ArticlesDecreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10
Introduction
The prevalence of atopic disorders is generally low in developing countries but has increased alarmingly in the industrialised world in the past few decades.1 The concurrent improvement in sanitation and reduction in childhood infections in developed countries had led to the speculation that infections in early childhood may reduce the risk of allergy, the so-called “hygiene hypothesis”.2 This theory gains support from the findings that children frequently exposed to infections in families with an anthroposophic lifestyle have fewer allergies.3 More direct evidence comes from epidemiological studies that show an inverse association between a variety of bacterial (Mycobacterium tuberculosis, Helicobacter pylori), viral (measles, hepatitis A), or protozoan (Toxoplasma gondii) infections and atopy.4, 5, 6 The mechanism proposed for this effect is that such infections would shift the balance of immune responses towards T-helper-1 (Th1), thereby reducing the expression of T-helper-2 (Th2) cytokines generally associated with allergy.7 Indeed, Japanese children with delayed hypersensitivity to tuberculin, a Th-1 type response, were less likely to have atopy.4 However, one important category of infections, which do not fit into the “Th1 shift” concept, needs to be considered. Helminths stimulate potent IgE responses, reflecting a strong Th2 expansion. In helminth-infested hosts, the balance of helper T-cell responses is more skewed towards Th2, when compared with that of European controls.8 Paradoxically, in countries where helminth infections have high prevalences and the immunological balance is shifted towards Th2-type responses, allergic disorders are least prevalent.1 Thus the hygiene hypothesis, which argues that the lower rate of allergies in developing countries is caused by the multiplicity of childhood infections that shift immune responses to Th1, needs to be modified to accommodate helminth infections that are highly prevalent in these countries and, in fact, shift the overall responses towards Th2.
The diminished prevalence of allergic diseases in helminth-infected populations, despite highly raised concentrations of IgE and Th2 cytokines, may be due to certain features of these infections such as raised polyclonal IgE, high concentrations of antigen-specific IgG4, or heightened capacity to produce interleukin-10, an anti-inflammatory cytokine.9, 10, 11
This paper presents the results of an immunoepidemiological study done in Lambaréné, Gabon, aimed at furthering our understanding of the relation between helminth infections and allergy.
Section snippets
Study population
Lambaréné, Gabon, is an area with little urbanisation, high vaccine coverage, and high prevalence of helminth infections. This study presents data from two populations: a large group of 520 schoolchildren aged 5–14 years, and a subsample of 132 of these children selected on the basis of their reactivity to house-dust mite. The children included in the larger survey were attending one of three schools in the area of Lambaréné, whereas children included in the smaller substudy were all from one
Results
The survey showed that the prevalence of skin reactivity to mite, cat, grass, and dog allergens was 11%, 2%, 1%, and less than 0·2%, respectively. Table 1 shows factors that were compared in children with and without atopy as defined by reactivity in skin-prick test. IgE antibodies to mite extract were present in substantial concentrations (>1 IU/mL) in 32% of the studied children and, as expected, higher concentrations of these antibodies were associated with a higher risk of skin reactivity
Discussion
It is clear that high concentrations of IgE are produced to D pteronyssinus antigen in the study population, an observation made in other studies in tropical countries.15 However, we show here that despite this sensitisation, the presence of a chronic tissue helminth infection, urinary schistosomiasis, strongly reduces hypersensitivity to house-dust mite.
Helminths, including schistosomes, stimulate a strong amplification of polyclonal non-specific IgE. Some researchers have argued that the
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