1887
  1. Home
  2. Eurosurveillance
  3. Volume 26, Issue 2, 14/Jan/2021
  4. Article
Research Open Access
Like 0
Download

Abstract

Background

The increasing demand for raw or undercooked fish products, supplied by both aquaculture and fisheries, raises concerns about the transmission risk to humans of zoonotic fish parasites. This has led to the current European Union (EU) Regulation No 1276/2011 amending Annex III of Regulation (EC) No 853/2004 and mandating a freezing treatment of such products. Zoonotic parasites, particularly anisakid larvae, have been well documented in wild fish. Data on their presence in European aquaculture products, however, are still scarce, except for Atlantic salmon (), where the zoonotic risk was assessed as negligible, exempting it from freezing treatment.

Aim

To evaluate the zoonotic Anisakidae parasite risk in European farmed marine fish other than Atlantic salmon.

Methods

From 2016 to 2018 an observational parasitological survey was undertaken on 6,549 farmed fish including 2,753 gilthead seabream (), 2,761 European seabass () and 1,035 turbot () from 14 farms in Italy, Spain and Greece. Furthermore, 200 rainbow trout () sea-caged in Denmark, as well as 352 seabream and 290 seabass imported in Italy and Spain from other countries were examined. Fish were subjected to visual inspection and candling. Fresh visceral organs/fillet samples were artificially digested or UV pressed and visually examined for zoonotic anisakid larvae.

Results

No zoonotic parasites were found in any of the fish investigated.

Conclusions

The risk linked to zoonotic Anisakidae in the examined fish species from European mariculture appears negligible. This study laid the groundwork for considerations to amend the current EU regulation.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2021.26.2.1900717
2021-01-14
2024-04-19
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2021.26.2.1900717
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/26/2/eurosurv-26-2-2.html?itemId=/content/10.2807/1560-7917.ES.2021.26.2.1900717&mimeType=html&fmt=ahah

References

  1. European Food Safety Authority (EFSA). Scientific Opinion on risk assessment of parasites in fishery products. EFSA panel on Biological Hazards (BIOHAZ). EFSA J. 2010;8(4):1543.  https://doi.org/10.2903/j.efsa.2010.1543 
  2. van Thiel P, Kuipers FC, Roskam RT. A nematode parasitic to herring, causing acute abdominal syndromes in man. Trop Geogr Med. 1960;12:97-113. PMID: 13776308 
  3. Audicana MT, Kennedy MW. Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clin Microbiol Rev. 2008;21(2):360-79.  https://doi.org/10.1128/CMR.00012-07  PMID: 18400801 
  4. Mattiucci S, Cipriani P, Levsen A, Paoletti M, Nascetti G. Chapter Four. Molecular epidemiology of Anisakis and Anisakiasis: an ecological and evolutionary road map. Adv Parasitol. 2018;99:93-263.  https://doi.org/10.1016/bs.apar.2017.12.001  PMID: 29530312 
  5. Mazzucco W, Raia DD, Marotta C, Costa A, Ferrantelli V, Vitale F, et al. Anisakis sensitization in different population groups and public health impact: A systematic review. PLoS One. 2018;13(9):e0203671.  https://doi.org/10.1371/journal.pone.0203671  PMID: 30235242 
  6. Buchmann K, Mehrdana F. Effects of anisakid nematodes Anisakis simplex (s.l.), Pseudoterranova decipiens (s.l.) and Contracaecum osculatum (s.l.) on fish and consumer health. Food Waterborne Parasitol.2016;4:13-22.  https://doi.org/10.1016/j.fawpar.2016.07.003 
  7. Marty GD. Anisakid larva in the viscera of a farmed Atlantic salmon (Salmo salar). Aquaculture. 2008;279(1-4):209-10.  https://doi.org/10.1016/j.aquaculture.2008.04.006 
  8. Shih HH, Ku CC, Wang CS. Anisakis simplex (Nematoda: Anisakidae) third-stage larval infections of marine cage cultured cobia, Rachycentron canadum L., in Taiwan. Vet Parasitol. 2010;171(3-4):277-85.  https://doi.org/10.1016/j.vetpar.2010.03.023  PMID: 20400227 
  9. Heuch PA, Jansen PA, Hansen H, Sterud E, MacKenzie K, Haugen P, et al. Parasite faunas of farmed cod and adjacent wild cod populations in Norway: a comparison. Aquacult Environ Interact. 2011;2(1):1-13.  https://doi.org/10.3354/aei00027 
  10. Mo TA, Gahr A, Hansen H, Hoel E, Oaland Ø, Poppe TT. 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. J Fish Dis. 2014;37(2):135-40.  https://doi.org/10.1111/jfd.12096  PMID: 23488892 
  11. Levsen A, Maage A. Absence of parasitic nematodes in farmed, harvest quality Atlantic salmon (Salmo salar) in Norway – Results from a large-scale survey. Food Control. 2016;68:25-9.  https://doi.org/10.1016/j.foodcont.2016.03.020 
  12. Roiha IS, Maage A, Levsen A. Nasjonal Undersøking av Førekomst av Anisakis Simplex i Norsk Oppdrettsaure (Oncorhynchus mykiss). [National Survey on the occurrence of Anisakis Simplex in Norwegian Farming (Oncorhynchus mykiss)]. Nasjonait institutt for ernaerings og sjømatforskning (NIFES). Technical Report. 2017:1-12.
  13. Cammilleri G, Costa A, Graci S, Buscemi MD, Collura R, Vella A, et al. Presence of Anisakis pegreffii in farmed sea bass (Dicentrarchus labrax L.) commercialized in Southern Italy: A first report. Vet Parasitol. 2018;259:13-6.  https://doi.org/10.1016/j.vetpar.2018.06.021  PMID: 30056978 
  14. 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. Official Journal of the European Union. 2011; L327/39: 9.12.2011. Available from: https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2011:327:0039:0041:EN:PDF
  15. The Federation of European Aquaculture Producers (FEAP). European Aquaculture Production Report 2014-2019. Brussels: FEAP; Sep 2020. Available from: http://feap.info/wp-content/uploads/2020/10/20201007_feap-production-report-2020.pdf
  16. Zuur AF, Ieno EN, Smith GM. Analyzing Ecological Data. New York: Springer; 2007:672pp.
  17. Skov J, Kania PW, Olsen MM, Lauridsen JH, Buchmann K. Nematode infections of maricultured and wild fishes in Danish waters: A comparative study. Aquaculture. 2009;298(1-2):24-8.  https://doi.org/10.1016/j.aquaculture.2009.09.024 
  18. Skov J, Mehrdana F, Marana MH, Bahlool QZM, Jaafar RM, Sindberg D, et al. Parasite infections of rainbow trout (Oncorhynchus mykiss) from Danish mariculture. Aquaculture. 2014;434:486-92.  https://doi.org/10.1016/j.aquaculture.2014.08.041 
  19. Council Directive 98/58/EC of 20 July 1998 concerning the protection of animals kept for farming purposes. Official Journal of the European Union. 1998;L221: 08.08.1998. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A31998L0058
  20. Council of Europe. Standing committee of the European convention for the protection of animals kept for farming purposes (t-ap). Recommendation concerning farmed fish adopted by the Standing Committee on 5 December 2005 (In accordance with Article 9, paragraph 3 of the Convention, this Recommendation entered into force on 5 June 2006). Brussels: Council of Europe; 5 Dec 2005. Available from: https://www.coe.int/t/e/legal_affairs/legal_co-operation/biological_safety_and_use_of_animals/Farming/Rec%20fish%20E.asp
  21. 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. Official Journal of the European Union. 2005; L338/27: 22.12.2005. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/HTML/?uri=CELEX:32005R2074&from=EN
  22. Gómez-Morales MA, Martínez-Castro C, Lalle M, Fernández R, Pezzotti P, Abollo E, et al. UV-press method versus artificial digestion method to detect Anisakidae L3 in fish fillets: Comparative study and suitability for the industry. Fish Res. 2018;202:22-8.  https://doi.org/10.1016/j.fishres.2016.12.011 
  23. Karl H, Leinemann M. A fast and quantitative detection method for nematodes in fish fillets and fishery product. Arch Lebensmittelhyg. 1993;44:124-5.
  24. Berland B. Nematodes from some Norwegian marine fishes. Sarsia. 1961;2(1):1-49.  https://doi.org/10.1080/00364827.1961.10410245 
  25. Tedesco P, Gustinelli A, Caffara M, Patarnello P, Terlizzi A, Fioravanti ML. Hysterothylacium fabri (Nematoda: Raphidascarididae) in Mullus surmuletus (Perciformes: Mullidae) and Uranoscopus scaber (Perciformes: Uranoscopidae) from the Mediterranean. J Parasitol. 2018;104(3):262-74.  https://doi.org/10.1645/17-115  PMID: 29424637 
  26. Deardorff TL, Kent ML. Prevalence of larval Anisakis simplex in pen-reared and wild-caught salmon (Salmonidae) from Puget Sound, Washington. J Wildl Dis. 1989;25(3):416-9.  https://doi.org/10.7589/0090-3558-25.3.416  PMID: 2761015 
  27. Angot V, Brasseur P. European farmed Atlantic salmon (Salmo salar L.) are safe from anisakid larvae. Aquaculture. 1993;118(3-4):339-44.  https://doi.org/10.1016/0044-8486(93)90468-E 
  28. Lunestad BT. Absence of nematodes in farmed Atlantic salmon (Salmo salar L.) in Norway. J Food Prot. 2003;66(1):122-4.  https://doi.org/10.4315/0362-028X-66.1.122  PMID: 12540192 
  29. Peñalver J, Dolores EM, Muñoz P. Absence of anisakid larvae in farmed European sea bass (Dicentrarchus labrax L.) and gilthead sea bream (Sparus aurata L.) in Southeast Spain. J Food Prot. 2010;73(7):1332-4.  https://doi.org/10.4315/0362-028X-73.7.1332  PMID: 20615348 
  30. APROMAR. Evaluación de la presencia de nematodos del género Anisakis en los pescados de acuicultura marina españoles. La Acuicultura en España. 2015:1-41.
  31. Sterud E. Parasites of wild sea bass Dicentrarchus labrax from Norway. Dis Aquat Organ. 2002;48(3):209-12.  https://doi.org/10.3354/dao048209  PMID: 12033707 
  32. Bernardi C, Gustinelli A, Fioravanti ML, Caffara M, Mattiucci S, Cattaneo P. Prevalence and mean intensity of Anisakis simplex (sensu stricto) in European sea bass (Dicentrarchus labrax) from Northeast Atlantic Ocean. Int J Food Microbiol. 2011;148(1):55-9.  https://doi.org/10.1016/j.ijfoodmicro.2011.04.027  PMID: 21620507 
  33. Macrì F, Lanteri G, Rapisarda G, Costa A, Marino F. Anisakis pegreffii experimental challenge in Dicentrarchus labrax: an endoscopic study. Aquaculture. 2012;338-341:297-9.  https://doi.org/10.1016/j.aquaculture.2012.01.015 
  34. Cavallero S, El Sherif RA, Pizzarelli A, El Fituri AA, El Showhdi M, Benmosa F, et al. Occurrence of Anisakis and Hysterothylacium Nematodes in Atlantic Chub Mackerels from Libyan Coasts. Helminthologia. 2019;56(4):347-52.  https://doi.org/10.2478/helm-2019-0034  PMID: 31708677 
  35. Crotta M, Ferrari N, Guitian J. Qualitative risk assessment of introduction of anisakid larvae in Atlantic salmon (Salmo salar) farms and commercialization of products infected with viable nematodes. Food Control. 2016;69:275-84.  https://doi.org/10.1016/j.foodcont.2016.04.058 
  36. Cammilleri G, Ferrantelli V, Pulvirenti A, Drago C, Stampone G, Del Rocio Quintero Macias G, et al. Validation of a Commercial Loop-Mediated Isothermal Amplification (LAMP) Assay for the Rapid Detection of Anisakis spp. DNA in Processed Fish Products. Foods. 2020;9(1):92.  https://doi.org/10.3390/foods9010092  PMID: 31963107 
Negligible risk of zoonotic anisakid nematodes in farmed fish from European mariculture, 2016 to 2018
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Maria+Letizia+Fioravanti&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Fioravanti Maria Letizia</a>, <a href="/search?value1=Andrea+Gustinelli&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Gustinelli Andrea</a>, <a href="/search?value1=George+Rigos&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Rigos George</a>, <a href="/search?value1=Kurt+Buchmann&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Buchmann Kurt</a>, <a href="/search?value1=Monica+Caffara&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Caffara Monica</a>, <a href="/search?value1=Santiago+Pascual&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pascual Santiago</a>, <a href="/search?value1=Miguel+%C3%81ngel+Pardo&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pardo Miguel Ángel</a></span>. Negligible risk of zoonotic anisakid nematodes in farmed fish from European mariculture, 2016 to 2018. <a href="/content/ecdc">Euro Surveill.</a> 2021;26(2):pii=1900717. <a href="https://doi.org/10.2807/1560-7917.ES.2021.26.2.1900717" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2021.26.2.1900717</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 20 Nov 2019;&nbsp;&nbsp; <span class="generated">Accepted</span>: 22 Jun 2020 </span> </p>
/content/10.2807/1560-7917.ES.2021.26.2.1900717
/content/10.2807/1560-7917.ES.2021.26.2.1900717
Loading

Data & Media loading...

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error