Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity

Abstract

Background: Multiple studies have demonstrated that early-life exposure to pets or siblings affords protection against allergic disease; these associations are commonly attributed to the "hygiene hypothesis". Recently, low diversity of the infant gut microbiota has also been linked to allergic disease. In this study, we characterize the infant gut microbiota in relation to pets and siblings.

Methods: The study population comprised a small sub-sample of 24 healthy, full term infants from the Canadian Healthy Infant Longitudinal Development (CHILD) birth cohort. Mothers reported on household pets and siblings. Fecal samples were collected at 4 months of age, and microbiota composition was characterized by high-throughput signature gene sequencing.

Results: Microbiota richness and diversity tended to be increased in infants living with pets, whereas these measures were decreased in infants with older siblings. Infants living with pets exhibited under-representation of Bifidobacteriaceae and over-representation of Peptostreptococcaceae; infants with older siblings exhibited under-representation of Peptostreptococcaceae.

Conclusions: This study provides new evidence that exposure to pets and siblings may influence the early development of the gut microbiota, with potential implications for allergic disease. These two traditionally protective "hygiene hypothesis" factors appear to differentially impact gut microbiota composition and diversity, calling into question the clinical significance of these measures. Further research is required to confirm and expand these findings.

Keywords: Allergic disease; Atopy; Environmental exposures; Gut microbiome; Gut microbiota; Hygiene hypothesis; Infants; Microflora hypothesis; Pets; Siblings.

Figure 1

Fecal microbiota composition for 24 infants (mean age 4 months) according to the presence of household pets and siblings. A) Relative abundance of dominant bacterial families; each column represents one infant. B) Selected differentially abundant families according to pets and siblings; bars indicate means. Relative abundance determined by 16S rRNA sequencing; comparisons conducted with Metastats (see Methods and Table 2).

Figure 2

Richness and diversity of infant fecal microbiota according to the presence of household pets and siblings. Richness (Chao1 estimator) and diversity (Shannon Index) were calculated from 16S rRNA sequencing data (see Methods and Table 3).

Figure 3

Model for the possible influence of pets and siblings on infant gut microbiota and subsequent development of atopic disease. Household pets (D, dogs; C, cats) and siblings increase infant exposure to environmental microbes, promoting enrichment for distinct combinations of organisms within the gut microbiota; overall richness and diversity are also impacted. Despite favoring different microbiota profiles, the net effect of both pets and siblings is to promote healthy immune system development and protect against atopic disease. Further research is required to characterize the underlying biological mechanisms.