčová slova
- Avian schistosomes, Cercarial dermatitis, Lungs, Skin, Trichobilharzia franki,
- Publikační typ
- časopisecké články MeSH
Cercarial dermatitis (CD; swimmer's itch) is a re-emerging skin disease caused by avian schistosomes, including Trichobilharzia franki. Here, we present morphological, genetic, and experimental evidence confirming the involvement of T. franki in recent CD outbreaks across Czechia. Ocellate furcocercariae were collected from Radix auricularia at four sites and identified as T. franki through ITS1 sequencing. Despite minor morphological differences from previously reported specimens, all isolates belonged to the genetically uniform T. franki "auricularia" clade. Experimental infection of mice with T. franki resulted in a ∼ 60 % penetration rate, accompanied by early-onset scratching and transient weight loss. Gross pathology demonstrated hemorrhages on lung surfaces and splenic atrophy at 2 days post-infection (dpi), along with a prominent enlargement of parotid lymph nodes at both 2 and 7 dpi. Histological examination of the skin revealed viable schistosomula, moderate leukocyte infiltration, epidermal hyperplasia, and the formation of hyperkeratotic crusts at 2 dpi. By 7 dpi, parasites were no longer detectable, but epidermal pathology persisted. In the lungs, eosinophil-rich foci and multifocal hemorrhages were observed at 2 dpi, transitioning to neutrophil-dominated lesions at 7 dpi, despite the absence of detectable schistosomula. Splenocytes from infected mice responded to homologous and heterologous cercarial antigens by producing IFN gamma, IL-4, and IL-10, indicating a mixed Th1/Th2/Treg profile and notable species cross-reactivity. However, parasite-specific IgG remained undetectable at 7 dpi. These findings confirm T. franki as the causative agent of CD outbreaks and underscore its capacity to induce localized and systemic pathology and immune response, cross-reacting with other schistosomes.
Department of Biology University of York York UK
Department of Parasitology Faculty of Science Charles University Prague Czechia
York Biomedical Research Institute University of York York UK
Zobrazit více v PubMed
Almeyda-Artigas R.J., Bargues M.D., Mas-Coma S. ITS-2 rDNA sequencing of Gnathostoma species (Nematoda) and elucidation of the species causing human gnathostomiasis in the Americas. J. Parasitol. 2000;86:537–544. doi: 10.1645/0022-3395(2000)086[0537:IRSOGS]2.0.CO;2. PubMed DOI
Ashrafi K., Sharifdini M., Darjani A., Brant S.V. Migratory routes, domesticated birds and cercarial dermatitis: the distribution of Trichobilharzia franki in northern Iran. Parasite. 2021;28:4. doi: 10.1051/parasite/2020073. PubMed DOI PMC
Bayssade-Dufour C., Martins C., Vuong P. Histopathologie pulmonaire d’un modèle mammifère et dermatite cercarienne humaine. Médecine Mal. Infect. 2001;31:713–722. doi: 10.1016/S0399-077X(01)00297-9. DOI
Bayssade-Dufour C., Vuong P.N., René M., Martin-Loehr C., Martins C. Lésions viscérales de mammifères et oiseaux,exposés aux agents de dermatite cercarienne. Bull. Soc. Pathol. Exot. 2002;95:229–237. PubMed
Bispo M.T., Calado M., Maurício I.L., Ferreira P.M., Belo S. Zoonotic threats: the (re)emergence of cercarial dermatitis, its dynamics, and impact in Europe. Pathogens. 2024;13:282. doi: 10.3390/pathogens13040282. PubMed DOI PMC
Bourke C.D., Prendergast C.T., Sanin D.E., Oulton T.E., Hall R.J., Mountford A.P. Epidermal keratinocytes initiate wound healing and pro-inflammatory immune responses following percutaneous schistosome infection. Int. J. Parasitol. 2015;45:215–224. doi: 10.1016/j.ijpara.2014.11.002. PubMed DOI PMC
Chanová M., Vuong S., Horák P. Trichobilharzia szidati: the lung phase of migration within avian and mammalian hosts. Parasitol. Res. 2007;100:1243–1247. doi: 10.1007/s00436-006-0398-2. PubMed DOI
Cort W.W. Schistosome dermatitis in the United States (Michigan) JAMA. 1928;90:1027–1029. doi: 10.1001/jama.1928.02690400023010. PubMed DOI
Crabtree J.E., Wilson R.A. Schistosoma mansoni: an ultrastructural examination of pulmonary migration. Parasitology. 1986;92:343–354. doi: 10.1017/S0031182000064118. PubMed DOI
Guindon S., Dufayard J.-F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI
Haas W., Pietsch U. Migration of Trichobilharzia ocellata schistosomula in the duck and in the abnormal murine host. Parasitol. Res. 1991;77:642–644. doi: 10.1007/BF00931029. PubMed DOI
Helmer N., Blatterer H., Hörweg C., Reier S., Sattmann H., Schindelar J., Szucsich N.U., Haring E. First record of Trichobilharzia physellae (Talbot, 1936) in Europe, a possible causative agent of cercarial dermatitis. Pathogens. 2021;10:1473. doi: 10.3390/pathogens10111473. PubMed DOI PMC
Horák P., Kolářová L. Survival of bird schistosomes in mammalian lungs. Int. J. Parasitol. 2000;30:65–68. doi: 10.1016/S0020-7519(99)00174-5. PubMed DOI
Horák P., Mikeš L., Lichtenbergová L., Skála V., Soldánová M., Brant S.V. Avian schistosomes and outbreaks of cercarial dermatitis. Clin. Microbiol. Rev. 2015;28:165–190. doi: 10.1128/CMR.00043-14. PubMed DOI PMC
Incani R.N., McLaren D.J. Histopathological and ultrastructural studies of cutaneous reactions elicited in naive and chronically infected mice by invading schistosomula of Schistosoma mansoni. Int. J. Parasitol. 1984;14:259–276. doi: 10.1016/0020-7519(84)90077-8. PubMed DOI
Inclan-Rico J.M., Napuri C.M., Lin C., Hung L.-Y., Ferguson A.A., Liu X., Wu Q., Pastore C.F., Stephenson A., Femoe U.M., Musaigwa F., Rossi H.L., Freedman B.D., Reed D.R., Macháček T., Horák P., Abdus-Saboor I., Luo W., Herbert D.R. MrgprA3 neurons drive cutaneous immunity against helminths through selective control of myeloid-derived IL-33. Nat. Immunol. 2024;25:2068–2084. doi: 10.1038/s41590-024-01982-y. PubMed DOI PMC
Jouet D., Ferté H., Depaquit J., Rudolfová J., Latour P., Zanella D., Kaltenbach M.L., Léger N. Trichobilharzia spp. in natural conditions in Annecy Lake, France. Parasitol. Res. 2008;103:51–58. doi: 10.1007/s00436-008-0926-3. PubMed DOI
Jouet D., Ferté H., Hologne C., Kaltenbach M.L., Depaquit J. Avian schistosomes in French aquatic birds: a molecular approach. J. Helminthol. 2009;83:181–189. doi: 10.1017/S0022149X09311712. PubMed DOI
Jouet D., Skírnisson K., Kolářová L., Ferté H. Molecular diversity of Trichobilharzia franki in two intermediate hosts (Radix auricularia and Radix peregra): a complex of species. Infect. Genet. Evol. 2010;10:1218–1227. doi: 10.1016/j.meegid.2010.08.001. PubMed DOI
Kock S. Investigations of intermediate host specificity help to elucidate the taxonomic status of Trichobilharzia ocellata (Digenea: Schistosomatidae) Parasitology. 2001;123:67–70. doi: 10.1017/S0031182001008101. PubMed DOI
Kouřilová P., Kolářová L. Variations in immunofluorescent antibody response against Trichobilharzia and Schistosoma antigens in compatible and incompatible hosts. Parasitol. Res. 2002;88:513–521. doi: 10.1007/s00436-002-0607-6. PubMed DOI
Kouřilová P., Hogg K.G., Kolářová L., Mountford A.P. Cercarial dermatitis caused by bird schistosomes comprises both immediate and late phase cutaneous hypersensitivity reactions. J. Immunol. 2004;172:3766–3774. doi: 10.4049/jimmunol.172.6.3766. PubMed DOI
Lawton S.P., Lim R.M., Dukes J.P., Cook R.T., Walker A.J., Kirk R.S. 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. 2014;7:277. doi: 10.1186/1756-3305-7-277. PubMed DOI PMC
Leigh J.W., Bryant D. POPART: full-feature software for haplotype network construction. Methods Ecol. Evol. 2015;6:1110–1116. doi: 10.1111/2041-210X.12410. DOI
Loker E.S., DeJong R.J., Brant S.V. Scratching the itch: updated perspectives on the schistosomes responsible for swimmer’s itch around the world. Pathogens. 2022;11:587. doi: 10.3390/pathogens11050587. PubMed DOI PMC
Macháček T., Turjanicová L., Bulantová J., Hrdý J., Horák P., Mikeš L. Cercarial dermatitis: a systematic follow-up study of human cases with implications for diagnostics. Parasitol. Res. 2018;117:3881–3895. doi: 10.1007/s00436-018-6095-0. PubMed DOI
Macháček T., Leontovyč R., Šmídová B., Majer M., Vondráček O., Vojtěchová I., Petrásek T., Horák P. Mechanisms of the host immune response and helminth-induced pathology during Trichobilharzia regenti (Schistosomatidae) neuroinvasion in mice. PLoS Pathog. 2022;18 doi: 10.1371/journal.ppat.1010302. PubMed DOI PMC
Macháček T., Fuchs C.D., Winkelmann F., Frank M., Scharnagl H., Stojakovic T., Sombetzki M., Trauner M. Bsep/Abcb11 knockout ameliorates Schistosoma mansoni liver pathology by reducing parasite fecundity. Liver Int. 2023;43:2469–2478. doi: 10.1111/liv.15710. PubMed DOI PMC
Majer M., Macháček T., Súkeníková L., Hrdý J., Horák P. The peripheral immune response of mice infected with a neuropathogenic schistosome. Parasite Immunol. 2020;42 doi: 10.1111/pim.12710. PubMed DOI
Mudavanhu A., Schols R., Goossens E., Nhiwatiwa T., Manyangadze T., Brendonck L., Huyse T. One health monitoring reveals invasive freshwater snail species, new records, and undescribed parasite diversity in Zimbabwe. Parasit. Vectors. 2024;17:234. doi: 10.1186/s13071-024-06307-4. PubMed DOI PMC
Müller V., Kimmig P. Trichobilharzia franki n. sp. – die Ursache für Badedermatitiden in südwestdeutschen Baggerseen. Appl. Parasitol. 1994;35:12–31. PubMed
Nation C.S., Da’dara A.A., Marchant J.K., Skelly P.J. Schistosome migration in the definitive host. PLoS Negl. Trop. Dis. 2020;14 doi: 10.1371/journal.pntd.0007951. PubMed DOI PMC
Olivier L. Schistosome dermatitis, a sensitization phenomenon. Am. J. Epidemiol. 1949;49:290–302. doi: 10.1093/oxfordjournals.aje.a119279. PubMed DOI
Olivier L. Observations on the migration of avian schistosomes in mammals previously unexposed to cercariae. J. Parasitol. 1953;39:237–246. doi: 10.2307/3273943. PubMed DOI
Olivier L., Weinstein P.P. Experimental schistosome dermatitis in rabbits. J. Parasitol. 1953;39:280. doi: 10.2307/3273951. PubMed DOI
Pedersen E.M., Christensen N.Ø., Frandsen F. Reduction in the severity of hepatosplenic schistosomiasis mansoni in mice by previous exposure to cercariae of the bird schistosome Trichobilharzia szidati. J. Helminthol. 1982;56:1–3. doi: 10.1017/S0022149X0003491X. PubMed DOI
Peterková K., Konečný L., Macháček T., Jedličková L., Winkelmann F., Sombetzki M., Dvořák J. Winners vs. losers: Schistosoma mansoni intestinal and liver eggs exhibit striking differences in gene expression and immunogenicity. PLoS Pathog. 2024;20 doi: 10.1371/journal.ppat.1012268. PubMed DOI PMC
Piipponen M., Li D., Landén N.X. The immune functions of keratinocytes in skin wound healing. Int. J. Mol. Sci. 2020;21:8790. doi: 10.3390/ijms21228790. PubMed DOI PMC
Podhorský M., Hůzová Z., Mikeš L., Horák P. Cercarial dimensions and surface structures as a tool for species determination of Trichobilharzia spp. Acta Parasitol. 2009;54:28–36. doi: 10.2478/s11686-009-0011-9. DOI
Procházka J., Bartoníček Z., Leontovyč R., Horák P., Macháček T. Molecular detection and identification of Trichobilharzia: development of a LAMP, qPCR, and multiplex PCR toolkit. Parasit. Vectors. 2025;18:195. doi: 10.1186/s13071-025-06822-y. PubMed DOI PMC
Reier S., Haring E., Billinger F., Blatterer H., Duda M., Gorofsky C., Grasser H.P., Heinisch W., Hörweg C., Kruckenhauser L., Szucsich N.U., Wanka A., Sattmann H. First confirmed record of Trichobilharzia franki Müller & Kimmig, 1994, from Radix auricularia (Linnaeus, 1758) for Austria. Parasitol. Res. 2020;119:4135–4141. doi: 10.1007/S00436-020-06938-3. PubMed DOI PMC
Rudko S.P., Turnbull A., Reimink R.L., Froelich K., Hanington P.C. Species-specific qPCR assays allow for high-resolution population assessment of four species avian schistosome that cause swimmer’s itch in recreational lakes. Int. J. Parasitol. Parasites Wildl. 2019;9:122–129. doi: 10.1016/j.ijppaw.2019.04.006. PubMed DOI PMC
Rudolfová J., Hampl V., Bayssade-Dufour C., Lockyer A.E., Littlewood D.T.J., Horák P. Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitol. Res. 2005;95:79–89. doi: 10.1007/s00436-004-1262-x. PubMed DOI
Soldánová M., Kundid P., Scholz T., Kristoffersen R., Knudsen R. Somatic dimorphism in cercariae of a bird schistosome. Pathogens. 2022;11:3. doi: 10.3390/pathogens11030290. PubMed DOI PMC
Spina, F., Baillie, S., Bairlein, F., Fiedler, W., Thorup, K., 2022a. Mallard:
Spina, F., Baillie, S., Bairlein, F., Fiedler, W., Thorup, K., 2022b. Mute Swan:
Templeton A.R., Crandall K.A., Sing C.F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics. 1992;132:619–633. doi: 10.1093/genetics/132.2.619. PubMed DOI PMC
Vondráček O., Mikeš L., Talacko P., Leontovyč R., Bulantová J., Horák P. Differential proteomic analysis of laser-microdissected penetration glands of avian schistosome cercariae with a focus on proteins involved in host invasion. Int. J. Parasitol. 2022;52:343–358. doi: 10.1016/j.ijpara.2021.12.003. PubMed DOI
Wulff C., Haeberlein S., Haas W. Cream formulations protecting against cercarial dermatitis by Trichobilharzia. Parasitol. Res. 2007;101:91–97. doi: 10.1007/s00436-006-0431-5. PubMed DOI
Yang C., Ding S., Niu Y., Zhang X., Li J. Characteristics of macrobenthic communities and their response to environmental changes in east Taihu Lake, China. Environ. Monit. Assess. 2025;197:642. doi: 10.1007/s10661-025-14084-5. PubMed DOI