Abstract
This study is a contribution to the molecular taxonomy and epidemiology of heterophyid (Trematoda: Heterophyidae) metacercariae found in the muscle of Mugilidae (Osteichthyes) from Sardinia (western Mediterranean Sea). Sixty specimens of mugilids (13 Chelon labrosus, 18 Liza aurata, 6 Liza ramada, 8 Liza saliens, 15 Mugil cephalus) were examined and 17,899 metacercariae isolated in 95 % of the hosts. Four types of metacercariae were identified: Heterophyes sp. (n = 14,113), Heterophyes sp. -small (1225), Stictodora sp. (1606), and Ascocotyle (Phagicola) sp. (955). The experimental infection of a hamster with Heterophyes sp. metacercariae produced six adults identified as Heterophyes heterophyes and two as Heterophyes cf. nocens. The morphology of Heterophyes sp. -small metacercariae matched with that of Heterophyes dispar. The sequence analysis of the ITS2 and 28S portions of rDNA confirmed the morphological identification of metacercariae, showing four clusters. All adults grouped together with the Heterophyes sp. metacercariae, whereas adults of Heterophyes nocens from Korea clustered separately, showing that this species is distinguished from H. heterophyes, and suggesting caution in the exclusive use of the number of rodlets of the genital sucker to separate the two species. The presence of metacercariae was high in all hosts; the highest prevalence is of Heterophyes sp. (prevalence ≥78 %; mean intensity ≥135 metacercariae/100 g muscle), and the most heavily infected host is M. cephalus (prevalence = 100 %; mean intensity = 841 metacercariae/100 g muscle).
Similar content being viewed by others
References
Alessandrini G (1906) Su di una specie del gen. Ascocotyle Lss. rinvenuta nel cane. Nota preventiva. Bollettino della Società Zoologica Italiana 15:221–224
Asada J (1934) On the Metagonimus yokogawai and its related species. Clinical Medicine 22:43–56
Balozet L, Callot J (1939) Trematodes de Tunisie, 3, Superfamille Heterophyoidea. Arch Inst Pasteur Tunis 28:34–63
Blair D, Wu B, Chang ZS, Gong H, Agatsuma T, Zhang YN, Chen SH, Lin JX, Chen MG, Waikagul J, Guevara AG, Feng Z, Davis GM (1999) A molecular perspective on the genera Paragonimus Braun, Euparagonimus Chen and Pagumogonimus Chen. J Helminthol 73:295–299. doi:10.1017/S0022149X99000499
Bowles J, Hope M, Tiu WU, Liu SX, McManus DP (1993) Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Trop 55:217–229. doi:10.1016/0001-706X(93)90079-Q
Burton PR (1958) A review of the taxonomy of the trematode genera Ascocotyle (Looss) and Phagicola (Faust) of the family Heterophyidae. Proc Helminthol Soc Wash 25:117–122
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583. doi:10.2307/3284227
Canestri-Trotti G, Fioravanti ML, Pampiglione S, Virga A (1992) Segnalazione di Heterophyes heterophyes (Trematoda, Heterophyidae) in un cane in Sicilia. Atti della Società Italiana delle Scienze Veterinarie 46:1423–1426
Chai JY, Lee SH (2002) Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int 51:129–154. doi:10.1016/S1383-5769(02)00008-9
Chai JY, Darwin Murrell K, Lymbery AJ (2005) Fish borne parasitic zoonoses: status and issues. Int J Parasitol 35:1233–1254. doi:10.1016/j.ijpara.2005.07.013
Chai JY, Shin EH, Lee SH, Rim HJ (2009) Foodborne intestinal flukes in Southeast Asia. Korean J Parasitol 47:S69–S102. doi:10.3347/kjp.2009.47.S.S69
Chontananarth T, Wongsawad C, Chomdej S, Krailas D, Chai JY (2014) Molecular phylogeny of trematodes in Family Heterophyidae based on mitochondrial cytochrome c oxidase subunit I (mCOI). Asian Pac J Trop Med 7:446–450. doi:10.1016/S1995-7645(14)60072-9
European Commission (2011) Commission Regulation (EU) No. 1276/2011 (8 December 2011) Amending Annex III to Regulation (EC) No. 853/2004 of the European Parliament and of the Council as regards the treatment to kill viable parasites in fishery products for human consumption. Off J Eur Union L327:39–41
Culurgioni J, Sabatini R, De Murtas R, Mattiucci S, Figus V (2014) Helminth parasites of fish and shellfish from the Santa Gilla Lagoon in southern Sardinia, Italy. J Helminthol 88:489–498. doi:10.1017/S0022149X13000461
Deiana S (1961) Phagicola italica (Alessandrini, 1906) ed Heterophyes heterophyes (Siebold, 1852) parassiti del cane in Sardegna. Riv Parassitol 22:185–192
Dzikowski R, Levy MG (2012) Heterophyidae. In: Liu D (ed) Molecular Detection of Human Parasitic Pathogens. Taylor & Francis CRC, London, pp 379–388
EFSA (2010) Scientific opinion on risk assessment of parasites in fishery products. EFSA J 8:1–91. doi:10.2903/j.efsa.2010.1543
El-Gayar AK (2007) Studies on some trematode parasites of stray dogs in Egypt with a key to the identification of intestinal trematodes of dogs. Vet Parasitol 144:360–365. doi:10.1016/j.vetpar.2006.09.043
Elsheikha HM, Elshazly AM (2008a) Preliminary observations on infection of brackish and fresh water fish by heterophyid encysted metacercariae in Egypt. Parasitol Res 103:971–977. doi:10.1007/s00436-008-1043-z
Elsheikha HM, Elshazly AM (2008b) Host-dependent variations in the seasonal prevalence and intensity of heterophyid encysted metacercariae (Digenea: Heterophyidea) in brackish water fish in Egypt. Vet Parasitol 153:65–72. doi:10.1016/j.vetpar.2008.01.026
Fahmy MAM, Selim MK (1959) Studies on some trematode parasites of dogs in Egypt with special reference to the role played by fish in their transmission. Z Parasitenkd 19:3–13. doi:10.1007/BF00260314
Fenza A, Olla G, Salati F, Viale I (2014) Stagni e lagune produttive della Sardegna tradizioni, sapori e ambiente. Agenzia Regionale Laore Sardegna, Cagliari
Georgiev BB, Biserkov V, Genov T (1986) In toto staining method for cestodes with iron acetocarmine. Helminthologia 23:279–281
Hamed MGE, Elias AN (1970) Effect of food-processing methods upon survival of the trematode Heterophyes sp. in flesh of mullet caught from brackish Egyptian waters. J Food Sci 35:386–388. doi:10.1111/j.1365-2621.1970.tb00938.x
Hillis DM (1996) Inferring complex phylogenies. Nature 383:130–131. doi:10.1038/383130a0
Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192. doi:10.1093/sysbio/42.2.182
Khalafalla RE (2011) A survey study on gastrointestinal parasites of stray cats in Northern Region of Nile Delta, Egypt. PLoS One 6:e20283. doi:10.1371/journal.pone.0020283
Lane C (1922) A note on Heterophyes nocens as a distinct species of trematode parasite. Lancet 200:505. doi:10.1016/S0140-6736(01)00488-3
Le TH, De NV, Agatsuma T, Nguyen TGT, Nguyen QD, McManus DP, Blair D (2008) Human fascioliasis and the presence of hybrid/introgressed forms of Fasciola in Vietnam. Int J Parasitol 38:725–730. doi:10.1016/j.ijpara.2007.10.003
Lee D, Choe S, Park H, Jeon HJ, Chai JY, Sohn WM, Yong TS, Min DY, Rim HJ, Eom KS (2013) Complete mitochondrial genome of Haplorchis taichui and comparative analysis with other trematodes. Korean J Parasitol 51:719–726. doi:10.3347/kjp.2013.51.6.719
Lee SU, Huh S, Sohn WM, Chai JY (2004) Sequence comparisons of 28S ribosomal DNA and mitochondrial cytochrome c oxidase subunit I of Metagonimus yokogawai, M. takahashii and M. miyatai. Korean J Parasitol 42:129–135. doi:10.3347/kjp.2004.42.3.129
Leiper RT (1922) A helminthological review. Tropical Diseases Bulletin 20:364–365
Lobna SMA, Metawea YF, Elsheikha HM (2010) Prevalence of heterophyiosis in Tilapia fish and humans in Northern Egypt. Parasitol Res 107:1029–1034. doi:10.1007/s00436-010-1976-x
Martinez-Alonso JC, Armentia A, Vega JM, Callejo A, Gomez A (1999) Reacción anafiláctica coincidente con infestación por Heterophyes heterophyes. Revista Española de Alergología e Inmunología Clínica 14:37–39
Martorelli SR, Lino A, Marcotegui P, Montes MM, Alda P, Panei CJ (2012) Morphological and molecular identification of the fish-borne metacercaria of Ascocotyle (Phagicola) longa Ransom, 1920 in Mugil liza from Argentina. Vet Parasitol 190:599–603. doi:10.1016/j.vetpar.2012.07.002
McCarthy J, Moore TA (2000) Emerging helminth zoonoses. Int J Parasitol 30:1351–1360. doi:10.1016/S0020-7519(00)00122-3
Merella P, Marino G, Garippa G (2004) Heterophyid metacercariae (Trematoda: Heterophyidae) in grey mullets (Osteichthyes: Mugilidae) from the Cabras and Mistras lagoons (Sardinia, western Mediterranean). Parassitologia 46:157
Mimioğlu MM, Sayin F (1957) Ankara köpeklerinde tesbit edilen ilk Heterophyes heterophyes (V. Siebold, 1852) stiles ve Hassal, 1900 Vak’asi. Ank Univ Vet Fak Derg 4:1–5. doi:10.1501/Vetfak_0000001699
Nardi E (1959) Su di un trematode parassita intestinale del cane e della volpe. Vet Ital 10:158–162
Nieddu AM, Lochi PG (1988) Heterophydi e ospiti intermedi in Sardegna. Riv Parassitol 5:261–267
O’Hear M, Pote L, Yost M, Doffitt C, King T, Panuska C (2014) Morphologic and molecular identifications of digenetic trematodes in double-crested Cormorants (Phalacrocorax auritus) from the Mississippi Delta, USA. J Wildl Dis 50:42–49. doi:10.7589/2012-10-249
Palm HW, Waeschenbach A, Olson PD, Littlewood DTJ (2009) Molecular phylogeny and evolution of the Trypanorhyncha Diesing, 1863 (Platyhelminthes: Cestoda). Mol Phylogenet Evol 52:351–367. doi:10.1016/j.ympev.2009.01.019
Paperna I, Overstreet RM (1981) Parasites and diseases of mullets (Mugilidae). In: Oren OH (ed) Aquaculture of Grey Mullets. Cambridge University Press, Cambridge, pp 411–493
Pearson J (2008) Family Heterophyidae Leiper, 1909. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CAB International and The Natural History Museum, Wallingford, pp 113–141
Pica R (1998) Indagine di laboratorio sulle parassitosi: esperienza dell’Ospedale San Giovanni di Roma. Parassitologia 40:134
Pica R, Castellano C, Cilia C, Errico FP (2003) Intestinal fluke infections: the heterophyids. Clin Ter 154:61–63
Reiczigel J, Rózsa L, Reiczigel A (2013) Quantitative Parasitology (QPweb)., http://www2.univet.hu/qpweb. Accessed 31 March 2015
Rousset JJ, Pasticier A (1972) A propos de deux cas de distomatose à Héterophydés. Aspects épidémiologiques et cliniques. Importance de la notion d’opsopathologie. Ann Parasitol Hum Comp 47:465–474
Scala A, Garippa G, Sanna E (1991) Heterophidi e mixosporidi nei muggini della laguna del Calich (Alghero - Sassari). Bollettino della Società Italiana di Patologia Ittica 5:88–91
Scholz T (1999) Taxonomic study of Ascocotyle (Phagicola) longa Ransom, 1920 (Digenea: Heterophyidae) and related taxa. Syst Parasitol 43:147–158. doi:10.1023/A:1006120500518
Scholz T, Aguirre-Macedo ML, Salgado-Maldonado G (2001) Trematodes of the family Heterophyidae (Digenea) in Mexico: a review of species and new host and geographical records. J Nat Hist 35:1733–1772. doi:10.1080/00222930152667087
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) Mega6: Molecular Evolutionary Genetic Analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197
Taraschewski H (1984) Heterophyasis, an intestinal fluke infection of man and vertebrates transmitted by euryhaline gastropods and fish. Helgol Meeresunters 37:463–478
Taraschewski H (1985) Transmission experiments on the host specificity of Heterophyes species in 16 potential definitive hosts. Z Parasitenk 71:505–518. doi:10.1007/BF00928353
Taraschewski H, Nicolaidou A (1987) Heterophyes species in Greece: record of H. heterophyes, H.aequalis and H. dispar from the first intermediate host, Pirenella conica. J Helminthol 61:28–32. doi:10.1017/S0022149X00009676
Thaenkham U, Nawa Y, Blair D, Pakdee W (2011) Confirmation of the paraphyletic relationship between families Opisthorchiidae and Heterophyidae using small and large subunit ribosomal DNA sequences. Parasitol Int 60:521–3. doi:10.1016/j.parint.2011.07.015
Thaenkham U, Blair D, Nawa Y, Waikagul J (2012) Families Opisthorchiidae and Heterophyidae: are they distinct? Parasitol Int 61:90–93. doi:10.1016/j.parint.2011.06.004
Thu ND, Dalsgaard A, Loan LTT, Murrell KD (2007) Survey for zoonotic liver and intestinal trematode metacercariae in cultured and wild fish in An Giang Province, Vietnam. Korean J Parasitol 45:45–54. doi:10.3347/kjp.2007.45.1.45
Wells WH, Randall BH (1956) New hosts for trematodes of the genus Heterophyes in Egypt. J Parasitol 42:287–292. doi:10.2307/3274854
Witenberg G (1929) Studies on the Trematode-Family Heterophyidae. Ann Trop Med Parasitol 23:131–239
Acknowledgments
Many thanks to the fishermen of the Mistras Lagoon who collaborated to the sampling. A special thank to A Kostadinova, T Scholz and S Georgieva for the support and helpful advices. The suggestions of an anonymous reviewer contributed to improve the final version of the paper. C Spanu revised the English of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Simonetta Masala and Maria Cristina Piras contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Masala, S., Piras, M.C., Sanna, D. et al. Epidemiological and molecular data on heterophyid trematode metacercariae found in the muscle of grey mullets (Osteichthyes: Mugilidae) from Sardinia (western Mediterranean Sea). Parasitol Res 115, 3409–3417 (2016). https://doi.org/10.1007/s00436-016-5101-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-016-5101-7