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. 2024 Nov 27;19(11):e0313078.
doi: 10.1371/journal.pone.0313078. eCollection 2024.

Gut microbiota markers in early childhood are linked to farm living, pets in household and allergy

Affiliations

Gut microbiota markers in early childhood are linked to farm living, pets in household and allergy

Annika Ljung et al. PLoS One. .

Abstract

Background: Children growing up on farms or with pets have a lower risk of developing allergy, which may be linked to their gut microbiota development during infancy.

Methods: Children from the FARMFLORA birth cohort (N = 65), of whom 28 (43%) lived on a dairy farm and 40 (62%) had pets, provided fecal samples at intervals from 3 days to 18 months of age. Gut microbiota composition was characterized using quantitative microbial culture of various typical anaerobic and facultatively anaerobic bacteria, with colonization rate and population counts of bacterial groups determined at the genus or species level. Allergy was diagnosed at three and eight years of age by experienced pediatricians. Generalized estimating equations were used to identify associations between farm residence or pet ownership, gut microbiota development and allergy. Adjustments were made for important potential confounders.

Results: Growing up on a farm was associated with a higher ratio of anaerobic to facultative bacteria in the first week, smaller Escherichia coli populations in colonized children in the first months of life and less frequent colonization by Clostridioides difficile at 12 months of age. Having pets in the household was associated with more frequent colonization by Bifidobacterium, Lactobacillus and Bacteroides in the first months. A higher ratio of anaerobic to facultative bacteria at one week of age, early colonization by Bifidobacterium, Lactobacillus and Bacteroides, and reduced carriage of C. difficile at 4-12 months of age all correlated negatively with subsequent allergy diagnosis.

Conclusions: Our findings indicate that lower rates of allergy in children growing up on farms or with pets may be related to early establishment of typical anaerobic commensals in their gut microbiota. However, further studies are needed to validate our observations in this small birth cohort study.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Gut microbiota in the FARMFLORA cohort (N = 65).
(A) Colonization frequencies (%) of facultative bacteria and (B) their median fecal population counts (log CFU/g) in colonized children. (C) Colonization frequencies (%) of anaerobic bacteria and (D) their median fecal population counts in colonized children. (E) Median ratio of anaerobe to facultative fecal bacterial counts (ratio anaerobe/facultative) at different ages. Error bars represent the interquartile range.
Fig 2
Fig 2. Gut microbiota composition in (A–C) children growing up on a farm vs control children and (D–F) children growing up with pets vs no pets.
A: Ratio of anaerobe to facultative fecal bacterial counts (ratio anaerobe/facultative) B: E. coli population counts in colonized children. C–F: Colonization by C. difficile, Bifidobacterium, Bacteroides and Lactobacillus spp.. Points are medians (A–B) and proportions (C–F). Error bars represent the interquartile range. Asterisks show significant differences between groups after adjustment for confounders (farm living adjusted for pets in household, sex, breastfeeding; pets in household adjusted for farm living, sex, breastfeeding). *p<0.05, **p<0.01, ***p<0.001.
Fig 3
Fig 3. Gut microbiota composition in relation to allergy at three years of age.
A–D: Colonization by Bacteroides, Bifidobacterium, Lactobacillus and C. difficile. Points are proportions of infants colonized (AD). Asterisks show significant differences between groups after adjustment for confounders (pets in household, growing up on a farm, sex, breastfeeding, allergic parent(s)) *p<0.05, **p<0.01, ***p<0.001.
Fig 4
Fig 4. Gut microbiota composition in relation to allergy at eight years of age.
A–C: Colonization by Bacteroides, Bifidobacterium and Lactobacillus spp. D: Ratio of anaerobe to facultative fecal bacterial counts (ratio anaerobe/facultative). E: Colonization by C. difficile. Points are proportions (AC, E) and medians (D). Error bars represent the interquartile range. Asterisks show significant differences between groups after adjustment for confounders (pets in household, growing up on a farm, sex, breastfeeding, allergic parent(s)). *p<0.05, **p<0.01, ***p<0.001, ****p<0.0001.

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Grants and funding

This work was supported by the Region Västra Götaland (agreement concerning medical research and education – ALF), https://www.alfvastragotaland.se [ALFGBG966243] [ALFGBG720181] (IA); the Swedish Medical Research Council (Vetenskapsrådet), https://www.vr.se/ [K98-06X-12612-01A] (AW); and the Health & Medical Care Committee of the Region Västra Götaland (Regional Research & Development funds Västra Götaland region) https://www.researchweb.org/is/vgregion/ [grant no. VGFOUREG-12007] (IA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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