Acta Parasitologica

, Volume 59, Issue 2, pp 276–283 | Cite as

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

  • Foojan MehrdanaEmail author
  • Hannah M. Jensen
  • Per W. Kania
  • Kurt Buchmann
Original Paper


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.


Xiphophorus maculatus fish-borne trematodes Centrocestus sp. metacercariae zoonosis 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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
  2. Anon. 2012. Importing and exporting live fish, molluscs and crustacean, Centre for Environment, Fisheries and Aquaculture Science. Available at:
  3. 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
  4. 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
  5. Brassard P., Rau M.E., Curtis M.A. 1982. Parasite-induced susceptibility to predation in diplostomiasis. Parasitology, 85, 495–501. DOI: 10.1017/S0031182000056274.CrossRefGoogle Scholar
  6. Buchmann K. 2007. An introduction to fish parasitological methods — Classical and molecular techniques. Biofolia press, Frederiksberg, Denmark, 130 pp.Google Scholar
  7. 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.PubMedCrossRefGoogle Scholar
  8. 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.PubMedCrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. Chong R., Bousfield B., Brown R. 2011. Fish Disease Management. Veterinary Bulletin — Agriculture, Fisheries and Conservation Department Newsletter, 1, 1–12.Google Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.Google Scholar
  15. 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.PubMedCrossRefGoogle Scholar
  16. Dove A.D.M. 2000. Richness patterns in the parasite communities of exotic poeciliid fishes. Parasitology, 120, 609–623. DOI: 10.1017/S0031182099005958.PubMedCrossRefGoogle Scholar
  17. Eddy S.R. 1998. Profile hidden Markov models. Bioinformatics, 14, 755–763. DOI: 10.1093/bioinformatics/14.9.755.PubMedCrossRefGoogle Scholar
  18. Evans B., Lester R. 2001. Parasites of ornamental fish imported in Australia. Bulletin of European Association of Fish Pathologists, 21, 51–55.Google Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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
  23. 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.PubMedCrossRefGoogle Scholar
  24. 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
  25. 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.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. Keiser J., Utzinger J. 2005. Emerging foodborne trematodiasis. Emerging Infectious Diseases, 11, 1507–1514.PubMedCentralPubMedCrossRefGoogle Scholar
  29. 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
  30. 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.CrossRefGoogle Scholar
  31. 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.PubMedCrossRefGoogle Scholar
  32. Kurokawa T. 1935. On a new trematode of genus Stamnosoma proved from a man. Tokyo Iji Shinshi, 1915, 293–298 (In Japanese).Google Scholar
  33. Larsen A.H., Bresciani J., Buchmann K. 2004. Increasing frequency of cercarial dermatitis at higher latitudes. Acta Parasitologica, 49(3), 217–221.Google Scholar
  34. 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
  35. 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.PubMedCrossRefGoogle Scholar
  36. 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.PubMedCrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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
  45. 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.PubMedCrossRefGoogle Scholar
  46. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  47. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  48. 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)CrossRefGoogle Scholar
  49. Sadler J., Goodwin A. 2007. Disease Prevention on Fish Farms, Southern Regional Aquaculture Center, Publication No. 4703.Google Scholar
  50. 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.PubMedGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. 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
  54. Scholz T. 1999. Parasites in cultured and feral fish. Veterinary Parasitology, 84, 317–335.PubMedCrossRefGoogle Scholar
  55. 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.CrossRefGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. 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
  58. Smith B. J. 1989. Traveling snails. Journal of Medical and Applied Malacology, 1, 195–204.Google Scholar
  59. 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.CrossRefGoogle Scholar
  60. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  61. 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
  62. 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.PubMedCrossRefGoogle Scholar
  63. 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.CrossRefGoogle Scholar
  64. 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.PubMedGoogle Scholar
  65. 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
  66. World Health Organization. 2002. Food-borne trematode infections in Asia. Report Joint WHO/FAO Workshop, Hanoi, Vietnam.Google Scholar
  67. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  68. Yu S.H., Mott K.E. 1994. Epidemiology and morbidity of food-borne intestinal trematode infections. Tropical Diseases Bulletin, 91, 125–152.Google Scholar
  69. 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)PubMedGoogle Scholar
  70. 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.PubMedCrossRefGoogle Scholar

Copyright information

© Versita Warsaw and Springer-Verlag Wien 2014

Authors and Affiliations

  • Foojan Mehrdana
    • 1
    Email author
  • Hannah M. Jensen
    • 1
  • Per W. Kania
    • 1
  • Kurt Buchmann
    • 1
  1. 1.Laboratory of Aquatic Pathobiology, Department of Veterinary Disease Biology, Faculty of Health and Medical SciencesUniversity of CopenhagenFrederiksberg CDenmark

Personalised recommendations