Abstract
Helminth infections and allergies are characterized by a predominant type-2 immune response. In schistosomiasis, the Th-2 response is usually accompanied by induction of immunoregulatory mechanisms that contribute to worm survival and less severe schistosomiasis. Although helminth-induced immunomodulatory mechanisms seem to affect atopy, epidemiological studies on the relationship between helminths and allergy have been inconsistent, and data suggest that the modulatory effects may be influenced by helminth species, chronicity of infection, and parasite burden. Here we performed a cross-sectional study to investigate the effects of Schistosoma mansoni parasite burden and immune response on allergic reactivity of individuals living in a schistosomiasis endemic area in Brazil. Fecal samples from the participants were collected for extensive parasitological examinations by spontaneous sedimentation, Kato-Katz, Helmintex and Saline Gradient tests and molecular detection of S. mansoni by qPCR. Additionally, the concentrations of cytokines and chemokines, total IgE and IgE-reactivity to common house dust allergens were quantified from serum samples. IgE reactivity to dust allergens was detected in 47 individuals (23.8%), and 140 individuals (54.4%) were diagnosed with S. mansoni infection. Most of the infected population (108 individuals) presented very low parasite burden (≤12 eggs/g of feces). The frequency and intensity (p ≤ 0.03) of allergic reactivity were lower in S. mansoni-infected compared with non-infected individuals. Multivariable logistic regression models adjusted by age revealed that allergic reactivity was positively associated with low IL-10 response (OR, 4.55, 95% CI, 0.56–7.36) and high concentration of the inflammatory mediators IL-33 (OR, 2.70, 95% CI, 1.02–7.15) or TNF-α (OR, 6.88, 95% CI, 0.32–143.39) in serum, and inversely associated with S. mansoni infection (OR, 0.38, 95% CI, 0.16–0.87). Most importantly, the logistic regression demonstrated that the modulatory effects of Schistosoma infection depend on parasite burden, with individuals infected with ≤12 eggs/g of feces showing allergic IgE-reactivity similar to non-infected individuals Altogether, our data show that immunomodulation of allergic reactivity depends on S. mansoni burden, low type-2 inflammatory response, and high level of IL-10.
Highlights
Allergies are chronic diseases characterized by an intense and uncontrolled type-2 inflammation, with increased expression of typical cytokines such as interleukin (IL)-4, IL-5, IL9, IL-13, eosinophilia and mast cell activation, elevated reactive immunoglobulin (Ig)E production, and increased mucus production in response to allergen exposition [1,2,3]
To better understand the impact of schistosomiasis infection on the development of allergic diseases in this new context, we evaluated the relationship between S. mansoni infection and the circulating levels of immune mediators and the IgE-reactivity to common household dust allergens in individuals from a rural community of a schistosomiasis endemic area in Brazil
A putative causal relationship between helminth infection and reduction of allergic diseases is mainly supported by data from experimental animal models, while evidence from human studies are still controversial and suggest that aspects such as helminth species, chronicity and site of infection, and parasite burden should be taken into consideration [45, 60, 61]
Summary
Allergies are chronic diseases characterized by an intense and uncontrolled type-2 inflammation, with increased expression of typical cytokines such as interleukin (IL)-4, IL-5, IL9, IL-13, eosinophilia and mast cell activation, elevated reactive immunoglobulin (Ig)E production, and increased mucus production in response to allergen exposition [1,2,3]. The genetic predisposition is, by itself, insufficient to explain the fast and heterogeneous increase of allergies in the human population, suggesting that environmental factors such as air pollution, diet, and exposition to infectious diseases could have an important role in increasing the risk of allergy [17,18,19,20]. Data from experimental models [21,22,23] and epidemiological studies [24,25,26,27] suggest an inverse association between allergies and helminthic infections
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