Abstract
BACKGROUND:
Prenatal exercise improves birth outcomes, but research into exercise dose-response effects is limited.
METHODS:
This study is a retrospective, secondary analysis of pooled data from three blinded, prospective, randomized controlled trials. Prenatal exercise frequency, intensity, type, time, and volume (FITT-V) were assessed in supervised sessions throughout pregnancy. Gestational age (GA), neonatal resting heart rate (rHR), morphometrics (body circumferences, weight-to-length and ponderal index) Apgar and reflex scores, and placental measures were obtained at birth. Stepwise regressions and Pearson correlations determined associations between FITT-V and birth outcomes.
RESULTS:
Prenatal exercise frequency reduces Ponderal Index (R2 = 0.15, F = 2.76, p = .05) and increased total number of reflexes present at birth (R2 = 0.24, F = 7.89, p < .001), while exercise intensity was related to greater gestational age and birth length (R2 = 0.08, F = 3.14; R2 = 0.12, F = 3.86, respectively; both p = .04); exercise weekly volume was associated with shorter hospital stay (R2 = 0.24, F = 4.73, p = .01). Furthermore, exercise type was associated with placenta size (R2 = 0.47, F = 3.51, p = .01).
CONCLUSIONS:
Prenatal exercise is positively related to birth and placental outcomes in a dose-dependent manner.
Keywords: Apgar, birthweight, dose, placenta, ponderal index, prenatal exercise
INTRODUCTION
Research suggests that there may be a dose-dependent beneficial effect of prenatal exercise for mothers [1-4]. Based on a preponderance of evidence, worldwide guidelines support 150 minutes of moderate intensity exercise spread over 3-4 times per week to obtain the benefits of prenatal exercise [5,6]. Furthermore, exercise dose at this level or higher appears safe and could in fact benefit offspring. Studies in healthy, overweight, or obese women have shown no adverse changes in birthweight in more frequent (5 times per week) exercisers [7,8]. Additional observational evidence suggests that intensity of prenatal exercise up to 85% of maximum HR also does not harm the fetus [9-11]; furthermore, vigorous exercise during pregnancy has been shown to decrease the risk of prematurity [12]. Studies combining metrics of exercise frequency, duration, and intensity confirm there is no increased risk for adverse birth outcomes in women exercising at or above the recommended volume (MET*minutes per week) [5,7,8,13]. As for the specific type of prenatal exercise, both aerobic and resistance/muscular strength exercise have been shown as safe to the fetus [14-16]. Furthermore, concurrent resistance/strength and aerobic exercise is safe and is associated with benefits for perinatal outcomes [17]. Reports show lower risk of preterm deliveries, abnormal birth weight [18], gestational weight gain, gestational diabetes mellitus (GDM) [19,20], and hypertension [21,22].
While large systematic reviews have elucidated some of the expected effects from manipulating the amount, dose, or intensity of exercise during pregnancy [8,23,24], large-scale randomized controlled trials are lacking. Further investigation is needed to elucidate the influence of prenatal exercise dose in five metrics of exercise training, “FITT-V”: Frequency (number of sessions), Intensity (metabolic equivalents, “METs”), Time (duration of sessions), Type (exercise mode), Volume (exercise MET*mins) on birth outcomes. The purpose of this study is to examine the effects of FITT-V on birth outcomes and placental size in a cohort of offspring born to women prescribed supervised exercise. Along the continuum of exercise volumes achieved during pregnancy, we predicted that greater prenatal exercise FIT-V would improve birth and placental outcomes, such as birthweight, ponderal index, hospital stay, and placental efficiency.
METHODS
Study Participants
The current report is a secondary analysis of pooled data from three prospective, randomized control trials (RCT) investigating the influence of different exercise types throughout pregnancy on fetal and infant outcomes. All protocols were approved by the East Carolina University Institutional Review Board. Women enrolled in each study met the following criteria: clearance from an obstetric provider to participate in exercise; between 18 and 40 years old; pre-pregnancy body mass index (BMI; kg▪m−2) between 18.5-39.9 kg▪m−2; singleton pregnancy; ≤ 16 weeks gestation; no current alcohol, tobacco, or medication use. Criteria for exclusion included smoking, pre-existing conditions (i.e., diabetes mellitus, hypertension, cardiovascular disease, and comorbidities, systemic lupus erythematosus), and/or medications known to affect fetal growth and well-being. The study population included women from diverse backgrounds, i.e., Black or Indigenous People of Color (BIPOC), and participant recruitment was conducted equally to represent different backgrounds and equity. The investigator and author teams are comprised of equal distribution of women and men.
Ethics Statement
These studies used data from birth records collected from participants enrolled in an initial pilot RCT study, a second RCT (ClinicalTrials.gov Identifier: NCT03517293), or a third RCT (ClinicalTrials.gov Identifier: NCT03838146). Approval for these studies were obtained from the East Carolina University Institutional Review Board. Written informed consent was obtained from each participant upon enrollment. All experimental procedures were conducted at East Carolina University.
Pre-Intervention Exercise Testing & Randomization
Following study enrollment, participants completed a submaximal exercise treadmill test to determine individual aerobic capacity, fitness level, and calculate specific target HR (THR) ranges for moderate-intensity exercise training. Peak oxygen consumption (VO2 peak), as a measure of cardiorespiratory fitness, was estimated using the modified Balke protocol previously validated for pregnant women [25]. After completing this test, participants were randomized via computerized sequencing (GraphPad software) to aerobic, resistance (defined as muscular strength exercise), combination (aerobic and resistance), or a stretching/breathing control group for the first and third RCT; for the second RCT, participants were randomized to either aerobic or control.
Exercise Intervention
All participants were supervised by trained exercise instructors in the university facilities and followed a standard protocol. The exercise intervention lasted ~24 weeks total, as all sessions started before 16 weeks gestation and were performed three times per week until delivery at ~40 weeks gestation [26]. All sessions began with a 5-minute warm-up, 50 minutes of assigned randomized group activity, and ended with a 5-minute cool-down. Women were supervised and THR corresponding to moderate intensity (40–59% VO2peak, and 12-15 rated perceived exertion) was the goal throughout the exercise session regardless of training mode. Target HR zones validated for pregnant women were utilized [25].
The aerobic exercise group completed training on treadmills, ellipticals, recumbent bicycles, rowing, and/or stair-stepping equipment. The resistance exercise group completed sessions of two to three sets of 15 repetitions of each of 10 to 12 exercises at ~60% of 1 repetition maximum (1-RM), which was determined as previously reported [27]. RE was performed in a circuit with minimal rest (~5 seconds) using seated machines (Cybex) (leg extension, leg curl, shoulder press, chest press, triceps extension, latissimus dorsi pull down), dumbbells (biceps curls, lateral shoulder raises, front shoulder raises), resistance bands, dumbbells, exercise balls, benches, and/or mats. The combination exercise group performed half of the aerobic protocol and half of the resistance protocol exercises. Resistance exercises were performed at 15 repetitions (same exercises and equipment as RE group), while the aerobic exercises were performed on the same equipment as the AE group. Light intensity stretching and breathing exercises were performed by an attention control (CON) group. To monitor intensity during each session, the Borg rating of perceived exertion (RPE 6-20) scale was used alongside target heart rate monitoring (Polar FS2C). Supervised exercise and stretching/breathing (control) sessions took place at one of two university-affiliated gyms.
Prenatal Exercise FITT-V
Exercising women were scheduled for exercise 3 times per week, for 50 minutes per session, at 3 – 6 METs. To control for the effect of interindividual differences in gestational length, e.g., premature, or late delivery, on total exercise volume throughout pregnancy, exercise FITT-V was analyzed between 16 and 36 weeks of gestation for all participants. Percent adherence to weekly volume and duration of exercise were calculated from data entered for each exercise session into a REDCap study database [28]. Frequency, intensity, time, and volume of exercise were calculated for all exercisers and analyzed both as pooled and type-specific exercise FITT-V.
Frequency was expressed as the average number of exercise sessions per week (Weekly Frequency), as well as the total number of exercise sessions across the pregnancy (Total Frequency) between 16 to 36 weeks. Intensity (METs) was determined using intensity measured from each exercise session, as well as the published compendium of physical activities [29], then averaged from all exercise sessions. Time was determined by averaging exercise duration, in minutes, from each week. Lastly, prenatal exercise volume (MET*minutes) was calculated by 1) multiplying METs by weekly duration for volume in MET*minutes per week (weekly volume), and 2) multiplying the weekly MET*minutes by the total number of weeks of prenatal exercise for total MET*minutes (total volume).
Birth and Placental Outcomes
At birth, delivery type (spontaneous vaginal delivery, C-section), neonate sex, gestational age, neonatal measures (heart rate; chest, head, and abdominal circumferences; birth weight, length, ponderal index (PI)) were measured by standard procedures of the labor & delivery nurses blinded to randomized group allocation and entered into the electronic health record. Within each neonate sex, z-scores for all morphometric measures (circumferences, weight, length, PI) were calculated as: (X – mean) / standard deviation. Women with pregnancy complications reported in the health record (gestational diabetes mellitus, gestational hypertension, preterm birth) were excluded from analysis. Head circumference: abdominal circumference (HC:AC) and weight-to-length ratios were calculated. Apgar scores were measured at 1 and 5 minutes after birth by labor and delivery nurse along with the presence of 7 reflexes (sucking, Moro, hand grasp, feet grasp, traction, Babinski, and stepping). At birth, the placenta was collected by the study team, blinded by group, and manual measurement of diameter (cm), thickness (cm), volume (cm3), weight (g), and density (g/cm3) were obtained. Two measures of placental efficiency by volume and by weight) were calculated by dividing birth weight by either 1) placental volume or 2) placental weight, respectively.
Maternal Covariates
Maternal age, gravida, parity, pre-pregnancy weight and height, as well as race, and ethnicity were collected from pre-screening eligibility questionnaires. Pre-pregnancy BMI (healthy BMI 18.0-24.99; Overweight 24.5-29.99, Obese >30) was calculated using height (m), measured by stadiometer, and weight (kg) collected from the pre-screening eligibility questionnaire. Maternal pre-pregnancy BMI was calculated via the following established equation: [weight (kg)] / [height (m)]2. Race and ethnicity were used to dichotomize participants into Black or Indigenous People of Color (BIPOC) or not. Maternal VO2 peak was also considered a covariate.
Statistical Analysis
To obtain statistical power of 80% with significance α = 0.05, analysis justified a sample size of 29 total subjects to detect a moderate two-tailed Pearson product-moment coefficient of 0.50 [30]. Analyses by exercise group was performed on all 4 groups (AE, RE, AERE, CON); however, the effect of exercise metrics, FITT-V, throughout pregnancy was analyzed on exercise subjects only, excluding controls. Stratified analyses were performed for exercise type. Pearson product-moment correlations were performed between each exercise FITT-V metric and each birth and placental outcome. In order to minimize the risk of too readily rejecting the null hypothesis, adjustments were not made for multiple comparisons [31]. Stepwise regressions were conducted to determine significant associated variables with birth and placental outcomes, controlling for covariates. One-Way ANOVA was performed for investigations of randomized exercise group effect, with Tukey post-hoc test applied to significant group effects. Correlations and ANOVAs were performed using SPSS software (version 28.0.1.1, SPSS Inc. IBM Corp., Chicago, IL), while regressions were completed with JMP Pro 17 (SAS, Cary, NC).
RESULTS
Birth outcomes were obtained for 358 women who enrolled in one of the studies. Across all births, 88 (25%) were Cesarean section, while 270 were spontaneous vaginal delivery. As this investigation focused on healthy pregnancies, subjects with adverse pregnancy outcomes were excluded from analysis (gestational diabetes mellitus (GDM) – 18; GDM & Pre-term – 2; Pre-term – 25, Pre-term & hypertensive disorder of pregnancy (HDP) – 1; HDP only - 13). The final study sample included 298 healthy neonates, with 140 females and 158 males. In addition to 83 control subjects, 215 intervention subjects (AE: 91, RE: 59, AERE: 65) had complete exercise FITT-V metrics and were included in final analysis (Table 1).
Table 1.
Maternal Characteristics Across Exercise Type.
| Maternal Characteristic | Control | AE | RE | AERE | p value |
|---|---|---|---|---|---|
| Age (years) | 29.6 ± 4.4 | 29.8 ± 4.4 | 30.1 ± 4.1 | 31.2 ± 4.0 | .14 |
| Pre-Pregnancy BMI (kg*m−2) | 28.0 ± 6.0 | 25.0 ± 5.2* | 25.0 ± 3.9* | 26.0 ± 5.0 | .002 |
| VO2peak (mL*kg−1*min−1) | 20.3 ± 5.3 | 23.0 ± 4.7* | 23.4 ± 6.2* | 23.7 ± 5.7* | .002 |
| % BIPOC | 37% | 24% | 10%* | 17% | .009 |
| Gravida | 2 (1,6) | 2 (1,4) | 2 (1,5) | 2 (1,4) | .11 |
| Parity | 1 (0,4) | 1 (0,2)* | 1 (0,3) | 1 (0,2)* | .03 |
| Pregnancy Complications (%) | 21% | 15% | 20% | 13% | .81 |
Data reported as mean ± SD. Maternal characteristics measured before commencement of exercise (12 – 16 weeks of gestation) or documented at birth (pregnancy complications). AE Aerobic Exercise, RE Resistance Exercise, AERE Combination Exercise. Tukey post-hoc results: *p < .05 vs. control. BIPOC Black or Indigenous People of Color.
Women on average were 30.3 years of age, BMI of 27.0 kg*m−2, with VO2 peak of 21.65 mL*kg−1* min−1, on their 2nd pregnancy. The population was diverse, with 25% of subjects identified as Black or Indigenous People of Color, 37% with overweightness, and 28% with obesity. Women participated in exercise for an average of 17 weeks during pregnancy (range 3 to 20 weeks). In the current study assessing from 16 to 36 weeks for standardization, exercise volume ranged between 100 - 850 MET*min/wk, spread over 10 - 76 total sessions, and resulting in 1,000 - 20,000 total MET*minutes through pregnancy.
There were no significant differences for exercise FITT-V between exercise types (Table 2), except for a significantly higher weekly duration of exercise in combination compared to aerobic (p < .05). Among exercise types, attendance to sessions averaged 80%. Participant compliance to weekly volume (MET*minutes/wk) averaged 92% for AE and AERE groups, and 100% for RE; exercise compliance to weekly duration (min) was 82% (AE), 78% (AERE), or 86% (RE). No differences between exercise types were seen for any of the birth outcomes measured (Table 3).
Table 2.
Prenatal Exercise FITT-V Across Exercise Type.
| Exercise Metrics | Control | AE | RE | AERE | p value |
|---|---|---|---|---|---|
|
Weekly Frequency
sessions/week |
- | 2.46 ± 0.55 | 2.48 ± 0.37 | 2.63 ± 0.40 | .20 |
|
Total Frequency
total # sessions |
- | 49.9 ± 15.3 | 52.2 ± 13.9 | 55.1 ± 13.4 | .25 |
|
Intensity
METs |
- | 3.94 ± 0.46 | 3.92 ± 0.17 | 3.99 ± 0.62 | .58 |
|
Time
minutes/week |
- | 123.2 ± 29.8 | 128.8 ± 23.5 | 136.6 ± 25.6* | .05 |
|
Weekly Volume
MET*minutes/week |
- | 483.3 ± 132.0 | 506.7 ± 102.2 | 537.1 ± 150.5 | .12 |
|
Total Volume
total MET*minutes |
- | 9739 ± 3579 | 10467 ± 3753 | 11469 ± 3977 | .26 |
Data reported as mean ± SD. Exercise FITT-V calculated within each group between 16 and 36 weeks of gestation. Tukey post-hoc results: *p < .05 combination vs. aerobic. METs Metabolic Equivalent. AE Aerobic Exercise, RE Resistance Exercise, AERE Combination Exercise.
Table 3.
Birth Outcomes Across Exercise Type.
| Birth Outcome | Control | AE | RE | AERE | p value |
|---|---|---|---|---|---|
| % Female | 46% | 40% | 44% | 60% | .67 |
| GA at Birth weeks | 39.2 ± 1.5 | 39.6 ± 1.1 | 39.5 ± 0.9 | 39.3 ± 1.2 | .24 |
| Hospital Stay days | 1.9 ± 0.8 | 2.1 ± 1.0 | 1.8 ± 0.6 | 2.1 ± 0.9 | .31 |
| % C-section | 36% | 20% | 19% | 25% | .30 |
| Resting HR beats/minute | 126 ± 16 | 123 ± 14 | 125 ± 14 | 126 ± 14 | .36 |
| Circumferences z-scores | |||||
| Chest | .73 | .82 | .79 | .85 | .38 |
| Abdominal | .82 | .91 | .88 | .95 | .12 |
| Head | .89 | .94 | .95 | .97 | .36 |
| HC:AC | .82 | .92 | .88 | .92 | .20 |
| Weight z-score | .97 | .99 | .97 | 1.0 | .37 |
| Length z-score | .92 | .97 | .96 | 1.0 | .10 |
| Weight: Length z-score | .89 | .98 | .97 | 1.0* | .01 |
| Ponderal Index z-score | .88 | .99* | .98 | 1.0* | .01 |
| 1-minute Apgar | 8 ± 1 | 8 ± 1 | 8 ± 1 | 8 ± 1 | .69 |
| 5-minute Apgar | 9 ± 1 | 9 ± 0 | 9 ± 1 | 9 ± 0 | .74 |
| # Reflexes Present at Birth | 6 ± 1 | 6 ± 1 | 6 ± 2 | 6 ± 2 | .93 |
Data reported as mean ± SD. Birth outcomes collected at delivery or documented upon hospital discharge (duration of hospital stay). No significant differences observed between groups for exercise type. GA Gestational Age. HR Heart Rate. HC:AC Head Circumference: Abdominal Circumference Ratio. AE Aerobic Exercise, RE Resistance Exercise, AERE Combination Exercise. Tukey post-hoc results: *p<.05 vs. control.
However, prenatal exercise in general tended to reduce the occurrence of cesarean section (7 – 13%; Table 3). Weekly and total volume of exercise was positively associated with gestational age at birth (Table S1). Greater exercise weekly volume, weekly frequency, intensity, and time were significantly associated with improved birth measures (e.g., head, and abdominal circumferences, BMI, birthweight) (Table S1). Although placental measures did not vary between prenatal exercise type (Table 4), multiple positive associations were seen between prenatal RE FITT-V and measures of placental weight, diameter, density, and efficiency by volume (Table 5). Further, exercise FITT-V metrics were associated with improved measures of gestational age, hospital stay, morphometrics, and reflexes at birth (Table 6), after controlling for maternal covariates such as BMI, age, race, and gravida/parity.
Table 4.
Placenta Measures Across Exercise Type
| Placenta Measure | Control | AE | RE | AERE | p value |
|---|---|---|---|---|---|
| Diameter cm | 18.7 ± 1.0 | 17.4 ± 1.6 | 18.5 ± 0.6 | 17.2 ± 2.8 | .26 |
| Thickness cm | 5.4 ± 0.9 | 4.5 ± 1.4 | 5.1 ± 1.2 | 4.6 ± 1.7 | .76 |
| Volume cm3 | 1806 ± 392 | 1113 ± 504 | 1365 ± 334 | 1113 ± 459 | .50 |
| Weight grams | 492 ± 13 | 453 ± 109 | 438 ± 23 | 430 ± 149 | .67 |
| Density g*cm−3 | 0.28 ± 0.10 | 0.50 ± 0.22 | 0.34 ± 0.08 | 0.44 ± 0.20 | .44 |
| Efficiency by volume (BW/Pvol) | 2.3 ± 0.9 | 4.3 ± 1.5 | 2.8 ± 0.4 | 3.8 ± 1.6 | .86 |
| Efficiency by wt (BW/PW) | 7.7 ± 0.5 | 8.4 ± 1.4 | 8.6 ± 1.2 | 8.1 ± 2.0 | .84 |
Data reported as mean ± SD. Placenta collected at delivery and immediately stored at 4°C. Processed and measured at 25°C. Diameter calculated as average of placental width and length. Efficiency by volume (BW/Pvol) calculated as dividing birth weight by placental volume. Efficiency by wt. (BW/PW) calculated as dividing birth weight by placental weight. No significant differences observed. AE Aerobic Exercise, RE Resistance Exercise, AERE Combination Exercise.
Table 5.
Associations Between Prenatal Exercise FITT-V and Placental Measures
| Outcome | Weekly Frequency Sessions/week |
Total Frequency total # sessions |
Intensity METs |
Time minutes per week |
Weekly Volume MET*min per week |
Total Volume total MET*min |
||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| AE | RE | AERE | AE | RE | AERE | AE | RE | AERE | AE | RE | AERE | AE | RE | AERE | AE | RE | AERE | |
| Diameter cm | .821 ** | .898 * | .653 * | .678 * | .654 | .774 ** | .844 ** | .995 ** | .670 ** | .643 * | .901 * | .589 * | .785 ** | .895 * | .469 | .678 * | .596 | .620 * |
| Thickness cm | .544 | .552 | .045 | .324 | .233 | .303 | .497 | .843 * | .461 | .329 | .554 | −.032 | .557 | .556 | .051 | .259 | .144 | .112 |
| Volume cm3 | .320 | .521 | −.053 | .084 | .155 | .314 | .359 | .825 * | .508 | .017 | .522 | −.037 | .351 | .522 | .088 | .108 | .072 | .454 |
| Weight g | .648 * | .923 ** | .259 | .369 | .724 | .393 | .396 | .995 ** | .630 * | .500 | .930 ** | .396 | .286 | .930 ** | .478 | .303 | .668 | .411 |
| Density g*cm−3 | .273 | .971 ** | .451 | .334 | .949 * | .284 | .396 | .832 * | .187 | .362 | .981 ** | .423 | .204 | .981 ** | .334 | .301 | .936 * | .123 |
| Efficiency by volume (BW/Pvol). | .268 | .965 ** | .538 | .601 | .874 | .327 | .519 | .934 ** | .224 | .383 | .976 ** | .517 | .410 | .980 ** | .433 | .583 | .836 | .087 |
| Efficiency by wt (BW/PW.) | .678 * | .733 | .681 * | .901 ** | .445 | .747 * | .810 ** | .949 ** | .409 | .707 * | .742 | .470 | .866 ** | .744 | .270 | .882 ** | .368 | .527 |
Pearson’s r correlation coefficient reported. *p < .05, **p < .01; Placental measures performed at 25°C. Min minutes, Efficiency by volume (BW/Pvol) calculated as dividing birth weight by placental volume. Efficiency by wt. (BW/PW) calculated as dividing birth weight by placental weight. AE Aerobic Exercise, RE Resistance Exercise, AERE Combination Exercise.
Table 6.
Associations of Prenatal Exercise with Birth Outcomes
| Birth Outcomes | Estimate | Std. Error | Lower 95% | Upper 95% | p value |
|---|---|---|---|---|---|
| Gestational Age1 | p value = 0.028* Adjusted R2 = 0.08, F = 3.14 | ||||
| Intensity METs | 0.718 | 0.356 | 0.013 | 1.423 | 0.046 |
| Gravida | −0.293 | 0.159 | −0.607 | 0.021 | 0.067 |
| Duration of Hospital Stay2 | p value = 0.0001* Adjusted R2 = 0.24, F = 4.73 | ||||
| Pre-pregnancy BMI | 1.196 | 0.679 | −0.149 | 2.542 | 0.081 |
| Race | 1.315 | 0.438 | 0.446 | 2.184 | 0.003 |
| Weekly Volume MET*min/week | −1.899 | 0.724 | −3.335 | −0.465 | 0.010 |
| Length z score3 | p value = 0.006* Adjusted R2 = 0.12, F = 3.86 | ||||
| Race | −0.010 | 0.003 | −0.017 | −0.004 | 0.001 |
| Intensity METs | 0.016 | 0.008 | 0.001 | 0.032 | 0.040 |
| Ponderal Index z score4 | p value = 0.016 Adjusted R2 = 0.15, F = 2.76 | ||||
| Weekly Frequency sessions/week | 0.608 | 0.310 | −0.008 | 1.224 | 0.053 |
| Placenta Weight5 | p value = 0.019 Adjusted R2 = 0.58, F = 4.93 | ||||
| Age | 106.53 | 29.54 | 39.71 | 173.4 | 0.006 |
| Race | −123.50 | 31.27 | −194.2 | −52.76 | 0.003 |
| Exercise Type AE | 101.79 | 31.66 | 30.17 | 173.4 | 0.011 |
| Exercise Type AERE | −70.609 | 23.78 | −124.4 | −16.82 | 0.016 |
| Weekly Volume MET*min/week | 85.103 | 42.16 | −10.27 | 180.5 | 0.074 |
| Placenta Diameter6 | p value = 0.049* Adjusted R2 = 0.47, F = 3.51 | ||||
| Gravida | 1.717 | 0.864 | −0.237 | 3.672 | 0.078 |
| Exercise Type AERE | −2.401 | 0.929 | −4.503 | −0.299 | 0.030 |
| Exercise Type RE | 2.538 | 0.751 | 0.838 | 4.237 | 0.008 |
| Reflexes Present at Birth8 | p value < 0.0001* Adjusted R2 = 0.24, F = 7.89 | ||||
| Total Frequency total # exercise sessions | 1.736 | 0.329 | 1.084 | 2.387 | <0.001 |
Models also included: 1) gravida, exercise duration; 2) BMI, race, gravida, parity, exercise group; 3) age, gravida, parity, total MET*minutes; 4) age, gravida, parity, total MET*minutes, VO2peak; 5) MET*minutes per week; 6) average METs, exercise frequency; 7) age; 8) race, parity, average METs. No significant influence on birth weight seen in exercise FITT-V. AE Aerobic Exercise, RE Resistance Exercise, AERE Combination Exercise.
DISCUSSION
The current study aimed to determine if there is an association between exercise FITT-V and birth and placental outcomes. We hypothesized that prenatal exercise FITT-V would, in general, improve outcomes at birth, such as birthweight, ponderal index, hospital stay, and placental efficiency. We found a plethora of significant associations between exercise FITT-V and gestational age, resting heart rate at birth, body circumferences and morphometrics, and reflexes at birth. Relationships were found for many specific FITT-V metrics. In brief, exercise weekly frequency was associated with Ponderal Index and total number of reflexes present at birth, while exercise intensity correlated with gestational age and birth length; weekly exercise volume was related to hospital stay, with trends influencing placenta weight. These effects were specific to exercise type, with RE generally showing more associations than AE, especially in placenta weight and diameter and Ponderal Index. Though pre-pregnancy BMI and VO2peak were found to be significantly between exercise and control groups, VO2peak was within acceptable range for this population, and average BMI across all groups was classified as overweight (25.0 – 29.9 kg*m−2), and neither variable was associated with birth outcomes.
Prenatal Exercise Volume
Similar to a previous systematic review in 2018 [23] and a longitudinal study in 2022 [32], we found that neither weekly nor total exercise volume were associated with birthweight within a healthy population of women and neonates. These findings differ from a Chinese cohort, which found self-report volume during pregnancy was associated with greater birthweight [33]; however, the Chinese cohort included preterm and small-for-gestational age births. Chasan-Taber et al. (2007) noted that while the effect of physical activity on birth outcomes is likely to be modest, effect might not be observed since the majority of previous studies have not consistently assessed type, frequency, intensity, and duration during each trimester of pregnancy [34].
Importantly, we found greater weekly prenatal exercise volume to decrease the duration of hospital stay of the baby after delivery. This is the first study showing a direct effect of prenatal exercise weekly volume in a diverse population of women on hospital stay after delivery. As prolonged hospital stay is associated with greater cost and risk of complications [35], this finding is clinically relevant. Further, a trend was found for a significant predictive effect of weekly RE volume on placental weight, which confirms previous findings in AE [36,37]. These findings support that exercise, in general, during pregnancy increases the exchange capability of the placenta, thus enhancing nutrients to the fetus.
Currently, the recommended exercise volume for pregnancy is 150 min/wk of moderate intensity, at a minimum moderate intensity (3 METs), produces the equivalent of 450 MET*min/wk [38], with 60 total sessions from 16 to 36 weeks, and thus 9,000 total MET*min. Higher prenatal exercise volume has been associated with improved birth outcomes [5,7,39]. Our data and others [1,37,40] support weekly volumes higher than the recommended level as safe based on birth and placental outcomes.
Prenatal Exercise Frequency
As hypothesized, weekly frequency, ranging from 1 to 4 sessions per week was positively correlated with improved ponderal index and reflexes present at birth. Weekly frequency predicted Ponderal Index (PI), such that greater frequency led to greater ponderal index, within normal ranges, a notion suggesting offspring could experience improved health outcomes long-term [41,42]. Previous work has shown an inverse relationship between exercise frequency and PI [43]. It is possible the greater PI seen in the current study reflects the advanced gestational age in high-frequency exercisers; potentially the neonates from exercisers have more muscle mass as well. Total number of exercise training sessions throughout pregnancy predicted critical neonatal reflexes present at birth, which may indicate enhanced neuromotor development in these offspring [44,45]. It has been previously shown that prenatal aerobic exercise enhances neuromotor development at 1-month of age [46], while a similar dose-response in cardiac autonomic responses is also present [47,48].
Prenatal Exercise Intensity
Average exercise METs were predictive of both gestational age and offspring length at birth. These findings coupled with multiple significant correlations with other markers of morphometrics, as well as placental volume and efficiency confirm that increasing exercise intensity benefits pregnancy and fetal growth [49-51]. This information aligns with a systematic review and meta-analysis (21, 37) which showed that vigorous intensity maternal exercise significantly increases gestational length and reduces risk of prematurity [12].
Prenatal Exercise Type
The current study used data from those who participated in aerobic (AE), resistance (RE) and combination exercise (AERE). While many birth outcome variables were not different between exercise groups, Ponderal Index and weight-to-length ratio were greater for both AE and AERE than controls. Non-significantly birth length was seen in all exercise groups compared to control, possibly explaining this finding. It is interesting that the correlations seen between exercise FITT-V and birth outcomes were different between exercise types. RE typically resulted in the strongest relationships in placental diameter, and the only positive association seen with placental thickness. This finding further supports that exercise enhances the exchange capacity of the placenta and thus nutrient exchange to the developing fetus. Although we did not analyze changes in early and late pregnancy, we noted the greatest changes with aerobic-only or resistance-only prenatal exercise types. Previous research [36] notes greater placental size with aerobic exercise as well; this innovative analysis compares aerobic-only, resistance-only, and combination exercise.
Strengths & Limitations
The current analysis was the first to show a direct effect of prenatal exercise FITT-V on birth and placental outcomes. The study is strengthened by a large sample size of participants from rigorous supervised RCT exercise intervention trials. The measures were done as standard procedure at the local hospital and thus were blinded to group allocation. The variety of outcomes obtained at birth offer a holistic image on the effects of prenatal exercise FITT-V on birth and placental outcomes. However, the study was limited in a couple aspects. First, prenatal exercise FITT-V was controlled within a prescribed range, which limits our investigation of high- and low- FITT-V; however, this is a critical step to demonstrating the dose-dependent influence of exercise on beneficial pregnancy and birth outcomes. Second, although some delivery measures were obtained as standard hospital procedures after delivery and may have interindividual differences between nurses, these are standard processes in the hospital setting, thus, most likely have a small margin of error [52,53]. Overall, these initial findings are supportive of growing research in this area and support further work on this topic.
CONCLUSION
These exploratory findings contribute significantly to guiding future prenatal exercise recommendations. Prenatal exercise frequency, intensity, and weekly and total volume are predictive measures of fetal growth and health. Interestingly, our data suggest that prenatal exercise FITT-V influences birth outcomes differentially across prenatal exercise types. Future research should address the potential benefits of a broader range of frequency, intensity, time, and volume in the pregnant population. These promising findings suggest that every minute and every session of exercise during pregnancy is important, as well as intensity, throughout the pregnancy for improved birth and placental outcomes.
Supplementary Material
Acknowledgements:
We thank the women who participated in this study and who gave their time and effort.
Sources of Funding:
American Heart Association grants #15GRNT24470029 and #18IPA34150006, as well as internal funds provided by East Carolina University. Curation of funds only. Funding sources were not involved in study design or the collection, analysis, and interpretation of data.
Footnotes
Conflicts of Interest: The authors report no conflict of interest.
Clinical Trial Registration: ClinicalTrials.gov Identifier: NCT03517293
Data Availability:
Data generated/analyzed during the current study is available upon request from the corresponding/senior author.
REFERENCES
- 1.McDonald SM, Mouro S, Wisseman B, et al. Influence of prenatal exercise on the relationship between maternal overweight and obesity and select delivery outcomes. Sci Rep. 2022;12:17343. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Allman BR, McDonald S, May L, et al. Resistance Training as a Countermeasure in Women with Gestational Diabetes Mellitus: A Review of Current Literature and Future Directions. Sports Medicine. 2022;52:2871–88. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Jevtovic F, Zheng D, Houmard JA, et al. Effects of Maternal Exercise Modes on Glucose and Lipid Metabolism in Offspring Stem Cells. J Clin Endocrinol Metab. 2023;108:e360–70. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.McDonald SM, May LE, Hinkle SN, et al. Maternal Moderate-to-Vigorous Physical Activity before and during Pregnancy and Maternal Glucose Tolerance: Does Timing Matter? Med Sci Sports Exerc. 2021;53:2520–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Takami M, Tsuchida A, Takamori A, et al. Effects of physical activity during pregnancy on preterm delivery and mode of delivery: The Japan Environment and Children’s Study, birth cohort study. PLoS One. 2018;13:e0206160. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.McDonald SM, Liu J, Wilcox S, et al. Does dose matter in reducing gestational weight gain in exercise interventions? A systematic review of literature. J Sci Med Sport. 2016;19:323–35. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Duncombe D, Skouteris H, Wertheim EH, et al. Vigorous exercise and birth outcomes in a sample of recreational exercisers: A prospective study across pregnancy. Aust N Z J Obstet Gynaecol. 2006;46:288–92. [DOI] [PubMed] [Google Scholar]
- 8.Davenport MH, Ruchat S-M, Sobierajski F, et al. Impact of prenatal exercise on maternal harms, labour and delivery outcomes: a systematic review and meta-analysis. Br J Sports Med. 2019;53:99–107. [DOI] [PubMed] [Google Scholar]
- 9.Clapp JF. The effects of maternal exercise on early pregnancy outcome. Am J Obstet Gynecol. 1989;161:1453–7. [DOI] [PubMed] [Google Scholar]
- 10.Bonnin P, Bazzi-Grossin C, Ciraru-Vigneron N, et al. Evidence of fetal cerebral vasodilatation induced by submaximal maternal dynamic exercise in human pregnancy. J Perinat Med. 1997;25:63–70. [DOI] [PubMed] [Google Scholar]
- 11.Wolfe LA, Hall P, Webb KA, et al. Prescription of Aerobic Exercise During Pregnancy. Sports Medicine. 1989;8:273–301. [DOI] [PubMed] [Google Scholar]
- 12.Beetham KS, Giles C, Noetel M, et al. The effects of vigorous intensity exercise in the third trimester of pregnancy: a systematic review and meta-analysis. BMC Pregnancy Childbirth. 2019;19:281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Lokey EA, Tran ZV, Wells CL, et al. Effects of physical exercise on pregnancy outcomes: a meta-analytic review. Med Sci Sports Exerc. 1991;23:1234–9. [PubMed] [Google Scholar]
- 14.Hall DC, Kaufmann DA. Effects of aerobic and strength conditioning on pregnancy outcomes. Am J Obstet Gynecol. 1987;157:1199–203. [DOI] [PubMed] [Google Scholar]
- 15.SMA statement the benefits and risks of exercise during pregnancy. J Sci Med Sport. 2002;5:11–9. [DOI] [PubMed] [Google Scholar]
- 16.Fernández-Buhigas I, Martin Arias A, Vargas-Terrones M, et al. Fetal and maternal Doppler adaptation to maternal exercise during pregnancy: a randomized controlled trial. The Journal of Maternal-Fetal & Neonatal Medicine. 2023;36. doi: 10.1080/14767058.2023.2183759 [DOI] [PubMed] [Google Scholar]
- 17.Perales M, Santos-Lozano A, Ruiz JR, et al. Benefits of aerobic or resistance training during pregnancy on maternal health and perinatal outcomes: A systematic review. Early Hum Dev. 2016;94:43–8. [DOI] [PubMed] [Google Scholar]
- 18.Silva-Jose C, Sánchez-Polán M, Barakat R, et al. A Virtual Exercise Program throughout Pregnancy during the COVID-19 Pandemic Modifies Maternal Weight Gain, Smoking Habits and Birth Weight-Randomized Clinical Trial. J Clin Med. 2022;11. doi: 10.3390/jcm11144045 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Uria-Minguito A, Silva-José C, Sánchez-Polán M, et al. The Effect of Online Supervised Exercise throughout Pregnancy on the Prevention of Gestational Diabetes in Healthy Pregnant Women during COVID-19 Pandemic: A Randomized Clinical Trial. Int J Environ Res Public Health. 2022;19. doi: 10.3390/ijerph192114104 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Silva-Jose C, Sánchez-Polán M, Barakat R, et al. Exercise throughout Pregnancy Prevents Excessive Maternal Weight Gain during the COVID-19 Pandemic: A Randomized Clinical Trial. J Clin Med. 2022;11. doi: 10.3390/jcm11123392 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Gascoigne EL, Webster CM, Honart AW, et al. Physical activity and pregnancy outcomes: an expert review. Am J Obstet Gynecol MFM. 2023;5:100758. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Juhl M, Andersen PK, Olsen J, et al. Physical Exercise during Pregnancy and the Risk of Preterm Birth: A Study within the Danish National Birth Cohort. Am J Epidemiol. 2008;167:859–66. [DOI] [PubMed] [Google Scholar]
- 23.Davenport MH, Meah VL, Ruchat S-M, et al. Impact of prenatal exercise on neonatal and childhood outcomes: a systematic review and meta-analysis. Br J Sports Med. 2018;52:1386–96. [DOI] [PubMed] [Google Scholar]
- 24.Davenport MH, Kathol AJ, Mottola MF, et al. Prenatal exercise is not associated with fetal mortality: a systematic review and meta-analysis. Br J Sports Med. 2019;53:108–15. [DOI] [PubMed] [Google Scholar]
- 25.Mottola MF. The role of exercise in the prevention and treatment of gestational diabetes mellitus. Curr Diab Rep. 2008;8:299–304. [DOI] [PubMed] [Google Scholar]
- 26.Birsner ML, Gyamfi-Bannerman C. Committee on Obstetric Practice Physical Activity and Exercise During Pregnancy and the Postpartum Period. ACOG Committee Opinion Number. 2015;804. [Google Scholar]
- 27.Moyer C, Reoyo OR, May L. The Influence of Prenatal Exercise on Offspring Health: A Review. Clin Med Insights Womens Health. 2016;9:37. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Harris PA, Taylor R, Thielke R, et al. Research electronic data capture (REDCap)—A metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42:377–81. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Ainsworth BE, Haskell WL, Herrmann SD, et al. 2011 Compendium of Physical Activities. Med Sci Sports Exerc. 2011;43:1575–81. [DOI] [PubMed] [Google Scholar]
- 30.Miot HA. Correlation analysis in clinical and experimental studies. J Vasc Bras. 2018;17:275–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Rothman KJ. No adjustments are needed for multiple comparisons. Epidemiology. 1990;1:43–6. [PubMed] [Google Scholar]
- 32.Beetham KS, Spathis JG, Hoffmann S, et al. Longitudinal association of physical activity during pregnancy with maternal and infant outcomes: Findings from the Australian longitudinal study of women’s health. Women’s Health. 2022;18:174550572211423. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Li J, Huang D, Liang J, et al. Physical activity during pregnancy and adverse birth outcome: a prospective cohort study in China. The Journal of Maternal-Fetal & Neonatal Medicine. 2023;36. doi: 10.1080/14767058.2022.2162819 [DOI] [PubMed] [Google Scholar]
- 34.Chasan-Taber L, Evenson KR, Sternfeld B, et al. Assessment of Recreational Physical Activity During Pregnancy in Epidemiologic Studies of Birthweight and Length of Gestation: Methodologic Aspects. Women Health. 2007;45:85–107. [DOI] [PubMed] [Google Scholar]
- 35.Sahiledengle B, Tekalegn Y, Zenbaba D, et al. Which Factors Predict Hospital Length-of-Stay for Children Admitted to the Neonatal Intensive Care Unit and Pediatric Ward? A Hospital-Based Prospective Study. Glob Pediatr Health. 2020;7:2333794X2096871. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Clapp JF. The effects of maternal exercise on fetal oxygenation and feto-placental growth. European Journal of Obstetrics & Gynecology and Reproductive Biology. 2003;110:S80–5. [DOI] [PubMed] [Google Scholar]
- 37.Clapp JF, Kim H, Burciu B, et al. Continuing regular exercise during pregnancy: Effect of exercise volume on fetoplacental growth. Am J Obstet Gynecol. 2002;186:142–7. [DOI] [PubMed] [Google Scholar]
- 38.American College of Obstetricians and Gynecologists. Physical Activity and Exercise During Pregnancy and the Postpartum Period. Obstetrics & Gynecology. 2020;135:e178–88. [DOI] [PubMed] [Google Scholar]
- 39.Hatch M, Levin B, Shu XO, et al. Maternal leisure-time exercise and timely delivery. Am J Public Health. 1998;88:1528–33. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.McDonald S, Satterfield NA, May LE, et al. Influence of maternal exercise on fetal heart response during labor and delivery. Health Sci Rep. 2018;1:e81. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Morris S. Length and ponderal index at birth: associations with mortality, hospitalizations, development and post-natal growth in Brazilian infants. Int J Epidemiol. 1998;27:242–7. [DOI] [PubMed] [Google Scholar]
- 42.Cole TJ, Henson GL, Tremble JM, et al. Birthweight for length: ponderal index, body mass index or Benn index? Ann Hum Biol. 1997;24:289–98. [DOI] [PubMed] [Google Scholar]
- 43.Pastorino S, Bishop T, Crozier S, et al. Associations between maternal physical activity in early and late pregnancy and offspring birth size: remote federated individual level meta-analysis from eight cohort studies. BJOG. 2019;126:459–70. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Edwards CW, Al Khalili Y. Moro Reflex. StatPearls Publishing; 2023. [Google Scholar]
- 45.Modrell AK, Tadi P. Primitive Reflexes. StatPearls Publishing; 2023. [Google Scholar]
- 46.McMillan AG, May LE, Gaines GG, et al. Effects of Aerobic Exercise during Pregnancy on 1-Month Infant Neuromotor Skills. Med Sci Sports Exerc. 2019;51:1671–6. [DOI] [PubMed] [Google Scholar]
- 47.May LE, Glaros A, Yeh HW, et al. Aerobic exercise during pregnancy influences fetal cardiac autonomic control of heart rate and heart rate variability. Early Hum Dev. 2010;86:213–7. [DOI] [PubMed] [Google Scholar]
- 48.May L, Drake W, Suminski R, et al. Effects of Exercise during Pregnancy on Pediatric Heart Measures. J Cardiobiol. 2014;1:6. [Google Scholar]
- 49.Yu H, Santos-Rocha R, Radzimiński Ł, et al. Effects of 8-Week Online, Supervised High-Intensity Interval Training on the Parameters Related to the Anaerobic Threshold, Body Weight, and Body Composition during Pregnancy: A Randomized Controlled Trial. Nutrients. 2022;14:5279. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Bø K, Artal R, Barakat R, et al. Exercise and pregnancy in recreational and elite athletes: 2016 evidence summary from the IOC expert group meeting, Lausanne. Part 1—exercise in women planning pregnancy and those who are pregnant. Br J Sports Med. 2016;50:571–89. [DOI] [PubMed] [Google Scholar]
- 51.Siebel AL, Carey AL, Kingwell BA. Can exercise training rescue the adverse cardiometabolic effects of low birth weight and prematurity? Clin Exp Pharmacol Physiol. 2012;39:944–57. [DOI] [PubMed] [Google Scholar]
- 52.Doull IJ, McCaughey ES, Bailey BJ, et al. Reliability of infant length measurement. Arch Dis Child. 1995;72:520–1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53.Bhushan V, Paneth N. The reliability of neonatal head circumference measurement. J Clin Epidemiol. 1991;44:1027–35. [DOI] [PubMed] [Google Scholar]
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Supplementary Materials
Data Availability Statement
Data generated/analyzed during the current study is available upon request from the corresponding/senior author.