Childhood obesity is continuing to increase with nearly one-third of US children 2–19 yr of age meeting the criteria for overweight or obese (1,2). This increase in obesity is associated with decreased physical activity (3), and poor performance of motor skills in childhood (4). The earliest intervention to attenuate this trend is in the prenatal period.
Moderate to vigorous aerobic exercise during pregnancy has been shown to contribute to improved cardiac autonomic health in offspring (5,6) in addition to its established benefits including reductions in preterm delivery, gestational weight gain, and risk of infant macrosomia (7,8). Previous studies also found 5-d-old offspring from exercised women had slightly improved neurobehavioral ability relative to same age offspring of controls (9). Thus, there is growing support for the positive influence of exercise at the recommended levels during pregnancy on offspring outcomes, according to the American College of Obstetrics and Gynecology (10). Furthermore, previous work suggests a modest relationship between earlier gross motor milestone achievement in the first year and lower adiposity at 3 yr of age (11). Children who develop movement skills earlier may be more likely to move and remain physically active throughout their childhood (12), which could decrease their risk of becoming overweight or obese, obesity-associated comorbidities (e.g., metabolic syndrome), improve bone density and mental health (13–15).
To date, research has not evaluated the neuromotor outcomes of offspring exposed to supervised maternal aerobic exercise at the recommended levels in a controlled randomized trial. The purpose of this study was to determine the effects of supervised moderate-intensity aerobic exercise during pregnancy on the early neuromotor development of offspring. We hypothesized that aerobic exercise during pregnancy would be associated with higher neuromotor scores in infants at 1 month of age, based on standard pediatric assessment of neuromotor skills.
METHODS
We conducted a randomized controlled study designed to investigate the effects of exercise during pregnancy on infant neuromotor outcomes. All procedures were approved by University and Medical Center Institutional Review Board at East Carolina University and in accordance with the Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving human participants. Women were recruited via study fliers at local obstetric clinics between July 2015 and January 2018. Pregnant women were screened and enrolled between 13 and 16 wk gestation. All participants signed informed consent.
Participants
We focused recruitment on low-risk, healthy women, 18 to 40 yr of age, with a prepregnancy body mass index (BMI) between 18.5 and 34.9 kg·m−2 with a singleton pregnancy. All women were healthy, nonsmokers, with no history of alcohol or drug use during the pregnancy, and no current medication use (e.g., antidepressants, blood pressure). Participants with any contraindications to exercise during pregnancy, according to American College of Sports and Medicine (16), American College of Obstetricians and Gynecologists (17), and Society for Obstetricians and Gynecologists of Canada (18) were excluded, as were those with preexisting diabetes mellitus, hypertension, cardiovascular disease, or other comorbidities known to effect fetal well-bring (e.g., systemic lupus erythematous).
Procedures
After written informed consent and physician clearance for exercise was obtained, participants were randomized into control or aerobic exercise intervention group using GraphPad software random sequence generator (GraphPad, San Diego, CA) that was concealed prior to group assignment. Study personnel (A.G.M., C.I., D.K.) were blinded to participant group assignment; however, due to the nature of an exercise intervention, participants and trainers could not be blinded to group assignment.
Before 16 wk gestation, each participant performed a modified Balke submaximal treadmill testing to determine target HR for moderate intensity exercise intervention, 40% to 59% HR reserve (HRR), as previously published (19). Heart rate (POLAR FS2c, Polar Electro Inc., Bethpage, NY) and 12 to 14 rating of perceived exertion (6–20 scale) was monitored before, during, and after each training session.
Aerobic exercise sessions were supervised by at least two staff members (1:3 maximum trainer-to-participant ratio) who were ACSM, First Aid, and CPR certified and occurred at one of two approved university exercise facilities. Participants exercised, individually, 3 d·wk−1, with each session including a 5-min warm-up, 45- to 50-min exercise, and 3- to 5-min cool down. Based on individual preference, aerobic exercise modality included treadmill, stationary bicycle, elliptical, or aerobics. Participants in the control group did not receive an exercise intervention; however, they were asked to engage in a 50-min supervised stretching and breathing routine, three times to per week. Control participants wore a HR monitor throughout each session to ensure their HR did not exceed light intensity (<40% HRR).
Data collection
The validated and reliable Modifiable Physical Activity Questionnaire (20–22) was provided at enrollment and after delivery to confirm compliance based on group assignment. This questionnaire also provided participant demographic information (age, prepregnancy weight, number of pregnancies, number of live children, breastfeeding, highest degree obtained, race) (20,21,23). Results from the Modifiable Physical Activity Questionnaire after delivery was used to verify participants activity levels respective of their assigned group (18,20). Importantly, participants in the control group were excluded from the analysis if their activity levels outside of their stretching/breathing routine exceeded the PA recommendations (i.e., 150 min·wk−1 of moderate activity). Height was measured in inches to the nearest 0.25 inch using a stadiometer and converted to meters. Using the standard formula for females, body mass index (BMI, kg·m−2) was calculated using height, and self-reported prepregnancy weight (24). At 36 wk gestation, weight was measured using a calibrated scale. Gestational weight gain was calculated by subtracting the participant’s prepregnancy weight from the weight taken at 36-wk visit.
One month after birth, each participant brought her infant for neurodevelopmental assessment using the Peabody Developmental Motor Scales, 2nd edition (PDMS-2) (25). The PDMS-2 is a standardized, norm-referenced tool used to assess gross motor skills. For infants up to 12 months of age, the PDMS-2 includes three subtests: Reflexes, Stationary, and Locomotion. Normalized standard score and percentile ranks can be calculated for each subtest. A composite score, the Gross Motor Quotient (GMQ), and a percentile ranking for this overall score, can also be calculated (25). The PDMS-2 was performed by an experienced pediatric physical therapist (A.G.M.) blinded to group classification and scored according to the standardized protocol.
Data analysis
Maternal and infant 1-month descriptive measures and infant PDMS-2 subtest percentiles, GMQ, and GMQ percentiles were summarized as means ± SD, and compared using independent t-tests to determine group differences; if data were not normally distributed, then the Mann–Whitney U test was used to analyze group differences. Research suggests breastfeeding may have positive influences on infant neurodevelopment (26), thus, data analyses were repeated with only breastfed infants; there were too few formula-fed infants to compare with breastfed infants. Pearson correlations were performed to determine relationships between maternal and infant variables. ANCOVA analyses were performed to determine differences between groups on neuromotor scores controlling for sex and breastfeeding. All statistical analyses were performed using the Statistical Package for Social Sciences (SPSS version 19.0, Chicago, 2009) with α < 0.05.
RESULTS
A total of 116 participants were enrolled; after excluding participants (Fig. 1), our final analysis included 60 participants (33 aerobic exercisers, 27 nonexercisers/controls). The average participant was 30.6 yr old, 23.9 BMI (healthy weight), had a bachelor’s degree, gained 29 pounds, were in their first pregnancy, and breastfed their child. We found no differences between group in regard to maternal demographic variables: age, BMI, number of pregnancies, number of live children, maternal years of education (Table 1). There were near significant differences between groups in gestational weight gain (P = 0.05) and prevalence of breastfeeding (P = 0.08) (Table 1). All infants included in the study were born healthy, full-term, and with no congenital abnormalities. One-month infants had similar gestational age, height, weight, and BMI between groups (Table 2). For exercisers, average exercise intervention compliance was 83%, but ranged from 29% to 100%. Most exercisers (81%) had compliance greater than 70% throughout the pregnancy.
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FIGURE 1: Study participants.
TABLE 1: Maternal participant demographics.
TABLE 2: Infant participant descriptors.
All infants scored within the range of typical gross motor development on the PDMS-2. The PDMS-2 Stationary and Locomotion percentiles, GMQ, and GMQ percentiles were all higher for infants of aerobic exercisers compared to infants of controls (Table 3). This difference was significant for the Locomotion subtest percentile score (Table 3). Based on previous literature (26), comparisons were repeated with only infants breastfed and findings are similar between groups (data not shown). Pearson correlation analysis found no significant associations between maternal measures (age, prepregnancy BMI, gravida, parity, gestational weight gain, and education) and infant BMI with infant neuromotor outcomes (data not shown).
TABLE 3: PDMS-2 gross motor quotient (GMQ) and subtest scores.
Since males and females may develop at different rates (27), we repeated infant analyses between sexes within groups and found males infants of controls did significantly better than female infants of controls on Reflex percentile, Locomotion percentile, GMQ, and GMQ percentile scores. Female infants of exercisers did slightly better than males in Reflex, Stationary, and GMQ scores, whereas male infants of exercisers did slightly better in Locomotion scores (Table 4). With differences between sex, we then compared within sexes between groups and noted female infants of exercises did significantly better on most scores (Stationary percentile, GMQ, GMQ percentile) compared with females of controls (Table 4). Conversely, male controls had significantly higher (P = 0.02) Reflex scores than male exercisers; except for Reflex scores, male infants of exercisers tended to have higher scores than male and female infants of controls (Table 4). With ANCOVA we found a significant effect of exercise–sex interaction on 1-month Reflex scores after controlling for breastfeeding (F(1,65) = 5.819, P = 0.02). The effect was almost significant for exercise group on 1-month Stationary scores after controlling for breastfeeding (F(1,65) = 3.235, P = 0.08). The effect was significant for sex (F(1,65) = 8.895, P = 0.004) and almost for exercise group (F(1,65) = 3.752, P = 0.057) on 1-month Locomotion scores after controlling for breastfeeding. With ANCOVA we found a significant effect of exercise–sex interaction on 1-month GMQ scores (F(1,65) = 4.509, P = 0.04) and GMQ percentiles (F(1,65) = 5.063, P = 0.03) after controlling for breastfeeding.
TABLE 4: PDMS-2 GMQ and subtest scores for males between groups.
DISCUSSION
The purpose of this study was to determine the effects of maternal exercise during pregnancy on the early neuromotor development of offspring. We hypothesized that exercise during pregnancy would be associated with higher neuromotor scores in infants at 1 month of age, based on standard assessment of infant motor skills. The data show, in support of our hypothesis, that infants of mothers who exercised during pregnancy scored higher on Stationary and Locomotion skills and on overall Gross Motor Quotient at 1-month relative to infants of mothers who did not exercise during pregnancy. Significant differences were also found in neuromotor skills within like sexes associated with the exercise intervention. This is the first evidence of its kind from a randomized control study of supervised exercise intervention in pregnancy and adds to the growing body of knowledge supporting the positive effects of maternal exercise on infants’ outcomes.
The findings of this study are consistent with previously reported positive effects of maternal exercise on neurobehavior in newborns and at 1 yr of age (9,28). Clapp et al. (29) reported higher scores in neuromotor skills in 5-yr-olds exposed to maternal aerobic exercise, ≥90 min of moderate intensity throughout the entire pregnancy, compared to 5-yr-olds of women in control group (29). Although Hellenes et al. (30) reported no difference in motor skills of 18-month-olds whose mothers had/had not exercised during pregnancy, the moderate intensity exercise was less than three times per week, whereas duration and type of exercise for each session was not reported, which may explain the lack of differences between groups. Overall, improved neuromotor skills in infancy may be related to later physical activity and performance, as has been reported previously (31–33). Sanchez et al. (31) reported that delays in gross motor development were related to decreased time in moderate-to-vigorous physical activity, and increased sedentary time, at 7 yr of age. Ridgway et al. (32,33) reported that earlier attainment of gross motor skills predicted increased sports participation at 14 yr of age, and greater muscle strength, muscle endurance, and aerobic fitness at 31 yr of age. Infants and children with higher motor competence will likely enjoy movement more and thus participate more in gross motor activities. Increased physical activity will contribute to a decreased risk for obesity and cardiovascular disease later in life. The current findings further support the positive influence of maternal exercise on fetal neurodevelopment and suggest exercise during pregnancy as a potential modifier of childhood and adult obesity risk.
A possible explanation for the neuromotor improvements in infants exposed to exercise in utero could be the release of growth hormone as well as intrauterine growth factor-1 (IGF-1) associated with maternal exercise (34). Although maternal growth hormone and IGF-1 do not cross the placenta, they can enhance fetal growth and development via improved fetal nutrient supply (35). Additionally, exercise during pregnancy may directly impact brain and nervous system development in utero by improving overall blood flow and oxygenation, decreasing inflammatory factors and oxidative stress (36), and increasing serum levels of growth factors (i.e., brain derived neurotrophic factor, IGF-1) (37). Newborn infants of mothers who exercised during pregnancy had enhanced cerebral maturation compared to infants whose mothers were inactive (38). Cerebral maturation is associated with myelination and motor skills. Newborn infants of mothers who exercised during pregnancy had enhanced cerebral maturation compared to infants whose mothers were inactive (38). Cerebral maturation is associated with myelination and motor skills (38–40). Conversely, studies of maternal obesity report infant motor milestones are delayed and associated with long-term consequences of cognitive function when mothers are classified as obese (41). Conversely, studies of maternal obesity find infant motor milestones are delayed and associated with long-term consequences of cognitive function when mothers are classified as obese (41).
An intriguing finding of this study was the sex dimorphism in the effects of prenatal exercise on neuromotor skills. Sex dimorphism during fetal and neonatal growth and development is common given the dramatic differences in growth rates, concentrations of sex hormones secreted (e.g., testosterone) and accretion of bodily tissues (e.g., lean body mass) between males and females. In this study, we found that male infants of nonaerobically trained mothers exhibited higher neuromotor skills at 1-month of age compared to their female counterparts, which is consistent with previous literature (42). At birth, male brain volume, especially in the motor cortex region, is larger compared with females. This accelerated growth is suggested to be consequent to the “masculinization” of the male brain via the heightened secretion of testosterone. Interestingly, when comparing male and female infants of aerobically-trained mothers, the sex differences in neuromotor skills disappeared. This observation offers a few speculations given its novelty. First, it is possible that the advanced development of male brain in utero presents a ceiling effect, whereby the documented augmentation of cerebral blood flow and oxygenation and subsequently maturation consequent to prenatal exercise, did not further enhance brain development in male fetuses. Relatedly, prenatal exercise may accelerate cerebral maturation in female fetuses, potentially resulting in increased motor skills, equivalent to that of males. Specific mechanisms for this hypothesis are not clear, requiring further investigation.
The clinical implications of this study relate to the promotion of healthy neuromotor development in infants, and potentially the prevention of childhood overweight and obesity. Maternal exercise has many positive effects on the offspring, as is shown in this and previous studies (6,43–46). The finding of consistently higher scores on the PDMS-2 stationary and locomotor subtests, and on overall GMQ, suggests improved ability of the infants in the exercise group to use sensory input, cognitive motivation, and muscular strength and coordination to voluntarily control head, trunk and extremities. Since poor neuromotor skills are associated with decreased physical activity of infants and children, which is a risk factor for obesity, the promotion of exercise during pregnancy may positively influence childhood health outcomes.
Limitations
Although our sample is relatively small, the fact that we found differences between two healthy, typically developing groups of infants is encouraging and suggests further research should be done in this area. Though we had a diverse population of women (BMI, race, education, etc.), all were healthy with a singleton pregnancy, therefore, these results may not be generalizable to all pregnant women, especially those considered high risk due to multiple gestation, comorbidities, etc. We did not control for other factors, such as maternal diet, sleep, sedentary behavior, or occupation, nor for postnatal infant environment and stimulation which may influence fetal/infant nervous system development. It is possible that women who exercised during pregnancy may be more likely to provide a stimulating postnatal environment; this and other potential confounding factors will need to be considered in future studies. Finally, this study reports only on gross motor skills at 1 month, and only on effects of aerobic exercise intervention compared to no exercise. The benefits of specific types of exercise (e.g., aerobic, resistance, circuit), and effects beyond 1 month of age, will need further study. A significant strength of this study was the high compliance to the exercise intervention (~89%), a common challenge in most prenatal exercise studies. We recommend employing similar compliance strategies used in this study, in future interventions including supervised exercise sessions, continuous tracking of maternal HR during exercise, individual exercise training sessions (dependent on the culture), and flexibility in training regimen (e.g., scheduling, equipment).
CONCLUSIONS
The current findings of greater neuromotor development in 1-month old infants of exercising women add to the growing body of evidence suggesting that exercise during pregnancy positively influences multiple body systems in the developing infant. Our study demonstrated distinct neurodevelopmental differences between male and female infants that require further investigation. We found that female, but not male infants, benefit from exercise exposure in utero, as evidenced by improved Stationary and Locomotion skills. The improved capacity for movement in female infants of exercisers is an important clinically relevant finding suggesting these children may be more physically active as they continue to grow and develop, potentially preventing childhood obesity, osteoporosis, and noncommunicable diseases (e.g., type 2 diabetes mellitus and cardiovascular disease) (47). Thus, exercise during pregnancy may be the earliest intervention to help reduce the prevalence of common morbidities among children and adolescents and improve the quality of life (15,48).
This study was funded, in part, by the American Heart Association (AHA grant 15GRNT24470029 to LEM) and by East Carolina University for funds to collect the data. The authors would like to acknowledge all the women who agreed to participate in this study. The authors are very grateful for their time. The authors would further like to thank the ECU Fitness, Instruction, Testing and Training (FITT) facility staff and students, and Department of Physical Therapy students, for their assistance in various tasks throughout the completion of this project.
The authors have no potential, perceived, or real conflict of interest to disclose in regards to professional relationships with companies or manufacturers. The study sponsors had no influence on the study design, interpretation of data, writing of the manuscript, nor decision to submit the manuscript. The results of the present study do not constitute endorsement by ACSM. The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation.
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