Gestational Diabetes During and After Pregnancy

5. Risk Factors for Gestational Diabetes: from an Epidemiological Standpoint

Cuilin Zhang 

(1)

Division of Epidemiology, Statistics and Prevention Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Rockville, MD, USA

Cuilin Zhang

Email: zhangcu@mail.nih.gov

Abstract

Gestational diabetes mellitus (GDM), a common pregnancy complication, continues to be a significant public health and clinical problem, as it carries significant short-term and long-term adverse health outcomes for both mothers and offspring. Moreover, accumulating evidence from in vivo and animal studies demonstrate that maternal hyperglycemia impairs embryogenesis as early as the pre-implantation stages of development. Collectively, these data highlight the significance of understanding risk factors for GDM and preventing GDM among high-risk populations. This chapter summarizes well-characterized risk factors for GDM and reviews major methodological concerns on available epidemiological studies of GDM risk factors. Moreover, this chapter provides a comprehensive review of emerging novel modifiable risk factors that may contribute to the early prevention of GDM. The majority of women with GDM have β-cell dysfunction against a background of chronic insulin resistance to which the insulin resistance of pregnancy is partially additive. Factors that contribute to insulin resistance before pregnancy may also have a deleterious effect during pregnancy, and may constitute risk factors for GDM. Therefore, this chapter reviews risk factors of GDM important in the time window both before and during pregnancy.

5.1 Introduction

5.1.1 Public Health and Clinical Implications of Risk Factors for GDM

Gestational diabetes mellitus (GDM) complicates approximately 1–14% of all pregnancies. With more than 200,000 cases diagnosed annually in U.S., it continues to be a significant public health and clinical problem.1 Importantly, this number is increasing with the increasing prevalence of obesity among women of reproductive age.2 GDM has been related to substantial short-term and long-term adverse health outcomes for both mothers and offspring. Women with GDM have increased risk for perinatal morbidity and a considerably elevated risk for impaired glucose tolerance and type 2 diabetes mellitus in the years following pregnancy.136 Children of women with GDM are more likely to be obese and have impaired glucose tolerance and diabetes in childhood and early adulthood.1 Moreover, accumulating evidence from in vivo and animal studies demonstrate that maternal hyperglycemia impairs embryogenesis as early as the pre-implantation stages of development.78 Collectively, these data highlight the importance of understanding risk factors for GDM and preventing GDM among high risk populations. Ongoing research and public health goals are to understand and short-circuit the vicious cycle involving GDM, childhood obesity and metabolic disorders, and adulthood obesity and diabetes.

5.1.2 Risk Factors Both Before and During Pregnancy are Relevant

Normal pregnancy, especially the third trimester, is characterized by profound metabolic stresses on maternal lipid and glucose homeostasis, including marked insulin resistance and hyperinsulinemia.911Although the underlying mechanisms are yet to be precisely identified, insulin resistance and inadequate insulin secretion to compensate for it play a central role in the pathophysiology of GDM.9 Women who develop GDM are thought to have a compromised capacity to adapt to the increased insulin resistance characteristic of late pregnancy, primarily during the 3rd trimester.9 Pregnancy-related metabolic challenges unmask a predisposition to glucose metabolic disorders in some women.9,12,13 The majority of women with GDM have β-cell dysfunction against a background of chronic insulin resistance to which the insulin resistance of pregnancy is partially additive.9 Factors that contribute to insulin resistance or relative insulin deficiency both before and during pregnancy may have a deleterious effect during pregnancy and may be risk factors for GDM. Less attention has been paid to pregravid risk factors for GDM. This chapter reviews major risk factors not only during, but also before pregnancy. Particular attention will be paid to emerging modifiable factors as these likely have substantial implications for the prevention of GDM.

5.2 Risk Factors

5.2.1 Overview of Risk Factors of GDM: Evidence from Epidemiologic Studies

Relatively few epidemiological studies have been conducted to identify risk factors of GDM.1415 As discussed in earlier chapters, the diagnostic criteria and screening strategy for GDM and the measurements of risk factors vary significantly across study periods and study populations, which makes it difficult to compare findings across studies. Moreover, substantial heterogeneity exists in the approach analyzing the association between risk factors and GDM risk. The majority of earlier studies on risk factors of GDM failed to address bias due to potential confounding by other risk factors. Further, the actual number of GDM cases in the majority of studies is rather low, hampering solid conclusions. Despite these methodological concerns, several GDM risk factors consistently emerge.

Excessive adiposity, advanced maternal age, a family history of type 2 diabetes, and a prior history of GDM are well recognized risk factors of GDM.1418 Among them, excessive adiposity is the most important modifiable risk factor, especially in view of the escalating burden of obesity among women of reproductive age across different race/ethnicity populations in the past decade.19 The risk of GDM increases significantly and progressively in overweight, obese, and morbidly obese women.2022 Women with a family history of type 2 diabetes (particularly maternal history), as compared with women without such a history, experience a 1.4–2-fold increase in the risk of GDM.1418,23 Cigarette smoking has not been consistently identified as a risk factor of GDM.14,16,18,2428 Available data suggest that the magnitude of possible association between maternal smoking (before and during pregnancy) and GDM may be modest. Asian, Hispanic, and Native American women, as compared with Caucasian women, have an increased risk of GDM.14,1618,29 African American women have been reported to have an increased risk of GDM, as compared with Caucasians, by some,18,30 although not all16,29investigators. A very small, but emerging literature also suggests that short maternal stature may be associated with an increased risk of GDM.3135 For instance, results from one study of Greek women demonstrated that the mean height of GDM patients was significantly shorter than normoglycemic controls (158 cm vs. 161 cm; p-value <0.05). This average reduction in height was independent of maternal prepregnancy obesity, age, and socio-economic status.32 Studies among women of other race/ethnicity also provided evidence suggestive of an increased risk of GDM associated with short maternal stature.31,3335 Other reported risk factors include, but are not limited to, polycystic ovary syndrome, previous stillbirth, high blood pressure during pregnancy, and multiple pregnancies.14

5.2.2 Modifiable Risk Factors

In the past decade, increasing efforts were made to identify risk factors for GDM, in part due to the escalating prevalence of diabetes and obesity worldwide. Subsequently, several potentially novel risk factors for GDM have been identified. A series of studies have linked physical activity before and/or during pregnancy with a reduced risk of GDM.3643 This effect seems to increase with increasing intensity of and time spent on the physical activity. Moreover, a few studies provided some suggestive evidence of dietary factors both before and during pregnancy acting as potentially modifiable contributors to GDM risk.4452 For instance, findings from some studies,46,47(although not all),4647,53 suggested that polyunsaturated fat intake may be protective against glucose intolerance in pregnancy, and high intake of saturated fat may be detrimental.48 Prepregnancy overall dietary patterns, in particular, a diet characterized by high intake of red meat, processed meat, refined grain products, sweets, French fries, and pizza was associated with an increased risk of developing GDM.50

5.2.3 Nonmodifiable (Genetic) Risk Factors

Available data suggests that genetic factors may also play a role in the etiology of GDM, as discussed in greater detail in a separate chapter in this book. For instance, GDM is clustered in families and displays a familial tendency.1754 Moreover, GDM recurred in at least 30% (range 30–91%) of women with a history of GDM14,52,5456 suggesting that there is a subgroup of women who may be genetically predisposed to developing this complication of pregnancy. Furthermore, defects in both insulin secretion and insulin activity are crucial in the pathogenesis of GDM. A recent study has shown major genetic components in both traits; more than 75% of the variations in insulin secretion trait can be explained by genetic component and at least 53% by peripheral insulin sensitivity.57 Very few studies have been conducted to identify susceptibility genes for GDM.5859 Inference from limited studies was hindered by small sample size, retrospective design, lack of systematic analysis of common variants of the candidate gene, and lack of consideration of the effect of nongenetic factors.

The remainder of this chapter concerns emerging modifiable risk factors that may contribute to the early prevention of GDM, which may help to dissect the vicious circle involving GDM, childhood obesity and metabolic disorders, and adulthood obesity and diabetes.

5.3 Modifiable Factors and GDM Risk

5.3.1 Physical Activity

Accumulating evidence from epidemiological and clinical studies among nonpregnant individuals support the thesis that physical activity can influence glucose homeostasis through its direct or indirect impact on insulin sensitivity and secretion. By increasing insulin sensitivity and improving glucose tolerance via several mechanisms, physical activity has a beneficial effect on many aspects of insulin resistance syndromes.6062 After an episode of physical activity, insulin sensitivity was improved for up to 48 h by increasing cellular sensitivity to circulating insulin.63 In addition to this acute effect, longer-term, even relatively modest, increases in habitual physical activity induce adaptations that can profoundly affect glucose tolerance61 and potentially reduce GDM risk. Long-term improvement in glucose tolerance and increased insulin sensitivity may also result from physical activity-induced reductions in fat mass and increases in lean muscle mass.6465

Recently emerging studies on the impact of physical activity on pregnant women are limited. The definitions used to classify intensity, amount, and type of physical activity varied considerably, making comparisons between studies difficult. Furthermore, the actual number of GDM cases in the majority of studies is rather low, hampering solid conclusions. Despite these limitations, several studies have linked physical activity before and/or during pregnancy to a reduced risk of GDM.3643 This effect seems to increase with increasing intensity of and time spent on the physical activity. For instance, in a prospective study of 21,765 women who reported at least one singleton pregnancy in the Nurses’ Health Study II, women in the highest quintile of habitual recreational physical activity before pregnancy (specifically vigorous activity, which is equivalent to approximately 30 min a day of brisk walking) had a ∼20% risk reduction for the development of GDM.43 Similarly, Oken et al observed that physical activity before pregnancy (particularly vigorous activity) was associated with a reduced risk of either GDM or any antepartum glucose intolerance (risk reductions of 44 and 24%, respectively).41 In both a prospective study and a case-control study, Dempsey et al found that leisure-time physical activity (i.e., nonoccupational activity) in the year prior to pregnancy was correlated with a significantly lower risk of GDM.37,38

Evidence of the effects of physical activity during pregnancy on GDM risk is suggestive but inconclusive. One study reported a significant protective effect,37 while others found an association,36,38,39,41,66albeit at statistically insignificant levels. In a case-control study, Dempsey et al found that participating in any recreational activities during the first 20 weeks of pregnancy reduced GDM risk by 48%.37 Both Dempsey et al and Oken et al38,41 in prospective cohort studies reported that physical activity during early pregnancy appeared to be associated with lower risk of developing GDM; however, the findings were not statistically significant. Dye et al observed that women who exercised weekly for at least 30 min, at some time during pregnancy, had lower risk of GDM, although this result was found only for morbidly obese women (body mass index (BMI) >33 kg/m2).39 Using data that were nationally representative of women with live births, Liu et al found considerable evidence that those who began physical activity during pregnancy had less risk of developing GDM than those who were inactive.40 Women with activity levels above the median had 67% lower odds of developing GDM.

5.3.2 Dietary Factors

Substantial evidence indicates that diet is linked to the development of glucose intolerance. An extensive body of literature has reported both protective and risk-enhancing associations between particular dietary factors and type 2 diabetes in adult men and nonpregnant women. These studies suggest that total carbohydrate and fat intake are not related to type 2 diabetes risk, but specific types of carbohydrates may be protective, e.g., whole grains,6770 and specific types of fats (e.g., trans and n-3 polyunsaturated fats)7175 may be risk-enhancing.7677 Dietary treatment/counseling has long been recommended for women who developed GDM. However, studies of the association of dietary factors with the risk of development of GDM have just emerged recently.

A limited number of studies have examined diet before and/or during pregnancy as a potentially modifiable contributor to the development of GDM.4452 Earlier studies on the effect of diet during pregnancy, many of which were cross-sectional or retrospective in design, suggested that macronutrient components of the diet in mid-pregnancy may predict incidence4648,49 or recurrence52 of GDM. For instance, findings from some studies,46,47although not all,464753 suggested that polyunsaturated fat intake may be protective against glucose intolerance in pregnancy and high intake of saturated fat may be detrimental.48 Of note, these analyses did not adjust for or consider the impact from other types of fat, which is important as intake of different fat subtypes tends to be correlated and may have opposing effects.76 A recent prospective study, considering the correlation of nutrients, showed that higher intake of fat and lower intake of carbohydrates may be associated with increased risk of GDM and IGT.49 The number of GDM cases in the majority of studies is rather low. Thus far, no concrete conclusion can be drawn as to the role of dietary factors during pregnancy in the development of GDM.

Emerging data,45,50 primarily from the Nurses’ Health Study II, suggested that pregravid diet is associated with the risk for glucose intolerance during pregnancy. In this large prospective study, strong associations were observed between the Western diet, on one hand, and prudent dietary patterns on the other, and GDM risk.50 The prudent pattern was characterized by a high intake of fruits, green leafy vegetables, poultry, and fish, whereas the Western pattern was characterized by high intake of red meat, processed meat, refined grain products, sweets, French fries, and pizza. The association with the Western pattern was largely explained by intake of red and processed meat products. Pregravid intake of red and processed meats were both significantly and positively associated with GDM risk, independent of known risk factors for type 2 diabetes and GDM. For instance, compared with those women who consumed less than two servings of red meat per week, those who consumed more than six servings of red meat per week had a 1.74-fold increased risk of GDM (relative risk (RR), 95% confidence interval (CI) 1.74 (1.35, 2.26)). In addition, pregravid consumption of dietary total fiber and cereal and fruit fiber were significantly and inversely associated with GDM risk.45 In contrast, dietary glycemic load was positively associated with GDM risk. The glycemic index is a relative measure of the glycemic impact of carbohydrates in different foods.78 Total glycemic load was calculated by first multiplying the carbohydrate content of each food by its glycemic index value, then by multiplying this value by the frequency of consumption and summing the values from all food. Dietary glycemic load thus represents the quality and quantity of carbohydrate intake and the interaction between the two. Each 10-g/day increment in total fiber intake was associated with a 26% (95% CI 9–49) reduction in risk; each 5-g/day increment in cereal or fruit fiber was associated with a 23%936 or 26%542 reduction, respectively. The combination of high glycemic load and low cereal fiber diet was associated with 2.15-fold (95% CI 1.04–4.29) increased risk of GDM compared with the reciprocal diet. Although the observational design of the study does not prove causality, these findings suggested that pregravid diet was associated with women’s susceptibility to GDM. Future clinical and metabolic studies are warranted to confirm these findings.

5.3.3 Cigarette Smoking

Cigarette smoking has been associated with increased insulin resistance and increased risk for developing type 2 diabetes among men and nonpregnant women.79 Despite some evidence for heterogeneity, the association was overall robust and consistent across a range and variety of smoking patterns, demographics, and study characteristics.80,81

Cigarette smoking is still common among pregnant women although an 8% reduction in the number of women who smoke during pregnancy was observed in the past decade.82 Cigarette smoking has not been repeatedly identified as a risk factor for GDM.141618,2428 Available data suggest that the magnitude of possible association is modest, with limited studies reported an elevated risk associated smoking.2425 Some of the variation between studies can be attributed to variations in study design, characteristics of study population, ascertainment of the dose of cigarette smoking, the content of cigarettes such as nicotine and additives, and the degree of adjustment for confounding effects. Although many women who smoke before pregnancy stop smoking or reduce the number of cigarettes smoked once they are pregnant, in the Nurses’ Health Study II, habitual smokers had a 1.43-fold increased risk for GDM in subsequent pregnancies (RR (95% CI): 1.43 (1.14, 1.80)) after the adjustment of potential confounders, including BMI.18

5.3.4 Weight Characteristics

Excessive adiposity is the major well-characterized modifiable risk factor for GDM. Numerous studies across diverse populations have reported an increased risk of GDM among women who are overweight or obese compared with lean or normal-weight women.1,1518,2022 In a recent meta-analyses20 of 20 relevant studies published between 1980 and 2006, the risk of developing GDM is approximately 2, 3, and 6 times higher among overweight, obese, and severely obese women, respectively, as compared with normal-weight pregnant women; the adjusted odds ratios (95% CI) of GDM were 1.86 (1.22–2.78), 3.34 (2.43–4.55), and 5.77 (3.60–9.39), respectively. Moreover, the meta-analysis found no evidence that these estimates were substantially affected by selected study characteristics (publication date, study location, parity, study design (prospective vs. retrospective), and the prevalence of GDM among normal-weight women).

In addition to prepregnancy adiposity, emerging evidence suggests that weight change, specifically excessive weight gain during various periods of adult life before pregnancy, is associated with increased risk of GDM. In two prospective studies,18,22 self-reported weight gain of 10.0 kg or more from 18 years to shortly before pregnancy was associated with more than a twofold increased risk for GDM as compared with relatively stable weight. Weight gain 2.3–10.0 kg within 5 years before pregnancy was related to a significantly increased risk of GDM in a recent nested case-control study.21 Taken together, all these data suggest that efforts to prevent obesity and weight gain among young women may help to reduce GDM risk.

5.4 Conclusions and Research Agenda

The escalating prevalence of obesity and diabetes worldwide, the substantial increase in the incidence of GDM during recent years, and the short-term and long-term adverse health outcomes for both women and offspring associated with GDM, highlight the significance of preventing GDM among women at high risk. Emerging evidence from observational studies suggest that several modifiable factors, in particular, pregravid excessive adiposity, recreational physical activity before and during pregnancy, and pregravid western dietary patterns may be related to elevated GDM risk. Pregnant women, or women planning pregnancy, are generally highly motivated to follow advice to improve the outcome of pregnancy, and hence pregnancy represents an ideal time in life to advocate a healthy lifestyle.

At present, there are no large-scale systematic lifestyle intervention studies of GDM for women at high risk. Before initiating such studies, adequately powered dose response studies are needed to evaluate the efficiency and efficacy of interventions and to define optimal interventions. Such interventions must also be evaluated in the context of neonatal outcomes and offspring’s long-term health outcomes.

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