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Diabetes and All-Cause and Coronary Heart Disease Mortality Among US Male Physicians
Paulo A. Lotufo, MD, DrPH;
J. Michael Gaziano, MD, MPH;
Claudia U. Chae, MD, MPH;
Umed A. Ajani, MBBS, MPH;
Gina Moreno-John, MD, MPH;
Julie E. Buring, ScD;
JoAnn E. Manson, MD, DrPH
Arch Intern Med. 2001;161:242-247.
ABSTRACT
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Background While diabetes has long been associated with increased risk of coronary
heart disease (CHD), the magnitude of risk of diabetes-related CHD is uncertain.
Objective To evaluate the impact of diabetes and prior CHD on all-cause and CHD
mortality.
Methods In a prospective cohort study of 91 285 US male physicians aged
40 to 84 years, participants were divided into 4 groups: (1) a reference group
of 82 247 men free of both diabetes and CHD (previous myocardial infarction
and/or angina) at baseline, (2) 2317 men with a history of diabetes but not
CHD, (3) 5906 men with a history of CHD but not diabetes, and (4) 815 men
with a history of both diabetes and CHD. Rates of all-cause and CHD mortality
were compared in these groups.
Results Over 5 years (49 7952 person-years of follow-up), 3627 deaths from all
causes were documented, including 1242 deaths from CHD. Compared with men
with no diabetes or CHD, the age-adjusted relative risk of death from any
cause was 2.3 (95% confidence interval [CI], 2.0-2.6) among men with diabetes
and without CHD, 2.2 (95% CI, 2.0-2.4) among men with CHD and without diabetes,
and 4.7 (95% CI, 4.0-5.4) among men with both diabetes and CHD. The relative
risk of CHD death was 3.3 (95% CI, 2.6-4.1) among men with diabetes and without
CHD, 5.6 (95% CI, 4.9-6.3) among men with CHD and without diabetes, and 12.0
(95% CI, 9.9-14.6) among men with both diabetes and CHD. Multivariate adjustment
for body mass index, smoking status, alcohol intake, and physical activity
as well as stratification by these variables did not materially alter these
associations.
Conclusions These prospective data indicate that diabetes is associated with a substantial
increase in all-cause and CHD mortality. For all-cause mortality, the magnitude
of excess risk conferred by diabetes is similar to that conferred by a history
of CHD; for mortality from CHD, a history of CHD is a more potent predictor
of death. The presence of both diabetes and CHD, however, identifies a particularly
high-risk group.
INTRODUCTION
DIABETES MELLITUS has long been linked with an excess risk of coronary
heart disease (CHD).1 Several epidemiologic
studies indicate that men with diabetes mellitus are 2 to 3 times more likely
to die from CHD than those without diabetes,2, 3, 4, 5
and women with diabetes face an even higher risk.6, 7
Diabetes increases the case-fatality rate of myocardial infarction (MI) events,8, 9, 10 and prehospital mortality
from acute coronary events is higher among people with diabetes.11
Patients with diabetes experienced a smaller decline in heart disease mortality
in the period between 1982 and 1984 vs the period between 1971 and 1975 compared
with nondiabetic individuals in the same periods.12
The magnitude of diabetes-related CHD risk and whether it rivals the excess
risk associated with prior MI, however, are matters of some controversy. The
National Cholesterol Education Program recommends more aggressive lipid-lowering
therapy for people with a history of MI than for those without known CHD but
with risk factors such as diabetes.13 However,
a recent analysis of middle-aged Finnish men and women found that subjects
who had diabetes but were free of cardiovascular disease had the same level
of risk of CHD mortality as those subjects with a history of MI but without
diabetes.14
The US Physicians' Health Study (PHS) enrollment cohort provided a unique
opportunity to address the relationships of diabetes and a history of CHD
to all-cause and CHD mortality. In this large, prospective cohort of 91 285
US men aged 40 to 84 years at baseline, we compared the risk of CHD mortality
and all-cause mortality among 4 subsets of participants: (1) men who were
free of diabetes and CHD (past MI and/or angina pectoris) at baseline, (2)
men diagnosed with diabetes but not CHD, (3) men diagnosed with CHD but not
diabetes, and (4) men diagnosed with both diabetes and CHD.
METHODS
STUDY POPULATION
The PHS was a randomized, double-blind, placebo-controlled trial testing
the benefits and risks of aspirin and beta carotene in the prevention of cardiovascular
disease and cancer.15, 16 Beginning
in 1982, letters of invitation, informed consent forms, and baseline questionnaires
were sent to 261 248 male physicians. By December 31, 1983, 104 388
physicians had answered the baseline enrollment questionnaire. Men with a
history of cancer, stroke, liver disease, or renal disease were excluded because
their preexisting conditions might have increased the likelihood of detecting
diabetes and CHD, leaving a total of 91 285 participants. Our analysis
includes a reference group of 82 247 men without a history of either
diabetes or CHD; 2317 men who, at baseline, reported a history of diabetes
but not CHD; 5906 men who reported a history of CHD (previous MI and/or angina
pectoris) but not diabetes; and 815 men who reported a diagnosis of both diabetes
and CHD. A subset of this cohort (approximately 25%) was subsequently randomized
into the trial.
DATA COLLECTION
On the baseline questionnaire, respondents were asked to report their
ages and previously diagnosed medical conditions, including history of MI,
angina pectoris, and diabetes mellitus. They were also asked to record data
on coronary risk factors, including systolic and diastolic blood pressure,
history of drug treatment for hypertension, cholesterol level, history of
drug treatment for high cholesterol, cigarette smoking (never, past, or current,
and number of cigarettes smoked daily for current smokers), frequency of vigorous
exercise (rarely/never, 1-3 times per month, 1-4 times per week, or 5 or more
times per week), and frequency of alcohol intake (never, rarely, monthly,
weekly, or daily). Body mass index was calculated from self-reported weight
and height.
Information was not collected about type and duration of diabetes. Based
on the age distribution of the participants, it is likely that the majority
had type 2 diabetes.
VALIDATION OF EXPOSURES AND OUTCOMES
Self-reports of the presence or absence of diabetes and/or CHD at baseline
among the enrollees in the PHS were not validated by medical record review.
However, during the randomized phase of the PHS, 95% of reports of postrandomization
angina and/or coronary revascularization were confirmed by a review of medical
records in a sample of 100 randomly selected participants who reported this
diagnosis,17 and previous studies of health
professionals show the reporting of diabetes and CHD to be reliable.18
Deaths were identified through systematic searches of the National Death
Index for the entire enrollment cohort, and death certificates were obtained
from state agencies for all deaths that occurred before February 1, 1988.
The deaths were classified by trained nosologists according to the International Classification of Diseases, Ninth Revision (ICD-9). The "Automated Classification of Medical Entities Decision
Tables" was used to select the underlying cause for deaths that occurred during
a mean follow-up period of 5 years. We chose as end points all deaths and
deaths caused by CHD (ICD-9 codes 410-414). The reliability
of the National Death Index for epidemiologic purposes among health professionals
has been validated.19 To detect a possible
shift of the death certification from CHD to other cardiovascular diseases,
all cardiovascular deaths (except stroke) were also analyzed as an end point,
but the results were not materially different from those obtained when considering
CHD deaths separately.
STATISTICAL ANALYSIS
We calculated means or proportions of baseline risk factors for the
reference group (subjects without diabetes and without CHD) and the other
3 categories (men with a history of diabetes without CHD, men with a history
of CHD without diabetes, and men with a history of both diabetes and CHD).
We used the Cox proportional hazards model to calculate age-adjusted and multivariate-adjusted
relative risks for each category compared with the reference group, primarily
because this model takes into account the time to event (in this case, time
to death).20 The multivariate analysis was
adjusted for age, body mass index, smoking, exercise, and alcohol consumption.
We did not adjust for hypertension and high cholesterol in the primary models
because diabetes increases the risk of these conditions, and thus they are
potential intermediates in the causal pathway. We included hypertension and
high cholesterol in secondary models to assess whether they mediated the effect
of diabetes, but the results were similar to those of the primary multivariate
model.
RESULTS
During a mean follow-up period of 5 years, 3627 (4%) of the physicians
in the study died. Cardiovascular diseases (excluding stroke) accounted for
1676 (46%) of the deaths; 1246 of these were classified as CHD deaths.
Table 1 presents the baseline
characteristics of the participants. Men who had both diabetes and CHD were
generally older, more likely to be smokers, and less physically active; drank
less alcohol; and had a higher frequency of hypertension and higher cholesterol
compared with men in the other 3 categories. Those with a history of CHD but
not diabetes had a higher frequency of high cholesterol compared with subjects
without CHD. Subjects with diabetes, regardless of their CHD status, reported
drinking less alcohol than subjects without diabetes. Those without CHD, regardless
of their diabetes status, were more likely to be never smokers.
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Table 1. Baseline Characteristics According to Presence or Absence
of Diabetes Mellitus (DM) and Coronary Heart Disease (CHD)*
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Among the 6721 participants who reported having CHD at baseline, 2509
(37.3%) reported having had at least one MI without concomitant angina pectoris;
2233 (33.2%) reported having only angina; and 1979 (29.4%) reported having
both conditions.
The age-adjusted relative risk of all-cause mortality was similar for
subjects with a history of diabetes but not CHD and subjects with a history
of CHD but not diabetes (Table 2).
As expected, the risk of all-cause mortality was much higher among those with
both diabetes and CHD. Compared with men with no diabetes or CHD, the age-adjusted
relative risk of CHD mortality was 3-fold higher for those with diabetes but
not CHD, 5-fold higher for those with CHD but not diabetes, and 12-fold higher
for those with both diabetes and CHD. For both all-cause and CHD mortality,
the results were not materially altered after multivariate adjustment for
body mass index, smoking habits, physical activity, and alcohol intake. These
results are also shown by Kaplan-Meier curves in
Figure 1 and
Figure 2.
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Table 2. Relative Risk (RR) of Death From All Causes, All Heart Diseases,
and Coronary Heart Disease (CHD) During 5 Years of Follow-up According to
Diabetes Mellitus (DM) and CHD Diagnoses at Baseline*
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Figure 1. All-cause mortality stratified
by history of diabetes melitus (DM) and coronary heart disease (CHD) among
91 285 men.
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Figure 2. Coronary heart disease (CHD) mortality
stratified by history of diabetes mellitus (DM) and CHD among 91 285
men.
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After categorizing participants into 3 age strata (40-54, 55-69, and
70-84 years), excess mortality risks associated with diabetes and/or CHD were
observed in all age groups. The magnitudes of the associations were greatest
for men in the youngest group (Table 3).
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Table 3. Relative Risk (RR) of Death From Coronary Heart Disease (CHD)
for Different Age Strata During 5 Years of Follow-up According to Diabetes
Mellitus (DM) and CHD Diagnoses at Baseline*
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Table 4 shows the modifying
effect of covariates other than age in our models. Diabetes and CHD were each
associated with elevated mortality risk in all strata of body mass index,
in the presence or absence of hypertension, in the presence or absence of
high cholesterol, with past or current smoking status, with vigorous exercise,
and with alcohol intake.
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Table 4. Multivariate Relative Risk (RR) of Death From Coronary Heart
Disease (CHD) During 5 Years of Follow-up Modified by Cardiovascular Risk
Factors According to CHD and Diabetes Mellitus (DM) Diagnoses at Baseline*
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COMMENT
These prospective data demonstrate that self-reported diabetes is associated
with a substantial increase in mortality from CHD and from all causes. The
total risk of death associated with diabetes was essentially equal to that
associated with prior CHD, each conferring a 2-fold increased risk of death.
The observed risk of all-cause mortality was similar for subjects with a history
of diabetes but not CHD and subjects with a history of CHD but not diabetes,
which is likely attributable to the increased burden of noncardiovascular
death among people with diabetes.21 In terms
of CHD mortality, diabetes alone more than tripled the risk of CHD death.
While a history of CHD carried a greater risk for CHD death than diabetes
alone, the combined presence of diabetes mellitus and CHD conferred a dramatic
12-fold increase in risk of CHD death compared with those men with neither
disease. These increased risks underscore the impact of diabetes on cardiovascular
health. Diabetes is associated with increases in traditional risk factors
for cardiovascular disease, including hypertension and dyslipidemia, increased
oxidative stress, and increased tissue glycosylation, as well as platelet
and fibrinolytic disorders that lead to a procoagulant state.22
Our data differ from the results of Haffner et al,14
whose 7-year follow-up of 2432 Finnish men and women aged 45 to 64 years found
similar high risks of CHD mortality among diabetic patients without a prior
MI and nondiabetic patients with a prior MI.14
Because diabetes is a weaker risk factor for CHD in elderly individuals than
in middle-aged individuals, the different mean ages of the Finnish and PHS
populations may account for the divergent results from that study and ours.
However, we were able to verify in the PHS enrollment cohort that a significant
difference in risk persisted even in the older age groups between subjects
with a history of diabetes without CHD and those with a history of CHD without
diabetes. Another important difference between the 2 studies is that all participants
in the PHS were male, while the Finnish study enrolled almost equal numbers
of men and women. Numerous prospective cohort studies have demonstrated that
diabetes is a stronger risk factor for CHD in women than in men, with age-adjusted
CHD mortality rates 3 to 7 times higher in diabetic women than in nondiabetic
women6, 7 and 2 to 3 times higher
in diabetic men than in nondiabetic men.2, 3, 4, 5
Our data demonstrate a striking 5-fold increased risk of all-cause mortality
and a 12-fold increased risk of CHD mortality in men with both diabetes and
CHD, highlighting the importance of aggressive secondary prevention in patients
with coexisting diabetes and CHD. This is further supported by secondary analyses
from the Scandinavian Simvastatin Survival Study,23
the Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto miocardico
3 (GISSI-3) trial,24 and the Heart Outcomes
Prevention Evaluation trial,25 in which post-MI
treatment with simvastatin, lisinopril, and ramipril, respectively, was associated
with significantly greater reductions in mortality in diabetic patients than
in nondiabetic patients. Greater efforts are needed to target this high-risk
population, however, as demonstrated in a recent study of survivors of first
MI in the United Kingdom, in which people with diabetes were less likely to
be treated with lipid-lowering agents, angiotensin-converting enzyme inhibitors,
and aspirin than were those without diabetes.26
In terms of primary prevention of CHD in people with diabetes, expert
panels currently recommend a more radical reduction in blood pressure among
people with diabetes and coexisting hypertension,27
the use of low-dose aspirin for people with diabetes and other CHD risk factors,28 and the use of lipid-lowering drugs for people with
diabetes who have elevated lipoprotein levels.29
However, these recommendations are aimed at diabetic persons who have concomitant
CHD risk factors. Our data suggest that diabetes is associated with an increased
risk of CHD mortality regardless of the presence or absence of other risk
factors (Table 4) and that having
diabetes alone warrants a more intensive application of primary prevention
measures, as recently recommended by the American Heart Association.30
The strengths of our study are its size, its prospective design, and
the relatively homogeneous nature of the cohort, which minimize confounding
by several variables, including early symptom awareness, access to medical
care, educational attainment, and socioeconomic status. At the same time,
the study has several potential limitations. The data were based on self-reports,
which can lead to misclassification. Studies of health professionals, however,
have found self-reporting to be reliable for cardiovascular risk factors,18 with a 95% rate of confirmation of CHD events in
the randomized phase of the PHS.17 Other limitations
include the use of medical death certificates to define CHD end points,31 the lack of data about the duration or type of diabetes,
and the lack of data about glycemic control. However, tight control of blood
glucose levels has not been conclusively documented to be associated with
cardiovascular end points in either type 1 or type 2 diabetes.32, 33
Our results may not be generalizable to women because diabetes is a
stronger risk factor for cardiovascular disease in women than in men; so far,
no observational studies among women using the same design as our study have
been published. Furthermore, because more than 90% of our participants were
white, these results may not be generalizable to men of other racial groups,
in whom the prevalence of diabetes34 and the
risk of CHD35 may differ.
The increased risk of all-cause and CHD mortality that we observed among
individuals with preexisting diabetes or CHD may, in fact, represent a best-case
scenario, given the relatively high access to medical insurance and medical
care in the PHS population. The relative risks may be even higher in a general
population with poorer access to health care, and thus possibly less prompt
and less aggressive diagnosis and care of diabetes and CHD.
In conclusion, our data demonstrate that diabetes is a strong risk factor
for mortality from all causes and from CHD and that individuals with coexisting
diabetes and CHD are part of a particularly high-risk group. These findings
support the need for aggressive primary and secondary prevention measures
in individuals with diabetes. Clinical trials addressing primary prevention
in people with diabetes free of coronary disease, such as the proposed Prevention
of Cardiovascular Disease in Diabetes Mellitus Study and the subgroup of diabetic
participants in the ongoing Antihypertensive and Lipid Lowering Treatment
to Prevent Heart Attack Trial (ALLHAT), and data from observational studies
are needed to develop new approaches to reduce the burden of cardiovascular
disease among people with diabetes.
AUTHOR INFORMATION
Accepted for publication July 10, 2000.
This study was supported by grant HL-42441 from the National Institutes
of Health, Bethesda, Md. Dr Lotufo is the recipient of fellowship 97-02424-8
from Fundação de Amparo a Pesquisa do Estado de São Paulo,
Sao Paulo, Brazil.
The authors thank Rimma Dushkes, MS, and P. J. Skerrett, MS, for their
expert assistance.
From the Division of Preventive Medicine (Drs Lotufo, Gaziano, Chae,
Ajani, Buring, and Manson), Division of Cardiovascular Disease (Dr Gaziano),
and Channing Laboratory (Dr Manson), Department of Medicine, Brigham and Women's
Hospital and Harvard Medical School, Boston, Mass; Massachusetts Veterans
Epidemiology Research and Information Center, Veterans Affairs Medical Center,
Brockton/West Roxbury (Dr Gaziano); Cardiology Division, Massachusetts General
Hospital, Boston (Dr Chae); Division of General Internal Medicine, University
of California, San Francisco (Dr Moreno-John); and Department of Epidemiology,
Harvard School of Public Health, Boston (Drs Buring and Manson).
Corresponding author and reprints: JoAnn E. Manson, MD, DrPH, Division
of Preventive Medicine, Brigham and Women's Hospital, 900 Commonwealth Ave
E, Boston, MA 02215-1204 (e-mail:
jmanson{at}rics.bwh.harvard.edu).
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Boccara and Cohen
Heart 2004;90:1371-1373.
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Cardiovascular disease incidence and mortality in older men with diabetes and in men with coronary heart disease
Wannamethee et al.
Heart 2004;90:1398-1403.
ABSTRACT
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Trends in Cardiovascular Complications of Diabetes
Fox et al.
JAMA 2004;292:2495-2499.
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The Independent Effect of Type 2 Diabetes Mellitus on Ischemic Heart Disease, Stroke, and Death: A Population-Based Study of 13 000 Men and Women With 20 Years of Follow-up
Almdal et al.
Arch Intern Med 2004;164:1422-1426.
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Impact of Diabetes and Previous Myocardial Infarction on Long-term Survival: 25-Year Mortality Follow-up of Primary Screenees of the Multiple Risk Factor Intervention Trial
Vaccaro et al.
Arch Intern Med 2004;164:1438-1443.
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Cardiovascular Events in Diabetic and Nondiabetic Adults With or Without History of Myocardial Infarction
Lee et al.
Circulation 2004;109:855-860.
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Importance of Weight Management in Type 2 Diabetes: Review with Meta-analysis of Clinical Studies
Anderson et al.
J. Am. Coll. Nutr. 2003;22:331-339.
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Prediction of Coronary Heart Disease in Middle-Aged Adults With Diabetes
Folsom et al.
Diabetes Care 2003;26:2777-2784.
ABSTRACT
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Diabetes abolishes the gender gap in coronary heart disease
Mak and Haffner
Eur Heart J 2003;24:1385-1386.
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Sex Differences in Risk for Coronary Heart Disease Mortality Associated With Diabetes and Established Coronary Heart Disease
Natarajan et al.
Arch Intern Med 2003;163:1735-1740.
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Disparities in Use of Lipid-Lowering Medications Among People With Type 2 Diabetes Mellitus
Safford et al.
Arch Intern Med 2003;163:922-928.
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Impact of Incident Diabetes and Incident Nonfatal Cardiovascular Disease on 18-Year Mortality: The Multiple Risk Factor Intervention Trial experience
Eberly et al.
Diabetes Care 2003;26:848-854.
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Time2Take on risk -- making the link between insulin resistance and cardiovascular risk: Report of a GSK symposium from Diabetes UK, Glasgow, March 19th 2003
British Journal of Diabetes & Vascular Disease 2003;3:S1-S8.
The Effects of Diabetes on the Risks of Major Cardiovascular Diseases and Death in the Asia-Pacific Region
Asia Pacific Cohort Studies Collaboration
Diabetes Care 2003;26:360-366.
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Diabetes, Plasma Insulin, and Cardiovascular Disease: Subgroup Analysis From the Department of Veterans Affairs High-Density Lipoprotein Intervention Trial (VA-HIT)
Rubins et al.
Arch Intern Med 2002;162:2597-2604.
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The impact of diabetes mellitus and prior myocardial infarction on mortality from all causes and from coronary heart disease in men
Cho et al.
J Am Coll Cardiol 2002;40:954-960.
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