Toxocara Infection Seroprevalence and Its Relationship with Atopic Features in a General Adult Population

Background: The relationship of helminth infection with atopy is controversial. Toxocariasis is the most common helminth infection in industrialized countries. The study aimed to investigate the association between Toxocara exposure and atopic features. Methods: The study is based on a cross-sectional survey of 463 subjects, randomly selected (stratified by decades of age) from a general adult population. Toxocara exposure was defined by the presence of serum Toxocara antibodies. Main outcome measures included total serum IgE levels, skin prick tests (SPT) to a panel of 13 relevant aeroallergens, specific IgE to aeroallergens (Phadiatop test), and respiratory symptoms evaluated by means of a questionnaire. Results: A total of 134 subjects (weighted proportion 28.6%, 95% CI 26.5–30.7%) showed Toxocara exposure. Pet ownership, rural habitat, farming, and low educational level were associated with Toxocara exposure. Toxocara exposure was associated with both positive SPT (particularly to mites) and positive specific IgE (Phadiatop test) after adjusting for potential confounders. The effect of Toxocara exposure on total serum IgE levels and blood eosinophil count was different in SPT-positive subjects and SPT-negative individuals. In SPT-negative individuals, Toxocara exposure was associated with an increase in both serum IgE levels and eosinophil counts, whereas an opposite trend was observed in SPT-positive individuals. Toxocara exposure was not associated with respiratory symptoms. Conclusions: In this adult population, Toxocara exposure is associated with allergic sensitization, particularly to mites. There is evidence of an intriguing interaction between Toxocara exposure and allergic sensitization for both total serum IgE levels and blood eosinophil counts.

[1]  D. Pritchard,et al.  Parasite role reversal: worms on trial. , 2005, Trends in parasitology.

[2]  F. Gudé,et al.  Association of hepatitis A virus infection with allergic sensitization in a population with high prevalence of hepatitis A virus exposure , 2005, Allergy.

[3]  F. Gudé,et al.  Evaluation of the phadiatop test in the diagnosis of allergic sensitization in a general adult population. , 2005, Journal of investigational allergology & clinical immunology.

[4]  D. Vuitton Echinococcosis and allergy , 2004, Clinical reviews in allergy & immunology.

[5]  M. Medeiros,et al.  Low frequency of positive skin tests in asthmatic patients infected with Schistosoma mansoni exposed to high levels of mite allergens , 2004, Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology.

[6]  F. Gudé,et al.  High prevalence of storage mite sensitization in a general adult population , 2004, Allergy.

[7]  R. Van Ree,et al.  Long-term treatment of intestinal helminths increases mite skin-test reactivity in Gabonese schoolchildren. , 2004, The Journal of infectious diseases.

[8]  A. Loukas,et al.  The innate allergenicity of helminth parasites , 2004, Clinical reviews in allergy & immunology.

[9]  R. Maizels,et al.  Regulation of allergy and autoimmunity in helminth infection , 2004, Clinical reviews in allergy & immunology.

[10]  R. Hubbard,et al.  Wheezing, allergy, and parasite infection in children in urban and rural Ethiopia. , 2003, American journal of respiratory and critical care medicine.

[11]  D. Strachan,et al.  Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics. , 2003, The Journal of allergy and clinical immunology.

[12]  D. Despommier,et al.  Toxocariasis: Clinical Aspects, Epidemiology, Medical Ecology, and Molecular Aspects , 2003, Clinical Microbiology Reviews.

[13]  F. Gudé,et al.  Association of alcohol consumption with total serum immunoglobulin E levels and allergic sensitization in an adult population‐based survey , 2003, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[14]  P. Andersen,et al.  An Enteric Helminth Infection Protects Against an Allergic Response to Dietary Antigen1 , 2002, The Journal of Immunology.

[15]  Y. Yeh,et al.  Negative association of Enterobius infestation with asthma and rhinitis in primary school children in Taipei , 2002, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[16]  Maria Yazdanbakhsh,et al.  Allergy, parasites, and the hygiene hypothesis. , 2002, Science.

[17]  A. Woodcock,et al.  Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: a nested case-control study , 2001, The Lancet.

[18]  J. Debruyne,et al.  Toxocara seroprevalence and childhood asthma among Malaysian children , 2001, Pediatrics international : official journal of the Japan Pediatric Society.

[19]  M. van Hage-Hamsten,et al.  Allergenic cross‐reactivity between the nematode Anisakis simplex and the dust mites Acarus siro, Lepidoglyphus destructor, Tyrophagus putrescentiae, and Dermatophagoides pteronyssinus , 2001, Allergy.

[20]  F. Ubeira,et al.  Prevalence of and risk factors for IgE sensitization to Anisakis simplex in a Spanish population , 2001, Allergy.

[21]  J. Zubeldia,et al.  Anisakis simplex-sensitized patients: should fish be excluded from their diet? , 2001, Annals of allergy, asthma & immunology : official publication of the American College of Allergy, Asthma, & Immunology.

[22]  F. Alonso,et al.  Prevalence and viability of eggs of Toxocara spp. and Toxascaris leonina in public parks in eastern Spain , 2001, Journal of Helminthology.

[23]  P. Hotez,et al.  Environmental exposure to Toxocara as a possible risk factor for asthma: a clinic-based case-control study. , 2001, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[24]  L. Glickman,et al.  Highlights of human toxocariasis. , 2001, The Korean journal of parasitology.

[25]  B. Lell,et al.  Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10 , 2000, The Lancet.

[26]  R. Maizels,et al.  Toxocara canis: genes expressed by the arrested infective larval stage of a parasitic nematode. , 2000, International journal for parasitology.

[27]  S. Weiss,et al.  Parasites and asthma/allergy: what is the relationship? , 2000, The Journal of allergy and clinical immunology.

[28]  J. Goldblatt,et al.  Nebulised corticosteroids in the treatment of patients with asthma , 1999, Thorax.

[29]  M. Wjst,et al.  Ascaris-specific IgE and allergic sensitization in a cohort of school children in the former East Germany. , 1998, The Journal of allergy and clinical immunology.

[30]  M. Moustafa,et al.  Toxocariasis as a possible cause of allergic diseases in children. , 1998, Journal of the Egyptian Society of Parasitology.

[31]  P. N. Souëf,et al.  Relationship between helminthic infection and IgE response in atopic and nonatopic children in a tropical environment. , 1998, The Journal of allergy and clinical immunology.

[32]  N. Lynch,et al.  Clinical improvement of asthma after anthelminthic treatment in a tropical situation. , 1997, American journal of respiratory and critical care medicine.

[33]  G. Borsboom,et al.  Relationship between allergic manifestations and Toxocara seropositivity: a cross-sectional study among elementary school children. , 1997, The European respiratory journal.

[34]  B. Valladares,et al.  A serologic study of human toxocariasis in the Canary Islands (Spain): environmental influences. , 1997, The American journal of tropical medicine and hygiene.

[35]  P. Overgaauw Aspects of Toxocara epidemiology: human toxocarosis. , 1997, Critical reviews in microbiology.

[36]  S. Fenoy,et al.  Seroprevalence of toxocariasis in children and adults in Madrid and Tenerife, Spain , 1996, Journal of Helminthology.

[37]  F. Ubeira,et al.  Antigenic cross-reactivity in mice between third-stage larvae of Anisakis simplex and other nematodes , 1996, Parasitology Research.

[38]  H. Savelkoul,et al.  Toxocara-induced eosinophilic inflammation. Airway function and effect of anti-IL-5. , 1995, American journal of respiratory and critical care medicine.

[39]  G. Borsboom,et al.  Toxocara seroprevalence in 5-year-old elementary schoolchildren: relation with allergic asthma. , 1994, American journal of epidemiology.

[40]  B. J. Sutton,et al.  The human IgE network , 1993, Nature.

[41]  N. Lynch,et al.  Allergic reactivity of children of different socioeconomic levels in tropical populations. , 1993, International archives of allergy and immunology.

[42]  Feldman Gj,et al.  Visceral larva migrans associated with the hypereosinophilic syndrome and the onset of severe asthma. , 1992 .

[43]  H. Parker,et al.  Visceral larva migrans associated with the hypereosinophilic syndrome and the onset of severe asthma. , 1992, Annals of internal medicine.

[44]  B. Gottstein,et al.  Immunodiagnosis of toxocarosis in humans: evaluation of a new enzyme-linked immunosorbent assay kit , 1991, Journal of clinical microbiology.

[45]  O. Barriga,et al.  A critical look at the importance, prevalence and control of toxocariasis and the possibilities of immunological control. , 1988, Veterinary parasitology.

[46]  E. Barrett-Connor,et al.  Parasites and asthma--predictive or protective? , 1985, Epidemiologic reviews.

[47]  N. Lynch,et al.  Incidence of atopic disease in a tropical environment: partial independence from intestinal helminthiasis. , 1984, The Journal of allergy and clinical immunology.

[48]  J. Barnwell,et al.  Antibodies to canine helminth parasites in asthmatic and nonasthmatic children. , 1981, International archives of allergy and applied immunology.

[49]  S. Karacadag,et al.  Bronchial asthma associated with intestinal parasites. , 1978, The American journal of gastroenterology.

[50]  D. C. Tullis,et al.  Bronchial asthma associated with intestinal parasites. , 1970, The New England journal of medicine.