Delayed gut microbiota maturation in the first year of life is a hallmark of pediatric allergic disease

Courtney Hoskinson, Darlene L. Y. Dai, Kate L. Bel, Allan B. Becker, Theo J. Moraes, Piushkumar J. Mandhane, B. Brett Finlay, Elinor Simons, Anita L. Kozyrskyj, Meghan B. Azad, Padmaja Subbarao, Charisse Petersen and Stuart E. Turvey (sturvey@cw.bc.ca)
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Courtney Hoskinson: University of British Columbia
Darlene L. Y. Dai: University of British Columbia
Kate L. Bel: University of British Columbia
Allan B. Becker: University of Manitoba
Theo J. Moraes: The Hospital for Sick Children
Piushkumar J. Mandhane: University of Alberta
B. Brett Finlay: University of British Columbia
Elinor Simons: University of Manitoba
Anita L. Kozyrskyj: University of Alberta
Meghan B. Azad: University of Manitoba
Padmaja Subbarao: The Hospital for Sick Children
Charisse Petersen: University of British Columbia
Stuart E. Turvey: University of British Columbia

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: Abstract Allergic diseases affect millions of people worldwide. An increase in their prevalence has been associated with alterations in the gut microbiome, i.e., the microorganisms and their genes within the gastrointestinal tract. Maturation of the infant immune system and gut microbiota occur in parallel; thus, the conformation of the microbiome may determine if tolerant immune programming arises within the infant. Here we show, using deeply phenotyped participants in the CHILD birth cohort (n = 1115), that there are early-life influences and microbiome features which are uniformly associated with four distinct allergic diagnoses at 5 years: atopic dermatitis (AD, n = 367), asthma (As, n = 165), food allergy (FA, n = 136), and allergic rhinitis (AR, n = 187). In a subset with shotgun metagenomic and metabolomic profiling (n = 589), we discover that impaired 1-year microbiota maturation may be universal to pediatric allergies (AD p = 0.000014; As p = 0.0073; FA p = 0.00083; and AR p = 0.0021). Extending this, we find a core set of functional and metabolic imbalances characterized by compromised mucous integrity, elevated oxidative activity, decreased secondary fermentation, and elevated trace amines, to be a significant mediator between microbiota maturation at age 1 year and allergic diagnoses at age 5 years (βindirect = −2.28; p = 0.0020). Microbiota maturation thus provides a focal point to identify deviations from normative development to predict and prevent allergic disease.

Date: 2023
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DOI: 10.1038/s41467-023-40336-4

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