Skip to main content
SpringerLink
Log in

Anisakis simplex only provokes allergic symptoms when the worm parasitises the gastrointestinal tract

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

We analysed patients with allergic or digestive symptoms after seafood ingestion in order to assess a correct diet in Anisakis simplex sensitised individuals. A total of 120 patients who suffered allergic and/or digestive symptoms after marine food ingestion were studied. We performed skin prick tests for A. simplex and seafood, total serum and specific serum immunoglobulin E to A. simplex in the acute stage and 1 month later. A gastroscopy was carried out to find larvae in those patients with persistent abdominal pain. A challenge with non-infective larvae was performed to assess a correct diet. Some 96 patients were sensitised to A. simplex. Gastroscopy was performed in 47 and we detected larvae in 24. We compared symptoms, skin tests, total and specific IgE and the latency of appearance of symptoms in patients positive for Anisakis larvae, patients without larvae at gastroscopy and patients without digestive symptoms. There was no difference among the groups. We challenged 22 patients with frozen A. simplex larvae. After allowing deep-frozen seafood in the diet for more than 2 years, no patient suffered a reaction. At this time, we allowed all our patients well-frozen seafood without any allergic reaction occurring. Allergic symptoms are the most frequent manifestation of A. simplex parasitism. We could not find any patient allergic to the thermostable proteins of parasite.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Acebes Rey JM, Fernandez Orcajo P, Díaz Gonzalez G et al. (1996) Dos casos de anisakiasis en el hospital Del Río Hortega. Rev Esp Enferm Dig 88:59–60

    PubMed  Google Scholar 

  • Akao N, Ohyama T, Kondo K (1990) Immunoblot analysis of serum IgG, IgA and IgE responses against larval excretory-secretory antigens of Anisakis simplex in patients with gastric anisakiasis. J Helminthol 64:310–318

    CAS  PubMed  Google Scholar 

  • Alonso A, Daschner A, Moreno-Ancillo A (1997) Anaphylaxis with Anisakis simplex in gastric mucosa. N Engl J Med 337:350–351

    Article  CAS  Google Scholar 

  • Alonso A, Moreno-Ancillo A, Daschner A, MC López Serrano(1999) Dietary assessment in five cases of allergic reactions due to gastro-allergic anisakiasis. Allergy 54:517–520

    Article  CAS  PubMed  Google Scholar 

  • Alonso-Gomez A, Daschner A, Moreno-Ancillo A, Barranco P, Suarez de Parga JM, López Serrano MC (1997) Características clínicas en Anisakiasis Gastroalérgica. Rev Port Inmunoalergol 5: abstract 6

    Google Scholar 

  • Appleby D, Kapoor W, Karpf M et al. (1982) Anisakiasis nematode infestation producing small bowel obstruction. Arch Surg 117:836–840

    CAS  PubMed  Google Scholar 

  • Arenal Vera JJ, Marcos Rodríguez JL, Borrego Pintado MH, Bowakin Dib W, Castro Lorenzo J, Blanco Alvarez JI (1991). Anisakiasis aguda como causa de apendicitis aguda y cuadro reumatológico: primer caso en la literatura médica. Rev Esp Enf Digest 79:355–358

    Google Scholar 

  • Asaishi K, Nishino C, Ebata T, Totsuka M, Hayasaka H, Suzuki T (1980a) Studies on the etiologic mechanism of anisakiasis. 1. Immunological reactions of digestive tract induce by anisakis larvae. Gastroenterol Jpn 15:120–127

    CAS  PubMed  Google Scholar 

  • Asaishi K, Nishino C, Totsuka M, Hayasaka H, Suzuki T (1980b) Studies on the etiologic mechanism of anisakiasis. 2. Epidemiologic study of inhabitants and questionnaire survey in Japan. Gastroenterol Jpn 15:128–134

    CAS  PubMed  Google Scholar 

  • Audicana MT, Fernandez de Corres L, Muñoz D et al. (1995a) Anisakis simplex: una nueva fuente de antigenos “alimentarios”. Estudio de sensibilizacion a otros parasitos del orden ascarididae. Rev Esp Alergol Immunol Clin 10:325–331

    Google Scholar 

  • Audicana MT, Fernandez de Corres L, Muñoz D et al. (1995b) Anisakis simplex a new sea-food allergen. Allergy 50 [Suppl 26]:127

  • Audicana T, et al (1995c) Recurrent anaphylaxis caused by Anisakis simplex parasitizing fish. J Allergy Clin Immunol 96:558–560

    CAS  PubMed  Google Scholar 

  • Bouree P, Paugam A, Petithory JC (1995) Anisakidosis: report of 25 cases and review of the literature. Comp Immunol Microbiol Infect Dis 18:75–84

    Article  CAS  PubMed  Google Scholar 

  • Canut Blasco A, Labora Loriz A, De Torre Ramirez JL, Romeo Ramirez JA(1996) Anisakiasis gastrica aguda causada por insuficiente cocción en microondas. Med Clin 106: 317–318

    Google Scholar 

  • Cheng TC (1978) Parasitología general. Superfamilia Heterocheloidea. Ed, Madrid, pp 6411–6451

  • Cocheton JJ, Cabou I, Lecomte I (1991) Anisakiase et infections par les Anisakidés. Ann Med Interne 142:121–131

    CAS  Google Scholar 

  • Daschner A, Alonso-Gomez A, Mora C, Moreno Ancillo A, Villanueva R, López Serrano MC (1997a) Anisakiasis gastro-alérgica con parasitación masiva. Rev Esp Alergol Inmunol Clin 12: 370–372

    Google Scholar 

  • Daschner A, Alonso-Gomez A, Moreno-Ancillo A, Barranco P, Suarez de Parga JM, López Serrano MC (1997b) Evolución analítica en Anisakiasis Gastroalérgica. Rev Port Inmunoalergol 5: abstract 7

    Google Scholar 

  • Daschner A, Alonso-Gomez A, Caballero T, Barranco P, Suarez de Parga JM, López Serrano MC (1998) Gastric anisakiasis: an under estimated cause of acute urticaria and angioedema. Br J Dermatol 139:822–828

    Article  CAS  PubMed  Google Scholar 

  • Daschner A, Alonso-Gomez A, Caballero T, Suarez de Parga JM, López Serrano MC (1999) Usefulness of early serial measurement of specific and total immunoglobulin E in the diagnosis of gastro-allergic anisakiasis. Clin Exp Allergy 29:1260–1264

    Article  CAS  PubMed  Google Scholar 

  • Daschner A, Alonso-Gomez A, Cabañas R, Suarez de Parga JM, López Serrano MC (2000) Gastro-allergic 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 105:176–181

    CAS  PubMed  Google Scholar 

  • Del Pozo MD, Moneo I, Fernandez de Corres L, Audicana T, Muñoz D, Fernandez E, Navarro JA, García M(1996) Laboratory findings in Anisakis simplex allergy. J Allergy Clin Immunol 97:977–984

    PubMed  Google Scholar 

  • Eugéne C, Penalba C, Gury B, Orbelin P (1983) Les lesions digestivas á éosinophiles. Il. Les formes diffuses ou gastroentérites á éosinophiles. Actual Digest 59:2249–2250

    Google Scholar 

  • Fabresse FX, Essioux H, Meiran M, Larroque P, Celton H (1984) Polyarthrite de l’anisakiase. Premiére cas. Presse Med 13:1004–1008

    CAS  PubMed  Google Scholar 

  • Huang W (1988) Anisakidés et anisakidoses humaines: enquéte sur les anisakidés des poissons commerciaux du marché parisien. Ann Parasitol Hum Comp 63:197–208

    CAS  PubMed  Google Scholar 

  • Huang W, Camus D, Levy D, Bussiepas J (1990) Les anisakidoses humaines: identification d’antigénes parasitaires spécifiques et production d’anticorps monoclonaux. Bull Soc Fr Parasitol 8:1011

    Google Scholar 

  • Iglesias R, Leiro J, Ubeira FM, Santamarina MT, San Martín ML(1993) Anisakis simplex: antigen recognition and antibody production in experimentaly infected mice. Parasite Immunol 15:243–250

    CAS  PubMed  Google Scholar 

  • Ishikura H, Kikuchi K, Nagasawa K, Ooiwa T, Takamiya H, Sato N, Sugane K (1994) Anisakidae and anisakidosis. Prog Clin Parasitol 3:43–101

    Google Scholar 

  • Kakizoe S, Kakizoe H, Kakizoe K, Kakizoe Y, Maruta M, Kakizoe T, Kakizoe S (1995) Endoscopic findings and clinical manifestation of gastric anisakiasis. Am J Gastroenterol 90:761–763

    CAS  PubMed  Google Scholar 

  • Kasuya S, Hamano H, Izumi S (1990) Mackerel induced urticaria and anisakis. Lancet 335:665

    Article  CAS  PubMed  Google Scholar 

  • Kim LS, Lee YH, Kim S, Park HR, Cho SY (1991) A case of anisakiasis causing intestinal obstruction. Kisaengchunghak Chapchi 29:93–96

    Article  PubMed  Google Scholar 

  • Kliks MM (1983) Anisakiasis in the western United States: four new case reports from California. Am J Trop Med Hyg 32:526–532

    CAS  PubMed  Google Scholar 

  • Kuipers FC (1964) Eosinophilic phlegmonous inflamation of the alimentary tract caused by a parasite from the herring. Pathol Microbiol 27:295–301

    Google Scholar 

  • López Serrano MC, Alonso-Gomez A, Daschner A, Moreno-Ancillo A, Suarez de Parga JM, Caballero T, Barranco P, Cabañas R (2000) Gastro-allergic anisakiasis: findings in 22 patients. J Gastroenterol Hepatol 15:503–506

    Article  PubMed  Google Scholar 

  • Lorenzo S, Iglesias J, Leiro F, Ubeira FM, Ansótegui I, García M, Fernández de Corres (2000) Usefulness of currently available methods for the diagnosis of Anisakis simplex allergy. Allergy 55:627–633

    Article  CAS  PubMed  Google Scholar 

  • Lucas SB, Cruse JB, Lewis AAM (1985) Anisakiasis in the United Kingdom. Lancet 1:843–844

    Article  Google Scholar 

  • Matsui K, Lida M, Kimura M, et al (1985) Intestinal anisakiasis: clinical and radiologic features. Radiology 157:299–302

    CAS  PubMed  Google Scholar 

  • Mira Gutiérrez J, García Martos P, Hilario Madrid LM, Rodríguez Iglesias MÁ (1995) Anisakiasis, una parasitosis emergente en nuestro medio. Rev Clin Esp 195:51–54

    Google Scholar 

  • Miyazato I (1980) Studies on the eosinophilic granuloma formation in parasitic infections with special reference to the experimental gastric anisakiasis. Med J Kuiki Univ 5:157–180

    Google Scholar 

  • Moneo I, Caballero ML, Gómez F, Ortega E, Alonso MJ (2000) Isolation and characterization of a major allergen from the fish parasite Anisakis simplex. J Allergy Clin Immunol 106:177–182

    Article  CAS  PubMed  Google Scholar 

  • Moreno-Ancillo A, Caballero MT, Cabañas R, Contreras J, Martín Barroso JA, Barranco P, López Serrano MC (1997) Allergic reactions to Anisakis simplex parasitizing sea food. Ann Allergy Asthma Immunol 79:246–250

    CAS  PubMed  Google Scholar 

  • Muraoka A, Suehiro I, Fujii M et al. (1996) Acute gastric anisakiasis: 28 cases during the last years. Dig Dis Sci 41:2362–2365

    CAS  PubMed  Google Scholar 

  • Mudry J, Lefebvre P, Dei-Cas E et al. (1986) Anisakiae humaine: 5 cas dans le norde de la France. Gastroenterol Clin Biol 10:83–87

    CAS  PubMed  Google Scholar 

  • Orecchia P, Paggi L, Mattiuc S, Di Cave D, Catalini N (1989) Infestazione da larva di As e Anisakis physeteris in spacie ittiche dei mari italiani. Parassitologia 31:37–43

    CAS  PubMed  Google Scholar 

  • Pereira Buena JM (1992) Algunos aspectos de la epidemiología y prevención de la anisakiasis. Revisión de biología del parásito; anisakiasis, diagnóstico, tratamiento, estudio de prevalencia de parasitación de las especies de pescado de consumo en nuestro país y normativa sanitaria. Consejeria de Sanidad y Bienestar Social. Junta de Castilla y León (Government of Castile, Spain), Valladolid, pp 1–56

  • Petithory JC, Lapierre J, Rousseau M, Clique MT (1986) Diagnostic serologique de l’anisakiase (granulome eosinophile digestif par precipitation en milieu gelifie (Ouchterlony, électrosynérése, immunoélectrophorése). Med Mal Infect 3:157–162

    Google Scholar 

  • Pinkus GS, Coodlige C (1975). Intestinal anisakiasis. First case report from North America. Am J Med 59:114–120

    CAS  PubMed  Google Scholar 

  • Sakanari JA, McKerrow JH (1989) Anisakiasis. Clin Microbiol Rev 2:278–284

    CAS  PubMed  Google Scholar 

  • Sanmartín ML, Quintero P, Iglesias et al. (1994) Nematodos parásitos en peces de las costas gallegas. Díaz de Santos, Madrid

  • Sugimachi K, Inokuchi K, Ooiwa T, Fujino T, Ishii Y (1985) Acute gastric anisakiasis. Analysis of 178 cases. JAMA 253:1012–1013

    Article  CAS  PubMed  Google Scholar 

  • Van Thiel PH (1960) Anisakis. Parasitology 53:16

    Google Scholar 

  • Van Thiel PH, Kuipers FC, Roskam RT (1962) A nematode parasitic to herring causing acute abdominal syndromes in man. Trop Geogr Med 2:97–113

    Google Scholar 

  • Williams LW, Bock SA (1999) Skin testing and food challenges in allergy and immunology practice. Clin Rev Allergy Immunol 17: 323–338

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Section of Allergy, Hospital “la Paz”, Madrid, Spain

    Alicia Alonso-Gómez, M. Concepción López-Serrano, M. Teresa Caballero, Pilar Barranco & Rosario Cabañas

  2. Allergy Unit, Hospital Virgen del Puerto, Plasencia (Cáceres), Spain

    Alvaro Moreno-Ancillo

  3. Gastroscopy Unit, Hospital “la Paz”, Madrid, Spain

    Jose M. Suarez-de-Parga

  4. Allergy Section, Hospital de la Princesa, Madrid, Spain

    Alvaro Daschner

Authors
  1. Alicia Alonso-Gómez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alvaro Moreno-Ancillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Concepción López-Serrano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jose M. Suarez-de-Parga
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alvaro Daschner
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Teresa Caballero
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pilar Barranco
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rosario Cabañas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alvaro Moreno-Ancillo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alonso-Gómez, A., Moreno-Ancillo, A., López-Serrano, M.C. et al. Anisakis simplex only provokes allergic symptoms when the worm parasitises the gastrointestinal tract. Parasitol Res 93, 378–384 (2004). https://doi.org/10.1007/s00436-004-1085-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-004-1085-9

Keywords

Search

Navigation