The presence of serum anti-Ascaris lumbricoides IgE antibodies and of Trichuris trichiura infection are risk factors for wheezing and/or atopy in preschool-aged Brazilian children

Abstract

BackgroundThe elucidation of factors that trigger the development of transient wheezing in early childhood may be an important step toward understanding the pathogenesis of asthma and other allergic diseases later in life. Transient wheezing has been mainly attributed to viral infections, although sensitisation to aeroallergens and food allergens may occur at an early age. In developing countries, intestinal helminthic infections have also been associated with allergy or atopy-related disorders.ObjectiveThe aim of this study was to explore the association of Trichuris trichiura and Ascaris lumbricoides infections with wheezing and atopy in early childhood.Study designA cross-sectional study using a Portuguese-language ISAAC phase I questionnaire, adapted for preschool-aged children, nested in a cohort study of childhood diarrhoea, was conducted on 682 children. Two faecal samples per child were examined for the presence of intestinal helminthic infection. IgE antibodies against three allergenic preparations (Dermatophagoides pteronyssinus, Blomia tropicalis and common child food), as well as against A. lumbricoides antigens, were measured in a sub-sample of these children, whose parents allowed the procedure. Atopy was defined by the presence of levels of serum IgE antibodies ≥0.35 kU/L against at least one of the three tested allergenic preparations.ResultsActive T. trichiura infection but not A. lumbricoides infection was positively associated with wheezing in the total studied children population [adjusted OR = 2.60; CI = 1.54;4.38] and in the atopic children sub-population [adjusted OR = 3.07; CI = 1.00;9.43]. The association with atopy was also positive and statistically significant only in the brute analysis [OR = 2.13; CI = 1.03;4.40]. Anti-A. lumbricoides IgE antibodies, but not current A. lumbricoides infection, were positively associated with wheezing in atopic children [adjusted OR = 2.01; CI = 1.00;4.50] and in non-atopic children [adjusted OR = 3.07; CI = 1.13;8.35] and it was also associated with atopy [adjusted OR = 7.29; CI = 3.90; 13.4]. On the other hands, reports of wheezing were not significantly associated with atopy.ConclusionsThese data corroborate previous studies showing that wheezing is predominantly associated with infection in early childhood and shows that anti-A. lumbricoides IgE antibodies, but not active Ascaris infections, are associated with wheezing and atopy. Additionally, the data demonstrate that T. trichiura infection may play a role in the pathogenesis of atopic wheezing in early childhood.

Determination of Geohelminthiasis and Its Association with Allergic Sensitization among Selected Children in Batangas, Philippines

“…It may also be deduced that those with trichuriasis may indeed, possibly mediate allergy especially with aeroallergens as exhibited by its highest total IgE level among the three types of parasitic infections. This is parallel with the sutdy of Cooper (2004) and Alcântara-Neves et al (2010) which proposed the idea that Trichuris trichiura infection may mediate allergy with inhalants. The data corroborate with prior investigations showing considerable increased serum IgE levels with children irrespective of age (Arbes et al, 2011) and type of allergy (Erwin et al, 2010;Levin, Le Souëf, & Motala, 2008).…”

“…It clearly indicates that many of the children with geohelminthiasis were more prone to be allergic to inhalants than seafood. According to Barreto et al (2006), Fallon and Mangan (2007) and Lee et al (2013), this may suggest that intestinal parasitic infection may play a role in the development of atopy notably, respiratory allergies Alcântara-Neves et al, 2010;Cauyan et al, 2012;Beyers et al, 2006).…”

“…Data regarding the children's demographic profile and allergic diseases were collected from the parent/guardian by employing the International Study of Asthma and Allergies in Childhood Phase I questionnaire as patterned from previous studies of Dubois, Kerkhof, Monchy, Postma, and Schouten (2003), Cauyan et al (2012), Alcântara-Neves, Badaró, Barreto, dos Santos, and Pontes-de-Carvalho (2010) and Amarasekera et al (2012). It was slightly modified with the addition of core questionnaire for food allergy, translated to Filipino and subjected to face validation from their advisers and a panel of experts such as pediatrician, immunologist, linguist and psychologist.…”

Human Ascariasis Increases the Allergic Response and Allergic Symptoms

“…The next link was the finding that both, helminthiases and allergy, were associated with high levels of total IgE, which was further extended to other features of the immune responses to both processes [65][66][67][68]. This has been followed by epidemiological reports that, using several approaches, have shown that ascariasis is a risk factor for asthma [69][70][71][72][73][74][75][76][77]. However, although there is abundant scientific literature supporting the boosting effect of ascariasis on allergic responses [5, 63- (Table 2), a number of questions remain regarding the mechanisms for inducing an increased allergic response and asthma symptoms in a condition naturally accompanied by immunosuppression (reviewed in [99,100]).…”

“…Natural infection is associated with a polarized Th2 cytokine response and high levels of total and anti-Ascaris IgE [5,65,73,[78][79][80][81][82][83][84][85] In some individuals, natural infection induces IgE-mediated allergic respiratory and cutaneous symptoms [63,86,87] In experimental human and animal models, bronchial challenges with Ascaris extract induce asthma symptoms [64,66,67] Experimental ascariasis in animals enhances IgE response to bystander antigens [88][89][90][91] Human ascariasis enhances IgE response to mite species-specific allergens [92, 93•, 94•] Several epidemiological surveys have found that ascariasis is a risk factor for asthma and atopy [69-75, 93•, 94•, 95, 96•] IgE responses to Ascaris allergens is more frequent and stronger in mite-sensitized asthmatic patients [76,81,97,98] could also increase symptoms and severity of this disease. Ascaris components and host genetic background influencing this boosting effect are only beginning to be unraveled, and deserve further investigations.…”