Schistosomiasis-induced IL-10 suppresses allergy prevalence.

Abstract

Allergy and other atopic disorders occur significantly less often in developing countries than in industrialized nations. In the latter, prevalence of atopy has increased dramatically over recent decades, concurrent with a reduction in childhood diseases that is associated with improved sanitation. This has led to speculation that infections in early childhood could reduce the risk of allergy, the so-called ‘hygiene hypothesis’. This theory has gained support from epidemiological studies that show an inverse association between several different bacterial or protozoan infections and atopy. The mechanism proposed for this effect is that infection with an intracellular microorganism causes a shift in the balance of immune responsiveness towards T-helper (Th) 1 polarization, thereby reducing the expression of Th2 cytokines that are linked with allergy. There is, however, one category of infections which does not fit this ‘Th1 shift’ concept. Helminth infections are well known to stimulate strong Th2 responses, notably polyclonal non-specific immunoglobulin (Ig) E. Moreover, helminth-infested individuals from the developing world exhibit a Th subset balance that is far more skewed towards Th2 than that of European uninfected controls. Paradoxically, atopic disorders are least prevalent in countries where the incidence of helminthiases is high. How can this be reconciled?van den Biggelaar et al. 1xDecreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. van den Biggelaar, A.H.J et al. Lancet. 2000; 356: 1723–1727Abstract | Full Text | Full Text PDF | PubMed | Scopus (495)See all References have now provided an attractive explanation for the reduced prevalence of allergic diseases among helminth-infected populations in the face of elevated levels of Th2 cytokines and IgE. They investigated the influence of chronic Schistosoma haematobium infection on the prevalence of atopy in Gabonese children. Each child was tested for skin reactivity to house dust-mite and other allergens, for S. haematobium eggs in urine and for microfilariae in blood samples. Total and mite-specific IgE were also measured. Children with urinary schistosomiasis had a significantly lower prevalence of house dust-mite sensitization than those free of infection, but the degree of reactivity to the allergen could not explain the difference in skin-test positivity. Infection was correlated with raised concentrations of each of the Th2-type cytokines interleukin-5 (IL-5), IL-10 and IL-13 in response to adult worm antigen, but, importantly, only parasite-induced IL-10 was associated with a low risk of skin reactivity to allergens. Furthermore, the effect on skin-test reaction of IgE clearly appeared to be suppressed by the parasite-induced IL-10. The conclusion that IL-10 might play a role in counteracting inflammation-mediated allergic diseases is consistent with the observation that production of this anti-inflammatory cytokine by mononuclear cells is diminished in asthma sufferers but raised in patients undergoing immunotherapy.The work of van den Biggelaar et al. 1xDecreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. van den Biggelaar, A.H.J et al. Lancet. 2000; 356: 1723–1727Abstract | Full Text | Full Text PDF | PubMed | Scopus (495)See all References indicates that the complexity of the relationship between infectious diseases and atopy is such that any immunological rationalization based solely on the Th1/Th2 paradigm might be too simplistic and also that the role of individual cytokines should be considered. The link between helminth-induced IL-10 production in children with suppression of responsiveness in vivo to allergens to which they are sensitized adds weight to the argument that IL-10 could be used in the therapeutic control of allergy.