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.
[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. Search in Google Scholar
[2] Anon. 2012. Importing and exporting live fish, molluscs and crustacean, Centre for Environment, Fisheries and Aquaculture Science. Available at: www.gov.uk Search in Google Scholar
[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. Search in 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. Search in 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. http://dx.doi.org/10.1017/S003118200005627410.1017/S0031182000056274Search in Google Scholar
[6] Buchmann K. 2007. An introduction to fish parasitological methods — Classical and molecular techniques. Biofolia press, Frederiksberg, Denmark, 130 pp. Search in 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. http://dx.doi.org/10.1016/S1383-5769(02)00008-910.1016/S1383-5769(02)00008-9Search in Google 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. http://dx.doi.org/10.1016/j.ijpara.2005.07.01310.1016/j.ijpara.2005.07.013Search in Google Scholar PubMed
[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. http://dx.doi.org/10.1007/978-0-387-71358-8_210.1007/978-0-387-71358-8_2Search in Google 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. http://dx.doi.org/10.3347/kjp.2009.47.S.S6910.3347/kjp.2009.47.S.S69Search in Google Scholar PubMed PubMed Central
[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. http://dx.doi.org/10.2307/327296610.2307/3272966Search in Google Scholar
[12] Chong R., Bousfield B., Brown R. 2011. Fish Disease Management. Veterinary Bulletin — Agriculture, Fisheries and Conservation Department Newsletter, 1, 1–12. Search in 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. http://dx.doi.org/10.1016/S0003-3472(80)80031-5Search in Google 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. Search in 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. http://dx.doi.org/10.1016/j.exppara.2011.09.00510.1016/j.exppara.2011.09.005Search in Google Scholar PubMed
[16] Dove A.D.M. 2000. Richness patterns in the parasite communities of exotic poeciliid fishes. Parasitology, 120, 609–623. DOI: 10.1017/S0031182099005958. http://dx.doi.org/10.1017/S003118209900595810.1017/S0031182099005958Search in Google Scholar
[17] Eddy S.R. 1998. Profile hidden Markov models. Bioinformatics, 14, 755–763. DOI: 10.1093/bioinformatics/14.9.755. http://dx.doi.org/10.1093/bioinformatics/14.9.75510.1093/bioinformatics/14.9.755Search in Google Scholar PubMed
[18] Evans B., Lester R. 2001. Parasites of ornamental fish imported in Australia. Bulletin of European Association of Fish Pathologists, 21, 51–55. Search in 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. http://dx.doi.org/10.1080/08997659.2011.61684010.1080/08997659.2011.616840Search in Google Scholar PubMed
[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. http://dx.doi.org/10.1016/S1473-3099(11)70294-810.1016/S1473-3099(11)70294-8Search in Google 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. http://dx.doi.org/10.1590/S0102-0935200900010002210.1590/S0102-09352009000100022Search in Google 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) Search in 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. http://dx.doi.org/10.1038/4351046a10.1038/4351046aSearch in Google Scholar PubMed
[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. Search in 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. http://dx.doi.org/10.3347/kjp.1988.26.1.5510.3347/kjp.1988.26.1.55Search in Google Scholar PubMed
[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. http://dx.doi.org/10.1007/s10750-008-9639-y10.1007/s10750-008-9639-ySearch in Google 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. http://dx.doi.org/10.1007/s10750-006-0224-y10.1007/s10750-006-0224-ySearch in Google Scholar
[28] Keiser J., Utzinger J. 2005. Emerging foodborne trematodiasis. Emerging Infectious Diseases, 11, 1507–1514. http://dx.doi.org/10.3201/eid1110.05061410.3201/eid1110.050614Search in Google Scholar PubMed PubMed Central
[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. Search in 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. http://dx.doi.org/10.2149/tmh.33.710.2149/tmh.33.7Search in Google 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. http://dx.doi.org/10.1016/j.vetpar.2007.02.03210.1016/j.vetpar.2007.02.032Search in Google Scholar PubMed
[32] Kurokawa T. 1935. On a new trematode of genus Stamnosoma proved from a man. Tokyo Iji Shinshi, 1915, 293–298 (In Japanese). Search in 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. Search in 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. Search in 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. http://dx.doi.org/10.2307/328417810.2307/3284178Search in Google 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. http://dx.doi.org/10.1111/j.1865-1682.2010.01150.x10.1111/j.1865-1682.2010.01150.xSearch in Google 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. http://dx.doi.org/10.1577/1548-8667(2000)012<0283:PAPOAH>2.0.CO;210.1577/1548-8667(2000)012<0283:PAPOAH>2.0.CO;2Search in Google 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. http://dx.doi.org/10.1577/1548-8454(2002)064<0055:EIOAEH>2.0.CO;210.1577/1548-8454(2002)064<0055:EIOAEH>2.0.CO;2Search in Google 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. http://dx.doi.org/10.1577/1548-8446(2005)30[11:SOAEFT]2.0.CO;2Search in Google 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. http://dx.doi.org/10.1577/FT03-178.110.1577/FT03-178.1Search in Google 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. http://dx.doi.org/10.1577/M06-252.110.1577/M06-252.1Search in Google 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. http://dx.doi.org/10.1590/S1519-6984201200020002610.1590/S1519-69842012000200026Search in Google 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. http://dx.doi.org/10.1007/s10530-010-9890-910.1007/s10530-010-9890-9Search in Google 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. Search in 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. http://dx.doi.org/10.1590/S0036-4665201000040000810.1590/S0036-46652010000400008Search in Google 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. http://dx.doi.org/10.3347/kjp.2008.46.4.25310.3347/kjp.2008.46.4.253Search in Google 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. http://dx.doi.org/10.3347/kjp.2013.51.1.10710.3347/kjp.2013.51.1.107Search in Google 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) http://dx.doi.org/10.3347/kjp.1991.29.3.22710.3347/kjp.1991.29.3.227Search in Google Scholar
[49] Sadler J., Goodwin A. 2007. Disease Prevention on Fish Farms, Southern Regional Aquaculture Center, Publication No. 4703. Search in 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. Search in Google 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. http://dx.doi.org/10.1080/0165052950936096310.1080/01650529509360963Search in Google 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. http://dx.doi.org/10.1111/j.1095-8649.2007.01532.x10.1111/j.1095-8649.2007.01532.xSearch in Google 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. Search in Google Scholar
[54] Scholz T. 1999. Parasites in cultured and feral fish. Veterinary Parasitology, 84, 317–335. http://dx.doi.org/10.1016/S0304-4017(99)00039-410.1016/S0304-4017(99)00039-4Search in Google 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. http://dx.doi.org/10.1674/0003-0031(2000)143[0185:TIADOC]2.0.CO;2Search in Google 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. http://dx.doi.org/10.1080/0022293015266708710.1080/00222930152667087Search in Google 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. Search in Google Scholar
[58] Smith B. J. 1989. Traveling snails. Journal of Medical and Applied Malacology, 1, 195–204. Search in 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. http://dx.doi.org/10.2478/v10120-012-0001-810.2478/v10120-012-0001-8Search in Google 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. http://dx.doi.org/10.3347/kjp.2005.43.3.9310.3347/kjp.2005.43.3.93Search in Google Scholar PubMed PubMed Central
[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. Search in 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. http://dx.doi.org/10.3354/dao05415710.3354/dao054157Search in Google Scholar PubMed
[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. http://dx.doi.org/10.1016/j.aquaculture.2010.02.00210.1016/j.aquaculture.2010.02.002Search in Google 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. Search in Google 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. Search in Google Scholar
[66] World Health Organization. 2002. Food-borne trematode infections in Asia. Report Joint WHO/FAO Workshop, Hanoi, Vietnam. Search in 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. http://dx.doi.org/10.3201/eid1012.04041010.3201/eid1012.040410Search in Google Scholar PubMed PubMed Central
[68] Yu S.H., Mott K.E. 1994. Epidemiology and morbidity of food-borne intestinal trematode infections. Tropical Diseases Bulletin, 91, 125–152. Search in 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) Search in Google 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. http://dx.doi.org/10.1007/s00436-007-0699-010.1007/s00436-007-0699-0Search in Google Scholar PubMed
© 2014 W. Stefański Institute of Parasitology, PAS
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.