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Original Investigation |

Explaining the Sex Difference in Coronary Heart Disease Mortality Among Patients With Type 2 Diabetes Mellitus:  A Meta-analysis FREE

Alka M. Kanaya, MD; Deborah Grady, MD, MPH; Elizabeth Barrett-Connor, MD
[+] Author Affiliations

From the Department of Medicine, Division of General Internal Medicine (Drs Kanaya and Grady), and the Department of Epidemiology and Biostatistics (Dr Grady), University of California, San Francisco; and the Department of Family and Preventive Medicine, University of California, San Diego (Dr Barrett-Connor).


Arch Intern Med. 2002;162(15):1737-1745. doi:10.1001/archinte.162.15.1737.
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Background  Most studies suggest that diabetes is a stronger coronary heart disease (CHD) risk factor for women than men, but few have adjusted their results for classic CHD risk factors: age, hypertension, total cholesterol level, and smoking.

Objective  To establish an accurate estimate of the odds ratio for fatal and nonfatal CHD due to diabetes in both men and women.

Methods  We compared the summary odds ratio for CHD mortality and the absolute rates of CHD mortality in men and women with diabetes. We searched the MEDLINE and Cochrane Collaboration databases and bibliographies of relevant articles and consulted experts. Studies that included a nondiabetic control group and provided sex-specific adjusted results for CHD mortality, nonfatal myocardial infarction, and cardiovascular or all-cause mortality were included. Of 4578 articles identified, 232 contained primary data, and 182 were excluded. Two reviewers recorded data on study characteristics, quality, and outcomes from 50 studies.

Results  Sixteen studies met all inclusion criteria. In unadjusted and age-adjusted analyses, odds of CHD death were higher in women than men with diabetes. From 8 prospective studies, the multivariate-adjusted summary odds ratio for CHD mortality due to diabetes was 2.3 (95% confidence interval, 1.9-2.8) for men and 2.9 (95% confidence interval, 2.2-3.8) for women. There were no significant sex differences in the adjusted risk associated with diabetes for CHD mortality, nonfatal myocardial infarction, and cardiovascular or all-cause mortality. Absolute CHD death rates were higher for diabetic men than women in every age strata except the very oldest.

Conclusions  The excess relative risk of CHD mortality in women vs men with diabetes was absent after adjusting for classic CHD risk factors, but men had more CHD deaths attributable to diabetes than women.

Figures in this Article

TYPE 2 diabetes mellitus is associated with an increased risk of coronary heart disease (CHD), cerebrovascular disease, and peripheral vascular disease.1 Estimates of CHD mortality in diabetic men have varied from 1- to 3-fold the rate in nondiabetic men,211 whereas estimates in diabetic women have ranged from 2- to 5-fold the rate in nondiabetic women.3,6,9,1113 The variation in relative risk estimates of cardiovascular disease makes it difficult to evaluate the strength of diabetes as a risk factor for either sex. Two previous meta-analyses that included studies that did not adjust for major cardiac risk factors concluded that diabetes is a stronger risk factor for CHD mortality in women than men.14,15 However, it is unclear whether these reported sex differences in CHD risk are real or attributable to differences between men and women with diabetes with respect to other major risk factors for CHD.

We systematically reviewed the results from published studies and aimed to establish an accurate estimate of the odds ratio (OR) for fatal and nonfatal CHD due to diabetes in both men and women. We compared the sex-specific risk of CHD mortality, nonfatal myocardial infarction (NFMI), and cardiovascular or all-cause mortality between diabetic men and women. We also calculated absolute CHD death rates attributable to diabetes for each sex. Our main analyses included only studies that provided multivariate-adjusted comparisons to determine the independent association between diabetes and cardiovascular disease outcomes.

DATA SOURCES

We performed a computerized search using MEDLINE and the Cochrane Collaboration database for all studies published from January 1966 through February 2000 using the keywords diabetes and cardiovascular disease, myocardial infarction, or ischemic heart disease. Additional studies were identified by review of bibliographies in relevant articles and consultation with experts. We limited our search to peer-reviewed articles. English language and non–English language articles were included. In the case of multiple publications from a single study, we used the most comprehensive or recent publication.

STUDY SELECTION

Studies were included if they met all of the following criteria: (1) the study population included both men and women and the outcomes were stratified by sex; (2) a control group of nondiabetic subjects was included (studies that used historical controls or standardized mortality ratios were excluded); (3) outcomes included CHD mortality, NFMI, and cardiovascular or all-cause mortality; (4) follow-up was at least 6 months; and (5) results were adjusted at least for age, hypertension, hypercholesterolemia, and smoking. In the event that results were not adjusted for these variables, we contacted the corresponding authors to request the results of adjusted analyses. We excluded studies that primarily followed up patients with prior myocardial infarction (MI). We planned to repeat the main comparisons in subgroups defined by race or ethnicity (white, black, Latino, Japanese American, and native American) and study design (prospective cohort or cross-sectional analyses).

Diabetes was defined by self-report, use of a diabetic medication, physician documentation in medical records, or fasting or 2-hour postchallenge glucose criteria. Most studies used the 1985 World Health Organization criteria for classification of diabetes. Most studies used age as a continuous variable in their multivariate analysis, but a few categorized age by 5- or 10-year increments. Most studies dichotomized smoking into current vs never or past use, whereas only 1 study considered number of cigarettes smoked per day as a continuous variable in their model. Total cholesterol level was considered a continuous variable by most studies, but some dichotomized the variable (by ≥240 mg/dL or >6.2 mmol/L cut points), whereas one study used quartiles of total cholesterol in their final model. Hypertension was managed more heterogeneously. Some studies used a combination of elevated systolic (≥140 mm Hg, >150 mm Hg, or >160 mm Hg) and diastolic (≥90 mm Hg or >95 mm Hg) blood pressures or an antihypertensive medication to define a dichotomous hypertension variable for the multivariable analysis. Other studies used a continuous systolic blood pressure measurement or categorized systolic blood pressure by increments of 5 or 10 mm Hg or used quartiles of systolic blood pressure for their model.

In all included studies, CHD mortality was defined by the International Classification of Diseases, Ninth Revision (ICD-9) codes 410 through 414 or by physician documentation of sudden cardiac death. Nonfatal myocardial infarction was defined by definite electrocardiographic criteria using the Minnesota code, enzyme levels consistent with MI, self-report (with or without Rose questionnaire criteria), or medical record documentation. We excluded outcomes that included both fatal and nonfatal coronary events aggregated in one estimate from the analysis. Cardiovascular mortality was defined by ICD-9 codes 389 through 459.

DATA EXTRACTION AND SYNTHESIS

One author reviewed titles and abstracts of articles retrieved from the search and excluded case reports, letters, comments, reviews, and reports without primary data. Two trained data abstractors (A.M.K. and Lily Chaput, MD) reviewed the 50 remaining manuscripts to determine study eligibility. Data were extracted on study quality, participant characteristics, length of follow-up, and outcomes (CHD mortality, NFMI, and cardiovascular or all-cause mortality). Discrepancies between reviewers were resolved by consensus.

We calculated summary estimates of the adjusted ORs and 95% confidence intervals (CIs) using a random-effects model16 with a general variance–based method17 that retains adjustment for confounding. We used an Excel-based (Microsoft Inc, Redmond, Wash) meta-analysis program developed by the University of California, San Francisco, for our analyses. We examined the heterogeneity of study findings using standard χ2 analyses with a criterion for statistical significance of .10. Summary estimates for men and women were compared using the z test, with a 2-tailed level of significance of P≤.05.

QUALITY ASSESSMENT AND SENSITIVITY ANALYSIS

We also performed analyses based on study quality. A study was rated high quality if it had a prospective cohort design, used a fasting plasma glucose or oral glucose tolerance test to define diabetes, and adjusted for covariates in addition to the 4 specified for inclusion. Since the mean follow-up years from the pooled prospective cohort studies was 14 years, we also required that high-quality studies have at least 14 years of follow-up with a less than 10% loss to follow-up. Intermediate-quality studies were adjusted for age, hypertension, hypercholesterolemia, and smoking but were of shorter duration or were cross-sectional and did not use laboratory tests in defining diabetes. A third category of studies did not meet inclusion criteria for our meta-analysis because the analyses were not adjusted for age, hypertension, smoking, and total cholesterol level (termed unadjusted studies). We analyzed the available crude or age-adjusted ORs from these unadjusted studies as a part of our quality analysis. We performed a separate sensitivity analysis using age-adjusted and unadjusted estimates from our included studies that provided CHD mortality outcomes. If studies did not report unadjusted risk estimates, we used the crude rates of CHD mortality to calculate relative risk estimates and 95% CIs.

ABSOLUTE RISK

To ascertain the effect of diabetes on the absolute numbers of deaths from CHD (ICD-9 codes 410-414), we used the 1998 US Vital Statistics data for coronary death rates for each sex and all races/ethnicities stratified by age.18 We calculated the expected death rate among men and women by multiplying the observed death rate by the summary OR due to diabetes in men and women. We then calculated the excess death rate by subtracting these 2 estimates.

The MEDLINE and Cochrane Collaboration search located 4578 articles. Of the 234 articles that contained primary data, 50 were duplicative publications, 46 studies did not include a nondiabetic control group, 44 did not provide information about the outcomes of interest, and 26 did not perform analyses based on diabetes status. Another 9 did not provide data stratified by sex,1927 7 were hospital-based studies with follow-up of less than 6 months,2834 and 9 were studies of patients with prior MI.3543 Another 7 studies were excluded since their study population consisted of a single sex only.4450

Of the 36 remaining studies, 10 studies met all of our inclusion criteria.13,22,5158 Twenty-two did not publish fully adjusted risk estimates,5,6,5978 2 did not report 95% CIs or P values for their adjusted results,3,9 and 2 provided only combined outcomes of nonfatal and fatal CHD.12,79 We contacted the corresponding authors of these 26 articles twice; authors of 6 studies64,65,72,74,75,77 provided the data necessary to satisfy inclusion criteria. Some authors were unable to recreate their original analyses,5,12,73,78 some did not have the necessary variables in the data set,63,66,76 and others did not provide the requested data.3,6,9,5962,6771,79 We compared the crude summary estimates from 8 of these excluded studies that reported unadjusted risks to evaluate the effect of adjustment for age and multiple covariates on the summary ORs.61,62,66,6871,73

Thus, after receiving additional information from authors, 16 studies fulfilled all of our inclusion requirements; 12 were prospective cohort studies13,22,5158,74,77 and 4 were cross-sectional analyses64,65,72,75 (Table 1). We included the results of separate reports based on the same cohort only when the type of outcome reported was different51,57 or additional information about ethnicity was provided.55,56 For example, one publication56 from the Chicago Heart Association Detection Project in Industry provided information on women, whereas another reported data stratified by ethnicity.55 Altogether, the meta-analysis includes adjusted findings of 13 distinct study populations.

Table Graphic Jump LocationTable 1. Characteristics of Studies of Coronary Heart Disease Risk in Diabetic vs Nondiabetic Subjects

Follow-up time in the 12 prospective cohort studies ranged from 5 to 32 years (mean, approximately 14 years). Most of the studies enrolled middle-aged participants with one notable exception: the Bernalillo County study72 included subjects older than 65 years. There were 6235 diabetic participants included in the studies (48% women) and 71 306 nondiabetic control subjects (52% women).

Table 2 presents the multivariate-adjusted ORs by sex and ethnicity for CHD mortality, NFMI, cardiovascular mortality, and/or all-cause mortality for each included study. Adjusted ORs for CHD mortality due to diabetes range from 0.8 to 5.3 for men and 1.3 to 20.7 for women. Of the 8 studies that reported CHD mortality outcomes, most show a higher OR for women compared with men. Two exceptions are the National Health and Nutrition Examination Survey I54 cohort and the Reykjavik study,13 which found fairly similar odds of CHD mortality for men and women. Among the 4 studies that report NFMI outcomes, most show higher ORs for women than men except for the King County study.64,65 The data for cardiovascular and all-cause mortality are mixed, with approximately half of the studies showing a higher OR for women than men.

Table Graphic Jump LocationTable 2. Adjusted Odds Ratios (95% Confidence Intervals) for Coronary Heart Disease (CHD) Mortality, Nonfatal Myocardial Infarction (NFMI), Cardiovascular Mortality, and All-Cause Mortality by Sex

Overall, the summary OR for CHD mortality due to diabetes from 8 prospective cohort studies was 2.3 (95% CI, 1.9-2.8) for men and 2.9 (95% CI, 2.2-3.8) for women for all race/ethnic groups combined, without heterogeneity in findings (Table 3) (Figure 1 A and B).

Table Graphic Jump LocationTable 3. Summary Odds Ratios (95% Confidence Intervals) for Coronary Heart Disease Mortality by Sex (Diabetes vs No Diabetes)
Place holder to copy figure label and caption
Figure 1.

Odds ratios and 95% confidence intervals for the risk of coronary heart disease mortality for diabetic vs nondiabetic men (A) and women (B). Summary odds ratios by random-effects model are presented below individual study results.

Graphic Jump Location

Most studies that reported CHD mortality were performed with white subjects; therefore, subgroup analysis by race was limited to white participants. Summary estimates for CHD mortality for white men and women were similar to those for all ethnicities combined (men: OR, 2.2; 95% CI, 1.8-2.8; women: OR, 2.8; 95% CI, 2.1-3.7).

Although the summary ORs for CHD mortality from diabetes for women were somewhat higher than those for men overall and for every subgroup, the ORs were not statistically different. In analyses based on the unadjusted studies that were not included in the main meta-analysis, the summary OR for women was significantly higher than for men (10.4 vs 2.2; P = .02 for the comparison of ORs). Sensitivity analyses that included age-adjusted estimates for whites from the included studies found a statistically significant difference between estimates for men and women (2.1 vs 3.4; P = .05). The unadjusted risk estimates from the included studies were similar to the age-adjusted estimates (2.2 in men vs 3.2 in women), with a trend toward a statistically significant difference between the sexes. In analyses based on studies in white race and adjusted for major cardiovascular risk factors, the difference in relative risk between men and women was smaller and not statistically significant (2.2 vs 2.8; P = .20) (Figure 2).

Place holder to copy figure label and caption
Figure 2.

Summary odds ratios for each sex are presented by adjustment of study results for white race only. Unadjusted and age-adjusted summary odds ratio show a trend or significant differences by sex, whereas multiple-adjusted results (for age, hypertension, total cholesterol level, and smoking) show no difference by sex. P values are for comparison of odds ratios between men and women in each category.

Graphic Jump Location

Based on 4 population-based studies, the summary OR for NFMI due to diabetes was 1.6 (95% CI, 1.1-2.2) for men and 1.7 (95% CI, 1.3-2.3) for women, a difference that was not statistically significant (Table 4). The summary ORs for cardiovascular mortality due to diabetes were higher than for CHD mortality or NFMI for both sexes (3.2 in men vs 4.1 in women), but the difference was not statistically different (P = .49). There was also little difference between the summary ORs for all-cause mortality due to diabetes between men and women (2.1 vs 1.9). There was heterogeneity among the findings of the individual studies for these 3 outcomes that could not be easily eliminated in subgroup analyses. Only the unadjusted studies showed significantly higher summary ORs in women than men for these 3 outcomes as well (data not shown).

Table Graphic Jump LocationTable 4. Summary Odds Ratios (95% Confidence Intervals) for Nonfatal Myocardial Infarction, Cardiovascular Mortality, and All-Cause Mortality*

Despite summarizing estimates from 13 distinct study populations, we lacked power to perform subgroup analyses by race/ethnicity for cardiovascular mortality and all-cause mortality and were unable to derive meaningful summary estimates for CHD mortality in African Americans, Japanese Americans, or native Americans. We were able to derive summary estimates for NFMI for Latinos only from 2 cross-sectional analyses.72,75 Diabetes did not significantly increase risk of NFMI for Latino men (OR, 1.2; 95% CI, 0.6-2.4) or for Latina women (OR, 1.4; 95% CI, 0.9-2.1). The summary estimates for Latino men and women were lower than those for non-Latino whites (men: OR, 1.7; 95% CI, 1.1-2.6; women: OR, 2.8; 95% CI, 1.7-4.4).

Table 5 presents the death rates from coronary disease by sex and age in the US population in 199880 and uses the overall summary OR for CHD mortality (2.3 for men and 2.9 for women) to calculate the expected coronary death rate and excess death rate among diabetic men and women. Even though the summary OR for coronary death due to diabetes is slightly higher in women, the higher absolute coronary death rate in men results in higher excess deaths due to diabetes in men at all ages except for the very oldest (>85 years).

Table Graphic Jump LocationTable 5. US Death Rates per 100 000 Population From Coronary Heart Disease by Sex and Age*

Using estimates adjusted for age, hypertension, total cholesterol level, and smoking, summary ORs for CHD mortality, NFMI, and cardiovascular mortality due to diabetes were higher among women than men, but differences were modest and not statistically significant. The summary OR for CHD mortality from the 8 prospective cohort studies was 2.3 for men with diabetes and 2.9 for women with diabetes. Differences in ORs can be misleading because CHD mortality rates are higher in men than women of the same age.80 Although the odds for CHD mortality were slightly higher for women than for men with diabetes, the number of excess deaths attributable to diabetes was higher among men than women at all ages except those older than 85 years.

A previous meta-analysis14 included 25 prospective, population-based studies that provided crude data to examine sex differences in relative risk of CHD mortality and MI associated with type 2 diabetes mellitus. The risk of fatal CHD was increased for diabetic women, suggesting women's natural protection from CHD is reduced in the presence of diabetes. However, many of the large cohort studies included in this meta-analysis did not control for the main established risk factors for coronary disease. A more recent meta-analysis15 that included 10 studies found that women with diabetes were at significantly higher risk of CHD mortality compared with men (2.58 vs 1.85, P = .04). This meta-analysis included studies that adjusted only for age, reported combined end points for CHD mortality and NFMI, and followed up subjects with prior CHD. In a subgroup analysis excluding studies of patients with existing CHD, there was no significant difference between summary ORs for diabetic men and women for CHD mortality (1.9 in men vs 2.4 in women, P = .18). These results are consistent with our findings.

The difference in relative risk for CHD mortality between men and women was progressively attenuated with adjustment for age and other major cardiovascular risk factors. Possible explanations for this phenomenon may be that diabetic women compared with nondiabetic women may have a more severe degree of risk factor abnormalities than diabetic men compared with nondiabetic men81 or the unfavorable cardiac risk factors may have a bigger impact on women than men. Other explanations could be that risk factors in women are managed less aggressively than in men82,83 or that women are more likely to have more than one risk factor.81 Adjustment for other cardiovascular risk factors that were not included in most of the studies in our analysis (high-density lipoprotein cholesterol, triglyceride levels, exercise, body mass index) or more specific adjustment using continuous measures of risk rather than risk categories might eliminate the remaining disparity between men and women. These data suggest that most of the observed difference in risk between men and women for CHD mortality from diabetes is mediated by traditional cardiac risk factors that are modifiable.

Four large, widely quoted prospective cohort studies5,9,12,79 did not meet criteria for inclusion in our meta-analysis. These 4 studies had conflicting results; 1 showed a higher diabetes-associated relative risk for CHD mortality in men compared with women,79 1 showed an increased relative risk among women,5 and the 2 remaining studies found no difference between the sexes.9,12 It is unlikely that the addition of the results of these 4 studies would have changed our summary estimates significantly.

It is now recommended that cardiovascular risk factors be treated as aggressively in diabetic patients without a history of CHD as in nondiabetic patients with a prior MI.84,85 Based on the present meta-analysis, diabetes independently increases the risk of fatal CHD in both men and women without preexisting CHD by 2- to 3-fold. Since dyslipidemia and hypertension often cluster with type 2 diabetes mellitus and there is an additive effect for each of these risk factors,49 diabetic patients are at high risk of CHD death and should be treated more aggressively than persons at low risk. The larger effect of adjusting for major risk factors in women vs men suggests that women with diabetes might benefit more from blood pressure and cholesterol-lowering treatment than diabetic men.

As with any meta-analysis, we are limited to the variables measured and end points reported in each study. We insisted that the outcomes be adjusted for major risk factors to study the association between diabetes and CHD, but these variables were defined differently in the studies. For example, some studies used categorical levels of elevated systolic blood pressure as evidence of hypertension, whereas others included the use of an antihypertensive medication as evidence. Likewise, there were differences in definition of outcomes among studies. Most studies used predefined electrocardiographic criteria to determine MI, but some used history of revascularization by coronary artery bypass surgery or angioplasty or patient history of MI for this outcome. Some studies differentiated patients with impaired glucose tolerance from those with frank diabetes, whereas others included the impaired glucose tolerance group with nondiabetic subjects. Most studies did not completely distinguish participants with type 1 diabetes mellitus from those with type 2. However, most of these errors of misclassification would be expected to occur similarly for men and women and should not explain the lack of sex difference in relative risk. Because most patients with type 2 diabetes mellitus have their conditions diagnosed years after disease onset, length of follow-up in cohort studies was used as a rough proxy for duration of diabetes. We found no significant sex difference for any outcome among the adjusted prospective studies with 14 or more years of follow-up. Lastly, we were unable to analyze results based on race/ethnicity for most of the outcomes owing to lack of studies meeting our inclusion criteria in nonwhite populations.

The advantage of the present meta-analysis is that it is restricted to the findings of studies controlled for age, hypertension, hypercholesterolemia, and smoking. The most accurate adjusted summary OR for CHD mortality due to diabetes for all race/ethnic groups combined is 2.3 for men and 2.9 for women. The difference in risk between the men and women is modest and not statistically significant. Most reports of a greatly elevated relative risk in women with diabetes did not control for major CHD risk factors. The present meta-analysis offers further evidence that much of the previously reported excess risk of coronary outcomes in diabetic women is mediated by well-established modifiable cardiac risk factors. Future prospective studies should present sex-specific fatal and nonfatal cardiovascular disease end points before and after adjustment for risk factors. Analyzing the effect of specific risk factors separately and in combination will help to clarify their role in the cardiovascular protection observed in women without diabetes. In addition, much remains to be learned about cardiovascular outcomes among ethnic minority groups with diabetes.

Accepted for publication November 19, 2001.

This study was supported in part by a grant from the Department of Health and Human Services (Dr Kanaya) (Faculty Development in General Internal Medicine 1D08PE50109-01).

We thank the following authors, assistants, and statisticians for their help in providing us with additional data from their studies: Leo Niskanen, MD, Wilfred Fujimoto, MD, Jane Shofer, MS, Edward J. Boyko, MD, MPH, Donna L. Leonetti, PhD, Marion Rewers, MD, Susan Shetterly, MS, Richard Hamman, MD, DrPH, William deGrauw, MD, Hans Bor, BS, Robert Lindeman, MD, C. Lillian Yau, MS, Maurice Sievers, MD, Robert Nelson, MD, PhD, Desmond Williams, MD, and Christine Hoehner, MPH. We are indebted to Lily Chaput, MD, for data abstraction and review and Eric Vittinghoff, PhD, for statistical expertise.

Corresponding author and reprints: Alka M. Kanaya, MD, 1701 Divisadero St, Suite 554, San Francisco, CA 94143-1732 (e-mail: alkak@itsa.ucsf.edu).

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Orlander  PRGoff  DCMorrissey  M  et al.  The relation of diabetes to the severity of acute myocardial infarction and post-myocardial infarction survival in Mexican-Americans and non-Hispanic whites: the Corpus Christi Heart Project. Diabetes. 1994;43897- 902
Rytter  LTroelsen  SBeck-Nielsen  H Prevalence and mortality of acute myocardial infarction in patients with diabetes. Diabetes Care. 1985;8230- 234
Zuanetti  GLatini  RMaggioni  APSantoro  LFranzosi  MG Influence of diabetes on mortality in acute myocardial infarction: data from the GISSI-2 Study. J Am Coll Cardiol. 1993;221788- 1794
Adlerberth  AMRosengren  AWilhelmsen  L Diabetes and long-term risk of mortality from coronary and other causes in middle-aged Swedish men: a general population study. Diabetes Care. 1998;21539- 545
Balkau  BEschwege  EPapoz  L  et al.  Risk factors for early death in non-insulin dependent diabetes and men with known glucose tolerance status. BMJ. 1993;307295- 299
Lapidus  L Ischaemic heart disease, stroke and total mortality in women: results from a prospective population study in Gothenburg, Sweden. Acta Med Scand Suppl. 1985;7051- 42
Manson  JEColditz  GAStampfer  MJ  et al.  A prospective study of maturity-onset diabetes mellitus and risk of coronary heart disease and stroke in women. Arch Intern Med. 1991;1511141- 1147
Rodriguez  BLLau  NBurchfiel  CM  et al.  Glucose intolerance and 23-year risk of coronary heart disease and total mortality: the Honolulu Heart Program. Diabetes Care. 1999;221262- 1265
Stamler  JVaccaro  ONeaton  JDWentworth  D Diabetes, other risk factors, and 12-year cardiovascular mortality for men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care. 1993;16434- 444
Stengard  JHTuomilehto  JPekkanen  J  et al.  Diabetes mellitus, impaired glucose tolerance and mortality among elderly men: the Finnish cohorts of the Seven Countries Study. Diabetologia. 1992;35760- 765
Barrett-Connor  ELCohn  BAWingard  DLEdelstein  SL Why is diabetes mellitus a stronger risk factor for fatal ischemic heart disease in women than in men? the Rancho Bernardo Study. JAMA. 1991;265627- 631[published erratum appears in JAMA. 1991;265:3249]
Collins  VRDowse  GKRam  PCabealawa  SZimmet  PZ Non-insulin-dependent diabetes and 11-year mortality in Asian Indian and Melanesian Fijians. Diabet Med. 1996;13125- 132
Keil  JESutherland  SEKnapp  RGLackland  DTGazes  PCTyroler  HA Mortality rates and risk factors for coronary disease in black as compared with white men and women. N Engl J Med. 1993;32973- 78
Kleinman  JCDonahue  RPHarris  MIFinucane  FFMadans  JHBrock  DB Mortality among diabetics in a national sample. Am J Epidemiol. 1988;128389- 401
Lowe  LPLiu  KGreenland  PMetzger  BEDyer  ARStamler  J Diabetes, asymptomatic hyperglycemia, and 22-year mortality in black and white men: the Chicago Heart Association Detection Project in Industry Study. Diabetes Care. 1997;20163- 169
Pan  WHCedres  LBLiu  K  et al.  Relationship of clinical diabetes and asymptomatic hyperglycemia to risk of coronary heart disease mortality in men and women. Am J Epidemiol. 1986;123504- 516
Scheidt-Nave  CBarrett-Connor  EWingard  DL Resting electrocardiographic abnormalities suggestive of asymptomatic ischemic heart disease associated with non–insulin-dependent diabetes mellitus in a defined population. Circulation. 1990;81899- 906
Wei  MGaskill  SPHaffner  SMStern  MP Effects of diabetes and level of glycemia on all-cause and cardiovascular mortality: the San Antonio Heart Study. Diabetes Care. 1998;211167- 1172
Cruz-Vidal  MGarcia-Palmieri  MRCostas  R  JrSorlie  PDHavlik  RJ Abnormal blood glucose and coronary heart disease: the Puerto Rico Heart Health Program. Diabetes Care. 1983;6556- 561
DeStefano  FFord  ESNewman  J  et al.  Risk factors for coronary heart disease mortality among persons with diabetes. Ann Epidemiol. 1993;327- 34
Feskens  EJKromhout  D Glucose tolerance and the risk of cardiovascular disease: the Zutphen Study. J Clin Epidemiol. 1992;451327- 1334
Fitzgerald  APJarrett  RJ Are conventional risk factors for mortality relevant in type 2 diabetes? Diabet Med. 1991;8475- 480
Fraser  GEStrahan  TMSabate  JBeeson  WLKissinger  D Effects of traditional coronary risk factors on rates of incident coronary events in a low-risk population: the Adventist Health Study. Circulation. 1992;86406- 413
Fujimoto  WYLeonetti  DLKinyoun  JLShuman  WPStolov  WCWahl  PW Prevalence of complications among second-generation Japanese-American men with diabetes, impaired glucose tolerance, or normal glucose tolerance. Diabetes. 1987;36730- 739
Fujimoto  WYLeonetti  DLBergstrom  RWKinyoun  JLStolov  WCWahl  PW Glucose intolerance and diabetic complications among Japanese-American women. Diabetes Res Clin Pract. 1991;13119- 129
de Grauw  WJvan den Hoogen  HJvan de Lisdonk  EHvan Gerwen  WHvan Weel  C Control group characteristics and study outcomes: empirical data from a study on mortality of patients with type 2 diabetes mellitus in Dutch general practice. J Epidemiol Community Health. 1998;52 (suppl 1) 9S- 12S
Howard  BVLee  ETCowan  LD  et al.  Coronary heart disease prevalence and its relation to risk factors in American Indians: the Strong Heart Study. Am J Epidemiol. 1995;142254- 268
Hoy  WLight  AMegill  D Cardiovascular disease in Navajo Indians with type 2 diabetes. Public Health Rep. 1995;11087- 94
Laakso  MRonnemaa  TPyorala  KKallio  VPuukka  PPenttila  I Atherosclerotic vascular disease and its risk factors in non–insulin-dependent diabetic and nondiabetic subjects in Finland. Diabetes Care. 1988;11449- 463
Laakso  MRonnemaa  TLehto  SPuukka  PKallio  VPyorala  K Does NIDDM increase the risk for coronary heart disease similarly in both low- and high-risk populations? Diabetologia. 1995;38487- 493
Kuusisto  JMykkanen  LPyorala  KLaakso  M NIDDM and its metabolic control predict coronary heart disease in elderly subjects. Diabetes. 1994;43960- 967
Lindeman  RDRomero  LJHundley  R  et al.  Prevalences of type 2 diabetes, the insulin resistance syndrome, and coronary heart disease in an elderly, biethnic population. Diabetes Care. 1998;21959- 966
Mitchell  BDHazuda  HPHaffner  SMPatterson  JKStern  MP Myocardial infarction in Mexican-Americans and non-Hispanic whites: the San Antonio Heart Study. Circulation. 1991;8345- 51
Niskanen  LTurpeinen  APenttila  IUusitupa  MI Hyperglycemia and compositional lipoprotein abnormalities as predictors of cardiovascular mortality in type 2 diabetes: a 15-year follow-up from the time of diagnosis. Diabetes Care. 1998;211861- 1869
Rewers  MShetterly  SMBaxter  JMarshall  JAHamman  RF Prevalence of coronary heart disease in subjects with normal and impaired glucose tolerance and non–insulin-dependent diabetes mellitus in a biethnic Colorado population: the San Luis Valley Diabetes Study. Am J Epidemiol. 1992;1351321- 1330
Seeman  TMendes de Leon  CBerkman  LOstfeld  A Risk factors for coronary heart disease among older men and women: a prospective study of community-dwelling elderly. Am J Epidemiol. 1993;1381037- 1049
Sievers  MLNelson  RGKnowler  WCBennett  PH Impact of NIDDM on mortality and causes of death in Pima Indians. Diabetes Care. 1992;151541- 1549
Simons  LAMcCallum  JFriedlander  YSimons  J Diabetes, mortality and coronary heart disease in the prospective Dubbo study of Australian elderly. Aust N Z J Med. 1996;2666- 74
Kannel  WBWilson  PW Risk factors that attenuate the female coronary disease advantage. Arch Intern Med. 1995;15557- 61
National Center for Health Statistics Web site, Death Rates for 72 Selected Causes, by 10-Year Age Groups, Race, and Sex: United States, 1979-98.  Atlanta, Ga Centers for Disease Control and Prevention2000;421- 432Available at: http://www.cdc.gov/nchs/data/statab/gm290-98.pdf. Accessed May 10, 2002.
Goldschmid  MGBarrett-Connor  EEdelstein  SLWingard  DLCohn  BAHerman  WH Dyslipidemia and ischemic heart disease mortality among men and women with diabetes. Circulation. 1994;89991- 997
Chandra  NCZiegelstein  RCRogers  WJ  et al.  Observations of the treatment of women in the United States with myocardial infarction: a report from the National Registry of Myocardial Infarction-I. Arch Intern Med. 1998;158981- 988
Steingart  RMPacker  MHamm  P  et al. for the Survival and Ventricular Enlargement Investigators, Sex differences in the management of coronary artery disease. N Engl J Med. 1991;325226- 230
Not Available, Standards of medical care for patients with diabetes mellitus. Diabetes Care. 2001;24 (suppl 1) S33- S43
Not Available, Executive summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA. 2001;2852486- 2497

Figures

Place holder to copy figure label and caption
Figure 1.

Odds ratios and 95% confidence intervals for the risk of coronary heart disease mortality for diabetic vs nondiabetic men (A) and women (B). Summary odds ratios by random-effects model are presented below individual study results.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Summary odds ratios for each sex are presented by adjustment of study results for white race only. Unadjusted and age-adjusted summary odds ratio show a trend or significant differences by sex, whereas multiple-adjusted results (for age, hypertension, total cholesterol level, and smoking) show no difference by sex. P values are for comparison of odds ratios between men and women in each category.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Characteristics of Studies of Coronary Heart Disease Risk in Diabetic vs Nondiabetic Subjects
Table Graphic Jump LocationTable 2. Adjusted Odds Ratios (95% Confidence Intervals) for Coronary Heart Disease (CHD) Mortality, Nonfatal Myocardial Infarction (NFMI), Cardiovascular Mortality, and All-Cause Mortality by Sex
Table Graphic Jump LocationTable 3. Summary Odds Ratios (95% Confidence Intervals) for Coronary Heart Disease Mortality by Sex (Diabetes vs No Diabetes)
Table Graphic Jump LocationTable 4. Summary Odds Ratios (95% Confidence Intervals) for Nonfatal Myocardial Infarction, Cardiovascular Mortality, and All-Cause Mortality*
Table Graphic Jump LocationTable 5. US Death Rates per 100 000 Population From Coronary Heart Disease by Sex and Age*

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Lomuscio  ACastagnone  MVergani  D  et al.  Clinical correlation between diabetic and nondiabetic patients with myocardial infarction. Acta Cardiol. 1991;46543- 554
Seyoum  BAbdulkadir  JBerhanu  PFeleke  FWorku  YAyana  G Profile of coronary artery risk factors in Ethiopian diabetic patients. East Afr Med J. 1999;76105- 107
Singer  DEMoulton  AWNathan  DM Diabetic myocardial infarction: interaction of diabetes with other preinfarction risk factors. Diabetes. 1989;38350- 357
Tansey  MJOpie  LHKennelly  BM High mortality in obese women diabetics with acute myocardial infarction. BMJ. 1977;11624- 1626
Abbott  RDDonahue  RPKannel  WBWilson  PW The impact of diabetes on survival following myocardial infarction in men vs women: the Framingham Study. JAMA. 1988;2603456- 3460[published erratum appears in JAMA. 1989;261:1884]
Abbud  ZAShindler  DMWilson  ACKostis  JBfor the Myocardial Infarction Data Acquisition System Study Group, Effect of diabetes mellitus on short- and long-term mortality rates of patients with acute myocardial infarction: a statewide study. Am Heart J. 1995;13051- 58
Behar  SBoyko  VReicher-Reiss  HGoldbourt  Ufor the SPRINT Study Group, Ten-year survival after acute myocardial infarction: comparison of patients with and without diabetes. Am Heart J. 1997;133290- 296
Donahue  RPGoldberg  RJChen  ZGore  JMAlpert  JS The influence of sex and diabetes mellitus on survival following acute myocardial infarction: a community-wide perspective. J Clin Epidemiol. 1993;46245- 252
Liao  YCooper  RSGhali  JKLansky  DCao  GLee  J Sex differences in the impact of coexistent diabetes on survival in patients with coronary heart disease. Diabetes Care. 1993;16708- 713
Miettinen  HLehto  SSalomaa  V  et al. for The FINMONICA Myocardial Infarction Register Study Group, Impact of diabetes on mortality after the first myocardial infarction. Diabetes Care. 1998;2169- 75
Orlander  PRGoff  DCMorrissey  M  et al.  The relation of diabetes to the severity of acute myocardial infarction and post-myocardial infarction survival in Mexican-Americans and non-Hispanic whites: the Corpus Christi Heart Project. Diabetes. 1994;43897- 902
Rytter  LTroelsen  SBeck-Nielsen  H Prevalence and mortality of acute myocardial infarction in patients with diabetes. Diabetes Care. 1985;8230- 234
Zuanetti  GLatini  RMaggioni  APSantoro  LFranzosi  MG Influence of diabetes on mortality in acute myocardial infarction: data from the GISSI-2 Study. J Am Coll Cardiol. 1993;221788- 1794
Adlerberth  AMRosengren  AWilhelmsen  L Diabetes and long-term risk of mortality from coronary and other causes in middle-aged Swedish men: a general population study. Diabetes Care. 1998;21539- 545
Balkau  BEschwege  EPapoz  L  et al.  Risk factors for early death in non-insulin dependent diabetes and men with known glucose tolerance status. BMJ. 1993;307295- 299
Lapidus  L Ischaemic heart disease, stroke and total mortality in women: results from a prospective population study in Gothenburg, Sweden. Acta Med Scand Suppl. 1985;7051- 42
Manson  JEColditz  GAStampfer  MJ  et al.  A prospective study of maturity-onset diabetes mellitus and risk of coronary heart disease and stroke in women. Arch Intern Med. 1991;1511141- 1147
Rodriguez  BLLau  NBurchfiel  CM  et al.  Glucose intolerance and 23-year risk of coronary heart disease and total mortality: the Honolulu Heart Program. Diabetes Care. 1999;221262- 1265
Stamler  JVaccaro  ONeaton  JDWentworth  D Diabetes, other risk factors, and 12-year cardiovascular mortality for men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care. 1993;16434- 444
Stengard  JHTuomilehto  JPekkanen  J  et al.  Diabetes mellitus, impaired glucose tolerance and mortality among elderly men: the Finnish cohorts of the Seven Countries Study. Diabetologia. 1992;35760- 765
Barrett-Connor  ELCohn  BAWingard  DLEdelstein  SL Why is diabetes mellitus a stronger risk factor for fatal ischemic heart disease in women than in men? the Rancho Bernardo Study. JAMA. 1991;265627- 631[published erratum appears in JAMA. 1991;265:3249]
Collins  VRDowse  GKRam  PCabealawa  SZimmet  PZ Non-insulin-dependent diabetes and 11-year mortality in Asian Indian and Melanesian Fijians. Diabet Med. 1996;13125- 132
Keil  JESutherland  SEKnapp  RGLackland  DTGazes  PCTyroler  HA Mortality rates and risk factors for coronary disease in black as compared with white men and women. N Engl J Med. 1993;32973- 78
Kleinman  JCDonahue  RPHarris  MIFinucane  FFMadans  JHBrock  DB Mortality among diabetics in a national sample. Am J Epidemiol. 1988;128389- 401
Lowe  LPLiu  KGreenland  PMetzger  BEDyer  ARStamler  J Diabetes, asymptomatic hyperglycemia, and 22-year mortality in black and white men: the Chicago Heart Association Detection Project in Industry Study. Diabetes Care. 1997;20163- 169
Pan  WHCedres  LBLiu  K  et al.  Relationship of clinical diabetes and asymptomatic hyperglycemia to risk of coronary heart disease mortality in men and women. Am J Epidemiol. 1986;123504- 516
Scheidt-Nave  CBarrett-Connor  EWingard  DL Resting electrocardiographic abnormalities suggestive of asymptomatic ischemic heart disease associated with non–insulin-dependent diabetes mellitus in a defined population. Circulation. 1990;81899- 906
Wei  MGaskill  SPHaffner  SMStern  MP Effects of diabetes and level of glycemia on all-cause and cardiovascular mortality: the San Antonio Heart Study. Diabetes Care. 1998;211167- 1172
Cruz-Vidal  MGarcia-Palmieri  MRCostas  R  JrSorlie  PDHavlik  RJ Abnormal blood glucose and coronary heart disease: the Puerto Rico Heart Health Program. Diabetes Care. 1983;6556- 561
DeStefano  FFord  ESNewman  J  et al.  Risk factors for coronary heart disease mortality among persons with diabetes. Ann Epidemiol. 1993;327- 34
Feskens  EJKromhout  D Glucose tolerance and the risk of cardiovascular disease: the Zutphen Study. J Clin Epidemiol. 1992;451327- 1334
Fitzgerald  APJarrett  RJ Are conventional risk factors for mortality relevant in type 2 diabetes? Diabet Med. 1991;8475- 480
Fraser  GEStrahan  TMSabate  JBeeson  WLKissinger  D Effects of traditional coronary risk factors on rates of incident coronary events in a low-risk population: the Adventist Health Study. Circulation. 1992;86406- 413
Fujimoto  WYLeonetti  DLKinyoun  JLShuman  WPStolov  WCWahl  PW Prevalence of complications among second-generation Japanese-American men with diabetes, impaired glucose tolerance, or normal glucose tolerance. Diabetes. 1987;36730- 739
Fujimoto  WYLeonetti  DLBergstrom  RWKinyoun  JLStolov  WCWahl  PW Glucose intolerance and diabetic complications among Japanese-American women. Diabetes Res Clin Pract. 1991;13119- 129
de Grauw  WJvan den Hoogen  HJvan de Lisdonk  EHvan Gerwen  WHvan Weel  C Control group characteristics and study outcomes: empirical data from a study on mortality of patients with type 2 diabetes mellitus in Dutch general practice. J Epidemiol Community Health. 1998;52 (suppl 1) 9S- 12S
Howard  BVLee  ETCowan  LD  et al.  Coronary heart disease prevalence and its relation to risk factors in American Indians: the Strong Heart Study. Am J Epidemiol. 1995;142254- 268
Hoy  WLight  AMegill  D Cardiovascular disease in Navajo Indians with type 2 diabetes. Public Health Rep. 1995;11087- 94
Laakso  MRonnemaa  TPyorala  KKallio  VPuukka  PPenttila  I Atherosclerotic vascular disease and its risk factors in non–insulin-dependent diabetic and nondiabetic subjects in Finland. Diabetes Care. 1988;11449- 463
Laakso  MRonnemaa  TLehto  SPuukka  PKallio  VPyorala  K Does NIDDM increase the risk for coronary heart disease similarly in both low- and high-risk populations? Diabetologia. 1995;38487- 493
Kuusisto  JMykkanen  LPyorala  KLaakso  M NIDDM and its metabolic control predict coronary heart disease in elderly subjects. Diabetes. 1994;43960- 967
Lindeman  RDRomero  LJHundley  R  et al.  Prevalences of type 2 diabetes, the insulin resistance syndrome, and coronary heart disease in an elderly, biethnic population. Diabetes Care. 1998;21959- 966
Mitchell  BDHazuda  HPHaffner  SMPatterson  JKStern  MP Myocardial infarction in Mexican-Americans and non-Hispanic whites: the San Antonio Heart Study. Circulation. 1991;8345- 51
Niskanen  LTurpeinen  APenttila  IUusitupa  MI Hyperglycemia and compositional lipoprotein abnormalities as predictors of cardiovascular mortality in type 2 diabetes: a 15-year follow-up from the time of diagnosis. Diabetes Care. 1998;211861- 1869
Rewers  MShetterly  SMBaxter  JMarshall  JAHamman  RF Prevalence of coronary heart disease in subjects with normal and impaired glucose tolerance and non–insulin-dependent diabetes mellitus in a biethnic Colorado population: the San Luis Valley Diabetes Study. Am J Epidemiol. 1992;1351321- 1330
Seeman  TMendes de Leon  CBerkman  LOstfeld  A Risk factors for coronary heart disease among older men and women: a prospective study of community-dwelling elderly. Am J Epidemiol. 1993;1381037- 1049
Sievers  MLNelson  RGKnowler  WCBennett  PH Impact of NIDDM on mortality and causes of death in Pima Indians. Diabetes Care. 1992;151541- 1549
Simons  LAMcCallum  JFriedlander  YSimons  J Diabetes, mortality and coronary heart disease in the prospective Dubbo study of Australian elderly. Aust N Z J Med. 1996;2666- 74
Kannel  WBWilson  PW Risk factors that attenuate the female coronary disease advantage. Arch Intern Med. 1995;15557- 61
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