Gut microbiota maturity mediates the protective effect of siblings on food allergy

Yuan Gao; Jakob Stokholm; Martin O'Hely; Anne-Louise Ponsonby; Mimi L K Tang; Sarath Ranganathan; Richard Saffery; Leonard C Harrison; Fiona Collier; Lawrence Gray; David Burgner; John Molloy; Peter D Sly; Susanne Brix; Hanne Frøkiær; Peter Vuillermin

doi:10.1016/j.jaci.2023.02.034

Gut microbiota maturity mediates the protective effect of siblings on food allergy

Yuan Gao, Jakob Stokholm, Martin O'Hely, Anne-Louise Ponsonby, Mimi L K Tang, Sarath Ranganathan, Richard Saffery, Leonard C Harrison, Fiona Collier, Lawrence Gray, David Burgner, John Molloy, Peter D Sly, Susanne Brix, Hanne Frøkiær, Peter Vuillermin

13 Citationer (Scopus)

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.

Originalsprog	Engelsk
Tidsskrift	The Journal of allergy and clinical immunology
Vol/bind	152
Udgave nummer	3
Sider (fra-til)	667-675
Antal sider	9
ISSN	0091-6749
DOI	https://doi.org/10.1016/j.jaci.2023.02.034
Status	Udgivet - sep. 2023

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10.1016/j.jaci.2023.02.034

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Gao, Y., Stokholm, J., O'Hely, M., Ponsonby, A.-L., Tang, M. L. K., Ranganathan, S., Saffery, R., Harrison, L. C., Collier, F., Gray, L., Burgner, D., Molloy, J., Sly, P. D., Brix, S., Frøkiær, H., & Vuillermin, P. (2023). Gut microbiota maturity mediates the protective effect of siblings on food allergy. The Journal of allergy and clinical immunology, 152(3), 667-675. https://doi.org/10.1016/j.jaci.2023.02.034

Gao, Y, Stokholm, J, O'Hely, M, Ponsonby, A-L, Tang, MLK, Ranganathan, S, Saffery, R, Harrison, LC, Collier, F, Gray, L, Burgner, D, Molloy, J, Sly, PD, Brix, S, Frøkiær, H & Vuillermin, P 2023, 'Gut microbiota maturity mediates the protective effect of siblings on food allergy', The Journal of allergy and clinical immunology, bind 152, nr. 3, s. 667-675. https://doi.org/10.1016/j.jaci.2023.02.034

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title = "Gut microbiota maturity mediates the protective effect of siblings on food allergy",

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.",

keywords = "Pregnancy, Infant, Humans, Female, Gastrointestinal Microbiome, Siblings, RNA, Ribosomal, 16S/genetics, Food Hypersensitivity/prevention & control, Immunoglobulin E",

author = "Yuan Gao and Jakob Stokholm and Martin O'Hely and Anne-Louise Ponsonby and Tang, {Mimi L K} and Sarath Ranganathan and Richard Saffery and Harrison, {Leonard C} and Fiona Collier and Lawrence Gray and David Burgner and John Molloy and Sly, {Peter D} and Susanne Brix and Hanne Fr{\o}ki{\ae}r and Peter Vuillermin",

year = "2023",

month = sep,

doi = "10.1016/j.jaci.2023.02.034",

language = "English",

volume = "152",

pages = "667--675",

journal = "The Journal of allergy and clinical immunology",

issn = "0091-6749",

publisher = "Elsevier Inc.",

number = "3",

}

TY - JOUR

T1 - Gut microbiota maturity mediates the protective effect of siblings on food allergy

AU - Gao, Yuan

AU - Stokholm, Jakob

AU - O'Hely, Martin

AU - Ponsonby, Anne-Louise

AU - Tang, Mimi L K

AU - Ranganathan, Sarath

AU - Saffery, Richard

AU - Harrison, Leonard C

AU - Collier, Fiona

AU - Gray, Lawrence

AU - Burgner, David

AU - Molloy, John

AU - Sly, Peter D

AU - Brix, Susanne

AU - Frøkiær, Hanne

AU - Vuillermin, Peter

PY - 2023/9

Y1 - 2023/9

N2 - 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.

AB - 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.

KW - Pregnancy

KW - Infant

KW - Humans

KW - Female

KW - Gastrointestinal Microbiome

KW - Siblings

KW - RNA, Ribosomal, 16S/genetics

KW - Food Hypersensitivity/prevention & control

KW - Immunoglobulin E

UR - http://www.scopus.com/inward/record.url?scp=85163821830&partnerID=8YFLogxK

U2 - 10.1016/j.jaci.2023.02.034

DO - 10.1016/j.jaci.2023.02.034

M3 - Journal article

C2 - 37150361

SN - 0091-6749

VL - 152

SP - 667

EP - 675

JO - The Journal of allergy and clinical immunology

JF - The Journal of allergy and clinical immunology

IS - 3

ER -

Gut microbiota maturity mediates the protective effect of siblings on food allergy

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