The life cycle of the potentially zoonotic trematode Metagonimus romanicus (Digenea: Heterophyidae): New insights from published and original data

. 2025 Sep ; 40 () : e00276. [epub] 20250705

Status PubMed-not-MEDLINE Jazyk angličtina Země Nizozemsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40697615
Odkazy

PubMed 40697615
PubMed Central PMC12281539
DOI 10.1016/j.fawpar.2025.e00276
PII: S2405-6766(25)00023-X
Knihovny.cz E-zdroje

Fish-borne zoonoses are emerging worldwide, and although most human cases remain confined to tropical regions, particularly Southeast and East Asia, a few cases have been reported in Europe. This review summarizes published and new data on the life cycle of Metagonimus romanicus (misidentified as M. yokogawai, a human pathogen common in East Asia), a heterophyid trematode and one of the potentially fish-borne parasites in Europe. Metagonimus romanicus is distributed from the middle Danube in Central Europe (Slovakia) to eastern Ukraine (including the rivers of the Black Sea basin). Its distribution area coincides with that of its first intermediate hosts, the melanopsid snails Microcolpia daudebartii acicularis and Esperiana esperi. While M. romanicus most likely has a strict specificity for its first snail hosts, metacercariae are generalists and have been detected in over 50 freshwater fish species from 18 families, especially leuciscids. Despite its wide distribution and frequent occurrence in freshwater fish, the zoonotic potential of M. romanicus appears to be low. This is probably due to the exclusive localization of the metacercariae in the fish scales rather than musculature, as well as the rare consumption of raw or undercooked fish in Europe. However, some risk remains and a small number of undiagnosed human infections due to accidental ingestion of scales during the preparation and cleaning of fish cannot be ruled out.

Zobrazit více v PubMed

Abràmoff M.D., Magalhães P.J., Ram S.J. Image processing with Image. J. Biophotonics Int. 2004;11:36–42.

Arabuli L., Murvanidze L., Faltýnková A., Mumladze L. Checklist of digeneans (Platyhelminthes, Trematoda, Digenea) of Georgia. Biodivers. J. 2024;12 doi: 10.3897/BDJ.12.e110201. PubMed DOI PMC

Besprozvannykh V.V. In: Investigation in Parasitology. Lebedev B.I., editor. Academy of Sciences of the USSR; Far Eastern Branch, Vladivostok: 1989. The fauna of trematode larvae of the genus Juga (Gastropoda: Pachychilidae) molluscs from the far-eastern rivers of the USSR; pp. 82–96. (in Russian)

Besprozvannykh V.V. Dalnauka; Vladivostok: 2000. Fauna, Biology, and Ecology of Parthenites and Cercariae of Trematodes in Snails of Genus Juga (Pachychilidae) from Rivers in Primorsky Region. (in Russian)

Bikashvili A., Mumladze L., Glaubrecht M., Neiber M.T. Trapped in a glacial refugium: phylogeography of the freshwater snail Melanopsis mingrelica (Mollusca, Gastropoda) in the Caucasus biodiversity hotspot. Zool. Scr. 2025;54:332–351. doi: 10.1111/zsc.12713. DOI

Bray R.A., Waeschenbach A., Cribb T., Weedall G., Dyal P., Littlewood D. The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: implications for their systematics and evolution. Acta Parasitol. 2009;54:310–329. doi: 10.2478/s11686-009-0045-z. DOI

Cakić P., Paunović M., Stojanović B., Ðikanović V., Kulišić Z. Metagonimus yokogawai (Katsurada, 1912), a new parasitic Trematoda species in ichtyoparasitofauna of the Serbia. Acta Vet. Brno. 2007;57:537–543. doi: 10.2298/avb0706537c. DOI

Cech G., Gyöngy M., Sándor D., Kálmán M., Boglárka S., Ádám V., Csaba S. Molecular evidence of the absence of Metagonimus yokogawai (Katsurada, 1912) in Europe: report of Metagonimus sp. in cyprinoid fish from the river Danube in Hungary. Parasitol. Res. 2023;122:2325–2334. doi: 10.1007/s00436-023-07932-1. PubMed DOI PMC

Čejka, T., 2011. From the Red Book of our molluscs –

Chai J.Y. Springer; Dordrecht: 2019. Human Intestinal Flukes: From Discovery to Treatment and Control. DOI

Chai J.Y., Jung B.K. In: Encyclopedia of Food Safety. Smithers G.W., editor. Elsevier; Oxford: 2024. Metagonimus yokogawai and other Metagonimus species; pp. 663–672. DOI

Chai J.Y., Darwin M., Lymbery A.J. Fish-borne parasitic zoonoses: status and issues. Int. J. Parasitol. 2005;35:1233–1254. doi: 10.1016/j.ijpara.2005.07.013. PubMed DOI

Chai J.Y., Shin E.H., Lee S.H., Rim H.J. Foodborne intestinal flukes in Southeast Asia. Korean J. Parasitol. 2009;47:S69–102. doi: 10.3347/kjp.2009.47.S.S69. PubMed DOI PMC

Chernomor O., von Haeseler A., Minh B.Q. Terrace aware data structure for phylogenomic inference from supermatrices. Syst. Biol. 2016;65:997–1008. doi: 10.1093/sysbio/syw037. PubMed DOI PMC

Chervy L. Manual for the study of tapeworms (Cestoda) parasitic in ray-finned fish, amphibians and reptiles. Folia Parasitol. 2024;71:1. doi: 10.14411/fp.2024.001. PubMed DOI

Ciurea I. Über einige neue Distomen aus dem Darm unserer Haustiere und des Pelikans, für welche die Fische als Infektionsquelle zu betrachten sind. Zeit. Infekt. Parasit. Krank. Hyg. Haust. 1915;16:445–458.

Ciurea I. Les vers parasites de l’homme, des mammifères et des oiseaux provenant des poissons du Danube et de la mer Noire. Arch. Roum. Pathol. Exp. Microbiol. 1933;6:5–134.

Ciurea I. Sur quelques larves des Vers parasites de I’homme, des mammiferes et des Oiseaux ichtyopages, trouveés chez les poissons des grands lacs de la Bessarabie, du Dniester et de son Liman. Arch. Roum. Pathol. Exp. Microbiol. 1933;6:151–170.

Davis G.M. A taxonomic study of some species of Semisulcospira in Japan (Mesogastropoda: Pleuroceridae) Malacologia. 1969;7:211–294.

Dzhikia V.V. Vol. 1. Gruzmedgiz; Tbilisi: 1934. Helminthofauna of Dogs from Georgia; pp. 3–14. (in Russian)

Dzikowski R., Levy M.G., Poore M.F., Flowers J.R., Paperna I. Use of rDNA polymorphism for identification of Heterophyidae infecting freshwater fishes. Dis. Aquat. Org. 2004;59:35–41. doi: 10.3354/dao059035. PubMed DOI

Engashev S.V., Shakhmurzov M.M., Bittirov A.M., Alieva K.G., Kaloshkina I.M., Medvedeva A.M. Epizootic and epidemic risks of the trematode Metagonimus yokogawai Katsurada, 1912 in Dagestan, as a biological threat to aquaculture of natural reservoirs and the population in the basin river Terek. Vet. Kubani. 2021;6:21.

Faltýnková A., Našincová V., Kablásková L. Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gastropoda, Pulmonata) in Central Europe: a survey of species and key to their identification. Parasite. 2007;14:39–51. doi: 10.1051/parasite/2007141039. PubMed DOI

Faltýnková A., Našincová V., Kablásková L. Larval trematodes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in Central Europe: a survey of species and key to their identification. Syst. Parasitol. 2008;69:155–178. doi: 10.1007/s11230-007-9127-1. PubMed DOI

Faltýnková A., Sures B., Kostadinova A. Biodiversity of trematodes in their intermediate mollusc and fish hosts in the freshwater ecosystems of Europe. Syst. Parasitol. 2016;93:283–293. doi: 10.1007/s11230-016-9627-y. PubMed DOI

Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 1994;3:294–299. PubMed

Francová K., Ondračková M., Polačik M., Jurajda P. Parasite fauna of native and non-native populations of Neogobius melanostomus (Pallas, 1814) (Gobiidae) in the longitudinal profile of the Danube River. J. Appl. Ichthyol. 2011;27:879–886. doi: 10.1111/j.1439-0426.2010.01582.x. DOI

Glöer P. Volume 1: Fresh- and Brakish Waters except Spring and Subterranean Snails. Published by the author, Biodiversity Research Lab; Hetlingen: 2019. The freshwater gastropods of the west-Palaearctis.

Gradowski V.M. Trematodes of the molluscs of the family Melanopsidae (Gastropoda, Pectinibranchia, Cerithiiformes) from the Western Polesie area, with description of new cercaria. Vestn. Zool. 1999;33:83–87. (in Russian)

Grevtseva M.A. VNIIGIS; Moscow: 1979. Helminth Fauna and Helminthoses of Fish in the Vyatka River Basin. Dissertation. (in Russian)

Gyöngy M., Sellyei B., Czeglédi I., Székely C., Cech G. Viability of Metagonimus romanicus (Ciurea, 1915) metacercariae after physico-chemical treatments. Food Waterborne Parasitol. 2024;36 doi: 10.1016/j.fawpar.2024.e00236. PubMed DOI PMC

Hoang D.T., Chernomor O., von Haeseler A., Minh B.Q., Vinh L.S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 2018;35:518–522. doi: 10.1093/molbev/msx281. PubMed DOI PMC

Horsák M., Juřičková L., Picka J. Kabourek; Zlín: 2013. Molluscs of the Czech and Slovak Republics.

Iskova N.I., Sharpilo V.P., Sharpilo L.D., Tkach V.V. Institut Zoologii; Kyiv: 1995. Catalogue of Helminths of Ukraine: Trematodes of Terrestrial Vertebrates, Natsional’na Akademiya Nauk Ukraine. (in Ukrainian)

Ismail N.S., Abdel-Hafez S.K., Toor M.A. Prevalence of gastrointestinal helminthes in cats from northern Jordan. Pak. Vet. J. 1983;3:129–132.

Ivasiuk Y., Losev A. Trematodes of gastropods of Kyiv reservoir. Sci. Issue Tern. Volod. H. Na.L Ped. Univ. 2019;78:11–15. (in Ukrainian)

Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A., Jermiin L.S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC

Kanarek G., Zaleśny G. Extrinsic- and intrinsic-dependent variation in component communities and patterns of aggregations in helminth parasites of great cormorant (Phalacrocorax carbo) from N.E. Poland. Parasitol. Res. 2014;113:837–850. doi: 10.1007/s00436-013-3714-7. PubMed DOI PMC

Kantor Y.I., Vinarski M.V., Schileyko A.A., Sysoev A.V. Catalogue of the Continental Mollusks of Russia and Adjacent Territories, Version 2.3.1. 2010. http://konstantinz.byethost32.com/books/kantor_2010.pdf?i=1 published online, Moscow.

Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Kostarev G.F. Perm University Publishing House; Perm: 2003. Parasites and Diseases of the Fish of the Middle Kama Basin under Pollution. (in Russian)

Koval B.P. Digenetic trematodes of fishes of the lower Dnieper. Tr. Biol. Fakul. Kyiv. Derzh. Univer. 1950;5:187–207. (in Russian)

Kozlov D.P. Nauka; Leningrad: 1977. Guide for the Determination of the Helminths of Carnivores of USSR. (in Russian)

Lamková K., Šimková A., Palíková M., Jurajda P., Lojek A. Seasonal changes of immunocompetence and parasitism in chub (Leuciscus cephalus), a freshwater cyprinid fish. Parasitol. Res. 2007;101:775–789. doi: 10.1007/s00436-007-0546-3. PubMed DOI

Leonov V.A. Dynamics of the helminth fauna of the herring gull nesting on the territory of the Black Sea nature reserve. Uchen. Zap. Gorkov. Gosud. Pedag. Instit. 1960;27:38–57. (in Russian)

Littlewood D.T.J., Olson P.D. In: Interrelationships of the Platyhelminthes. Littlewood D.T.J., Bray R.A., editors. Taylor & Francis; London: 2001. Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise; pp. 262–278. DOI

Ložek V. Publishing House of the Slovak Academy of Sciences; Bratislava. (in Czech): 1956. Key to Czechoslovak Molluscs.

Manafov A.A. Some results of the study of the trematode fauna of the freshwater mollusk Melanopsis praemorsa (L.) in the water bodies of Azerbaijan. Parazitologiya. 2011;45:367–378. (in Russian) PubMed

Markevich A.P. Izdavatelstvo Akademii Nauk USSR; Kyiv: 1951. Parasite Fauna of Freshwater Fish of the Ukrainian SSR. (in Russian)

Minh B.Q., Schmidt H.A., Chernomor O., Schrempf D., Woodhams M.D., von Haeseler A., Lanfear R. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 2020;37:1530–1534. doi: 10.1093/molbev/msaa015. PubMed DOI PMC

Molodozhnikova N.M., Zhokhov A.E. The taxonomic diversity of the parasites of fishes in the Volga basin. III. Aspidogastrea and Trematoda. Parazitologiya. 2007;41:28–54. (in Russian) PubMed

Neiber M.T., Glaubrecht M. Unparalleled disjunction or unexpected relationships? Molecular phylogeny and biogeography of Melanopsidae (Caenogastropoda: Cerithioidea), with the description of a new family and a new genus from the ancient continent Zealandia. Cladistics. 2019;35:401–425. doi: 10.1111/cla.12361. PubMed DOI

Olenev A.V. In: Ecology and Experimental Parasitology. Polyanski Y.I., editor. Leningradskiy Gosudarstvennii Universitet; St. Petersburg: 1979. Cercarial fauna of the freshwater mollusk Melanopsis praemorsa (L.) from Western Georgia; pp. 30–41. (in Russian)

Olson P.D., Cribb T.H., Tkach V.V., Bray R.A., Littlewood D.T.J. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda) Int. J. Parasitol. 2003;33:733–755. doi: 10.1016/s0020-7519(03)00049-3. PubMed DOI

Percie du Sert N., Hurst V., Ahluwalia A., et al. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. BMC Vet. Res. 2020;16(242) doi: 10.1186/s12917-020-02451-y. PubMed DOI PMC

Rácz O.Z., Zemankovics E. Survival of metacercariae of Metagonimus yokogawai (Digenea: Heterophyidae) on fish from river Danube. Hung. Vet. J. 2002;124:437–444. (in Hungarian)

Rodonaya T.E. Metsniereba. Nauka; Tbilisi: 1967. About Detection of Trematodes of USSR – Dexiogonimus ciureanus Witenberg, 1929, in: Gelmintofauna Zhivotnykh i Rastelniy v Gruzii; pp. 95–97. (in Russian)

Scholz T., Kuchta R., Barčák D., Cech G., Oros M. Small intestinal flukes of the genus Metagonimus (Digenea: Heterophyidae) in Europe and the Middle East: a review of parasites with zoonotic potential. Parasite. 2024;31:20. doi: 10.1051/parasite/2024016. PubMed DOI PMC

Semyonova N.N., Ivanov V.P., Ivanov V.M. ASTU Publishing House; Astrakhan: 2007. Parasite Fauna and Diseases of Fish in the Caspian Sea. (in Russian)

Shumenko P.G., Tatonova Y.V., Besprozvannykh V.V. Metagonimus suifunensis sp. n. (Trematoda: Heterophyidae) from the Russian southern Far East: morphology, life cycle, and molecular data. Parasitol. Int. 2017;66:982–991. doi: 10.1016/j.parint.2016.11.002. PubMed DOI

Sitko J., Faltýnková A., Scholz T. Academia; Prague: 2006. Checklist of the Trematodes (Digenea) of Birds of the Czech and Slovak Republics.

Soldánová M., Selbach C., Sures B., Kostadinova A., Pérez-Del-Olmo A. Larval trematode communities in Radix auricularia and Lymnaea stagnalis in a reservoir system of the Ruhr River. Parasit. Vectors. 2010;3:56. doi: 10.1186/1756-3305-3-56. PubMed DOI PMC

Starobogatov Y.A.I., Prozorova L.A., Bogatov V.V., Saenko E.M. In: Key to Freshwater Invertebrates of Russia and Adjacent Lands. Tsalolikhin, S.Ya., editor. vol. 6. Nemerteans. Nauka, St. Petersburg; Molluscs, Polychaetes: 2004. Molluscs; pp. 9–492. (in Russian)

Strong E.E., Köhler F. Morphological and molecular analysis of ‘Melania’ jacqueti Dautzenberg and Fischer, 1906: from anonymous orphan to critical basal offshoot of the Semisulcospiridae (Gastropoda: Cerithioidea) Zool. Scr. 2009;38:483–502. doi: 10.1111/j.1463-6409.2008.00385.x. DOI

Tatonova Y.V., Shumenko P.G., Besprozvannykh V.V. Description of Metagonimus pusillus sp. nov. (Trematoda: Heterophyidae): phylogenetic relationships within the genus. J. Helminthol. 2013;92:703–712. doi: 10.1017/s0022149x17001146. PubMed DOI

Tomović J., Paunović M., Atanacković A., Marković V., Gačić Z., Csányi B., Simić V. Biotic typology of the Danube River based on distribution of mollusc fauna as revealed by the second joint Danube survey (2007) Acta Zool. Bulgar. 2014;66:527–537.

Tytar V., Makarova N. Distribution of the freshwater snail species Fagotia (Gastropoda, Melanopsidae) in Ukraine according to climatic factors. I. Fagotia esperi. Vestn. Zool. 2015;49:341–350.

Vojtek J. Metacercariae from fishes of Czechoslovakia. Folia Fac. Sci. Nat. Univ. Purkynianae Brun. 1974;15:13–51. (in Czech).

Werle E., Schneider C., Renner M., Völker M., Fiehn W. Convenient single-step, one tube purification of PCR products for direct sequencing. Nucl. Acids Res. 1994;22:4354–4355. doi: 10.1093/nar/22.20.4354. PubMed DOI PMC

Witenberg G. Studies on the trematode–family Heterophyidae. An. Trop. Med. Parasitol. 1929;23:131–239. doi: 10.1080/00034983.1929.11684600. DOI

Xiao L., Ryan U., Feng Y. CRC Press/Taylor & Francis Group; Boca Raton: 2015. Biology of Foodborne Parasites. DOI

Zdun V.I. Publishing House of the Ukrainian Academy of Sciences; Kyiv: 1961. Larval Trematodes in Freshwater Molluscs of the Ukraine. (in Russian)

Zhokhov A.E., Pugacheva M.N., Molodozhnikova N.M., Berechikidze I.A. Alien parasite species of the fish in the Volga River basin: a review of data on the species number and distribution. Russ. J. Biol. Inv. 2019;10:136–152. doi: 10.1134/s2075111719020140. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...