Gut microbiota maturity mediates the protective effect of siblings on food allergy - 08/09/23

Doi : 10.1016/j.jaci.2023.02.034

Yuan Gao, BSc ^a,^b,^c, Jakob Stokholm, MD, PhD ^d,^e, Martin O’Hely, PhD ^a,^f, Anne-Louise Ponsonby, MBBS, FAFPHM, PhD ^f,^g, Mimi L.K. Tang, MBBS, FRACP, FRCPA, PhD ^f,^h, Sarath Ranganathan, MD, PhD ^f,^h, Richard Saffery, PhD ^f,^h, Leonard C. Harrison, MD, MBBS, DSc, FRACP, FRCPA, FAHMS ^i,^j, Fiona Collier, PhD ^a, Lawrence Gray, MBBS, PhD ^a,^b, David Burgner, PhD ^f,^h, John Molloy, MB, FRCPCH, PhD ^a,^b, Peter D. Sly, MBBS, MD, DSc ^k,^l, Susanne Brix, MSc, PhD ^m, Hanne Frøkiær, PhD ^c, Peter Vuillermin, MBBS, BMedSci, FRACP, PhD ^a,^b,^⁎
on behalf of the
BIS Investigator Group
^a Institute for Physical and Mental Health and Clinical Transformation, Deakin University, Geelong, Australia
^b Child Health Research Unit, Barwon Health, Geelong, Australia
^c Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
^d COPSAC, Copenhagen Prospective Studies on Asthma in Childhood, Herlev and Gentofte Hospital, University of Copenhagen, Copenhagen, Denmark
^e Department of Food Science, University of Copenhagen, Frederiksberg, Denmark
^f Murdoch Children’s Research Institute, Royal Children’s Hospital, Melbourne, Australia
^g Developing Brain Division, The Florey Institute for Neuroscience and Mental Health, Melbourne, Australia
^h Department of Pediatrics, University of Melbourne, Melbourne, Australia
ⁱ Population Health and Immunity Division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia
^j Department of Medical Biology, University of Melbourne, Melbourne, Australia
^k Children’s Health and Environment Program, Child Health Research Centre, The University of Queensland, Brisbane, Australia
^l Faculty of Health, Deakin University, Geelong, Australia
^m Department of Biotechnology and Biomedicine, Technical University of Denmark, Kongens Lyngby, Denmark

^∗Corresponding author: Peter Vuilllermin, MBBS, BMedSci, FRACP, PhD, Institute for Physical and Mental Health and Clinical Transformation, Deakin University, Geelong 3220, Australia.Institute for Physical and Mental Health and Clinical TransformationDeakin UniversityGeelong3220Australia

Graphical abstract

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Abstract

Background

The mechanisms underlying the protective effect of older siblings on allergic disease remain unclear but may relate to the infant gut microbiota.

Objective

We sought to investigate whether having older siblings decreases the risk of IgE-mediated food allergy by accelerating the maturation of the infant gut microbiota.

Methods

In a birth cohort assembled using an unselected antenatal sampling frame (n = 1074), fecal samples were collected at 1 month, 6 months, and 1 year, and food allergy status at 1 year was determined by skin prick test and in-hospital food challenge. We used 16S rRNA gene amplicon sequencing to derive amplicon sequence variants. Among a random subcohort (n = 323), microbiota-by-age z scores at each time point were calculated using fecal amplicon sequence variants to represent the gut microbiota maturation over the first year of life.

Results

A greater number of siblings was associated with a higher microbiota-by-age z score at age 1 year (β = 0.15 per an additional sibling; 95% CI, 0.05-0.24; P = .003), which was in turn associated with decreased odds of food allergy (odds ratio, 0.45; 95% CI, 0.33-0.61; P < .001). Microbiota-by-age z scores mediated 63% of the protective effect of siblings. Analogous associations were not observed at younger ages.

Conclusions

The protective effect of older siblings on the risk of developing IgE-mediated food allergy during infancy is substantially mediated by advanced maturation of the gut microbiota at age 1 year.

Il testo completo di questo articolo è disponibile in PDF.

Key words : Food allergy, microbiota maturation, birth cohort, siblings

Abbreviations used : ASV, BIS, clr, MAZ, nTreg, OR, SCFA, SPT, Treg

Mappa

Fecal sample collection and processing

Short-chain fatty acids

Blood sample collection and processing

Flow cytometry of immune cells

Statistics and data analysis

Results

Characteristics of study participants

Microbial composition changes during first year of life

Gut microbiota maturity at age 1 year and food allergy

Environmental factors and MAZ

MAZ at age 1 year mediates the protective effect of greater sibling numbers on food allergy

Fecal SCFAs and MAZ at age 1 year

Discussion

Disclosure statement

Esportazione

Vol 152 - N° 3

P. 667-675 - Settembre 2023 Ritorno al numero

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Gut microbiota maturity mediates the protective effect of siblings on food allergy - 08/09/23

Graphical abstract

Abstract

Background

Objective

Methods

Results

Conclusions

Mappa

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