Abstract
Research has continued to demonstrate that exercise during pregnancy is safe. Growing evidence supports that exercise during pregnancy is beneficial for mother and fetus during gestation, with benefits persisting for the child into adulthood. Regardless of income or socioeconomic status, exercise during pregnancy is associated with increased incidence of full-term delivery. Additionally, normalization of birth measures, such as birth weight, occurs when women perform regular exercise throughout gestation. Measures of growth and development further indicate that exercise during pregnancy does not harm and may stimulate healthy growth throughout childhood. Measures of cognition and intelligence demonstrate that exercise during pregnancy causes no harm and may be beneficial. Overall, the benefits of exercise during pregnancy decrease the risk of chronic disease for both mother and child.
Keywords: pregnancy, childhood, physical activity/exercise, health outcomes
Introduction
In 2014, 41 million children were reported to be overweight or obese.1 Being overweight or obese increases the risk of developing type 2 diabetes mellitus and cardiovascular disease (CVD).2–4 In part, the increased prevalence of obesity, overweight, and diabetes is due to negative lifestyle habits (ie, physical inactivity, diet lacking fruits and vegetables).3,4 Therefore, positive lifestyle habits (ie, physical activity) may act as a nonpharmaceutical therapy for obesity and overweight, thus delaying or preventing the onset of type 2 diabetes and CVD. Numerous physical activity interventions are being done to treat and prevent these conditions in children; however, the earliest intervention to treat these conditions is during pregnancy.
Reports state that over half of pregnant women in the US and Norway and 85% in Canada participate in physical activity during pregnancy.5–8 Women who exercise throughout gestation show significantly decreased risk of preeclampsia, hypertension, gestational diabetes mellitus (GDM), weight gain, rate of spontaneous abortion, congenital abnormalities, and incidence of preterm labor, and offspring have normal growth and development.9–16 The developmental origins hypothesis states that the in utero environment influences, or programs, fetal organ development, which has implications for the infants after birth into adulthood.17 Since there is a growing body of evidence supporting the safety and efficacy of maternal exercise for the offspring, this article provides a review of human studies related to physical health of offspring exposed to maternal exercise throughout gestation and the risk of developing diseases later, such as GDM.
Gestational Age at Birth
Some research suggests that women who exercise may be more likely to deliver closer to the estimated due date.14,18–20 Although there are many studies that have compared gestational age between groups of women who exercise or not during pregnancy, most exercise was below the current recommended guidelines. The current guidelines of many nations suggest that pregnant women participate in at least 150 minutes per week of moderate-intensity aerobic activity.21–26 Three intervention studies have met the current guidelines for the frequency, intensity, and duration of exercise throughout pregnancy, two of which found no differences in gestational age between exercise and control groups.27,28 Furthermore, one study utilized aerobic activity only28 and two studies used aerobic with resistance27,29 exercise to meet the guidelines. One of these studies found no difference in gestational age between women participating in varying intensity levels (below and at recommended guidelines) of exercise relative to controls.29 A similar study using self-reported data found no difference in gestational age at birth between high-intensity (met guidelines), low-intensity (below guidelines), and control groups.30 Of the high-quality studies, evidence suggests that exercise, regardless of amount or intensity, does not influence the length of gestation.
In conjunction with these findings, other studies suggest that this pattern may be different for low-income minorities. Several studies have observed that women of low socioeconomic status (SES) are less likely to seek prenatal care services31 and have a positive association with preterm birth and work activity (walking and stair climbing).32 However, pregnant women of minority ethnicity in low SES who participate in leisure-time exercise have decreased risk of preterm birth.32–34 Another study found that moderate-intensity exercise at least 30 minutes per day in low-income African American (AA) women was associated with decreased preterm births.35 Similar to other study populations, pregnancy outcomes for women in low income/low SES associated with the necessity of walking to work or climbing stairs show increased adverse outcomes, while choosing to walk for health is associated with positive outcomes. These data should be interpreted with caution since the exercise data are self-reported and were either below the current recommended guidelines or not reported.
Birth Measures
Numerous studies have found that exercise during pregnancy, whether acute or chronic, is not harmful to the fetus and may benefit development in utero and after birth.36 The primary measures to assess proper growth at birth are weight, length, and circumference measures.
Birth weight, in general, may show increase,19,20,37,38 decrease,39–43 or no change28,37,44–47 in response to exercise during pregnancy. To control for some variables, we focused on those studies that used exercise throughout pregnancy at the current recommended level, which left six studies to be reviewed on this topic. Of these six studies, two found increased,20,37 three found decreased,40,42,43 and one found no differences28 in birth weight associated with maternal exercise. One of the studies reporting an increased birth weight, within normal weight ranges, also reports increased lean body mass and decreased fat mass40 in exercise-exposed infants relative to infants of nonexercisers. The two studies that reported increased birth weight, within normal weight ranges, found a dose response, such that higher levels of intensity in the final weeks of pregnancy are associated with lower birth weights, while lower levels of intensity are associated with higher birth weights.20,37 Additionally, one study observed that higher levels of physical activity (above the recommended guidelines of 30 or more minutes, most, if not all, days of the week) protected against both large and small for gestational age infants.48–51 This parabolic relationship between infant birth weight and chronic disease morbidity later in life is of current research interest, such that small infants have an increased risk of developing CVD, type 2 diabetes, metabolic syndrome, and hypertension,52,53 while heavier infants are at an increased risk of developing obesity and type 2 diabetes.52–54 Finally, the one article that reports no difference in birth weight, regardless of exercise during pregnancy or not, is the only randomized control trial that had an exercise intervention throughout pregnancy at the recommended level of exercise, while all other articles utilized self-reported exercise. Altogether, these findings suggest that birth weight may be normalized by exercise during pregnancy; however, there are many other confounding factors of this crude measure of fetal growth.55
In light of the fact that newborn birth weights have increased across generations, other factors related to health disparities of women may influence fetal growth as evidenced by birth weight.54 Two large population-based cohort studies suggest that birth weight is determined mainly by non-exercise variables, such as maternal body composition, diet, uteroplacental blood flow, placental transfer of nutrients, and fetal genetics, with the influence of maternal exercise being minimal.48,56–58 These findings are supported by studies examining the influence of racial/ethnic group and physical activity on birth weight. One study examining the relationship of exercise activity in urban, low-income AA women found no association with exercise participation and low birth weight.33,34 Another study found that urban AA women have a positive association between exercise and birth weight.59 Other research found that physical activity did not influence birth weight, but when controlling for maternal age, nationality, SES, substance use, and prenatal care, AAs were two times more likely to have low birth weight infants relative to whites.60 However, when controlling for confounding variables, neither physical activity nor race/ethnicity influenced macrosomia, but maternal body mass index (BMI) was the main factor.60 Despite attempts to decrease macrosomia in some populations, its occurrence is often due to cultural shifts.61 Overall, these findings suggest that maternal exercise does not adversely influence birth weight.
Body morphometry (ie, circumferences) at birth can also be utilized as an indicator of fetal growth during gestation. In general, studies report similar morphometric parameters for newborns of both active and nonactive pregnant women. No differences are found in birth length of babies exposed or not exposed to gestational exercise.40,62–65 Three of these studies met the current guidelines for exercise level.40,48,65 One study found no differences in measurements of neonatal head circumference, abdominal circumference, and ponderal index, regardless of maternal exercise exposure, but also utilized self-reported exercise level.40 A large Danish cohort study, using self-reported exercise level, found no differences in neonatal measures related to maternal exercise; however, they reported trends of decreasing birth length with increasing maternal exercise when controlling for confounding variables such as maternal BMI, age, and smoking (more common in lower income individuals).48 The third study utilized an exercise intervention in physically active women, and despite lower energy intakes than recommended (ie, iron, dairy), birth measures were within normal ranges.65 Overall, data suggest that maternal exercise does not adversely influence offspring growth measures.
Postnatal Measures
Although birth data are the most available and easiest to acquire, it does not provide a complete picture of changes that influence development after birth.66 Studies are currently underway regarding the continued growth and development of children exposed to exercise in utero. At one year of age, there are no differences in growth measures (ie, height, weight, head circumference, chest circumference, abdominal circumference) between children exposed or not exposed to exercise in utero.15,16 Similarly, there are no differences in height and circumferences (arm, head, chest, abdominal) at five years of age, regardless of exercise exposure in utero.67 A follow-up of children at five years of age found no differences in some measures of growth (ie, head and chest circumference); however, children exposed to exercise in utero weight less and had less fat mass relative to children from women who did not exercise while pregnant.67 Current research is analyzing associations between body weight and fat in prepubertal children and associated factors in an effort to determine intrauterine programming toward or away from disease risk. One study finds, after adjusting for the child’s BMI, age, sex, current physical activity level, and SES, that birth weight is a better predictor of percent body fat and height during childhood and adolescence compared to parental morphometrics.68 These findings support the idea that prepubertal body morphometric measures are programmed in utero.
Various measures have been used to determine off-spring heart and nervous system health and development. For example, heart rate (HR) and HR variability, beat-to-beat fluctuation demonstrating cardiac autonomic nervous system maturation, are used during and after pregnancy to determine appropriate development of the fetus. Similar to an adult who is exercised trained, May et al69,70 found that exercise throughout gestation is associated with lower fetal HR and increased fetal HR variability that persists after birth. Further analysis demonstrated a dose–response relationship between maternal exercise intensity, or time, and offspring cardiac autonomic adaptation.71,72 It is important to note that the upper limit of maternal exercise was not tested in these studies; all participants trained in the moderate to vigorous range as recommended by the American Congress of Obstetricians of Gynecologists.21 The differences in cardiac autonomic regulation are attributed to exercise exposure in utero since no other variables (ie, maternal age, maternal BMI, maternal education, etc.) are significantly associated with these findings.69,70 In addition, children exposed to exercise in utero exhibited no evidence of CVD into adulthood.73 The persistence of healthy heart measures of offspring through childhood into adulthood supports the premise of prenatal programming.17,74
Other studies have used measures of neuromotor, cognition, and intelligence to determine if neurodevelopment is improved in offspring due to maternal exercise exposure. Overall, findings have been positive (Table 1) with most measurement tools: Brazelton scale, a measure of neonatal behavioral responses and neurodevelopment;75 neurophysiological brain potentials;76 intelligence quotient (IQ);77 and Wechsler test scales.67 Two studies showed equivalent cognition between exercise-exposed and nonexercise-exposed children, and both utilized the Bayley Scales of Infant Development, which assesses neonatal cognitive, motor, and behavioral development.16,78 Cognition, however, has been found to be associated with SES, mediated by environmental factors.79 Furthermore, research shows that more education and higher SES are associated with exercise during pregnancy.5,80–86 Similar to the exercise and pregnancy studies, other studies have found that the fetus or children with slower HR and increased HR variability are associated with positive psychomotor and language developmental outcomes at 8 and 12 months of age,87 2 years of age,36 and 3 years of age36 and have faster reaction times and attention during a task88,89 than children of similar age. Altogether, these findings support that exercise while pregnant may be beneficial to cardiac and neuromotor development of offspring.
Table 1.
REFERENCES | INFANT AGE | OUTCOME MEASURE | SUMMARY |
---|---|---|---|
Clapp et al 199975 | 5-day olds | Brazelton scores | =/+ |
LeMoyne et al 201276 | 8–12 day olds | Neurophysiology brain potentials (EEG) | + |
Clapp et al 199816 | 1-year olds | Bayley scores | = |
Hellenes et al 201578 | 1.5 year olds | Bayley scores | = |
Domingues et al 201477 | 1, 2, and 4 year olds | IQ scores | + |
Clapp 199667 | 5 year olds | Wechsler scores (and language scores) | + |
Pivarnik et al 200673 | 8–12 years old | Academic, coordination, balance, strength, speed and endurance | + |
Pivarnik et al 200673 | 17–20 years old | Academic and sports performance | + |
Abbreviations: EEG, electroencephalography; +, statistically significant increase; =, no statistical differences.
Gestational Diabetes
Being overweight or obese can lead to development of type 2 diabetes.3,4,90 Baeten et al91 observed that one-third of women of reproductive age are overweight. This condition during pregnancy is similar to the nonpregnant state10 and increases the risk of developing GDM. GDM is defined as the onset or first recognition of diabetes during pregnancy and is related to adverse maternal and neonatal health outcomes.92,93 Women with GDM and borderline GDM have increased risk of negative long-term effects on maternal and neonatal health.10,94 Gestational diabetic women and borderline GDM93 have an increased risk of perinatal complications such as preeclampsia,93 C-section, and induced delivery.68 A recent study of primiparous women observed that GDM diagnoses were greater among women in lower SES levels.95 They also found that the incidence of GDM was increased in women older than 35 years of age, with a greater incidence in those falling in lower SES levels. However, younger women had similar GDM incidence rates across all SES levels. Furthermore, the incidence of GDM was greatest in women of Asian background who were older and fell within the lowest levels of SES.95 GDM also increases the risk of maternal development of type 2 diabetes, with 40% of GDM pregnancies diagnosed with type 2 diabetes postpartum.93 Diabetes, or borderline diabetes, during gestation affects the intrauterine environment. At delivery, there are complications, such as macrosomia, shoulder dystocia, neonatal hypoglycemia, and hyperbilirubinemia.68,93 It has been suggested that GDM could affect the intrauterine environment, increasing the genetic risk of developing childhood obesity and/or type 2 diabetes in adulthood.93
Physical activity during pregnancy, however, decreases the risk and incidence of GDM, in part by decreasing excessive gestational weight gain and stimulating a better control of glucose metabolism.92 This phenomenon is also true for high-risk groups such as women who are overweight or obese prior to pregnancy, especially those who are inactive. Physical activity starting at the beginning of pregnancy can be used as an early therapy to prevent excessive weight gain and GDM. Women who develop GDM during pregnancy can utilize physical activity as an adjunctive therapy and are able to decrease their insulin therapy and thus have better metabolic control compared to sedentary pregnant women.42
Conclusion
Evidence continues to grow in support of the notion that exercise during pregnancy is beneficial for fetal health and well-being, extending into childhood. Benefits for offspring are observable related to body weight and composition, cardiovascular health, and nervous system development. Exercise during pregnancy may elicit a prenatal programming effect, creating a healthy environment in utero during a critical time of organ development. Women of various SES and BMI can adopt healthy lifestyle behaviors that can positively impact postnatal health and decrease their child’s risk of developing chronic diseases such as obesity, diabetes, and CVD.
Footnotes
ACADEMIC EDITOR: Nicole Powell-Dunford, Editor in Chief
PEER REVIEW: Five peer reviewers contributed to the peer review report. Reviewers’ reports totaled 1327 words, excluding any confidential comments to the academic editor.
FUNDING: We would like to thank East Carolina University for their internal funds to support the continued work in the area of exercise and pregnancy. The authors confirm that the funder had no influence over the study design, content of the article, or selection of this journal.
COMPETING INTERESTS: Authors disclose no potential conflicts of interest.
Paper subject to independent expert single-blind peer review. All editorial decisions made by independent academic editor. Upon submission manuscript was subject to anti-plagiarism scanning. Prior to publication all authors have given signed confirmation of agreement to article publication and compliance with all applicable ethical and legal requirements, including the accuracy of author and contributor information, disclosure of competing interests and funding sources, compliance with ethical requirements relating to human and animal study participants, and compliance with any copyright requirements of third parties. This journal is a member of the Committee on Publication Ethics (COPE).
Author Contributions
Conceived and designed the experiments: LM, CM. Analyzed the data: LM, CM, ORR. Wrote the first draft of the manuscript: LM, CM. Contributed to the writing of the manuscript: LM, CM, ORR. Agree with manuscript results and conclusions: LM, CM, ORR. Jointly developed the structure and arguments for the paper: LM, CM, ORR. Made critical revisions and approved final version: LM, CM, ORR. All authors reviewed and approved of the final manuscript.
REFERENCES
- 1.Organization WH . Obesity and overweight. WHO Fact Sheets [webpage]; 2016. [Accessed July 7, 2016]. Available at: http://www.who.int/mediacentre/factsheets/fs311/en/ [Google Scholar]
- 2.Association AD Overweight. Lower Your Risk. 2014. [Accessed April 20, 2016]. Available at: http://www.diabetes.org/are-you-at-risk/lower-your-risk/overweight.html?loc=atrisk-slabnav.
- 3.Koo BK, Moon MK. Are we in the same risk of diabetes mellitus? Gender- and age-specific epidemiology of diabetes in 2001 to 2014 in the Korean population. Diabetes Metab J. 2016;40(3):175–181. doi: 10.4093/dmj.2016.40.3.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Society O Your Weight and Diabetes. 2015. [Accessed April 20, 2016]. Available at: http://www.obesity.org/content/weight-diabetes.
- 5.Evenson KR, Savitz DA, Huston SL. Leisure-time physical activity among pregnant women in the US. Paediatr Perinat Epidemiol. 2004;18(6):400–407. doi: 10.1111/j.1365-3016.2004.00595.x. [DOI] [PubMed] [Google Scholar]
- 6.Evenson KR, Wen F. Measuring physical activity among pregnant women using a structured one-week recall questionnaire: evidence for validity and reliability. Int J Behav Nutr Phys Act. 2010;7:21. doi: 10.1186/1479-5868-7-21. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Gaston A, Vamos CA. Leisure-time physical activity patterns and correlates among pregnant women in Ontario, Canada. Matern Child Health J. 2013;17(3):477–484. doi: 10.1007/s10995-012-1021-z. [DOI] [PubMed] [Google Scholar]
- 8.Owe KM, Nystad W, Bo K. Correlates of regular exercise during pregnancy: the Norwegian Mother and Child Cohort Study. Scand J Med Sci Sports. 2009;19(5):637–645. doi: 10.1111/j.1600-0838.2008.00840.x. [DOI] [PubMed] [Google Scholar]
- 9.Collings CA, Curet LB, Mullin JP. Maternal and fetal responses to a maternal aerobic exercise program. Am J Obstet Gynecol. 1983;145(6):702–707. doi: 10.1016/0002-9378(83)90576-8. [DOI] [PubMed] [Google Scholar]
- 10.Dye TD, Knox KL, Artal R, Aubry RH, Wojtowycz MA. Physical activity, obesity, and diabetes in pregnancy. Am J Epidemiol. 1997;146(11):961–965. doi: 10.1093/oxfordjournals.aje.a009223. [DOI] [PubMed] [Google Scholar]
- 11.Marcoux S, Brisson J, Fabia J. The effect of leisure time physical activity on the risk of pre-eclampsia and gestational hypertension. J Epidemiol Community Health. 1989;43(2):147–152. doi: 10.1136/jech.43.2.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Mudd LM, Owe KM, Mottola MF, Pivarnik JM. Health benefits of physical activity during pregnancy: an international perspective. Med Sci Sports Exerc. 2013;45(2):268–277. doi: 10.1249/MSS.0b013e31826cebcb. [DOI] [PubMed] [Google Scholar]
- 13.Dempsey JC, Butler CL, Sorensen TK, et al. A case-control study of maternal recreational physical activity and risk of gestational diabetes mellitus. Diabetes Res Clin Pract. 2004;66(2):203–215. doi: 10.1016/j.diabres.2004.03.010. [DOI] [PubMed] [Google Scholar]
- 14.Clapp JF., III Exercise during pregnancy. A clinical update. Clin Sports Med. 2000;19(2):273–286. doi: 10.1016/s0278-5919(05)70203-9. [DOI] [PubMed] [Google Scholar]
- 15.Clapp JF., III Exercise and fetal health. J Dev Physiol. 1991;15(1):9–14. [PubMed] [Google Scholar]
- 16.Clapp JF, III, Simonian S, Lopez B, Appleby-Wineberg S, Harcar-Sevcik R. The one-year morphometric and neurodevelopmental outcome of the offspring of women who continued to exercise regularly throughout pregnancy. Am J Obstet Gynecol. 1998;178(3):594–599. doi: 10.1016/s0002-9378(98)70444-2. [DOI] [PubMed] [Google Scholar]
- 17.Barker DJ. Intrauterine programming of coronary heart disease and stroke. Acta Paediatr Suppl. 1997;423:178–182. doi: 10.1111/j.1651-2227.1997.tb18408.x. discussion 183. [DOI] [PubMed] [Google Scholar]
- 18.Clapp JF., III The effect of continuing regular endurance exercise on the physiologic adaptations to pregnancy and pregnancy outcome. Am J Sports Med. 1996;24(6 suppl):S28–S29. [PubMed] [Google Scholar]
- 19.Clapp JF, III, Kim H, Burciu B, Lopez B. Beginning regular exercise in early pregnancy: effect on fetoplacental growth. Am J Obstet Gynecol. 2000;183(6):1484–1488. doi: 10.1067/mob.2000.107096. [DOI] [PubMed] [Google Scholar]
- 20.Clapp JF, III, Kim H, Burciu B, Schmidt S, Petry K, Lopez B. Continuing regular exercise during pregnancy: effect of exercise volume on fetoplacental growth. Am J Obstet Gynecol. 2002;186(1):142–147. doi: 10.1067/mob.2002.119109. [DOI] [PubMed] [Google Scholar]
- 21.ACOG Committee Obstetric Practice ACOG Committee opinion. Number 267, January 2002: exercise during pregnancy and the postpartum period. Obstet Gynecol. 2002;99(1):171–173. doi: 10.1016/s0029-7844(01)01749-5. [DOI] [PubMed] [Google Scholar]
- 22.SMA statement the benefits and risks of exercise during pregnancy. Sport Medicine Australia. J Sci Med Sport. 2002;5(1):11–19. doi: 10.1016/s1440-2440(02)80293-6. [DOI] [PubMed] [Google Scholar]
- 23.Davies GA, Wolfe LA, Mottola MF, MacKinnon C. Society of O, gynecologists of Canada SCPOC. Joint SOGC/CSEP clinical practice guideline: exercise in pregnancy and the postpartum period. Can J Appl Physiol. 2003;28(3):330–341. [PubMed] [Google Scholar]
- 24.Authority DH Recommendations for Pregnant Women. Health and Lifestyle: Pregnancy. 2014. [Accessed August 1, 2016]. Available at: http://sundhedsstyrelsen.dk/en/health-and-lifestyle/physical-activity/recommendations/pregnant-women.
- 25.Gynaecologists RCoOa Exercise in Pregnancy. Royal College of Obstetricians and Gynaecologists Statements. 2006. [Accessed August 1, 2016]. Available at: https://www.rcog.org.uk/global-assets/documents/guidelines/statements/statement-no-4.pdf.
- 26.Holan S, Mathiesen M, Petersen K. A National Clinical Guideline for Antenatal Care. Directorate for Health and Social Affairs; 2005. [Accessed August 1, 2016]. Available at: http://folk.uio.no/steinrod/medsem9/a-national-clinical-guideline-for-antenatal-care_short-version.pdf. [Google Scholar]
- 27.Barakat R, Pelaez M, Lopez C, Lucia A, Ruiz JR. Exercise during pregnancy and gestational diabetes-related adverse effects: a randomised controlled trial. Br J Sports Med. 2013;47(10):630–636. doi: 10.1136/bjsports-2012-091788. [DOI] [PubMed] [Google Scholar]
- 28.Marquez-Sterling S, Perry AC, Kaplan TA, Halberstein RA, Signorile JF. Physical and psychological changes with vigorous exercise in sedentary primi-gravidae. Med Sci Sports Exerc. 2000;32(1):58–62. doi: 10.1097/00005768-200001000-00010. [DOI] [PubMed] [Google Scholar]
- 29.Hall DC, Kaufmann DA. Effects of aerobic and strength conditioning on pregnancy outcomes. Am J Obstet Gynecol. 1987;157(5):1199–1203. doi: 10.1016/s0002-9378(87)80294-6. [DOI] [PubMed] [Google Scholar]
- 30.Szymanski LM, Satin AJ. Exercise during pregnancy: fetal responses to current public health guidelines. Obstet Gynecol. 2012;119(3):603–610. doi: 10.1097/AOG.0b013e31824760b5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Simkhada B, Teijlingen ER, Porter M, Simkhada P. Factors affecting the utilization of antenatal care in developing countries: systematic review of the literature. J Adv Nurs. 2008;61(3):244–260. doi: 10.1111/j.1365-2648.2007.04532.x. [DOI] [PubMed] [Google Scholar]
- 32.Misra DP, Strobino DM, Stashinko EE, Nagey DA, Nanda J. Effects of physical activity on preterm birth. Am J Epidemiol. 1998;147(7):628–635. doi: 10.1093/oxfordjournals.aje.a009503. [DOI] [PubMed] [Google Scholar]
- 33.Orr ST, James SA, Garry J, Newton E. Exercise participation before and during pregnancy among low-income, urban, Black women: the Baltimore Preterm Birth Study. Ethn Dis. 2006;16(4):909–913. [PubMed] [Google Scholar]
- 34.Orr ST, James SA, Garry J, Prince CB, Newton ER. Exercise and pregnancy outcome among urban, low-income, black women. Ethn Dis. 2006;16(4):933–937. [PubMed] [Google Scholar]
- 35.Sealy-Jefferson S, Hegner K, Misra DP. Linking nontraditional physical activity and preterm delivery in urban African-American women. Womens Health Issues. 2014;24(4):e389–e395. doi: 10.1016/j.whi.2014.04.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.DiPietro JA, Bornstein MH, Hahn CS, Costigan K, Achy-Brou A. Fetal heart rate and variability: stability and prediction to developmental outcomes in early childhood. Child Dev. 2007;78(6):1788–1798. doi: 10.1111/j.1467-8624.2007.01099.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Hatch MC, Shu XO, McLean DE, et al. Maternal exercise during pregnancy, physical fitness, and fetal growth. Am J Epidemiol. 1993;137(10):1105–1114. doi: 10.1093/oxfordjournals.aje.a116614. [DOI] [PubMed] [Google Scholar]
- 38.Bell R, O’Neill M. Exercise and pregnancy: a review. Birth. 1994;21(2):85–95. doi: 10.1111/j.1523-536x.1994.tb00240.x. [DOI] [PubMed] [Google Scholar]
- 39.Kramer MS. Aerobic exercise for women during pregnancy. Cochrane Database Syst Rev. 2002;(2):CD000180. doi: 10.1002/14651858.CD000180. [DOI] [PubMed] [Google Scholar]
- 40.Clapp JF, III, Capeless EL. Neonatal morphometrics after endurance exercise during pregnancy. Am J Obstet Gynecol. 1990;163(6 pt 1):1805–1811. doi: 10.1016/0002-9378(90)90754-u. [DOI] [PubMed] [Google Scholar]
- 41.Clapp JF, III, Dickstein S. Endurance exercise and pregnancy outcome. Med Sci Sports Exerc. 1984;16(6):556–562. [PubMed] [Google Scholar]
- 42.Hopkins SA, Baldi JC, Cutfield WS, McCowan L, Hofman PL. Exercise training in pregnancy reduces offspring size without changes in maternal insulin sensitivity. J Clin Endocrinol Metab. 2010;95(5):2080–2088. doi: 10.1210/jc.2009-2255. [DOI] [PubMed] [Google Scholar]
- 43.Bell RJ, Palma SM, Lumley JM. The effect of vigorous exercise during pregnancy on birth-weight. Aust N Z J Obstet Gynaecol. 1995;35(1):46–51. doi: 10.1111/j.1479-828x.1995.tb01829.x. [DOI] [PubMed] [Google Scholar]
- 44.Horns PN, Ratcliffe LP, Leggett JC, Swanson MS. Pregnancy outcomes among active and sedentary primiparous women. J Obstet Gynecol Neonatal Nurs. 1996;25(1):49–54. doi: 10.1111/j.1552-6909.1996.tb02512.x. [DOI] [PubMed] [Google Scholar]
- 45.Rose NC, Haddow JE, Palomaki GE, Knight GJ. Self-rated physical activity level during the second trimester and pregnancy outcome. Obstet Gynecol. 1991;78(6):1078–1080. [PubMed] [Google Scholar]
- 46.Sternfeld B, Quesenberry CP, Jr, Eskenazi B, Newman LA. Exercise during pregnancy and pregnancy outcome. Med Sci Sports Exerc. 1995;27(5):634–640. [PubMed] [Google Scholar]
- 47.Beckmann CR, Beckmann CA. Effect of a structured antepartum exercise program on pregnancy and labor outcome in primiparas. J Reprod Med. 1990;35(7):704–709. [PubMed] [Google Scholar]
- 48.Juhl M, Olsen J, Andersen PK, Nohr EA, Andersen AM. Physical exercise during pregnancy and fetal growth measures: a study within the Danish National Birth Cohort. Am J Obstet Gynecol. 2010;202(1):e61–e68. doi: 10.1016/j.ajog.2009.07.033. [DOI] [PubMed] [Google Scholar]
- 49.Hegaard HK, Pedersen BK, Nielsen BB, Damm P. Leisure time physical activity during pregnancy and impact on gestational diabetes mellitus, pre-eclampsia, preterm delivery and birth weight: a review. Acta Obstet Gynecol Scand. 2007;86(11):1290–1296. doi: 10.1080/00016340701647341. [DOI] [PubMed] [Google Scholar]
- 50.Mudd LM, Pivarnik JM, Pfeiffer KA, Paneth N, Chung H, Holzman C. Maternal physical activity during pregnancy, child leisure-time activity, and child weight status at 3 to 9 years. J Phys Act Health. 2015;12(4):506–514. doi: 10.1123/jpah.2013-0173. [DOI] [PubMed] [Google Scholar]
- 51.Owe KM, Nystad W, Bo K. Association between regular exercise and excessive newborn birth weight. Obstet Gynecol. 2009;114(4):770–776. doi: 10.1097/AOG.0b013e3181b6c105. [DOI] [PubMed] [Google Scholar]
- 52.Barker DJ, Eriksson JG, Forsen T, Osmond C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol. 2002;31(6):1235–1239. doi: 10.1093/ije/31.6.1235. [DOI] [PubMed] [Google Scholar]
- 53.Dietz WH. Overweight in childhood and adolescence. N Engl J Med. 2004;350(9):855–857. doi: 10.1056/NEJMp048008. [DOI] [PubMed] [Google Scholar]
- 54.Hopkins SA, Cutfield WS. Exercise in pregnancy: weighing up the long-term impact on the next generation. Exerc Sport Sci Rev. 2011;39(3):120–127. doi: 10.1097/JES.0b013e31821a5527. [DOI] [PubMed] [Google Scholar]
- 55.Perales M, Santos-Lozano A, Ruiz JR, Lucia A, Barakat R. Benefits of aerobic or resistance training during pregnancy on maternal health and perinatal outcomes: a systematic review. Early Hum Dev. 2016;94:43–48. doi: 10.1016/j.earlhumdev.2016.01.004. [DOI] [PubMed] [Google Scholar]
- 56.Schlotz W, Phillips DI. Fetal origins of mental health: evidence and mechanisms. Brain Behav Immun. 2009;23(7):905–916. doi: 10.1016/j.bbi.2009.02.001. [DOI] [PubMed] [Google Scholar]
- 57.Fleten C, Stigum H, Magnus P, Nystad W. Exercise during pregnancy, maternal prepregnancy body mass index, and birth weight. Obstet Gynecol. 2010;115(2 pt 1):331–337. doi: 10.1097/AOG.0b013e3181ca4414. [DOI] [PubMed] [Google Scholar]
- 58.Hegaard HK, Petersson K, Hedegaard M, et al. Sports and leisure-time physical activity in pregnancy and birth weight: a population-based study. Scand J Med Sci Sports. 2010;20(1):e96–e102. doi: 10.1111/j.1600-0838.2009.00918.x. [DOI] [PubMed] [Google Scholar]
- 59.Johnson AA, Knight EM, Edwards CH, et al. Selected lifestyle practices in urban African American women—relationships to pregnancy outcome, dietary intakes and anthropometric measurements. J Nutr. 1994;124(6 suppl):963S–972S. doi: 10.1093/jn/124.suppl_6.963S. [DOI] [PubMed] [Google Scholar]
- 60.Strutz KL, Richardson LJ, Hussey JM. Selected preconception health indicators and birth weight disparities in a national study. Womens Health Issues. 2014;24(1):e89–e97. doi: 10.1016/j.whi.2013.10.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Gray-Donald K, Robinson E, Collier A, David K, Renaud L, Rodrigues S. Intervening to reduce weight gain in pregnancy and gestational diabetes mellitus in Cree communities: an evaluation. CMAJ. 2000;163(10):1247–1251. [PMC free article] [PubMed] [Google Scholar]
- 62.Alderman BW, Zhao H, Holt VL, Watts DH, Beresford SA. Maternal physical activity in pregnancy and infant size for gestational age. Ann Epidemiol. 1998;8(8):513–519. doi: 10.1016/s1047-2797(98)00020-9. [DOI] [PubMed] [Google Scholar]
- 63.Barakat R, Lucia A, Ruiz JR. Resistance exercise training during pregnancy and newborn’s birth size: a randomised controlled trial. Int J Obes (Lond) 2009;33(9):1048–1057. doi: 10.1038/ijo.2009.150. [DOI] [PubMed] [Google Scholar]
- 64.Botkin C, Driscoll CE. Maternal aerobic exercise: newborn effects. Fam Pract Res J. 1991;11(4):387–393. [PubMed] [Google Scholar]
- 65.Giroux I, Inglis SD, Lander S, Gerrie S, Mottola MF. Dietary intake, weight gain, and birth outcomes of physically active pregnant women: a pilot study. Appl Physiol Nutr Metab. 2006;31(5):483–489. doi: 10.1139/h06-024. [DOI] [PubMed] [Google Scholar]
- 66.DiPietro JA, Costigan KA, Pressman EK, Doussard-Roosevelt JA. Antenatal origins of individual differences in heart rate. Dev Psychobiol. 2000;37(4):221–228. doi: 10.1002/1098-2302(2000)37:4<221::aid-dev2>3.0.co;2-a. [DOI] [PubMed] [Google Scholar]
- 67.Clapp JF., III Morphometric and neurodevelopmental outcome at age five years of the offspring of women who continued to exercise regularly throughout pregnancy. J Pediatr. 1996;129(6):856–863. doi: 10.1016/s0022-3476(96)70029-x. [DOI] [PubMed] [Google Scholar]
- 68.Elia M, Betts P, Jackson DM, Mulligan J. Fetal programming of body dimensions and percentage body fat measured in prepubertal children with a 4-component model of body composition, dual-energy X-ray absorptiometry, deuterium dilution, densitometry, and skinfold thicknesses. Am J Clin Nutr. 2007;86(3):618–624. doi: 10.1093/ajcn/86.3.618. [DOI] [PubMed] [Google Scholar]
- 69.May LE, Glaros A, Yeh HW, Clapp JF, III, Gustafson KM. Aerobic exercise during pregnancy influences fetal cardiac autonomic control of heart rate and heart rate variability. Early Hum Dev. 2010;86(4):213–217. doi: 10.1016/j.earlhumdev.2010.03.002. [DOI] [PubMed] [Google Scholar]
- 70.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):33–38. doi: 10.1016/j.earlhumdev.2013.11.001. [DOI] [PubMed] [Google Scholar]
- 71.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):1252–1258. doi: 10.1249/MSS.0b013e318247b324. [DOI] [PubMed] [Google Scholar]
- 72.May L, Suminski RS. Amount of physical activity in pregnancy and infant heart outcomes. J Neonat Biol. 2014;3(5) in press. [Google Scholar]
- 73.Pivarnik J, Chambliss H, 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. doi: 10.1249/01.mss.0000218147.51025.8a. [DOI] [PubMed] [Google Scholar]
- 74.Barker DJ. The fetal origins of coronary heart disease. Eur Heart J. 1997;18(6):883–884. doi: 10.1093/oxfordjournals.eurheartj.a015368. [DOI] [PubMed] [Google Scholar]
- 75.Clapp JF, III, Lopez B, Harcar-Sevcik R. Neonatal behavioral profile of the offspring of women who continued to exercise regularly throughout pregnancy. Am J Obstet Gynecol. 1999;180(1 pt 1):91–94. doi: 10.1016/s0002-9378(99)70155-9. [DOI] [PubMed] [Google Scholar]
- 76.LeMoyne EL, Curnier D, St-Jacques S, Ellemberg D. The effects of exercise during pregnancy on the newborn’s brain: study protocol for a randomized controlled trial. Trials. 2012;13:68. doi: 10.1186/1745-6215-13-68. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 77.Domingues MR, Matijasevich A, Barros AJ, Santos IS, Horta BL, Hallal PC. Physical activity during pregnancy and offspring neurodevelopment and IQ in the first 4 years of life. PLoS One. 2014;9(10):e110050. doi: 10.1371/journal.pone.0110050. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 78.Hellenes OM, Vik T, Lohaugen GC, et al. Regular moderate exercise during pregnancy does not have an adverse effect on the neurodevelopment of the child. Acta Paediatr. 2015;104(3):285–291. doi: 10.1111/apa.12890. [DOI] [PubMed] [Google Scholar]
- 79.Santos DN, Assis AM, Bastos AC, et al. Determinants of cognitive function in childhood: a cohort study in a middle income context. BMC Public Health. 2008;8:202. doi: 10.1186/1471-2458-8-202. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80.Chasan-Taber L, Schmidt MD, Pekow P, Sternfeld B, Manson J, Markenson G. Correlates of physical activity in pregnancy among Latina women. Matern Child Health J. 2007;11(4):353–363. doi: 10.1007/s10995-007-0201-8. [DOI] [PubMed] [Google Scholar]
- 81.Zhang J, Savitz DA. Exercise during pregnancy among US women. Ann Epidemiol. 1996;6(1):53–59. doi: 10.1016/1047-2797(95)00093-3. [DOI] [PubMed] [Google Scholar]
- 82.Ning Y, Williams MA, Dempsey JC, Sorensen TK, Frederick IO, Luthy DA. Correlates of recreational physical activity in early pregnancy. J Matern Fetal Neonatal Med. 2003;13(6):385–393. doi: 10.1080/jmf.13.6.385.393. [DOI] [PubMed] [Google Scholar]
- 83.Petersen AM, Leet TL, Brownson RC. Correlates of physical activity among pregnant women in the United States. Med Sci Sports Exerc. 2005;37(10):1748–1753. doi: 10.1249/01.mss.0000181302.97948.90. [DOI] [PubMed] [Google Scholar]
- 84.Kieffer EC, Willis SK, Arellano N, Guzman R. Perspectives of pregnant and postpartum latino women on diabetes, physical activity, and health. Health Educ Behav. 2002;29(5):542–556. doi: 10.1177/109019802237023. [DOI] [PubMed] [Google Scholar]
- 85.Sternfeld B, Ainsworth BE, Quesenberry CP. Physical activity patterns in a diverse population of women. Prev Med. 1999;28(3):313–323. doi: 10.1006/pmed.1998.0470. [DOI] [PubMed] [Google Scholar]
- 86.Domingues MR, Barros AJ. Leisure-time physical activity during pregnancy in the 2004 Pelotas Birth Cohort Study. Rev Saude Publica. 2007;41(2):173–180. doi: 10.1590/s0034-89102007000200002. [DOI] [PubMed] [Google Scholar]
- 87.Fox NA, Porges SW. The relation between neonatal heart period patterns and developmental outcome. Child Dev. 1985;56(1):28–37. [PubMed] [Google Scholar]
- 88.Porges SW. Heart rate variability and deceleration as indexes of reaction time. J Exp Psychol. 1972;92(1):103–110. doi: 10.1037/h0032181. [DOI] [PubMed] [Google Scholar]
- 89.Porges SW, Humphrey MM. Cardiac and respiratory responses during visual search in nonretarded children and retarded adolescents. Am J Ment Defic. 1977;82(2):162–169. [PubMed] [Google Scholar]
- 90.Sakurai M, Nakamura K, Miura K, et al. Dietary carbohydrate intake, presence of obesity and the incident risk of type 2 diabetes in Japanese men. J Diabetes Investig. 2016;7(3):343–351. doi: 10.1111/jdi.12433. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 91.Baeten JM, Bukusi EA, Lambe M. Pregnancy complications and outcomes among overweight and obese nulliparous women. Am J Public Health. 2001;91(3):436–440. doi: 10.2105/ajph.91.3.436. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 92.Cordero L, Oza-Frank R, Landon MB, Nankervis CA. Breastfeeding initiation among macrosomic infants born to obese nondiabetic mothers. Breastfeed Med. 2015;10(5):239–245. doi: 10.1089/bfm.2015.0028. [DOI] [PubMed] [Google Scholar]
- 93.Kaaja R, Ronnemaa T. Gestational diabetes: pathogenesis and consequences to mother and offspring. Rev Diabet Stud. 2008;5(4):194–202. doi: 10.1900/RDS.2008.5.194. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 94.Hopkins SA, Artal R. The role of exercise in reducing the risks of gestational diabetes mellitus. Womens Health (Lond Engl) 2013;9(6):569–581. doi: 10.2217/whe.13.52. [DOI] [PubMed] [Google Scholar]
- 95.Abouzeid M, Versace VL, Janus ED, et al. Socio-cultural disparities in GDM burden differ by maternal age at first delivery. PLoS One. 2015;10(2):e0117085. doi: 10.1371/journal.pone.0117085. [DOI] [PMC free article] [PubMed] [Google Scholar]