Modulation of the allergic reactivity of slum children by helminthic infection

Abstract

Infection by helminthic parasites can cause the polyclonal stimulation of IgE synthesis, possibly via an enhanced production of interleukin-4 (IL-4), and this has been suggested to influence the allergic reactivity of tropical populations where these parasites are endemic. We evaluated a group of urban slum children in Caracas, Venezuela, with a high prevalence of helminthic infection (70.8%), to establish the relationship between the elevated IgE levels (3696 IU/ml) induced by these parasites and various aspects of the allergic response. Although the absolute levels of IL-4 detected in the sera of these children were low (0.65 +/- 0.20 ng/ml), a strong positive correlation (r = 0.78) was found between these and serum IgE. The cutaneous immediate hypersensitivity reactivity to extracts of common environmental allergens was relatively low (17.5% to house dust), although that to Ascaris extract was moderately high (49.4%). Significant inverse correlations were found between total IgE levels and the different skin test reaction diameters, including Ascaris. The positivity of Prausnitz-Kustner passive transfer tests was low in this group (34%), with a strong inverse correlation (r = -0.75) being found between this and total IgE levels. Significant inverse correlations were also found between total IgE levels and specific IgE antibody to environmental allergens, and to Ascaris antigen. We suggest that the polyclonal production of IgE stimulated by helminthic infection can suppress the allergic response to environmental and parasite allergens via both mast cell saturation and inhibition of specific IgE production.

Helminth Infection Protects Mice from Anaphylaxis via IL-10-Producing B Cells

“…Using different anaphylaxis models, it is evident that worm infection does not alter Ag sensitization, but protects the mice from anaphylaxis when they are rechallenged with the allergen. Therefore, resistance of schistosome-infected mice to anaphylaxis was not due to the known propensity of helminth infections to alter responses to vaccination (57) or the stimulation of polyclonal IgE, which can saturate Fc⑀Rs and thereby prevent mast cell degranulation (27). Protection from anaphylaxis is thus primarily mediated when the sensitized mice are rechallenged with the appropriate allergen.…”

“…The reduced susceptibility of worm-infected mice to Pen V-induced anaphylaxis could be due to the infection modifying the production of anti-Pen V Ab or to the known role for helminthinduced, nonspecific, polyclonal IgE-saturating mast cells (27). However, ELISA for Pen V-specific Ab responses of sera from Pen V-OVA-immunized uninfected and worm-infected mice demonstrated that both groups had comparable titers of allergen-specific IgE and IgG1 (data not shown).…”

Asthma and atopy – the price of affluence?

“…Parasitic infections appeared to be the major factor explaining this difference. A protective role by intestinal parasitic (helminth) infection against the development of allergic diseases has been reported by several studies (132)(133)(134)(135)(136), although some authors have reported an opposite result (137,138). The evidence of an inverse relationship between helminths and atopic disease applies mostly to asthma, whereas for e.g.…”

Ascaris reinfection of slum children: relation with the IgE response

“…This concept is based on evidence that polyclonal IgE stimulation can suppress specific IgE responses to individual antigens [12][13][14], and can also inhibit the activity of mast cells via a saturation of their Fee receptors [12][13][14][15][16]. In this respeci, in the present study we found an inverse correlation between total and specific )M\i\-Ascaris IgE, and have previously reported the existence of mast cell saturation in these slum children [13.21], This suppression of allergic reactivity may reduce the pathological consequences of immune reactions against the parasite, or may represent a mechanism of parasite evasion, as has been proposed for IgG4 antibodies thai block anlibody-dcpendenl killing of schistosomula by human eosinophils [5,6], Thus, immunity to helminth infeclion may be a balance beiween ihe stimulation of immunologicai effector functions and the activation of blocking mechanisms.…”

“…For example, the allergic-type reactions mediated by the interaction beiween IgE and mast cells may be important accessory mechanisms in helminih expulsion [8]. and more direct cellular cytoioxicity mechanisms have been described involving IgE and eosinophils [4], Helminthic infection can also cause a non-specific polyclonal stimulalion of IgE synthesis [3.9] thai leads lo highly elevated serum IgE levels in endemic populations [10 12], This polyclonal stimulalion may decrease the capacity lo mount an effective sf)ecific IgE antibody response [9,13.14] and can cause mast cell saturation [13][14][15][16], thus suppressing the allergic response to environmental allergens, and possibly parasite antigens [13,14].…”