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Smoking and Risk of Coronary Heart Disease Among Women With Type 2 Diabetes Mellitus
Wael K. Al-Delaimy, MD, PhD;
JoAnn E. Manson, MD, DrPH;
Caren G. Solomon, MD, MPH;
Ichiro Kawachi, MD, PhD;
Meir J. Stampfer, MD, DrPH;
Walter C. Willett, MD, DrPH;
Frank B. Hu, MD, PhD
Arch Intern Med. 2002;162:273-279.
ABSTRACT
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Background Although the association between smoking and increased risk of coronary
heart disease (CHD) is well established in the general population, this relationship
is less well-defined among individuals with diabetes.
Objective To assess the relationship between cigarette smoking and risk of CHD
among women with type 2 diabetes mellitus in the Nurses' Health Study cohort.
Methods The Nurses' Health Study, a prospective cohort study of 121 700
US female registered nurses surveyed in 11 states and followed up from July
1, 1976, through July 1, 1996, involved a total of 6547 women diagnosed as
having type 2 diabetes mellitus. Incident cases of CHD were our main outcome
measure in this study.
Results We documented 458 incident cases of CHD (200 fatal CHD-related cases
and 258 nonfatal myocardial infarctions) during 20 years (68 227 person-years)
of follow-up. We found a dose-response relationship between current smoking
status and risk of CHD among diabetic women. Compared with never smokers,
the relative risks (RRs) for CHD were 1.21 (95% confidence interval [CI],
0.97-1.51) for past smokers, 1.66 (95% CI, 1.10-2.52) for current smokers
of 1 to 14 cigarettes per day, and 2.68 (95% CI, 2.07-3.48) for current smokers
of 15 or more cigarettes per day in multivariate analyses (P<.001 for trend). The multivariate RR of CHD among diabetic women
who had stopped smoking for more than 10 years was similar to that among diabetic
women who were never smokers (RR, 1.01; 95% CI, 0.73-1.38). In secondary analyses
involving diabetic and nondiabetic women, the multivariate-adjusted RR of
CHD for those with diabetes who currently smoked ( 15 cigarettes per day)
compared with those who never smoked was 7.67 (95% CI, 5.88-10.01).
Conclusions Cigarette smoking is strongly associated with an increased risk of CHD
among women with type 2 diabetes mellitus. Furthermore, quitting smoking seems
to decrease this excess risk substantially; women with diabetes should be
strongly advised against smoking.
INTRODUCTION
DIABETES CONFERS a substantially increased risk of coronary heart disease
(CHD),1-3 especially
among women.4-5 Smoking is an
established risk factor for CHD among the general population.6
However, the magnitude of the association between smoking and CHD risk among
diabetic women has not been well studied.7
Furthermore, the impact of quitting smoking, using quantitative measures of
quitting history, on this CHD risk has not been investigated fully. Therefore,
we assessed the relationships of smoking and quitting smoking to the risk
of CHD among diabetic women in the Nurses' Health Study cohort during 20 years
of follow-up.
SUBJECTS AND METHODS
STUDY POPULATION
The Nurses' Health Study was established in 1976, when 121 700
US female registered nurses aged 30 to 55 years who each resided in 1 of 11
states completed a mailed questionnaire regarding medical history and lifestyle
factors. This information has been updated every 2 years. The population for
this analysis included women who were diagnosed as having type 2 diabetes
mellitus at baseline or during follow-up between July 1, 1976, and July 1,
1996.
ASSESSMENT OF SMOKING
Smoking status was assessed on each biennial questionnaire. Participants
were classified as current, past, or never smokers. Current smokers were categorized
into those who smoked 1 to 4, 5 to 14, 15 to 24, 25 to 34, 35 to 44, or 45
or more cigarettes per day. In this study, these categories were collapsed
into 1 to 14 and 15 or more cigarettes per day because of the small number
of cases. For time since quitting, former smokers were categorized as having
stopped smoking for 1 to 5, 6 to 10, 11 to 15, and more than 15 years. The
last 2 categories were also combined to assess the effect of quitting for
more than 10 years. Coronary heart disease–related events were allocated
to the smoking exposure status defined on the most recent questionnaire.
DOCUMENTATION OF DIABETES
When a participant reported a diagnosis of diabetes, we mailed her a
supplementary questionnaire requesting information on the details of the diagnosis
(ie, diagnostic tests, symptoms, and year of diagnosis) and therapy (insulin
or oral hypoglycemic treatment). Using the National Diabetes Data Group criteria,8 diabetes was considered confirmed if the questionnaire
indicated one of the following: (1) classic symptoms (excessive thirst, polyuria,
weight loss, and hunger) associated with an elevated plasma glucose level
(fasting value, 141 mg/dL [7.8 mmol/L]; random value, 200 mg/dL
[11.1 mmol/L]; or a 2-hour postglucose challenge value of 200
mg/dL [11.1 mmol/L]); (2) there were no symptoms, but at least 2 plasma
glucose values were elevated by the criteria previously described on different
occasions; or (3) treatment with a hypoglycemic medication (insulin or an
oral hypoglycemic agent).
We depended on self-reported information for the diagnosis of diabetes
by these nurses, but validated the reports in a random sample of women by
obtaining their medical records. Among 84 women classified by the supplementary
questionnaire as having type 2 diabetes mellitus, 71 provided permission to
review their medical records and 62 had records available. An endocrinologist
(J.E.M.) blinded to the information reported on the supplementary questionnaire
reviewed the records according to the National Diabetes Data Group criteria.8 The diagnosis of type 2 diabetes mellitus was confirmed
in 61 (98%) of the 62 women.9
Those with diabetes diagnosed before the age of 30 years (most likely
type 1 diabetes mellitus) or a previous diagnosis of cancer or cardiovascular
disease (CVD) were excluded from all analyses. In the primary analyses, self-reported
diabetes was used to define the analytic cohort (n = 6547 diabetic women).
Secondary analyses including only diabetic cases confirmed by the supplementary
questionnaire (n = 4863) yielded similar results.
DIAGNOSIS OF CHD
The primary end point in our analysis was incident CHD (including nonfatal
myocardial infarction [MI] and fatal CHD). We analyzed stroke and total CVD
(CHD and stroke) as secondary end points. All CVD-related cases were included
in the analysis if they were diagnosed after the 1976 questionnaire, and after
the diagnosis of diabetes. Women who reported a nonfatal MI were asked permission
to review their medical records, which were used to confirm the diagnosis
according to the World Health Organization diagnostic criteria (ie, symptoms
plus either cardiac enzyme level elevations or diagnostic electrocardiographic
changes). Physicians blinded to exposure status conducted the record reviews.
Infarctions were classified as probable if a patient required hospital admission,
and confirmatory information was obtained by interview or letter without medical
records. All confirmed and probable nonfatal MI cases were included in the
analyses.
Fatal CHD cases were ascertained by reviewing the state vital records
and by a search of the National Death Index. This search was supplemented
by reports from the next of kin, and their written permission was sought to
review the medical records. Fatal CHD was defined as a fatal MI if confirmed
by hospital records or autopsy or as a CHD-related death when recorded on
the death certificate if this was the underlying and most plausible cause
and there was previous evidence of CHD. We designated as presumed fatal CHD
those cases in which CHD was the underlying cause on the death certificate
but no records were available. Also included under fatal CHD were cases of
sudden death (within 1 hour of the onset of symptoms) with no plausible explanation
other than CHD.
Stroke was defined according to the National Survey of Stroke criteria10 by the presence of a typical neurological deficit
of sudden or rapid onset, persisting for more than 24 hours or until death.
Stroke classifications included ischemic stroke due to thrombotic or embolic
occlusion of a cerebral artery or rupture of a vessel resulting in subarachnoid
or intraparenchymal hemorrhage. Vascular disease due to traumatic, neoplastic,
or infectious processes was excluded.
STATISTICAL ANALYSIS
Participants contributed person-time from the date of return of the
1976 questionnaire (for those with prevalent diabetes) or from the date of
diabetes diagnosis (for those with incident diabetes) until the date of occurrence
of MI, the date of death from CHD, or June 1, 1996, whichever came first.
Incident cases of CHD were allocated to the exposure status defined in the
most recent questionnaire. For comparison of the excess risk of smoking among
diabetic and nondiabetic women, incidence rates of CHD were calculated by
dividing the number of new cases by the cumulated person-time of follow-up
and were adjusted to the age distribution of diabetic and nondiabetic women
by direct standardization.
Relative risks were calculated as the incidence rate in each smoking
category divided by the corresponding rate among never smokers. All relative
risks (RRs) were age adjusted, and 95% confidence intervals (CIs) were calculated.
The population attributable risk was calculated by using the formula
provided by Rothman and Greenland11 to determine
the fraction of cases in the study population that would not have occurred
if exposure had not occurred.
Pooled logistic regression models with 2-year increments were used to
control simultaneously for known CHD risk factors. Most of the covariates
were updated biennially, including age (<50, 50-54, 55-59, 60-64, or 65
years); postmenopausal hormone use (premenopausal status, never used, current
use, or past use); alcohol use (0, 0.1-4.9, 5.0-14.9, or 15.0 g/d); duration
of diabetes (0-5, 6-10, 11-15, or >15 years); body mass index, calculated
as weight in kilograms divided by the square of height in meters (21, 22,
23-24, 25-28, or 29); physical activity (<1, 1-<2, 2-<4, 4-<7,
or 7 h/wk of moderate to vigorous activity); diabetes medication (assessed
in the supplementary diabetes questionnaire and in the 1988 and 1994 main
questionnaires: none, oral medication only, or insulin use); history of high
cholesterol (yes or no); history of high blood pressure (yes or no); and parental
history of MI before the age of 60 years (assessed in 1976 and 1984: yes or
no).
Several dichotomous variables were used for stratified analyses to assess
potential effect modification: body mass index (<25 or 25kg/m2), insulin use (yes or no), parental history of MI (yes or no), postmenopausal
hormone use (yes or no), alcohol use (yes or no), duration of diabetes ( 10
or >10 years), physical activity (<3.5 or 3.5 h/wk), age (<60 or 60
years), aspirin use (yes or no), and menopause status (premenopausal or postmenopausal).
In an additional analysis, we examined the joint effects of smoking and diabetes
on the risk of CHD.
Values of covariates that were not collected in a given follow-up questionnaire
were carried over from the previous questionnaire or carried backward for
covariates not recorded at baseline. For example, because alcohol was not
recorded in the 1976 and 1978 questionnaires, the 1980 value was carried backward
to be used for the 1976 and 1978 cycles.
Tests for trend were conducted using the median value for each category
of smoking status as a continuous variable. All P
values were 2-sided. The SAS statistical software package was used for the
analyses.12
RESULTS
At baseline, 1754 women reported physician-diagnosed diabetes at 30
years or older. During the follow-up, an additional 4793 women reported a
diagnosis of diabetes. During 68 227 person-years of follow-up among
these women, we documented 458 incident cases of CHD (200 fatal CHD-related
cases and 258 nonfatal MI cases) from 1976 to 1996.
Table 1 shows the characteristics
of the diabetic women in relation to their smoking habits in 1986. Current
smokers were leaner and more likely to consume alcohol. Past smokers had a
higher prevalence of diagnosed high blood pressure. Current smokers were less
likely to use vitamin E supplementation.
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Table 1. Age-Adjusted Characteristics of Diabetic Women According to
Smoking Status in 1986*
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The risk of CHD increased monotonically with greater smoking (Table 2). Compared with never smokers,
the RRs for CHD were 1.21 for past smokers, 1.66 for current smokers of 1
to 14 cigarettes per day, and 2.68 for current smokers of 15 or more cigarettes
per day in the multivariate analysis. The association for nonfatal MI was
somewhat stronger than for fatal CHD (Table
2). Further adjustment for vitamin E supplement use did not alter
the results. Current smokers had an RR of 2.17 of developing CHD compared
with nonsmokers (never or past smokers) in multivariate-adjusted analyses,
and the CHD risk attributable to smoking in this population was 19% (current
smoking prevalence, 20%).
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Table 2. Age- and Multivariate-Adjusted RRs (95% CIs) for Total CHD,
Fatal CHD, and Nonfatal MI According to Smoking Status Among Diabetic Women*
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Analyses stratified by body mass index, parental history of MI, postmenopausal
hormone use, diabetes medication, duration of diabetes, and alcohol use showed
consistent associations between smoking and risk of CHD (Table 3). This association was stronger among women younger than
60 years than among women 60 years and older.
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Table 3. Multivariate-Adjusted RR (95% CIs) for Total CHD Incidence
According to Smoking Status in Diabetic Women, Stratified by Coronary Covariates*
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Past smokers were divided into those who stopped smoking for more than
15, 11 to 15, 6 to 10, and 1 to 5 years (Figure 1). The multivariate RR of CHD among diabetic women who had
stopped smoking for more than 10 years was similar to that among diabetic
women who were never smokers. Women who had stopped smoking within the past
10 years still had an increased risk (RR, 1.32 [95% CI, 0.96-1.84] for those
who quit for 6-10 years; and RR, 1.40 [95% CI, 1.04-1.88] for those who quit
for 1-5 years) compared with the never smokers. Nevertheless, the latter 2
groups of past smokers were still at a lower risk compared with current smokers.
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Figure 1. Multivariate-adjusted relative
risk of coronary heart disease (CHD) according to smoking status and duration
of quitting smoking among diabetic women. The vertical bars indicate the 95%
confidence intervals.
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In secondary analyses, we examined smoking in relation to the risk of
stroke and total CVD (stroke and CHD). The multivariate RRs for stroke were
0.69 (95% CI, 0.48-1.00) among past smokers, 1.04 (95% CI, 0.50-2.17) among
current smokers of 1 to 14 cigarettes per day, and 1.84 (95% CI, 1.21-2.81)
among current smokers of 15 or more cigarettes per day (P = .004 for trend). The multivariate RRs of CVD were 1.03 (95% CI,
0.86-1.25) for past smokers, 1.46 (95% CI, 1.02-2.10) for current smokers
of 1 to 14 cigarettes per day, and 2.42 (95% CI, 1.94-3.02) for current smokers
of 15 or more cigarettes per day (P<.001 for trend).
We also compared age-adjusted rates of CHD in women with diabetes with
those in nondiabetic women according to smoking status. The age-adjusted incidence
rate of CHD among diabetic women was much higher than that of nondiabetic
women of similar smoking status (Figure 2). The joint impact of smoking and diabetes status on the risk of
CHD was substantial; compared with nondiabetic women who had never smoked,
diabetic women who smoked 15 or more cigarettes per day had an age-adjusted
RR of 19.01 (95% CI, 15.42-23.45). This RR was attenuated to 7.67 (95% CI,
5.88-10.01) in the multivariate-adjusted model. Among nondiabetic women, the
multivariate RR comparing current smokers (15 cigarettes per day) with
never smokers was 5.13 (95% CI, 4.53-5.80). The corresponding RR among diabetic
women was 2.65 (95% CI, 2.06-3.40). The likelihood ratio test and interaction
was significant (P<.001). The higher RR of CHD
of nondiabetic women who smoked compared with diabetic women who smoked can
be explained by the much higher baseline risk of diabetic women compared with
nondiabetic women.
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Figure 2. Age-adjusted coronary heart disease
(CHD) incidence rates (per 100 000 person-years) among women with and
without diabetes according to smoking status.
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COMMENT
We observed a strong positive association between cigarette smoking
and CHD among diabetic women. Cigarette smoking amplified the excess risk
of CHD associated with type 2 diabetes mellitus. On the other hand, smokers
who quit smoking for more than 10 years had a risk of developing CHD similar
to that of diabetic women who had never smoked.
The strengths of the study include the large number of diabetic women
and the long duration of follow-up, which allows the assessment of smoking
and CHD risk in different subgroups. The follow-up rate for fatal and nonfatal
events was high (approximately 98%), minimizing potential bias due to loss
to and unavailability for follow-up. The prospective design minimized selection
and recall bias, which can occur in case-control studies.
Potential weaknesses should be noted. Some women with diabetes may have
been undiagnosed in the cohort because we did not screen for glucose intolerance.
However, these cases would not alter the case status of women reporting a
diagnosis of diabetes, which was validated in a separate study.9
The criteria for type 2 diabetes mellitus have recently changed, so that those
with a glucose level higher than 126 mg/dL (>7.0 mmol/L) are believed to have
diabetes, instead of the 141 mg/dL (7.8 mmol/L) used before the publication
of the new criteria in 1997.13 So, more nondiabetic
persons would be classified as having diabetes using the new definition. Nevertheless,
inclusion of diabetic persons in the nondiabetic group in our study as a result
of using the old definition would have attenuated the associations we observed
and is unlikely to change our findings.
The smoking assessment was based on self-reports and was not verified
by other objective measures. However, reporting of smoking should not be biased
in relation to CHD incidence because smoking was assessed before the development
of CHD. In addition, because the smoking variable was updated every 2 years,
our analyses were able to take into account changes in smoking behavior.
Few previous studies have prospectively examined the association between
smoking and CHD among diabetic persons. A Finnish prospective study14 among 313 men and women with type 2 diabetes mellitus
did not find smoking to be related to fatal or nonfatal CHD in a univariate
logistic regression analysis. Also, in the Whitehall study,15
smoking was not significantly associated with CHD-related mortality rates
among 224 diabetic and glucose-intolerant men. Both studies involved fewer
diabetic subjects and had a shorter follow-up than our study; thus, statistical
power to detect an association was limited. On the other hand, in the National
Health and Nutrition Examination Survey study,16
CHD-related mortality risk was higher among 492 diabetic smokers compared
with never smokers, and in the Multiple Risk Factor Intervention Trial,17 risk of CVD-related mortality among 5625 diabetic
men increased with higher levels of smoking. This was also supported more
recently by the results from the United Kingdom Prospective Diabetes Study,18 in which smoking was a significant risk factor for
fatal and nonfatal MI (P = .02) among diabetic women
and men in multivariate analyses.
Diabetes may increase the risk of CHD through various proposed mechanisms,
including lipoprotein changes, increased vascular endothelial injury and permeability,
thrombotic disorders, increased oxidative stress, and fibrinolytic factors
and platelet activities leading to atheroma formation.19-21
Smoking may exacerbate these conditions and contribute to a dramatically increased
risk of CHD among diabetic persons by a combination of short-term effects
(coronary artery spasm, arrythmias, and increased platelet aggregation) and
long-term effects (increased triglyceride levels, decreased high-density lipoprotein
levels, and other metabolic effects that lead to atherogenesis)19, 22
on the cardiovascular system. Smoking is also thought to increase insulin
resistance and aggravate metabolic disturbances among diabetic persons.23-24 Targher et al,25
for example, found among 40 diabetic patients that insulin resistance was
markedly aggravated among smokers. In previous studies, smoking 25 cigarettes
per day or more, compared with never smoking, was associated with a higher
risk of developing diabetes among women (RR, 1.42; 95% CI, 1.18-1.72)26 and men (RR, 1.94; 95% CI, 1.25-3.03).27
Our results also indicate that diabetic women who smoked 15 or more
cigarettes per day had an 84% higher risk of developing stroke compared with
never smokers. These results are consistent with earlier findings9 that smoking amplifies the risk of stroke among diabetic
women.
Quitting smoking and maintaining cessation for more than 10 years seem
to substantially reduce the high risk of developing CHD among diabetic women
who smoked. The benefits of smoking cessation are associated with total mortality
rate,28 with CHD and stroke incidence among
the Nurses' Health Study and general populations,29-32
and, more recently, with CHD risk in the United Kingdom Prospective Diabetes
Study cohort of diabetic persons.18 The United
Kingdom Prospective Diabetes Study found that, compared with never smokers,
past smokers were at lower risk of nonfatal and fatal MI (RR, 1.27) than current
smokers (RR, 1.74). However, that study did not provide detailed analysis
of past smokers according to the duration of quitting and its association
with CHD risk.
The American Diabetic Association33 recently
emphasized the importance of targeted smoking cessation programs for diabetic
persons, calling for health care providers to (1) routinely assess tobacco
use among diabetic persons, (2) counsel on smoking prevention and cessation,
and (3) routinely implement smoking cessation guidelines. Although smoking
rates were slightly lower among the diabetic women in our study compared with
the nondiabetic population, it is alarming that others found smoking rates
among diabetic persons to be similar to24 or
even higher than17, 34 those of
nondiabetic persons. However, individuals with diabetes seem to be more receptive
to their physician's advice and to the prospect of smoking cessation.35-36
Smoking cessation may have an important effect on CHD risk reduction
among diabetic persons compared with the effects reported with cholesterol
lowering or high blood pressure treatment. Clinical trials to lower cholesterol
levels among diabetic persons achieved 25% to 55% reduction in the risk of
major CHD-related events,37-38
and tight blood pressure control achieved 21% reduction in the risk of fatal
and nonfatal MI and sudden death (although the results were not statistically
significant).39 Our results suggest that the
risk of CHD among diabetic women who smoke could have been reduced by about
54% if they had not smoked. In the overall diabetic population, which comprises
20% smokers, the population attributable risk due to current smoking was 19%.
Our findings have important clinical and public health implications
and provide strong support for the American Diabetic Association recommendations.
Given that cigarette smoking is such a strong, yet modifiable, risk factor
for CHD among diabetic individuals, physicians should discourage their diabetic
patients from smoking.
AUTHOR INFORMATION
Accepted for publication May 8, 2001.
This study was supported by research grants HL24074, HL34594, and CA87969
from the National Institutes of Health, Bethesda, Md; and a research award
from the American Diabetic Association, Alexandria, Va (Dr Hu).
We thank Al Wing for his support and help and the subjects who participated
in the Nurses' Health Study.
Corresponding author: Wael K. Al-Delaimy, MD, PhD, Department of
Nutrition, Harvard School of Public Health, 665 Huntington Ave, Boston, MA
02115 (e-mail: wael{at}hsph.harvard.edu).
From the Departments of Nutrition (Drs Al-Delaimy, Willett, and Hu),
Epidemiology (Drs Manson, Stampfer, and Willett), and Health and Social Behavior
(Dr Kawachi), Harvard School of Public Health, Boston, Mass; and the Channing
Laboratory (Drs Manson, Kawachi, Stampfer, and Willett) and the Divisions
of Preventive Medicine (Dr Manson) and General Medicine and Women's Health
(Dr Solomon), Department of Medicine, Harvard Medical School and Brigham and
Women's Hospital, Boston.
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