Skip to main content
Log in

Allergic Reactions to Anisakis Found in Fish

  • FOOD ALLERGY (D ATKINS, SECTION EDITOR)
  • Published:
Current Allergy and Asthma Reports Aims and scope Submit manuscript

Abstract

The food-borne parasite Anisakis is an important hidden food allergen. Anisakis is a parasitic nematode which has a third-stage larval form that infects mainly fish, and ingestion of contaminated seafood can result in severe allergic reactions. Symptoms experienced due to exposure to this parasite include gastrointestinal disorders, urticaria, dermatitis, asthma and even anaphylaxis. Accurate prevalence data of allergic sensitisation to Anisakis are difficult to estimate due to the lack of well-designed population-based studies. Current diagnostic approaches rely on the detection of serum IgE antibodies to allergenic proteins, which however demonstrate considerable immunological cross-reactivity to other invertebrate allergens. While exposure to this parasite seems to increase due to the increasing consumption of seafood worldwide, the immunology of infection and allergic sensitization is not fully understood.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Smith JW, Wootten R. Anisakis and anisakiasis. Adv Parasitol. 1978;16:93–163.

    Article  CAS  PubMed  Google Scholar 

  2. Blaxter ML et al. A molecular evolutionary framework for the phylum Nematoda. Nature. 1998;392:71–5.

    Article  CAS  PubMed  Google Scholar 

  3. Nielsen C. Sequences lead to tree of worms. Nature. 1998;392:25–6.

    Article  CAS  PubMed  Google Scholar 

  4. Mattiucci S, Nascetti G. Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite. 2006;13:99–113.

    Article  CAS  PubMed  Google Scholar 

  5. Mattiucci S et al. Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). J Parasitol. 1997;83:401–16.

    Article  CAS  PubMed  Google Scholar 

  6. Paggi L, Mattiucci S, D’Amelio S. Allozyme and PCR-RFLP markers in anisakid nematodes, aethiological agents of human anisakidosis. Parassitologia. 2001;43 Suppl 1:21–7.

    PubMed  Google Scholar 

  7. Jabbar A et al. Molecular characterization of anisakid nematode larvae from 13 species of fish from Western Australia. Int J Food Microbiol. 2013;161:247–53.

    Article  CAS  PubMed  Google Scholar 

  8. Jabbar A et al. Molecular characterization of anisakid nematode larvae from 13 species of fish from Western Australia. Electrophoresis. 2012;33:499–505. Mutation scanning-based analysis of anisakid larvae from Sillago flindersi from Bass Strait, Australia.

    Article  CAS  PubMed  Google Scholar 

  9. D’Amelio S et al. 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. Int J Parasitol. 2000;30:223–6.

    Article  PubMed  Google Scholar 

  10. Mattiucci S et al. Genetic divergence and reproductive isolation between Anisakis brevispiculata and Anisakis physeteris (Nematoda: Anisakidae)s. Int J Parasitol. 2001;31:9–14.

    Article  CAS  PubMed  Google Scholar 

  11. Paggi L, Nascetti G, Orecchia P, Mattiucci S, Bullini L. Biochemical taxonomy of ascaridoid nematodes. Parassitologia. 1985;27:105–12.

    CAS  PubMed  Google Scholar 

  12. Gasser RB et al. Single-strand conformation polymorphism (SSCP) for the analysis of genetic variation. Nat Protoc. 2006;1:3121–8.

    Article  CAS  PubMed  Google Scholar 

  13. Ishikura H et al. Anisakidae and anisakidosis. Prog Clin Parasitol. 1993;3:43–102.

    Article  CAS  PubMed  Google Scholar 

  14. Audicana MT, Ansotegui IJ, de Corres LF, Kennedy MW. Anisakis simplex: dangerous—dead and alive? Trends Parasitol. 2002;18:20–5.

    Article  PubMed  Google Scholar 

  15. Shamsi S et al. Occurrence and abundance of anisakid nematode larvae in five species of fish from southern Australian waters. Parasitol Res. 2011;108:927–34.

    Article  PubMed  Google Scholar 

  16. Baird FJ, Gasser RB, Jabbar A, Lopata AL. Foodborne anisakiasis and allergy. Mol Cell Probes. 2014

  17. Meeusen EN, Balic A. Do eosinophils have a role in the killing of helminth parasites? Parasitol Today. 2000;16:95–101.

    Article  CAS  PubMed  Google Scholar 

  18. Galioto AM et al. Role of eosinophils and neutrophils in innate and adaptive protective immunity to larval strongyloides stercoralis in mice. Infect Immun. 2006;74:5730–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Gomez B et al. Eosinophilic gastroenteritis and Anisakis. Allergy. 1998;53:1148–54.

    Article  CAS  PubMed  Google Scholar 

  20. Nieuwenhuizen NE, Lopata AL. Anisakis—a food-borne parasite that triggers allergic host defences. Int J Parasitol. 2013;43:1047–57. A recent detailed review on the immunological reactions after exposure to Anisakis.

    Article  CAS  PubMed  Google Scholar 

  21. Audicana MT et al. Recurrent anaphylaxis caused by Anisakis simplex parasitizing fish. J Allergy Clin Immunol. 1995;96:558–60.

    Article  CAS  PubMed  Google Scholar 

  22. Del Pozo MD et al. Anisakis simplex, a relevant etiologic factor in acute urticaria. Allergy. 1997;52:576–9.

    Article  PubMed  Google Scholar 

  23. Daschner A, Vega de la Osada F, Pascual CY. Allergy and parasites reevaluated: wide-scale induction of chronic urticaria by the ubiquitous fish-nematode Anisakis simplex in an endemic region. Allergol Immunopathol (Madr). 2005;33:31–7.

    Article  CAS  Google Scholar 

  24. Scala E et al. Occupational generalised urticaria and allergic airborne asthma due to Anisakis simplex. Eur J Dermatol. 2001;11:249–50.

    CAS  PubMed  Google Scholar 

  25. Kirstein F et al. Anisakis pegreffii-induced airway hyperresponsiveness is mediated by gamma interferon in the absence of interleukin-4 receptor alpha responsiveness. Infect Immun. 2010;78:4077–86.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Nieuwenhuizen N, Herbert DR, Brombacher F, Lopata AL. Differential requirements for interleukin (IL)-4 and IL-13 in protein contact dermatitis induced by Anisakis. Allergy. 2009;64:1309–18.

    Article  CAS  PubMed  Google Scholar 

  27. Nieuwenhuizen N et al. Exposure to the fish parasite Anisakis causes allergic airway hyperreactivity and dermatitis. J Allergy Clin Immunol. 2006;117:1098–105. First detailed study to demonstrate sensitization to Anisakis among seafood processing workers and highlights possible sensitisation to Anisakis derived proteins in the absence of infection.

    Article  CAS  PubMed  Google Scholar 

  28. Lopata AL, Jeebhay MF. Airborne seafood allergens as a cause of occupational allergy and asthma. Curr Allergy Asthm R. 2013;13:288–97.

    Article  CAS  Google Scholar 

  29. Caballero ML, Moneo I. Several allergens from Anisakis simplex are highly resistant to heat and pepsin treatments. Parasitol Res. 2004;93:248–51.

    Article  PubMed  Google Scholar 

  30. Carballeda-Sangiao N et al. Identification of autoclave-resistant Anisakis simplex allergens. J Food Prot. 2014;77:605–9.

    Article  CAS  PubMed  Google Scholar 

  31. Daschner A, Alonso-Gómez A, Cabanas R, Suarez-de-Parga JM, López-Serrano MC. Gastroallergic anisakiasis: borderline between food allergy and parasitic disease-clinical and allergologic evaluation of 20 patients with confirmed acute parasitism by Anisakis simplex. J Allergy Clin Immunol. 2000;105:176–81.

    Article  CAS  PubMed  Google Scholar 

  32. Baeza ML, Zubeldia JM, Rubio M. Anisakis simplex allergy. ACI International. 2001;13:242–9.

    Google Scholar 

  33. Carretero Anibarro P et al. Protein contact dermatitis caused by Anisakis simplex. Contact Dermatitis. 1997;37:247.

    Article  CAS  PubMed  Google Scholar 

  34. Montoro A, Perteguer MJ, Chivato T, Laguna R, Cuellar C. Recidivous acute urticaria caused by Anisakis simplex. Allergy. 1997;52:985–91.

    Article  CAS  PubMed  Google Scholar 

  35. Pascual CY et al. Cross-reactivity between IgE-binding proteins from Anisakis, German cockroach, and chironomids. Allergy. 1997;52:514–20.

    Article  CAS  PubMed  Google Scholar 

  36. Gamboa PM et al. Diagnostic utility of components in allergy to Anisakis simplex. J Investig Allergol Clin Immunol. 2012;22:13–9.

    CAS  PubMed  Google Scholar 

  37. Rodriguez-Perez R et al. Cross-reactivity between Anisakis spp. and wasp venom allergens. Int Arch Allergy Immunol. 2014;163:179–84. Provides data on the cross-sensitivity between the allergen Ani s 9 and wasp venom due to cross-reactive carbohydrates.

    Article  CAS  PubMed  Google Scholar 

  38. Garcia F et al. Freezing protects against allergy to Anisakis simplex. J Investig Allergol Clin Immunol. 2001;11:49–52.

    CAS  PubMed  Google Scholar 

  39. Baeza ML et al. Characterization of allergens secreted by Anisakis simplex parasite: clinical relevance in comparison with somatic allergens. Clin Exp Allergy. 2004;34:296–302.

    Article  CAS  PubMed  Google Scholar 

  40. Moneo I et al. Isolation of a heat-resistant allergen from the fish parasite Anisakis simplex. Parasitol Res. 2005;96:285–9.

    Article  PubMed  Google Scholar 

  41. Audicana MT, Kennedy MW. Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clin Microbiol Rev. 2008;21:360–79, table of contents.

  42. Fitzsimmons CM, Falcone FH, Dunne DW. Helminth allergens, parasite-specific IgE, and its protective role in human immunity. Front Immunol. 2014;5:61. This recent review compares dominant IgE-antigens in parasites with clinically important environmental allergens.

    Article  PubMed Central  PubMed  Google Scholar 

  43. Caballero ML et al. Isolation of Ani s 5, an excretory-secretory and highly heat-resistant allergen useful for the diagnosis of Anisakis larvae sensitization. Parasitol Res. 2008;103:1231–3.

    Article  PubMed  Google Scholar 

  44. Chapman MD, Pomes A, Breiteneder H, Ferreira F. Nomenclature and structural biology of allergens. J Allergy Clin Immunol. 2007;119:414–20.

    Article  CAS  PubMed  Google Scholar 

  45. Anadon AM et al. The Anisakis simplex Ani s 7 major allergen as an indicator of true Anisakis infections. Clin Exp Immunol. 2009;156:471–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Moneo I, Caballero ML, Gomez F, Ortega E, Alonso MJ. Isolation and characterization of a major allergen from the fish parasite Anisakis simplex. J Allergy Clin Immunol. 2000;106:177–82.

    Article  CAS  PubMed  Google Scholar 

  47. Shimakura K et al. Purification and molecular cloning of a major allergen from Anisakis simplex. Mol Biochem Parasitol. 2004;135:69–75.

    Article  CAS  PubMed  Google Scholar 

  48. Rodriguez E et al. Novel sequences and epitopes of diagnostic value derived from the Anisakis simplex Ani s 7 major allergen. Allergy. 2008;63:219–25.

    Article  CAS  PubMed  Google Scholar 

  49. Iglesias R, Leiro J, Santamarina MT, Sanmartin ML, Ubeira FM. Monoclonal antibodies against diagnostic Anisakis simplex antigens. Parasitol Res. 1997;83:755–61.

    Article  CAS  PubMed  Google Scholar 

  50. Moneo I et al. Isolation of a heat-resistant allergen from the fish parasite Anisakis simplex. Parasitol Res. 2005;96:285–9.

    Article  PubMed  Google Scholar 

  51. Rodriguez-Mahillo AI et al. Cloning and characterisation of the Anisakis simplex allergen Ani s 4 as a cysteine-protease inhibitor. Int J Parasitol. 2007;37:907–17.

    Article  CAS  PubMed  Google Scholar 

  52. Rodriguez-Perez R, Moneo I, Rodriguez-Mahillo A, Caballero ML. Cloning and expression of Ani s 9, a new Anisakis simplex allergen. Mol Biochem Parasitol. 2008;159:92–7.

    Article  CAS  PubMed  Google Scholar 

  53. Kobayashi Y, Shimakura K, Ishizaki S, Nagashima Y, Shiomi K. Purification and cDNA cloning of a new heat-stable allergen from Anisakis simplex. Mol Biochem Parasitol. 2007;155:138–45.

    Article  CAS  PubMed  Google Scholar 

  54. Asturias JA, Eraso E, Moneo I, Martinez A. Is tropomyosin an allergen in Anisakis? Allergy. 2000;55:898–9.

    Article  CAS  PubMed  Google Scholar 

  55. Guarneri F, Guarneri C, Benvenga S. Cross-reactivity of Anisakis simplex: possible role of Ani s 2 and Ani s 3. Int J Dermatol. 2007;46:146–50.

    CAS  PubMed  Google Scholar 

  56. Lopata AL, Lehrer SB. New insights into seafood allergy. Curr Opin Allergy Clin Immunol. 2009;9:270–7.

    Article  CAS  PubMed  Google Scholar 

  57. Kamath SD, et al. Molecular and immunological approaches in quantifying the air-borne food allergen tropomyosin in crab processing facilities. Int J Hyg Environ Health 2014.

  58. Kamath SD et al. Effect of heat processing on antibody reactivity to allergen variants and fragments of black tiger prawn: a comprehensive allergenomic approach. Mol Nutr Food Res. 2014;58:1144–55.

    Article  CAS  PubMed  Google Scholar 

  59. Kamath SD, Abdel Rahman AM, Komoda T, Lopata AL. Impact of heat processing on the detection of the major shellfish allergen tropomyosin in crustaceans and molluscs using specific monoclonal antibodies. Food Chem. 2013;141:4031–9. Provides detailed data that heating has a profound effect on the detection of the major shellfish allergen tropomyosin, which could have considerable implications for the detection and quantification of other invertebrate tropomyosins in processed food.

    Article  CAS  PubMed  Google Scholar 

  60. Abdel Rahman AM, Lopata AL, Randell EW, Helleur RJ. Absolute quantification method and validation of airborne snow crab allergen tropomyosin using tandem mass spectrometry. Anal Chim Acta. 2010;681:49–55.

    Article  PubMed  Google Scholar 

  61. Moneo I, Caballero ML, Rodriguez-Perez R, Rodriguez-Mahillo AI, Gonzalez-Munoz M. Sensitization to the fish parasite Anisakis simplex: clinical and laboratory aspects. Parasitol Res. 2007;101:1051–5.

    Article  PubMed  Google Scholar 

  62. Nieuwenhuizen NE et al. A cross-reactive monoclonal antibody to nematode haemoglobin enhances protective immune responses to Nippostrongylus brasiliensis. PLoS Negl Trop Dis. 2013;7:e2395.

    Article  PubMed Central  PubMed  Google Scholar 

  63. Feldmeier H, Poggensee G, Poggensee U. The epidemiology, natural history, and diagnosis of human anisakiasis. Eur Microbiol. 1993;2:30–6.

    Google Scholar 

Download references

Acknowledgments

The authors thank the NRF, South Africa, for financial support and the Australian Biological Resource Study (ABRS) to AL. AL is supported by an ARC Future Fellowship.

Compliance with Ethics Guidelines

Conflict of Interest

Dr. Lopata and Dr. Nieuwenhuizen declare that they have nothing to disclose.

Human and Animal Rights and Informed Consent

This article does not contain any studies

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andreas L. Lopata.

Additional information

This article is part of the Topical Collection on Food Allergy.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nieuwenhuizen, N.E., Lopata, A.L. Allergic Reactions to Anisakis Found in Fish. Curr Allergy Asthma Rep 14, 455 (2014). https://doi.org/10.1007/s11882-014-0455-3

Download citation

  • Published:

  • DOI: https://doi.org/10.1007/s11882-014-0455-3

Keywords

Navigation