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Positive associations between infections of Toxoplasma gondii and seropositivity with Anisakis simplex in human patients suffering from chronic urticaria

Published online by Cambridge University Press:  03 July 2014

V. Fernández-Fígares
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad Complutense, Madrid, 28040, Spain
M. Rodero
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad Complutense, Madrid, 28040, Spain
A. Valls
Affiliation:
Servicio de Alergia, Instituto de Investigación Sanitaria, Hospital Universitario de la Princesa, Madrid, 28006, Spain
C. De Frutos
Affiliation:
Servicio de Alergia, Instituto de Investigación Sanitaria, Hospital Universitario de la Princesa, Madrid, 28006, Spain
A. Daschner
Affiliation:
Servicio de Alergia, Instituto de Investigación Sanitaria, Hospital Universitario de la Princesa, Madrid, 28006, Spain
C. Cuéllar*
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad Complutense, Madrid, 28040, Spain
*
*Fax: 34-9-1394-1815 E-mail: cuellarh@ucm.es

Abstract

Toxoplasma gondii is a food-borne and orofecal microorganism which produces chronic infection, and attempts have been made to prove its negative association with atopy in the context of the hygiene hypothesis. Anisakis simplex is a fish parasite associated with chronic urticaria (CU) in endemic regions. We analysed the relationship between both infectious agents in CU. We included 42 patients with chronic urticaria (18 patients with CU associated with A. simplex sensitization and 24 not sensitized CU patients). Patients were assessed for atopy by a skin prick test (SPT) against common aeroallergens and for respiratory symptoms. Anisakis simplex sensitization was assessed by SPT and specific IgE by CAP fluoro-enzyme immunoassay (CAP-FEIA). Anti-T. gondii IgG levels were measured by enzyme-linked immunosorbent assay (ELISA). CU patients were analysed with respect to T. gondii seropositivity, A. simplex sensitization, atopy and immigrant status. The seroprevalence of T. gondii was 40.5% in CU patients and 42.1% in the control group. Immigrants were more frequently infected by T. gondii (41.2% versus 12%; P =0.036). Anti-T. gondii IgG antibodies were associated with past A. simplex parasitism (odds ratio 6.73; P =0.03) and independently with atopic sensitization (odds ratio 5.85; P =0.04). In CU patients, T. gondii has no protective effect on atopic sensitization or A. simplex sensitization.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2014 

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References

Aliberti, J., Serhan, C. & Sher, A. (2002) Parasite-induced lipoxin A4 is an endogenous regulator of IL-12 production and immunopathology in Toxoplasma gondii infection. Journal of Experimental Medicine 196, 12531262.CrossRefGoogle ScholarPubMed
Alonso-Gómez, A., Moreno-Ancillo, A., López-Serrano, M.C., Suarez-de-Parga, J.M., Daschner, A., Caballero, M.T., Barranco, P. & Cabañas, R. (2004) Anisakis simplex only provokes allergic symptoms when the worm parasitises the gastrointestinal tract. Parasitology Research 93, 378384.CrossRefGoogle ScholarPubMed
Bach, J.F. (2002) The effect of infections on susceptibility to autoimmune and allergic diseases. New England Journal of Medicine 347, 911920.CrossRefGoogle ScholarPubMed
Bermudez, L.E., Covaro, G. & Remington, J. (1993) Infection of murine macrophages with Toxoplasma gondii is associated with release of transforming growth factor beta and downregulation of expression of tumor necrosis factor receptors. Infection and Immunity 61, 41264130.CrossRefGoogle ScholarPubMed
Bodner, C., Anderson, W.J., Reid, T.S. & Godden, D.J. (2000) Childhood exposure to infection and risk of adult onset wheeze and atopy. Thorax 55, 383387.CrossRefGoogle ScholarPubMed
Cuéllar, C., Rodero, M. & Daschner, A. (2010) Inhibition of cytokine production in gastro-allergic anisakiasis and Anisakis simplex sensitization-associated chronic urticaria. Parasite Immunology 32, 528.CrossRefGoogle ScholarPubMed
Cuéllar, C., Daschner, A., Valls, A., De Frutos, C., Fernández-Fígares, V., Anadón, A.M., Rodríguez, E., Gárate, 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 304, 283288.CrossRefGoogle Scholar
Daschner, A. & Cuéllar, C. (2010) The hidden sense of symptoms: urticaria can be beneficial. Medical Hypotheses 75, 623626.CrossRefGoogle ScholarPubMed
Daschner, A. & Pascual, C.Y. (2005) Anisakis simplex: sensitization and clinical allergy. Current Opinion in Allergy and Clinical Immunology 5, 281285.CrossRefGoogle ScholarPubMed
Daschner, A., Alonso-Gómez, A., Cabañas, R., Suárez de Parga, J.M. & López-Serrano, M.C. (2000) Gastroallergic anisakiasis: borderline between food allergy and parasitic disease - clinical and allergologic evaluation of 20 patients with confirmed acute parasitism by Anisakis simplex. Journal of Allergy and Clinical Immunology 105, 176181.CrossRefGoogle ScholarPubMed
Daschner, A., Cuéllar, C., Alonso-Gómez, A., Pascual, C.Y. & Martín-Esteban, M. (2001) Serum CD23 is not altered in gastroallergic anisakiasis, but correlates with the production of specific IgE and the amount of polyclonal stimulation. Allergy 56, 10031007.CrossRefGoogle Scholar
Daschner, A., Cuéllar, C. & Valls, A. (2008) Towards a differential definition of atopy: Anisakis simplex and the relationship between parasites and arthropods in respiratory allergy. Parasite Immunology 30, 417424.CrossRefGoogle ScholarPubMed
Daschner, A., Rodero, M., De Frutos, C., Valls, A. & Cuéllar, C. (2010a) Chronic urticaria is associated with a differential helminth-arthropod-related atopy phenotype. Journal of Dermatology 37, 780785.CrossRefGoogle ScholarPubMed
Daschner, A., De Frutos, C., Valls, A. & Vega, F. (2010b) Anisakis simplex sensitization-associated urticaria: short-lived immediate type or prolonged acute urticaria. Archives of Dermatological Research 302, 625629.CrossRefGoogle ScholarPubMed
Daschner, A., Rodero, M., De Frutos, C., Valls, A., Vega, F., Blanco, C. & Cuéllar, C. (2011) Different serum cytokine levels in chronic vs. acute Anisakis simplex sensitization-associated urticaria. Parasite Immunology 33, 357362.CrossRefGoogle ScholarPubMed
Daschner, A., Fernández-Fígares, V., Valls, A., de Frutos, C., Rodero, M., Ubeira, F.M. & Cuéllar, C. (2013) Different fish-eating habits and cytokine production in chronic urticaria with and without sensitization against the fish-parasite Anisakis simplex. Allergology International 62, 191201.CrossRefGoogle ScholarPubMed
Dos Santos, J.C., Azor, M.H., Nojima, V.Y., Lourenço, F.D., Prearo, E., Maruta, C.W., Rivitti, E.A., da Silva Duarte, A. & Sato, M.N. (2008) Increased circulating pro-inflammatory cytokines and imbalanced regulatory T-cell cytokines production in chronic idiopathic urticaria. International Immunopharmacology 8, 14331440.CrossRefGoogle ScholarPubMed
Ellertsen, L.K., Hetland, G. & Lovik, M. (2008) Specific IgE to respiratory allergens and IgG antibodies to Toxoplasma gondii and Streptococcus pneumoniae in Norwegian military recruits. Scandinavian Journal of Immunology 67, 496500.CrossRefGoogle Scholar
Fenoy, I., Giovannoni, M., Batalla, E., Martin, V., Frank, F.M., Piazzon, I. & Goldman, A. (2009) Toxoplasma gondii infection blocks the development of allergic airway inflammation in BALB/c mice. Clinical and Experimental Immunology 155, 275284.CrossRefGoogle ScholarPubMed
Fernandes, J.F., Taketomi, E.A., Mineo, J.R., Miranda, D.O., Alves, R., Resende, R.O., Ynoue, L.H., Sung, S.S. & Silva, D.A. (2010) Antibody and cytokine responses to house dust mite allergens and Toxoplasma gondii antigens in atopic and non-atopic Brazilian subjects. Clinical Immunology 136, 148156.CrossRefGoogle ScholarPubMed
Ferrer, M., Luquin, E., Sanchez-Ibarrola, A., Moreno, C., Sanz, M.L. & Kaplan, A.P. (2002) Secretion of cytokines, histamine and leukotrienes in chronic urticaria. International Archives of Allergy and Immunology 129, 254260.CrossRefGoogle ScholarPubMed
Flegr, J. & Stríž, I. (2011) Potential immunomodulatory effects of latent toxoplasmosis in humans. BMC Infectious Diseases 11, 274.doi: 10.1186/1471-2334-11-274.CrossRefGoogle ScholarPubMed
Grattan, C.E., Francis, D.M., Hide, M. & Greaves, M.W. (1991) Detection of circulating histamine releasing autoantibodies with functional properties of anti-IgE in chronic urticaria. Clinical and Experimental Allergy 21, 695704.CrossRefGoogle ScholarPubMed
Hill, D. & Dubey, J.P. (2002) Toxoplasma gondii: transmission, diagnosis and prevention. Clinical Microbiology and Infection 8, 634640.CrossRefGoogle ScholarPubMed
Janson, C., Asbjornsdottir, H., Birgisdottir, A., Sigurjonsdottir, R.B., Gunnbjörnsdottir, M., Gislason, D., Olafsson, I., Cook, E., Jögi, R., Gislason, T. & Thjodleifsson, B. (2007) The effect of infectious burden on the prevalence of atopy and respiratory allergies in Iceland, Estonia, and Sweden. Journal of Allergy and Clinical Immunology 120, 673679.CrossRefGoogle ScholarPubMed
Jones, J.L., Kruszon-Moran, D., Won, K., Wilson, M. & Schantz, P.M. (2008) Toxoplasma gondii and Toxocara spp. co-infection. American Journal of Tropical Medicine and Hygiene 78, 3539.CrossRefGoogle ScholarPubMed
Linneberg, A., Ostergaard, C., Tvede, M., Andersen, L.P., Nielsen, N.H., Madsen, F., Frølund, L., Dirksen, A. & Jørgensen, T. (2003) IgG antibodies against microorganisms and atopic disease in Danish adults: the Copenhagen Allergy Study. Journal of Allergy and Clinical Immunology 111, 847853.CrossRefGoogle ScholarPubMed
López Serrano, M., Moreno-Ancillo, A., Alonso Gómez, A. & Daschner, A. (2000) Anisakiasis in the year 2000. Revista Española de Enfermedades Digestivas 92, 127131.Google ScholarPubMed
Maizels, R.M. (2005) Infections and allergy – helminths, hygiene and host immune regulation. Current Opinion in Immunology 17, 656661.CrossRefGoogle ScholarPubMed
Matowicka-Karna, J., Dymicka-Piekarska, V. & Kemona, H. (2009) Does Toxoplasma gondii infection affect the levels of IgE and cytokines (IL-5, IL-6, IL-10, IL-12, and TNF-alpha)? Clinical and Developmental Immunology 2009, 374696. doi: 10.1155/2009/374696.CrossRefGoogle ScholarPubMed
Matricardi, P.M., Rosmini, F., Riondino, S., Fortini, M., Ferrigno, L., Rapicetta, M. & Bonini, S. (2000) Exposure to foodborne and orofecal microbes versus airborne viruses in relation to atopy and allergic asthma: epidemiological study. British Medical Journal 320, 412417.CrossRefGoogle ScholarPubMed
Montoya, J.G. & Liesenfeld, O. (2004) Toxoplasmosis. Lancet 363, 19651976.CrossRefGoogle ScholarPubMed
Okada, H., Kuhn, C., Feillet, H. & Bach, J.F. (2010) The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update. Clinical and Experimental Immunology 160, 19.CrossRefGoogle ScholarPubMed
Perona-Wright, G., Mohrs, K., Szaba, F.M., Kummer, L.W., Madan, R., Karp, C.L., Johnson, L.L., Smiley, S.T. & Mohrs, M. (2009) Systemic but not local infections elicit immunosuppressive IL-10 production by natural killer cells. Cell Host and Microbe 6, 503512.CrossRefGoogle Scholar
Ramos, J.M., Milla, A., Rodríguez, J.C., Padilla, S., Masiá, M. & Gutiérrez, F. (2011) Seroprevalence of Toxoplasma gondii infection among immigrant and native pregnant women in Eastern Spain. Parasitology Research 109, 6774.CrossRefGoogle ScholarPubMed
Rook, G.A. (2007) The hygiene hypothesis and the increasing prevalence of chronic inflammatory disorders. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 10721074.CrossRefGoogle ScholarPubMed
Seiskari, T., Kondrashova, A., Viskari, H., Kaila, M., Haapala, A.M., Aittoniemi, J., Virta, M., Hurme, M., Uibo, R., Knip, M. & Hyöty, H. (2007) Allergic sensitization and microbal load - a comparison between Finland and Russian Karelia. Clinical and Experimental Immunology 148, 4752.Google Scholar
Sheikh, A., Smeeth, L. & Hubbard, R. (2003) There is no evidence of an inverse relationship between TH2-mediated atopy and TH1-mediated autoimmune disorders: lack of support for the hygiene hypothesis. Journal of Allergy and Clinical Immunology 111, 131135.CrossRefGoogle ScholarPubMed
Strachan, D.P. (1989) Hay fever, hygiene, and household size. British Medical Journal 299, 12591260.CrossRefGoogle ScholarPubMed
Wagner, A., Förster-Waldl, E., Garner-Spitzer, E., Schabussova, I., Kundi, M., Pollak, A., Scheiner, O., Joachim, A. & Wiedermann, U. (2009) Immunoregulation by Toxoplasma gondii infection prevents allergic immune responses in mice. International Journal for Parasitology 39, 465472.CrossRefGoogle ScholarPubMed
Wedi, B., Wagner, S., Werfel, T., Manns, M.P. & Kapp, A. (1998) Prevalence of Helicobacter pylori-associated gastritis in chronic urticaria. International Archives of Allergy and Immunology 116, 288294.CrossRefGoogle ScholarPubMed
Wedi, B., Raap, U. & Kapp, A. (2004) Chronic urticaria and infections. Current Opinion in Allergy and Clinical Immunology 4, 387396.CrossRefGoogle ScholarPubMed
Yazdanbakhsh, M. & Matricardi, P.M. (2004) Parasites and the hygiene hypothesis: regulating the immune system? Clinical Reviews in Allergy and Immunology 26, 1524.CrossRefGoogle ScholarPubMed
Zuberbier, T., Balke, M., Worm, M., Edenharter, G. & Maurer, M. (2010) Epidemiology of urticaria: a representative cross-sectional population survey. Clinical and Experimental Dermatology 35, 869873.CrossRefGoogle ScholarPubMed