Green areas around homes reduce atopic sensitization in children

Abstract

Background: Western lifestyle is associated with high prevalence of allergy, asthma and other chronic inflammatory disorders. To explain this association, we tested the 'biodiversity hypothesis', which posits that reduced contact of children with environmental biodiversity, including environmental microbiota in natural habitats, has adverse consequences on the assembly of human commensal microbiota and its contribution to immune tolerance.

Methods: We analysed four study cohorts from Finland and Estonia (n = 1044) comprising children and adolescents aged 0.5-20 years. The prevalence of atopic sensitization was assessed by measuring serum IgE specific to inhalant allergens. We calculated the proportion of five land-use types--forest, agricultural land, built areas, wetlands and water bodies--in the landscape around the homes using the CORINE2006 classification.

Results: The cover of forest and agricultural land within 2-5 km from the home was inversely and significantly associated with atopic sensitization. This relationship was observed for children 6 years of age and older. Land-use pattern explained 20% of the variation in the relative abundance of Proteobacteria on the skin of healthy individuals, supporting the hypothesis of a strong environmental effect on the commensal microbiota.

Conclusions: The amount of green environment (forest and agricultural land) around homes was inversely associated with the risk of atopic sensitization in children. The results indicate that early-life exposure to green environments is especially important. The environmental effect may be mediated via the effect of environmental microbiota on the commensal microbiota influencing immunotolerance.

Keywords: Proteobacteria; allergen-specific IgE; biodiversity hypothesis; farming environment; skin microbiota.

Figure 1

Land-use description. (A) PCA biplot of land-use types in the different data sets: DIABIMMUNE Espoo (red) and Tarto (blue), LUKAS (orange), and KARA (green). Increasing the proportion of both forest and agricultural land in the landscape is associated with a decrease in the average prevalence of atopic sensitization (atopy; red contour lines) in the (B) LUKAS and (C) KARA data sets. Open symbols indicate healthy individuals, and black dots represent atopic individuals (cut-off IgE_th = 0.5). Atopy was diagnosed for 6-year-olds in the LUKAS cohort and for 13- to 20-year-olds in the KARA cohort.

Figure 2

Logistic regression of the prevalence of atopic sensitization against the land-use gradient in three data sets representing different age groups. (A) 3-year-olds from DIABIMMUNE Espoo (red) and Tartu (blue). (B) 6-year-olds from the LUKAS data set, with either farmer or nonfarmer children. (C) Children of 6–12 years and 13–20 years of age from the KARA data set. The lines indicate the regression fit for each cohort. The IgE_th for determining atopy was 0.5. Results for other threshold values are given in Supporting Information (Fig. S2).

Figure 3

The spatial scale of land-use description. (A) Variance in land-use types (mean across individuals). (B) Variance in the land-use gradient. (C) Statistical significance of the land-use gradient in explaining the prevalence of atopic sensitization (on log-scale). In addition to the land-use gradient, logistic regression models include residence on a farm (LUKAS data set) or age (KARA data set). The IgE_th for determining atopy is 0.5 in both cases.

Figure 4

Relative abundance of Proteobacteria on the skin of healthy individuals is associated with the land-use gradient. The log₁₀ relative abundance of all Proteobacteria (Alpha, Beta, Gamma, Delta and Epsilon) plotted against the land-use gradient (proportion of forest and agricultural land around homes, Fig.1). The data are from the KARA cohort.