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

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.

SUBMITTER: Peng Y

PROVIDER: S-EPMC10913716 | biostudies-literature | 2024 Jan-Dec

REPOSITORIES: biostudies-literature

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

Peng Ye Y Tun Hein M HM Ng Siew C SC Wai Hogan Kok-Fung HK Zhang Xi X Parks Jaclyn J Field Catherine J CJ Mandhane Piush P Moraes Theo J TJ Simons Elinor E Turvey Stuart E SE Subbarao Padmaja P Brook Jeffrey R JR Takaro Tim K TK Scott James A JA Chan Francis Kl FK Kozyrskyj Anita L AL

Gut microbes 20240101 1

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 a ...[more]

PMID: 38436093

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Project description:IntroductionThere is a lack of comprehensive review on associations of maternal smoking cessation (versus nonsmokers) with childhood overweight and obesity.Aims and methodsWe conducted a systematic review and meta-analysis of existing evidence in this field. Within PubMed, EMBASE, and CENTRAL databases, we identified and screened 1147 abstracts. We reviewed full-texts and extracted related information from 10 eligible articles. We pooled odds ratios for overweight/obesity and mean differences in BMI z-scores by maternal smoking status around pregnancy.ResultsAmong 10 eligible studies, 71 393 children were included from ages 2 to 18 years. Compared to children of nonsmokers, the pooled unadjusted odds ratio (OR) for overweight was 1.36 (95% Confidence Interval CI: 1.14, 1.62) in children of quitters and 1.44 (1.27, 1.64) in children of continued smokers. The pooled unadjusted OR for obesity was 1.65 (1.17, 2.32) in children of quitters and 1.94 (1.38, 2.73) in children of continued smokers. The pooled unadjusted mean difference in BMI z-score was 0.51 (0.41, 0.61) in children of quitters and 0.64 (0.58, 0.70) in children of continued smokers. The pooled unadjusted OR for overweight in children of mothers quitting before pregnancy was 1.46 (1.15, 1.85), during the first trimester was 1.52 (1.27, 1.82), and during pregnancy (mixed timing, mostly first trimester) was 0.97 (0.79, 1.20).ConclusionThe risk of offspring overweight and obesity was moderately higher for quitters during pregnancy compared to nonsmokers, although it might not be as high as continued smokers.ImplicationsMaternal smoking during pregnancy is an established risk factor of childhood overweight and obesity. Based on our systematic review, intervention to help mothers quit smoking has the potential to reduce the risk of childhood overweight and obesity in offspring related to prenatal tobacco exposure. Quitting before pregnancy is ideal, but quitting in early pregnancy is still helpful for reducing risk.

Project description:BackgroundOverweight or obesity among pregnant women may compromise maternal and neonatal iron status by upregulating hepcidin.ObjectivesThis study determined the association of 1) maternal and neonatal iron status with maternal and neonatal hepcidin concentrations, and 2) maternal prepregnancy weight status with maternal and neonatal hepcidin concentrations.MethodsWe examined hematologic data from 405 pregnant women and their infants from the placebo treatment group of a pregnancy iron supplementation trial in rural China. We measured hepcidin, serum ferritin (SF), soluble transferrin receptor (sTfR), and high-sensitivity C-reactive protein in maternal blood samples at mid-pregnancy and in cord blood at delivery. We used regression analysis to examine the association of maternal prepregnancy overweight or obese status with maternal hepcidin concentration in mid-pregnancy and cord hepcidin concentrations. We also used path analysis to examine mediation of the association of maternal prepregnancy overweight or obese status with maternal iron status by maternal hepcidin, as well as with neonatal hepcidin by neonatal iron status.ResultsMaternal iron status was positively correlated with maternal hepcidin at mid-pregnancy (SF: r = 0.63, P < 0.001; sTfR: r = -0.37, P < 0.001). Neonatal iron status was also positively correlated with cord hepcidin (SF: r = 0.61, P < 0.001; sTfR: r = -0.39, P < 0.001). In multiple linear regression models, maternal prepregnancy overweight or obese status was not associated with maternal hepcidin at mid-pregnancy but was associated with lower cord hepcidin (coefficient = -0.21, P = 0.004). Using path analysis, we observed a significant indirect effect of maternal prepregnancy overweight or obese status on cord hepcidin, mediated by neonatal iron status.ConclusionsIn both pregnant women and neonates, hepcidin was responsive to iron status. Maternal prepregnancy overweight status, with or without including obese women, was associated with lower cord blood hepcidin, likely driven by lower iron status among the neonates of these mothers.

Project description:BackgroundThe maternal microbiome has emerged as an important factor in gestational health and outcome and is associated with risk of preterm birth and offspring morbidity. Epidemiological evidence also points to successive pregnancies-referred to as maternal parity-as a risk factor for preterm birth, infant mortality, and impaired neonatal growth. Despite the fact that both the maternal microbiome and parity are linked to maternal-infant health, the impact of parity on the microbiome remains largely unexplored, in part due to the challenges of studying parity in humans.ResultsUsing synchronized pregnancies and dense longitudinal monitoring of the microbiome in pigs, we describe a microbiome trajectory during pregnancy and determine the extent to which parity modulates this trajectory. We show that the microbiome changes reproducibly during gestation and that this remodeling occurs more rapidly as parity increases. At the time of parturition, parity was linked to the relative abundance of several bacterial species, including Treponema bryantii, Lactobacillus amylovorus, and Lactobacillus reuteri. Strain tracking carried out in 18 maternal-offspring "quadrads"-each consisting of one mother sow and three piglets-linked maternal parity to altered levels of Akkermansia muciniphila, Prevotella stercorea, and Campylobacter coli in the infant gut 10 days after birth.ConclusionsCollectively, these results identify parity as an important environmental factor that modulates the gut microbiome during pregnancy and highlight the utility of a swine model for investigating the microbiome in maternal-infant health. In addition, our data show that the impact of parity extends beyond the mother and is associated with alterations in the community of bacteria that colonize the offspring gut early in life. The bacterial species we identified as parity-associated in the mother and offspring have been shown to influence host metabolism in other systems, raising the possibility that such changes may influence host nutrient acquisition or utilization. These findings, taken together with our observation that even subtle differences in parity are associated with microbiome changes, underscore the importance of considering parity in the design and analysis of human microbiome studies during pregnancy and in infants. Video abstract.

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

Publications

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

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