Development of the early-life gut microbiome and associations with eczema in a prospective Chinese cohort

ABSTRACT The first few years of life is a key period for the development of the gut microbiome. However, our current understanding of this topic is largely biased toward Western populations. In this study, we characterized the development and determinants of the gut microbiome in a prospective cohor...

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Main Authors: Man Kit Cheung, Ting Fan Leung, Wing Hung Tam, Agnes S. Y. Leung, Oi Man Chan, Rita W. Y. Ng, Jennifer W. K. Yau, Lai-yuk Yuen, Sylvia L. Y. Tong, Wendy C. S. Ho, Apple C. M. Yeung, Zigui Chen, Paul K. S. Chan
Format: Article
Language:English
Published: American Society for Microbiology 2023-10-01
Series:mSystems
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msystems.00521-23
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author Man Kit Cheung
Ting Fan Leung
Wing Hung Tam
Agnes S. Y. Leung
Oi Man Chan
Rita W. Y. Ng
Jennifer W. K. Yau
Lai-yuk Yuen
Sylvia L. Y. Tong
Wendy C. S. Ho
Apple C. M. Yeung
Zigui Chen
Paul K. S. Chan
author_facet Man Kit Cheung
Ting Fan Leung
Wing Hung Tam
Agnes S. Y. Leung
Oi Man Chan
Rita W. Y. Ng
Jennifer W. K. Yau
Lai-yuk Yuen
Sylvia L. Y. Tong
Wendy C. S. Ho
Apple C. M. Yeung
Zigui Chen
Paul K. S. Chan
author_sort Man Kit Cheung
collection DOAJ
description ABSTRACT The first few years of life is a key period for the development of the gut microbiome. However, our current understanding of this topic is largely biased toward Western populations. In this study, we characterized the development and determinants of the gut microbiome in a prospective cohort of 112 term Chinese children by sequencing 713 stool samples collected at nine time points from birth to 3 years of age using 16S rRNA gene sequencing. We revealed alterations in the composition and alpha and beta diversities of the gut microbiota across the first 3 years of life. We identified mode of delivery, feeding mode, and intrapartum antibiotics as the major determinants of the early-life gut microbiome, the effects of all of which persisted up to 12 months. Importantly, by conducting a nested case–control study, we showed that alterations in the infant gut microbiota precede the development of eczema. Interestingly, we identified a depletion of Bacteroides and an enrichment of Clostridium sensu stricto 1 in the gut microbiome of infants with eczema at 1 year old. The same patterns were also observed in C-section-born infants within the same time frames, suggesting a role of the gut microbiota in previously reported associations between C-section and increased risk of eczema. Our study has revealed important associations between the gut microbiome and eczema in infancy and has established the basis for potential prevention/treatment of eczema via modulation of the gut microbiota. IMPORTANCE Eczema is a major allergic disease in children, which is particularly prevalent in Chinese children during their first year of life. In this study, we showed that alterations in the infant gut microbiota precede the development of eczema in a prospective Chinese cohort. In particular, we discovered enrichments of the genera Clostridium sensu stricto 1 and Finegoldia in the cases at 3 and 1 month of age, respectively, which may represent potential targets for intervention to prevent eczema. Besides, we identified a depletion of Bacteroides from 1 to 6 months of age and an enrichment of Clostridium sensu stricto 1 at 3 months in the eczema cases, patterns also observed in C-section-born infants within the same time frames, providing first evidence to support a role of the gut microbiota in previously reported associations between C-section and increased risk of eczema in infancy.
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spelling doaj.art-ac4b79eceff548bb80c34d9d754448982023-11-17T03:22:37ZengAmerican Society for MicrobiologymSystems2379-50772023-10-018510.1128/msystems.00521-23Development of the early-life gut microbiome and associations with eczema in a prospective Chinese cohortMan Kit Cheung0Ting Fan Leung1Wing Hung Tam2Agnes S. Y. Leung3Oi Man Chan4Rita W. Y. Ng5Jennifer W. K. Yau6Lai-yuk Yuen7Sylvia L. Y. Tong8Wendy C. S. Ho9Apple C. M. Yeung10Zigui Chen11Paul K. S. Chan12Department of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaDepartment of Paediatrics, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaCentre for Gut Microbiota Research, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaDepartment of Paediatrics, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaDepartment of Paediatrics, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaDepartment of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaDepartment of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaDepartment of Obstetrics and Gynaecology, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaDepartment of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaDepartment of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaDepartment of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaDepartment of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaDepartment of Microbiology, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region , Hong Kong, ChinaABSTRACT The first few years of life is a key period for the development of the gut microbiome. However, our current understanding of this topic is largely biased toward Western populations. In this study, we characterized the development and determinants of the gut microbiome in a prospective cohort of 112 term Chinese children by sequencing 713 stool samples collected at nine time points from birth to 3 years of age using 16S rRNA gene sequencing. We revealed alterations in the composition and alpha and beta diversities of the gut microbiota across the first 3 years of life. We identified mode of delivery, feeding mode, and intrapartum antibiotics as the major determinants of the early-life gut microbiome, the effects of all of which persisted up to 12 months. Importantly, by conducting a nested case–control study, we showed that alterations in the infant gut microbiota precede the development of eczema. Interestingly, we identified a depletion of Bacteroides and an enrichment of Clostridium sensu stricto 1 in the gut microbiome of infants with eczema at 1 year old. The same patterns were also observed in C-section-born infants within the same time frames, suggesting a role of the gut microbiota in previously reported associations between C-section and increased risk of eczema. Our study has revealed important associations between the gut microbiome and eczema in infancy and has established the basis for potential prevention/treatment of eczema via modulation of the gut microbiota. IMPORTANCE Eczema is a major allergic disease in children, which is particularly prevalent in Chinese children during their first year of life. In this study, we showed that alterations in the infant gut microbiota precede the development of eczema in a prospective Chinese cohort. In particular, we discovered enrichments of the genera Clostridium sensu stricto 1 and Finegoldia in the cases at 3 and 1 month of age, respectively, which may represent potential targets for intervention to prevent eczema. Besides, we identified a depletion of Bacteroides from 1 to 6 months of age and an enrichment of Clostridium sensu stricto 1 at 3 months in the eczema cases, patterns also observed in C-section-born infants within the same time frames, providing first evidence to support a role of the gut microbiota in previously reported associations between C-section and increased risk of eczema in infancy.https://journals.asm.org/doi/10.1128/msystems.00521-23atopic dermatitiscesarean sectionClostridium sensu stricto 1early childhoodgut microbiotainfancy
spellingShingle Man Kit Cheung
Ting Fan Leung
Wing Hung Tam
Agnes S. Y. Leung
Oi Man Chan
Rita W. Y. Ng
Jennifer W. K. Yau
Lai-yuk Yuen
Sylvia L. Y. Tong
Wendy C. S. Ho
Apple C. M. Yeung
Zigui Chen
Paul K. S. Chan
Development of the early-life gut microbiome and associations with eczema in a prospective Chinese cohort
mSystems
atopic dermatitis
cesarean section
Clostridium sensu stricto 1
early childhood
gut microbiota
infancy
title Development of the early-life gut microbiome and associations with eczema in a prospective Chinese cohort
title_full Development of the early-life gut microbiome and associations with eczema in a prospective Chinese cohort
title_fullStr Development of the early-life gut microbiome and associations with eczema in a prospective Chinese cohort
title_full_unstemmed Development of the early-life gut microbiome and associations with eczema in a prospective Chinese cohort
title_short Development of the early-life gut microbiome and associations with eczema in a prospective Chinese cohort
title_sort development of the early life gut microbiome and associations with eczema in a prospective chinese cohort
topic atopic dermatitis
cesarean section
Clostridium sensu stricto 1
early childhood
gut microbiota
infancy
url https://journals.asm.org/doi/10.1128/msystems.00521-23
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