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. 2024 Jan-Dec;16(1):2323234.
doi: 10.1080/19490976.2024.2323234. Epub 2024 Mar 4.

Maternal smoking during pregnancy increases the risk of gut microbiome-associated childhood overweight and obesity

Ye Peng  1   2   3 , Hein M Tun  1   2   3 , Siew C Ng  2   3   4 , Hogan Kok-Fung Wai  5 , Xi Zhang  1   3 , Jaclyn Parks  6   7 , Catherine J Field  8 , Piush Mandhane  9 , Theo J Moraes  10 , Elinor Simons  11 , Stuart E Turvey  12 , Padmaja Subbarao  10 , Jeffrey R Brook  13 , Tim K Takaro  6 , James A Scott  13 , Francis Kl Chan  2   3 , Anita L Kozyrskyj  9
Affiliations

Maternal smoking during pregnancy increases the risk of gut microbiome-associated childhood overweight and obesity

Ye Peng et al. Gut Microbes. 2024 Jan-Dec.

Abstract

Childhood obesity is linked to maternal smoking during pregnancy. Gut microbiota may partially mediate this association and could be potential targets for intervention; however, its role is understudied. We included 1,592 infants from the Canadian Healthy Infants Longitudinal Development Cohort. Data on environmental exposure and lifestyle factors were collected prenatally and throughout the first three years. Weight outcomes were measured at one and three years of age. Stool samples collected at 3 and 12 months were analyzed by sequencing the V4 region of 16S rRNA to profile microbial compositions and magnetic resonance spectroscopy to quantify the metabolites. We showed that quitting smoking during pregnancy did not lower the risk of offspring being overweight. However, exclusive breastfeeding until the third month of age may alleviate these risks. We also reported that maternal smoking during pregnancy significantly increased Firmicutes abundance and diversity. We further revealed that Firmicutes diversity mediates the elevated risk of childhood overweight and obesity linked to maternal prenatal smoking. This effect possibly occurs through excessive microbial butyrate production. These findings add to the evidence that women should quit smoking before their pregnancies to prevent microbiome-mediated childhood overweight and obesity risk, and indicate the potential obesogenic role of excessive butyrate production in early life.

Keywords: Maternal smoking; butyrate production; childhood obesity; gut microbiota.

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Conflict of interest statement

Francis Ka-Leung Chan is Board Member of CUHK Medical Centre. He is a co-founder, non-executive Board Chairman and shareholder of GenieBiome Ltd. He receives patent royalties through his affiliated institutions. He has received fees as an advisor and honoraria as a speaker for Eisai Co. Ltd., AstraZeneca, Pfizer Inc., Takeda Pharmaceutical Co., and Takeda (China) Holdings Co. Ltd. Siew Chien Ng has served as an advisory board member for Pfizer, Ferring, Janssen, and Abbvie and received honoraria as a speaker for Ferring, Tillotts, Menarini, Janssen, Abbvie, and Takeda. Siew Chien Ng has received research grants through her affiliated institutions from Olympus, Ferring, and Abbvie. Siew Chien Ng is a founder member, non-executive director, non-executive scientific advisor, and shareholder of GenieBiome Ltd. Siew Chien Ng receives patent royalties through her affiliated institutions. Francis Ka-Leung Chan, Siew Chien Ng, and Hein Min Tun are named inventors of patent applications held by the CUHK and MagIC that cover the therapeutic and diagnostic use of microbiome. All other coauthors have no conflict of interest.

Figures

None
Graphical abstract
Figure 1.
Figure 1.
Schematic diagram for data collection and the association between maternal smoking during pregnancy and BMI z-scores of infants.
Figure 2.
Figure 2.
Associations between maternal smoking during pregnancy and profiles of gut microbiota in infancy.
Figure 3.
Figure 3.
Early-infancy microbial mediators in the pathway from maternal smoking during pregnancy to weight outcomes at 1 and 3 years.
Figure 4.
Figure 4.
Metabolite mediators.
See this image and copyright information in PMC

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Publication types

Grants and funding

This study was partially funded by the startup funding of the Chinese University of Hong Kong and by grants from the Research Grants Council of the Hong Kong Special Administrative Region, China (Project No. 14113923) to Dr. Tun, and the Canadian Institutes of Health Research Canadian Microbiome Initiative grant (Project No. 227312) to Dr. Kozyrskyj. The Canadian Institutes of Health Research and the Allergy, Genes, and Environment (AllerGen) Network of Centres of Excellence provided core support for the Canadian Healthy Infant Longitudinal Development (CHILD) Study. Dr. Ye Peng was partially supported by the Research Committee Postdoctoral Fellowship Scheme of the Chinese University of Hong Kong. This study was also partially supported by InnoHK, the Government of Hong Kong, Special Administrative Region of the People’s Republic of China.