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The Journal of Clinical Endocrinology & Metabolism Vol. 93, No. 6 2142-2148
Copyright © 2008 by The Endocrine Society

Reproductive History and Hormonal Birth Control Use Are Associated with Coronary Calcium Progression in Women with Type 1 Diabetes Mellitus

Janet K. Snell-Bergeon, Dana Dabelea, Lorraine G. Ogden, John E. Hokanson, Gregory L. Kinney, James Ehrlich and Marian Rewers

Barbara Davis Center for Childhood Diabetes (J.K.S.-B., G.L.K., M.R.) and Departments of Preventive Medicine and Biometrics (D.D., L.G.O., J.E.H.) and Medicine (J.E.), University of Colorado at Denver and Health Sciences Center, Denver, Colorado 80045; and George Washington University Medical Center (J.E.), Washington, D.C. 20037

Address all correspondence and requests for reprints to: Janet K. Snell-Bergeon, Barbara Davis Center for Childhood Diabetes, University of Colorado at Denver and Health Sciences Center, P.O. Box 6511, Mail Stop A-140, Aurora, Colorado 80045. E-mail: janet.snell-bergeon{at}uchsc.edu.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Context: Coronary artery disease is increased in women with type 1 diabetes (T1D), compared with nondiabetic (Non-DM) women. Women with T1D have more menstrual dysfunction and are less likely to use hormonal birth control (BC) than Non-DM women.

Objective: The purpose of this study was to determine whether coronary artery calcium (CAC) is associated with menstrual dysfunction and BC use in women with T1D.

Materials and Methods: This was a prospective cohort study, and participants were followed up for an average of 2.4 yr.

Patients: Patients included 612 women (293 T1D, 319 Non-DM) between the ages of 19 and 55 yr who had CAC measured twice by electron beam tomography.

Results: Irregular menses and amenorrhea were more common in T1D than Non-DM women (22.1 vs. 14.9%, P < 0.05 and 16.6 vs. 7.0%, P < 0.001). T1D women reported less BC use than Non-DM women (79.8 vs. 89.9%, P < 0.001) and reached menarche at an older age (13.1 ± 1.8 vs. 12.8 ± 1.5 yr, P < 0.05). Use of BC was associated with less CAC progression in all women, but this association was stronger in T1D women (P value for interaction = 0.02). Irregular menses were associated with greater CAC progression only among T1D women.

Conclusions: A prior history of BC use is associated with reduced CAC progression among all women, with a stronger association in T1D than in Non-DM women. Women with T1D who report irregular menses have increased CAC progression, compared with those with regular menses.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
Whereas coronary artery disease (CAD) is the leading cause of death among both men and women with T1D (1), the relative increase in risk is much greater in women than men (2). It is estimated that women with T1D may have an increase in CAD risk at least 9 times that of women without diabetes, in contrast to an estimated 4-fold increase in risk among men with T1D, compared with nondiabetic men (1, 3, 4, 5). Premenopausal women normally have a significantly lower risk of CAD than men, but women with T1D lose much, if not all, of this protection (2, 6, 7). Whereas gender differences have been reported in the risk factors associated with CAD, women with T1D experience the same rates of CAD events as men (2).

Differences in conventional risk factors do not explain all of the increased CAD risk associated with T1D in women, and these women lose the normal premenopausal protection against CAD (2). The reason for this loss of normal premenopausal protection against CAD is presently unknown. Ovarian dysfunction and irregular menstrual cycles have been shown to be associated with increased CAD risk in nondiabetic women (8) and are more common in women with T1D than women without diabetes (9, 10, 11). Previous studies have shown that women with T1D who have abnormal menstrual cycles and no residual insulin secretion have reduced estrogen and estradiol levels, in addition to low levels of LH, suggesting suppression of ovarian function (12). A recent study of angiographic CAD among premenopausal women found a more than 7-fold increase in CAD associated with hypoestrogenemia due to hypothalamic suppression of ovarian function (13). Given this evidence, it is possible that at least part of the increased risk of CAD in women with T1D may be related to hypoestrogenemia.

The use of exogenous estrogen may have beneficial effects on CAD risk in premenopausal women with low estrogen. However, there has been some concern that oral contraceptives may not be appropriate for use in women with T1D or other metabolic problems (14, 15) because there is some evidence they may increase insulin resistance (16), lipoprotein abnormalities, and microalbuminuria (17). Several studies have supported the use of oral contraceptives in T1D, showing that the use of oral contraceptives does not appear to affect glycemic control or insulin resistance (14, 18, 19). The American College of Obstetrics and Gynecology practice bulletin states that hormonal contraception in diabetes should be limited to nonsmoking women younger than 35 yr old with no hypertension or vascular disease, including retinopathy and nephropathy (20). As a result, women with T1D are less likely to use hormonal birth control than nondiabetic women (10).

It is now increasingly recognized that women with T1D have more menstrual dysfunction than women without diabetes (9, 10, 11, 21, 22, 23), and alterations in menstrual function and reproductive hormone levels have been shown to be associated with increased CAD risk in nondiabetic women (8, 24, 25). However, to our knowledge no studies have yet examined whether menstrual dysfunction is associated with CAD in women with T1D, and the long-term relationship between exogenous hormone use and CAD in these women is poorly understood. Several small studies reported a protective effect of oral contraceptive use on CAD risk in women with T1D (26, 27), but the effect of oral contraceptive use or other hormonal contraceptives on long-term risk of CAD in women with T1D needs further study. The purpose of this study was to determine whether menstrual irregularity is associated with increased coronary artery calcium (CAC) progression in women with and without T1D, whether HBC therapy is associated with decreased CAC progression in women with and without T1D, and whether these relationships differ by diabetes status.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Study participants

A total of 1420 people, including 737 women, were enrolled in the Coronary Artery Calcification in Type 1 Diabetes study. The purpose of this study was to determine which factors predict a significant increase in coronary artery calcium or the development of clinical CAD in people with T1D. An additional study goal was to investigate potential explanations for the relatively greater impact of diabetes on CAD risk in women than men. One female participant and three male participants did not meet the inclusion criteria and were dropped from the study as previously described (28). Of the 736 female study participants, 612 completed two visits with coronary calcium measurements. Study participants were 293 women with T1D and 319 women who reported never having been diagnosed with diabetes, including gestational diabetes, and were recruited from among the spouses and friends of the participants with diabetes. All participants were 19–55 yr of age and had no history of myocardial infarction, coronary artery bypass surgery, or angioplasty. Inclusion criteria for participants with diabetes were diagnosis before the age of 30 yr or positive antibodies or a clinical course consistent with T1D; insulin therapy within 1 yr of diagnosis; and long-standing diabetes (mean duration 24 yr, range 4–52 yr). Despite the use of these entrance criteria, it is possible that some women had type 2 diabetes. All participants provided informed consent, and the study protocol was approved by the Colorado Combined Institutional Review Board.

Examination and laboratory measurements

Participants completed a baseline examination between March 2000 and April 2002, and a follow-up examination between December of 2002 and March of 2005. At each visit, participants came to the clinic after a 12-h fast for blood collection, anthropometric measurements, and examination as previously described (6). Hypertension was defined as a blood pressure 140/90 mm Hg or greater or current antihypertensive treatment as outlined in the National Cholesterol Education Program Adult Treatment Panel III final report (29). Participants self-reported their smoking history and reproductive history.

CAC measurement by electron beam computed tomography (EBCT)

At each visit, two sets of high-resolution, noncontrast, contiguous 3-mm tomographic images were acquired at 100-msec exposure on an Imatron C-150XLP EBCT scanner (Imatron, San Francisco, CA) as previously described (6). The two sets of scans were acquired within 5 min.

Hormonal birth control use

Women were asked a single question regarding use of hormonal methods of birth control, which asked them whether they had ever used oral contraceptives, Norplant, or Depo-Provera. It is therefore not possible to separate out these methods. However, this study is ongoing and women are now being asked about their lifetime history of use of each of these methods separately. Based on the 506 women who have returned for an additional visit to date, the use of Norplant was rare, with only one woman reporting the use of Norplant and never having used oral contraceptives. Similarly, the use of Depo-Provera was uncommon, with only six women reporting the use of Depo-Provera and no use of oral contraceptives. Among the 506 women, the use of oral contraceptives before the baseline visit when assessed separately from other hormonal birth control methods was reported in 422 of women overall (83.4%): 197 of the 245 women with T1D (80.4%) and 225 of the 261 women without diabetes (86.2%).

Statistical analysis

Continuous variables were examined for a linear relationship with CAC progression. CAC scores were positively skewed, with a high frequency of zero values. Coronary calcium interpolated volume from each scan was square root transformed to reduce the variance across coronary calcium scores (30), and the square root transformed volumes were averaged for each visit. The difference between mean square root transformed coronary calcium volumes was calculated from the baseline visit to the follow-up visit. Progression of coronary calcium was defined as an increase in square root transformed coronary calcium volume 2.5 or greater over the course of the two visits (30) or development of clinical CAD between the baseline and follow-up visit (myocardial infarction, coronary artery bypass graft surgery, or angioplasty). Variables of interest were compared between women with and without T1D using a two-sample t test for continuous variables and a {chi}2 test for categorical variables.

The change in square root transformed coronary artery calcium volume over the follow-up period was examined using linear regression. Logistic regression was used to examine the age-adjusted association between variables of interest and progression of CAC. All statistical tests were two sided, with P < 0.05 considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Characteristics of the study cohort are shown in Table 1Go, stratified by diabetes status. Women with T1D were younger on average than the nondiabetic women enrolled in the study. Coronary artery calcium volume at baseline, change in calcium volume from baseline to visit 2, and progression of calcium volume were all significantly higher in women with T1D than women without diabetes. There were five women who developed clinical CAD, all with T1D.


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  		TABLE 1. Women’s reproductive history by diabetes status

 
A significantly lower proportion of women with T1D reported ever using hormonal birth control (oral contraceptives, Depo-Provera, or Norplant) than women without diabetes (79.8 vs. 89.9%, P < 0.001), although the proportion of women reporting current use of hormonal birth control did not differ by diabetes status (27.4 vs. 26.5%).

Menstrual history differed significantly by diabetes status, with women with T1D reporting significantly later menarche, longer menstrual cycles, more irregular menstrual periods, and more amenorrhea. Altogether, 30.5% of women with T1D reported menstrual dysfunction (irregular periods and/or amenorrhea), compared with 19.0% of nondiabetic women (P < 0.001).

The proportion of women who had ever been pregnant did not differ by diabetes status, and neither did the total number of pregnancies reported. However, the number of live births was significantly lower among women with T1D. The percentage of women who were postmenopausal by self-report did not differ by diabetes status.

Characteristics of the study participants by diabetes and history of hormonal birth control (BC) use is shown in Table 2Go. Among women with T1D, those who had never used BC were older and had longer diabetes duration, were more likely to be hypertensive, and had a later average age at menarche. In addition, women with T1D who had never used BC had higher CAC scores at baseline, a greater change in coronary calcium volume, and were more likely to have significant progression of CAC than women with T1D who had used BC. The only significant difference among women without diabetes by BC status was a higher number of total pregnancies and live births among never BC users than among BC users.


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  		TABLE 2. Characteristics by diabetes status and ever use of BC

 
Results of a linear regression analysis are shown in Table 3Go. Among both women with and without T1D, use of hormonal birth control was associated with significantly less progression of calcium volume, although this association was stronger in women with T1D (P value for interaction term = 0.02). A history of irregular menstrual periods was associated with increased progression of calcium volume among women with T1D but not among nondiabetic women (P value for interaction term = 0.04). Additional covariates that were significantly associated with progression of calcium volume in women with T1D were longer diabetes duration, greater baseline coronary artery calcium volume (square root transformed), hypertension, and smoking. Older age (P = 0.07) and race (P = 0.05) were also associated with progression of calcium volume in women with T1D, although these did not reach significance. Among nondiabetic women, the only other significant covariates were older age, baseline CAC volume, and body mass index. There was no significant association of high-density lipoprotein (HDL) cholesterol, low-density lipoprotein (LDL) cholesterol, or years of school completed with progression of calcium volume in either group.


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  		TABLE 3. Determinants of CAC progression in multiple linear regression analysis, stratified by diabetes status1

 
We then examined whether the duration of hormonal birth control use was significantly associated with calcium volume progression in a linear fashion. As shown in Fig. 1Go, a dose-response relationship was found between duration of hormonal birth control among both women with (P value for linear trend =0.007) and without T1D (P value for linear trend = 0.02).


Figure 1
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  		FIG. 1. Association between duration of hormonal BC use and CAC progression by diabetes status.

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
In this study, use of hormonal birth control was associated with reduced progression of coronary artery calcium in all women, although this association was stronger among women with T1D. Only two previous studies have examined whether prior use of hormonal birth control is associated with cardiovascular disease in women with diabetes. Klein et al. (27) reported in 1999 on a study of women with younger- and older-onset diabetes and mortality. Among the younger-onset diabetes patients, use of oral contraceptives was associated with reduced all-cause mortality and a nonsignificant 55% reduction in heart disease deaths, although a lack of power in this study to detect heart disease events was noted. A recent report from the Women’s Ischemia Syndrome Evaluation study found that past use of oral contraceptives was associated with significantly less angiographic coronary artery disease among postmenopausal women with and without diabetes (31).

Irregular menstrual periods were associated with increased progression of CAC only among women with T1D in this study. To our knowledge, no prior studies have reported on an association of irregular menstrual periods with CAD among women with T1D. However, the Nurses’ Health Study reported that in their cohort irregular and very irregular menstrual periods were associated with increased risk of fatal and nonfatal CAD (8). Irregular and long menstrual cycles are indicative of underlying disturbances of the reproductive axis, and sex hormones have both direct and indirect effects on the vasculature. Irregular and anovulatory cycles are a marker of polycystic ovary syndrome (PCOS), an endocrine condition associated with elevated testosterone levels and obesity.

Elevated androgen levels are associated with increased CAD risk factors, although prospective mortality studies have not demonstrated an increased risk of fatal CAD. Androgens affect the vasculature through increasing proliferation of smooth muscle cells and adhesion molecules. Whereas menstrual cycle irregularity is a common finding in women with T1D, reproductive hormone levels associated with irregular, long, or anovulatory cycles in these women have not been well characterized. PCOS and elevated androgen levels have been reported to be common among women with T1D, with PCOS reported in 19% of women with T1D, compared with an estimated 6% of women in the general population.

Amenorrhea in women with T1D is associated with low levels of estrogen, suggesting suppression of ovarian function (12, 32). It appears that this may be due to disturbances in the GnRH pulse generator rather than pituitary insufficiency because stimulated gonadotropin levels are normal in amenorrheic women with T1D (33). In a study of amenorrheic vs. normally menstruating women with T1D, la Marca et al. (33) found that 24-h cortisol levels were elevated, and LH, FSH, and estradiol were lower in women with amenorrhea than normally menstruating women. This suggests that chronic stress could increase cortisol releasing hormone, leading to inhibition of GnRH secretion and hypogonadotrophic amenorrhea. Low estrogen levels are associated with increased angiographic coronary artery disease (13), and it has been demonstrated that estrogen increases nitric oxide uptake by the endothelium and also has effects on lipids, which can inhibit the formation of fatty streaks and thereby prevent the development of atherosclerosis (34, 35).

Evidence from primate animal studies demonstrates that combination oral contraceptives protect against atherosclerosis in female monkeys with stress-induced estrogen deficiency, which suggests a possible mechanism for a protective effect of oral contraceptive use in women with T1D (36), who are at risk of hypoestrogenism (32, 33). Furthermore, premenopausal stress was shown to increase atherosclerosis in postmenopausal female monkeys, and intake of oral contraceptives during the premenopausal period ameliorated the effect of stress on postmenopausal atherosclerosis (37), which is consistent with the theory that earlier exposure to estrogen can prevent future development of coronary artery disease.

The results from this study also confirm prior reports (10) that women with T1D, when compared with nondiabetic women, are significantly less likely to use hormonal birth control and more likely to experience menstrual dysfunction, including irregular periods, amenorrhea, and long menstrual cycles. In addition, we found that women with T1D experienced later menarche (10, 38).

A limitation of this study is that the use of hormonal birth control was assessed in a single question regarding use of oral contraceptives, Depo-Provera, and Norplant. As described in Subjects and Methods, the use of Norplant and Depo-Provera by themselves are rare in this cohort. As a result, whereas there may be some misclassification, the main hormonal birth control method used by women in this cohort is oral contraceptives. The effect seen in this study would be biased in the direction of the null if some users of progestin are misclassified as oral contraceptive users.

In conclusion, the results of this study suggest that hormonal birth control therapy may be associated with a reduction in the development of atherosclerosis in all women, and the strength of this association may be greater in women with T1D. This finding is important because women with T1D are at increased risk for CAD and may also be more likely to have estrogen deficiency, menstrual dysfunction, elevated androgens, and early menopause. In addition, our data also suggest that hormonal birth control use in premenopausal women may protect against the development of fatty streaks, thus reducing the development of atherosclerosis and calcified plaque in the coronary arteries later in life.


   Acknowledgments
 
The study was performed at the Adult General Clinical Research Center at the University of Colorado Health Sciences Center, the Barbara Davis Center for Childhood Diabetes (Denver, CO), and Colorado Heart Imaging Center (Denver, CO).


   Footnotes
 
This work was supported by National Institutes of Health National Heart, Lung, and Blood Institute Grants R01 HL61753 and R01 HL079611, American Heart Association Predoctoral Fellowship 0510138Z, and Diabetes and Endocrinology Research Center Clinical Investigation Core P30 DK57516. The study was performed at the Adult General Clinical Research Center at the University of Colorado Health Sciences Center supported by the National Institutes of Health Grant M01 RR000051.

Disclosure Statement: J.K.S.-B., D.D., L.G.O., J.E.H., G.L.K., and M.R. have nothing to disclose. J.E. is a current shareholder and previously employed by Colorado Heart Imaging, LLC, owner of the EBCT scanner.

First Published Online March 18, 2008

Abbreviations: BC, Birth control; CAC, coronary artery calcium; CAD, coronary artery disease; EBCT, electron beam computed tomography; HDL, high-density lipoprotein; LDL, low-density lipoprotein; PCOS, polycystic ovary syndrome; T1D, type 1 diabetes.

Received September 10, 2007.

Accepted March 6, 2008.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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Endocrinology Endocrine Reviews J. Clin. End. & Metab.
Molecular Endocrinology Recent Prog. Horm. Res. All Endocrine Journals