Conserved Covarying Gut Microbial Network in Preterm Infants and Childhood Growth During the First 5 Years of Life: A Prospective Cohort Study

Jie Jia; Menglei Shuai; Weihui Yan; Qingya Tang; Bei Wang; Wenjing Tang; Panliang Wang; Tian Zhang; Shihan Yang; Yimeng Zhang; Qianruo Liu; Yuanqing Fu; Wei Cai; Ju-Sheng Zheng

doi:10.1016/j.ajcnut.2023.07.019

Conserved Covarying Gut Microbial Network in Preterm Infants and Childhood Growth During the First 5 Years of Life: A Prospective Cohort Study

Am J Clin Nutr. 2023 Sep;118(3):561-571. doi: 10.1016/j.ajcnut.2023.07.019. Epub 2023 Jul 29.

Authors

Jie Jia¹, Menglei Shuai², Weihui Yan³, Qingya Tang⁴, Bei Wang⁵, Wenjing Tang⁶, Panliang Wang⁷, Tian Zhang⁷, Shihan Yang⁸, Yimeng Zhang⁸, Qianruo Liu⁸, Yuanqing Fu⁹, Wei Cai¹⁰, Ju-Sheng Zheng²

Affiliations

¹ Department of Clinical Nutrition, Xin Hua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China; College of Health Science and Technology, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai, China; Shanghai Institute of Pediatric Research, Shanghai, China.
² School of Life Sciences, Westlake University, Hangzhou, China; Westlake Intelligent Biomarker Discovery Lab, Westlake Laboratory of Life Sciences and Biomedicine, Hangzhou, China; Institute of Basic Medical Sciences, Westlake Institute for Advanced Study, Hangzhou, China.
³ Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai, China; Shanghai Institute of Pediatric Research, Shanghai, China; Division of Pediatric Gastroenterology and Nutrition, Xin Hua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁴ Department of Clinical Nutrition, Xin Hua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁵ Department of Obstetrics & Gynecology, Xin Hua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁶ Department of Clinical Nutrition, Xin Hua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China; College of Health Science and Technology, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁷ Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai, China; Shanghai Institute of Pediatric Research, Shanghai, China.
⁸ College of Health Science and Technology, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁹ School of Life Sciences, Westlake University, Hangzhou, China; Westlake Intelligent Biomarker Discovery Lab, Westlake Laboratory of Life Sciences and Biomedicine, Hangzhou, China; Institute of Basic Medical Sciences, Westlake Institute for Advanced Study, Hangzhou, China. Electronic address: fuyuanqing@westlake.edu.cn.
¹⁰ Shanghai Key Laboratory of Pediatric Gastroenterology and Nutrition, Shanghai, China; Shanghai Institute of Pediatric Research, Shanghai, China; Division of Pediatric Gastroenterology and Nutrition, Xin Hua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Electronic address: caiw1978@163.com.

PMID: 37517614
DOI: 10.1016/j.ajcnut.2023.07.019

Abstract

Background: Longitudinally conserved microbe-microbe interactions may provide insights to understand the complex dynamic system of early-life gut microbiota among preterm infants.

Objectives: We aimed to profile the covarying network of gut microbiota among preterm infants and investigate its potential influence on host growth (2-5 y).

Methods: We collected time-series stool samples (n = 717 from children and n = 116 from mothers) among 51 preterm and 51 full-term infants from birth up to 5 y of age and among 53 mothers. The included infants underwent time-series measurements of early-life gut microbiota (0-5 y) and growth (2-5 y) from June 2014 to April 2017. The covarying taxa that exhibited consistent covariation from day 1 to year 5 were defined as conserved features in the development of gut microbiota. Childrens' height-for-age z score (HAZ) and weight-for-age z score were calculated according to World Health Organization Child Growth Standards.

Results: We observed distinct dynamic patterns of both microbial alpha and beta diversity comparing preterm infants with full-term controls during the very early stage (<3 mo). Moreover, we identified a covarying network containing 10 taxa as a conserved gut microbial feature of these preterm infants from birth to 5 y old. This covarying network was distinctive between preterm and full-term infants before 3 mo of age (P < 0.001) and tended to be similar as the infants grew up. Several covarying taxa of the network during early life (<3 mo) were associated with childhood growth (2-5 y) (eg, Clostridium_sensu_stricto_1 with HAZ, β = -0.32, q < 0.01), and the human milk feeding duration was a main modulating factor.

Conclusions: Preterm born children possess conserved and distinct covarying microbiota during very early life, which may have a profound influence on their growth later in life. This trial was registered at clinicaltrials.gov as NCT03373721.

Keywords: covarying network; growth; gut microbiota; longitudinally; preterm infants.

Publication types

Observational Study
Research Support, Non-U.S. Gov't

MeSH terms

Child
Female
Gastrointestinal Microbiome*
Humans
Infant
Infant, Newborn
Infant, Premature*
Milk, Human
Prospective Studies

Associated data

ClinicalTrials.gov/NCT03373721