A national retrospective survey of anisakidosis in France (2010-2014): decreasing incidence, female predominance, and emerging allergic potential

Hélène Yera; Émilie Fréalle; Emmanuel Dutoit; Jean Dupouy-Camet

doi:10.1051/parasite/2018016

All issues

Volume 25 (2018)

Parasite, 25 (2018) 23

References

Open Access

Research Article

Issue		Parasite Volume 25, 2018


Article Number		23
Number of page(s)		6
DOI		https://doi.org/10.1051/parasite/2018016
Published online		11 April 2018

AAITO-IFIACI Anisakis Consortium. 2011. Anisakis hypersensitivity in Italy: prevalence and clinical features: a multicenter study. Allergy, 66, 1563-1569. [Google Scholar]
Audicana, MT, Kennedy, MW. 2008. Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clinical Microbiological Review, 21, 360-379. [CrossRef] [PubMed] [Google Scholar]
Bourée, P., Paugam, A., Petithory, J.C. 1995. Anisakidosis: report of 25 cases and review of the literature. Comparative Immunology, Microbiology and Infectious Diseases, 18, 75-84. [CrossRef] [PubMed] [Google Scholar]
Brunet J, Pesson B, Royant M, Lemoine JP, Pfaff AW, Abou-Bacar A, Yera H, Fréalle E, Dupouy-Camet J, Merino-Espinosa G, Gómez-Mateos M, Martin-Sanchez J, Candolfi E. 2017, Molecular diagnosis of Pseudoterranova decipiens s.s in human, France. BMC Infectious Diseases, 6, 397. [Google Scholar]
Chen W, Mempel M, Schober W, Behrendt H, Ring J. 2008. Gender difference, sex hormones, and immediate type hypersensitivity reactions. Allergy, 63, 1418-1427. [CrossRef] [PubMed] [Google Scholar]
Daschner A, Pascual CY. 2005. Anisakis simplex: sensitization and clinical allergy. Current Opinion in Allergy and Clinical Immunology, 5, 281-285. [CrossRef] [PubMed] [Google Scholar]
De Silva D, Yamao M. 2006. A yen for sushi: an analysis of demographic and behavioral patterns of sushi consumption in Japan. Journal of Foodservice, 17, 63-76. [CrossRef] [Google Scholar]
Dupouy-Camet J, Gay M, Bourgau O, Nouchi A, Léger E, Dei-Cas E. 2014. L’atteinte œsophagienne : une complication rare de l’anisakidose à Pseudoterranova. Presse Médicale, 43, 81-83. [CrossRef] [Google Scholar]
Dupouy-Camet J, Touabet-Azouzi N, Fréalle E, Van Cauteren D, Yera H, Moneret-Vautrin A. Incidence de l’anisakidose en France. Enquête rétrospective 2010-2014. 2016. Bulletin Epidémiologique Hebdomadaire, 5-6. 64-70. Retrieved 8 January 2018 from http://www.invs.sante.fr/beh/2016/5-6/2016_5-6_1.html [Google Scholar]
Eldin de Pécoulas P, Paugam A., Bourée P. 2014. Anisakiose et allergie : une association morbide négligée ? Revue Francophone des Laboratoires, 464, 89-95. [CrossRef] [Google Scholar]
European Food Safety Authority. 2010. Scientific opinion on risk assessment of parasites in fishery products. EFSA panel on biologic hazards (BIOHAZ). EFSA Journal, 8, 1543. [Google Scholar]
Falcão H, Lunet N, Neves E, Iglésias I, Barros H. 2008. Anisakis simplex as a risk factor for relapsing acute urticaria: a case-control study. Journal of Epidemiology and Community Health, 62, 634-637. [CrossRef] [PubMed] [Google Scholar]
FranceAgriMer, 2015. Consommation des produits de la pêche et de l’aquaculture, 2014. pp.28 Retrieved 8th of January 2018 from http://www.franceagrimer.fr/content/download/38313/352902/file/STA-MER-CONSO%202014-mai2015.pdf [Google Scholar]
INVS. 2004. Morbidité et mortalité dues aux maladies infectieuses d’origine alimentaire en France Institut de Veille Sanitaire St Maurice, France Retrieved 8^th of January 2018 from http://invs.santepubliquefrance.fr/publications/2004/inf_origine_alimentaire/inf_origine_alimentaire.pdf. [Google Scholar]
Hochberg NS, Hamer DH, 2010. Anisakidosis: Perils of the deep. Clinical Infectious Diseases, 51, 806-812 [CrossRef] [Google Scholar]
Hubert B, Bacou J, Belveze H. 1989. Epidemiology of human anisakiasis: incidence and sources in France. American Journal of Tropical Medicine and Hygiene, 40, 301-303. [CrossRef] [Google Scholar]
Lunestad BT. 2003. Absence of nematodes in farmed Atlantic salmon (Salmo salar L.) in Norway. Journal of Food Protection. 66, 122-124. [CrossRef] [PubMed] [Google Scholar]
Martínez-Aranguren RM, Gamboa PM, García-Lirio E, Asturias J, Goikoetxea MJ, Sanz ML, 2014. In vivo and in vitro testing with rAni s 1 can facilitate diagnosis of Anisakis simplex allergy. Journal of Investigational Allergology and Clinical Immunology, 24, 431-438. [Google Scholar]
Mattiucci S & D’Amelio S. 2014. Anisakiasis, in Helminth Infections and their Impact on Global Public Health, Bruschi F, Editor. Springer-Verlag: Wien. P., 325-365. [Google Scholar]
Mattiucci S, Colantoni A, Crisafi B, Mori-Ubaldini F, Caponi L, Fazii P, Nascetti G, Bruschi F. 2017. IgE sensitization to Anisakis pegreffii in Italy: Comparison of two methods for the diagnosis of allergic anisakiasis. Parasite Immunology, 39 (7). DOI: 10.1111/pim.12440. [Google Scholar]
Moro Moro, M., Tejedor Alonso, M.A., Esteban Hernández, J, Múgica García M.V., Rosado Ingelmo, A., Vila Albelda, C., 2011. Incidence of anaphylaxis and subtypes of anaphylaxis in a general hospital emergency department. Journal of Investigational Allergology and Clinical Immunology, 21, 142-149. [Google Scholar]
Petithory JC. 2007. Données nouvelles sur l’anisakidose. Bulletin de l’Académie Nationale de Médecine (Paris), 191, 53-65. [Google Scholar]
Petithory JC. 2008. Actualités sur l’anisakidose. Revue Française des Laboratoires, 399, 87-93. [CrossRef] [Google Scholar]
Pozio E. 2013. Integrating animal health surveillance and food safety: the example of Anisakis. Scientific and Technical Review of the Office International des Epizooties (Paris), 32, 487-496. [CrossRef] [Google Scholar]
Pravettoni V, Primavesi L, Piantanida M. 2012. Anisakis simplex: current knowledge. European Annals of Allergy and Clinical Immunology, 44, 150-156. [PubMed] [Google Scholar]
Seesao Y. 2015. Caractérisation des Anisakidae dans les poissons marins : développement d’une méthode d’identification par séquençage à haut-débit et étude de prévalence. Thèse de doctorat en Biologie. Université Lille 2. [Google Scholar]
Setyobudi E, Jeon CH, Lee CH, Seong KB, Kim JH. 2011. Occurrence and identification of Anisakis spp. (Nematoda: Anisakidae) isolated from chum salmon (Oncorhynchus keta) in Korea. Parasitology Research. 108, 585-592. [CrossRef] [PubMed] [Google Scholar]
Shiferaw B, Verrill L, Booth H, Zansky SM, Norton DM, Crim S, Henao OL. 2012. Sex-based differences in food consumption: Foodborne Diseases Active Surveillance Network (FoodNet) Population Survey, 2006-2007. Clinical Infectious Disease, 54 Suppl 5, S453-S457. [CrossRef] [Google Scholar]
Sohn WM, Na BK, Kim TH, Park TJ. 2015. Anisakiasis: Report of 15 gastric cases caused by Anisakis Type I larvae and a brief review of Korean anisakiasis cases. Korean Journal of Parasitology, 53, 465-470. [CrossRef] [Google Scholar]
Ventura MT, Tummolo RA, Di Leo E, D’Ersasmo M, Arsieni A. 2008. Immediate and cell-mediated reactions in parasitic infections by Anisakis simplex. Journal of Investigational Allergology and Clinical Immunology 18(4), 253-259. [Google Scholar]
Verrez-Bagnis V, Seesao Y, Thebault A, Gay M, Aliouat-Denis CM, Le Fur B, Cuzzucoli D, Cos I, Jérôme, M, Kolypczuk L, Bruzac S, Audebert C, Dei-Cas E, Viscogliosi E. and the “Fish-Parasites” consortium. 2015. Prevalence of nematodes (Anisakidae) in fish species most consumed in France. Abstract book of the 5th Trans-Atlantic Fisheries Technology conference, Nantes, France. Retrieved 8 January 2018 from http://wwz.ifremer.fr/taft2015/content/download/90381/1110052/file/book%20of%20abstracts%20final.pdf [Google Scholar]
Vidacek S, de las Heras C, Solas MT, Mendizábal A, Rodriguez-Mahillo AI, Tejada M. 2010. Antigenicity and viability of Anisakis larvae infesting hake heated at different time-temperature conditions. Journal of Food Protection, 73, 62-68. [Google Scholar]
Yera H, Estran C, Delaunay P, Gari-Toussaint M, Dupouy-Camet J, Marty P. 2006. Putative Diphyllobothrium nihonkaiense acquired from a Pacific salmon (Oncorhynchus keta) eaten in France; genomic identification and case report. Parasitology International. 55, 45-49. [Google Scholar]
Yera H, Fréalle E, Dupouy-Camet J. 2016. Molecular confirmation of Anisakis pegreffii as a causative agent of anisakidosis in France. Digestive and Liver Disease, 48, 970. [Google Scholar]

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[1] AAITO-IFIACI Anisakis Consortium. 2011. Anisakis hypersensitivity in Italy: prevalence and clinical features: a multicenter study. Allergy, 66, 1563-1569. [Google Scholar]

[2] Audicana, MT, Kennedy, MW. 2008. Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clinical Microbiological Review, 21, 360-379. [CrossRef] [PubMed] [Google Scholar]

[3] Bourée, P., Paugam, A., Petithory, J.C. 1995. Anisakidosis: report of 25 cases and review of the literature. Comparative Immunology, Microbiology and Infectious Diseases, 18, 75-84. [CrossRef] [PubMed] [Google Scholar]

[4] Brunet J, Pesson B, Royant M, Lemoine JP, Pfaff AW, Abou-Bacar A, Yera H, Fréalle E, Dupouy-Camet J, Merino-Espinosa G, Gómez-Mateos M, Martin-Sanchez J, Candolfi E. 2017, Molecular diagnosis of Pseudoterranova decipiens s.s in human, France. BMC Infectious Diseases, 6, 397. [Google Scholar]

[5] Chen W, Mempel M, Schober W, Behrendt H, Ring J. 2008. Gender difference, sex hormones, and immediate type hypersensitivity reactions. Allergy, 63, 1418-1427. [CrossRef] [PubMed] [Google Scholar]

[6] Daschner A, Pascual CY. 2005. Anisakis simplex: sensitization and clinical allergy. Current Opinion in Allergy and Clinical Immunology, 5, 281-285. [CrossRef] [PubMed] [Google Scholar]

[7] De Silva D, Yamao M. 2006. A yen for sushi: an analysis of demographic and behavioral patterns of sushi consumption in Japan. Journal of Foodservice, 17, 63-76. [CrossRef] [Google Scholar]

[8] Dupouy-Camet J, Gay M, Bourgau O, Nouchi A, Léger E, Dei-Cas E. 2014. L’atteinte œsophagienne : une complication rare de l’anisakidose à Pseudoterranova. Presse Médicale, 43, 81-83. [CrossRef] [Google Scholar]

[9] Dupouy-Camet J, Touabet-Azouzi N, Fréalle E, Van Cauteren D, Yera H, Moneret-Vautrin A. Incidence de l’anisakidose en France. Enquête rétrospective 2010-2014. 2016. Bulletin Epidémiologique Hebdomadaire, 5-6. 64-70. Retrieved 8 January 2018 from http://www.invs.sante.fr/beh/2016/5-6/2016_5-6_1.html [Google Scholar]

[10] Eldin de Pécoulas P, Paugam A., Bourée P. 2014. Anisakiose et allergie : une association morbide négligée ? Revue Francophone des Laboratoires, 464, 89-95. [CrossRef] [Google Scholar]

[11] European Food Safety Authority. 2010. Scientific opinion on risk assessment of parasites in fishery products. EFSA panel on biologic hazards (BIOHAZ). EFSA Journal, 8, 1543. [Google Scholar]

[12] Falcão H, Lunet N, Neves E, Iglésias I, Barros H. 2008. Anisakis simplex as a risk factor for relapsing acute urticaria: a case-control study. Journal of Epidemiology and Community Health, 62, 634-637. [CrossRef] [PubMed] [Google Scholar]

[13] FranceAgriMer, 2015. Consommation des produits de la pêche et de l’aquaculture, 2014. pp.28 Retrieved 8th of January 2018 from http://www.franceagrimer.fr/content/download/38313/352902/file/STA-MER-CONSO%202014-mai2015.pdf [Google Scholar]

[14] INVS. 2004. Morbidité et mortalité dues aux maladies infectieuses d’origine alimentaire en France Institut de Veille Sanitaire St Maurice, France Retrieved 8^th of January 2018 from http://invs.santepubliquefrance.fr/publications/2004/inf_origine_alimentaire/inf_origine_alimentaire.pdf. [Google Scholar]

[15] Hochberg NS, Hamer DH, 2010. Anisakidosis: Perils of the deep. Clinical Infectious Diseases, 51, 806-812 [CrossRef] [Google Scholar]

[16] Hubert B, Bacou J, Belveze H. 1989. Epidemiology of human anisakiasis: incidence and sources in France. American Journal of Tropical Medicine and Hygiene, 40, 301-303. [CrossRef] [Google Scholar]

[17] Lunestad BT. 2003. Absence of nematodes in farmed Atlantic salmon (Salmo salar L.) in Norway. Journal of Food Protection. 66, 122-124. [CrossRef] [PubMed] [Google Scholar]

[18] Martínez-Aranguren RM, Gamboa PM, García-Lirio E, Asturias J, Goikoetxea MJ, Sanz ML, 2014. In vivo and in vitro testing with rAni s 1 can facilitate diagnosis of Anisakis simplex allergy. Journal of Investigational Allergology and Clinical Immunology, 24, 431-438. [Google Scholar]

[19] Mattiucci S & D’Amelio S. 2014. Anisakiasis, in Helminth Infections and their Impact on Global Public Health, Bruschi F, Editor. Springer-Verlag: Wien. P., 325-365. [Google Scholar]

[20] Mattiucci S, Colantoni A, Crisafi B, Mori-Ubaldini F, Caponi L, Fazii P, Nascetti G, Bruschi F. 2017. IgE sensitization to Anisakis pegreffii in Italy: Comparison of two methods for the diagnosis of allergic anisakiasis. Parasite Immunology, 39 (7). DOI: 10.1111/pim.12440. [Google Scholar]

[21] Moro Moro, M., Tejedor Alonso, M.A., Esteban Hernández, J, Múgica García M.V., Rosado Ingelmo, A., Vila Albelda, C., 2011. Incidence of anaphylaxis and subtypes of anaphylaxis in a general hospital emergency department. Journal of Investigational Allergology and Clinical Immunology, 21, 142-149. [Google Scholar]

[22] Petithory JC. 2007. Données nouvelles sur l’anisakidose. Bulletin de l’Académie Nationale de Médecine (Paris), 191, 53-65. [Google Scholar]

[23] Petithory JC. 2008. Actualités sur l’anisakidose. Revue Française des Laboratoires, 399, 87-93. [CrossRef] [Google Scholar]

[24] Pozio E. 2013. Integrating animal health surveillance and food safety: the example of Anisakis. Scientific and Technical Review of the Office International des Epizooties (Paris), 32, 487-496. [CrossRef] [Google Scholar]

[25] Pravettoni V, Primavesi L, Piantanida M. 2012. Anisakis simplex: current knowledge. European Annals of Allergy and Clinical Immunology, 44, 150-156. [PubMed] [Google Scholar]

[26] Seesao Y. 2015. Caractérisation des Anisakidae dans les poissons marins : développement d’une méthode d’identification par séquençage à haut-débit et étude de prévalence. Thèse de doctorat en Biologie. Université Lille 2. [Google Scholar]

[27] Setyobudi E, Jeon CH, Lee CH, Seong KB, Kim JH. 2011. Occurrence and identification of Anisakis spp. (Nematoda: Anisakidae) isolated from chum salmon (Oncorhynchus keta) in Korea. Parasitology Research. 108, 585-592. [CrossRef] [PubMed] [Google Scholar]

[28] Shiferaw B, Verrill L, Booth H, Zansky SM, Norton DM, Crim S, Henao OL. 2012. Sex-based differences in food consumption: Foodborne Diseases Active Surveillance Network (FoodNet) Population Survey, 2006-2007. Clinical Infectious Disease, 54 Suppl 5, S453-S457. [CrossRef] [Google Scholar]

[29] Sohn WM, Na BK, Kim TH, Park TJ. 2015. Anisakiasis: Report of 15 gastric cases caused by Anisakis Type I larvae and a brief review of Korean anisakiasis cases. Korean Journal of Parasitology, 53, 465-470. [CrossRef] [Google Scholar]

[30] Ventura MT, Tummolo RA, Di Leo E, D’Ersasmo M, Arsieni A. 2008. Immediate and cell-mediated reactions in parasitic infections by Anisakis simplex. Journal of Investigational Allergology and Clinical Immunology 18(4), 253-259. [Google Scholar]

[31] Verrez-Bagnis V, Seesao Y, Thebault A, Gay M, Aliouat-Denis CM, Le Fur B, Cuzzucoli D, Cos I, Jérôme, M, Kolypczuk L, Bruzac S, Audebert C, Dei-Cas E, Viscogliosi E. and the “Fish-Parasites” consortium. 2015. Prevalence of nematodes (Anisakidae) in fish species most consumed in France. Abstract book of the 5th Trans-Atlantic Fisheries Technology conference, Nantes, France. Retrieved 8 January 2018 from http://wwz.ifremer.fr/taft2015/content/download/90381/1110052/file/book%20of%20abstracts%20final.pdf [Google Scholar]

[32] Vidacek S, de las Heras C, Solas MT, Mendizábal A, Rodriguez-Mahillo AI, Tejada M. 2010. Antigenicity and viability of Anisakis larvae infesting hake heated at different time-temperature conditions. Journal of Food Protection, 73, 62-68. [Google Scholar]

[33] Yera H, Estran C, Delaunay P, Gari-Toussaint M, Dupouy-Camet J, Marty P. 2006. Putative Diphyllobothrium nihonkaiense acquired from a Pacific salmon (Oncorhynchus keta) eaten in France; genomic identification and case report. Parasitology International. 55, 45-49. [Google Scholar]

[34] Yera H, Fréalle E, Dupouy-Camet J. 2016. Molecular confirmation of Anisakis pegreffii as a causative agent of anisakidosis in France. Digestive and Liver Disease, 48, 970. [Google Scholar]