Abstract
Exercise is often recommended in addition to diet and medication in the management of gestational diabetes mellitus (GDM). Our aim was to determine if strength training compared with aerobic exercise had an impact on glycaemic control, maternal and neonatal outcomes. The Cochrane library, Embase, PubMed, CINAHL, Medline, Google Scholar, and OpenGrey were searched. Over 758 pregnant women (mother-baby pairs) from 14 studies are included in this systematic review. Interventions ranged from cycling, aerobic exercises, walking, yoga, or combined aerobic and resistance exercises. Of the studies identified, none directly compared aerobic exercise with strength training. Half of the studies showed benefit in glycaemic control with additional exercise compared with usual physical activity. There was largely no impact on obstetric or neonatal outcomes. Studies on exercise in GDM have reiterated the safety of exercise in pregnancy and shown mixed effects on maternal glycaemic control, with no apparent impact on pregnancy outcomes. The heterogenicity of reported studies make it difficult to make specific recommendations on the optimum exercise modality for the management of GDM. The use of a core outcome set for GDM may improve reporting of studies on the role of exercise in its management.
Keywords: exercise, pregnancy, gestational diabetes, aerobic, strength
1. Introduction
Gestational diabetes (GDM) is defined as new onset maternal hyperglycemia in pregnancy that resolves after birth [1]. Diabetes affects one in six pregnancies worldwide, of which the majority is GDM [2]. The rate of GDM diagnosed in pregnancy has increased over the last decade, with predictions of further increases worldwide [2,3]. GDM is associated with increased maternal and fetal morbidity and mortality [4,5]. Women with GDM are at a significantly increased risk of developing type 2 diabetes (T2DM) in later life [6]. Maintaining good glycaemic control can improve maternal and infant health outcomes [7].
Exercise is considered to be an important component of the management of GDM [8,9]. Outside of pregnancy, structured exercise is effective in improving diabetic control in patients with insulin resistance [10,11,12]. Pregnancy is a state of relative insulin resistance. Aerobic and resistance exercise have different metabolic effects and therefore both have a potential role in the treatment of insulin resistance seen in GDM [13,14,15].
Many studies have looked at the effect of exercise in the prevention of hypertensive disorders of pregnancy [16,17], pelvic or back pain [18,19,20], preterm birth [21,22], incontinence [23,24], and mental health disorders [25,26]. Most of the systematic reviews published on exercise in GDM have concentrated on exercise as a preventive measure to reduce the rate of GDM diagnosis [27,28,29].
We hypothesise that the type of exercise (either strength, aerobic, or combination) has an impact on glycaemic control and therefore health outcomes for both the mother and fetus. The aim of this systematic review was to update and consolidate the evidence on the effect of exercise modality on both glycaemic control and obstetric outcomes in patients with GDM.
2. Materials and Methods
This systematic review of randomised controlled trials (RCTs) and cohort and case control studies was carried out following the protocol described in the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) statement [30]. Searches were initially performed from September to November 2019 and re-run in May 2021 prior to the final analyses so that further studies could be retrieved for inclusion. Electronic database searches were carried out using the following databases: Cochrane library, Embase, PubMed, Cochrane Central Register of Controlled Trial (CENTRAL), CINAHL, and Web of Science. Grey literature databases were also searched (Google Scholar and OpenGrey). Citation pearl indexing was also performed of previous systematic reviews, literature reviews, and guidelines. Studies were initially restricted to the last 15 years. There were no restrictions on language.
2.1. Data Sources and Search Strategy
Two reviewers (NK and CC) performed a search to identify RCTs that studied the effect of exercise (aerobic/resistance/any exercise) on glycaemic control or obstetric outcomes in pregnancies affected by GDM. The search strategy followed the PICO framework, using key words, free text, and MeSH terms as appropriate and combining Boolean operators of (AND/OR/NOT/quotation marks/brackets):
-
-
Participants: women, pregnancy, gestational diabetes, hyperglycaemia, diabetes
-
-
Intervention: exercise, aerobic, resistance
-
-
Comparison: physical activity, aerobic, resistance, control
-
-
Outcome: medication (insulin, metformin), glycaemic control, maternal outcome
Inclusion criteria were as follows:
Randomised controlled trials
Gestational diabetes mellitus
Intervention of resistance exercise or aerobic exercise alone or in combination
Comparator or control of either resistance, aerobic or no exercise
Exclusion criteria were:
Review or opinion articles
Studies without published results
Studies involving women with pre-existing diabetes
The primary outcome was glycaemic control in women with GDM (defined as average blood glucose levels or use of insulin and insulin requirements where it was required to maintain euglycaemia). Secondary outcomes were obstetric outcomes including rate of caesarean birth, perineal trauma, or duration of labour.
2.2. Study Selection
All articles retrieved for review were imported to Endnote and duplicates were removed. Titles, abstracts, and full text were independently reviewed by two reviewers (N.K. and C.C.) with reference to a third reviewer (M.F.H.) if required. Inclusion and exclusion criteria are reported in Table 1.
Table 1.
PICOS criteria for inclusion and exclusion of studies in this Systematic Review.
| Parameter | Inclusion | Exclusion |
|---|---|---|
|
Population/
participant |
Women Pregnancy Gestational diabetes Hyperglycaemia Diabetes in pregnancy Treatment of Gestational Diabetes |
Pre-gestational Diabetes Type 1 Diabetes Type 2 Diabetes Prevention of Gestational Diabetes |
| Intervention | Exercise, aerobic, resistance Lasting at least two weeks |
|
| Comparison | Normal physical activity Aerobic exercise Resistance Control Lasting at least two weeks |
|
| Outcome | Glycaemic control Maternal outcomes |
|
| Study Design | Randomised controlled trial No language restriction Published paper Published abstract |
Case report Case-control study Cohort study Commentary Guideline |
2.3. Data Extraction
Data extraction was independently performed by two researchers (N.K. and M.F.H.) using standardised electronic data extraction forms, saved on a shared drive after initial assessment, with reference to a third researcher (C.C.) as required. Missing data was to be requested from study authors. Data extraction was performed in accordance with the Cochrane Handbook for Systematic Review of Interventions [31]. Extracted data items included study reference details, study context, study design, study population, data analysis and methods, and research findings.
2.4. Quality Assessment
Bias of randomised trials was assessed using the Cochrane Risk of Bias (RoB2) tool [32]. This study was registered with PROSPERO (2020 CRD42020161454) [33] and is reported following the PRISMA statement for systematic reviews [30].
3. Results
3.1. Literature Search
Flow of studies through the stages of identification, screening, eligibility, and final inclusion is shown in Figure 1. Fourteen randomised controlled studies were selected for inclusion in this systematic review [34,35,36,37,38,39,40,41,42,43,44,45,46,47,48]. Two of the papers [41,47] reported different outcomes from one trial and for the purpose of this manuscript are referred to as one paper.
Figure 1.
Flow of studies through the systematic searching of the literature.
3.2. Characteristics
Characteristics of the fourteen studies are shown in Table 2 with risk of bias summary in Table 3 and results in Table 4. Study sizes ranged from six participants to 200 participants. In total, over 758 pregnant women (mother-baby pairs) are included in this systematic review. Length of intervention ranged from four to twelve weeks. Of the 14 papers analysed, five used aerobic exercise as the intervention, five used strength/flexibility-based exercise, two used a combined intervention, one did not specify the type of exercise used, and one compared strength or aerobic exercise with a control. Interventions ranged from supervised follow-up with a kinesiologist to cycling, aerobic exercises, walking, yoga, or combined aerobic and resistance exercises.
Table 2.
Characteristics of studies included: Sample characteristics, Duration of interventions, Intervention (Exercise) Characteristics and Outcomes.
| Author of RCT; Year Published Country |
Sample Characteristics | Duration of Intervention | Intervention (Exercise) Characteristics | Outcomes |
|---|---|---|---|---|
| Adam 2014 [34] |
Control n − 4 Intervention n = 39 |
Duration of pregnancy | Standard counselling for physical activity Supervised individuals follow up with kinesiologist |
Addition of insulin Mean dose of insulin Time to start insulin Weight gain |
| Avery 1997 [35] United States |
Control n = 14 GDM diagnosis 26.3 ± 8 weeks Intervention n = 15 GDM diagnosis 28.7 ± 3 weeks |
Six weeks | Usual physical activity 30 min supervised cycling with 30 min unsupervised walking |
Addition of insulin Caesarean birth Hypertensive disorders Maternal weight gain |
| Awad 2019 [48] Egypt |
Control n = 30 Diet plus insulin Intervention n = 30 Moderate intensity aerobic and circuit resistance exercise 3–4 times/week in addition to diet plus insulin |
24 weeks’ gestation until delivery | Diet plus insulin alone compared with combined strength and aerobic exercise plus diet plus insulin | Mode of delivery |
| Bambicini 2012 [36] |
Control n = 6 Intervention (aerobic) n = 6 Intervention (resistance) n = 5 |
Duration of pregnancy | Seated listening to explanations about exercise Aerobic or resistance exercises |
Mean glucose immediately after session and one hour later |
| Bo 2014 [37] Italy |
Control n = 99 GDM diagnosis 24–26 weeks Intervention n = 101 GDM diagnosis 24–26 weeks |
12–14 weeks | Not applicable Twenty minutes of unsupervised brisk walking seven times a week |
Addition of insulin Caesarean birth Glycaemic control |
| Brankston 2004 [38] Canada |
Control n = 16 GDM diagnosis: not reported Intervention n = 16 GDM diagnosis: not reported |
Eight weeks | Usual physical activity Resistance exercise on circuit: supervised for three sessions then supervised for three sessions per week |
Additional medications Glycaemic control |
| Bung 1991 [39] United States |
Control n = 17 GDM diagnosis: 30.3 ± 2 weeks Intervention n = 17 GDM diagnosis: 30.3 ± 1.9 weeks Note: control was diet and insulin; diagnosis of GDM was persistent fasting glucose >5.88 mM but <7.22 mM and “failed diet therapy for a week” |
Remainder of the pregnancy | Standard care Supervised in exercise laboratory: 45 min with breaks on recumbent bicycle |
Adherence to intervention Caesarean birth Hypoglycaemia Glycaemic control |
| De Barros 2010 [40] Brazil |
Control n = 32 GDM Diagnosis 27.5 ± 3 weeks Intervention n = 32 GDM Diagnosis 28.4 ± 2.5 weeks |
Eight weeks | Usual physical activity Resistance exercise (two supervised and one unsupervised) for 30–40 min |
Additional medications Caesarean birth Weight gain |
| Halse 2014 [41] Australia |
Control n = 20 GDM Diagnosis 28.8 ± 1 week Intervention n = 20 GDM Diagnosis 28.9 ± 1 week |
Six weeks | Usual physical activity Home cycle ergometer supervised three times a week and unsupervised for two sessions a week |
Additional medications Caesarean birth Induction of labour Patient views Weight gain |
| Jovanovic-Peterson 1989 [42] United States |
Control n = 9 GDM diagnosis at 28 weeks Intervention n = 10 GDM diagnosis at 28 weeks |
Six weeks | Usual physical activity Aerobic exercise: 20 min for three times a week, supervised, using ergometer |
Additional medications Adherence to intervention Hypertensive disorders Glycaemic control |
| Qadir 2018 [44] Singapore |
Control n = 5 GDM “newly diagnosed” Intervention n = 5 GDM “newly diagnosed” |
Eight weeks | Usual physical activity measured by pedometer Patient education and structured exercise class once a week Usual physical activity measured by pedometer |
Average daily steps Glycaemic control |
| Ramos 2015 [43] |
Control n = 4 Intervention n = 2 |
Ten weeks | 50 min stretching and relaxation once a week 50 min aerobic session three times a week |
Mean HbA1c Homeostatic model assessment (HOMA) |
| Sklempe Kocic 2018 [45] Croatia |
Control n = 20 GDM diagnosis: 20.8 ± 6 weeks Intervention n = 18 GDM diagnosis 22.2 ± 6 weeks |
Six weeks | Usual physical activity Combined aerobic and resistance exercise (two supervised sessions) plus seven sessions of unsupervised walking |
Additional medications Caesarean Birth Glycaemic control Weight gain |
| Youngwanichsetha 2014 [46] Thailand |
Control n = 85 GDM diagnosis: 24–30 weeks Intervention n = 85 GDM diagnosis: 24–30 weeks |
Eight weeks | Not applicable Fifteen to twenty minutes of supervised yoga five times a week |
Glycaemic control |
Table 3.
Risk of Bias Summary.
| Author of RCT; Year Published |
Selection Bias (Random Sequence Generation) |
Selection Bias (Allocation Concealment) | Performance Bias (Double Blinding) | Detection Bias (Blinding of Outcome Assessment) | Attrition Bias (Incomplete Outcome Data) | Reporting Bias (Selective Reporting) | Other Bias |
|---|---|---|---|---|---|---|---|
| Adam 2014 [34] | Unclear | Unclear | Unclear | Unclear | Unclear | Unclear | Unclear |
| Avery 1997 [35] | Low | Unclear | High | Unclear | High | Unclear | Low |
| Awad 2019 [48] | Unclear | Unclear | High | Unclear | Unclear | Unclear | Low |
| Bambicini 2012 [36] | Unclear | Unclear | Unclear | Unclear | Unclear | Unclear | Unclear |
| Bo 2014 [37] | Unclear | Low | High | Low | Low | Low | Low |
| Brankston 2004 [38] | Low | Low | High | High | Unclear | High | Unclear |
| Bung 1991 [39] | Unclear | Unclear | Unclear | Unclear | High | Unclear | Unclear |
| De Barros 2010 [40] | Low | Low | High | High | Low | Unclear | Low |
| Halse 2014 [41] | Unclear | Low | High | High | High | High | Low |
| Jovanovic-Peterson 1989 [42] | Low | Unclear | High | Unclear | Low | High | High |
| Qadir [44] | Unclear | Unclear | Unclear | Unclear | Unclear | Unclear | Unclear |
| Ramos 2015 [43] | Unclear | Unclear | Unclear | Unclear | Unclear | Unclear | Unclear |
| Sklempe Kocic 2018 [45] | Low | Unclear | High | Low | Low | High | Low |
| Youngwanichsetha 2014 [46] | Unclear | Unclear | High | Low | Low | High | Low |
Table 4.
Results.
| Paper | Intervention | Sample Characteristics | Main Outcome | Findings |
|---|---|---|---|---|
| Adam et al. [34] | Standard counselling for physical activity compared with supervised individual follow up with kinesiologist | Control n − 40 Intervention n = 39 |
Addition of insulin Mean dose of insulin Time to start insulin Weight gain |
No difference |
| Avery et al. [35] | Usual physical activity compared with supervised cycling and unsupervised walking | Control n = 14 GDM diagnosis 26.3 ± 8 weeks Intervention n = 15 GDM diagnosis 28.7 ± 3 weeks |
Addition of insulin Apgar < 7 at 1 min Apgar < 7 at 5 min Birthweight Caesarean birth Gestation at birth Hypertensive disorders Maternal weight gain |
No difference in insulin requirement No difference in CS, hypertensive disorders |
| Awad et al. [48] | Diet plus insulin alone compared with combined strength and aerobic exercise plus diet plus insulin | Control n = 30 Diet plus insulin Intervention = 30 Moderate intensity aerobic and circuit resistance exercise 3–4 times/week in addition to diet plus insulin |
Mode of delivery | Reduced CS rate in control group |
| Bambicini et al. [36] | Explanation about exercise compared with aerobic or strength-based exercise | Control n = 6 Intervention (aerobic) n = 6 Intervention (resistance) n = 5 |
Mean glucose immediately after session and one hour later | No difference |
| Bo et al. [37] | Twenty minutes of brisk walking 7 times per week | Control n = 99 GDM diagnosis 24–26 weeks Intervention n = 101 GDM diagnosis 24–26 weeks |
Addition of insulin Caesarean birth Glycaemic control |
No difference in insulin requirements, CS, macrosomia, fasting glucose Reduction in postprandial glucose and HbA1C with intervention |
| Brankston et al. [38] | Usual physical activity Resistance exercise on circuit: supervised for three sessions then supervised for three sessions per week |
Control n = 16 GDM diagnosis: not reported Intervention n = 16 GDM diagnosis: not reported |
Additional medications Glycaemic control |
Increased latency to insulin treatment in intervention group No difference in number of women requiring insulin or the dose used No difference in fasting or postprandial glucose levels |
| Bung et al. [39] | Standard care Supervised 45 min session on recumbent bicycle |
Control n = 17 GDM diagnosis: 30.3 ± 2 weeks Intervention n = 17 GDM diagnosis: 30.3 ± 1.9 weeks Note: control was diet and insulin; diagnosis of GDM was persistent fasting glucose >5.88 mM but <7.22 mM and “failed diet therapy for a week” |
Adherence intervention Caesarean birth Hypoglycaemia Glycaemic control |
No difference in CS, average glucose levels |
| De Barros et al. [40] | Usual physical activity Resistance exercise (two supervised and one unsupervised) for 30–40 min |
Control n = 32 GDM Diagnosis 27.5 ± 3 weeks Intervention n = 32 GDM Diagnosis 28.4 ± 2.5 weeks |
Additional medications Caesarean birth Weight gain |
No difference in latency to use of insulin or dose required Reduction in number of women requiring insulin No difference in caesarean section |
| Halse et al. [41] | Usual physical activity Home cycle ergometer supervised three times a week and unsupervised for two sessions a week |
Control n = 20 GDM Diagnosis 28.8 ± 1 week Intervention n = 20 GDM Diagnosis 28.9 ± 1 week |
Compliance, maternal attitudes to exercise, aerobic fitness, onset of labour, mode of delivery, duration of labour | No difference in maternal obstetric outcomes, improved fitness, attitude, and exercise intention |
| Halse et al. [47] | Usual physical activity Home cycle ergometer supervised three times a week and unsupervised for two sessions a week |
Control n = 9 GDM diagnosis at 28 weeks Intervention n = 10 GDM diagnosis at 28 weeks |
Glycaemic control | No difference in fasting glucose, HbA1C, insulin use, dose, or latency to starting insulin Improved post prandial glucose and average glucose |
| Jovanovic-Peterson et al. [42] | Usual physical activity Aerobic exercise: 20 min for three times a week, supervised, using ergometer |
Control n = 5 GDM “newly diagnosed” Intervention n = 5 GDM “newly diagnosed” |
Additional medications Adherence to intervention Hypertensive disorders Glycaemic control |
Improved fasting glucose with intervention No difference in obstetric or maternal outcomes |
| Qadir et al. [44] | Usual physical activity measured by pedometer Patient education and structured exercise class once a week Usual physical activity measured by pedometer |
Control n = 4 Intervention n = 2 |
Average daily steps Glycaemic control |
No difference in glycaemic control |
| Ramos et al. [43] | 50 min stretching and relaxation once a week 50 min aerobic session three times a week |
Control n = 20 GDM diagnosis: 20.8 ± 6 weeks Intervention n = 18 GDM diagnosis 22.2 ± 6 weeks |
Improved HbA1C in intervention | |
| Sklempe Kokic [45] | Usual physical activity Combined aerobic and resistance exercise (two supervised sessions) plus seven sessions of unsupervised walking |
Control n = 85 GDM diagnosis: 24–30 weeks Intervention n = 85 GDM diagnosis: 24–30 weeks |
Additional medications Caesarean Birth Glycaemic control Weight gain |
Improved postprandial glucose with intervention, no difference in maternal obstetric outcomes |
| Youngwanichsetha et al. [46] | Not applicable Fifteen to twenty minutes of supervised yoga five times a week |
Glycaemic control | Improved fasting glucose, post prandial glucose, HbA1C with intervention |
No randomised studies were identified that directly compared aerobic to resistance exercise. Study summaries are shown in Table 4. One study compared aerobic or resistance exercise to controls, but the numbers were small, and the study was reported as a pilot study within a conference abstract, with plans to continue the study [36]. The most common comparison was “usual physical activity”.
3.3. Fasting Glucose
Seven of the studies included fasting glucose as a primary outcome. Two papers [43,46] showed an improvement in fasting glucose in the intervention group. Youngwanichseta et al. [46] showed a statistically significant difference in fasting plasma glucose with intervention vs. control (post-test mean 83.39 ± 7.69 mmol/L vs. 87.85 mmol/L ± 7.94, p = 0.012). Jovanovic-Peterson [42] et al. found a reduction in fasting glucose with intervention vs. control (70.1 mmol/L ± 6.6 vs. 87.6 mmol/L ± 6.2, p < 0.001). The remaining showed no difference in fasting glucose with exercise.
3.4. Postprandial Glucose
Seven of the papers looked at postprandial glucose as an outcome measure. Five papers [38,39,41,45,46] showed an improvement in postprandial glucose results in the intervention group. In Bo’s [37] study, postprandial glucose in the intervention group was 117.2 ± 16.5 mmol/L vs. 106.1 mmol/L ± 19.0 in the control group, giving an adjusted difference of minus 11.1 mmol/L (minus 16.1, minus 6.1, 95% CI, p < 0.001). In Halse’s [41] paper, there was a significant difference in postprandial glucose at breakfast, with lower levels in the intervention group compared with the control, (p = 0.046); postprandial glucose levels at dinner approached significance with lower levels in the exercise group, (p = 0.054), compared with the control. There was no difference in postprandial levels at lunch, (p = 0.312). Sklempe-Kokic et al. [45] showed an improvement in postprandial blood glucose in the intervention vs. control (mean 4.66 mmol/L ± 0.46 vs. 5.3 mmol/L ± 0.47, p < 0.001). In Youngwanicheta’s [46] paper, there was statistically significant difference in two hour postprandial glucose in the intervention vs. control (mean post-test glucose 103.67 mmol/L ± 9.93 vs. 114.36 mmol/L ± 10.15, p = 0.001). Brankston et al.’s [38] study showed a significant reduction in pooled post-meal glucose levels in the diet plus exercise group compared to diet alone with no difference in individual breakfast, lunch, and supper postprandial glucose levels. Two studies ([35,43]) showed no difference in postprandial blood sugar.
3.5. Average Glucose
Five studies reported average glucose levels as an outcome. One study, by Halse [41], showed an improvement in mean postprandial glucose levels in the exercise group compared with the control (p = 0.004). The remaining four studies showed no difference [36,39,40,45].
3.6. HbA1C
Five papers recorded HbA1C as an outcome with four of these ([37,43,44,46]) showing a reduction in HbA1C with exercise intervention. In Bo’s [37] paper, HbA1C reduced from 4.9% ± 0.4 in the non-exercise group to 4.6% ± 0.5 in the exercise group with an adjusted difference of minus 0.3, p < 0.001. In Youngwanichseta’s [46] paper, there was a significant difference in post-test HbA1C with intervention vs. control (mean HbA1C 5.23% ± 0.22 vs. 5.68% ± 0.38, p = 0.03). Qadir [44] showed a significant difference in average HbA1c between the intervention and control groups (4.9% vs. 5.38%, p = 0.04). The paper by Ramos [43] is a conference abstract reporting the preliminary results of a pilot study. Post intervention mean HbA1c in the study group (n = 2) was 5.5% ± 0.4 compared with 6.3% ± 4.0 in the control group (n = 4). Halse [41] showed was no difference in HbA1C post study between intervention and control.
3.7. Insulin Use
Six papers studied the need for insulin treatment as an outcome, with one paper showing a reduction in the number of women requiring insulin with exercise intervention. There was a significant difference in De Barros’s paper [40] in the number of women who required insulin: 21.9% in the exercise group (7/32) vs. 56.3% (18/32) in the control group, p = 0.005. Five studies showed no difference [34,35,37,38,41].
Four papers reported changes in insulin dose. One paper (Brankston [38]) showed a reduction in insulin dose requirements with exercise intervention (diet plus exercise) vs. diet alone (0.22 units/kg ± 0.2 vs. 0.48 units/kg ± 0.3, p < 0.05). Halse’s paper [47] reported a clinical difference with a lower mean dose of insulin in the intervention (7 iu ± 1) group compared with the control (13 iu ± 1); the numbers of participants were too small to draw a statistically meaningful conclusion. Adam [34] and deBarros [40] showed no difference in mean dose of insulin between exercise intervention and control. Four studies reported latency to insulin requirement as an outcome. One paper [38] showed a statistically significant delay in starting insulin with intervention vs. control (3.71 weeks ± 3.1 vs. 1.11 weeks ± 0.8, 0 < 0.05), with three studies showing no difference [34,40,41].
3.8. Maternal Hypoglycaemia
There were no reports of maternal hypoglycaemia in the 14 papers analysed.
3.9. Caesarean Section
Six papers reported rate of Caesarean section (CS) as an outcome. There was a significant difference in Awad’s [48] paper: the rate of CS was higher in the control group (63.4% (n = 19/30) compared with 16% (n = 5/30) in the exercise group, (p= 0.001). Five studies showed no difference in CS rates between the exercise intervention and control groups [35,37,39,47].
3.10. Induction of Labour Rates and Labour Duration
Halse [41] was the only paper to report on induction of labour with no difference shown between intervention (55%) and control (42%), p > 0.05. They were also the only group to report on duration of labour with no difference between exercise intervention and control (445 min ± 309 vs. 348 min ± 187, p > 0.05)
3.11. Other Outcomes
None of the studies included reported on the use of Metformin, perineal trauma (third- or fourth-degree tears), or shoulder dystocia as an outcome.
4. Discussion
There were no well-designed RCTs identified comparing aerobic and strength exercise in the management of GDM and therefore we are unable to comment on our primary outcome, but we were able to provide a narrative review for glycaemic control parameters and maternal outcomes related to exercise.
Pregnancy is a state of relative insulin resistance. Exercise has its insulin sensitising effects by increasing GLUT-4, increasing sensitivity GLUT-4 to insulin and increased glycogen synthase [49]. By this mechanism, uptake of glucose into muscles is increased. Aerobic and resistance exercise have different metabolic effects and therefore both have a potential role in the treatment of states of insulin resistance such as that seen in GDM. As skeletal muscle is the largest mass of insulin sensitive tissue, an increase in muscle mass through resistance training is associated with improved glycaemic control [13,14]. Aerobic exercise reduces visceral obesity which improves insulin sensitivity [15]. Aerobic exercise has been shown to be more beneficial in modulating insulin resistance and inflammatory cytokines in obese patients with T2DM when compared with resistance exercise [50]; however, it has been proposed that both methods likely incur benefit through their different mechanisms of action [51].
Previously, women had been advised against moderate exercise in pregnancy due to concerns about the risk of harm to the fetus including growth restriction and preterm birth. A systematic review [22] of over 2000 women found that in singleton, uncomplicated pregnancies, moderate exercise did not increase the risk of preterm birth or growth restriction. Other systematic reviews and meta-analyses have supported this finding [52,53], including showing a reduction in the rate of caesarean birth and gestational weight gain with exercise [54]. The American College of Obstetricians and Gynecologists (ACOG) [55] recommend 30 min or more of moderate exercise on most days for women without medical or obstetric risks. In one study [56], over half of women believed that weight-based exercise was unsafe in pregnancy. A lack of awareness of exercise in pregnancy guidelines among physicians has previously been shown [57]. As this review shows, there were no adverse effects reported in women with GDM, i.e., a pregnancy that may be considered “high risk”. A meta-analysis of women with risk factors such as obesity, hypertension, and GDM showed no adverse effect on the fetus with moderate intensity exercise [58]. An RCT largely comprised of previously sedentary women showed no increase in maternal or neonatal adverse effects with combined aerobic and resistance training [52]. Studies looking at the role of exercise in preventing GDM have shown conflicting results, with some studies showing a reduced incidence [59] and others showing no impact [60,61].
Of the studies analysed, eight out of the 14 showed some benefit with exercise intervention on parameters of glycaemic control, particularly lower fasting glucose [47,49], postprandial glucose [38,39,40,46,50,51,52], HbA1c [38,43,44,46], reduced need for insulin, and increased latency to starting insulin [38,40]. Different makers of glycaemic control were used which makes it difficult to compare results. Of the seven studies that included resistance training either alone or in combination, four of these demonstrated improved glycaemic control with intervention [38,40,45,46]. Two of these studies involving strength-based exercise as an intervention showed a reduction in the need for insulin or delayed the onset of starting insulin. The need for insulin treatment in GDM is an important clinical indicator of the degree of hyperglycaemia. Hyperglycaemia in pregnancy is associated with adverse outcomes [62] and pregnant women who require insulin as treatment are at a higher risk of adverse outcomes [63]. The impact of resistance exercise on eliminating the need for or delaying starting insulin in GDM is an important finding and more research supporting this would be helpful in advising patients.
Of the five studies using aerobic exercise alone as an intervention, three [38,41,43] of these showed some improvement in glycaemic control. Of note, none of the studies included showed any negative effect of exercise. There is insufficient evidence to recommend one modality of exercise over another for the management of GDM and in practice, a combination of aerobic and strength is likely to show the most overall benefit in pregnancy as has been shown in the management of Type 2 DM [10].
The potential positive effect of exercise in GDM pregnancies on obstetric outcomes is largely theoretical modelling of the benefits of exercise in reducing hyperglycaemia. The studies presented have had mixed reports with many studies showing no difference with intervention. One study [48] showed a reduction in the CS rate among women with insulin controlled GDM who participated in a combined aerobic and strength exercise regime compared with standard care. When considering the global impact of GDM, it is notable that there are relatively few studies published in exercise as a treatment. Exercise is generally a free or low-cost intervention and is safe with few, if any, potential adverse effects and can be modified to all degrees of fitness and physical ability. Of the studies presented here, they appear to have been powered to look at variation in glycaemic control but were perhaps not large enough to report on maternal outcomes.
A core outcome set (COS) for studies of GDM was published in 2020 [64] with 14 outcomes reported in the final set. All the papers included in this systematic review were published before the development of a core outcome set and much variation is seen in the outcomes measured; this reiterates the need for such a COS for consistency in reporting outcomes in publications.
Several systematic reviews have been published on the topic of exercise for treatment for GDM. Cremona [65] looked at the effect of exercise modality on markers of insulin sensitivity in women with or at risk of GDM. They concluded that exercise sessions three times per week of either aerobic or strength training targeting major muscle groups could improve glycaemic control. Women with a high body mass index (BMI) at risk of GDM would also benefit; however, women with previous GDM pregnancies and a normal BMI do not appear to reduce their risk of GDM through exercise intervention. Huang [66] studied the effects of difference exercise modalities on glycaemic control alone but did not include five studies included in this review [34,36,43,44,48]. They performed a meta-analysis of nine RCTs involving 618 women which demonstrated high heterogenicity. The results showed that aerobic exercise reduced the fasting blood glucose, postprandial blood glucose, and HbA1C in patients with GDM compared to conventional treatment. They included Youngwanichestha et al.’s [46] study as an aerobic intervention although yoga is not generally considered aerobic as the intention is not to increase the heart rate. The dosage of insulin was reduced in the resistance exercise group compared with conventional treatment; however, this was based on two studies [38,40]. The combination of aerobic and strength exercise compared with conventional treatment reduced postprandial glucose levels, but this was based on only one study [45]. Brown [67] performed a systematic review of 11 studies involving 638 women and concluded that the evidence is poorly reported and confounded by the variety of exercise interventions. Harrison [68] studied eight studies with self-monitored postprandial glucose as the primary outcome and concluded that exercise performed at moderate intensity a minimum of three times a week appears to be effective in managing GDM, although again this review was limited by the limited number of studies, heterogenicity in study design, and reporting of outcomes. Bgengski [69] included the same eight studies in their systematic review but only studied the effect of exercise on fasting plasma glucose as their primary outcome, concluding there was no difference between exercise and physical activity counselling compared with standard care on fasting plasma glucose levels. There was no difference on secondary outcomes which were macrosomia, preterm birth, CS, GA at delivery, and birth weight. Allehandan [70] included eight studies in their systematic review and concluded that diet plus exercise for women with GDM lowered fasting and postprandial glucose levels compared with diet alone.
Only two of the systematic reviews in this area [69,70] included both maternal outcomes as well as glycaemic control. While glycaemic control is an important predictor of morbidity in GDM, it is crucial that obstetric and neonatal outcomes are reported, as ultimately this is the information that will be used to counsel patients and inform guidelines. Some abstracts from the grey literature included in this analysis have not been reported in previous systematic reviews. Given the lack of large RCTs, it is important that smaller studies such as those published at conferences be included in systematic reviews to allow a complete review of the available literature.
Strengths and Limitations
A strength of this study is the inclusion of studies not included in previous systematic reviews and inclusion of obstetric outcomes which have often been excluded previously. As with previous systematic reviews, it is limited by the small number of studies and the lack of large RCTs. We could not identify a study that directly compared strength training with aerobic exercise in the management of GDM and therefore cannot answer our primary research question.
5. Conclusions
Studies on exercise for the management of GDM have shown mixed effects on maternal glycaemic control, with disappointingly no apparent impact on pregnancy outcomes.
Despite exercise being integral to GDM management, the evidence bases for medium to long term benefit remains lacking. This is an important topic for discussion that reveals a paucity of data to guide healthcare providers in recommendations on exercise modality for the management of GDM. Further well designed large RCTs using a core outcome set are needed to determine the most efficient way to use exercise to treat GDM. Ideally, future studies would continue into the postpartum period to determine the effect of resistance or aerobic exercise on long term progression to T2DM following a pregnancy with GDM.
The development of a COS for diabetes will improve reporting in studies on the role of exercise in GDM. The heterogenicity of reported studies make it difficult to make specific recommendations on the optimum exercise regime. Given the different effects aerobic and strength training have on glucose metabolism, it is plausible that a combination of both modalities is useful in controlling GDM.
Author Contributions
N.K. made a substantial contribution to the conception of this work, the acquisition, analysis, and interpretation of data, drafted the work, gives final approval of this version to be published, and agrees to be accountable for all aspects of the work in ensuring that questions relating to the accuracy or integrity of any part of the work are appropriately investigated and rewarded. C.C. made a substantial contribution to the conception of this work, the acquisition, analysis, and interpretation of data, revised this version critically for important intellectual content, gives final approval of this version to be published, and agrees to be accountable for all aspects of the work in ensuring that questions relating to the accuracy or integrity of any part of the work are appropriately investigated and rewarded. F.M.M. made a substantial contribution to the conception of this work, revised this version critically for important intellectual content, gives final approval of this version to be published, and agrees to be accountable for all aspects of the work in ensuring that questions relating to the accuracy or integrity of any part of the work are appropriately investigated and rewarded. M.F.H. made a substantial contribution to the conception of this work, the acquisition, analysis, and interpretation of data, drafted the work, gives final approval of this version to be published, and agrees to be accountable for all aspects of the work in ensuring that questions relating to the accuracy or integrity of any part of the work are appropriately investigated and rewarded. All authors have read and agreed to the published version of the manuscript.
Institutional Review Board Statement
As a systematic review of published literature, this paper was exempt from Research Ethics Committee approval.
Informed Consent Statement
Not applicable.
Data Availability Statement
Not applicable.
Conflicts of Interest
Mary Higgins declares a potential conflict of interest as she is an Editor of this special issue in Maternal Medicine for the journal.
Funding Statement
Niamh Keating completed this work as part of a two-year research and fellowship in Maternal Medicine programme funded by the National Maternity Hospital.
Footnotes
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.American Diabetes Association 14. Management of Diabetes in Pregnancy: Standards of Medical Care in Diabetes-2021. Diabetes Care. 2021;44((Suppl. 1)):S200–S210. doi: 10.2337/dc21-S014. [DOI] [PubMed] [Google Scholar]
- 2.Cho N.H., Shaw J.E., Karuranga S., Huang Y., da Rocha Fernandes J.D., Ohlrogge A.W., Malanda B. IDF Diabetes Atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res. Clin. Pract. 2018;138:271–281. doi: 10.1016/j.diabres.2018.02.023. [DOI] [PubMed] [Google Scholar]
- 3.Khalifeh A., Breathnach F., Coulter-Smith S., Robson M., Fitzpatrick C., Malone F. Changing trends in diabetes mellitus in pregnancy. J. Obstet. Gynaecol. 2014;34:135–137. doi: 10.3109/01443615.2013.830596. [DOI] [PubMed] [Google Scholar]
- 4.Egan A.M., Dennedy M.C., Al-Ramli W., Heerey A., Avalos G., Dunne F. ATLANTIC-DIP: Excessive gestational weight gain and pregnancy outcomes in women with gestational or pregestational diabetes mellitus. J. Clin. Endocrinol. Metab. 2014;99:212–219. doi: 10.1210/jc.2013-2684. [DOI] [PubMed] [Google Scholar]
- 5.Bogdanet D., Egan A., Reddin C., Kirwan B., Carmody L., Dunne F. ATLANTIC DIP: Despite insulin therapy in women with IADPSG diagnosed GDM, desired pregnancy outcomes are still not achieved. What are we missing? Diabetes Res. Clin. Pract. 2018;136:116–123. doi: 10.1016/j.diabres.2017.12.003. [DOI] [PubMed] [Google Scholar]
- 6.Lowe W.L., Scholtens D.M., Lowe L.P., Kuang A., Nodzenski M., Talbot O., Catalano P.M., Linder B., Brickman W.J., Clayton P., et al. Association of gestational diabetes with maternal disorders of glucose metabolism and childhood adiposity. JAMA. 2018;320:1005–1016. doi: 10.1001/jama.2018.11628. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Kgosidialwa O., Egan A.M., Carmody L., Kirwan B., Gunning P., Dunne F.P. Treatment with diet and exercise for women with gestational diabetes mellitus diagnosed using IADPSG criteria. J. Clin. Endocrinol. Metab. 2015;100:4629–4636. doi: 10.1210/jc.2015-3259. [DOI] [PubMed] [Google Scholar]
- 8.Wang C., Zhu W., Wei Y., Feng H., Su R., Yang H. Exercise intervention during pregnancy can be used to manage weight gain and improve pregnancy outcomes in women with gestational diabetes mellitus. BMC Pregnancy Childbirth. 2015;15:255. doi: 10.1186/s12884-015-0682-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Hayashi A., Oguchi H., Kozawa Y., Ban Y., Shinoda J., Suganuma N. Daily walking is effective for the management of pregnant women with gestational diabetes mellitus. J. Obstet. Gynaecol. Res. 2018;44:1731–1738. doi: 10.1111/jog.13698. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Umpierre D., Ribeiro P.A., Kramer C.K., Leitão C.B., Zucatti A.T., Azevedo M.J., Gross J.L., Ribeiro J.P., Schaan B.D. Physical activity advice only or structured exercise training and association with HbA1c levels in type 2 diabetes: A systematic review and meta-analysis. JAMA. 2011;305:1790–1799. doi: 10.1001/jama.2011.576. [DOI] [PubMed] [Google Scholar]
- 11.Röhling M., Herder C., Roden M., Stemper T., Müssig K. Effects of Long-Term Exercise Interventions on Glycaemic Control in Type 1 and Type 2 Diabetes: A Systematic Review. Exp. Clin. Endocrinol. Diabetes. 2016;124:487–494. doi: 10.1055/s-0042-106293. [DOI] [PubMed] [Google Scholar]
- 12.Yang Z., Scott C.A., Mao C., Tang J., Farmer A.J. Resistance exercise versus aerobic exercise for type 2 diabetes: A systematic review and meta-analysis. Sports Med. 2014;44:487–499. doi: 10.1007/s40279-013-0128-8. [DOI] [PubMed] [Google Scholar]
- 13.Ryan A.S., Pratley R.E., Elahi D., Goldberg A.P. Changes in plasma leptin and insulin action with resistive training in postmenopausal women. Int. J. Obes. 2000;24:27–32. doi: 10.1038/sj.ijo.0801080. [DOI] [PubMed] [Google Scholar]
- 14.Miller J.P., Pratley R.E., Goldberg A.P., Gordon P., Rubin M., Treuth M.S., Ryan A.S., Hurley B.F. Strength training increases insulin action in healthy 50- to 65-yr-old men. J. Appl. Physiol. 1994;77:1122–1127. doi: 10.1152/jappl.1994.77.3.1122. [DOI] [PubMed] [Google Scholar]
- 15.Stewart K.J. Role of exercise training on cardiovascular disease in persons who have type 2 diabetes and hypertension. Cardiol. Clin. 2004;22:569–586. doi: 10.1016/j.ccl.2004.06.007. [DOI] [PubMed] [Google Scholar]
- 16.Syngelaki A., Sequeira Campos M., Roberge S., Andrade W., Nicolaides K.H. Diet and exercise for preeclampsia prevention in overweight and obese pregnant women: Systematic review and meta-analysis. J. Matern. Fetal Neonatal Med. 2019;32:3495–3501. doi: 10.1080/14767058.2018.1481037. [DOI] [PubMed] [Google Scholar]
- 17.Magro-Malosso E.R., Saccone G., Di Tommaso M., Roman A., Berghella V. Exercise during pregnancy and risk of gestational hypertensive disorders: A systematic review and meta-analysis. Acta Obstet. Gynecol. Scand. 2017;96:921–931. doi: 10.1111/aogs.13151. [DOI] [PubMed] [Google Scholar]
- 18.Almousa S., Lamprianidou E., Kitsoulis G. The effectiveness of stabilising exercises in pelvic girdle pain during pregnancy and after delivery: A systematic review. Physiother. Res. Int. 2018;23:e1699. doi: 10.1002/pri.1699. [DOI] [PubMed] [Google Scholar]
- 19.Davenport M.H., Marchand A.A., Mottola M.F., Poitras V.J., Gray C.E., Jaramillo Garcia A., Barrowman N., Sobierajski F., James M., Meah V.L., et al. Exercise for the prevention and treatment of low back, pelvic girdle and lumbopelvic pain during pregnancy: A systematic review and meta-analysis. Br. J. Sports Med. 2019;53:90–98. doi: 10.1136/bjsports-2018-099400. [DOI] [PubMed] [Google Scholar]
- 20.Hu X., Ma M., Zhao X., Sun W., Liu Y., Zheng Z., Xu L. Effects of exercise therapy for pregnancy-related low back pain and pelvic pain: A protocol for systematic review and meta-analysis. Medicine. 2020;99:e17318. doi: 10.1097/md.0000000000017318. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Magro-Malosso E.R., Saccone G., Di Mascio D., Di Tommaso M., Berghella V. Exercise during pregnancy and risk of preterm birth in overweight and obese women: A systematic review and meta-analysis of randomized controlled trials. Acta Obstet. Gynecol. Scand. 2017;96:263–273. doi: 10.1111/aogs.13087. [DOI] [PubMed] [Google Scholar]
- 22.Di Mascio D., Magro-Malosso E.R., Saccone G., Marhefka G.D., Berghella V. Exercise during pregnancy in normal-weight women and risk of preterm birth: A systematic review and meta-analysis of randomized controlled trials. Am. J. Obstet. Gynecol. 2016;215:561–571. doi: 10.1016/j.ajog.2016.06.014. [DOI] [PubMed] [Google Scholar]
- 23.Davenport M.H., Nagpal T.S., Mottola M.F., Skow R.J., Riske L., Poitras V.J., Jaramillo Garcia A., Gray C.E., Barrowman N., Meah V.L., et al. Prenatal exercise (including but not limited to pelvic floor muscle training) and urinary incontinence during and following pregnancy: A systematic review and meta-analysis. Br. J. Sports Med. 2018;52:1397–1404. doi: 10.1136/bjsports-2018-099780. [DOI] [PubMed] [Google Scholar]
- 24.Woodley S.J., Lawrenson P., Boyle R., Cody J.D., Mørkved S., Kernohan A., Hay-Smith E.J.C. Pelvic floor muscle training for preventing and treating urinary and faecal incontinence in antenatal and postnatal women. Cochrane Database Syst. Rev. 2020;5:Cd007471. doi: 10.1002/14651858.CD007471.pub4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Davenport M.H., McCurdy A.P., Mottola M.F., Skow R.J., Meah V.L., Poitras V.J., Jaramillo Garcia A., Gray C.E., Barrowman N., Riske L., et al. Impact of prenatal exercise on both prenatal and postnatal anxiety and depressive symptoms: A systematic review and meta-analysis. Br. J. Sports Med. 2018;52:1376–1385. doi: 10.1136/bjsports-2018-099697. [DOI] [PubMed] [Google Scholar]
- 26.Kołomańska D., Zarawski M., Mazur-Bialy A. Physical Activity and Depressive Disorders in Pregnant Women-A Systematic Review. Medicina. 2019;55:212. doi: 10.3390/medicina55050212. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Davenport M.H., Ruchat S.M., Poitras V.J., Jaramillo Garcia A., Gray C.E., Barrowman N., Skow R.J., Meah V.L., Riske L., Sobierajski F., et al. Prenatal exercise for the prevention of gestational diabetes mellitus and hypertensive disorders of pregnancy: A systematic review and meta-analysis. Br. J. Sports Med. 2018;52:1367–1375. doi: 10.1136/bjsports-2018-099355. [DOI] [PubMed] [Google Scholar]
- 28.Yu Y., Xie R., Shen C., Shu L. Effect of exercise during pregnancy to prevent gestational diabetes mellitus: A systematic review and meta-analysis. J. Matern. Fetal Neonatal Med. 2018;31:1632–1637. doi: 10.1080/14767058.2017.1319929. [DOI] [PubMed] [Google Scholar]
- 29.Ming W.K., Ding W., Zhang C.J.P., Zhong L., Long Y., Li Z., Sun C., Wu Y., Chen H., Chen H., et al. The effect of exercise during pregnancy on gestational diabetes mellitus in normal-weight women: A systematic review and meta-analysis. BMC Pregnancy Childbirth. 2018;18:440. doi: 10.1186/s12884-018-2068-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Moher D., Liberati A., Tetzlaff J., Altman D.G. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Bmj. 2009;339:b2535. doi: 10.1136/bmj.b2535. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Higgins J.P., Thomas J., Chandler J., Cumpston M., Li T., Page M.J., Welch V.A., editors. Cochrane Handbook for Systematic Reviews of Interventions. 2nd ed. John Wiley & Sons; Hoboken, NJ, USA: 2019. [Google Scholar]
- 32.Higgins J.P., Altman D.G., Gøtzsche P.C., Jüni P., Moher D., Oxman A.D., Savovic J., Schulz K.F., Weeks L., Sterne J.A. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928. doi: 10.1136/bmj.d5928. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Keating N., Coveney C. Aerobic or Resistance Exercise for Improved Glycaemic Control and Obstetric Outcomes in Women with Gestational Diabetes. A Protocol for a Systematic Review. [(accessed on 11 May 2021)]. Available online: https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42020161454. [DOI] [PMC free article] [PubMed]
- 34.Adam C., L’Abbe C., Lachapelle J., Ourabah S., Rakel A., De Guise M. Impact of an individualised counselling on physical activity in women with Gestational Diabetes: Interim analysis of a randomised controlled trial. Endocr. Rev. 2014;35:SUN-1035. [Google Scholar]
- 35.Avery M.D., Leon A.S., Kopher R.A. Effects of a partially home-based exercise program for women with gestational diabetes. Obstet. Gynecol. 1997;89:10–15. doi: 10.1016/s0029-7844(97)84256-1. [DOI] [PubMed] [Google Scholar]
- 36.Bambicini J.T., Soares V.C.M., Zanetti M.R.D., Torloni M.R., Ribeiro M.C., Mattar R. M221 effects of aerobic and resistance exercises on glycemic levels of patients with gestational diabetes: Pilot study. Int. J. Gynecol. Obstet. 2012;119:S603. [Google Scholar]
- 37.Bo S., Rosato R., Ciccone G., Canil S., Gambino R., Poala C.B., Leone F., Valla A., Grassi G., Ghigo E., et al. Simple lifestyle recommendations and the outome of gestational diabetes. A 2 × 2 factorial randomized trial. Diabetes Obes. Metab. 2014;16:1032. doi: 10.1111/dom.12289. [DOI] [PubMed] [Google Scholar]
- 38.Brankston G.N., Mitchell B.F., Ryan E.A., Okun N.B. Resistance exercise decreases the need for insulin in overweight women with gestational diabetes mellitus. Am. J. Obstet. Gynecol. 2004;190:188–193. doi: 10.1016/s0002-9378(03)00951-7. [DOI] [PubMed] [Google Scholar]
- 39.Bung P., Artal R., Khodiguian N., Kjos S. Exercise in gestational diabetes. An optional therapeutic approach? Diabetes. 1991;40((Suppl. 2)):182–185. doi: 10.2337/diab.40.2.s182. [DOI] [PubMed] [Google Scholar]
- 40.De Barros M.C., Lopes M.A., Francisco R.P., Sapienza A.D., Zugaib M. Resistance exercise and glycaemic control in women with gestational daibetes mellitus. Am. J. Obstet. Gynecol. 2010;203:e551–e556. doi: 10.1016/j.ajog.2010.07.015. [DOI] [PubMed] [Google Scholar]
- 41.Halse R.E., Wallman K.E., Newnham J.P., Guelfi K.J. Home-based exercise training improves capillary glucose profile in women with gestational diabetes. Med. Sci. Sports Exerc. 2014;46:1702–1709. doi: 10.1249/mss.0000000000000302. [DOI] [PubMed] [Google Scholar]
- 42.Jovanovic-Peterson L., Durak E.P., Peterson C.M. Randomized trial of diet versus diet plus cardiovascular conditioning on glucose levels in gestational diabetes. Am. J. Obstet. Gynecol. 1989;161:415–419. doi: 10.1016/0002-9378(89)90534-6. [DOI] [PubMed] [Google Scholar]
- 43.Ramos J.G., Bgeginski R., Opperman M.L., Martins-Costa S., Delevatti R., Schuch R., Kruel L.F. Effect of aerobic training in pregnant women diagnosed with gestational diabetes: A preliminary report. Pregnancy Hypertens. 2015;5:105. [Google Scholar]
- 44.Qadir D.E.W. Effects of structured exercise on HbA1c level in Gestational Diabetes Mellitus—A Pilot Study. Int. J. Gynecol. Obstet. 2018;143:569–579. [Google Scholar]
- 45.Sklempe Kokic I., Ivanisevic M., Kokic T., Simunic B., Pisot R. Acute responses to structured aerobic and resistance exercise in women with gestational diabetes mellitus. Scand. J. Med. Sci. Sports. 2018;28:1793–1800. doi: 10.1111/sms.13076. [DOI] [PubMed] [Google Scholar]
- 46.Youngwanichsetha S., Phumdoung S., Ingkathawornwong T. The effects of mindfulness eating and yoga exercise on blood sugar levels of pregnant women with gestational diabetes mellitus. Appl. Nurs. Res. 2014;27:227–230. doi: 10.1016/j.apnr.2014.02.002. [DOI] [PubMed] [Google Scholar]
- 47.Halse R.E., Wallman K.E., Dimmock J.A., Newnham J.P., Guelfi K.J. Home-Based Exercise Improves Fitness and Exercise Attitude and Intention in Women with GDM. Med. Sci. Sports Exerc. 2015;47:1698–1704. doi: 10.1249/mss.0000000000000587. [DOI] [PubMed] [Google Scholar]
- 48.Awad E., Ahmed H., Yousef A., Saab I.M. Effect of antenatal exercise on mode of delivery in gestational diabetic females: A single-blind randomized controlled trial. Physiother. Q. 2019;27:1–5. doi: 10.5114/pq.2019.84270. [DOI] [Google Scholar]
- 49.Hawley J.A., Lessard S.J. Exercise training-induced improvements in insulin action. Acta Physiol. 2008;192:127–135. doi: 10.1111/j.1748-1716.2007.01783.x. [DOI] [PubMed] [Google Scholar]
- 50.Abd El-Kader S.M. Aerobic versus resistance exercise training in modulation of insulin resistance, adipocytokines and inflammatory cytokine levels in obese type 2 diabetic patients. J. Adv. Res. 2011;2:179–183. [Google Scholar]
- 51.Maiorana A., O’Driscoll G., Goodman C., Taylor R., Green D. Combined aerobic and resistance exercise improves glycemic control and fitness in type 2 diabetes. Diabetes Res. Clin. Pract. 2002;56:115–123. doi: 10.1016/s0168-8227(01)00368-0. [DOI] [PubMed] [Google Scholar]
- 52.Barakat R., Pelaez M., Cordero Y., Perales M., Lopez C., Coteron J., Mottola M.F. Exercise during pregnancy protects against hypertension and macrosomia: Randomized clinical trial. Am. J. Obstet. Gynecol. 2016;214:649.e1–649.e8. doi: 10.1016/j.ajog.2015.11.039. [DOI] [PubMed] [Google Scholar]
- 53.Beetham K.S., Giles C., Noetel M., Clifton V., Jones J.C., Naughton G. 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: 10.1186/s12884-019-2441-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54.The International Weight Management in Pregnancy (i-WIP) Collaborative Group Effect of diet and physical activity based interventions in pregnancy on gestational weight gain and pregnancy outcomes: Meta-analysis of individual participant data from randomised trials. BMJ. 2017;358:j3119. doi: 10.1136/bmj.j3119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Physical Activity and Exercise During Pregnancy and the Postpartum Period: ACOG Committee Opinion, Number 804. Obstet Gynecol. 2020;135:e178–e188. doi: 10.1097/AOG.0000000000003772. [DOI] [PubMed] [Google Scholar]
- 56.Duncombe D., Wertheim E.H., Skouteris H., Paxton S.J., Kelly L. Factors related to exercise over the course of pregnancy including women’s beliefs about the safety of exercise during pregnancy. Midwifery. 2009;25:430–438. doi: 10.1016/j.midw.2007.03.002. [DOI] [PubMed] [Google Scholar]
- 57.Bauer P.W., Broman C.L., Pivarnik J.M. Exercise and pregnancy knowledge among healthcare providers. J. Womens Health. 2010;19:335–341. doi: 10.1089/jwh.2008.1295. [DOI] [PubMed] [Google Scholar]
- 58.Wiebe H.W., Boule N.G., Chari R., Davenport M.H. The effect of supervised prenatal exercise on fetal growth: A meta-analysis. Obstet. Gynecol. 2015;125:1185–1194. doi: 10.1097/AOG.0000000000000801. [DOI] [PubMed] [Google Scholar]
- 59.Wang C., Wei Y., Zhang X., Zhang Y., Xu Q., Sun Y., Su S., Zhang L., Liu C., Feng Y., et al. A randomized clinical trial of exercise during pregnancy to prevent gestational diabetes mellitus and improve pregnancy outcome in overweight and obese pregnant women. Am. J. Obstet. Gynecol. 2017;216:340–351. doi: 10.1016/j.ajog.2017.01.037. [DOI] [PubMed] [Google Scholar]
- 60.Daly N., Farren M., McKeating A., O’Kelly R., Stapleton M., Turner M.J. A Medically Supervised Pregnancy Exercise Intervention in Obese Women: A Randomized Controlled Trial. Obstet. Gynecol. 2017;130:1001–1010. doi: 10.1097/AOG.0000000000002267. [DOI] [PubMed] [Google Scholar]
- 61.Nobles C., Marcus B.H., Stanek E.J., 3rd, Braun B., Whitcomb B.W., Solomon C.G., Manson J.E., Markenson G., Chasan-Taber L. Effect of an exercise intervention on gestational diabetes mellitus: A randomized controlled trial. Obstet Gynecol. 2015;125:1195–1204. doi: 10.1097/AOG.0000000000000738. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62.The HAPO Study Cooperative Research Group Hyperglycaemia and Adverse Pregnancy Outcomes. N. Engl. J. Med. 2008;358:1991–2002. doi: 10.1056/NEJMoa0707943. [DOI] [PubMed] [Google Scholar]
- 63.Billionnet C., Mitanchez D., Weill A., Nizard J., Alla F., Hartemann A., Jacqueminet S. Gestational diabetes and adverse perinatal outcomes from 716,152 births in France in 2012. Diabetologia. 2017;60:636–644. doi: 10.1007/s00125-017-4206-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64.Egan A.M., Bogdanet D., Griffin T.P., Kgosidialwa O., Cervar-Zivkovic M., Dempsey E., Allotey J., Alvarado F., Clarson C., Cooray S.D., et al. A core outcome set for studies of gestational diabetes mellitus prevention and treatment. Diabetologia. 2020;63:1120–1127. doi: 10.1007/s00125-020-05123-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65.Cremona A., O’Gorman C., Cotter A., Saunders J., Donnelly A. Effect of exercise modality on markers of insulin sensitivity and blood glucose control in pregnancies complicated with gestational diabetes mellitus: A systematic review. Obes. Sci. Pract. 2018;4:455–467. doi: 10.1002/osp4.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Huang X., Huang J., Wu J., Li M., Yang Z., Liu L., Lin T., Lan Y., Chen K. Different exercises for pregnant women with gestational diabetes: A meta-analysis of randomized controlled trials. J. Sports Med. Phys. Fitness. 2020;60:464–471. doi: 10.23736/S0022-4707.19.10131-4. [DOI] [PubMed] [Google Scholar]
- 67.Brown J., Ceysens G., Boulvain M. Exercise for pregnant women with gestational diabetes for improving maternal and fetal outcomes. Cochrane Database Syst. Rev. 2017;6:Cd012202. doi: 10.1002/14651858.CD012202.pub2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 68.Harrison A.L., Shields N., Taylor N.F., Frawley H.C. Exercise improves glycaemic control in women diagnosed with gestational diabetes mellitus: A systematic review. J. Physiother. 2016;62:188–196. doi: 10.1016/j.jphys.2016.08.003. [DOI] [PubMed] [Google Scholar]
- 69.Bgeginski R., Ribeiro P.A.B., Mottola M.F., Ramos J.G.L. Effects of weekly supervised exercise or physical activity counseling on fasting blood glucose in women diagnosed with gestational diabetes mellitus: A systematic review and meta-analysis of randomized trials. J. Diabetes. 2017;9:1023–1032. doi: 10.1111/1753-0407.12519. [DOI] [PubMed] [Google Scholar]
- 70.Allehdan S.S., Basha A.S., Asali F.F., Tayyem R.F. Dietary and exercise interventions and glycemic control and maternal and newborn outcomes in women diagnosed with gestational diabetes: Systematic review. Diabetes Metab. Syndr. Clin. Res. Rev. 2019;13:2775–2784. doi: 10.1016/j.dsx.2019.07.040. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Not applicable.

