LARVAL STAGES OF SULCASCARIS SULCATA (NEMATODA: ANISAKIDAE) IN SCALLOPS FROM THE NORTHERN ADRIATIC SEA: IMPLICATIONS FOR SEAFOOD CONTROL AND SURVEILLANCE
Main Article Content
Keywords
emerging parasites, food legislation, nematode, RFLP, scallop, Sulcascaris sulcata
Abstract
A survey of fresh great Mediterranean scallops (Pecten jacobaeus) and frozen queen scallops (Aequipecten opercularis) collected from the northern Adriatic Sea demonstrated the presence of nematode larvae that were morphologically and molecularly identified as Sulcascaris sulcata. The presence of this nematode in the northern Adriatic Sea has been described in the logger head sea turtle, which is the final host, but it was only recently described in the intermediate molluscan host. Affected scallops present rust-brown lesions in the adductor muscle. In this study, necroscopic and histopathological lesions are described in affected scallops. Furthermore, the detrimental effects of this parasite on the commercialization of scallops under the current European legislation concerning the hygiene of seafood products are evaluated.
References
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Cobb N.A. 1930. A nemic parasite of Pecten. J. Parasitol. 17:104-105.
D’Amelio S., Mathiopoulos K.D., Santos C.P., Pugachev O.N., Webb S.C., Picanco M. and Paggi L. 1999. Genetic markers in ribosomial DNA for the identification of the genus Anisakis (Nematoda: Ascaridoidea) defined by polymerase chain reaction-based restriction fragment length polymorphism. Int. J. Parasitol. 30(2):223-226.
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EC-European Community. 2004. Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. Off. J. Europ. Union L 139:55-205
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Manfredi M.T., Piccolo G. and Meotti C. 1998. Parasites in Italian sea turtles. II. Loggerhead turtle. Parassitologia. 40:305-308.
Marangi M., Carlino P., Profico C., Olivieri V., Totaro G., Furii G., Marzano G. and Papini R.A. 2020. First multicenter coprological survey on helminth parasite communities of free-living loggerhead sea turtles Caretta caretta (Linnaeus, 1758) from the Adriatic Sea and Northern Ionian Sea. Int. J. Parasitol. Parasites Wildl. 21:207-212.
Marcer F., Tosi F., Franzo G., Vetri A., Ravagnan S., Santoro M. and Marchiori E. 2020. Updates on ecology and life cycle of Sulcascaris sulcata (Nematoda: Anisakidae) in Mediterranean grounds: molecular identification of larvae infecting edible scallops. Frontiers in Vet. Science. 7:1-7.
Rudders D., Roman S., Fisher R. A., Bushek D., MunroeD., Bochenek E. A., McGurk E. and Borsetti S. 2019. An investigation into the scallop parasite outbreak on the mid-atlantic shelf: transmission pathways, spatio-temporal variation of infection and consequences to marketability: final report. Marine Resource Report No. 02. Virginia Institute of Marine Science, Gloucester Point, VA.
Santoro M., Badillo F.J., Mattiucci S., Nascetti G., Bentivegna F., Insacco G., Travaglini A., Paoletti M., Kinsella J.M., Tomás J., Raga J.A. and Aznar F.J. 2010. Helminth communities of loggerhead turtles (Caretta caretta) from Central and Western Mediterranean Sea: the importance of host’s ontogeny. Parasitol. Int. 59(3):367-375.
Santoro M., Marchiori E., Iaccarino D., Uberti B.D., Cassini R., Di Nocera F., Cerrone A., Galiero G. and Marcer F. 2019. Epidemiology of Sulcascaris sulcata (Nematoda: Anisakidae) ulcerous gastritis in the Mediterranean loggerhead sea turtle (Caretta caretta). Parasitol. Res. 118:1457-1463.
Santoro M., Marchiori E., Palomba ML., Degli Uberti B., Marcer F. and Mattiucci S. 2020. The Mediterranean mussel (Mytilus galloprovincialis) as intermediate host for the anisakid Sulcascaris sulcata (Nematoda), a pathogen parasite of the Mediterranean loggerhead turtle (Caretta caretta). Pathogens. 118:1-8.
Werneck M.R., Martos Thomazini C., Shigueru Mori E., Gonçalves V.T., Gallo B.M.G. and Da Silva R.J. 2008. Gastrointestinal helminth parasites of loggerhead turtle Caretta caretta (Linnaeus 1758) (Testudines, Cheloniidae) in Brazil. Pan-Am. J. Aquat. Sci. 3(3):351-354.
Zhu X., D'Amelio S., Paggi L. and Gasser R.B. 2000. Assessing sequence variation in the internal transcribed spacers of ribosomal DNA within and among members of the Contracaecum osculatum complex (Nematoda: Ascaridoidea: Anisakidae).Parasitol. Res. 86:677-83.
Berry G.N. and Cannon L.R.G. 1981. The life history of Sulcascaris sulcata (Nematoda: Ascaridoidea), a parasite of marine molluscs and turtles. Int. J. Parasitol. 11:43-54.
Cobb N.A. 1930. A nemic parasite of Pecten. J. Parasitol. 17:104-105.
D’Amelio S., Mathiopoulos K.D., Santos C.P., Pugachev O.N., Webb S.C., Picanco M. and Paggi L. 1999. Genetic markers in ribosomial DNA for the identification of the genus Anisakis (Nematoda: Ascaridoidea) defined by polymerase chain reaction-based restriction fragment length polymorphism. Int. J. Parasitol. 30(2):223-226.
Daschner A. 2016. Risks and possible health effects of raw fish intake. Ch. 31. In: “Fish and Fish Oil in Health and Disease Prevention”. S.K. Raatz and D.M. Bibus (Ed.), pp. 341-353. Academic Press, Cambridge, MA. Deardorff T.L. 1989. Occurrence of larval Sulcascaris sulcata (Nematoda: Anisakidae) in the calico scallop, Argopecten gibbus, collected along the Eastern coast of Florida, with comments on histopathology. P. Helm. Soc. Wash. 56:82-85.
EC-European Community. 2005. Commission Regulation (EC) No 2074/2005 of 5 December 2005 laying down implementing measures for certain products under Regulation (EC) No 853/2004 of the European Parliament and of the Council and for the organisation of official controls under Regulation (EC) No 854/2004 of the European Parliament and of the Council and Regulation (EC) No 882/2004 of the European Parliament and of the Council, derogating from Regulation (EC) No 852/2004 of the European Parliament and of the Council and amending Regulations (EC) No 853/2004 and (EC) No 854/2004. GU L 338/27, 22.12.2005.
EC-European Community. 2004. Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. Off. J. Europ. Union L 139:55-205
EU-European Union. 2011. Commission Regulation (EU) No 1276/2011 of 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. GU L 327, 9.12.2011.
Garbin L., Mattiucci S., Paoletti M., González-Acuña D. and Nascetti G. 2011. Genetic and morphological evidences for the existence of a new species of Contracaecum (Nematoda: Anisakidae) parasite of Phalacrocorax brasilianus (Gmelin) from Chile and its genetic relationships with congeners from fish-eating birds. J. Parasitol. 97:476-492.
González-Amores Y., Clavijo-Frutos E., Salas-Casanova C. and Alcain-Martínez G. 2017. Direct parasitological diagnosis of infection with Hysterothylacium aduncum in a patient with epigastralgia. Rev. Esp. Enferm. Dig. 107:699-700.
Gra?an R., Burši? M., Mladineo I., Ku?ini? M., Lazar B. and Lackovi? G. 2012. Gastrointestinal helminth community of loggerhead sea turtles Caretta carettain the Adriatic Sea. Dis. Aquat. Org. 99:227-236.
Greiner E.C. 2013. Parasites of marine turtles. Ch. 16. In: “The Biology of Sea Turtles”. J. Wyneken, K.J. Lohmann and J.A. Musick (Ed.), pp. 427-446. CRC Press, Boca Raton, FL.
Howard D.W., Lewis E. J., Keller B. J. and Smith C.S. 2004.Histological techniques for marine bivalve mollusks and crustaceans. 2nd ed. NOAA Technical Memorandum NOS NCCOS 5 (Ed.), pp. 69-84. Oxford, MD.
Jackson G.J., Bier J.W., Payne W.L. and McClure F.D. 1981. Recovery of parasitic nematodes from fish by digestion or elution. Appl. Environ. Microbiol. 41:912-914.
Lauckner G. 1983. Diseases of mollusca: Bivalvia. In “Diseases of Marine Animals: 2. Introduction, Bivalvia to Scaphopoda”. O. Kinne (Ed.), pp. 520-608. Biologische Anstalt Helgoland, Hamburg, DE.
Lazar B., Gra?an R., Kati? J., Zavodnik D., Jaklin A. and Tvrtkovi? N. 2011. Loggerhead sea turtles (Caretta caretta) as bioturbators in neritic habitats: an insight through the analysis of benthic molluscs in the diet. Marine Ecology. 32:65-74.
Lester R.J.G., Blair D. and Heald D. 1980. Nematodes from scallops and turtles from Shark Bay, Western Australia. Aust. J. Mar. Freshwater Res. 3:713-717.
Lichtenfels J. R., Bier J.W. and Madden P.A. 1978. Larval anisakid (Sulcascaris) nematodes from Atlantic molluscs with marine turtles as definitive hosts. T. Am. Microsc. Soc. 97:199-207.
Manfredi M.T., Piccolo G. and Meotti C. 1998. Parasites in Italian sea turtles. II. Loggerhead turtle. Parassitologia. 40:305-308.
Marangi M., Carlino P., Profico C., Olivieri V., Totaro G., Furii G., Marzano G. and Papini R.A. 2020. First multicenter coprological survey on helminth parasite communities of free-living loggerhead sea turtles Caretta caretta (Linnaeus, 1758) from the Adriatic Sea and Northern Ionian Sea. Int. J. Parasitol. Parasites Wildl. 21:207-212.
Marcer F., Tosi F., Franzo G., Vetri A., Ravagnan S., Santoro M. and Marchiori E. 2020. Updates on ecology and life cycle of Sulcascaris sulcata (Nematoda: Anisakidae) in Mediterranean grounds: molecular identification of larvae infecting edible scallops. Frontiers in Vet. Science. 7:1-7.
Rudders D., Roman S., Fisher R. A., Bushek D., MunroeD., Bochenek E. A., McGurk E. and Borsetti S. 2019. An investigation into the scallop parasite outbreak on the mid-atlantic shelf: transmission pathways, spatio-temporal variation of infection and consequences to marketability: final report. Marine Resource Report No. 02. Virginia Institute of Marine Science, Gloucester Point, VA.
Santoro M., Badillo F.J., Mattiucci S., Nascetti G., Bentivegna F., Insacco G., Travaglini A., Paoletti M., Kinsella J.M., Tomás J., Raga J.A. and Aznar F.J. 2010. Helminth communities of loggerhead turtles (Caretta caretta) from Central and Western Mediterranean Sea: the importance of host’s ontogeny. Parasitol. Int. 59(3):367-375.
Santoro M., Marchiori E., Iaccarino D., Uberti B.D., Cassini R., Di Nocera F., Cerrone A., Galiero G. and Marcer F. 2019. Epidemiology of Sulcascaris sulcata (Nematoda: Anisakidae) ulcerous gastritis in the Mediterranean loggerhead sea turtle (Caretta caretta). Parasitol. Res. 118:1457-1463.
Santoro M., Marchiori E., Palomba ML., Degli Uberti B., Marcer F. and Mattiucci S. 2020. The Mediterranean mussel (Mytilus galloprovincialis) as intermediate host for the anisakid Sulcascaris sulcata (Nematoda), a pathogen parasite of the Mediterranean loggerhead turtle (Caretta caretta). Pathogens. 118:1-8.
Werneck M.R., Martos Thomazini C., Shigueru Mori E., Gonçalves V.T., Gallo B.M.G. and Da Silva R.J. 2008. Gastrointestinal helminth parasites of loggerhead turtle Caretta caretta (Linnaeus 1758) (Testudines, Cheloniidae) in Brazil. Pan-Am. J. Aquat. Sci. 3(3):351-354.
Zhu X., D'Amelio S., Paggi L. and Gasser R.B. 2000. Assessing sequence variation in the internal transcribed spacers of ribosomal DNA within and among members of the Contracaecum osculatum complex (Nematoda: Ascaridoidea: Anisakidae).Parasitol. Res. 86:677-83.