Abstract
In animal experimental models, parasitic helminth infections can protect the host from auto-immune diseases. We conducted a population-scale human study investigating the relationship between helminth parasitism and auto-reactive antibodies and the subsequent effect of anti-helminthic treatment on this relationship. Levels of antinuclear antibodies (ANA) and plasma IL-10 were measured by enzyme linked immunosorbent assay in 613 Zimbabweans (aged 2–86 years) naturally exposed to the blood fluke Schistosoma haematobium. ANA levels were related to schistosome infection intensity and systemic IL-10 levels. All participants were offered treatment with the anti-helminthic drug praziquantel and 102 treated schoolchildren (5–16 years) were followed up 6 months post-antihelminthic treatment. ANA levels were inversely associated with current infection intensity but were independent of host age, sex and HIV status. Furthermore, after allowing for the confounding effects of schistosome infection intensity, ANA levels were inversely associated with systemic levels of IL-10. ANA levels increased significantly 6 months after anti-helminthic treatment. Our study shows that ANA levels are attenuated in helminth-infected humans and that anti-helminthic treatment of helminth-infected people can significantly increase ANA levels. The implications of these findings are relevant for understanding both the aetiology of immune disorders mediated by auto-reactive antibodies and in predicting the long-term consequences of large-scale schistosomiasis control programs.
Highlights
Three billion people are estimated to be infected with helminths in tropical and subtropical regions
Our results showed that anti-nuclear antibodies (ANA) levels were significantly lower in a population exposed to higher levels of S. haematobium infection compared to a population exposed to lower levels
None of the participants in this study were positive for malaria infection; ANA levels in these populations cannot be attributed to malaria infection as has been reported in other settings [40]
Summary
Three billion people are estimated to be infected with helminths in tropical and subtropical regions. Several epidemiological studies have shown an inverse association in the prevalence of helminth infections and allergy as well as reduced allergic reactivity in individuals infected with helminth infections [1,2,3,4]. Auto-immune diseases cause significant and chronic morbidity and disability [10]. Their epidemiology and aetiology remain poorly understood [10,11], but experimental studies in mice suggest that infections with parasitic helminths such as Schistosoma mansoni can protect against auto-immune diseases including experimental auto-immune encephalomyelitis, the experimental model of multiple sclerosis [12], Graves hyperthyroidism [13], type 1 diabetes and experimental colitis [14,15,16]
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