Effects of Maternal Exercise During Pregnancy on Perinatal Growth and Childhood Obesity Outcomes: A Meta-analysis and Meta-regression

Summary Background Sarcolipin and uncoupling protein 3 (UCP3) mediate muscle-based non-shivering thermogenesis (NST) to improve metabolic homeostasis. The impacts of maternal obesity (MO) and maternal exercise (ME) on NST in offspring muscle remain unexamined. Methods Female mice were fed with a control diet or high fat diet to induce obesity. Then, obese mice were further separated into two groups: obesity only (OB) and OB plus daily exercise (OB/Ex). Fetal muscle was collected at embryonic day 18.5 and offspring mice at 3-month-old. Apelin administration during pregnancy and apelin receptor (APJ) knockout mouse were further used for investigating the mediatory role of APJ on muscle-based thermogenesis. To explore the direct effects of exercise on AMP-activated protein kinase (AMPK) downstream targets, AMPK knockout mouse was used. Findings MO inhibited while ME activated AMPK and peroxisome proliferator-activated receptor γ coactivator-1α (PGC-1α) in fetal muscle. AMPK activation increased sarcolipin expression, which inhibited the uptake of calcium ions into sarcoplasmic reticulum, thereby activating CaMKK2. Consistently, the expression of UCP3 and sarcolipin was suppressed due to MO but activated in ME fetal muscle. Importantly, changes of UCP3 and sarcolipin maintained in offspring muscle, showing the transgenerational effects. Furthermore, apelin administration during pregnancy mimicked the effects of ME on AMPK and CaMKK2 activation, and UCP3 and sarcolipin expression, underscoring the mediatory roles of apelin-AMPK signaling in improving fetal muscle development. Interpretation ME, via activation of apelin signaling-AMPK axis, enhances NST gene expression in fetal and offspring muscle impaired due to MO, which intergenerationally protects offspring from diet-induced obesity and metabolic disorders. Funding This work was supported by National Institutes of Health Grant R01-HD067449.

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“… 10 Our data are consistent with previous meta-analyses where children outcomes are improved due to ME. 48 , 49 …”

Section: Discussionmentioning

confidence: 99%

Maternal exercise intergenerationally drives muscle-based thermogenesis via activation of apelin-AMPK signaling

et al. 2022

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“…There is a considerable body of evidence that shows that risk of underweight or obesity was lower among offspring whose mothers maintained a healthy BMI, engaged in regular physical exercise and did not smoke. [22][23][24][25] On the other hand, the positive legacy of the Games mentioned above in healthy behaviours and services may play a mediating role in the pathway of the relationship of the BOG and children's growth. Most directly, the Games may promote the enthusiasm and action of individual sports participation through the centralised publicity of sports in a short period of time, and even cultivate long-term family sports atmosphere and habits.…”

Section: Original Researchmentioning

confidence: 99%

Association between Olympic Games and children’s growth: evidence from China

Guo

et al. 2022

Br J Sports Med

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ObjectivesTo estimate the association between the 2008 Beijing Olympic Games (BOG) and growth of children in China.MethodsA total sample of 6 951 children aged 3–10 years were included, among which 3 201 were interviewed in 2014 and 3 750 were interviewed in 2018. The BOG was used as a natural experiment. Exposure to the BOG was established by triple differences measured by age group, survey period and whether child participants were living in BOG areas or not, respectively. Children’s growth was assessed by binary variables of stunting, underweight, overweight and obesity. The difference-in-difference-in-differences (DDD) method was used to estimate the association between the BOG and children’s growth.ResultsDDD estimates showed that the BOG was significantly associated with decreased risks of children’s underweight (OR 0.12; 95% CI 0.02 to 0.69) and overweight (OR 0.43; 95% CI 0.19 to 0.98) after controlling for multiple covariates in fractional polynomial models. There was significant sex heterogeneity with regard to the association between BOG and obesity, that is, lower odds of obesity (OR 0.24; 95% CI 0.06 to 0.94) were found in female children but not in male children.ConclusionThe BOG was positively associated with healthier growth of children including decreased risks of both undernutrition and overnutrition. More attention should be given to the improvement of health surveillance and services before and after sporting events so that the active role of such mega-events in the lasting well-being of the public can be determined in more detail.

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“…Jönsson et al [21] and Antoun et al [17], both undertaking RCTs, investigated a diet combined with a physical activity intervention and both found an effect on DNA methylation in cord blood. In a recent meta-analysis [36], the effect of maternal exercise during pregnancy on growth and childhood obesity was examined, and a reduced risk of large for gestational age (LGA) and reduced childhood obesity in offspring from mothers with normal weight was found. Perhaps the epigenetic changes such as those found by Jonsson et al and Antoun et al are the explanation for the beneficial effect of physical activity.…”

Section: Genome-wide Approachmentioning

confidence: 99%

The Impact of Lifestyle, Diet and Physical Activity on Epigenetic Changes in the Offspring—A Systematic Review

et al. 2021

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Aims: This systematic review examines the association between maternal lifestyle, diet and physical activity, and epigenetic changes in the offspring. Methods: A literature search was conducted using multiple science databases: PubMed, Embase and Cochrane Library, on 10 March 2021. RCT and Cohort studies in English or Scandinavian languages were included. Exposure variables included diet, lifestyle, meal patterns or physical activity. Studies using dietary supplements as exposure variables were excluded. Outcome variables included were DNA methylation, microRNA or histone changes in placenta, cord blood or offspring. Two independent authors screened, read and extracted data from the included papers. The Cochrane risk-of-bias tool for randomized trials (RoB2) and The Critical Appraisal Skills Program (CASP) Cohort Study Checklist were used to assess risk of bias in the included studies. A qualitative approach was employed due to heterogeneity of exposures and results of the studies. Results: 16 studies and 3617 participants were included in the final analysis. The exposure variables included physical activity, carbohydrate, low glycemic index diet, added sugar, fat, Mediterranean diet and pro-inflammatory diet. The outcome variables identified were differences in DNA methylation and microRNA. Most studies described epigenetic changes in either placenta or cord blood. Genes reported to be methylated were GR, HSD2, IGF-2, PLAG1, MEG-3, H19 and RXRA. However, not all studies found epigenetic changes strong enough to pass multiple testing, and the study quality varied. Conclusion: Despite the variable quality of the included studies, the results in this review suggest that there may be an association between the mother’s lifestyle, diet and level of physical activity during pregnancy and epigenetic changes in the offspring.

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Effects of Maternal Exercise During Pregnancy on Perinatal Growth and Childhood Obesity Outcomes: A Meta-analysis and Meta-regression

Cited by 40 publications

References 183 publications

Maternal exercise intergenerationally drives muscle-based thermogenesis via activation of apelin-AMPK signaling

Maternal exercise intergenerationally drives muscle-based thermogenesis via activation of apelin-AMPK signaling

Association between Olympic Games and children’s growth: evidence from China

The Impact of Lifestyle, Diet and Physical Activity on Epigenetic Changes in the Offspring—A Systematic Review

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