Acta Parasitologica

, Volume 58, Issue 3, pp 399–404 | Cite as

Cross-sectional study of serum reactivity to Anisakis simplex in healthy adults in Niterói, Brazil

  • Israel Figueiredo Junior
  • Mauricio Afonso Vericimo
  • Luciana Ramos Cardoso
  • Sergio Carmona São Clemente
  • Elmiro Rosendo do Nascimento
  • Gerlinde Agate Platais Brasil Teixeira
Original Paper

Abstract

Although the incidence of anisakiasis is rising worldwide, its frequency is still unknown in Brazil. The aim of this study was to verify immunoreactivity to Anisakis simplex antigens in healthy adults and determine its possible relationship with frequency of fish consumption and allergy symptoms. A prospective cross-sectional study was carried out with 67 volunteers recruited from a military facility in Niterói, Brazil. The subjects completed a structured questionnaire and serum titers of specific anti-Anisakis IgE and IgG antibodies were measured. The association between frequency of fish intake and IgE reactivity was evaluated by Fisher’s exact test. Almost all subjects (97.0%, 65/67) that consumed seafood; 64.6% (42/65) ate fish at least once weekly. Of all seafood consumers, 56.9% (37/65) reported allergy symptoms, being gut allergies most often cited (35.5%). IgE seroreactivity to Anisakis simplex was found in 20.9% of subjects (14/67), with 13.4% (9/67) reacting exclusively to somatic antigen, 3.0% (2/67) exclusively to excretory/secretory antigens and 4.5% (3/67) to both antigens. There was a significant association between frequency of fish consumption and positive serology (p = 0.019). An immunoblot assay for Anisakis antigens showed different positive bands for IgG. The direct relationship between ELISA reactivity and frequency of fish intake and absence of association with allergy symptoms suggests previous contact with Anisakis simplex antigens.

Keywords

Anisakis simplex fish excretory/secretory antigen ELISA immunoblotting 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anadon A.M., Rodriguez E., Garate M.T., Cuellar C., Romaris F., Chivato T., Rodero M., Gonzalez-Diaz H., Ubeira F.M. 2010. Diagnosing human anisakiasis: recombinant Ani s 1 and Ani s 7 allergens versus the UniCAP 100 fluorescence enzyme immunoassay. Clinical and Vaccine Immunology, 17, 496–502. DOI: CVI.00443-09 [pii] 10.1128/CVI.00443-09.PubMedCrossRefGoogle Scholar
  2. Anadon A.M., Romaris F., Escalante M., Rodriguez E., Garate T., Cuellar C., Ubeira F.M. 2009. The Anisakis simplex Ani s 7 major allergen as an indicator of true Anisakis infections. Clinical and Experimental Immunology, 156, 471–478. DOI: CEI3919 [pii] 10.1111/j.1365-2249.2009.03919.x.PubMedCrossRefGoogle Scholar
  3. Audicana M.T., Ansotegui I.J., De Corres L.F., Kennedy M.W. 2002. Anisakis simplex: dangerous-dead and alive? Trends Parasitology, 18, 20–25. DOI: S1471492201021523 [pii].CrossRefGoogle Scholar
  4. Audicana M.T., Kennedy M.W. 2008. Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clinical Microbiology Reviews, 21, 360–379. DOI: 21/2/360[pii] 10.1128/CMR.00012-07.PubMedCrossRefGoogle Scholar
  5. Caballero M.L., Moneo I., Gomez-Aguado F., Corcuera M.T., Casado I., Rodriguez-Perez R. 2008. Isolation of Ani s 5, an excretory-secretory and highly heat-resistant allergen useful for the diagnosis of Anisakis larvae sensitization. Parasitology Research, 103, 1231–1233. DOI: 10.1007/s00436-008-1105-2.PubMedCrossRefGoogle Scholar
  6. Ceasa R.J. 2007. Rio de Janeiro tem o maior consumo de pescado do país. P. Secretaria Agricultura, Pesca E Abastecimento. Rio de Janeiro, http://www.ceasa.rj.gov.br/detalhe_noticia.asp?ident=13.Google Scholar
  7. Corres L.F., Del Pozo M.D., Aizpuru F. 2001. Prevalence of Anisakis simplex sensitisation in three Spanish areas, in relation to the fish intake rates. Relevance of Anisakis simplex allergy. Allergologia e Immunologia Clinica, 16, 337–346.Google Scholar
  8. Cruz A.R., Souto P.C.D.S., Ferrari C.K.B., Allegretti S.M., Arrais-Silva W.W. 2010. Endoscopic imaging of the first clinical case of anisakidosis in Brazil. Scientia Parasitologica, 11, 97–100.Google Scholar
  9. Cuellar C., Daschner A., Valls A., De Frutos C., Fernandez-Figares V., Anadon A.M., Rodriguez E., Garate T., Rodero M., Ubeira F.M. 2012. Ani s 1 and Ani s 7 recombinant allergens are able to differentiate distinct Anisakis simplex-associated allergic clinical disorders. Archives of Dermatological Research, DOI: 10.1007/s00403-012-1206-8.Google Scholar
  10. Daschner A., Alonso-Gomez A., Caballero T., Barranco P., Suarez-De-Parga J.M., Lopez-Serrano M.C. 1998. Gastric anisakiasis: an underestimated cause of acute urticaria and angiooedema? British Journal of Dermatology, 139, 822–828.PubMedCrossRefGoogle Scholar
  11. Daschner A., Cuellar C., Rodero M. 2012. The Anisakis allergy debate: does an evolutionary approach help? Trends Parasitology, 28, 9–15. DOI: S1471-4922(11)00179-6[pii]10.1016/j.pt.2011.10.001.CrossRefGoogle Scholar
  12. Daschner A., De Frutos C., Valls A., Vega De La Osada F. 2010. Different clinical presentation of Anisakis simplex associated urticaria is dependent on the frequency of raw fish intake. Allergologia et Immunopathologia (Madr). DOI: S0301-0546(09)00128-1 [pii] 10.1016/j.aller.2009.09.004.Google Scholar
  13. Del Pozo M.D., Moneo I., Corres L.F., Audicana M.T., Munoz D., Fernandez E., Navarro J.A., Garcia M. 1996. Laboratory determinations in Anisakis simplex allergy. Journal of Allergy and Clinical Immunology, 97, 977–984. DOI: S0091674996000917 [pii].PubMedCrossRefGoogle Scholar
  14. Del Rey Moreno A., Valero A., Mayorga C., Gomez B., Torres M.J., Hernandez J., Ortiz M., Lozano Maldonado J. 2006. Sensitization to Anisakis simplex s.l. in a healthy population. Acta Tropica, 97, 265–269. DOI: S0001-706X(05)00358-X[pii]10.1016/j.actatropica.2005.11.007.CrossRefGoogle Scholar
  15. Dias F.J., Sao Clemente S.C., Pinto R.M., Knoff M. 2011. Anisakidae nematodes and Trypanorhyncha cestodes of hygienic importance infecting the king mackerel Scomberomorus cavalla (Osteichthyes: Scombridae) in Brazil. Veterinary Parasitology, 175, 351–355. DOI: S0304-4017(10)00561-3.[pii] 10.1016/j.vetpar.2010.10.014.PubMedCrossRefGoogle Scholar
  16. Fernandez-Caldas E., Quirce S., Maranon F., Diez Gomez M.L., Gijon Botella H., Lopez Roman R. 1998. Allergenic crossreactivity between third stage larvae of Hysterothylacium aduncum and Anisakis simplex. Journal of Allergy and Clinical Immunology, 101, 554–555. DOI: S009167499800116X [pii].PubMedCrossRefGoogle Scholar
  17. Gutiérrez-Galindo J.F., Osanz-Mur A.C., Mora-Ventura M.T. 2010. Occurrence and infection dynamics of anisakid larvae in Scomber scombrus, Trachurus trachurus, Sardina pilchardus, and Engraulis encrasicolus from Tarragona (NE Spain). Food Control, 21, 1550–1555.CrossRefGoogle Scholar
  18. Kim J., Jo J.O., Choi S.H., Cho M.K., Yu H.S., Cha H.J., Ock M. 2011. Seroprevalence of antibodies against Anisakis simplex larvae among health-examined residents in three hospitals of southern parts of Korea. Korean Journal of Parasitology, 49, 139–144. DOI: 10.3347/kjp.2011.49.2.139.PubMedCrossRefGoogle Scholar
  19. Knoff M., São Clemente S.C., Fonseca M.C.G., Andrada C.G., Padovanii R.E.S., Gomes D.C. 2007. Anisakidae parasitos de congro-rosa, Genypterus brasiliensis Regan, 1903 comercializados no estado do Rio de Janeiro, Brasil de interesse na saúde pública. Parasitología Latinoamericana, 62, 127–133.CrossRefGoogle Scholar
  20. Knoff M., São Clemente S.C., Pinto R.M., Gomes D.C. 2001. Nematodes of elasmobranch fishes from the southern coast of Brazil. Memórias do Instituto Oswaldo Cruz, 96, 81–87. DOI: S0074-02762001000100009 [pii].PubMedCrossRefGoogle Scholar
  21. Kobayashi Y., Ohsaki K., Ikeda K., Kakemoto S., Ishizaki S., Shimakura K., Nagashima Y., Shiomi K. 2011. Identification of novel three allergens from Anisakis simplex by chemiluminescent immunoscreening of an expression cDNA library. Parasitology International, 60, 144–150. DOI: S1383-5769(11)00010-9 [pii] 10.1016/j.parint.2011.01.004.PubMedCrossRefGoogle Scholar
  22. Laemmli U. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 277, 680–685.CrossRefGoogle Scholar
  23. Lowry O.H., Rosebrough N.J., Farr A.L., J. R. 1951. Protein Measurement with the Folin Phenol Reagent. Journal of Biological Chemistry, 193, 265–275.PubMedGoogle Scholar
  24. Luque J.L., Cordeiro A.S., Oliva M.E. 2010. Metazoan parasites as biological tags for stock discrimination of whitemouth croaker Micropogonias furnieri. Journal of Fish Biology, 76, 591–600. DOI: 10.1111/j.1095-8649.2009.02515.x.PubMedCrossRefGoogle Scholar
  25. Luque J.L., Poulin R. 2004. Use of fish as intermediate hosts by helminth parasites: A comparative analysis. Acta Parasitologica, 49, 353–361.Google Scholar
  26. Melo O., Ramos R., Di Beneditto A. 2006. Helminths of the marine tucuxi, Sotalia fluviatilis (Gervais, 1853) (Cetacea: Delphinidae), in northern Rio de Janeiro State, Brazil. Brazilian Archives of Biology and Technology, 49. DOI: 10.1590/S1516-89132006000100017.Google Scholar
  27. Moro Moro M., Tejedor Alonso M.A., Esteban Hernandez J., Mugica Garcia 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.PubMedGoogle Scholar
  28. Motta M.R.A., Pinheiro D.C.S.N., Carvalho V.L., Viana D.A., Vicente A.C.P., Iñiguez A.M. 2008. Gastric lesions associated with the presence of Anisakis spp. Dujardin, 1845 (Nematoda: Anisakidae) in Cetaceans stranded on the coast of Ceara, Brazil. Biota Neotropica, 8, 91–95.CrossRefGoogle Scholar
  29. Neto V.A., Amato J.G.D.P., Amato V.S. 2007. Probable recognition of human anisakiasis in Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 49, 261–262.Google Scholar
  30. Park J.S., Cho M.K., Yu H.S., Ahn S.C. 2012. Identification of a 24 kDa excretory secretory protein in Anisakis simplex. Experimental Parasitology, 130, 69–72. DOI: S0014-4894(11)00280-3 [pii] 10.1016/j.exppara.2011.09.008.PubMedCrossRefGoogle Scholar
  31. Pereira A.D., Atui M.B., Torres D.M.A.G., Mangini A.C., Zamboni C.Q. 2000. Incidência de parasitos da família Anisakidae em bacalhau (Gadus morhua) comercializado no estado de São Paulo. Revista do Instituto Adolfo Lutz, 59, 45–49.Google Scholar
  32. Pinkus G.S., Coolidge C., Little M.D. 1975. Intestinal anisakiasis. First case report from North America. American Journal of Medicine, 59, 114–120.Google Scholar
  33. Polimeno L., Loiacono M., Pesetti B., Mallamaci R., Mastrodonato M., Azzarone A., Annoscia E., Gatti F., Amoruso A., Ventura M.T. 2010. Anisakiasis, an underestimated infection: effect on intestinal permeability of Anisakis simplex-sensitized patients. Foodborne Pathogens and Disease, 7, 809–814. DOI: 10.1089/fpd.2009.0484.PubMedCrossRefGoogle Scholar
  34. Puente P., Anadon A.M., Rodero M., Romaris F., Ubeira F.M., Cuellar C. 2008. Anisakis simplex: the high prevalence in Madrid (Spain) and its relation with fish consumption. Experimental Parasitology, 118, 271–274. DOI: S0014-4894(07)00190-7[pii]10.1016/j.exppara.2007.07.002.PubMedCrossRefGoogle Scholar
  35. Silva M.E.R., Eiras J.C. 2003. Occurrence of Anisakis sp. in fishes off the Portuguese West coast and evaluation of its zoonotic potencial. Bulletin European Association of Fish Pathologists, 23, 13–17.Google Scholar
  36. Towbin H., Staehlin T., Gordon G. 1979. Electrophoretic transfer of proteins from polycrylamide gels to nitrocellulose sheets: Procedures and some applications. Proceedings of the National Academy of Sciences, 76, 4330–4335.CrossRefGoogle Scholar
  37. Valls A., Pascual C., Esteban M. 2005. Anisakis allergy: an update. Revue Françise d’Allergologie, 45, 108–113.Google Scholar
  38. Weiler C.R. 2007. Anisakis simplex and cross-reacting antigens. International Journal of Dermatology, 46, 224–225. DOI: IJD3090 [pii] 10.1111/j.1365-4632.2006.03090.x.PubMedGoogle Scholar
  39. Wilson R.J.M. 1966. Yp-Antibodies in Guinea-Pigs Infected with the Cattle Lungworm. Immunology, 11, 199–209.PubMedGoogle Scholar

Copyright information

© Versita Warsaw and Springer-Verlag Wien 2013

Authors and Affiliations

  • Israel Figueiredo Junior
    • 1
  • Mauricio Afonso Vericimo
    • 2
  • Luciana Ramos Cardoso
    • 2
  • Sergio Carmona São Clemente
    • 3
  • Elmiro Rosendo do Nascimento
    • 3
  • Gerlinde Agate Platais Brasil Teixeira
    • 2
  1. 1.Departamento Materno-Infantil, Faculdade de Medicina; Hospital Universitário Antonio PedroUniversidade Federal FluminenseCentro; Niterói, Rio de JaneiroBrasil
  2. 2.Departamento de Imunobiologia, Instituto de BiologiaUniversidade Federal FluminenseNiteróiBrazil
  3. 3.Departamento de Tecnologia de Produtos de Origem Animal, Faculdade de VeterináriaUniversidade Federal FluminenseNiteróiBrazil

Personalised recommendations