Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-24T10:24:55.080Z Has data issue: false hasContentIssue false
  • English
  • Français

Digenean Holostephanus (Trematoda: Digenea: Cyathocotylidae) metacercariae in common carp (Cyprinus carpio Linnaeus, 1758) muscle: zoonotic potential and sensitivity to physico-chemical treatments

Published online by Cambridge University Press:  17 January 2020

D. Sándor Open the ORCID record for D. Sándor [Opens in a new window] ,
M. Gyöngy ,
K. Nyeste ,
I. Czeglédi ,
C. Székely ,
K. Buchmann  and
G. Cech
D. Sándor*
Affiliation:
Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, Hungary Eötvös Loránd University, Doctoral School of Biology Program of Zootaxonomy, Animal Ecology and Hydrobiology, Budapest, Hungary
M. Gyöngy
Affiliation:
Department of Hydrobiology, University of Debrecen, Debrecen, Hungary Pál Juhász-Nagy Doctoral School of Biology and Environmental Sciences, University of Debrecen, Debrecen, Hungary
K. Nyeste
Affiliation:
Department of Hydrobiology, University of Debrecen, Debrecen, Hungary Pál Juhász-Nagy Doctoral School of Biology and Environmental Sciences, University of Debrecen, Debrecen, Hungary
I. Czeglédi
Affiliation:
Centre for Ecological Research, Balaton Limnological Institute, Hungarian Academy of Sciences, Tihany, Hungary
C. Székely
Affiliation:
Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, Hungary
K. Buchmann
Affiliation:
Department of Veterinary and Animal Science, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
G. Cech
Affiliation:
Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, Hungary
*
Author for correspondence: D. Sandor, E-mail: sandor.diana@agrar.mta.hu
Get access Rights & Permissions [Opens in a new window]

Abstract

Metacercariae of various species within the genus Holostephanus Szidat, 1936 (Trematoda: Digenea: Cyathocotylidae) occur in muscles of both farmed and wild fish, including common carp (Cyprinus carpio Linnaeus, 1758). The life cycle includes a snail as first intermediate host, fish as second intermediate host and birds or mammals as final hosts. We studied the zoonotic potential and the viability of Holostephanus metacercariae from common carp following exposure to various physical and chemical treatments. Muscle tissue samples of common carp specimens from a fish farm in the north-eastern part of Hungary were examined and metacercariae recovered. The zoonotic potential was evaluated experimentally by using small mammals as models (albino mice, n = 2; and Syrian hamsters, n = 4) infected per os with Holostephanus cysts. Parallelly, Metagonimus metacercariae were used as positive controls. We could not confirm the zoonotic potential of Holostephanus metacercariae as they did not survive in the mammalian intestine whereas Metagonimus metacercariae developed to the adult stage. We assessed the viability of metacercariae isolated from common carp specimens during exposure to different physical treatments (temperatures of −18°C, +20°C, +40°C and +60°C) and chemical agents (5% and 10% acetic acid and 10% sodium chloride (NaCl)). Metacercariae lost viability by freezing at −18°C (2 h), heating at 60°C (20 min), incubation in 5% and 10% acetic acid (5 min) and 10% NaCl (2 h). These methods served as models to investigate the effectiveness of food preparation techniques (such as cold and hot smoking, freezing, salting and pickling) on the survival of metacercariae.

Keywords

Common carpdigenean trematodeszoonosisviabilitymuscle metacercariae
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e117
Copyright
Copyright © Cambridge University Press 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdallah, KF, Hamadto, HH, El-Hayawan, IA, El-Motayam, MH and Ahmed, Wel-A (2009) Effect of different temperatures on viability of seven encysted metacercariae recovered from freshwater fishes in Qualyobia, Egypt. Journal of the Egyptian Society of Parasitology 39(2), 413–420.Google ScholarPubMed
Abdussalam, M, Käferstein, FK and Mott, KE (1995) Food safety measures for the control of foodborne trematode infections. Food Control 6, 71–79.CrossRefGoogle Scholar
Armignacco, O, Caterini L, Marucci G, et al. (2008) Human illnesses caused by Opisthorchis felineus flukes, Italy. Emerging Infectious Diseases 14, 1902–1905.CrossRefGoogle ScholarPubMed
Beldsoe, EG and Oria, M (2006) Potential hazards in cold-smoked fish: parasites. Journal of Food Science 66(7), 1100–1103.CrossRefGoogle Scholar
Bernhard, K (1985) Nachweis besonderer Helminthenarten bei DDR-Bürgern. Angewandte Parasitologie 26, 223–224.Google Scholar
Besprozvannykh, VV (2003) Life cycle of a trematode Holostephanus nipponicus (Cyathocotylidae) in conditions of Primor'e. Parazitologiia 37, 346–351.Google ScholarPubMed
Borges, JN, Skov, J, Bahlool, QZM, Møller, OS, Kania, PW, Santos, CP and Buchmann, K (2014) Viability of Cryptocotyle lingua metacercariae from Atlantic cod (Gadus morhua) after exposure to freezing and heating in the temperature range from -80 °C to 100 °C. Food Control 50, 371–377.CrossRefGoogle Scholar
Chai, JY, Murrell, KD and Lymbery, AJ (2005) Fish-borne parasitic zoonoses: status and issues. International Journal for Parasitology 35, 1233–1254.CrossRefGoogle ScholarPubMed
Chai, JY, Kang, YJ, Choi, SY, Guk, SM, Yu, JR and Lee, SH (1998) Surface ultrastructure of Metagonimus miyatai metacercariae and adults. The Korean Journal of Parasitology 36, 217–225.CrossRefGoogle ScholarPubMed
Chandler, AC (1950) Mesostephanus longisaccus, a new cyathocotylid trematode from a dog. The International Journal for Parasitology 36, 90.CrossRefGoogle ScholarPubMed
Crotti, D, D'Annibale, ML and Crotti, S (2007) Opistorchiasi autoctona del Lago Trasimeno (Perugia): descrizione di due episodi epidemici da Opisthorchis felineus e problematiche diagnostiche differenziali. Microbiologia Medica 42, 36–41.Google Scholar
Dubois, G (1983) Le genre Holostephanus Szidat, 1936 (Trematoda: Strigeata: Cyathocotyloidea). Commentaire sur les espèces et érection de Holostephanoides gen. nov. Bull. Soc. neuchâtel. The Science of Nature 106, 87–99.Google Scholar
EFSA (European Food Safety Authority) (2004) Regulation (EC) N° 853/2004 of the European parliament and council of 29 of April 2004 laying down specific hygiene rules for food of animal origin. Available at https://www.fsai.ie/uploadedFiles/Food_Business/Reg853_2004.pdf (accessed 19 March 2014).Google Scholar
EFSA (European Food Safety Authority) (2010) Panel on Biological Hazards (BIOHAZ) scientific opinion on risk assessment of parasites in fishery products. EFSA Journal 8, 1543.CrossRefGoogle Scholar
Erasmus, DA (1962) Studies on the adult and metacercaria of Holostephanus lühei Szidat, 1936. Parasitology 52, 353–374.CrossRefGoogle Scholar
Erhardt, A, Germer, WD and Hörning, B (1962) Die Opisthorchiasis, hervorgerufen durch den Katzenleberegel Opisthorchis felineus (Riv.). Parasitologische Schriftenreihe, vol. 15. Jena, Veb Gustav Fischer Verlag.Google Scholar
Fan, PC (1998) Viability of metacercariae of Clonorchis sinensis in frozen or salted freshwater fish. International Journal for Parasitology 28(4), 603–605.CrossRefGoogle ScholarPubMed
FAO (Food and Agriculture Organization) (1998) Seafood safety e Economics of hazard analysis and critical control point (HACCP) programs. FAO Fisheries Technical Papers, T381. Available at http://www.fao.org/DOCREP/003/X0465E/X0465E00.HTM (accessed 18 March 2014).Google Scholar
Fattakhov, RG (1989) Low-temperature regimes for decontamination of fish of the larvae Opisthorchis. Medicine Parazitology (Mosk) 5, 63–65 (in Russian).Google Scholar
Fried, B, Graczyk, TK and Tamang, L (2004) Food-borne intestinal trematodiases in humans. Parasitology Research 93, 159–170.CrossRefGoogle ScholarPubMed
Gettová, L, Gilles, A and Šimková, A (2016) Metazoan parasite communities: support for the biological invasion of Barbus barbus and its hybridization with the endemic Barbus meridionalis. Parasites and Vectors 9, 588.CrossRefGoogle ScholarPubMed
Gibson, DI, Jones, A and Bray, RA (2002) Key to the Trematoda. Volume 1. Wallingford, CABI Publishing, 206.CrossRefGoogle Scholar
Grundy-Warr, C, Andrews, RH, Sithithaworn, P, Petney, TN, Sripa, B, Laithavewat, L and Ziegler, AD, (2012) Raw attitudes, wetland cultures, life-cycles: socio-cultural dynamics relating to Opisthorchis viverrini in the Mekong Basin. Parasitology International 61, 65–70.CrossRefGoogle ScholarPubMed
Harrington, DP and Fleming, TR (1982) A class of rank test procedures for censored survival data. Biometrika 69, 553–566.CrossRefGoogle Scholar
Healy, GR (1970) Trematodes transmitted to man by fish, frogs, and crustacea. Journal of Wildlife Diseases 6, 255–261.CrossRefGoogle Scholar
Kaenjampa, P, Tangkawattana, S, Smith, JF, Sukon, P and Tangkawattana, P (2017) Elimination of Haplochis taichui metacercaria in cyprinoid fish with freezing temperature and soured fish (plasom) with salinity. The Southeast Asian Journal of Tropical Medicine and Public Health 48(4), 777–785.Google Scholar
Kanarek, G, Sitko, J, Rolbiecki, L and Rokicki, J (2003) Digenean fauna of the great cormorant Phalacrocorax carbo sinensis (Blumenbach, 1798) in the brackish waters of the Vistula Lagoon and the Gulf of Gdańsk (Poland). Wiadomości Parazytologiczne 49, 293–299.Google Scholar
Kang, SY, Cho, SY, Chai, JY, Lee, JB and Jang, DH (1983) A study on intestinal lesions of experimentally reinfected dogs with Metagonimus yokogawai. The Korean Journal of Parasitology 21(1), 58–73.CrossRefGoogle Scholar
Keiser, J and Utzinger, J (2009) Food-borne trematodiases. Clinical Microbiology Reviews 22(3), 466–483.CrossRefGoogle ScholarPubMed
Kim, TI, Oh, SR, Dai, F, Yang, HJ, Ha, SD and Hong, SJ (2017) Inactivation of Paragonimus westermani metacercariae in soy sauce-marinated and frozen freshwater crabs. Parasitology Research 116(3), 1003–1006.CrossRefGoogle ScholarPubMed
Kruatrachue, M, Chitramvong, YP, Upatham, ES, Vichasri, S and Viyanant, V (1982) Effects of physico-chemical factors on the infection of hamsters by metacercariae of Opisthorchis viverrini. The Southeast Asian Journal of Tropical Medicine and Public Health 13, 614–617.Google ScholarPubMed
Kudo, N, Ota, C, Saka, F, Ikeda, Y, Tomihisa, Y, Itoi, Y and Oyamada, T (2014) Experimental final hosts of Metagonimus hakubaensis (Trematoda: Heterophyidae) and their suitability to the fluke. Journal of Veterinary Medical Science 76(12), 1651–1654.CrossRefGoogle ScholarPubMed
Kvach, Y, Ondračková, M and Jurajda, P (2016) First report of metacercariae of Cyathocotyle prussica parasitising a fish host in the Czech Republic, Central Europe. Helminthologia 53(3), 257–261.CrossRefGoogle Scholar
Kvach, Y, Boldyrev, V, Lohner, R and Stepien, CA (2015) The parasite community of gobiid fishes (Actinopterygii: Gobiidae) from the Lower Volga River region. Biologia 70, 948–957.CrossRefGoogle Scholar
Mierzejewska, K, Kvach, Y, Stańczak, K, Grabowska, J, Woźniak, M, Dziekonska-Rynko, J and Ovcharenko, M (2014) Parasites of non-native gobies in the Włocławek Reservoiron the lower Vistula River, first comprehensive study in Poland. Knowledge and Management of Aquatic Ecosystems 414, 1.CrossRefGoogle Scholar
Moravec, F and Scholz, T (2016) Helminth parasites of the lesser great cormorant Phalacrocorax carbo sinensis from two nesting regions in the Czech Republic. Folia Parasitologica 63, 22.CrossRefGoogle ScholarPubMed
Näreaho, A, Eriksson-Kallio, AM, Heikkinen, P, Snellman, A, Sukura, A and Koski, P (2017) High prevalence of zoonotic trematodes in roach (Rutilus rutilus) in the Gulf of Finland. Acta Veterinaria Scandinavica 59, 75.CrossRefGoogle Scholar
Ondračková, M, Dávidová, M, Blazek, R, Gelnar, M and Jurajda, P (2009) The interaction between an introduced fish host and local parasite fauna: Neogobius kessleri in the middle Danube River. Parasitology Research 105, 201–208.CrossRefGoogle ScholarPubMed
Onsurathum, S, Pinlaor P, Charoensuk L, et al. (2016) Contamination of Opisthorchis viverrini and Haplorchis taichui metacercariae in fermented fish products in northeastern Thailand markets. Food Control 59, 493–498.CrossRefGoogle Scholar
Phan, VT, Ersbøll, AK, Bui, TQ, Nguyen, HT, Murrell, D and Dalsgaard, A (2010) Fish-borne zoonotic trematodes in cultured and wild-caught freshwater fish from the Red River Delta, Vietnam. Vector-Borne and Zoonotic Diseases 10(9), 861–866.CrossRefGoogle ScholarPubMed
Pinlaor, S, Onsurathum S, Boonmars T, et al. (2013) Distribution and abundance of Opisthorchis viverrini metacercariae in cyprinid fish in northeastern Thailand. Korean Journal of Parasitology 51(6), 703–710.CrossRefGoogle ScholarPubMed
Pornruseetairatn, S, Kino H, Shimazu T, et al. (2016) A molecular phylogeny of Asian species of the genus Metagonimus (Digenea)—small intestinal flukes—based on representative Japanese populations. Parasitology Research 115(3), 1123–1130.CrossRefGoogle ScholarPubMed
Pozio, E, Armignacco, O, Ferri, F and Gomez Morales, MA (2013) Opisthorchis felineus, an emerging infection in Italy and its implication for the European Union. Acta Tropica 126(1), 54–62.CrossRefGoogle ScholarPubMed
Rácz, OZ and Zemankovics, E (2002) Survival of metacercariae of Metagonimus yokogawai (Digenea: Heterophyidae) on fish from River Danube. Hungarian Veterinary Journal 124(7), 437–444.Google Scholar
R Core Team (2015) R: a language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available at http://www.R-project.org (accessed 25 November 2019).Google Scholar
Rim, HJ (2005) Clonorchiasis: an update. Journal of Helminthology 79, 269–281.CrossRefGoogle ScholarPubMed
Sänger, R, Möller, FW, Lafrenz, M and Ziegler, K (1991) An endemic focus of Opistorchis felineus in Mecklenburg-Pommerania/Germany. Tropical Medicine and Parasitology 42, 463.Google Scholar
Seo, M, Guk, SM, Chai, JY, Sim, S and Sohn, WM (2008) Holostephanus metorchis (Digenea: Cyathocotylidae) from chicks experimentally infected with metacercariae from a fish, Pseudorasbora parva, in the Republic of Korea. Korean Journal of Parasitology 46(2), 83–86.CrossRefGoogle ScholarPubMed
Shimazu, T (2002) Life cycle and morphology of Metagonimus miyatai (Digenea: Heterophyidae) from Nagano, Japan. Parasitology International 51(3), 271–280.CrossRefGoogle ScholarPubMed
Sithithaworn, P and Haswell-Elkins, M (2003) Epidemiology of Opisthorchis viverrini. Acta Tropica 88, 187–194.CrossRefGoogle ScholarPubMed
Stang, JC and Cable, RM (1966) The life history of Holostephanus ictaluri Vernberg, 1952 (Trematoda: Digenea), and immature stages of other North American fresh-water cyathocotylids. The American Midland Naturalist 75, 404–415.CrossRefGoogle Scholar
Sulgostowska, T (2007) Intestinal digeneans of birds (superfamily Diplostomoidea) of the Masurian lakes. Wiadomości Parazytologiczne 53, 117–28 (in Polish).Google ScholarPubMed
Toledo, R, Esteban, JG and Fried, B (2012) Current status of food-borne trematode infections. European Journal of Clinical Microbiology and Infectious Diseases 31(8), 1705–1718.CrossRefGoogle ScholarPubMed
Traverso, A, Repetto E, Magnani S, et al. (2012) A large outbreak of Opisthorchis felineus in Italy suggests that opisthorchiasis develops as a febrile eosinophilic syndrome with cholestasis rather than a hepatitis-like syndrome. European Journal of Clinical Microbiology and Infectious Diseases 31, 1089–1093.CrossRefGoogle ScholarPubMed
Tselepatiotis, E, Mantadakis, E, Papoulis, S, Vassalou, E, Kotsakis, P and Samonis, G (2003) A case of Opisthorchis felineus infestation in a pilot from Greece. Infection 31, 430–432.CrossRefGoogle Scholar
Watanapa, P and Watanapa, WB (2002) Liver fluke-associated cholangiocarcinoma. British Journal of Surgery 89, 962–970.CrossRefGoogle ScholarPubMed
WHO (2011) Report of the WHO expert consultation on foodborne trematode infections and taeniasis/cysticercosis. World Health Organisation. Available at https://www.who.int/neglected_diseases/preventive_chemotherapy/WHO_HTM_NTD_PCT_2011.3.pdf.Google Scholar
Yamaguti, S (1939) Studies on the helminth fauna of Japan. Part 25. Trematodes of birds, IV. Japanese Journal of Zoology 8, 131–210.Google Scholar