Relationship between helminthic infection and IgE response in atopic and nonatopic children in a tropical environment

Abstract

Background: Although IgE antibody is clearly involved in allergic reactions to environmental allergens, this immunoglobulin is an important component of host-protective immune responses against the helminthic parasites that are endemic in the majority of the world population. However, these infections not only stimulate the production of antiparasite IgE antibody but can nonspecifically induce polyclonal IgE synthesis that results in highly elevated total serum IgE levels. Such polyclonal stimulation can diminish specific IgE antibody responses and cause saturation of mast cell Fcϵ receptors, thus inhibiting allergic reactivity. This may represent a mechanism of immune evasion by the parasite. Objective: Because an atopic disposition is generally recognized to be associated with elevated IgE synthesis against environmental allergens, the aim of this study was to evaluate the influence of atopy on the antiparasite response. To this end, we examined two groups of Venezuelan children in whom the intestinal helminth Ascaris lumbricoides is endemic but that differ greatly in their level of atopy. One group was from an island population (Coche Island) that has a very strong atopic background and in which the prevalence of allergic disease is extremely high. The other was a group of nonatopic children belonging to a mainland population (Barrio Los Erasos) that is of comparable socioeconomic level and has an exposure to helminthic infection similar to that of the island group but a relatively low expression of allergic diseases. Results: Although the living conditions and the prevalence of Ascaris infection of the two groups were comparable, the intensity of the parasitic infection was considerably higher in the nonatopic mainland children (geometric mean values of eggs per gram of feces: Barrio Los Erasos, 7621; Coche Island, 1435; p < 0.001). In addition, their total serum IgE levels were significantly more elevated than in the atopic island group (geometric mean: Barrio Los Erasos, 2172; Coche Island, 941 IU/ml; p < 0.001). In contrast, the specific anti- Ascaris response was much stronger in the atopic children (geometric mean: Barrio Los Erasos, 0.30; Coche Island, 0.91 PRU/ml; p < 0.001), which resulted in the ratio of specific to total IgE being nine times higher than in the nonatopic mainland subjects. These differences were maintained even when the children were matched on the basis of infection intensity, thus indicating that the atopic children have an intrinsic propensity to favor specific over polyclonal IgE responses to the parasite. Conclusions: The children with a strong atopic background demonstrated IgE responses concordant with an enhanced protective response against helminthic parasites and had significantly lower intensities of infection than their nonatopic counterparts. These observations support the concept that the atopic state has conferred a selective evolutionary advantage that could compensate for its involvement in allergic disease. (J Allergy Clin Immunol 1998;101:217-21.)