Articles7 August 2007

Mortality Trends in Men and Women with Diabetes, 1971 to 2000

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    Abstract

    Background:

    Whether mortality rates among diabetic adults or excess mortality associated with diabetes in the United States has declined in recent decades is not known.

    Objective:

    To examine whether all-cause and cardiovascular disease mortality rates have declined among the U.S. population with and without self-reported diabetes.

    Design:

    Comparison of 3 consecutive, nationally representative cohorts.

    Setting:

    Population-based health surveys (National Health and Nutrition Examination Surveys I, II, and III) with mortality follow-up assessment.

    Patients:

    Survey participants age 35 to 74 years with and without diabetes.

    Measurements:

    Diabetes was determined by self-report for each survey (1971–1975, 1976–1980, and 1988–1994), and mortality rates were determined through 1986, 1992, and 2000 for the 3 surveys, respectively.

    Results:

    Among diabetic men, the all-cause mortality rate decreased by 18.2 annual deaths per 1000 persons (from 42.6 to 24.4 annual deaths per 1000 persons; P = 0.03) between 1971 to 1986 and 1988 to 2000, accompanying decreases in the nondiabetic population. Trends for cardiovascular disease mortality paralleled those of all-cause mortality, with 26.4 annual deaths per 1000 persons in 1971 to 1986 and 12.8 annual deaths per 1000 persons in 1988 to 2000 (P = 0.06). Among women with diabetes, however, neither all-cause nor cardiovascular disease mortality declined between 1971 to 1986 and 1988 to 2000, and the all-cause mortality rate difference between diabetic and nondiabetic women more than doubled (from a difference of 8.3 to 18.2 annual deaths per 1000 persons). The difference in all-cause mortality rates by sex among people with diabetes in 1971 to 1986 were essentially eliminated in 1988 to 2000.

    Limitations:

    Diabetes was assessed by self-report, and statistical power to examine the factors explaining mortality trends was limited.

    Conclusions:

    Progress in reducing mortality rates among persons with diabetes has been limited to men. Diabetes continues to greatly increase the risk for death, particularly among women.

    Context
    • Whether the mortality reductions observed over recent decades in the United States have been similar among diabetic and nondiabetic persons is unknown.

    Contribution
    • The 1971–2000 National Health and Nutrition Examination Surveys and vital statistics data reveal higher mortality in the diabetic population than in the nondiabetic population. Over this period, diabetic men experienced mortality reductions that paralleled those of nondiabetic men. However, mortality rates in women have not changed, and the mortality difference between diabetic and nondiabetic women more than doubled.

    Implications
    • Mortality among diabetic women does not reflect improvements in the care of diabetes and other cardiovascular risk factors. Understanding the sex differences in diabetes outcomes should be a research priority.

    —The Editors

    The decrease in cardiovascular disease (CVD) mortality rates and the accompanying increases in overall longevity are major public health successes in the United States over the past 40 years (1). These have been attributed to decreases in CVD risk factors, as well as advances in medical management and revascularization, among persons with diagnosed CVD (2, 3). Aggressive management of CVD risk factors has been shown to be particularly effective among persons with diabetes, and implementation of these findings into practice along with aggressive diabetes care should, in theory, result in increased longevity among persons with diabetes (4–9).

    The quality of diabetes care and levels of certain CVD risk factors have improved among the U.S. population with diagnosed diabetes (10, 11). Whether reductions in mortality have occurred among persons with diabetes, however, remains unclear. Although regional studies of persons with diabetes suggest that rates of all-cause mortality and cardiovascular complications have declined in recent decades (12–15), the only nationally representative study to examine trends in mortality rates of adults with diabetes found no improvement between 1971 and 1992 (16). However, no national studies of mortality trends of the U.S. diabetic population have extended through the 1990s, a period of major advances in clinical diabetes management, leaving the question of whether longevity in this population has improved (4, 11, 17).

    Thus, we assembled data from 3 consecutive nationally representative cohorts to assess whether all-cause and CVD mortality have declined among the U.S. population with diabetes and whether the disparity in mortality rates between persons with and without diabetes has decreased.

    Methods
    Study Design and Population

    The National Health and Nutrition Examination Survey (NHANES) is a series of independent, nationally representative health surveys of the U.S. noninstitutionalized population conducted from 1971 to 1975 (NHANES I), 1976 to 1980 (NHANES II), and 1988 to 1994 (NHANES III) (18–20). Each survey used a stratified, multistage probability design that sampled, interviewed, and examined participants to determine their health status. Sampling approaches, interview, and examination methods were standardized across surveys, and data were linked to death certificate data (21). To minimize bias from differential follow-up, we limited follow-up to 12.2 years, which was the maximum period for the survey with the shortest follow-up (NHANES III). Thus, the follow-up years for the 3 survey cohorts were 1971 to 1986, 1976 to 1992, and 1988 to 2000. Overall, 28 043 persons, 27 801 persons, and 39 695 persons were selected for NHANES I, II, and III, respectively, and 75% (20 749 persons), 73% (20 322 persons), and 78% (30 818 persons) were examined. We restricted our analyses to adults age 35 to 74 years who were examined at baseline. These groups included 8654 (80%), 8213 (76%), and 9399 (90%) persons from each of the 3 cohorts. After excluding persons without information on diabetes (7, 3, and 12 persons) or death (176, 5, and 6 persons), we were left with 8471, 8205, and 9381 persons in the primary analyses. Previous analyses have indicated little bias due to nonresponse (22, 23).

    Measurements

    Demographic characteristics, self-reported diabetes status, duration of disease, insulin use, and history of CVD (heart attack, heart failure, or stroke) were determined by interview. Weight and height were measured and were used to calculate body mass index (BMI). Underlying causes of death were classified according to the International Classification of Diseases, Ninth Revision, with CVD coded as 390 to 448.

    Statistical Analysis

    We completed mortality rates as the number of deaths divided by the sum of person-years and standardized by age and sex to the 2000 U.S. population. We examined changes in absolute standardized mortality rates over time by using t tests. We also used proportional hazards models to estimate the hazard rate ratios for the NHANES II and III cohorts compared with the NHANES I cohort among the diabetic and nondiabetic populations, with primary models controlling for age, sex, and race or ethnicity and additional models controlling for duration of diabetes and prevalent CVD. We also examined 2-way interactions of survey among persons with diabetes with each of the covariates mentioned above. We assessed the validity of the proportional hazards assumption by adding time-dependent variables to the model (that is, the interaction of age, sex, or race or ethnicity and the logarithm of follow-up duration). Because this assumption was not met across sex, we fit models separately by sex.

    Mortality rate estimation and proportional hazards regression incorporated survey weights such that results are representative of the U.S. noninstitutionalized population and account for the stratified, clustered design and the unequal probabilities of selection from oversampling and nonresponse (24). We combined data across the 3 surveys for regression analyses, using the original survey weights and design variables. We renumbered strata to appropriately represent their respective surveys, and we calculated degrees of freedom as the number of primary sampling units minus the number of strata. Because we used original survey weights (as opposed to constructing new weights for pooled analyses), these analyses make the assumption that each survey sample is drawn from a different population, as opposed to 3 surveys from a single underlying population (25). We conducted all statistical analyses by using SUDAAN, version 9.1 (RTI International, Research Triangle Park, North Carolina), which uses Taylor series linearization to estimate variances.

    Role of the Funding Source

    The U.S. Department of Health and Human Services is the funding source for NHANES and oversees the conduct and reporting of the NHANES surveys.

    Results

    Among both men and women with diabetes, the proportion of nonwhite persons roughly doubled across the survey years, the level of education increased substantially, and mean BMI increased (Table 1). In diabetic women—but not diabetic men—the average age at diagnosis decreased statistically significantly (mean decrease, 2.9 years) across the 3 surveys, and the average age of the diabetic population decreased by 2.5 years, from 59.1 to 56.6 years. Almost all of the secular trends in race or ethnicity, education, and BMI observed in persons with diabetes also occurred in those without diabetes.

    Table 1. Characteristics of the U.S. Population Age 35 to 74 Years with and without Diagnosed Diabetes

    Table 1.

    Between 1971 to 1986 and 1988 to 2000 in the overall nondiabetic population (both men and women), all-cause mortality rates decreased from 14.4 to 9.5 annual deaths per 1000 persons (P < 0.001) and CVD deaths decreased from 7.0 to 3.4 annual deaths per 1000 persons (P < 0.001) (Table 2). Among the overall diabetic population, the all-cause mortality rate did not statistically significantly change (30 annual deaths per 1000 persons in 1971 to 1986 vs. 25.2 annual deaths per 1000 persons in 1988 to 2000). For CVD mortality, the absolute difference in mortality among the diabetic population between 1971 to 1986 and 1988 to 2000 (18.2 vs. 11.1 annual deaths per 1000 persons) was greater than that of the nondiabetic population, but this decrease was not significant (P = 0.09).

    Table 2. Trends in Mortality Rates in the U.S. Population Age 35 to 74 Years, by Diabetes Status and Sex, 1971–2000

    Table 2.

    Findings in the overall population, however, obscured important sex-related differences, wherein mortality rates decreased among diabetic men but not among diabetic women (interaction between survey year and sex, P = 0.005 for all-cause mortality and P = 0.59 for CVD mortality) (Figure 1). All-cause mortality rates among diabetic men decreased by 43% (from 42.6 to 24.4 annual deaths per 1000 persons) between 1971 to 1986 and 1988 to 2000 (P = 0.03). In an analysis that controlled for age and race or ethnicity, the all-cause mortality rate ratio for diabetic men in 1988 to 2000 compared with 1971 to 1986 was 0.61 (95% CI, 0.43 to 0.86). Trends for the CVD mortality rate paralleled those of all-cause mortality (26.4 vs. 12.8 annual deaths per 1000 persons; P = 0.06 for difference) (Table 2 and Figure 2). In an analysis that controlled for age, sex, and race or ethnicity, the CVD mortality rate ratio for diabetic men in 1988 to 2000 compared with 1971 to 1986 was 0.62 (CI, 0.39 to 1.01) (Table 2 and Figure 2). Additional adjustment for diabetes duration, BMI, and prevalent CVD had no appreciable effect on the mortality rate ratios (data not shown).

    Figure 1. Age-adjusted all-cause mortality rates among the U.S. population age 35 to 74 years with and without diabetes, by cohort and sex.

    Mortality rates are calculated as annual deaths per 1000 persons. Error bars represent 95% CIs.

    Figure 2. Age-adjusted cardiovascular disease mortality rates among the U.S. population age 35 to 74 years with and without diabetes, by cohort and sex.

    Mortality rates are calculated as annual deaths per 1000 persons. Error bars represent 95% CIs.

    The absolute difference in all-cause mortality rates between men with and without diabetes was 23.6 annual deaths per 1000 persons (42.6 vs. 19.0 deaths) in 1971 to 1986 compared with 12.8 annual deaths per 1000 persons (24.4 vs. 11.6 deaths) in 1988 to 2000 (Figure 1). For CVD mortality, the absolute difference was 16.8 annual deaths per 1000 persons (26.4 vs. 9.6 deaths) in 1971 to 1986 compared with 8.1 annual deaths per 1000 persons (12.8 vs. 4.7 deaths) in 1988 to 2000 (Table 2 and Figure 2). Although absolute changes in mortality rates among diabetic men were at least as great as those among nondiabetic men, an 88% higher all-cause mortality rate and 153% higher CVD mortality rate in diabetic men persisted in 1988 to 2000.

    Among diabetic women, however, neither the all-cause nor CVD mortality rate decreased between 1971 to 1986 and 1988 to 2000, and the difference in all-cause mortality rate between women with and without diabetes more than doubled (from 8.3 to 18.2 annual deaths per 1000 persons; P = 0.04) (Figure 1). The hazard rate ratios for diabetic women in 1988 to 2000 compared with 1971 to 1986 were 1.31 (CI, 0.86 to 1.98) for all-cause mortality and 0.89 (CI, 0.49 to 1.59) for CVD mortality. Further adjustment for duration of diabetes, BMI, and prevalent CVD attenuated the hazard rate ratios somewhat (1.15 [CI, 0.75 to 1.75] and 0.73 [CI, 0.41 to 1.30], respectively). In 1988 to 2000, the mortality rate ratio associated with diabetes (compared with women without diabetes) was 2.84 (CI, 2.08 to 3.89) for all-cause mortality and 3.66 (CI, 2.48 to 5.42) for CVD mortality (Table 2). Finally, a comparison of NHANES I and NHANES III (Table 2) revealed that the differences in all-cause mortality rates by sex among people with diabetes in 1971 to 1986 (42.6 vs. 18.4 annual deaths per 1000 persons) were essentially eliminated in 1988 to 2000 (24.4 vs. 25.9 annual deaths per 1000 persons). This occurred to a lesser extent with CVD mortality.

    Discussion

    Our examination of U.S. adults with self-reported diabetes suggests that the well-documented reductions in mortality rates in the general U.S. adult population in the past 25 years have included men with diabetes, but their female diabetic peers have been left behind. Men with diabetes experienced a 43% relative reduction in the age-adjusted mortality rate, which is similar to that of nondiabetic men. Among women with diabetes, however, mortality rates did not decrease, and the difference in mortality rates between diabetic and nondiabetic women doubled.

    Several factors could explain the decrease among diabetic men, ranging from primary prevention of CVD risk factors to use of improved lifesaving technology among persons with CVD or diabetes complications (1–3, 26–28). Rates of smoking, lipid concentrations, and glycemic control have improved, and more patients use aspirin, have an annual lipid profile, and receive influenza vaccination (10, 11, 29). Accompanying dietary trends have favored a less atherogenic profile in the overall U.S. population (1, 26–28). Reductions in hospitalization rates for CVD, ischemic heart disease, and stroke among people with diabetes (particularly men) have also been observed (30).

    The lack of improvement among women is concerning. Some studies have documented less improvement in CVD risk factors among women and smaller increases in the use of antihypertensive therapy and aspirin (10, 31, 32). Female sex is also linked to both less aggressive medical management and worse outcomes after revascularization and hospitalization for CVD (33–38). Sex differences in the pathophysiology of coronary heart disease have been proposed, including a greater tendency for women to have microvascular coronary heart disease and left ventricular hypertrophy, differences in inflammatory and hormonal responses to risk factors, more complicated patterns of symptoms, and less accurate diagnoses of coronary heart disease (39–42). Whether these factors differentially influence mortality rates among women with diabetes is not clear. A greater decrease in age at diagnosis among women than men may also have influenced mortality rates (29, 43, 44), although adjustment for duration of diabetes in our analyses did not alter the results.

    Our findings for men are consistent with reports from regional U.S. populations (14, 15), as well as a recent report from Ontario, Canada (45). The finding among women is consistent with an earlier comparison of the 1970s and 1980s NHANES I cohorts, as well as the finding of an increased ischemic heart disease mortality rate among Native American women (44, 46). Our conclusions differ from those of the Framingham Heart Study, in which incidence and mortality rates for CVD have declined (15); of a study in North Dakota, in which mortality declined among both men and women with diabetes in the 1990s (14); and of the Ontario study over the past 10 years (45). However, those studies examined largely white populations and different periods. The Framingham Heart Study compared mortality rates from cohorts of the 1950s and 1960s, when CVD mortality rates were notably high, with cohorts of the 1980s and 1990s. The North Dakota study was limited to the 1990s.

    One limitation of our study is our reliance on self-report to identify diabetes status, because glucose was not measured in NHANES I and was limited to subsamples of the later surveys. Self-reported diabetes has high specificity and positive predictive value but has low sensitivity, because many persons with undetected hyperglycemia are classified as nondiabetic (47). Surveillance data suggest that the proportion of undiagnosed cases of diabetes has declined somewhat over recent decades, albeit not statistically significantly (48, 49). This issue is further complicated by changes in diagnostic criteria during this period. We controlled for demographic factors, BMI, and years since diagnosis to account for these factors, but we cannot rule out the possibility that increasing detection or changing diagnostic criteria led to subtle changes in the severity or type of diabetes cases over the surveys. We consider it unlikely, however, that shifts in the characteristics of diabetes would explain the sex differences in mortality trends that we observed.

    Another limitation was the relatively small samples in our sex-specific analyses. Combined with the lack of detailed information on treatments and incident medical events, this limitation precluded a thorough analysis of the factors that might have explained the trends in mortality rates. Finally, the lack of institutionalized persons means that our findings may not fully reflect the experience of people with end-stage cardiovascular and renal disease. In light of these limitations, we interpret our findings as representative of the community-dwelling population with self-reported diabetes but suggest that further study is needed to describe mortality trends in the entire diabetic population, especially in women.

    In summary, these national data reveal 3 key findings. First, reductions in mortality occurred among diabetic men but not among diabetic women. Second, disparities in mortality rates between women with and without diabetes have worsened. Finally, the female-over-male advantage in mortality rates among the diabetic population has been eliminated. These findings should stimulate more research on why the improvements in diabetes care and important risk factors are not reflected in reduced mortality for women with diabetes, as well as continued public health efforts to reduce the excess mortality risk among men and especially among women with diabetes.

    References

    • 1. Cooper RCutler JDesvigne-Nickens PFortmann SPFriedman LHavlik Ret alTrends and disparities in coronary heart disease, stroke, and other cardiovascular diseases in the United States: findings of the national conference on cardiovascular disease prevention. Circulation2000;102:3137-47. [PMID: 11120707] CrossrefMedlineGoogle Scholar
    • 2. Ergin AMuntner PSherwin RHe JSecular trends in cardiovascular disease mortality, incidence, and case fatality rates in adults in the United States. Am J Med2004;117:219-27. [PMID: 15308430] CrossrefMedlineGoogle Scholar
    • 3. Ford ESAjani UACroft JBCritchley JALabarthe DRKottke TEet alExplaining the decrease in U.S. deaths from coronary disease, 1980-2000. N Engl J Med2007;356:2388-98. [PMID: 17554120] CrossrefMedlineGoogle Scholar
    • 4. Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. UK Prospective Diabetes Study Group. BMJ1998;317:703-13. [PMID: 9732337] CrossrefMedlineGoogle Scholar
    • 5. Gaede PVedel PLarsen NJensen GVParving HHPedersen OMultifactorial intervention and cardiovascular disease in patients with type 2 diabetes. N Engl J Med2003;348:383-93. [PMID: 12556541] CrossrefMedlineGoogle Scholar
    • 6. Goldberg RBMellies MJSacks FMMoyé LAHoward BVHoward WJet alCardiovascular events and their reduction with pravastatin in diabetic and glucose-intolerant myocardial infarction survivors with average cholesterol levels: subgroup analyses in the cholesterol and recurrent events (CARE) trial. The Care Investigators. Circulation1998;98:2513-9. [PMID: 9843456] CrossrefMedlineGoogle Scholar
    • 7. Stettler CAllemann SJüni PCull CAHolman RREgger Met alGlycemic control and macrovascular disease in types 1 and 2 diabetes mellitus: Meta-analysis of randomized trials. Am Heart J2006;152:27-38. [PMID: 16824829] CrossrefMedlineGoogle Scholar
    • 8. Sustained effect of intensive treatment of type 1 diabetes mellitus on development and progression of diabetic nephropathy: the Epidemiology of Diabetes Interventions and Complications (EDIC) study. JAMA2003;290:2159-67. [PMID: 14570951] CrossrefMedlineGoogle Scholar
    • 9. Nichol KLWuorenma Jvon Sternberg TBenefits of influenza vaccination for low-, intermediate-, and high-risk senior citizens. Arch Intern Med1998;158:1769-76. [PMID: 9738606] CrossrefMedlineGoogle Scholar
    • 10. Imperatore GCadwell BLGeiss LSaadinne JBWilliams DEFord ESet alThirty-year trends in cardiovascular risk factor levels among US adults with diabetes: National Health and Nutrition Examination Surveys, 1971-2000. Am J Epidemiol2004;160:531-9. [PMID: 15353413] CrossrefMedlineGoogle Scholar
    • 11. Saaddine JBCadwell BGregg EWEngelgau MMVinicor FImperatore Get alImprovements in diabetes processes of care and intermediate outcomes: United States, 1988-2002. Ann Intern Med2006;144:465-74. [PMID: 16585660] LinkGoogle Scholar
    • 12. Pambianco GCostacou TEllis DBecker DJKlein ROrchard TJThe 30-year natural history of type 1 diabetes complications: the Pittsburgh Epidemiology of Diabetes Complications Study experience. Diabetes2006;55:1463-9. [PMID: 16644706] CrossrefMedlineGoogle Scholar
    • 13. Thomas RJPalumbo PJMelton LJRoger VLRansom JO'Brien PCet alTrends in the mortality burden associated with diabetes mellitus: a population-based study in Rochester, Minn, 1970-1994. Arch Intern Med2003;163:445-51. [PMID: 12588203] CrossrefMedlineGoogle Scholar
    • 14. Tierney EFCadwell BLEngelgau MMShireley LParsons SLMoum Ket alDeclining mortality rate among people with diabetes in North Dakota, 1997-2002. Diabetes Care2004;27:2723-5. [PMID: 15505011] CrossrefMedlineGoogle Scholar
    • 15. Fox CSCoady SSorlie PDLevy DMeigs JBD'Agostino RBet alTrends in cardiovascular complications of diabetes. JAMA2004;292:2495-9. [PMID: 15562129] CrossrefMedlineGoogle Scholar
    • 16. Gu KCowie CCHarris MIDiabetes and decline in heart disease mortality in US adults. JAMA1999;281:1291-7. [PMID: 10208144] CrossrefMedlineGoogle Scholar
    • 17. Narayan KMGregg EWFagot-Campagna AEngelgau MMVinicor FDiabetes—a common, growing, serious, costly, and potentially preventable public health problem. Diabetes Res Clin Pract2000;50 suppl 2 S77-84. [PMID: 11024588] CrossrefMedlineGoogle Scholar
    • 18. Plan and operation of the Third National Health and Nutrition Examination Survey, 1988-94. Series 1: programs and collection procedures. Vital Health Stat 11994;:1-407. [PMID: 7975354] MedlineGoogle Scholar
    • 19. Cohen BBBarbano HECox CSFeldman JJFinucane FFKleinman JCet alPlan and operation of the NHANES I Epidemiologic Followup Study: 1982-84. Vital Health Stat 11987;:1-142. [PMID: 3672939] MedlineGoogle Scholar
    • 20. McDowell AEngel AMassey JTMaurer KPlan and operation of the Second National Health and Nutrition Examination Survey, 1976-1980. Vital Health Stat 11981;:1-144. [PMID: 7344293] MedlineGoogle Scholar
    • 21. Loria CMSempos CTVuong CPlan and operation of the NHANES II Mortality Study, 1992. Vital Health Stat 11999;:1-16. [PMID: 10464470] MedlineGoogle Scholar
    • 22. Forthofer RNInvestigation of nonresponse bias in NHANES II. Am J Epidemiol1983;117:507-15. [PMID: 6837562] CrossrefMedlineGoogle Scholar
    • 23. Mohadjer LBWaksberg JNational Health and Nutrition Examination Survey III: Accounting for Nonresponse Bias. Rockville, MD: WESTAT; 1996. Google Scholar
    • 24. National Center for Health StatisticsAnalytic and Reporting Guidelines: The Third National Health and Nutrition Examination Survey, NHANES III (1988–94). Atlanta: Centers for Disease Control and Prevention; 1996. Google Scholar
    • 25. Korn ELGraubard BIAnalysis of Health Surveys. New York: Wiley; 1999:279-80. Google Scholar
    • 26. Briefel RRJohnson CLSecular trends in dietary intake in the United States. Annu Rev Nutr2004;24:401-31. [PMID: 15189126] CrossrefMedlineGoogle Scholar
    • 27. Trends in intake of energy and macronutrients—United States, 1971-2000. MMWR Morb Mortal Wkly Rep2004;53:80-2. [PMID: 14762332] MedlineGoogle Scholar
    • 28. Ernst NDSempos CTBriefel RRClark MBConsistency between US dietary fat intake and serum total cholesterol concentrations: the National Health and Nutrition Examination Surveys. Am J Clin Nutr1997;66:965S-972S. [PMID: 9322575] CrossrefMedlineGoogle Scholar
    • 29. Saydah SHFradkin JCowie CCPoor control of risk factors for vascular disease among adults with previously diagnosed diabetes. JAMA2004;291:335-42. [PMID: 14734596] CrossrefMedlineGoogle Scholar
    • 30. Geiss LEngelgau MPogach LActon KFleming BRoman Set alA national progress report on diabetes: successes and challenges. Diabetes Technol Ther2005;7:198-203. [PMID: 15738716] CrossrefMedlineGoogle Scholar
    • 31. Hajjar IKotchen TATrends in prevalence, awareness, treatment, and control of hypertension in the United States, 1988-2000. JAMA2003;290:199-206. [PMID: 12851274] CrossrefMedlineGoogle Scholar
    • 32. Persell SDBaker DWAspirin use among adults with diabetes: recent trends and emerging sex disparities. Arch Intern Med2004;164:2492-9. [PMID: 15596642] CrossrefMedlineGoogle Scholar
    • 33. Steingart RMPacker MHamm PCoglianese MEGersh BGeltman EMet alSex differences in the management of coronary artery disease. Survival and Ventricular Enlargement Investigators. N Engl J Med1991;325:226-30. [PMID: 2057023] CrossrefMedlineGoogle Scholar
    • 34. Chandra NCZiegelstein RCRogers WJTiefenbrunn AJGore JMFrench WJet alObservations of the treatment of women in the United States with myocardial infarction: a report from the National Registry of Myocardial Infarction-I. Arch Intern Med1998;158:981-8. [PMID: 9588431] CrossrefMedlineGoogle Scholar
    • 35. Flaherty JDDavidson CJDiabetes and coronary revascularization. JAMA2005;293:1501-8. [PMID: 15784875] CrossrefMedlineGoogle Scholar
    • 36. Abbott RDDonahue RPKannel WBWilson PWThe impact of diabetes on survival following myocardial infarction in men vs women. The Framingham Study. JAMA1988;260:3456-60. [PMID: 2974889] CrossrefMedlineGoogle Scholar
    • 37. Barrett-Connor EWingard DLSex differential in ischemic heart disease mortality in diabetics: a prospective population-based study. Am J Epidemiol1983;118:489-96. [PMID: 6637976] CrossrefMedlineGoogle Scholar
    • 38. Gustafsson IBrendorp BSeibaek MBurchardt HHildebrandt PKøber Let alInfluence of diabetes and diabetes-gender interaction on the risk of death in patients hospitalized with congestive heart failure. J Am Coll Cardiol2004;43:771-7. [PMID: 14998615] CrossrefMedlineGoogle Scholar
    • 39. Kanaya AMGrady DBarrett-Connor EExplaining the sex difference in coronary heart disease mortality among patients with type 2 diabetes mellitus: a meta-analysis. Arch Intern Med2002;162:1737-45. [PMID: 12153377] CrossrefMedlineGoogle Scholar
    • 40. Natarajan SLiao YCao GLipsitz SRMcGee DLSex differences in risk for coronary heart disease mortality associated with diabetes and established coronary heart disease. Arch Intern Med2003;163:1735-40. [PMID: 12885690] CrossrefMedlineGoogle Scholar
    • 41. Natarajan SLiao YSinha DCao GMcGee DLLipsitz SRSex differences in the effect of diabetes duration on coronary heart disease mortality. Arch Intern Med2005;165:430-5. [PMID: 15738373] CrossrefMedlineGoogle Scholar
    • 42. L'abbate ALarge and micro coronary vascular involvement in diabetes. Pharmacol Rep2005;57 suppl 3-9. [PMID: 16415482] MedlineGoogle Scholar
    • 43. Koopman RJMainous AGDiaz VAGeesey MEChanges in age at diagnosis of type 2 diabetes mellitus in the United States, 1988 to 2000. Ann Fam Med2005;3:60-3. [PMID: 15671192] CrossrefMedlineGoogle Scholar
    • 44. Pavkov MESievers MLKnowler WCBennett PHNelson RGAn explanation for the increase in heart disease mortality rates in diabetic Pima Indians: effect of renal replacement therapy. Diabetes Care2004;27:1132-6. [PMID: 15111533] CrossrefMedlineGoogle Scholar
    • 45. Lipscombe LLHux JETrends in diabetes prevalence, incidence, and mortality in Ontario, Canada 1995-2005: a population-based study. Lancet2007;369:750-6. [PMID: 17336651] CrossrefMedlineGoogle Scholar
    • 46. Hoehner CMWilliams DESievers MLKnowler WCBennett PHNelson RGTrends in heart disease death rates in diabetic and nondiabetic Pima Indians. J Diabetes Complications2006;20:8-13. [PMID: 16389161] CrossrefMedlineGoogle Scholar
    • 47. Saydah SHGeiss LSTierney EBenjamin SMEngelgau MBrancati FReview of the performance of methods to identify diabetes cases among vital statistics, administrative, and survey data. Ann Epidemiol2004;14:507-16. [PMID: 15301787] CrossrefMedlineGoogle Scholar
    • 48. Cowie CCRust KFByrd-Holt DDEberhardt MSFlegal KMEngelgau MMet alPrevalence of diabetes and impaired fasting glucose in adults in the U.S. population: National Health And Nutrition Examination Survey 1999-2002. Diabetes Care2006;29:1263-8. [PMID: 16732006] CrossrefMedlineGoogle Scholar
    • 49. Gregg EWCadwell BLCheng YJCowie CCWilliams DEGeiss Let alTrends in the prevalence and ratio of diagnosed to undiagnosed diabetes according to obesity levels in the U.S. Diabetes Care2004;27:2806-12. [PMID: 15562189] CrossrefMedlineGoogle Scholar

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