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(Stroke. 2004;35:1836.)
© 2004 American Heart Association, Inc.

Original Contributions

Cigarette Smoking as a Risk Factor for Stroke Death in Japan

NIPPON DATA80

Hirotsugu Ueshima, MD; Sohel Reza Choudhury, MD; Akira Okayama, MD; Takehito Hayakawa, PhD; Yoshikuni Kita, PhD; Takashi Kadowaki, MD; Tomonori Okamura, MD; Masumi Minowa, MD Osamu Iimura, MD NIPPON DATA80 Research Group

From the Department of Health Science (H.U., Y.K., T.K., T.O.), Shiga University of Medical Science, Otsu, Japan; the Department of Community Medicine (S.R.C.), School of Medical Sciences, Universiti Sains Malaysia, Kota Bharu, Malaysia; the Department of Hygiene and Preventive Medicine (A.O.), School of Medicine, Iwate Medical University, Morioka, Japan; the Department of Environmental Medicine (T.H.), Shimane Medical University, Izumo, Japan; the Department of Epidemiology (M.M.), National Institute of Public Health, Wako, Japan; and Hokkaido JR Sapporo Hospital (O.I.), Sapporo, Hokkaido, Japan.

Correspondence to Dr Hirotsugu Ueshima, Department of Health Science, Shiga University of Medical Science, Tsukinowa-cho Seta, Otsu, Shiga, 520-2192, Japan. E-mail hueshima{at}belle.shiga-med.ac.jp

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose— Some previous Japanese cohort studies failed to show an association between smoking and stroke risk. Because such an association has been noted in other populations, this issue should be re-examined in a recent representative Japanese cohort with a higher total cholesterol level.

Methods— A total of 9638 men and women aged 30 years and older without a history of cardiovascular disease (CVD) at baseline in 1980 were followed-up for 14 years.

Results— We observed 203 stroke deaths (107 cerebral infarctions, 45 cerebral hemorrhages, and 51 others), 191 heart disease deaths, and 413 CVD deaths. The average serum total cholesterol level was 4.91 mmol/L. Cox proportional hazard ratios were calculated adjusting for age, systolic blood pressure, and other conventional risk factors. The hazard ratios for men who smoked 1 to 20 cigarettes/day for all strokes, cerebral infarction, and cerebral hemorrhage were 1.60 (95% CI, 0.91 to 2.79), 2.97 (CI, 1.27 to 6.98), and 0.42 (CI, 0.16 to 1.09), respectively, and for those who smoked 21 cigarettes/day, they were 2.17 (CI, 1.09 to 4.30), 3.26 (CI, 1.11 to 9.56), and 0.68 (CI, 0.20 to 2.33), respectively. For women who smoked 21 cigarettes/day, the hazard ratio for all strokes was 3.91 (CI, 1.18 to 12.90). For CVD, all heart disease, and ischemic heart disease, the hazard risks of smoking were significant (1.49 to 4.25) for men but not significant for women.

Conclusions— Smoking in a cohort with moderate serum total cholesterol level was a potent risk factor for stroke, especially cerebral infarction, for both men and women, and for CVD and ischemic heart disease for men.

Key Words: epidemiology • cerebrovascular disorders • stroke • risk factors

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
It is well known that cigarette smoking is associated with an increased risk of cardiovascular disease (CVD).¹ Many epidemiological studies in Western populations have identified smoking as an independent risk factor for stroke, ^2,3 and this association has also been found in people of Japanese descent living in Hawaii.⁴ However, epidemiological data regarding the relationship between smoking and stroke in Japanese people living in Japan remain inconclusive.^5–8 The Hisayama study involving 1600 rural subjects followed-up for 23 years⁶ did not find any association between smoking and cerebral infarction. Although smoking prevalence was high in this population, mean blood cholesterol level was low and hypertension appeared to be the sole cause of stroke from the 1960s to 1975.⁷ However, recent analysis of the Hisayama study revealed that from 1961 to 1993, smoking was a risk factor for lacunar stroke.⁹

We therefore hypothesized that with the recent increase in dietary fat intake and the relative increase in the population blood cholesterol level, ^10,11 the risk of stroke, particularly cerebral infarction, in smokers should be higher^8,12 than that observed in previous cohort studies.^5,6 In this study, we investigated the association between smoking and the risk of death from stroke and stroke subtype, CVD, all heart diseases, ischemic heart disease (IHD), and all causes.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Baseline Survey
The subjects of this cohort study were the participants of the National Cardiovascular Survey of 1980 that was conducted with the National Nutrition Survey. The National Nutrition Survey in Japan is performed each year using a similar method and questionnaire. The standardized procedures used in this survey have been described elsewhere.¹³ This survey was performed for all household members aged 30 years or older in 300 census tracts, which were randomly selected throughout Japan. The baseline survey included medical examinations, blood pressure measurements, blood tests, and a self-administered questionnaire about lifestyle from 10 897 subjects. The survey response rate was 79.4%. Trained staff at local health centers in the respective districts performed the examinations in community centers. A history of past illnesses, including heart disease, stroke, and diabetes, and smoking and drinking habits were obtained from the questionnaire. Subjects were asked to note whether they were current smokers, had quit smoking, or had never smoked. Smokers were asked to note the number of cigarettes smoked each day. With regard to drinking habits, subjects were asked to note whether they were "nonsmokers" or "ex-smokers" and if they were "sometimes" drinkers or "everyday" drinkers. Body weight was measured while the subjects wore light clothing and no shoes. Single blood pressure was measured by a standard sphygmomanometer to obtain systolic and diastolic blood pressure (SBP and DBP). Nonfasting blood samples were drawn. The measurement precision and accuracy for serum cholesterol were certified in the Lipid Standardization Program administered by the Center for Disease Control and Prevention, Atlanta, Ga.

Follow-Up Survey
A total of 10 546 subjects aged 30 years or older for whom we had complete baseline information regarding age, sex, and blood pressure in the 1980 data set were defined as the cohort (NIPPON DATA80). They were followed-up until 1994, and a follow-up survey was performed in 1994 to ascertain the vital status of cohort subjects.¹³ Vital statistics for determining causes of death were obtained from the Management and Coordination Agency, Government of Japan. Approval for this study was obtained from the Institutional Review Board of Shiga University of Medical Science (number 12-8, 2000).

The underlying causes of death were coded according to the 9th International Classification of Disease. Number of deaths from all causes, CVD (ICD 9 code: 393 to 459), stroke (ICD 9 code: 430 to 438), hemorrhagic stroke (ICD 9 code: 431 to 432), cerebral infarction (ICD 9 code: 433, 434, 437.7A, 437.7B), heart disease (ICD 9 code: 393 to 398, 410 to 414, 415 to 429), and IHD (ICD 9 code: 410 to 414) were identified.

Out of 10 546 cohort subjects, the vital status of 9638 subjects (91.4%) could be ascertained in 1994. A total of 1617 subjects were excluded because of the following reasons: past history of CVD (n=697), missing information on smoking at baseline (n=12), and lost to follow-up (n=908). We analyzed the data of the remaining 8929 subjects (3972 men and 4957 women).

Although there was no difference in smoking rate between men who were and were not followed-up, there was a significant difference between women who were and were not followed-up (8.8% versus 20.0%). The mean ages (±standard deviation [SD]) at baseline were 50.0 (±13.0) and 50.2 (±13.1) years for men and women, respectively; the mean ages at the end of follow-up were 63.1 (±12.2) and 63.6 (±12.5) years, respectively.

Statistical Analysis
Subjects were divided into 4 smoking categories according to their baseline smoking habits: nonsmoker, ex-smoker, moderate smoker (1 to 20 cigarettes/d), and heavy smoker (21 cigarettes/d). The body mass index (BMI) was calculated as weight (kg) divided by the square of height (m). A current drinker was defined as an occasional or everyday drinker. Age-adjusted mortality rates were calculated by the direct method using the Japanese standard population of 1985. Analysis of variance was used for comparisons of several means. The ² test was used to compare the frequencies among the categories. Age-adjusted and multivariate-adjusted relative risks were calculated using the Cox proportional hazard model. All P values were 2-tailed and all CIs were estimated at the 95% level. The Statistical Package for the Social Sciences (SPSS Japan Inc, version 10) was used for the analyses.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
There was a large difference in smoking rate between men and women: 50% to 70% of the men smoked whereas only 7% to 12% of the women smoked. The prevalence of heavy smokers, as defined by subjects who smoked 21 cigarettes/d, was highest in younger men (age 30 to 39 years). At the opposite end of the spectrum, the prevalence of quitters was highest in the elderly. For women, the prevalences of heavy smokers and of ex-smokers were relatively low. The drinking rate was also higher in men than in women.

Means and SDs or frequencies of selected variables by smoking habit at baseline are shown in Table 1. Among the smoking categories, the mean BMI was the highest in nonsmoking men, whereas among women, moderate smokers (20 cigarettes/d) had the highest BMI. SBP was significantly different among the smoking categories for both men and women: for both sexes, ex-smokers had the highest mean SBP. Serum total cholesterol significantly differed among smoking categories for men; however, the absolute differences among the categories were small.

View this table: [in this window] [in a new window]   TABLE 1. Distribution of Selected Risk Factors (Mean±SD or Percentage) by Smoking Habits at Baseline in 1980, NIPPON DATA80

Table 2 shows the number of deaths and age-adjusted death rates per 100 000 person-years of observation for all causes of death and cause-specific deaths according to smoking habits and sex. The mean follow-up period was 13.2 years; in total, there were 118 044 person-years of observation and 1112 deaths occurred during this period for men and women combined. Approximately one third of all deaths were CVD-related. The numbers of deaths from stroke and from heart disease were very similar. The mean ages (±SD) of stroke death cases were 76.9 (±10.9) and 77.3 (±11.2) years for men and women, respectively. Among the stroke subtypes, the incidence of cerebral infarction death was almost double for both men and women than that of hemorrhagic stroke death. The incidence of IHD death was almost one third that of total heart disease death in both men and women.

View this table: [in this window] [in a new window]   TABLE 2. Number of Deaths and Age-Adjusted Death Rates per 100 000 Person-Years for All-Cause and Cardiovascular Disease Deaths According to Smoking Habit in Japan During 1980–1990, NIPPON DATA80

Table 3 shows the multivariate-adjusted relative risks of death from all causes and for CVD-specific death according to smoking habit. These relative risks were adjusted for age, SBP, BMI, serum total cholesterol, drinking habit, and diabetes mellitus.

View this table: [in this window] [in a new window]   TABLE 3. Multivariate-Adjusted Relative Risk (95% CI) for All-Cause and Cardiovascular Disease According to Smoking Habit in Japan, NIPPON DATA80

For all causes of death, the adjusted risks of daily smokers for both men and women were 14% to 55% higher than those of nonsmokers, and the relative risk for male heavy smokers was 1.55 (95% CI, 1.17 to 2.04). For CVD death, 50% to 100% increase in risk was observed in male smokers compared with male nonsmokers, which was statistically significant. The relative risk of CVD death in female smokers was 40% to 135% higher than in female nonsmokers, although significance was borderline.

For all stroke death, the relative risks for male moderate and heavy smokers were 1.60 (95% CI, 0.91 to 2.79) and 2.17 (95% CI, 1.09 to 4.30), respectively, whereas that for ex-smokers was 1.56 (95% CI, 0.84 to 2.90). The relative risk of cerebral infarction for men was higher than that of all strokes: 3.06 for ex-smokers, 2.97 for moderate smokers, and 3.26 for heavy smokers compared with nonsmokers (P<0.05 for all). For women, the relative risk for stroke death for heavy smokers was significantly higher (relative risk [RR], 3.91; 95% CI, 1.18 to 12.90) than that for nonsmokers; however, moderate smokers had a 42% higher risk of stroke death, although this was not statistically significant. Smoking was not associated with hemorrhagic stroke in either men or women, even in heavy smokers.

For all heart disease, the relative risk of death gradually increased in men from ex-smokers (0.98) to moderate smokers (1.40) to heavy smokers (2.15) (P<0.05). Similarly, the risk of IHD-associated death for men also showed a graded increase from ex-smokers (1.00) to moderate smokers (1.56) to heavy smokers (4.25) compared with nonsmokers (P<0.05). The relative risk of IHD-associated death in women was higher in smokers than in nonsmokers, but this was not statistically significant.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
In the present study, we demonstrated that smoking is an independent risk factor for stroke death in both men and women. The graded association was clearly evident for both cerebral infarction and IHD death as well as for total CVD death. In addition, our study results showed that heavy smoking in women is also a risk factor for all stroke death. These findings reveal a recent trend among Japanese smokers, because the NIPPON DATA80 was the first follow-up study for a representative Japanese population randomly selected throughout Japan. Therefore, the death rate and cause-specific death determinations made in this study represent the actual figure in Japan.

Both 12-year and 20-year follow-up studies of the Honolulu Heart Program involving Japanese Americans living in Hawaii showed smoking to be a risk factor for cerebral infarction and for hemorrhagic stroke.^4,14 These findings combined with those of the present study have led us to conclude that smoking is a risk factor for stroke in Japanese people.

Previously, some cohort studies in Japan revealed smoking to be a risk factor for IHD, but they failed to demonstrate a convincing association between smoking and all strokes, hemorrhagic stroke, or nonhemorrhagic stroke.^5,6 It was puzzling that these studies did not show smoking to be a risk factor for stroke in Japan. One possible explanation for this result may be that associations between smoking and stroke risk are only evident in populations with moderate or high levels of serum total cholesterol. Recent changes in lifestyle and environmental conditions in Japanese people have caused an increase in fat consumption.¹⁰ In 1965, the per-capita energy intake from fat in Japan was 15% according to the National Nutrition Survey.¹⁰ This figure is now 26% overall and close to 30% for the younger generation.^11,15,16 Additionally, a gradual change in the occurrence of stroke subtype has occurred; that is, the number of deaths from hemorrhagic stroke has decreased sharply since 1965, and at present it is only one third of the total number of cerebral infarction-associated deaths.^16–18 Individuals who smoke are much more susceptible to cerebral infarction or lacunar stroke than to hemorrhagic stroke.^18,19 Therefore, in previous Japanese cohort studies, which were performed in a population with low cholesterol, a high mean blood pressure, and a relatively high occurrence of hemorrhagic stroke, an association between smoking and stroke did not emerge. A similar situation currently exists in China. Although China has a very high smoking rate, a recent report from a cohort study in rural areas of China failed to show a significant association between smoking and stroke.²⁰

Hypertension is a well known risk factor for stroke. Our data clearly show that smoking is also a potent risk factor for cerebral infarction, even in populations with moderate cholesterol levels such as those in certain Asian and other developing countries. Therefore, reducing the incidence of smoking as well as hypertension should be a high priority in attempts to overcome the increase in CVD in developing countries and for reducing the number of disabled people in most industrialized countries.

To identify cause of death, we used underlying cause of death determined by a government officer through a review of death certificates written by medical doctors. Misdiagnosis of stroke and its subtypes as well as IHD by a clinician occasionally occurred, which may have caused underestimation or overestimation of the number of cause-specific deaths. We could not validate the recorded cause of death with autopsy findings in this cohort. However, most of the stroke cases in Japan are referred to hospitals for admission and computerized tomography (CT) is performed on >90% of the admitted cases, even in rural areas.^17,21 The >9000 CT machines available throughout Japan in 1996 made this possible.²² It has also been reported that according to autopsy studies, the death certificate diagnosis for stroke in the Hisayama and Hiroshima/Nagasaki studies were quite accurate.^23,24 Therefore, we believe that the diagnoses of stroke as well as its subtypes were mostly correct. In contrast, IHD may have been underestimated to some extent; however, Japanese people do have the lowest incidence of and mortality from IHD in the world.^7,16,25,26

The effect of smoking on the risk of CVD may have been underestimated in our cohort study because smoking habits were identified only once at baseline by a questionnaire in 1980.²⁷ In addition, the lost female subjects had a higher smoking rate than those who were followed-up, and some of the individuals who smoked at baseline may have quit during the follow-up period. Because the risk of CVD after smoking cessation approaches that of nonsmokers within a few years,^2,28 the risk of CVD in smokers may have been underestimated because those who quit were still considered to be smokers in this study. Actually, the prevalence of male and female ex-smokers increased by 3.9% and 0.6%, respectively, between 1980 and 1990.²⁷ A similar underestimation may have occurred regarding the risk of hypertension because of an increased treatment rate for hypertension (from 12.8% to 15.6% between 1980 and 1990 in men and women combined) and regarding hypercholesterolemia for IHD caused by the 0.026-mmol/L increase in serum total cholesterol.²⁷

In conclusion, smoking is a potent risk factor for death from stroke, IHD, all CVD, and all causes of death for both Japanese men and women. We therefore need to more rigorously promote antismoking programs and policy not only in Japan but also in other Asian countries with high smoking rates.

	Acknowledgments

 
This study was supported by a grant-in-aid of the Ministry of Health and Welfare, 7A-2 and H11-Chouju-046, H14-Chouju-003.

	Footnotes

 
Members of the NIPPON DATA80 Research Group are listed in reference 13.

Received March 24, 2004; accepted April 13, 2004.

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This Article Abstract Full Text (PDF) All Versions of this Article: 35/8/1836    most recent 01.STR.0000131747.84423.74v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ueshima, H. Search for Related Content PubMed PubMed Citation Articles by Ueshima, H. Pubmed/NCBI databases Compound via MeSH Substance via MeSH Hazardous Substances DB CHOLESTEROL Medline Plus Health Information Smoking Stroke Related Collections Behavioral/psychosocial - stroke Cerebrovascular disease/stroke Risk Factors Epidemiology