Thermal patterns of heat treated Anisakis L3-infected fishery products allow separation into low, intermediate and high risk groups of potential use in risk management

Abstract Anisakis third-stage larvae (L3) is moderately tolerant to heat and, to mitigate the risk of live L3 intake in cooked seafood, it is important to define with precision at which point after heat treatment the parasite is no longer infective. We aimed to find thermal patterns that allowed to classify fish sandwiches spiked with Anisakis L3 into “low” (100% probability of mortality), “intermediate” and “high” risk groups. For that, experiments with varying set temperatures and heating times have been performed in conditions of different external heating temperatures. Decision points to classify the samples into terminal nodes associated to different risk groups have been obtained with decision tree analyses and then confirmed with linear discriminant analysis. Separation into two (i.e. low vs high + intermediate risk) or three (i.e. low, intermediate, and high risk) distinct thermal patterns (98% and 95.9% correct classifications by cross-validation respectively) was achieved. These results refine heating conditions reported in the EU Regulation, since reaching 60 °C for 1 min in the thermal centre is not sufficient to kill all L3. However, when factors such as relative temperature of heating or time to reach the set temperature are taken into account, other thermal conditions are found that are equally safe in terms of Anisakis L3 inactivation. This, together with the description of “intermediate” and “high” risk groups can help in the risk identification and management, as well as in providing clearer recommendations to consumers.

[1]  J. C. Jaeger,et al.  Conduction of Heat in Solids , 1952 .

[2]  M. Tejada,et al.  Antigenicity and viability of Anisakis larvae infesting hake heated at different time-temperature conditions. , 2010, Journal of food protection.

[3]  E. Ruitenberg Anisakiasis. Pathogenesis, serodiagnosis and prevention. , 1970 .

[4]  K. Davey,et al.  Stimuli for cuticle formation and ecdysis in vitro of the infective larva of Anisakis sp. (Nematoda: Ascaridoidea). , 1976, International journal for parasitology.

[5]  K. Ronald THE EFFECTS OF PHYSICAL STIMULI ON THE LARVAL STAGE OF TERRANOVA DECIPIENS (KRABBE, 1878) (NEMATODA:ANISAKIDAE): I. TEMPERATURE , 1960 .

[6]  R. Cecere,et al.  Anisakis simplex Hypersensitivity Is Associated with Chronic Urticaria in Endemic Areas , 2012, International Archives of Allergy and Immunology.

[7]  M. Tejada,et al.  Viability and antigenicity of anisakis simplex after conventional and microwave heating at fixed temperatures. , 2011, Journal of Food Protection.

[8]  S. Magnino,et al.  Risk assessment of parasites in fishery products , 2011 .

[9]  M. Tejada,et al.  Scanning electron microscopy of Anisakis larvae following different treatments. , 2006, Journal of food protection.

[10]  M. Prado-Rosas,et al.  Changes in the Anatomical Organization of Contracaecum multipapillatum L3 sensu lato (Nematoda: Anisakidae) Larvae Subjected to Different Culinary Treatments in La Paz, Baja California Sur, Mexico , 2014 .

[11]  N. Nieuwenhuizen,et al.  Allergic Reactions to Anisakis Found in Fish , 2014, Current Allergy and Asthma Reports.

[12]  N. Marcon,et al.  Common Symptoms from an Uncommon Infection: Gastrointestinal Anisakiasis , 2016, Canadian journal of gastroenterology & hepatology.

[13]  M. Tejada,et al.  Pathogenic potential of Anisakis L3 after freezing in domestic freezers , 2018 .

[14]  G. Pierce,et al.  Human health, legislative and socioeconomic issues caused by the fish-borne zoonotic parasite Anisakis: Challenges in risk assessment , 2019, Trends in Food Science & Technology.

[15]  Mercedes Careche,et al.  Estimation of freezing storage time and quality changes in hake (Merluccius merluccius, L.) by low field NMR. , 2012, Food chemistry.

[16]  A. Navas,et al.  Freezing kinetic parameters influence allergenic and infective potential of Anisakis simplex L3 present in fish muscle , 2020 .

[17]  M. Tejada,et al.  Anisakis simplex allergens remain active after conventional or microwave heating and pepsin treatments of chilled and frozen L3 larvae , 2009 .

[18]  I. Martinez,et al.  Estimation of frozen storage time or temperature by kinetic modeling of the Kramer shear resistance and water holding capacity (WHC) of hake (Merluccius merluccius, L.) muscle , 2014 .

[19]  Minoru Yamada,et al.  Anisakis simplex sensu stricto and Anisakis pegreffii: biological characteristics and pathogenetic potential in human anisakiasis. , 2012, Foodborne pathogens and disease.

[20]  M. Kennedy,et al.  Anisakis simplex: from Obscure Infectious Worm to Inducer of Immune Hypersensitivity , 2008, Clinical Microbiology Reviews.

[21]  J. W. Bier Experimental Anisakiasis: Cultivation and Temperature Tolerance Determinations1 , 1976 .

[22]  I. Moneo,et al.  New Perspectives on the Diagnosis of Allergy to Anisakis spp. , 2017, Current Allergy and Asthma Reports.

[23]  L. Margolis Public Health Aspects of "Codworm" Infection: A Review , 1977 .

[24]  R. Benítez,et al.  A scanning electron microscopy study of early development in vitro of Contracaecum multipapillatum s.l. (Nematoda: Anisakidae) from a brown pelican (Pelecanus occidentalis) from the Gulf of California, Mexico , 2017, Parasitology Research.

[25]  G. Nascetti,et al.  No more time to stay ‘single’ in the detection of Anisakis pegreffii, A. simplex (s. s.) and hybridization events between them: a multi-marker nuclear genotyping approach , 2016, Parasitology.

[26]  Jun Suzuki,et al.  Risk factors for human Anisakis infection and association between the geographic origins of Scomber japonicus and anisakid nematodes. , 2010, International journal of food microbiology.

[27]  K. Oishi,et al.  Food Hygienic Studies on Anisakis Larva-III , 1972 .

[28]  M. Wekell,et al.  Survival of Anisakis simplex in microwave-processed arrowtooth flounder (Atheresthes stomias). , 1999, Journal of food protection.