Racial Differences in the Association Between Gestational Diabetes Mellitus and Risk of Type 2 Diabetes

Abstract

Background:

It is recognized that a history of gestational diabetes mellitus (GDM) predicts incident type 2 diabetes in women. However, it is unclear if there is a racial disparity between the association of GDM and type 2 diabetes.

Methods:

We studied 1,142 women with a history of GDM and 18,856 women without a history of GDM aged 13–50 years with their first record of pregnancy in Louisiana State University Hospital-Based Longitudinal Study database between 1990 and 2009. History of GDM was used to predict incident type 2 diabetes.

Results:

During a mean follow-up of 8.6 years, 1,394 women developed type 2 diabetes. The multivariable adjusted hazard ratio (HR) of type 2 diabetes was 6.52 (95% confidence interval [CI] 5.73-7.43) among women with GDM compared to women without GDM. Stratification by age, race, and body mass index (BMI) gave similar results. Compared with African American and white women without a history of GDM, the relative risk for type 2 diabetes was higher in African American women than in white women with a history of GDM. Compared with non-GDM women compartments, GDM women after delivery for <1, 1.0–3.9, 4.0–5.9, 6.0–7.9, 8–9.9, and ≥10.0 years had 4.00, 5.44, 4.26, 3.16, 4.49, and 4.17 times higher risk of having type 2 diabetes, respectively.

Conclusions:

A history of GDM is a strong predictor of subsequent type 2 diabetes among Louisiana women, especially among African American women.

Introduction

Type 2 diabetes, a common and serious condition associated with reduced life expectancy and considerable morbidity, has posed a great burden on patients, their families, and healthcare systems.¹ Several studies have demonstrated that type 2 diabetes can be prevented or delayed by implementing lifestyle modifications.^2,3 In order to be cost-effective, lifestyle interventions to prevent or delay type 2 diabetes should be directed toward individuals at increased risk for the disease.^4,5 Therefore, it is of great importance to find clinical predictors of type 2 diabetes. It is recognized that a history of gestational diabetes mellitus (GDM) predicts incident type 2 diabetes in women.^6
–8 It is unclear, however, if there is a racial disparity between the association of GDM and type 2 diabetes because a few studies^9

–12 reporting the association between GDM and type 2 diabetes included subjects from mixed race, and even fewer¹³ studies reported the risk of development of type 2 diabetes after a GDM pregnancy by race. The present study aims to assess the race-specific association between a history of GDM and incidence of type 2 diabetes and evaluate how the risk changes over years after the index pregnancy by using the well-characterized Louisiana State University Hospital-Based Longitudinal Study (LSUHLS) database.

Subjects and Methods

Subjects

Louisiana State University Health Care Services Division (LSUHCSD) operates seven public hospitals and affiliated clinics in different areas in Louisiana that provide quality medical care to residents of Louisiana regardless of their income or insurance coverage.¹⁴ Overall, LSUHCSD facilities have served about 1.6 million unique patients (35% of the Louisiana population) since 1990. In the population served by the LSUHCSD hospitals, about 46% of patients qualify for free care (by virtue of being low income and uninsured), about 10% of patients are self-pay (uninsured, but incomes not low enough to qualify for free care), about 20% of patients are covered by Medicaid, about 14% of patients have Medicare, and about 10% of patients are covered by commercial insurance. The LSUHCSD, the division responsible for the management of the LSUHCSD clinical facilities, has access to the administrative, anthropometric, laboratory, and clinical diagnosis data collected at these facilities. All these data are available in electronic form since 1990 for both inpatients and outpatients (the LSUHCSD Disease Management Evaluation Database [DMED]). Using these data, we have set up the LSUHLS database to follow patients with major chronic diseases. Patients' information on birth date, race, sex, address, types of insurance, family income, smoking habits, date of examination, measurements of height and weight and blood pressure at each visit, diagnosis of various diseases and date of diagnosis, laboratory tests, and medication history were all included in the LSUHLS database.

The cohort of pregnancies, which is part of the LSUHLS, was identified through the LSUHLS database between January 1, 1990, and December 31, 2009. After excluding participants with a history of diabetes at baseline and participants with incomplete data on any required variables, the present analyses include 1,142 women with a history of GDM and 18,856 women without a history of GDM, aged 13–50 years, who presented their first record of pregnancy in the LSUHLS database between 1990 and 2009. The study was approved by both the Pennington Biomedical Research Center and LSU Health Sciences Center Institutional Review Boards.

Assessments

The gestational women's characteristics, such as age, race/ethnicity, postpartum blood pressure, postpartum body mass index (BMI), smoking status, parity and family income, were also extracted from the LSUHLS database. In this dataset, self-reported race/ethnicity was classified as white, African American, Asian, Hispanic, Indian, native Hawaiian or Pacific Islander, other, and unknown. The analyses were restricted to the white, African American, Asian, Hispanic, and Indian groups. Smoking information was recorded as yes or no based on the answers to the question: Have you used tobacco in the past 30 days? Family income was categorized into quartile, ranked from the lowest to the highest. Women with a history of GDM were identified using who had the Ninth Revision of the International Classification of Disease (ICD-9) code 648.8.¹⁴ GDM was defined as follows in the LSUHCSD system: (1) at least two plasma glucose measurements during a 100-g 3-hour or a 75-g 2-hour oral glucose tolerance test (OGTT) equal to or greater than the cutoffs recommended by the American Diabetes Association (ADA) (fasting ≥95 mg/dL; 1-hour ≥180 mg/dL; 2-hour ≥155 mg/dL; 3-hour ≥40 mg/dL),¹⁵ (2) 2-hour plasma glucose or random plasma glucose concentration ≥200 mg/dL according to the World Health Organization (WHO)¹⁶ and ADA recommendation,¹⁷ or (3) fasting plasma glucose ≥126 mg/dL, 2-hour plasma glucose after a 75-g OGTT between 140 and 199 mg/dL (impaired glucose tolerance), or fasting plasma glucose between 110 (from 1997 to 2003)/100 (from 2003) and 125 mg/dL (impaired fasting glucose), according to WHO¹⁶ and ADA criteria.^17,18

Prospective follow-up

Follow-up information was obtained from the LSUHLS database by using the unique number assigned to each patient who visits the LSUHCSD hospitals. ICD-9 codes 250.*0 and 250.*2 were used to identify type 2 diabetes cases during follow-up.¹⁹ Since 1990, LSUHCSD's internal diabetes disease management guidelines call for physician confirmation of diabetes diagnoses by applying the ADA¹⁷ or WHO criteria²⁰: a fasting plasma glucose level ≥7.8 mmol/L (≥7.0 mmol/L from 1998), 2-hour glucose level ≥11.1 mmol/L after a 75-g 2-hour OGTT, one or more classic symptoms plus a random plasma glucose level ≥11.1 mmol/L. Follow-up of each cohort member continued until the date of the diagnosis of type 2 diabetes, the date of the last visit if the subject stopped to use LSUHCSD hospitals, or January 31, 2010.

Statistical analyses

Differences in risk factors at baseline of GDM women and non-GDM women were tested using general linear model after adjustment for age. Cox proportional hazards regression models were used to estimate overall the association of a history of GDM with the risk of incident type 2 diabetes. The proportional hazards assumption in the Cox model was assessed with graphic methods and with models including time-by-covariate interactions.²¹ In general, all proportionality assumptions were appropriate. The analyses were first carried out adjusting for age and further for smoking, income, BMI, systolic blood pressure, parity, and race. A chi-square log-likelihood ratio test will be carried out to test the significance of the interaction terms of prior GDM and age, BMI, and race on the risk of type 2 diabetes. The association between a history of GDM and the risk of type 2 diabetes in different postpartum periods was examined using logistic regression, with adjustment for the noted confounding factors. Postpartum year was categorized as <1, 1.0–3.9, 4.0–5.9, 6.0–7.9, 8.0–9.9, and ≥10.0 years. Statistical significance was considered to be p<0.05. All analyses were performed using the statistical package PASW for Windows, version 18.0 (SPSS Inc, Chicago, IL).

Results

From 1990 to 2009, 19,998 women aged 13–50 years with their first record of pregnancy in LSUHCSD hospitals were identified from the LSUHLS database. Among them, a total of 1,142 women had GDM. During a mean follow-up period of 8.6 years, 1,067 women without a history of GDM and 327 women with a history of GDM developed diabetes. The general characteristics of the study population at baseline by GDM status are presented in Table 1. After adjustment for age, GDM women had significantly higher average postpartum BMI and systolic blood pressure compared with non-GDM women. After adjustment for age, women with a history of GDM had a 7.02 times (95% confidence interval [CI] 6.18-7.96) higher risk of type 2 diabetes compared with women without a history of GDM (Table 2). Additional adjustment for smoking, income, BMI, systolic blood pressure, and race did not appreciably alter the results. Stratification by age, race, and BMI gave similar results. There was no significant interaction of BMI and a history of GDM on the risk of type 2 diabetes. However, there was a significant interaction between age and a history of GDM on risk of type 2 diabetes, which suggested that the extent of risk was stronger among women with gestational age 13–29.9 years than among those with gestational age 30–50 years.

Table 1.

Baseline and Follow-Up Characteristics of Women with and without Previously Diagnosed Gestational Diabetes Mellitus Who Delivered a Baby in Louisiana State University Health Care Services Division Hospitals

Characteristic ^a	Non-GDM women	GDM women	p value for trend
No. of participants	18,856	1,142
No. of incident type 2 diabetes cases	1,067	327
Maternal age, years	24.3 (0.1)	26.8 (0.2)	<0.001
Postpartum body mass index, kg/m²	41.1 (0.4)	48.2 (1.7)	<0.001
Postpartum systolic blood pressure, mm Hg	128 (0.1)	131 (0.6)	<0.001
Postpartum diastolic blood pressure, mm Hg	76 (0.1)	76 (0.4)	0.24
Current smoker, %	19.5	17.9	0.18
Parity,^b %	36.1	53.5	<0.001
Annual family income, $	21,049 (452)	24,494 (1747)	0.056

Data are means (standard deviation [SD]) unless otherwise indicated; all data, except age, adjusted for age.

Parity was defined as birth to more than one baby.

Table 2.

Hazard Ratios for Type 2 Diabetes According to Gestational Diabetes Mellitus Status for Total Study Samples and Stratified by Age, Body Mass Index, and Race

	No. of case/No. of sample		Person-years		Hazard ratios (95% CIs)
	Non-GDM women	GDM women	Non-GDM women	GDM women	Non-GDM women	GDM women	p value for trend	p for interaction
Total sample
Adjustment for age	1,067/18,856	327/1,142	163,703	6,503	1.00	7.02 (6.18-7.96)	<0.001
Multivariate adjustment^a	1,067/18,856	327/1,142	163,703	6,503	1.00	6.52 (5.73-7.43)	<0.001
Age (years)^a								0.001
13–29.9	669/15,233	183/776	132,139	4,204	1.00	8.97 (7.57-10.6)	<0.001
30–39.9	325/3,136	131/337	27,626	2,131	1.00	5.27 (4.27-6.51)	<0.001
40–50	73/487	13/29	3,938	167	1.00	5.30 (2.88-9.76)	<0.001
Body mass index (kg/m²)^a								>0.50
<25	114/4,933	25/170	39,984	1,008	1.00	7.10 (4.53-11.1)	<0.001
25–29.9	161/4,511	40/236	39,109	1,495	1.00	5.64 (3.93-8.09)	<0.001
30–34.9	182/3,482	71/240	30,850	1,330	1.00	8.39 (6.29-11.2)	<0.001
≥35	610/5,930	191/496	53,760	2,670	1.00	6.03 (5.31-7.48)	<0.001
Race^a								>0.10
African American	733/12,484	206/638	112,511	3,758	1.00	7.43 (6.34-8.72)	<0.001
White	300/5,145	89/337	43,954	2,036	1.00	4.63 (3.61-5.94)	<0.001
Asian	2/114	1/20	863	109	1.00	18.1 (0.27-205)	0.177
Hispanic	13/452	14/71	2,826	293	1.00	11.3 (4.37-29.4)	<0.001
Indian	8/101	4/13	939	64	1.00	6.14 (1.63-23.2)	0.007
Race^a,b								<0.025
African American	733/12,484	206/638	112,511	3,758	1.00	7.43 (6.34-8.72)	<0.001
White	300/5,145	89/337	43,954	2,036	1.00	4.63 (3.61-5.94)	<0.001

Adjusted for age, smoking, income, body mass index, systolic blood pressure, parity, and race, other than the variable for stratification.

The analysis was restricted to African American women and white American women, chi-square=5.51, 1 df, p<0.025.

CI, confidence interval.

In race-stratified analysis, white women tended to have the lowest risk to develop type 2 diabetes if they had a history of GDM (Table 2). Although there was no overall significant interaction between race and a history of GDM on the risk of type 2 diabetes (p>0.1), the risk of type 2 diabetes was significantly different between African American women and white women (chi-square=5.51, 1df, p<0.025), suggesting that the risk for developing type 2 diabetes was higher in African American women with a history of GDM than in white women with a history of GDM compared with African American and white women without a history of GDM (Table 2).

The incident rate of type 2 diabetes declined over years during the postpartum period in both GDM and non-GDM women (Table 3); however, GDM women had a higher incident rate at any given years compared to non-GDM women. Compared with non-GDM women, GDM women after delivery for <1, 1.0–3.9, 4.0–5.9, 6.0–7.9, 8–9.9, and ≥10.0 years had a 4.00 (95% CI 2.40-6.67), 5.44 (CI 4.00-7.41), 4.26 (CI 2.74-6.65), 3.16 (CI 1.99-5.06), 4.49 (CI 2.83-7.11), and 4.17 (2.61-6.66) times higher risk of having type 2 diabetes, respectively.

Table 3.

Odds Ratio for Type 2 Diabetes According to Different Follow-Up Periods After Delivery

	No. of participants		No. of cases		Person-years		Incidence rate/1,000 person-years			Odds ratio^a (95% CI)
Postpartum years	Non-GDM	GDM	Non-GDM	GDM	Non-GDM	GDM	Non-GDM	GDM	Incidence rate ratio GDM/non-GDM	Non-GDM	GDM
GDM <1.0	538	149	108	77	505	96	213.9	802.1	3.75	1.00	4.00 (2.40-6.67)
GDM 1.0-3.9	3,131	366	202	119	10,033	965	20.1	123.3	6.13	1.00	5.44 (4.00-7.41)
GDM 4.0-5.9	2,553	158	174	44	14,537	826	12.0	53.3	4.44	1.00	4.26 (2.74-6.65)
GDM 6.0-7.9	3,020	166	171	29	23,174	1,215	7.4	23.9	3.23	1.00	3.16 (1.99-5.06)
GDM 8.0-9.9	3,477	135	158	32	33,575	1,235	4.7	25.9	5.51	1.00	4.49 (2.83-7.11)
GDM ≥10.0	6,137	168	254	26	81,879	2,166	3.1	12.0	3.87	1.00	4.17 (2.61-6.66)

Adjusted for age, smoking, income, body mass index, systolic blood pressure, parity, and race.

Discussion

The present study, involving 19,998 Louisiana women free of type 2 diabetes at baseline, suggested a direct association between a history of GDM and the risk of type 2 diabetes. African American women with a history of GDM showed a higher relative risk for incident type 2 diabetes than white women with a history of GDM. In addition, risk of type 2 diabetes was decreased by the time after index delivery.

The effect of previous GDM on subsequent type 2 diabetes has been studied extensively.^{10,13,22
–24} These studies consistently recognized GDM as an important risk factor for subsequent type 2 diabetes. One early meta-analysis of six controlled follow-up studies indicated that the overall relative risk for developing diabetes after GDM was 6.0.²⁵ In a more recent meta-analysis of 20 cohort studies,⁷ women with a history of GDM were associated with at least a 7-fold increased risk of incident type 2 diabetes. Our results are consistent with previous studies and are in the same magnitude of risk estimates: women with a history of GDM have an overall 5.5-fold increased risk of type 2 diabetes compared with women without a history of GDM after the index pregnancy. Therefore, adequate emphasis should be attached to preventing type 2 diabetes in women with a history of GDM.

Although several studies assessing the association between a history of GDM and type 2 diabetes included mixed ethnic origin subjects,^9

–13 no previous study has compared the relative risk of developing future type 2 diabetes between African American women and white women with a history of GDM. In the current study, African American women with a history of GDM are more prone to developing subsequent type 2 diabetes than white women with a history of GDM, which may partly explain the much higher prevalence of diabetes in African American women than in white women²⁶ even though the rate of GDM is a little lower in African American women than in white women.²⁷ This is also supported by our data, which indicated that the incident rate of type 2 diabetes was similar in African American and white women who did not have a history of GDM. The underlying explanation for the observed African American/white disparity in the association of GDM history with the risk of type 2 diabetes is not clear. The racial disparity observed in vitamin D deficiency, which has been associated with increased inflammatory response and increased risk of type 2 diabetes,²⁸ might play a role.²⁹ In addition, our study provides the risk of development of type 2 diabetes in women with a history of GDM from three other races: Asian, Hispanic, and Indian, although the sample sizes were smaller and the CIs were wide in these races. The risk is highest in the Hispanic and Asian groups, which is consistent with other studies that show these two racial groups having the highest GDM and type 2 diabetes prevalence estimates.^30

–35 Poor medical care and genetic factors may contribute to the higher GDM and type 2 diabetes incidence in Hispanic and Asian women.

In our study, parous women with a history of GDM had a marked risk of progressing to diabetes: an 802.1 incident rate per 1000 person-years over the subsequent year and a 53.3-123.3 incident rate per 1000 person-years over the following 1–5 years, which is in line with the finding from others that the cumulative incidence of type 2 diabetes increased markedly in the first 5 years postpartum.⁸ However, there is no sign of a plateau after 10 year (12.0 incident rate per 1000 person-years). This may be partly explained by different durations of follow-up, different definitions of cohort, ethnic variation, and differences in the diagnosis criteria of GDM and type 2 diabetes. Although several studies have shown barriers to introducing interventions in the early postpartum period,^36
–38 our results again highlight the importance of these interventions and may motivate GDM mothers to attend these interventions.

In light of a growing body of evidence, it is generally accepted that progression to type 2 diabetes of parous women with previous GDM is faster than that of parous women without previous GDM.^{6
–8,10,13,22

–25} However, the exact mechanism linking GDM to type 2 diabetes is not well understood. Because GDM and type 2 diabetes share the same risk factors, such as obesity, physical inactivity, advanced age, ethnic group, and family history of diabetes, and the two conditions are strongly associated with each other, GDM and type 2 diabetes are regarded as sharing a common genetic background more strongly than ever before.^6,39,40 This hypothesis was confirmed by two recent studies that showed that women with previous GDM more frequently display some alleles associated with a high risk of type 2 diabetes.^39,40 As several intervention studies have showed that it is possible to delay or prevent the development of type 2 diabetes among those at high risk^2,3 and a recent clinical trial⁴¹ proved that women with a history of GDM who remained at high risk of developing diabetes benefited from either lifestyle or pharmacologic interventions, determining the true risk of type 2 diabetes in women with a history of GDM and researching into the mechanism behind this association continues to be important.

There are several strengths in our study, including large sample size, high proportion of minorities, long follow-up time, and the use of administrative databases to avoid the problem of differential recall bias. In addition, women in this study use the same public healthcare system, which minimizes the influence of accessibility of healthcare, particularly in comparing African American and white women. One limitation of our study is that our analysis was not performed on a state representative sample of Louisiana, which would limit the generalizability of the study; however, LSUHCSD hospitals are public hospitals and cover over 1.6 million patients, most of whom were middle-income or low-income women. Nevertheless, the present study employed the design of a cohort study and reported both the unadjusted and the adjusted hazard ratios for type 2 diabetes in women who received medical care from Louisiana public hospitals, which provide important information for understanding the scope and burden of type 2 diabetes in Louisiana women, especially those of middle or low income. Second, we do not have enough sample size to fully address other ethnicity-specific associations between GDM history and diabetes risk except the African American/white disparity. In addition, we have no data on possible changes in the lifestyle patterns during the follow-up period. Misclassification during the follow-up period is probably not systematically related to the outcome, but it may weaken the observed association. Even though our analyses were adjusted for age, smoking, income, BMI, systolic blood pressure, parity, and race, and residual confounding due to measurement error in the assessment of confounding factors, such unmeasured factors as physical activity, education, dietary factors, family history of diabetes, gestational characteristics, and adherence to postpartum screening cannot be excluded.

Conclusions

In the current study, a history of GDM is a strong predictor of incident type 2 diabetes later in life. African American women with a history of GDM showed a higher relative risk for incident type 2 diabetes than white women with a history of GDM. A lifestyle intervention targeting women, especially African American women, with a history of GDM may be effective in reducing the burden of type 2 diabetes in Louisiana.

Footnotes

Acknowledgments

This study was supported by the Louisiana State University Improving Clinical Outcomes Network (LSU ICON).

Disclosure Statement

The authors declare that no competing financial interests exist.

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