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Quantification and distribution of Anisakis simplex sensu stricto in wild, one sea winter Atlantic salmon, Salmo salar, returning to Scottish rivers

Published online by Cambridge University Press:  07 October 2014

Patricia Noguera ,
Campbell Pert ,
Catherine Collins ,
Nichola Still  and
David Bruno
Patricia Noguera*
Affiliation:
Marine Laboratory, Marine Scotland Science, 375 Victoria Road, Aberdeen AB11 9DB, Scotland
Campbell Pert
Affiliation:
Marine Laboratory, Marine Scotland Science, 375 Victoria Road, Aberdeen AB11 9DB, Scotland
Catherine Collins
Affiliation:
Marine Laboratory, Marine Scotland Science, 375 Victoria Road, Aberdeen AB11 9DB, Scotland
Nichola Still
Affiliation:
Marine Laboratory, Marine Scotland Science, 375 Victoria Road, Aberdeen AB11 9DB, Scotland
David Bruno
Affiliation:
Marine Laboratory, Marine Scotland Science, 375 Victoria Road, Aberdeen AB11 9DB, Scotland
*
Correspondence should be addressed to: P. Noguera, Marine Laboratory, Marine Scotland Science, 375 Victoria Road, Aberdeen AB11 9DB, Scotland email: [email protected]
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Abstract

Red vent syndrome (RVS) has previously been reported in returning wild Atlantic salmon, Salmo salar from Canada, Iceland, Ireland, Norway and the UK. Affected fish show reddening and swelling in the perianal/vent area, with scale loss, ulceration and bleeding in severe cases. Studies in the UK and elsewhere report the condition to be induced by Anisakis simplex sensu stricto (s.s.) larvae. This parasite, commonly reported in several marine fish species, is typically found in the body cavity and the skeletal muscle, but has recently been reported within the vent tissues of salmon. This latter finding may reflect greater efforts in examining this body portion due to current awareness of the parasite presence in this atypical location. Based on clinical observations, affected fish are classified into three categories according to the severity of the external lesions, but quantification of the vent parasite numbers in relation to the categories, and assessment of the relative importance of this area as a site of infestation, are missing to date. This investigation aimed to provide data on parasite number and distribution in the viscera, skeletal muscle, peduncle and vent area and to confirm the identity of the larvae found in the vent and the viscera. The study showed the perianal/vent region harbours the highest total number of A. simplex larvae per fish and, proportionally to fish biomass, is the most heavily infested body location irrespective of external severity levels of RVS.

Keywords

red ventAnisakis simplex sensu strictoAtlantic salmonwild fish
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 2 , March 2015 , pp. 391 - 399
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

REFERENCES

Abollo, E., Paggi, L., Pascual, S. and D'Amelio, S. (2003) Occurrence of recombinant genotypes of Anisakis simplex s.s. and Anisakis pegreffii (Nematoda: Anisakidae) in an area of sympatry. Infection, Genetics and Evolution 3, 175–181.CrossRefGoogle Scholar
Angot, V. and Brasseur, P. (1993) European farmed salmon (Salmo salar L.) are safe from anisakid larvae. Aquaculture 118, 339–344.CrossRefGoogle Scholar
Audicana, M.T. and Kennedy, M.W. (2008) Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clinical Microbiology Reviews 21, 360–379.CrossRefGoogle ScholarPubMed
Audicana, M.T., Ansotegui, I.J., Fernández de Corres, L. and Kennedy, M.W. (2002) Anisakis simplex: dangerous – dead and alive? Trends in Parasitology 18, 20–25.CrossRefGoogle ScholarPubMed
Audicana, M.T., del Pozo, M.D., Iglesias, R. and Ubeira, F.M. (2003) Anisakis simplex and Pseudoterranove decipiens. In Miliotis, M.D. and Bier, J.W. (eds) International handbook of foodborne pathogens, New York, NY: Marcel Dekker, pp. 613–636.Google Scholar
Bachellerie, J.P. and Qu, L.H. (1993) Ribosomal RNA probe for detection and identification of species. In Hyde, J.E. (ed.) Protocols in molecular parasitology, Clifton, NJ: Humana Press, pp. 249–264.CrossRefGoogle Scholar
Beaugrand, G., Reid, P.C., Ibañez, F., Lindley, J.A. and Edwards, M. (2002) Reorganisation of North Atlantic copepod biodiversity and climate. Science 296, 1692–1694.CrossRefGoogle Scholar
Beck, M., Evans, R., Feist, S.W., Stebbing, P., Longshaw, M. and Harris, E. (2008) Anisakis simplex sensu lato associated with red vent syndrome in wild Atlantic salmon Salmo salar in England. Diseases of Aquatic Organisms 82, 61–65.CrossRefGoogle ScholarPubMed
Beverley-Burton, M. and Pippy, J.H.C. (1978) Distribution, prevalence and mean numbers of larval Anisakis simplex (Nematoda: Ascaridoidea) in Atlantic salmon, Salmo salar L. and their use as biological indicators of host stocks. Environmental Biology of Fishes 3, 211–222.CrossRefGoogle Scholar
Bristow, G.A. and Berland, B. (1991) A report on some metazoan parasites of wild marine salmon (Salmo salar L.) from the west coast of Norway with comments on their interactions with farmed salmon. Aquaculture 98, 311–348.CrossRefGoogle Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. and Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al., revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Couture, C., Measures, L., Gagnon, J. and Desbiens, C. (2003) Human intestinal anisakiosis due to consumption of raw salmon. American Journal of Pathology 27, 1167–1172.Google ScholarPubMed
Cunningham, C.O., Mo, T.A., Collins, C.M., Buchmann, K., Thiery, R., Blanc, G. and Lautraite, A. (2001) Redescription of Gyrodactylus teucjis Lautraite, Blanc, Thiery, Daniel & Vigneulle, 1999 (Monogenea: Gyrodactylidae); a species identified by ribosomal RNA sequence. Systematic Parasitology 48, 141–150.CrossRefGoogle ScholarPubMed
D'Amelio, S., Mathiopoulus, K.D., Santos, C.P., Pugachev, O.N., Webb, S.C., Picanço, M. and Paggi, L. (2000) Genetic markers in ribosomal DNA for the identification of members of the genus Anisakis (Nematoda: Ascaridoidea) defined by polymerase chain reaction-based restriction fragment length polymorphism. International Journal of Parasitology 30, 223–226.CrossRefGoogle ScholarPubMed
Deardorff, L. and Kent, M.L. (1989) Prevalence of larval Anisakis simplex in pen-reared and wild-caught salmon (Salmonidae) from Puget Sound, Washington. Journal of Wildlife Diseases 25, 416–419.CrossRefGoogle Scholar
Dittmer, K. (2013) Changing streamflow on Columbia basin tribal lands – climate change and salmon. Climate Change 120, 627–641.CrossRefGoogle Scholar
EFSA. (2010) Scientific Opinion on risk assessment of parasites in fishery products EFSA Panel on Biological Hazards (BIOHAZ). European Food Safety Authority Journal 8, 91.Google Scholar
Friedland, K.D., Shank, B.V., Todd, C.D., McGinnity, P. and Nye, J.A. (2013) Differential response of continental stock complexes of Atlantic salmon (Salmo salar) to the Atlantic Multidecadal Oscillation. Journal of Marine Sciences. doi: 10.1016/j.jmarsys.2013.03.003.CrossRefGoogle Scholar
Gutiérrez-Galindo, J.F., Osanz-Mur, A.C. and Mora-Ventura, M.T. (2010) Occurrence and infection dynamics of anisakid larvae in Scomber scombrus, Trachurus trachurus, Sardina pilchardus, and Engraulis encrasicolus from Tarragona (NE Spain). Food Control 21, 1550–1555.CrossRefGoogle Scholar
Haarder, S., Kania, P.W. and Buchmann, K. (2013) Comparative infectivity of three larval nematode species in three different salmonids. Parasitology Research 112, 2997–3004.CrossRefGoogle ScholarPubMed
Hauck, A.K. and May, E.B. (1977) Histopathologic alterations with Anisakis larvae in pacific herring from Oregon. Journal of Wildlife Diseases 13, 290–293.CrossRefGoogle ScholarPubMed
Helgason, S., Slavko, H.B. and Kristmundsson, A. (2008) Red vent syndrome in wild Atlantic salmon (Salmo salar) in Icelandic waters. In International Conference of Fish Diseases and Fish Immunology, Reykjavik, Iceland, pp. 4–7.Google Scholar
Jackson, G.J., Bier, J.W., Payne, W.L. and McClure, F.D. (1981) Recovery of parasitic nematodes from fish by digestion or elution. Applied and Environmental Microbiology 41, 912–914.CrossRefGoogle ScholarPubMed
Karl, H., Baumann, F., Ostermeyer, U., Kuhn, T. and Klimpel, S. (2011) Anisakis simplex (s.s.) larvae in wild Alaska salmon: no indication of post-mortem migration from viscera into flesh. Diseases of Aquatic Organisms 94, 201–209.CrossRefGoogle ScholarPubMed
Kuhn, T., García-Màrquez, J. and Klimpel, S. (2011) Adaptive radiation within marine anisakid nematodes: a zoogeographical modeling of cosmopolitan, zoonotic parasites. PLoS ONE 6, e28642. doi: 10.1371/journal.pone.0028642.CrossRefGoogle ScholarPubMed
Lamps, L.W. (ed.) (2010) Anisakis simplex and related nematodes. In Surgical pathology of the gastrointestinal system: bacterial, fungal, viral, and parasitic infections. New York, NY: Springer, pp. 211–213.CrossRefGoogle Scholar
Larrat, S., Bouchard, F., Séguin, G. and Lair, S. (2013) Relationship between red vent syndrome and anisakid larvae burden in wild Atlantic salmon (Salmo salar). Journal of Wildlife Diseases 49, 229–234.CrossRefGoogle ScholarPubMed
Levsen, A. and Karl, H. (2014) Anisakis simplex (s.l.) in Grey gurnard (Eutrigla gurnardus) from the North Sea: food safety considerations in relation to fishing ground and distribution in the flesh. Food Control 36, 15–19.CrossRefGoogle Scholar
Levsen, A. and Lunestad, B.T. (2010) Anisakis simplex third stage larvae in Norwegian spring spawning herring (Clupea harengus L.), with emphasis on larval distribution in the flesh. Veterinary Parasitology 171, 247–253.CrossRefGoogle ScholarPubMed
Mattiucci, S. and Nascetti, G. (2006) Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite 13, 99–113.CrossRefGoogle ScholarPubMed
Mattiucci, S. and Nascetti, G. (2008) Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Advances in Parasitology 66, 47–148.CrossRefGoogle ScholarPubMed
Mattiucci, S., D'Amelio, S. and Rokicki, J. (1989) Electrophoretic identification of Anisakis sp. larvae (Ascaridida: Anisakidae) from Clupea harengus L. in Baltic Sea. Parassitologia 31, 45–49.Google ScholarPubMed
Mattiucci, S., Nascetti, G., Cianchi, R., Paggi, L., Arduino, P., Margolis, L., Brattey, J., Webb, S., D'Amelio, S., Orecchia, P. and Bullini, L. (1997) Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). Journal of Parasitology 83, 401–406.CrossRefGoogle ScholarPubMed
Mattiucci, S., Paoletti, M., Borrini, F., Palumbo, M., Macarone Palmieri, R., Gomes, V., Casati, A. and Nascetti, F. (2011) First molecular identification of the zoonotic parasite Anisakis pegreffii (Nematoda: Anisakidae) in a paraffin-embedded granuloma taken from a case of human intestinal anisakiasis in Italy. BMC Infectious Diseases 11, 82.CrossRefGoogle Scholar
Mills, K.E., Pershing, A.J., Sheehan, T.F. and Mountain, D. (2013) Climate and ecosystem linkages explain widespread declines in North American Atlantic salmon populations. Global Change Biology 19, 3046–3061.CrossRefGoogle ScholarPubMed
Mo, T.A., Senos, R., Hansen, H. and Poppe, T.T. (2010) Red vent syndrome associated with Anisakis simplex diagnosed in Norway. Bulletin of the European Association of Fish Pathologists 30, 197–201.Google Scholar
Mo, T.A., Gahr, A., Hansen, H., Hoel, E., Oaland, Ø. and Poppe, T.T. (2014) Presence of Anisakis simplex (Rudolphi, 1809 det. Krabbe, 1878) and Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda; Anisakidae) in runts of farmed Atlantic salmon, Salmo salar L. Journal of Fish Diseases 37, 135–140.CrossRefGoogle ScholarPubMed
Möllmann, C., Diekmann, R., Müller-Karulis, B., Kornilovs, G., Plikshs, M. and Axe, P. (2009) Reorganization of a large marine ecosystem due to atmospheric and anthropogenic pressure: a discontinuous regime shift in the Central Baltic Sea. Global Change Biology 15, 1377–1393.CrossRefGoogle Scholar
Moravec, F. (2004) Some aspects of the taxonomy and biology of dracunculoid nematodes parasitic in fishes: a review. Folia Parasitologica (Praha) 51, 1–13.CrossRefGoogle ScholarPubMed
Murphy, T.M., Berzano, M., O'Keeffe, S.M., Cotter, D.M., McEvoy, S.E., Thomas, K.A., Maoiléidigh, N.P.Ó. and Whelan, K.F. (2010) Anisakid larvae in Atlantic salmon (Salmo salar L.) grilse and post-smolts: molecular identification and histopathology. Journal of Parasitology 96, 77–82.CrossRefGoogle ScholarPubMed
Noguera, P., Bruno, D.W., Pert, C.C. and Webb, J. (2008) Red vent syndrome (RVS) in wild Atlantic salmon: an update on research and monitoring in Scotland. Atlantic Salmon Trust Journal Summer, 25–27.Google Scholar
Noguera, P., Beck, M., Williams, C. and Longshaw, M. (2009a) Observations on red vent syndrome (RVS) in wild Atlantic salmon in the UK. Fin Fish News 7, 30–33.Google Scholar
Noguera, P., Collins, C., Bruno, D., Pert, C., Turnbull, A., McIntosh, A., Lester, K., Bricknell, I., Wallace, S. and Cook, P. (2009b) Anisakis simplex sensu stricto (Nematoda: Anisakidae) in red vent syndrome affected wild Atlantic salmon Salmo salar in Scotland. Diseases of Aquatic Organisms 87, 199–215.CrossRefGoogle ScholarPubMed
Novotny, A.J. and Uzmann, J.R. (1960) A statistical analysis of the distribution of a larval nematode (Anisakis sp.) in the musculature of chum salmon (Oncorhynchus keta). Experimental Parasitology 10, 245–262.CrossRefGoogle Scholar
Pert, C.C., Noguera, P.A. and Bruno, D.W. (2009) Scottish red vent survey (2008). Marine Scotland internal report 07/09. http://www.scotland.gov.uk/Uploads/Documents/Int0709c.pdf.Google Scholar
Podolska, M. and Horbowy, J. (2003) Infection of Baltic herring (Clupea harengus membras) with Anisakis simplex larvae, 1992–1999: a statistical analysis using generalized linear models. ICES Journal of Marine Science 60, 85–93.CrossRefGoogle Scholar
Pontes, T., D'Amelio, S., Costa, G. and Paggi, L. (2005) Molecular characterisation of larval anisakid nematodes from marine fishes of Maderia by a PCR-based approach, with evidence for a new species. Journal of Parasitology 91, 1430–1434.CrossRefGoogle Scholar
Pörtner, H.O. (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 132, 739–761.CrossRefGoogle ScholarPubMed
Pörtner, H.O. and Farrell, A.P. (2008) Physiology and climate change. Science 322, 690–692.CrossRefGoogle ScholarPubMed
Pörtner, H.O. and Peck, M.A. (2010) Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. Journal of Fish Biology 77, 1745–1779.CrossRefGoogle ScholarPubMed
Quiazon, K.M.A., Yoshinaga, T. and Ogawa, K. (2011) Experimental challenge of Anisakis simplex sensu stricto and Anisakis pegreffii (Nematoda: Anisakidae) in rainbow trout and olive flounder. Parasitology International 60, 126–131.CrossRefGoogle ScholarPubMed
Senos, M., Poppe, T.T., Hansen, H. and Mo, T.A. (2013) Tissue distribution of Anisakis simplex larvae (Nematoda; Anisakidae) in wild Atlantic salmon, Salmo salar, from the Drammenselva river, south-east Norway. Bulletin of the European Association of Fish Pathologists 33, 111–117.Google Scholar
Setyobudi, E., Seong, K.-B., Lee, C.H. and Kim, J.-H. (2009) Anisakis simplex (Nematode: Anisakidae) larvae infection in Chum salmon (Oncorhynchus keta) from Namdae River, Korea in 2008. North Pacific Anadromous Fish Commission Doc. 1200, 6 pp.Google Scholar
Setyobudi, E., Seong, K.-B. and Kim, J.-H. (2010) Anisakis simplex (Nematode: Anisakidae) L3 larvae infection in chum salmon (Oncorhynchus keta) from Namdae river, South Korea in 2009. North Pacific Anadromous Fish Commission Doc. 1257, 4 pp.Google Scholar
Shearer, W.M. (1992) The Atlantic salmon: natural history, exploitation and future management. Oxford: Blackwell Scientific.Google Scholar
Smith, J.W. and Hemmingsen, W. (2003) Atlantic cod Gadus morhua L.: visceral organ topography and the asymetrical distribution of larval ascaridoid nematodes in the musculature. Ophelia 57, 137–144.CrossRefGoogle Scholar
Strømnes, E. and Andersen, K. (1998) Distribution of whaleworm (Anisakis simplex, Nematoda, Ascaridoidea) L3 larvae in three species of marine fish; saithe (Pollachius virens (L.)), cod (Gadus morhua L.) and redfish (Sebastes marinus (L.)) from Norwegian waters. Parasitology Research 84, 281–285.Google ScholarPubMed
Suzuki, J., Murat, R., Hosaka, M. and Araki, J. (2010) Risk factors for human Anisakis infection and association between the geographic origins of Scomber japonicus and anisakid nematodes. International Journal of Food Microbiology 137, 88–93.CrossRefGoogle ScholarPubMed
Todd, C.D., Hughes, S.L., Marshall, C.T., MacLean, J.C., Lonergan, M.E. and Biuw, E.M. (2008) Detrimental effects of recent ocean surface warming on growth condition of Atlantic salmon. Global Change Ecology 14, 958–970.CrossRefGoogle Scholar
Todd, C.D., Friedland, K.D., MacLean, J.C., Whyte, B.D., Russell, I.C., Lonergan, M.E. and Morrissey, M.B. (2012) Phenological and phenotypic changes in Atlantic salmon populations in response to a changing climate. ICES Journal of Marine Science 69, 1686–1698.CrossRefGoogle Scholar
Umehara, A., Kawakami, Y., Araki, J. and Uchida, A. (2007) Molecular identification of the etiological agent of the human anisakiasis in Japan. Parasitology International 56, 211–215.CrossRefGoogle ScholarPubMed
Valdimarsson, G., Einarsson, H. and King, F.J. (1985) Detection of parasites in fish muscle by candling technique. Journal of the Association of Official Analytical Chemists 68, 549–551.Google Scholar
Valtonen, T.E., Rintamäki, P. and Karvonen, A. (2007) Climate change and parasitic problems in fish farms. Parassitologia 49, 277.Google Scholar
Wootten, R. and Waddell, I.F. (1977) Studies on the biology of larval nematodes from the musculature of cod and whiting in Scottish waters. Journal du Conseil International pour l'Exploration de la Mer 37, 266–273.CrossRefGoogle Scholar