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The role of exercise in reducing the risks of gestational diabetes mellitus in obese women

https://doi.org/10.1016/j.bpobgyn.2014.05.013Get rights and content

The global obesity epidemic continues unabated, now rapidly expanding to developing countries. Multiple comorbidities and premature mortality are associated with obesity, most frequently diabetes. The associated financial and economical burden is escalating as well. The sedentary lifestyle adopted by many pregnant women because of traditional practices and the current recommendation for gestational weight gain are contributing factors to the obesity and diabetes epidemic.

Physical inactivity is recognized as an independent risk factor for obesity insulin resistance and type 2 diabetes; the physiological and hormonal changes associated with pregnancy magnify this risk. Conversely, evidence and accumulated experience indicate that antenatal lifestyle interventions that include physical activity and judicious dieting could improve the pregnancy outcome and reduce the risk of gestational diabetes and is effective as an adjunctive therapy for diabetes in pregnancy. All major professional organizations, among them American Congress of Obstetricians and Gynecologists (ACOG), American Diabetes Association (ADA), Royal College of Obstetricians and Gynaecologists (RCOG), and Society of Obstetricians and Gynaecologists of Canada (SOGC), recommend lifestyle interventions that include diet and exercise to prevent or manage gestational diabetes or diabetes mellitus.

Introduction

In 2008, it was estimated that 508 million people worldwide were obese and another 1.46 billion people overweight and many more currently [2]. The associated comorbidities, particularly diabetes, and consequences are staggering and the financial burden is of historic proportions. Globally, 366 million are affected by diabetes; it is expected that there will be 552 million diabetics by 2030 [3]. For many women, gestational diabetes is the first manifestation of diabetes.

Several large trials conducted in nonpregnant subjects in China, Finland and United States have proven that adopting a healthy lifestyle that includes weight reduction and physical activity can prevent, manage, or reverse diabetes [4], [5], [6]. Recommendations for the prevention of type 2 diabetes in nonpregnant women include pharmacotherapy, surgery, diet, aerobic exercise, and, most recently, also resistance training [7]. For pregnant women, the only management option available is lifestyle modification. The most effective interventions have combined judicious weight gain and physical activity.

Normal pregnancy has been characterized as a diabetogenic event due to hormonal changes, and the progressive insulin resistance begins near mid-pregnancy and progresses through the third trimester to levels that approximate the insulin resistance of patients with type 2 diabetes [8]. Insulin resistance develops at the level of skeletal muscles; thus, exercise is a logical intervention that can counteract this activity. However, caloric restriction also plays an important role in improving insulin sensitivity.

In overweight and obese patients, insulin resistance is further increased in pregnancy. Obese women are at an increased risk of gestational diabetes mellitus (GDM) (odds ratio (OR) 2.6; 95% confidence interval (CI) 2.1–3.4). The increased fat deposition leads to an increase in adiponectin and leptin. Adiponectin regulates insulin sensitivity and glucose homeostasis. Additional weight gain leads to a further increase in adipokines and leptin, which increase the oxidative stress that contributes to the insulin resistance. Adiponectin regulates insulin sensitivity; low levels of adiponectin are associated with beta cell dysfunction. Muscles bind adiponectin which translocates glucose transporter 4 (GLUT4). GLUT4 is responsible for the transport of glucose into cells. Exercise enhances glucose uptake by GLUT4 translocation. Exercise regulates glycemia through two mechanisms:

  • 1)

    Insulin-stimulated muscle glucose uptake

  • 2)

    Insulin-independent glucose transport (GLUT4)

The production of leptin by the adipose tissue is also a major cause for insulin resistance. Exercise reduces the leptin levels.

Judicious caloric restriction also plays an important role in enhancing insulin sensitivity. It was demonstrated that obese subjects with impaired glucose tolerance or mild type 2 diabetes after 10 days of caloric restriction and a body weight reduction of only 3.5% will experience a 35% increase in glucose disposal rate during a hyperglycemic clamp, thus enhancing significantly the insulin sensitivity [9].

The glucose homeostasis is also altered by placental hormones such as human placental lactogen, progesterone, cytokines (tumor necrosis factor alpha (TNFα)), and others. It is also worth noting that fat deposits in the body are used as an energy source, and when large amounts of energy are required the duration and intensity of physical activity can make a difference. The utilization of fat involves several processes: lipolysis, mobilization, transportation, uptake, activation, translocation, and β-oxidation. The process is stimulated by multiple hormones, among them catecholamines. In our previous studies, we have demonstrated that in sedentary pregnant diabetic patients who exercised at 50–70% of their maximal aerobic capacity they elicit a proper catecholamine response, predominantly norepinephrine, sufficient to facilitate the skeletal muscle uptake of glucose [10].

Adopting the 2009 Institute of Medicine (IOM) recommendations [11] for additional gestational weight gain for overweight and obese pregnant women could further amplify the risk of gestational diabetes as insulin resistance worsens with additional weight gain.

The IOM guidelines for gestational weight gain are based on prepregnancy body mass index (BMI). In the IOM report, it is specified that basing the recommendation on prepregnancy BMI is an approach that reflects imprecision and needs to be considered for the individual woman. Further weight gain, independent of maternal glycemia, is strongly associated with pregnancy complications particularly in overweight and obese women as has been demonstrated by the Hyperglycemic and Adverse Outcome (HAPO) Study [12], including maternal and fetal complications.

In its 2014 Standards of Medical Care in Diabetes, the American Diabetes Association (ADA) recommends that nonpregnant subjects at a risk of type 2 diabetes be referred to an effective ongoing support program targeting a weight loss of 7% of body weight and increasing physical activity to at least 150 min/week of moderate activity such as walking [7]. The ADA Clinical Practice Recommendations have suggested a 30% caloric restriction for obese women with GDM, noting a minimum 1800 calories/day level since the year 2000. The concerns for potential adverse consequences from ketonuria/ketonemia in pregnancy do not have credible scientific support, unless the patient is at a risk of ketoacidosis.

In the ADA position statement, it is quoted that based on large studies in nonpregnant type 2 diabetes subjects a structured exercise intervention of at least 8-week duration will result in a lower A1C by an average of 0.66% even with no significant change in BMI [13]. In our experience, within 10 days of initiating an exercise program in GDM patients and depending on regimen compliance, 60% of the subjects will attain euglycemia [14].

The American Congress of Obstetricians and Gynecologists (ACOG), ADA, Royal College of Obstetricians and Gynaecologists (RCOG), and Society of Obstetricians and Gynaecologists of Canada (SOGC) recommend a moderate exercise program for the management of gestational diabetes *[1], *[7], [15], *[38], [39]. In addition, the ACOG recommendations on gestational weight gain emphasize that “individualized care and clinical judgment are necessary in the management of overweight or obese women” and “… for the overweight pregnant who is gaining less than the recommended amount but has an appropriately growing fetus, no evidence exists that encouraging increased weight gain to conform with the current IOM guidelines will improve maternal or fetal outcomes [16].”

For obese pregnant women, no target gestational weight gain or loss has been established to prevent gestational diabetes; however, we and others have determined that obese pregnant women, particularly class III who gain no weight or even lose up to 10 pounds in pregnancy, show an improvement in glycemic control and experience less maternal comorbidities such as preeclampsia and less fetal morbidities such as macrosomia [17], [18] (Fig. 1).

Historically pregnant women were recommended sedentary lifestyle, and pregnant diabetics were hospitalized for prolonged periods [19]; only in the past 20–30 years have recommendations changed.

Despite current recommendations, there is still reluctance to prescribe lifestyle modification to obese diabetic pregnant women. Pregnancy should not be a state of confinement or uncontrolled dietary indulgence; in the absence of specific contraindications to exercise (see Table 1), pregnant women, including obese and diabetic women, should be encouraged to participate in aerobic and strength-conditioning exercises [20].

Several observational trials have determined that women who engage in regular physical activity prior and during pregnancy lower their risk of developing GDM [21], [22], [23], [24].

The exercise prescription includes the following components: frequency, intensity, duration, and type.

Light physical activity is defined as requiring <3 metabolic equivalents (METs), moderate activities 3–6 METs, and strenuous activities >6 METs. METs are used to quantify the metabolic cost of exercise in terms of oxygen consumption (VO2). One MET obtained at rest is equivalent to 3.5 ml O2/kg/min. A brisk walk at 3–4 mph for 1 h will generate approximately 3–5 METs. During moderate physical activity, the subject is still capable of freely conversing and not experiencing respiratory difficulties. Ideally, pregnant women at a risk of GDM should expend between 400 and 600 kcal/day in exercise, at the minimum 300 kcal/day, exercise being performed preferably for 20–30 min after each meal 3 times/day (Table 2) [25]. Most subjects can engage safely in additional physical activities (Table 3).

Additional weight maintenance or loss can be accomplished with longer sessions of exercise. To lose 1 pound of body weight a week from exercise alone, an individual should walk 5 miles per day, 7 days per week.

Several studies including a large number of subjects have been published, and despite methodological shortcomings they point towards the clinical importance of physical activity as an intervention to prevent GDM.

Oken et al. assessed the duration and intensity of physical activity among 1805 women, participants who completed questionnaires regarding their physical activities 12 months prior to pregnancy [26]. The study revealed that women who engaged in any vigorous activity (jogging, swimming, or aerobic classes) had a lower risk of both gestational diabetes (OR 0.49, 95% CI 0.24–1.01) and abnormal glucose tolerance test (OR 0.70, 95% CI 0.49–1.01) compared with women reporting no physical activities. Walking only or some physical activity provided modest benefits. These authors determined that nulliparous women with normal prepregnancy BMI (<25 kg/m2) benefited the most from physical activity in reducing the risk of GDM, although they were at the lowest risk. No data were provided on neonatal outcomes.

In another prospective pregravid physical activity cohort study that included 21,765 women in the Nurses Health Study II, Zhang et al. compared the highest with the lowest quintiles of vigorous activity and determined that the relative risk (RR) was 0.77 (95% CI, 0.69–0.94); conversely, women who spent 20 h/week watching television but did not engage in vigorous activity had a higher risk of gestational diabetes (RR 2.30; 95% CI, 1.06–4.97). The study report did not include data on neonatal outcome. [21]

Dempsey et al. in a prospective cohort study analyzed structured questionnaires administered to 900 women about recreational physical activities prior to and during pregnancy. Women who exercised >4.2 h/week (≥21.1 METs – hours per week) reduced their risk of GDM by 74%. [22]

These and other studies clearly demonstrated that, prior to pregnancy, women have to expend at least 1700 kcal/week (the equivalent of 16 h/week) of light exercise or at least 840 kcal/week (the equivalent of 8 h/week) of vigorous exercise per week to reduce the risk of developing gestational diabetes.

Rudra updated the results for the Dempsey [23] studies and concluded that the risk of gestational diabetes is inversely related to the exertion perceived during recreational physical activity and that perceived exertion may be another valuable indicator of behavior and fitness measure in assessing the relations between physical activity and pregnancy outcomes.

Research studies conducted in different laboratories have determined that subjects who expend >900 kcal per one bout of strenuous exercise will decrease insulin resistance by 30% as illustrated in the study by Zhang et al. [21] (Fig. 2).

Clearly, the total duration of exercise each week of at least 150 min and the intensity of exercise determine the efficacy of an exercise program in reducing the risk of gestational diabetes.

Exercise as intervention prior to and during pregnancy to reduce the risk or manage GDM has been the focus of several studies and meta-analyses.(Table 4)

Han et al. conducted a meta-analysis of fire trials recorded in the Cochrane Pregnancy and Childbirth Group's Trials Register (2 April 2012) comparing women receiving exercise interventions with those receiving routine antenatal care, and they found no significant difference in GDM incidence [28]. However, on a closer look at the studies included in the analysis, it appears that apart from the biases noted the subjects engaged in different and insufficient level of activities; many were lost to follow-up (10–20% of subjects), no or very few obese subjects included in the studies (BMI > 30). In addition, the Stafne et al. [29] study determined that exercise programs do not significantly improve insulin resistance in normal BMI subjects. Hopkins et al. also observed no difference in any parameters of glucose regulation between the exercise intervention group and the control group; most of the subjects included in this study either had normal BMI or were just overweight [30]. However, in a large cohort study by Dye et al., it was determined that physical activity was associated with 50% reduced rates of GDM for women who had a prepregnancy BMI >33 kg/m2 [31]. Clearly, patients with higher BMI will have more adipose tissue and respond significantly better to lifestyle interventions as demonstrated in studies conducted in nonpregnant subjects as well.

In the past years, a few trials for the prevention of GDM have mirrored those conducted in nonpregnant subjects at a risk of diabetes.

We investigated 39 patients with GDM on a diet and exercise program. The diet was a consistent carbohydrate meal plan based on the following caloric needs: 25 kcal/kg (overweight BMI = 25–29.9 kg/m2), 20 kcal/kg (obese BMI = 30–39.9 kg/m2), and 15 kcal/kg (morbidly obese BMI >40 kg/m2). The meal plan was designed to maintain euglycemia with a carbohydrate content of 40–45% of calories, with a distribution of 12.5% at breakfast and each of the three snacks, and 25% at the lunch and supper meals. The target blood glucose values were established at <95 mg/dl for fasting values and <130 mg/dl. [32]

A moderate exercise program was prescribed not to exceed 60% VO2 max. The participants were encouraged to exercise in the laboratory once a week under supervision and prescribed an unsupervised exercise routine the remaining 6 days/week at home [33] (see Table 5). This group of patients was compared to the other 57 GDM patients managed with the above routinely prescribed diet.

Although both groups of patients normalized their blood glucose level, the weight gain per week was significantly lower in the exercise and diet group and they had significantly fewer macrosomic infants.

To achieve or maintain normoglycemia, previously sedentary women should engage in moderate exercise (such as brisk walking) for ≥30 min at least 5 times/week, preferably daily as insulin sensitivity declines rapidly, typically after 48 h of rest [33].

Pregnant women should not engage in moderate to vigorous activities longer than 60 min because of the risk of hypoglycemia. We conducted studies to assess the effect of prolonged exercise in pregnancy at 55–60% VO2 max for 60 min on glucose and insulin levels in the same subjects during and after pregnancy, and we determined that in pregnancy continuous exercise for >45 min can significantly lower the level of glucose approaching hypoglycemia (Fig. 3, Fig. 4) [34].

For subjects that are managed with insulin or oral hypoglycemia agents, appropriate adjustments will have to be made.

In general, one session of exercise is approximately equivalent to one oral hypoglycemic agent.

Mottola et al. demonstrated in their studies that low-risk pregnant women who engage in mild ergometer exercise (30% VO2 max) have a better response to oral glucose tolerance tests than in response to moderate-intensity exercise (at 70% VO2 max) later in pregnancy [35]. After obtaining biopsies from the vastus lateralis muscle in women in late pregnancy, they determined that GLUT4 (glucose transporters sensitive to insulin) was elevated in the mild-exercise subjects (at 16–20 weeks until delivery) compared to moderate-trained subjects [36].

Subsequently, after prescribing a 200-g carbohydrate diet/day, the combination of diet regimen and exercise resulted in improved blood glucose control and gestational weight gain [37].

Section snippets

Concluding remarks

Pregnancy is an opportune time for lifestyle modification, access to medical care is frequent, medical supervision is more intense than during other phases in life, and certainly the motivation is very high.

The many large trials conducted in nonpregnant obese adults provide compelling evidence that lifestyle interventions can prevent or reverse type II diabetes. This has led to the recommendations being issued by the ADA that patients with impaired glucose tolerance or an A1C of 5.7–6.4 should

Conflict of interest

The author has no conflict of interest to declare.

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