Prenatal PM2.5 Exposure Associated with Neonatal Gut Bacterial Colonization and Early Children's Cognitive Development

Yang Liu; Liyi Zhang; Jieming Wang; Xinyao Sui; Jiufeng Li; Yuyan Gui; Hang Wang; Yue Zhao; Yaqi Xu; Weizhao Cao; Pengpeng Wang; Yunhui Zhang

doi:10.1021/envhealth.4c00050

Prenatal PM_2.5 Exposure Associated with Neonatal Gut Bacterial Colonization and Early Children's Cognitive Development

Environ Health (Wash). 2024 Jul 2;2(11):802-815. doi: 10.1021/envhealth.4c00050. eCollection 2024 Nov 15.

Authors

Yang Liu^{1

2}, Liyi Zhang^{1

2}, Jieming Wang^{1

2}, Xinyao Sui^{1

2}, Jiufeng Li^{1

2}, Yuyan Gui^{1

2}, Hang Wang^{1

2}, Yue Zhao^{1

2}, Yaqi Xu^{1

2}, Weizhao Cao^{1

2}, Pengpeng Wang³, Yunhui Zhang^{1

2}

Affiliations

¹ Key Lab of Health Technology Assessment, National Health Commission of the People's Republic of China (Fudan University), Shanghai 200032, China.
² Key Laboratory of Public Health Safety, Ministry of Education, School of Public Health, Fudan University, Shanghai 200032, China.
³ Department of Environmental and Occupational Health, School of Public Health, Zhengzhou University, Henan 450001, China.

Abstract

Previous research indicated that fine particulate matter (PM_2.5) exposure affected both offspring neurodevelopment and the colonization of gut microbiota (GM), while the underlying mechanism remained unclear. Our study aimed to evaluate the impacts of prenatal PM_2.5 exposure on child cognitive development and investigate the role of neonatal GM colonization in the association. Based on the Shanghai Maternal-Child Pairs Cohort, 361 maternal-child pairs were recruited. Prenatal PM_2.5 exposure concentrations were estimated using a high-spatial-resolution prediction model, and child neurodevelopment was assessed by the Ages and Stages Questionnaire. Multivariable linear regression models, logistic regression models, linear discriminant analysis effect size, and random forest model were applied to explore the associations among PM_2.5 exposure, GM colonization, and children's neurodevelopment. The present study revealed a negative correlation between PM_2.5 exposure throughout pregnancy and child neurodevelopment. Prenatal PM_2.5 exposure was associated with an increased risk of suspected developmental delay (SDD) (OR = 1.683, 95% CI: 1.138, 2.489) in infants aged 2 months. Additionally, potential operational taxonomic unit markers were identified for PM_2.5-related neurotoxicity, demonstrating promising classification potential for early SDD screening (AUC = 71.27%). Prenatal PM_2.5 exposure might disrupt the composition, richness, and evenness of meconium GM, thereby influencing cognitive development and the occurrence of SDD in offspring. Seven PM_2.5-related genera, Ruminococcus gnavus group, Romboutsia, Burkholderiaceae Caballeronia Paraburkholderia, Blautia, Alistipes, Parabacteroides, and Bacteroides, were validated as correlated with prenatal PM_2.5 exposure and the occurrence of SDD. Moreover, alterations of GM related to PM_2.5 exposure and SDD might be accompanied by changes in functional pathways of amino acid, lipid, and vitamin metabolism as indicated by differentially enriched species in the Kyoto Encyclopedia of Genes and Genomes.