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Impact of Maternal Exercise during Pregnancy on Offspring Chronic Disease Susceptibility

Blaize, A. Nicole1; Pearson, Kevin J.2; Newcomer, Sean C.3

Exercise and Sport Sciences Reviews: October 2015 - Volume 43 - Issue 4 - p 198–203
doi: 10.1249/JES.0000000000000058
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Maternal behaviors during pregnancy have been reported to impact offspring health in adulthood. In this article we explore the novel hypothesis that exercise during pregnancy can protect against chronic disease susceptibility in the offspring. To date, research has demonstrated that improvements in metabolic outcomes, cardiovascular risk, and cancer can occur in response to maternal exercise during pregnancy.

This article explores the novel hypothesis that maternal exercise during pregnancy can protect against chronic disease susceptibility in the offspring.

1Department of Health and Kinesiology, Purdue University, West Lafayette, IN; 2Department of Pharmacology and Nutritional Sciences, College of Medicine, University of Kentucky, Lexington, KY; and 3Department of Kinesiology, California State University San Marcos, San Marcos, CA

Address for correspondence: Sean Newcomer, Ph.D., California State University San Marcos, 333 S. Twin Oaks Valley R. San Marcos, CA (E-mail: snewcomer@csusm.edu).

Accepted for publication: June 9, 2015.

Associate Editor: Benjamin F. Miller, Ph.D., FACSM

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INTRODUCTION

It is well established that maternal exercise during pregnancy has many beneficial health outcomes for mothers, such as improved fitness, a reduction of excessive weight gain, reduced risk for gestational diabetes, and better postpartum recovery (5). Based partly on these data, the American College of Obstetricians and Gynecologist (ACOG) recommends that pregnant women, free of complications, participate in at least 30 min of moderate-intensity exercise on most, if not all, days of the week (1). Similarly, the 2008 Physical Activity Guidelines from the Department of Health and Human Services (DHHS) recommend that healthy pregnant mothers perform at least 150 min of moderate-intensity aerobic activity per week during pregnancy and the postpartum period (32). Surprisingly, even in light of the countless data that support the safety and health benefits of maternal exercise during pregnancy, it has been reported that only 15% of women adhere to this recommendation (5).

Studies have indicated that pregnant mothers have the perception that physical activity during pregnancy can help control weight gain and glucose levels, maintain fitness, improve their energy and mood, ease labor, and improve infant health (19,26,31). However, women may not reach the recommendations for exercising during pregnancy because of feelings of discomfort, fatigue, illness, and lack of enjoyment while exercising (11,26). In addition, although women recognize the benefits of exercising during pregnancy, they rate rest and relaxation as more important than exercise during pregnancy (11,26). Although this review does not address ways to improve adherence to the exercise recommendations during pregnancy, it does provide more in-depth information on the impact exercise can have on offspring health during adolescence and adulthood. The goal is to explore the published literature examining the central hypothesis that maternal exercise during pregnancy can protect against chronic disease susceptibility in the offspring (Figure). Health care providers can use these data to encourage women to exercise during pregnancy. The influence of maternal exercise on offspring birth weight has been reported extensively elsewhere (26), so this review article will not cover birth weight or morphometric outcomes in the offspring.

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METABOLIC DISORDERS

Prior work has established a link between offspring low birth weight and type 2 diabetes mellitus (T2DM) risk later in life (17,33). Although considerable research has been conducted to examine the influence of negative maternal behaviors and offspring risk for T2DM, little attention has been given to positive maternal behaviors, such as exercise, during pregnancy. We hypothesized that maternal exercise during pregnancy would decrease offspring risk for T2DM later in life. Consistent with this hypothesis, our laboratory recently reported that maternal voluntary exercise in mice fed a normal diet positively influenced both male and female offspring glucose and insulin tolerance during adulthood (7). We also found that female rat offspring born to exercising dams had significantly improved insulin sensitivity (measured by hyperinsulinemic-euglycemic clamp) compared with those born to sedentary dams (8). Beneficial effects on insulin sensitivity are observed in mice and rats, which suggest that the findings are not species specific. Maternal exercise also may affect obesity outcomes in a sex-specific manner because body composition was affected significantly in male mouse offspring only. Male offspring from exercised dams showed decreased fat and increased lean mass percentages compared with offspring born to sedentary dams, but maternal exercise did not affect body composition significantly in female mouse or rat offspring (7,8). Unfortunately, male offspring insulin sensitivity and body composition were not measured as part of the rat study (8). We also have found that maternal exercise during pregnancy can increase insulin-stimulated glucose uptake in offspring skeletal muscle (mice and rats) and adipose tissue (mice) and decrease uptake in heart tissue (rats) compared with offspring born to sedentary dams (7,8). These data suggest that maternal exercise in normal chow-fed dams can improve metabolic outcomes in normal chow-fed offspring.

Adverse health outcomes and birth weight are now thought to form a U-shape relationship, with offspring born at low birth weights from undernourished mothers and high birth weights from overnourished mothers having the greatest risk for disease later in life (15). Recently, it was reported that rodent offspring from mothers who consumed a low-protein diet and exercised during pregnancy displayed improved growth and development and glucose homeostasis compared with offspring from mothers who consumed the low-protein diet and did not exercise (13). Data such as these suggest that maternal exercise can attenuate the effects of a maternal low-protein diet on metabolic outcomes in the offspring. With the growing incidence of women of reproductive age being classified as overweight or obese, it is important to determine if this has an impact on the metabolic changes observed in offspring from mothers who exercise. Research using obese pregnant rats has shown that maternal exercise helps improve offspring metabolism by increasing lean mass and decreasing fat mass percentage in male offspring (34). In addition, work in mice has shown that offspring from mothers who consume a high-fat diet, a known factor that can lead to obesity, demonstrated hypermethylation of a metabolic master regulator, peroxisome proliferator-activated receptor γ coactivator-1α (PGC-1α) (21). Although the offspring of mothers who consumed a high-fat diet and did not exercise had hypermethylation of PGC-1α, those exercising mothers fed the same diet produced offspring that did not have hypermethylated PGC-1α (21). These data indicate that maternal exercise during pregnancy can prevent metabolic dysregulation in the offspring that is associated with maternal high-fat diet consumption (21). Likewise, a recent study examined the impact of exercise during pregnancy on mouse offspring from dams that were fed either standard chow or a high-fat diet and further divided into four experimental subgroups: exercise trained before gestation only, exercise trained before and during gestation, exercise trained only during gestation, or sedentary before and during gestation (30). The offspring from mothers who were sedentary and consumed a high-fat diet had impaired glucose tolerance, increased serum insulin, and increased percentage body fat compared with the offspring from mothers who exercised before and during gestation (30). This indicates that maternal exercise before and during pregnancy can protect the offspring’s metabolic profile from the detrimental effects of a maternal high-fat diet. Therefore, maternal exercise during pregnancy helps break the endocrine cycle that promotes obesity and, instead, improves the offspring’s metabolic profile.

Not all studies have shown beneficial effects of maternal exercise on offspring glucose homeostasis. A recent report examined the effects of exercise ancestry on metabolic phenotypes in multiple generations of mouse offspring (16). The F0 generation mothers exercised during pregnancy, producing the F1 generation. Breeding of the F1 generation produced F2 offspring with either a sedentary or exercise ancestry (16). Glucose tolerance test results indicated that only the female F2 generation offspring were affected, with those offspring from an exercise ancestry displaying impaired glucose tolerance compared with their sedentary counterpart (16). Although these data do not fall in line with previous reports (7,8), it is important to note that the mouse offspring from Guth et al. (16) were only 8 wk old at the time of testing, whereas the offspring from other studies were 31 to 32 wk (7) or 10 months of age (8). This discrepancy in whether or not maternal exercise during pregnancy produces an improved glucose profile in the offspring points to a further need to examine offspring at varying ages and under additional metabolic stressors.

Most data suggest that maternal exercise during pregnancy positively impacts offspring metabolic health. Offspring from exercised mothers have improved insulin sensitivity, glucose handling, increased lean mass, and decreased fat mass compared with offspring from sedentary mothers (7,8). Interestingly, the improved metabolic profile of the offspring is not limited to those born to normal-weight healthy mothers but rather these improvements also can be seen in offspring from mothers who are undernourished or obese and exercise during pregnancy (13,21,30,33). These data can be used further to support the claim that exercise during pregnancy is safe for both mothers and their offspring.

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CARDIOVASCULAR DISEASE

Cardiovascular disease (CVD) was once thought of as a disease of the aging; however, reports have shown that atherosclerotic lesions can occur in infants, which suggests that the intrauterine environment may play a role in atherosclerosis disease risk (15). Therefore, we hypothesized that maternal exercise during pregnancy would result in decreased CVD risk in the offspring later in life. To this effect, recent research supports the notion that the prenatal environment can impact human fetal cardiovascular health (23–25). Data have shown that at 36 wk of gestation, maternal exercise during pregnancy lowers fetal heart rate (HR) and increases HR variability (HRV) (23). These results indicate a maturation of the central nervous system, specifically the autonomic nervous system (ANS) and brainstem, in response to maternal exercise during pregnancy. This is important because abnormalities in the ANS have been reported to promote the progression of atherosclerosis (20). The results from these initial studies suggested a protective effect of exercise during pregnancy against CVD development in the offspring. In the past, reports on the impact of maternal exercise during pregnancy listed that fetal hypoxia could occur because of the decreased blood flow to the placenta during the time course of exercise (29). However, the results of May et al. (23) suggest that this is not the case, as fetal hypoxia would lead to lower HRV. In addition, there is evidence for a dose-response relationship between maternal exercise and fetal cardiac ANS control, with women who engage in higher-intensity exercise having fetuses with lower resting HR and higher HRV (25). Regular moderate- to vigorous-intensity exercise is known to lower HR and improve cardiovascular well-being in adults. Therefore, these data suggest that exercise during pregnancy may be the earliest intervention to improve offspring cardiovascular health (23).

In response to the above data indicating that maternal exercise during pregnancy can impact cardiac ANS control in the offspring positively, our laboratory has used various animal models to examine the impact of exercise during pregnancy on offspring arterial function and atherosclerosis risk (2–4,27). Our first report on the impact of maternal exercise on swine offspring vascular health revealed phenotypic changes to the offspring’s vasculature (27). At birth, female offspring from treadmill exercise-trained mothers had significantly greater thoracic aorta endothelial cell function, as assessed through in vitro wire myography and cumulative doses of bradykinin, when compared with the male and female offspring from sedentary gilts (27). We speculated that these improvements in offspring vascular function might be linked to increases in fetal HR and subsequent increases in blood flow through the thoracic aorta, which could have increased the availability of nitric oxide (NO). It is well documented that increases in exercise blood flow cause frictional changes across the endothelium that increase NO bioavailability through the upregulation of endothelial NO synthase (22). These increases in fetal blood flow may be linked to reported increases in fetal HR during maternal exercise (10). The fact that the endothelium-dependent relaxation response was abolished when an NO inhibitor (L-NAME) was administered suggests that the increased relaxation response to bradykinin in the female exercise offspring was likely a result of increased NO bioavailability (27). These data indicate that maternal exercise during pregnancy may have an atheroprotective effect on the offspring at birth.

Although our first report indicated improvements in offspring vascular function in response to maternal exercise during pregnancy, we recently revealed that maternal exercise during pregnancy decreased endothelium-independent vascular function in adult swine offspring (2). This study used offspring from the same mothers and in vitro methodology as the Newcomer et al. (27) study but examined offspring’s femoral artery at ages 3, 5, and 9 months. The differences in vascular smooth muscle function between the exercise and sedentary offspring decreased with advancing age (2). Differential expression of genes and proteins associated with vascular tone between the exercise and sedentary offspring could explain the observed functional phenotype (2). To date, this is the first report to demonstrate that maternal exercise during pregnancy can induce vascular programming in adult offspring. However, it is important to note that the observed decreases in vascular smooth muscle function could be interpreted potentially as a negative phenotype for the offspring.

The disconnect between our laboratory-observed increase in endothelium-dependent vasorelaxation function at 48 h after birth in the swine exercise offspring and decreased endothelium-independent vasorelaxation function at 3, 5, and 9 months warranted further examination. Our previous studies were limited by the fact that we used healthy offspring that did not develop atherosclerosis. In addition, it was unclear if the vascular function differences seen in the thoracic and femoral arteries from our previous studies would be observed in the coronary arteries. Therefore, we recently examined the impact of maternal exercise during pregnancy on vascular function in swine offspring fed an atherogenic high-fat diet (4). We followed the same maternal exercise and in vitro vascular function procedures as our previous studies (2,27) and examined the left anterior descending (LAD) and femoral arteries of 4- and 8-month-old high-fat diet–fed swine offspring. Contrary to our previous reports, there were no significant differences in offspring coronary or femoral artery endothelium-dependent or endothelium-independent vascular function at 4 or 8 months of age.

The majority of research conducted by our laboratory to examine the impact of maternal exercise during pregnancy on offspring vascular health has used a swine model because of the similarities of the swine cardiovascular system to a human (2,4,27). Although swine may be an ideal model for studying CVD, fetal programming work has commonly used rodents because of placental similarities to humans, short gestation lengths, and their ability to generate large sample sizes (3). Therefore, we examined the impact of maternal voluntary wheel running during pregnancy on rodent offspring vascular function at 4 and 8 months of age (3). Similar to our last study using a swine model, we found no differences in endothelium-independent or endothelium-dependent relaxation between offspring from exercise and sedentary mothers. One can speculate that the differences observed between our rat and pig studies may be influenced by dissimilarities in species and experimental design. Specifically, the two models have dramatically different types of placentation, gestational lengths, and different states of offspring maturity at birth. Furthermore, the lack of differences in vascular function between the offspring from exercise and sedentary mothers in the rodent study also could be a result of the exercise intensity. In our previous study using swine, the mothers were forced to exercise on a treadmill 5 d wk-1 at an intensity of 65% to 85% of maximal HR (2,27). In the rodent study, the exercise dams had free access to a running wheel throughout gestation. Because the exercise protocol was voluntary, it is possible that the dams did not meet the exercise intensity required for vascular programming.

Although the existing data have some variations, most of the literature support the notion that exercise during pregnancy positively influences or does not impact offspring cardiovascular health. Mothers who exercise during pregnancy have produced offspring with a lower resting HR, a higher HRV, and an improved vascular health. In line with previous areas of research, this work mostly supports the view that exercise during pregnancy is beneficial for both mother and offspring.

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CANCER

Physical activity in adolescents and adults plays a pivotal role in the prevention of chronic diseases, including cancer (14). Although there has been an increasing body of literature examining maternal exercise during pregnancy and risk for chronic diseases in the offspring in recent years, only one study to date has explored the risk of cancer development. Maternal high-methyl diet consumption during pregnancy has been shown to suppress mammary carcinogenesis in female rat offspring (9). This evidence indicates a link between maternal behaviors and reduced mammary cancer risk in the offspring. Data such as these led us to investigate the impact that maternal exercise during pregnancy had on offspring mammary cancer development. We hypothesized that maternal exercise during pregnancy would decrease the risk of breast cancer in the offspring. Female rats were divided into two experimental groups during pregnancy: sedentary and voluntary wheel exercise (6). After weaning, female offspring from both sedentary and exercise mothers were fed a high-fat diet. All of the pups were injected with the carcinogen N-methyl-N-nitrosourea at 6 wk of age. Mammary tumor development in all pups was monitored for 15 wk. These data revealed that offspring from mothers who exercise during pregnancy have a mammary tumor incidence of 42.9% compared with 100% incidence in sedentary offspring (6). Therefore, these preliminary data suggest that maternal exercise can reduce offspring mammary cancer risk (6). Camarillo et al. (6) hypothesized that maternal metabolism or factors released into the maternal circulation in response to exercise could lead to programming changes in the offspring; however, there currently are no data to support this claim. Future work should seek to elucidate the mechanisms by which protective effects of maternal exercise during pregnancy on offspring breast cancer risk occur.

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FUTURE DIRECTIONS

The area of research examining maternal exercise during pregnancy and offspring chronic disease progression is growing. Although the work that has been completed to date has answered a number of questions, there are still areas that need to be explored. Specifically, there are many unknowns about how the type, timing, intensity, and dose (i.e., amount) of maternal exercise during pregnancy may impact offspring chronic disease risk later in life. In addition, future work should explore mechanisms by which any changes in the offspring are occurring in response to maternal exercise during pregnancy.

The majority of research to date examining the impact of maternal exercise during pregnancy on long-term health outcomes in offspring has used some form of aerobic exercise (i.e., human aerobic trained, rodent treadmill or wheel running, or swine treadmill exercise). Future work needs to use different modes of exercise to determine whether the metabolic, cancer, and CVD risk in the offspring is changed based on varying types of exercise. A number of studies exploring the impact of maternal resistance training during pregnancy have been published in recent years; however, they have focused on maternal and/or perinatal outcomes (28,35). Therefore, randomized controlled trial studies examining the impact of maternal resistance training on chronic disease outcomes in the offspring would be an important addition to the literature. In addition, the research to date has not used a specific intensity or amount of exercise during pregnancy when examining offspring chronic disease risk outcomes (Table). For instance, some studies use animal models that allow dams to exercise voluntarily on a running wheel, whereas others force dams to exercise, thus controlling the amount, duration, and intensity of exercise. Future research should continue to explore the impact of exercise modality, intensity, and dose of exercise during pregnancy on offspring chronic disease risk.

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Timing of exercise during pregnancy also needs to be considered in future fetal programming studies. The published work to date has not exposed pregnant mothers to exercise for the same duration during pregnancy. Although some studies have only allowed mothers to exercise during the finite duration of gestation, other studies have allowed exercise before, during, and after pregnancy. For example, recent work examining the impact of exercise during pregnancy on offspring metabolic health used an experimental design where pregnant dams exercised during different time points of pregnancy (30). The data indicated that there were differences in metabolic health outcomes between offspring from the various experimental maternal exercise groups. Therefore, future work should explore the impact of the timing of exercise during pregnancy on offspring chronic disease risk.

As stated previously, the use of animal models is common in fetal programming research. The data from studies using animal models have provided an important foundation for the field. However, future work needs to focus on experimental designs that can determine if the offspring health changes that have been identified in animal models are translated to humans. Particularly, researchers should explore the mechanisms by which these phenotypes occur in the offspring in response to maternal exercise during pregnancy. Researchers have predicted that these phenotypes are attributed to epigenetic alterations, but there has only been one study demonstrating that maternal exercise during pregnancy causes DNA methylation or histone modifications in the offspring (18). Furthermore, if these phenotypes are produced by epigenetic alterations, studies should explore what specifically about maternal exercise causes these changes.

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CONCLUSIONS

In general, research examining the impact of maternal exercise during pregnancy on offspring chronic disease risk has been positive. Although there have been a few reports of detrimental health outcomes in the offspring in response to maternal exercise during pregnancy, the vast majority has shown improvements in offspring metabolic, cancer, and cardiovascular health and disease risk. Thus, overall, the current body of work supports the recommendations for exercise during pregnancy set by the ACOG and DHHS. Health care providers can use these data to educate pregnant mothers on the benefits of exercise during pregnancy for their offspring and encourage them to incorporate exercise into their prenatal care.

K.J. Pearson was supported by a US National Institutes of Health grant from The National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK090460), and S.C. Newcomer was supported by an American Heart Association grant (no. 12SDG85400001).

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References

1. ACOG Committee Obstetric Practice. ACOG Committee opinion no. 267, January 2002: exercise during pregnancy and the postpartum period. Obstet. Gynecol. 2002; 99(1): 171–3.
2. Bahls M, Sheldon RD, Taheripour P, et al. Mother’s exercise during pregnancy programmes vasomotor function in adult offspring. Exp. Physiol. 2014; 99(1): 205–19.
3. Blaize A. Nicole, Breslin E, Donkin SS, Cabot R, Pearson KJ, Newcomer SC. Maternal exercise does not significantly alter adult rat offspring vascular function. Med. Sci. Sports Exerc. 2015; 47(11): 00.
4. Blaize A. Nicole, Zartman E, Biel T, et al. Impact of maternal exercise during pregnancy on arterial function and atherosclerosis formation in swine offspring fed a high-fat diet. Enliven: Gynecol. Obestet. 2015; 1(1): 5–15.
5. Borodulin KM, Evenson KR, Wen F, Herring AH, Benson AM. Physical activity patterns during pregnancy. Med. Sci. Sports Exerc. 2008; 40(11): 1901–8.
6. Camarillo IG, Clah L, Zheng W, et al. Maternal exercise during pregnancy reduces risk of mammary tumorigenesis in rat offspring. Eur. J. Cancer Prev. 2014; 23(6): 502–5.
7. Carter LG, Lewis KN, Wilkerson DC, et al. Perinatal exercise improves glucose homeostasis in adult offspring. Am. J. Physiol. Endocrinol. Metab. 2012; 303(8): E1061–8.
8. Carter LG, Qi NR, De Cabo R, Pearson KJ. Maternal exercise improves insulin sensitivity in mature rat offspring. Med. Sci. Sports Exerc. 2013; 45(5): 832–40.
9. Cho K, Mabasa L, Bae S, Walters MW, Park CS. Maternal high-methyl diet suppresses mammary carcinogenesis in female rat offspring. Carcinogenesis. 2012; 33(5): 1106–12.
10. Clapp JF 3rd. The effects of maternal exercise on fetal oxygenation and feto-placental growth. Eur. J. Obstet. Gynecol. Reprod. Biol. 2003; 110(Suppl. 1): S80–5.
11. Clarke PE, Gross H. Women’s behaviour, beliefs and information sources about physical exercise in pregnancy. Midwifery. 2004; 20(2): 133–41.
12. Evenson KR, Moos MS, Carrie K, Siega-Riz AM. Perceived barriers to physical activity among pregnant women. Matern. Child Health J. 2009; 13: 364–75.
13. Fidalgo M, Falcão-Tebas F, Bento-Santos A, et al. Programmed changes in the adult rat offspring caused by maternal protein restriction during gestation and lactation are attenuated by maternal moderate-low physical training. Br. J. Nutr. 2013; 109(3): 449–56.
14. Friedenreich CM, Courneya KS, Bryant HE. Influence of physical activity in different age and life periods on the risk of breast cancer. Epidemiology. 2001; 12(6): 604–12.
15. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 2008; 359(1): 61–73.
16. Guth LM, Ludlow AT, Witkowski S, et al. Sex-specific effects of exercise ancestry on metabolic, morphological and gene expression phenotypes in multiple generations of mouse offspring. Exp. Physiol. 2013; 98(10): 1469–84.
17. Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35(7): 595–601.
18. Hanson MA, Gluckman PD. Developmental origins of health and disease: new insights. Basic Clin. Pharmacol. Toxicol. 2008; 102(2): 90–3.
19. Krans EE, Gearhart JG, Dubbert PM, Klar PM, Miller AL, Replogle WH. Pregnant women’s beliefs and influences regarding exercise during pregnancy. J. Miss. State Med. Assoc. 2005; 46: 67–73.
20. Huikuri HV, Jokinen V, Syvänne M, et al. Heart rate variability and progression of coronary atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 1999; 19(8): 1979–85.
21. Laker RC, Lillard TS, Okutsu M, et al. Exercise prevents maternal high-fat diet–induced hypermethylation of the Pgc-1α gene and age-dependent metabolic dysfunction in the offspring. Diabetes. 2014; 63(5): 1605–11.
22. Laughlin MH, Newcomer SC, Bender SB. Importance of hemodynamic forces as signals for exercise-induced changes in endothelial cell phenotype. J. Appl. Physiol. (1985). 2008; 104(3): 588–600.
23. May LE, Glaros A, Yeh HW, Clapp JF 3rd, Gustafson KM. Aerobic exercise during pregnancy influences fetal cardiac autonomic control of heart rate and heart rate variability. Early Hum. Dev. 2010; 86(4): 213–7.
24. May LE, Scholtz SA, Suminski R, Gustafson KM. Aerobic exercise during pregnancy influences infant heart rate variability at one month of age. Early Hum. Dev. 2014; 90(1): 33–8.
25. May LE, Suminski RR, Langaker MD, Yeh HW, Gustafson KM. Regular maternal exercise dose and fetal heart outcome. Med. Sci. Sports Exerc. 2012; 44(7): 1252–8.
26. Mudd LM, Nechuta S, Pivarnik JM, Paneth N; Michigan Alliance for National Children’s Study. Factors associated with women’s perceptions of physical activity safety during pregnancy. Prev. Med. 2009; 49(2–3): 194–9.
27. Newcomer SC, Taheripour P, Bahls M, et al. Impact of porcine maternal aerobic exercise training during pregnancy on endothelial cell function of offspring at birth. J. Dev. Orig. Health Dis. 2012; 3(1): 4–9.
28. Petrov Fieril K, Glantz A, Fagevik Olsen M. The efficacy of moderate-to-vigorous resistance exercise during pregnancy: a randomized controlled trial. Acta Obstet. Gynecol. Scand. 2015; 94(1): 35–42.
29. Pivarnik JM, Chambliss HO, Clapp JF, et al. Impact of physical activity during pregnancy and postpartum on chronic disease risk. Med. Sci. Sports Exerc. 2006; 38(5): 989–1006.
30. Stanford KI, Lee MY, Getchell KM, So K, Hirshman MF, Goodyear LJ. Exercise before and during pregnancy prevents the deleterious effects of maternal high-fat feeding on metabolic health of male offspring. Diabetes. 2015; 64(2): 427–33.
31. Symons Downs D, Hausenblas HA. Women’s exercise beliefs and behaviors during their pregnancy and postpartum. J. Midwifery Womens Health. 2004; 49(2): 138–44.
32. US Department of Health and Human Services. Physical Activity Guidelines for Americans. Washington: HHS; 2008.
33. Vaag AA, Grunnet LG, Arora GP, Brøns C. The thrifty phenotype hypothesis revisited. Diabetologia. 2012; 55(8): 2085–8.
34. Vega CC, Reyes-Castro LA, Bautista CJ, Larrea F, Nathanielsz PW, Zambrano E. Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. Int. J. Obes. (Lond). 2015; 39(4): 712–9.
35. White E, Pivarnik J, Pfeiffer K. Resistance training during pregnancy and perinatal outcomes. J. Phys. Act. Health. 2014; 11(6): 1141–8.
Keywords:

exercise; pregnancy; offspring; cardiovascular disease; diabetes; cancer

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