Maternal obesity has emerged as one of the greatest challenges in modern obstetrics. Approximately half of women of reproductive age are either overweight (body mass index [BMI, calculated as weight (kg)/[height (m)]2] 25.0 or greater) or obese (30.0 or greater).1,2 Maternal obesity has been linked with adverse pregnancy outcomes, including gestational diabetes mellitus (GDM), which is defined as “glucose intolerance with onset or first recognition during pregnancy.”3,4 Increasing severity of maternal obesity leads to a higher risk of GDM with a two-, four-, and eightfold risk of GDM for overweight, obese, and severely obese women, respectively.5
With growing obesity internationally and escalating GDM rates, effective preventive strategies are required to avoid the adverse outcomes associated with obesity and hyperglycemia during pregnancy.6 Outside pregnancy, lifestyle interventions have reduced the incidence of subsequent type 2 diabetes mellitus.7,8 Pregnancy often results in a reduction in exercise and physical activity levels with obese women exercising least before and during pregnancy.9,10
This study aimed to evaluate whether an intensive, medically supervised exercise intervention for women with BMIs of 30.0 or greater reduced the mean fasting plasma glucose concentration by 6.9 mg/dL (0.4 mmol/L) at 24–28 weeks of gestation in the intervention group compared with women undergoing routine prenatal care alone. This was deemed clinically important following the Hyperglycemia and Adverse Pregnancy Outcomes (HAPO) Study, which demonstrated increased risk of adverse pregnancy outcomes with an increase of fasting plasma glucose by 1 SD, that is, 6.9 mg/dL (0.4 mmol/L).11
MATERIALS AND METHODS
The Healthy eating, Exercise and Lifestyle Trial study was a single-center randomized controlled trial (RCT) that was conducted from November 2013 through April 2016 at the Coombe Women and Infants University Hospital, Dublin, Ireland. All women provided written informed consent before recruitment. Eligible women had BMIs at their first prenatal visit of 30 or greater, underwent ultrasound confirmation of an ongoing pregnancy less than 17 weeks of gestation, understood English, were older than 18 years, and were able to give consent. Exclusion criteria were multiple pregnancy, pre-existing diabetes, hypertension, alcohol or drug abuse, medication affecting insulin secretion or sensitivity, serious cardiorespiratory disorders, hepatic or renal impairment, systemic lupus erythematosus, hematologic disorders, celiac disease, thyroid disorders, current psychosis, malignant disease, or known fetal anomaly.
The ParMed-X for pregnancy form was used to rule out contraindications to exercise in pregnancy.12 At assessment for eligibility, women were informed that this was a RCT of closely supervised exercise during pregnancy to evaluate its ability to improve maternal glycemia. The control group received standard hospital written information on exercise. As part of routine prenatal care in Ireland, all women receive a pamphlet with information on healthy eating based on our national guidelines for nutrition and pregnancy. All obese women are routinely offered screening for GDM with a 75-g oral glucose tolerance test (OGTT) at 24–28 weeks of gestation and the diagnosis is based on the International Association of Diabetes in Pregnancy Studies Group criteria.13
The randomization sequence was computer-generated by an independent statistician and was stratified by parity and World Health Organization BMI category.14 Sequentially numbered opaque sealed envelopes were prepared by an independent research administrator. Women were randomized by another independent research administrator into either the exercise intervention or control arm. The clinical teams caring for the women were blinded to the randomization result.
Women randomized to the exercise intervention group were invited to participate in three medically supervised exercise classes per week for the duration of their pregnancy and for up to 6 weeks postpartum. The potential benefits of participation were outlined, and individual “SMART” (specific, measurable, achievable, relevant, and time-specific) personal goals were set.
Attendance at the intervention class was recorded by both participants and the researcher. Women in the intervention arm also received an invitation to a secret Facebook group to create a sense of community among participants, to share healthy lifestyle advice, and to improve compliance with the exercise intervention. The program consisted of 50–60 minutes of exercise with a 10-minute warm-up, 15–20 minutes of resistance or weights, 15–20 minutes of aerobic exercises, and a 10-minute cool-down. The warm-up focused on core and pelvic floor exercises. The resistance session worked muscle groups important for a healthy pregnancy and birth recovery, the lower limb, upper limb, back, and core muscle groups. Exercises were scaled according to ability. Cardiovascular training aimed to increase maternal heart rates and exertion was monitored with the Borg Scale of Perceived Exertion, as recommended by the American College of Obstetricians and Gynecologists.15,16
Measures were taken to improve compliance with the intervention, including goal-setting and journaling of class. Classes were designed such that no woman was alone or isolated during a class. A “kids’ corner” with toys and a mat and playpen for babies helped ensure that childcare was not a barrier. Eleven classes were taught each week, on a choice of days, at 7:30 AM, 11:45 AM, and 5:30 PM. Classes varied each day to maintain interest.
The primary outcome was a clinically important reduction in the mean fasting plasma glucose in the intervention group by 6.9 mg/dL (0.4 mmol/L) when compared with the control group, measured at the time of a standard 75-g OGTT at 24–28 weeks of gestation to screen for GDM.
The secondary outcomes investigated the effects of the exercise intervention on longitudinal fasting plasma glucose concentrations and the incidence of GDM at the time of the OGTT at 24–28 weeks of gestation; birth outcomes: induction of labor, mode of delivery and length of labor, birth weight, birth weight centile less than 10th and greater than 90th centiles, gestational age at delivery, preterm births, admission to neonatal intensive care unit, abnormal Apgar scores less than 7 at 1 and 5 minutes; and gestational weight gain: mean gestational weight gain at 24–28 and 36 weeks of gestation, excessive gestational weight gain greater than 9.1 kg at 36 weeks of gestation, and mean postpartum weight retention at 6 weeks postpartum.
The data were anonymized on an Excel spreadsheet before being exported to the statistical software program SPSS 20.0.0 for statistical analysis. The normality of continuous data was assessed using descriptive statistics for kurtosis and skewness, visual inspection of distribution histograms, and the Kolmogorov-Smirnoff statistics. Data were analyzed by intention to treat, including women who did not participate in the intervention and excluding women without follow-up measurements. Because glucose tolerance testing at 24–28 weeks of gestation is part of routine care for obese women, even among those who did not return to the research team for follow-up, we were able to obtain their glucose results. For those who did not return to the research team for follow-up of other outcome measures, there were no differences in demographic, anthropometric, or fasting plasma glucose measurements in early pregnancy or at 28 weeks of gestation. Missing data were therefore coded for in the statistical software program and discarded in the analysis. The relevant continuous data were collapsed into categories. Descriptive statistics were used to describe the characteristics of the study cohort. Categorical data were reported as proportions and calculated as proportions of those with available data. Continuous data were reported as mean and SD or median and interquartile range and were calculated on available data. χ2, Fisher exact test, and nonparametric tests were used to assess differences in proportions and independent t tests were used to assess differences in means between control and exercise intervention groups.
Each woman visited the research team for data collection at recruitment, 24–28 weeks of gestation and 36 weeks of gestation, at delivery, and at 6 weeks postpartum. Because the primary outcome was a reduction in the mean fasting plasma glucose, the accuracy of this measurement was of critical importance. The American Diabetes Association and the International Association of Diabetes and Pregnancy Study Groups recommend implementing antiglycolytic strategies when using glucose measurements to diagnose diabetes mellitus.4,13
Glycolysis rates in sample tubes depend on the length of time before separation of the cells from the plasma, the temperature at which the tube is held, and the antiglycolytic agents in the tubes.4,13,17 Unless glucose samples are collected into a tube containing fluoride and immediately placed on an iced slurry and analyzed within 30 minutes of collection (as recommended by the American Diabetes Association), the glucose concentration will drop. In previous studies, a lack of preanalytical vigilance resulted in missing 58% of cases of GDM.4,18,19
For the purpose of this study, research glucose samples were collected according to the American Diabetes Association recommendations.4,17–21 Concurrently, each woman had a second sample collected under routine conditions (into a fluoride tube, not placed on ice, all three transported to the laboratory together). The routine sample was reported to the clinical team and not to the research team. The research sample was blinded to clinical and research teams and reported to the research team at the end of the study.
Weight and height were measured directly at the first prenatal visit and used to calculate BMI for eligibility for the study.22 Weight was measured directly at each research visit thereafter. Gestational weight gain was measured as the difference between the weight at 36 weeks of gestation and the weight at the first visit. Gestational weight gain was determined at 36 weeks of gestation to avoid missing data because women delivered after this point. Excessive gestational weight gain in obese patients is defined as greater than 9.1 kg by the Institute of Medicine.23
Delivery outcomes were entered in computerized form by the midwife in the labor ward. Each woman's details were checked by a member of the research team. Data collected included mode of onset of labor, mode of delivery, length of labor, birth weight, Apgar scores, and admission to the neonatal intensive care unit.
Power calculation determined that a sample size of 24 per group would be required based on an independent-sample t test for statistical power of 80% at a type I error rate of 0.05 to detect a difference of 0.4 mmol/L (6.9 mg/dL) in fasting plasma glucose between groups and assuming a SD of 0.48 mmol/L averaged across previous reported values.11,18 Based on previous studies on obese pregnant women and the personal time commitment required from women in the intervention arm, we expected a high rate of dropouts in the intervention arm. As such, we planned to recruit 44 to each arm to allow for a 33% dropout rate.10,24
The study protocol was approved by the Coombe Women and Infants University Hospital Research Ethics Committee in October 2012 (ref: 26-2011). The trial was prospectively registered with the International Standard Randomised Controlled Trials Number Registry and assigned the trial number ISRCTN31045925.
From November 2013 to August 2015, 337 women were assessed for eligibility for the study (Fig. 1). Fifty-nine women met the exclusion criteria. Of these, four did not have adequate English, 20 were greater than 17 weeks of gestation at recruitment, there were two multiple pregnancies, 27 had maternal medical problems, and six had fetal complications including miscarriage. One hundred ninety women declined to participate, citing no time or work commitments as the most common primary reasons. Therefore, 88 women were recruited, 44 in the intervention group and 44 in the control group. There were no differences in the characteristics of the women between the two arms of the study (Table 1). Eight women in the control group and 11 in the intervention group did not complete the trial at 6 weeks postpartum (P=.61), but 43 in each group attended the 24- to 28-week glucose screen.
Of 44 women randomized to the exercise group, five women did not participate. Four were nulliparous; mean age was 30.0±7.3 years, mean weight was 86.7±19.3 kg, and mean BMI was 33.2 (range 30.4–40.7). Two women cited lack of time and three did not explain why. Four of the five attended the clinical team for their OGTT and the results were analyzed by intention to treat. All 88 women in the study had access to the internet. Of the women receiving the intervention, 75% (n=33) attended for follow-up at 6 weeks postpartum compared with 81.8% (n=36) in the control group (P=.44). The mean antenatal attendance was 28±16 exercise classes (range 2–65). Women commenced classes at a mean of 13 4/7±1 2/7 weeks of gestation. The overall attendance rate was 78.9% (671/850 of classes offered were attended). Of the 44 women in the intervention group, 64% (n=28) attended on average a minimum of one class per week; 41% (n=18) attended a minimum of 50% of classes (three classes every 2 weeks). The mean number of classes attended before the OGTT was 15±10 classes. All women attended more classes before than after the OGTT.
Of the glucose samples, 97.5% (477/489) were handled strictly according to the American Diabetes Association preanalytical handling recommendations. The mean gestation at which the early pregnancy fasting plasma glucose was measured was 13 2/7±1 4/7 weeks of gestation. The number of women with an elevated fasting plasma glucose (92–125 mg/dL) in early pregnancy was 51.1% (n=45/88). There was no difference in the primary outcome—mean fasting plasma glucose at 24–28 weeks of gestation—between groups: 90.0±9.0 mg/dL in the control group compared with 93.6±7.2 mg/dL in the exercise group (P=.13), as shown in Tables 2 and 3. There was no difference in mean fasting plasma glucose concentrations at each research visit or in the 1- and 2-hour glucose concentrations between groups as presented in Tables 2 and 3. The incidence of GDM at 24–28 weeks of gestation was 48.8% (n=21/43) in the control group compared with 58.1% (n=25/43) in the exercise group (P=.51). There were no cases of type 2 diabetes mellitus at 6 weeks postpartum (n=0/69).
A breakdown of the number of women with a fasting plasma glucose 92 mg/dL or greater in early pregnancy and at 24–28 weeks of gestation and a positive OGTT at 24–28 weeks of gestation is shown in Figures 2 and 3, respectively. The overall positive predictive value and negative predictive value of an early pregnancy fasting plasma glucose 92 mg/dL or greater for a positive OGTT at 24–28 weeks of gestation were 34 of 44 (77.3%; 95% CI 64.9–89.7%) and 30 of 42 (71.4%; 95% CI 57.7–85.1%), respectively. Figures 4 and 5 outline the proportion of positive OGTTs at 24–28 weeks of gestation in the control and exercise intervention groups, respectively, according to the fasting 1- and 2-hour tests.
In the early pregnancy clinical samples, 25% (n=11/44) in the control arm and 22.7% (n=10/44) in the intervention arm had a fasting plasma glucose 92 mg/dL or greater (lower than in the research samples, owing to preanalytical sample handling). Of the 21, all underwent an OGTT under routine conditions. Five were positive and were directed to the multidisciplinary team for further management. All five were advised to self-monitor blood glucose levels. Two women were from the control group and three were in the exercise group. Of the three in the exercise group, one required insulin treatment immediately, one received metformin treatment, and one received diet and lifestyle advice alone. Of the two women from the control group, one received diet and lifestyle advice alone and one received metformin treatment. None of the women had fasting plasma glucose levels diagnostic of overt diabetes in early pregnancy but were diagnosed with GDM and were left in the analysis because our predefined exclusion criteria excluded women at recruitment with pre-existing diabetes mellitus, not newly diagnosed GDM.
The mean weights at recruitment, 24–28 weeks of gestation, 36 weeks of gestation, and 6 weeks postpartum were 95.8±15.8 (n=44) compared with 93.9±14.8 kg (n=44) (P=.56); 101.1±15.4 (n=43) compared with 98.8±13.7 kg (n=43) (P=.49); 103.6±15.6 (n=42) compared with 101.1±13.9 kg (n=34) (P=.46); and 96.8±16.2 (n=36) compared with 91.9±14.1 kg (n=33) (P=.19) in the control and exercise intervention groups, respectively. In those with complete data collected, there was no difference in mean gestational weight gain at 28 (4.9±3.8 [n=43] compared with 3.8±3.9 kg [n=43], P=.19) or 36 weeks of gestation (7.9±4.8 [n=42] compared with 6.2±6.0 [n=34] kg, P=.15) nor was there a difference in postpartum weight retention (0.2±5.4 [n=36] compared with –1.6±1.2 kg [n=33], P=.22) at 6 weeks postpartum. Excessive gestational weight gain was, however, lower in the intervention group: 22.2% (n=8) compared with 43.2% (n=19; P<.05). Mean gestational weight gain is shown in Figure 6. One outlier in the intervention group did not receive the intervention. At 6 weeks postpartum, 67% (n=22/33) of the exercise group and 47% (n=17/36) women in the control group returned to their prepregnancy weight or less (P=.10). There was no correlation between gestational weight gain and the number of exercise classes attended (Fig. 7).
There were no differences in birth outcomes between the control and intervention groups (Table 4). There was no difference in mean birth weight: 3,534.0±552.3 g in the control group compared with 3,532.2±477.1 g in the exercise group (P=.99). Using customized birth weight centiles, there was no difference between groups in neonates greater than the 90th centile or less than the 10th centile. No adverse events were reported for the intervention group. In particular, there was no increase in preterm birth or low birth weight with the exercise intervention, although the study was not powered statistically for these outcomes.
We found that an intensive, medically supervised exercise intervention from early pregnancy did not improve maternal glycemia in obese women by the time of their OGTT at 24–28 weeks of gestation, although it did reduce the number of women with excessive gestational weight gain greater than 9.1 kg at 36 weeks of gestation. More women had an abnormal fasting plasma glucose 92 mg/dL or greater in early pregnancy (n=45/88 [51.1%]) than we expected. This may be because 26.1% (n=23/88) of the women in our study were in the obese II category and 11.4% (n=10/88) in the obese III category. It is also because of preanalytical sample handling.
A strength of our study was the strict standardization of the measurements of maternal plasma glucose, BMI, and gestational weight gain.4,17–22 We also contribute data on glucose concentrations throughout pregnancy, data that are limited in the literature. We achieved improved levels of engagement with the intervention arm compared with another study with a similar population (28/44 [63.6%] attended one class per week compared with 10/62 [16.3%], P<.001).24 This was augmented by compliance-improving measures. It was disappointing that two thirds of eligible women declined to participate. Nonetheless, the recruitment rates compared favorably with two other prenatal exercise RCTs.24,25
Our study may have failed to improve maternal glycemia because the ideal time to begin such a program could be before pregnancy. Preconceptional recruitment of obese women for an RCT of structured exercise, however, would be difficult. Furthermore, attendance at our exercise classes occurred at a rate of approximately one class per week, which is insufficient to affect maternal glucose levels. There may have been no correlation between exercise classes attended and gestational weight gain because only one of the five women who did not participate in the intervention attended the 36-week research appointment for data collection; therefore, we did not have follow-up data on those who did not attend.
Recent exercise studies aiming to optimize pregnancy outcomes have faced challenges.24–27 The UPBEAT study, a large multicenter lifestyle intervention RCT of more than 1,500 obese women in the United Kingdom, showed a reduction in gestational weight gain of 430 g without an effect on GDM.25 Although on a much larger scale, this intervention was not as intensive as ours in terms of frequency and intensity of the intervention and personal contact. Each participant attended a single one-on-one appointment with the trainer, was invited to weekly behavior modification group sessions for 8 consecutive weeks from 19 weeks of gestation, and received an exercise DVD.28
The single-center Norwegian ETIP exercise RCT for obese pregnant women did not affect gestational weight gain. There was a reduction in the incidence of GDM (6.1% compared with 27.3%, P=.04) as defined by the World Health Organization 2009 criteria but no reduction using the International Association of Diabetes and Pregnancy Study Groups criteria (14.7% compared with 24.2%, P=.42). Half of the exercise group adhered to the protocol.29
Some studies have reported a reduction in the risk of GDM with exercise, but these studies included both normal and overweight women and commenced early in pregnancy from 6 to 10 weeks of gestation.30–32 Explanations for a lack of success included suboptimal compliance or an intervention not vigorous enough to improve maternal glycemia. None of these studies reported their preanalytical or analytical laboratory standards.24–32
It might be argued that a fasting plasma glucose 92 mg/dL or greater in early pregnancy is not diagnostic of GDM as recommended by the International Association of Diabetes and Pregnancy Study Groups, because the criteria were based on data collected for the Hyperglycemia and Adverse Pregnancy Outcomes Study in the late second and early third trimesters, not in early pregnancy. Early pregnancy fasting plasma glucose 92–125 mg/dL was previously reported to have poor predictability for the diagnosis of GDM. McIntyre et al,33 however, did not describe their preanalytical glucose sample handling methods. In contrast, our findings suggest that fasting plasma glucose in early pregnancy has better positive and negative predictive value for the diagnosis of GDM at 24–28 weeks of gestation.
This study showed that an intensive, medically supervised exercise intervention for obese women from early pregnancy did not improve maternal glycemia. Pregnant women who are obese, however, should be advised to exercise because it attenuates excessive gestational weight gain.
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© 2017 by The American College of Obstetricians and Gynecologists. Published by Wolters Kluwer Health, Inc. All rights reserved.
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