As the prevalence of diabetes mellitus (DM) continues to rise worldwide,1 it becomes increasingly important to identify high-risk populations that may benefit from an early diagnosis of DM and to implement strategies to delay or prevent the onset of diabetic complications.2,3 Women with a history of gestational diabetes mellitus (GDM) are at high risk for future diabetes, with 17–63% developing DM within 5–16 years of delivery.4,5 It has been estimated that, in some populations, women with a history of GDM may account for up to one third of diabetes cases among parous women.6 Furthermore, there is evidence that the incidence of both GDM and postpartum DM after a diagnosis of GDM may be increasing.7–9 Thus, strategies aimed at prevention and early diagnosis of DM among women who have had GDM could have an impact on population health.6
The American College of Obstetricians and Gynecologists (ACOG) recognizes the risk that GDM confers for the future development of DM but does not make a clear recommendation for postpartum diabetes testing.10 The practice bulletin “Gestational Diabetes”10 notes that such postpartum testing may be performed but also states that no studies verify the benefit of such testing. Furthermore, no stipulation for postpartum DM testing is included in ACOG’s Guidelines for Perinatal Care.11 In contrast, the American Diabetes Association specifically recommends reassessment of maternal glycemic status at least 6 weeks postpartum in women diagnosed with GDM.12 According to the American Diabetes Association, appropriate screening tests, in the absence of symptoms of DM, include either a fasting glucose or an oral glucose tolerance test (OGTT).12,13 If glucose levels are normal in the postpartum period, the American Diabetes Association recommends that women be reassessed at a minimum of every 3 years.12 However, if impaired fasting glucose or impaired glucose tolerance is found without establishing a diagnosis of DM, annual testing is recommended.12 Similarly, the Fourth International Workshop on Gestational Diabetes recommended that glucose tolerance be reevaluated initially at 6–12 weeks postpartum,14 and subsequently as recommended in the Report of the Expert Committee.13 Although American Diabetes Association and ACOG recommendations vary, 75% of surveyed ACOG Fellows, all of whom were practicing obstetricians, reported that they routinely performed postpartum glucose testing in patients with GDM.15 However, actual practice patterns may vary from the self-reported survey data, and women may receive postpartum care from nonobstetric providers. Given the potential benefit of early DM diagnosis in women with a history of GDM and the discrepancy in practice guidelines, we sought to examine postpartum glycemic testing by any practitioner in women diagnosed with GDM at 2 large academic medical centers.
MATERIALS AND METHODS
The study population consisted of women diagnosed with GDM (as identified by International Classification of Diseases, Ninth Revision, code for GDM) at the Massachusetts General Hospital and Baystate Medical Center between the years 2000 and 2001. Women with GDM were considered eligible if the pregnancy resulted in a liveborn infant and follow-up care was performed at the same institution (n = 367). We performed chart review to exclude women with pregestational DM (n = 156) and women in whom documentation of GDM could not be confirmed (n = 14). Therefore, the final sample size was 197. We estimated, based on pilot data, that our sample size would give us 90% power to detect a hazard ratio of 1.7 with a 2-sided type 1 error rate of 0.05. The Massachusetts General Hospital and Baystate Medical Center human subjects committees approved the study.
Clinical and demographic data were obtained from the electronic medical record, including maternal age at the time of delivery, maternal race/ethnicity, body mass index (BMI) at the time of the first prenatal visit, primary language, marital status, type of insurance, and ZIP code of the mother’s primary residence. Race/ethnicity was self-reported as non-Hispanic white, Black, Hispanic, Asian, Other, or Unknown. Median income was estimated from the 2000 census using maternal zip codes. When available, we obtained the 1-hour postchallenge serum glucose level from the 50-g oral glucose loading test administered during pregnancy, and each of the 4 glucose levels from the 100-g fasting diagnostic glucose tolerance test (GTT) performed during pregnancy (fasting, 1-hour, 2-hour, and 3-hour postchallenge levels). For the Massachusetts General Hospital, we were also able to obtain data on the self-reported highest level of education and the site of the primary care physician’s clinic (hospital-based practice, community-based practice, or a practice outside of the institution).
Our primary outcome was the time from delivery to the first postpartum DM screening test. We used several definitions of postpartum DM screening. The first (broad) definition included a random or fasting glucose, glycosylated hemoglobin, or OGTT. We then removed random glucose from our definition, thus defining DM screening as a fasting glucose, glycosylated hemoglobin, or OGTT (intermediate definition). Finally, we defined DM screening according to the American Diabetes Association recommendations as a fasting glucose or OGTT (strict definition). These latter 2 analyses were restricted to the health center (Massachusetts General Hospital) with information on fasting versus random glucose testing (n = 160). As a means of evaluating access to postpartum care, we also examined postpartum Papanicolaou (Pap) testing in the study participants.
Kaplan-Meier estimates of the time from delivery to the first postpartum DM screening test were calculated. Subjects who were not screened were censored at the time of the last laboratory test or clinic visit documented in the electronic medical record. Women with a subsequent pregnancy were censored at 4 weeks gestation during the subsequent pregnancy, because assessment of glycemic status during a subsequent pregnancy could represent a screen for recurrent GDM rather than a screen for DM.
Univariate and multivariable hazards ratios (HRs) were calculated using Cox proportional hazards models. Potential predictors of postpartum DM screening were included in multivariable models as categorical variables. P < .05 was considered statistically significant. Analyses were performed with Stata 7.0 statistical package (Stata Corporation, College Station, TX).
Demographic characteristics of the study subjects are presented in Table 1. The mean age of study participants was 32.2 ± 5.5 years, and the mean BMI was 29.6 ± 7.1 kg/m2. Slightly less than half of the subjects were non-Hispanic white (45.2%). The median annual household income was $43,139, and the majority of subjects (64.5%) had private insurance.
We first used a broad definition of postpartum DM screening that was intended to capture all possible tests that might be used in clinical practice and included a random or fasting glucose, glycosylated hemoglobin, or OGTT. Using this broad definition, only two thirds of women diagnosed with GDM (67%) underwent any postpartum DM screening. The median time from delivery to the first assessment of maternal glycemic status was 136 days (Fig. 1). Of the women who did not undergo postpartum glycemic testing, 40% had over 2 years of follow-up care at the participating institutions, and 25% had over 3 years of follow-up. Because random glucose testing may not have been performed for the purpose of DM screening, we then removed it from our next (intermediate) screening definition. This analysis was restricted to the health center that had information on fasting versus random glucose testing (Massachusetts General Hospital; n = 160). One half (50%) of subjects from this health center underwent a postpartum fasting glucose test, glycosylated hemoglobin test, or OGTT, with a median time from delivery to the first such testing of 295 days. Finally, at the same health center, we examined postpartum DM screening according to the recommendations of the American Diabetes Association, determining the time from delivery to the first fasting glucose test or OGTT (strict definition). Slightly more than one third of subjects (37%) received a postpartum fasting glucose or OGTT, with a median time from delivery to the first such testing of 428 days (Fig. 1). As a means of assessing both access to postpartum care and compliance with a published ACOG screening recommendation, we examined cervical cancer screening in the same group of women. Ninety-four percent of all subjects (from both health centers) underwent postpartum cervical cancer screening using a Papanicolaou (Pap) test, and the median time from delivery to Pap testing was 49 days (Fig. 1).
We then assessed covariates as potential predictors of postpartum DM screening (Table 2). Given that random glucose testing is performed in many clinical settings and is unlikely to be a reliable indicator of postpartum DM screening, we focused subsequent analyses on the 2 stricter screening definitions. The majority of demographic covariates had no effect on postpartum screening according to either definition, including age (> 32 years versus ≪ 32 years), race (non-Hispanic white versus all other), ethnicity (Hispanic versus non-Hispanic), primary language (English-speaking versus non–English-speaking), annual household income (< $31,000 versus ≥ $31,000, which corresponded to the 25th percentile of income in the sample), and insurance status (Medicaid or no insurance versus private insurance). Similarly, BMI (≥ 30 kg/m2 versus < 30 kg/m2) and the 1-hour, 2-hour, and 3-hour post-GTT glucose results from the diagnostic pregnancy GTT (above the geometric mean compared with below the geometric mean for each time point) had no effect on postpartum DM screening according to either the intermediate or the strict definition.
Women with a 1-hour postglucose loading test glucose level at or above the geometric mean (≥ 171 mg/dL) were more likely to undergo postpartum DM screening than were women with a 1-hour postglucose loading test glucose level below 171 mg/dL, according to both the intermediate and the strict definitions (multivariable HRs 2.1, 95% confidence intervals [CIs] 1.3–3.6, and 2.0, 95% CI 1.1–3.5, respectively; Table 2). Similarly, after adjustment for potential confounders, women with a fasting glucose from the pregnancy diagnostic GTT at or above the geometric mean (≥ 98 mg/dL) were more likely to undergo postpartum DM screening than were women with a fasting GTT glucose below 98 mg/dL, according to both the intermediate and the strict definitions (multivariable HRs 2.0, 95% CI 1.2–3.4, and 2.1, 95% CI 1.2–3.9, respectively; Table 2). Although univariate analysis showed an effect of education level on postpartum DM screening according to both the intermediate and the strict definitions, adjustment for potential confounders eliminated this effect (Table 2). Similarly, the site of the primary care physician’s practice had a borderline effect on postpartum DM screening according to the strict definition in univariate analysis but not after adjustment for potential confounding variables (Table 2).
We found that few women diagnosed with GDM at 2 academic health centers were screened for postpartum DM according to the guidelines of the American Diabetes Association. Lack of access to postpartum care is an unlikely explanation for these findings because 94% of all subjects underwent postpartum Pap testing, with a median time from delivery to the first Pap test of 49 days. There are several potential barriers to postpartum DM screening among women diagnosed with GDM. First, conflicting recommendations by professional organizations may contribute to the low rates of postpartum DM screening that we found in our study. Although the 1995 American College of Obstetrics and Gynecology (ACOG) recommendations for postpartum DM screening after GDM were similar to those of the American Diabetes Association (specifically, initial testing in the first few months after delivery and annual testing thereafter16), current ACOG guidelines do not specifically stipulate that a postpartum glycemic evaluation should be performed following pregnancies characterized by GDM.10 Many obstetricians may be unfamiliar with the current American Diabetes Association guidelines, which do recommend postpartum DM screening for women with GDM. The observation that 94% of women underwent Pap testing at approximately 6 weeks postpartum, as recommended by ACOG,10 suggests that consensus on testing guidelines may improve the prevalence of GDM follow-up screening.
Secondly, confusion over provider responsibility (ie, obstetrician or primary care provider) for postpartum DM testing may lead to poor guideline adherence.17 In addition, the termination of “pregnancy-only” medical insurance in the postpartum period may lead some women to not receive postpartum DM screening.18 Clear delineation of provider responsibility, and perhaps state-mandated insurance coverage for postpartum glycemic testing in women with GDM, should be considered given the burden that undiagnosed diabetes places on both the individual and the health care system.
Thirdly, lack of patient awareness of the increased risk of developing postpartum DM may contribute to low rates of postpartum screening. There are limited data on GDM patients’ awareness of the risk of postpartum DM. However, among 28 women with a history of GDM who participated in a long-term pregnancy follow-up study in Sweden, 54% reported that they had never been informed of their increased risk for type 2 diabetes.19 Lack of patient and/or provider awareness of increased DM risk may also mean that women fail to take advantage of strategies aimed at the primary prevention of DM.20
Finally, even if women with GDM are aware of the risk of postpartum DM, they may be unlikely to focus on their own health in the postpartum period given the increase in family obligations. Despite the provision of laboratory requisition slips and instructions for a 4–6 week postpartum OGTT to all new mothers with GDM who delivered at a single U.S. medical center during an 18-month period, only 17.6% of the women (n = 179) underwent postpartum OGTT testing.21 This suggests that barriers to DM screening exist beyond maternal awareness of DM risk and the availability of postpartum glycemic testing.
Although lower socioeconomic status has been associated with reduced access to care,22 reduced quality of care,22 and an increased risk of insulin resistance after GDM,23 we found no effect of education level, primary language, insurance status, median income, or race or ethnicity on postpartum DM screening in multivariable adjusted models. Similarly, elevated BMI, which has been shown to increase the risk of postpartum DM,9,24–26 had no effect on postpartum DM screening. We did find that a higher 1-hour postglucose loading test glucose and a higher fasting glucose from the pregnancy diagnostic GTT, both of which increase the risk of postpartum DM,18,24,27 were associated with postpartum DM screening according to both our intermediate and strict definitions, even after adjustment for potential confounders. Whether awareness of this increased risk influenced postpartum DM screening in our group is unclear.
Our results expand upon prior studies of postpartum DM screening after GDM. In a questionnaire-based study of 66 U.S. women with a history of GDM, all of whom had participated in an initial GDM follow-up study 5 years earlier, Kaufmann et al28 found low self-reported rates of postpartum diabetes testing. Low rates of postpartum DM screening among women with a history of GDM have also been reported in Canada,29 even after the 1998 publication of Canadian Diabetes Association guidelines recommending that women with GDM undergo a postpartum OGTT 6 weeks to 6 months after delivery.30
There are several potential limitations to this study. Because screening was defined by medical record review, it is not possible to know whether glucose testing was performed for the purpose of DM screening. Thus, our broadest definition of DM screening likely overestimates true screening, especially given that random glucose testing may have been performed for other purposes, whereas our strict definition may underestimate DM screening. A second possible limitation is that some women may have undergone DM screening at a nonparticipating institution and would be misclassified as having not been screened when they actually were screened. However, we limited participants of this study to women who had follow-up care at the participating institutions. Furthermore, we chose conservative measures for censoring women, which would lead to an underestimate of the true median time to postpartum DM screening. In addition, the participating institutions have several affiliated outpatient clinics, increasing the likelihood that a woman would receive postpartum care within the participating health care systems. Any laboratory screening that occurred at hospital-affiliated practices would be captured in the centralized electronic medical record. A final limitation of this study is that of generalizability because the work reflects practice at 2 large institutions in a single state. However, the consistency of our findings with those of other studies28,29 suggests that our results may be reflective of general clinical practice.
Further studies are necessary to determine whether our findings are generalizable to other populations of women with GDM and to devise interventions to improve postpartum screening among women with a history of GDM. Among the interventions that should be considered is a formal ACOG recommendation for postpartum DM screening after pregnancies complicated by GDM, a recommendation that might be incorporated into the organization’s Guidelines for Perinatal Care.11 Such studies and recommendations are critically important, given that an early diagnosis of DM could potentially reduce the burden of diabetes complications and improve the outcomes of future pregnancies among young women.
1. King H, Aubert R, Herman W. Global burden of diabetes, 1995–2025: prevalence, numerical estimates, and projections. Diabetes Care 1998;21:1414–31.
2. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33) [published erratum in Lancet 1999;354:602]. UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998; 352: 837–53.
3. Adler AI, Stratton IM, Neil HA, Yudkin JS, Matthews DR, Cull CA, et al. Association of systolic blood pressure with macrovascular and microvascular complications of type 2 diabetes (UKPDS 36): prospective observational study. BMJ 2000;321:412–9.
4. Kjos S. Postpartum care of the woman with diabetes. Clin Obstet Gynecol 2000;43:75–86.
5. Kim C, Newton K, Knopp R. Gestational diabetes and the incidence of type 2 diabetes: a systematic review. Diabetes Care 2002;25:1862–8.
6. Cheung N, Byth K. Population health significance of gestational diabetes. Diabetes Care 2003;26:2005–9.
7. Ferrara A, Kahn H, Quesenberry C, Riley C, Hedderson M. An increase in the incidence of gestational diabetes mellitus: Northern California, 1991-2000 [published erratum in Obstet Gynecol 2004;103:799]. Obstet Gynecol 2004;103:526–33.
8. Dabelea D, Snell-Bergeon J, Hartsfield C, Bischoff K, Hamman R, McDuffie R. Increasing prevalence of gestational diabetes mellitus (GDM) over time and by birth cohort: Kaiser Permanente of Colorado GDM Screening Program. Diabetes Care 2005;28:579–84.
9. Lauenborg J, Hansen T, Jensen D, Vestergaard H, Molsted-Pedersen L, Hornnes P, et al. Increasing incidence of diabetes after gestational diabetes: a long-term follow-up in a Danish population. Diabetes Care 2004;27:1194–9.
10. Gestational diabetes. ACOG Practice Bulletin No. 30. The American College of Obstetricians and Gynecologists. Obstet Gynecol 2001;98:525–38.
11. The American Academy of Pediatrics and The American College of Obstetricians and Gynecologists. Guidelines for perinatal Care. 5th ed. Elk Grove Village (IL): AAP; Washington, DC: ACOG; 2002.
12. American Diabetes Association. Gestational diabetes mellitus. Diabetes Care 2004;27 Suppl 1:S88–S90.
13. Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care 1997;20:1183–97.
14. Metzger B, Coustan DR. Summary and recommendations of the 4th International Workshop-Conference on Gestational Diabetes Mellitus. Diabetes Care 1998;21 suppl 2:B161–7.
15. Gabbe SG, Gregory RP, Power ML, Williams SB, Schulkin J. Management of diabetes mellitus by obstetrician-gynecologists. Obstet Gynecol 2004;103:1229–34.
16. American College of Obstetricians and Gynecologists. Diabetes and pregnancy. ACOG Technical Bulletin 200. Int J Gynecol Obstet 1995;48:331–9.
17. Dornhorst A, Rossi M. Risk and prevention of type 2 diabetes in women with gestational diabetes. Diabetes Care 1998;21 suppl:B43–9.
18. Greenberg L, Moore T, Murphy H. Gestational diabetes mellitus: antenatal variables as predictors of postpartum glucose intolerance. Obstet Gynecol 1995;86:97–101.
19. Linne Y, Barkeling B, Rossner S. Natural course of gestational diabetes mellitus: long term follow up of women in the SPAWN study. BJOG 2002;109:1227–31.
20. Knowler WC, Barrett-Connor E, Fowler SE, Hamman RF, Lachin JM, Walker EA. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 2002; 346: 393–403.
21. Conway D, Langer O. Effects of new criteria for type 2 diabetes on the rate of postpartum glucose intolerance in women with gestational diabetes. Am J Obstet Gynecol 1999;181:610–4.
22. Kelley E, Moy E, Stryer D, Burstin H, Clancy C. The national healthcare quality and disparities reports: an overview. Med Care 2005;43 suppl:I3–8.
23. Kerenyi Z, Tabak A, Stella P, Bosnyak A, Simon K, Karadi I, et al. Association between socioeconomic factors and the metabolic syndrome in women with prior gestational diabetes mellitus. Diabetes Care 2000;23:1444–5.
24. Coustan D, Carpenter M, O’Sullivan P, Carr S. Gestational diabetes: predictors of subsequent disordered glucose metabolism. Am J Obstet Gynecol 1993;168:1139–45.
25. Kerenyi Z, Stella P, Bosnyak Z, Tabak A, Tamas G. Association between central adiposity and multimetabolic syndrome in a special cohort of women with prior gestational diabetes. Diabetes Care 1999;22:876–7.
26. Albareda M, Caballero A, Badell G, Piquer S, Ortiz A, de Leiva A, et al. Diabetes and abnormal glucose tolerance in women with previous gestational diabetes. Diabetes Care 2003;26:1199–205.
27. Schaefer-Graf U, Buchanan T, Xiang A, Peters R, Kjos S. Clinical predictors for a high risk for the development of diabetes mellitus in the early puerperium in women with recent gestational diabetes mellitus. Am J Obstet Gynecol 2002;186:751–6.
28. Kaufmann R, Smith T, Bochantin T, Khardori R, Evans M, Steahly L. Failure to obtain follow-up testing for gestational diabetic patients in a rural population. Obstet Gynecol 1999;93:734–7.
29. Clark H, van Walraven C, Code C, Karovitch A, Keely E. Did publication of a clinical practice guideline recommendation to screen for type 2 diabetes in women with gestational diabetes change practice? Diabetes Care 2003;26:265–8.
30. Meltzer S, Letier L, Daneman D, Gerstein H, Lu D, Ludwig S, et al. 1998 Clinical practice guidelines for the management of diabetes in Canada. CMAJ 1998;159:S1–29.
Figure. No caption available.