Skip to main content
SpringerLink
Log in

Import of exotic and zoonotic trematodes (Heterophyidae: Centrocestus sp.) in Xiphophorus maculatus: Implications for ornamental fish import control in Europe

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Ornamental fish, Xiphophorus maculatus, were imported from Singapore to Denmark for distribution to local aquarists. Importers observed lethargic and erratic swimming patterns among fish and forwarded a total of 30 fish for pathological examination to a university diagnostic service. All fish were diagnosed infected with encysted Centrocestus sp. metacercariae in gills (prevalence of 100% and mean intensity of 454.5 ± 161.9 parasites per fish). Metacercariae were identified by morphological and molecular methods. Cysts (mean length 163.3 ± 13.7 μm and mean width 113.3 ± 10.6 μm) contained a bent metacercaria with an X-shaped excretory bladder. PCR amplification of a rDNA region (5.8S rRNA gene, ITS-2, 28S rRNA gene) and subsequent sequencing confirmed the diagnosis. Metacercariae were found in gill filaments adjacent to the cartilage associated with cartilage hypertrophy, epithelial and mucous cell hyperplasia, clubbing and lamellar fusion. Host cell encapsulation of cysts comprised several layers of leucocytes, chondroblast-like and fibroblast-like cells. The observations raise concerns with regard to veterinary inspection and quarantine procedures. The zoonotic potential of these trematodes and a possible spread of the parasites in natural habitats in Europe should be regarded as a public health issue. So far, several cases of human infections have been reported only in Asia, but the potential intermediate host snail, Melanoides tuberculata, has been recorded in Germany. Accordingly, establishment of the parasite in Europe with climate changes should be considered a risk.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amaya-Huerta D., Almeyda-Artigas J. 1994. Confirmation of Centrocestus formosanus (Nishigori, 1924) Price, 1932 (Trematoda: Heterophyidae) in Mexico. Research and Reviews in Parasitology, 54, 99–103.

    Google Scholar 

  • Anon. 2012. Importing and exporting live fish, molluscs and crustacean, Centre for Environment, Fisheries and Aquaculture Science. Available at: www.gov.uk

  • Boeger W.A., Piasecki W., Sobecka E. 2002. Neotropical Monogenoidea. 44. Mymarothecium viatorum sp.n. [Ancyrocephalinae] from the gills of Piaractus brachypomus [Serrasalmidae, Teleostei] captured in a warm-water canal of a power plant in Szczecin, Poland. Acta Ichthyologica et Piscatoria, 32, 157–161.

    Google Scholar 

  • Bolaji D.A., Edokpayi C.A., Samuel O.B., Akinnigbagbe R.O., Ajulo A.A. 2011. Morphological characteristics and salinity tolerance of Melanoides tuberculatus (Muller, 1774). World Journal of Biological Research, 4, 1–11.

    Google Scholar 

  • Brassard P., Rau M.E., Curtis M.A. 1982. Parasite-induced susceptibility to predation in diplostomiasis. Parasitology, 85, 495–501. DOI: 10.1017/S0031182000056274.

    Article  Google Scholar 

  • Buchmann K. 2007. An introduction to fish parasitological methods — Classical and molecular techniques. Biofolia press, Frederiksberg, Denmark, 130 pp.

    Google Scholar 

  • Chai J.Y., Lee S.H. 2002. Food-borne intestinal trematode infections in the Republic of Korea. Parasitology International, 51, 129–154. DOI: 10.1016/S1383-5769(02)00008-9.

    Article  PubMed  Google Scholar 

  • Chai J.Y., Murrell K.D., Lymbery A. 2005. Fish-borne parasitic zoonoses: status and issues. International Journal for Parasitology, 35, 1233–1254. DOI:10.1016/j.ijpara.2005.07.013.

    Article  PubMed  Google Scholar 

  • Chai J.Y. 2007. Intestinal flukes. In: (Eds. K.D. Murrell and B. Fried) Food-Borne Parasitic Zoonoses: Fish and Plant-Borne Parasites. Vol. 11. Springer, New York, USA, 53–115. DOI: 10.1007/978-0-387-71358-8_2.

    Chapter  Google Scholar 

  • Chai J.Y., Shin E.H., Lee S.H., Rim H.J. 2009. Foodborne intestinal flukes in Southeast Asia. Korean Journal of Parasitology, 47(Suppl.), 69–102, Review. DOI: 10.3347/kjp.2009.47.S.S69.

    Article  Google Scholar 

  • Chen H.T. 1942. The metacercaria and adult of Centrocestus formosanus (Nishigori, 1924), with notes on the natural infection of rats and cats with C. armatus (Tanabe, 1922). The Journal of Parasitology, 28, 285–298.

    Article  Google Scholar 

  • Chong R., Bousfield B., Brown R. 2011. Fish Disease Management. Veterinary Bulletin — Agriculture, Fisheries and Conservation Department Newsletter, 1, 1–12.

    Google Scholar 

  • Crowden A.E., Broom D.M. 1980. Effects of the eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Animal Behaviour, 28, 287–294. DOI: 10.1016/sS0003-3472(80)80031-5.

    Article  Google Scholar 

  • Davenport K.E. 1996. Characteristics of the current international trade in ornamental fish, with special reference to the European Union. Scientific and Technical Review of the Office International des Epizooties, 15, 435–443.

    CAS  Google Scholar 

  • De N.V., Le T.H. 2011. Human infections of fish-borne trematodes in Vietnam: Prevalence and molecular specific identification at an endemic commune in Nam Dinh province. Experimental Parasitology, 129, 355–361. DOI: 10.1016/j.exppara.2011.09.005.

    Article  PubMed  Google Scholar 

  • Dove A.D.M. 2000. Richness patterns in the parasite communities of exotic poeciliid fishes. Parasitology, 120, 609–623. DOI: 10.1017/S0031182099005958.

    Article  PubMed  Google Scholar 

  • Eddy S.R. 1998. Profile hidden Markov models. Bioinformatics, 14, 755–763. DOI: 10.1093/bioinformatics/14.9.755.

    Article  CAS  PubMed  Google Scholar 

  • Evans B., Lester R. 2001. Parasites of ornamental fish imported in Australia. Bulletin of European Association of Fish Pathologists, 21, 51–55.

    Google Scholar 

  • Fleming B.P., Huffman D.G., Bonner T.H., Brandt T.M. 2011. Metacercarial distribution of Centrocestus formosanus among fish hosts in the Guadalupe River drainage of Texas. Journal of Aquatic Animal Health, 23, 117–124. DOI: 10.1080/08997659.2011.616840.

    Article  PubMed  Google Scholar 

  • Fürst T., Keiser J., Utzinger J. 2012. Global burden of human foodborne trematodiasis: a systematic review and meta-analysis. The Lancet Infectious Diseases, 12, 210–221. DOI: 10.1016/S1473-3099(11)70294-8.

    Article  PubMed  Google Scholar 

  • Garcia F., Fujimoto R.Y., Martins M.L., Moraes F.R. 2009. Protozoan parasites of Xiphophorus spp. (Poeciliidae) and their relation with water characteristics. Arquivo Brasileiro de Medicina Veterinaria e Zootecnia, 61, 156–162. DOI: 10.1590/S0102-09352009000100022.

    Article  Google Scholar 

  • Glöer P. 2002. Die Süsswassergastropoden Nord- und Mitteleuropas: Bestimmungsschlüssel, Lebensweise, Verbreitung. Die Tier welt Deutschlands. 73. Teil. Conch Books, Hackenheim, Germany, 327 pp. (In German)

    Google Scholar 

  • Gozlan R.E., St-Hilaire S., Feist S.W., Martin P., Kent M.L. 2005. Biodiversity: Disease threat to European fish. Nature, 435(7045), 1046. DOI: 10.1038/4351046a.

    Article  CAS  PubMed  Google Scholar 

  • Hernandez L.E., Diaz M.T., Bashirullah A.K. 2003. Description of different developmental stages of Centrocestus formosanus (Nishigori, 1924) (Digenea: Heterophyidae). Revista Cientifica, FCV-LUZ, 13(4), 285–292.

    Google Scholar 

  • Hong S.J., Seo B.S., Lee S.H., Chai J.Y. 1988. A human case of Centrocestus armatus infection in Korea. The Korean Journal of Parasitology, 26, 55–60. DOI: 10.3347/kjp.1988.26.1.55.

    Article  Google Scholar 

  • Karatayev A.Y., Burlakova L.E., Karatayev V. A., Padilla D.K. 2009. Introduction, distribution, spread, and impacts of exotic freshwater gastropods in Texas. Hydrobiologia, 619, 181–194. DOI: 10.1007/s10750-008-9639-y.

    Article  Google Scholar 

  • Kazibwe F., Makanga B., Rubaire-Akiiki C., Ouma J., Kariuki C., Kabatereine N.B., Booth M., Vennervald B.J., Sturrock R.F., Stothard J.R. 2006. Ecology of Biomphalaria (Gastropoda: Planorbidae) in Lake Albert, Western Uganda: snail distributions, infection with schistosomes and temporal associations with environmental dynamics. Hydrobiologia, 568, 433–444. DOI 10.1007/s10750-006-0224-y.

    Article  Google Scholar 

  • Keiser J., Utzinger J. 2005. Emerging foodborne trematodiasis. Emerging Infectious Diseases, 11, 1507–1514.

    Article  PubMed Central  PubMed  Google Scholar 

  • Kennedy C.R. 1994. The ecology of introductions. In: (Eds. A.W. Pike and J.W. Lewis) Parasitic diseases of fish. Samara Publishing Limited, Cardigan, UK, 189–208.

    Google Scholar 

  • Kimura D., Uga S. 2005. Epidemiological study on Centrocestus armatus metacercariae in the Chikusa River, Hyogo Prefecture, Japan. Tropical Medicine and Health, 33, 7–11.

    Article  Google Scholar 

  • Kimura D., Paller V.G., Uga S. 2007. Development of Centrocestus armatus in different final hosts. Veterinary Parasitology, 146(3–4), 367–371. DOI:10.1016/j.vetpar.2007.02.032.

    Article  PubMed  Google Scholar 

  • Kurokawa T. 1935. On a new trematode of genus Stamnosoma proved from a man. Tokyo Iji Shinshi, 1915, 293–298 (In Japanese).

    Google Scholar 

  • Larsen A.H., Bresciani J., Buchmann K. 2004. Increasing frequency of cercarial dermatitis at higher latitudes. Acta Parasitologica, 49(3), 217–221.

    Google Scholar 

  • Levsen A., Mo T.A., Sterud E. 2003. De vanligste infeksjoner hos importert akvariefisk: En mulig trussel mot norsk fauna. Norsk Veterinaertidsskrift, 115, 639–649.

    Google Scholar 

  • Lo C.T., Lee K.M. 1996. Pattern of emergence and the effects of temperature and light on the emergence and survival of heterophyid cercariae (Centrocestus formosanus and Haplorchis pumilio). Journal of Parasitology, 82, 347–350.

    Article  CAS  PubMed  Google Scholar 

  • Marcos-López M., Gale P., Oidtmann B.C., Peeler E.J. 2010. Assessing the impact of climate change on disease emergence in freshwater fish in the United Kingdom. Transboundary Emerging Diseases, 57, 293–304. DOI: 10.1111/j.1865-1682.2010.01150.x.

    Article  PubMed  Google Scholar 

  • Mitchell A.J., Salmon M.J., Huffman D.G., Goodwin A.E., Brandt T.M. 2000. Prevalence and pathogenicity of a heterophyid trematode infecting the gills of an endangered fish Etheostoma fonticola in two central Texas spring-fed rivers. Journal of Aquatic Animal Health, 12, 283–289. DOI: 10.1577/1548-8667(2000)012〈0283:PAPOAH〉2.0.CO;2.

    Article  Google Scholar 

  • Mitchell A.J., Goodwin A.E., Salmon M.J., Brandt T.M. 2002. Experimental infection of an exotic heterophyid trematode, Centrocestus formosanus, in four aquaculture fishes. North American Journal of Aquaculture, 64, 55–59. DOI: 10.1577/1548 8454(2002)064<0055:EIOAEH〉2.0.CO;2.

    Article  Google Scholar 

  • Mitchell A.J., Overstreet R.M., Goodwin A.E., Brandt T.M. 2005a. Spread of an exotic fish-gill trematode: A far-reaching and complex problem. Fisheries, 30, 11–16.

    Article  Google Scholar 

  • Mitchell A.J., Brandt T.M. 2005b. Temperature tolerance of redrim melania, Melanoides tuberculatus, an exotic aquatic snail established in the United States. Transactions of the American Fisheries Society, 134, 126–131. DOI: 10.1577/FT03-178.1.

    Article  Google Scholar 

  • Mitchell A.J., Hobbs M.S., Brandt T.M. 2007. The effect of chemical treatments on red-rim melania Melanoides tuberculata, an exotic aquatic snail that serves as a vector of trematodes to fish and other species in the USA. North American Journal of Fisheries Management, 27, 1287–1293. DOI: 10.1577/M06-252.1.

    Article  Google Scholar 

  • Paula-Andrade C., Pinto H.A., Coscarelli D., Vidigal T.H., Melo A.L. 2012. The natural infection of Melanoides tuberculata (Müller, 1774) (Mollusca: Gastropoda) by Centrocestus formosanus (Nishigori, 1924) (Platyhelminthes: Trematoda) in Paranoá lake, Brasília, Brazil. Brazilian Journal of Biology, 72, 419–420. DOI: 10.1590/S1519-69842012000200026.

    Article  CAS  Google Scholar 

  • Peeler E.J., Oidtmann B.C., Midtlyng P.J., Miossec L., Gozlan R.E. 2011. Non-native aquatic animals introductions have driven disease emergence in Europe. Biological Invasions, 13, 1291–1303. DOI: 10.1007/s10530-010-9890-9.

    Article  Google Scholar 

  • Piazza R.S., Martins M.L., Guiraldelli L., Yamashita M.M. 2006. Parasitic diseases of freshwater ornamental fishes commercialized in Florianópolis, Santa Catarina, Brazil. Boletim do Instituto de Pesca, Săo Paulo, 32, 51–57.

    Google Scholar 

  • Pinto H.A., Melo A.L. 2010. Melanoides tuberculata (Mollusca: Thiaridae) as an intermediate host of Centrocestus formosanus (Trematoda: Heterophyidae) in Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 52, 207–210. DOI: 10.1590/S0036-46652010000400008.

    Article  PubMed  Google Scholar 

  • Rim H.J., Sohn W.M., Yong T.S., Eom K.S., Chai J.Y., Min D.Y., Lee S.H., Hoang E.H., Phommasack B., Insisengmay S. 2008. Fish-borne trematode metacercariae detected in freshwater fish from Vientiane municipality and Savannakhet province, Lao PDR. The Korean Journal of Parasitology, 46, 253–260. DOI: 10.3347/kjp.2008.46.4.253.

    Article  PubMed Central  PubMed  Google Scholar 

  • Rim H.J., Sohn W.M., Yong T.S., Eom K.S., Chai J.Y., Min D.Y., Lee S.H., Hoang E.H., Phommasack B., Insisiengmay S. 2013. Fish-borne trematode metacercariae in Luang Prabang, Khammouane, and Saravane province, Lao PDR. Korean Journal of Parasitology, 51, 107–114. DOI: 10.3347/kjp.2013.51.1.107.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ryang Y.S., Ahn Y.K., Yoon M.B. 1991. Trematode infections in the small intestine of Egretta alba medesta in Kangwondo. The Korean Journal of Parasitology, 29, 227–233. DOI: 10.3347/kjp.1991.29.3.227 (In Korean)

    Article  CAS  Google Scholar 

  • Sadler J., Goodwin A. 2007. Disease Prevention on Fish Farms, Southern Regional Aquaculture Center, Publication No. 4703.

    Google Scholar 

  • Saenphet S., Wongsawad C., Saenphet K., Rojanapaibul A., Vanittanakom P., Chai J.Y. 2006. Chronological observations of intestinal histopathology in rats (Rattus norvegicus) infected with Centrocestus caninus. The Southeast Asian Journal of Tropical Medicine and Public Health, 37(suppl 3), 69–73.

    PubMed  Google Scholar 

  • Salgado-Maldonado G., Rodriguez-Vargas M.I., Campos-Perez J.J. 1995. Metacercariae of Centrocestus formosanus (Nishigori, 1924) (Trematoda) in freshwater fishes in Mexico and their transmission by the thiarid snail Melanoides tuberculata. Studies on Neotropical Fauna and Environment, 30, 245–250. DOI: 10.1080/01650529509360963.

    Article  Google Scholar 

  • Santiago Bass C., Khan S., Weis J.S. 2007. Morphological changes to the gills of killifish associated with severe parasite infection. Journal of Fish Biology, 71, 920–925. DOI: 10.1111/j.1095-8649.2007.01532.x.

    Article  Google Scholar 

  • Scholz T., Vargas-Vázquez J., Moravec F., Vivas-Rodríguez C., Mendoza-Franco E. 1995. Metacercariae of trematodes of fishes from cenotes (sinkholes) of the Yucatan Peninsula, Mexico. Folia Parasitologica, 42, 173–192.

    Google Scholar 

  • Scholz T. 1999. Parasites in cultured and feral fish. Veterinary Parasitology, 84, 317–335.

    Article  CAS  PubMed  Google Scholar 

  • Scholz T., Salgado-Maldonado G. 2000. The introduction and dispersal of Centrocestus formosanus (Nishigori, 1924) (Digenea: Heterophyidae) in Mexico: A review. The American Midland Naturalist, 143, 185–200. DOI: 10.1674/00030031(2000)143[0185:TIADOC]2.0.CO;2.

    Article  Google Scholar 

  • Scholz T., Aguirre-Macedo M.L., Salgado-Maldonado G. 2001. Trematodes of the family Heterophyidae (Digenea) in Mexico: a review of species and new host and geographical records. Journal of Natural History, 35, 1733–1772. DOI: 10.1080/00222930152667087.

    Article  Google Scholar 

  • Shoaibi Omrani B., Ebrahimzadeh Mousavi H.A., Sharifpour I. 2010. Occurrence and histopathology of Ascocotyle tenuicollis metacercaria in gill of platyfish (Xiphophorus maculatus) imported to Iran. Iranian Journal of Fisheries Sciences, 9(3), 472–477.

    Google Scholar 

  • Smith B. J. 1989. Traveling snails. Journal of Medical and Applied Malacology, 1, 195–204.

    Google Scholar 

  • Sobecka E., Łuczak E., Marcinkiewicz M. 2012. New cases of pathogens imported with ornamental fish. Biological Letters, 49, 3–10. DOI: 10.2478/v10120-012-0001-8.

    Article  Google Scholar 

  • Sohn W.M., Chai J.Y. 2005. Infection status with helminthes in feral cats purchased from a market in Busan, Republic of Korea. The Korean Journal of Parasitology, 43, 93–100. DOI: 10.3347/kjp.2005.43.3.93.

    Article  PubMed Central  PubMed  Google Scholar 

  • Steele E., Hicks T. 2003. Histological effect of Ascocotyle tenuicollis (Digenea: Heterophyidae) metacercarial infection on the heart of Fundulus heteroclitus (Teleostei: Cyprinodontidae). Journal of the South Carolina Academy of Science, 1, 10–18.

    Google Scholar 

  • Thilakaratne I.D.S.I.P., Rajapaksha G., Hewakopara A., Rajapakse R.P.V.J., Faizal A.C.M. 2003. Parasitic infections in freshwater ornamental fish in Sri Lanka. Diseases of Aquatic Organisms, 54, 157–162.

    Article  CAS  PubMed  Google Scholar 

  • Thuy D.T., Kania P.W., Buchmann K. 2010. Infection status of zoonotic trematode metacercariae in Sutchi catfish (Pangasianodon hypophthalmus) in Vietnam: Associations with season, management and host age. Aquaculture, 302, 19–25.

    Article  Google Scholar 

  • Waikagul J., Wongsaroj T., Radomyos P., Meesomboon V., Praewanich R., Jongsuksuntikul P. 1997. Human infection of Centrocestus caninus in Thailand. Southeast Asian Journal of Tropical Medicine and Public Health, 28, 831–835.

    CAS  PubMed  Google Scholar 

  • World Health Organization. 1995. Control of food-borne trematode infections: report of a WHO Study Group, Issue 849 of Technical report series, 157 pages.

    Google Scholar 

  • World Health Organization. 2002. Food-borne trematode infections in Asia. Report Joint WHO/FAO Workshop, Hanoi, Vietnam.

    Google Scholar 

  • Yossepowitch O., Gotesman T., Assous M., Marva E., Zimlichman R., Dan M. 2004. Opisthorchiasis from imported raw fish. Emerging Infectious Diseases, 10, 2122–2126. DOI: 10.3201/eid1012.040410.

    Article  PubMed Central  PubMed  Google Scholar 

  • Yu S.H., Mott K.E. 1994. Epidemiology and morbidity of food-borne intestinal trematode infections. Tropical Diseases Bulletin, 91, 125–152.

    Google Scholar 

  • Yu S., Xu L., Jiang Z., Xu S., Han J., Zhu Y., Chang J., Lin J., Xu F. 1994. Report on the first nationwide survey of the distribution of human parasites in China. 1. Regional distribution of parasite species. Chinese Journal of Parasitology and Parasitic Diseases, 12, 241–247. (In Chinese)

    CAS  PubMed  Google Scholar 

  • Zhu X., Podolska M., Liu J.S., Yu H.S., Chen H.H., Lin Z.X., Luo C.B., Song H.Q., Lin R.Q. 2007. Identification of anisakid nematodes with zoonotic potential from Europe and China by single strand conformation polymorphism analysis of nuclear ribosomal DNA. Parasitology Research, 101, 1703–1707. DOI: 10.1007/s00436-007-0699-0.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Aquatic Pathobiology, Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, 1870, Frederiksberg C, Denmark

    Foojan Mehrdana, Hannah M. Jensen, Per W. Kania & Kurt Buchmann

Authors
  1. Foojan Mehrdana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hannah M. Jensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Per W. Kania
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kurt Buchmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Foojan Mehrdana.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mehrdana, F., Jensen, H.M., Kania, P.W. et al. Import of exotic and zoonotic trematodes (Heterophyidae: Centrocestus sp.) in Xiphophorus maculatus: Implications for ornamental fish import control in Europe. Acta Parasit. 59, 276–283 (2014). https://doi.org/10.2478/s11686-014-0237-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11686-014-0237-z

Keywords

Search

Navigation