IJE Advance Access originally published online on September 10, 2007
International Journal of Epidemiology 2007 36(5):1060-1067; doi:10.1093/ije/dym169
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Is weak association between cigarette smoking and cardiovascular disease mortality observed in Japan explained by low total cholesterol?—NIPPON DATA80
1Department of Health Science, Shiga University of Medical Science, Shiga, Japan.
2Department of Hygiene and Preventive Medicine, Fukushima Medical University, Fukushima, Japan.
3Cardiovascular Epidemiology, Faculty of Home Economics, Kyoto Women's University, Kyoto, Japan.
4Department of Preventive Cardiology, National Cardiovascular Center, Osaka, Japan.
* Corresponding author. Department of Health Science, Shiga University of Medical Science, SetaTsukinowa –cho, Otsu 520-2192, Shiga, Japan. E-mail: ahozawa{at}belle.shiga-med.ac.jp
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Abstract |
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Background An international comparison has indicated that the association between smoking and cardiovascular disease (CVD) differs according to total cholesterol (TC) levels. However, little has been published about the relationship between smoking and CVD mortality among populations with various cholesterol levels.
Methods We calculated the adjusted relative hazard (RH) of smoking for CVD mortality among 8912 Japanese individuals without a history of stroke or heart disease, who were separated according to TC levels of 
5.40, 4.81–5.39, 4.26–4.80 and <4.25 mmol/l into groups Q4, Q3, Q2 and Q1, respectively. The P-values for multiple interactions between TC and smoking status for CVD mortality were calculated using TC as a continuous variable, dichotomized smoking status (never vs current), and by including cross-product terms in the regression models.
Results After 19 years of follow-up, 313 men and 291 women died of CVD. The RH of CVD mortality among men who currently smoked compared with those who never smoked was increased with higher TC (RH = 2.36 in Q4) and decreased in those with lower TC (RH = 0.85 in Q1) (interaction, P < 0.01). The profiles for coronary heart disease (CHD) mortality and ischaemic CVD (composite endpoint of CHD and ischaemic stroke) in men and for ischaemic CVD mortality in women were identical. The interaction might be explained by a biological mechanism and by frailty of those who have never smoked with lower TC.
Conclusions Counteractive measures should be implemented against smoking targeted towards Japanese with elevated TC levels.
Keywords Cigarette smoking, total cholesterol, cardiovascular diseases, interaction, prospective studies, Japan
Accepted 24 July 2007
Cigarette smoking is a known risk factor for both coronary heart disease (CHD) and stroke.1 However, although the rate of cigarette smoking is high among Japanese men, mortality from ischaemic heart disease is strikingly lower than that in the USA.2,3 Smoking is thus considered a weaker CHD risk factor in Japan than in Western countries.4,5 However, cigarette smoking is closely related to CHD among Japanese immigrants living in Hawaii.4 Thus, the between-population difference in CHD might be explained not by ethnicity but by environmental factors. Similar to Japan, the Seven Countries Study showed a weaker relationship between smoking and the incidence of CHD in southern Europe than in Northern Europe and Yugoslavia.6 People living in Asia and in southern Europe at the time of the early follow up by the Seven Countries Study had low average total cholesterol (TC) levels.4–6 Furthermore, some recent studies investigating the aetiology of subclinical atherosclerosis found that low-density lipoprotein cholesterol is more important for early atheroma formation, whereas smoking plays a more important role at the later stages of atherosclerosis.7,8
Japanese studies reported before 2000 indicated that cigarette smoking is not a consistent risk factor for stroke.9–11 However, recent analyses have revealed a close relationship between cigarette smoking and stroke in Japan.12–15 Some investigators have postulated that this change is due to a recent increase in dietary fat intake and a relative increase of the blood TC level in the general population.3,13 Thus, the association between smoking and cardiovascular diseases (CVD) might differ according to TC level. The aim of the present study was to determine whether TC level affects the association between smoking and CVD using a representative Japanese sample.
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Methods |
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The subjects of this cohort study participated in the Japanese 1980 National Cardiovascular Survey, which was conducted together with a National Nutrition Survey. Nutrition is surveyed annually in Japan using standardized procedures and a questionnaire.13,16 All household members aged 30 years or older in 300 randomly selected census tracts throughout Japan are included. The 1980 survey included medical examinations, blood pressure (BP) measurements, blood tests and a self-administered questionnaire about lifestyle. Trained staff at local health centres in the respective districts performed the medical examinations at local health and community centres. A history of illness, including heart disease, stroke and diabetes, as well as smoking and drinking habits was obtained from the questionnaire. Height and body weight were measured, while the subjects wore light clothing and no shoes. The participants were questioned about whether they were current smokers, ex-smokers or had never smoked. Smokers were asked to describe the number of cigarettes smoked per day. Similarly, alcohol consumption was determined as never, past, current occasionally or current daily. A standard sphygmomanometer was used to measure systolic and diastolic BP. The precision and accuracy of serum TC in non-fasting blood samples were verified by the Lipid Standardization Program administered by the Center for Disease Control and Prevention, Atlanta, GA, USA.17 Diabetes was defined as non-fasting serum glucose of 11.1 mmol/l (200 mg/dl) or a self-reported history of diabetes.
A total of 10 546 individuals, aged 30 years or older, for whom baseline information regarding age, gender and blood pressure was complete in the 1980 data set constituted the study cohort (NIPPON DATA80).13,16 We excluded those with a history of stroke (n = 117), CHD (n = 163), other heart disease (n = 475), no information about confounding factors (n = 4), those without complete information about smoking or TC (n = 28) and 847 participants who were lost to follow-up. Consequently, we analysed data from 8912 participants.
As described elsewhere,12,15 the underlying causes of death in the Japanese National Vital Statistics were coded according to the 9th (ICD-9) and 10th (ICD-10) International Classifications of Disease for deaths through 1994 and thereafter, respectively. Details about the classification and permission to use the National Vital Statistics were obtained from the Management and Coordination Agency of the Government of Japan. The Institutional Review Board of the Shiga University of Medical Science approved the study protocol (No. 12–18, 2000).
Statistical analysis
To examine the association between cigarette smoking and CVD mortality according to TC level, participants were divided into quartiles Q4, Q3, Q2 and Q1 according to TC levels of 5.40 mmol/l (209 mg/dl), 4.81–5.39 mmol/l (186–208 mg/dl), 4.26–4.80 mmol/l (165–185 mg/dl) and Q1 (TC, <4.25 mmol/l (<164 mg/dl). We compared the basic characteristics among the groups according to a combination of smoking and TC levels using the mean for continuous variables and ratios (%) for dichotomous variables.
Age-adjusted CVD mortality rate, relative hazards (RH) and the 95% confidence intervals (95%CI) for cigarette smoking was estimated according to TC level using the Cox proportional hazard model. Individuals who had never smoked were categorized as the reference group. We estimated the RH using age-adjusted and multivariate-adjusted models, and included the following possible confounding factors in the latter model: age, body mass index (BMI), systolic BP, use of anti-hypertensive medication, diabetes and alcohol consumption (never, past, occasional and daily). The significance of multiplicative interactions between TC (continuous) and smoking status were examined using cross-product terms in the regression model. The interaction was assessed for CVD mortality, CHD mortality, ischaemic stroke mortality and ischaemic CVD (composite endpoint of CHD and ischaemic stroke) mortality. We also separately analysed the relationship between smoking and CVD or ischaemic CVD mortality according to cholesterol level by age group (
69 and >69 years, as the median age of the deceased was 69 years). SAS software (version 9.1) was used for all statistical analyses.
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Results |
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The mean ± SD baseline age of the participants was 50.1 ± 13.1 years and 55.5% were women. The mean TC level was 4.81 ± 0.85 mmol/l (186.2 ± 32.8 mg/dl) for men and 4.91 ± 0.88 mmol/l (190.2 ± 33.9 mg/dl) for women. Proportions of current smokers, ex-smokers and never smokers were 63.7, 18.1 and 18.2% for men and 8.8, 2.1 and 89.2% for women, respectively.
Table 1 shows the baseline characteristics of the study participants according to smoking status and TC level. Proportions of current smokers across ascending TC groups were 68.8, 65.6, 62.0 and 57.6% for men and 7.7, 8.6, 9.3 and 9.3% for women in Q1, Q2, Q3, and Q4, respectively. The mean BMI and systolic BP were higher in groups of both men and women with higher TC. Similarly, the proportion of participants taking anti-hypertensive medication was higher in the groups with higher TC. The mean age of the women was higher in the higher TC group, but this did not apparently differ among the men. Compared with current smokers and those who had never smoked, ex-smokers tended to be older and more of them were taking anti-hypertensive medication and had diabetes. The proportions of those who had never consumed alcohol were higher among those who had never smoked.
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After 19 years of follow-up, 313 men and 291 women died of CVD. Table 2 shows the risk of CVD mortality associated with cigarette smoking according to TC levels. The adjusted RH of current cigarette smoking for CVD mortality among men was the highest in Q4 (RH = 2.36; 95%CI: 1.14–4.87) and the lowest in Q1 (RH = 0.85; 95%CI: 0.49–1.49). The P-value for interactions between smoking status (ever vs never) and TC level (continuous) for CVD mortality were 0.01. This interaction was also unchanged, when we excluded ex-smokers (P for interaction <0.01). Table 2 indicates that the findings for women were inconsistent.
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Because the higher CVD mortality rate in those who had never smoked with lower TC was due to frailty, we further excluded early death that occurred within 5 years. However, the observed significant interactions were unchanged (P for interaction, 0.02).
Disease-specific analyses revealed that the P-values for interactions between smoking status and total cholesterol were 0.03 for CHD deaths and 0.01 for ischaemic CVD (CHD + ischaemic stroke) in men (Table 3). Although an interaction between smoking status and TC for total CVD mortality was not apparent in women, the relationship between cholesterol and ischaemic CVD was closer in smokers than in non-smokers among women (P for interaction, 0.02 for ischaemic CVD).
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Because the age distribution differed by TC categories in women, we analysed interactions between smoking and cholesterol for CVD or ischaemic CVD separately by age group (
69 and >69 years). For most of the age-specific analyses except the relationship between smoking and CVD mortality according to TC level in women aged >69 years, the relationship of TC with diseases was also closer in current smokers than in those who had never smoked (data not shown). |
Discussion |
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The present study found that the relationship between cigarette smoking and CVD mortality is affected by TC level in men. This pattern was also observed for CHD mortality and ischaemic CVD in men and for ischaemic CVD mortality in women. The strengths of our study are that we used a representative Japanese population from a national survey, as well as a validated and standardized TC measurement.
Several possibilities could explain the interaction. From a biological viewpoint, the findings that the association of smoking with ischaemic CVD is closer among individuals with higher, than with lower TC, were consistent with those of recent studies indicating that smoking is associated more closely with advanced, than with early, subclinical atherosclerosis.7,8 In both the Atherosclerosis Risk in Communities (ARIC) study and in the Multiethnic Study of Atherosclerosis, Sharrett et al. showed that smoking was more closely associated with severe atherosclerosis (lower extremity artery disease or severe carotid artery intimal medial thickness, IMT) than with moderate IMT, and that low density lipoprotein cholesterol (LDL-C) was a more important determinant than smoking of the earliest ultrasound-detectable stage of atherosclerosis. A study of young adults similarly found that the determinants of carotid IMT were only lifetime LDL-C and (inversely) high density lipoprotein cholesterol (HDL-C), but not smoking pack-years or diabetes.18 Thus, the impact of smoking could be higher in those with high TC and lower in those with low TC. The second possibility is that higher CVD mortality among those who never smoked with lower TC explains the interaction. Although men with lower TC who had never smoked had a preferable CVD risk factor profile, they had a higher age-adjusted CVD mortality rate. We considered two explanations for this. One is that the risk of haemorrhagic stroke mortality is higher in men who had never smoked with low TC. Haemorrhagic stroke is not atheromatous, and is affected by hypertension but not by serum TC. Furthermore, some epidemiological studies suggested that lower TC is associated with higher haemorrhagic stroke risk19. Thus, haemorrhagic stroke might increase the CVD risk. However, the higher CVD mortality rates in men with lower TC who had never smoked persisted even when CHD or ischaemic CVD were the endpoints. Another explanation for the higher CVD mortality rate in the subgroup of non-smokers with low TC might be personal characteristics. Most Japanese men, especially the elderly, have smoked cigarettes at some point during their lives. For example, almost 80% (77.5%) of men aged 20 years smoked in 1970,20 and the remainder of those who had never smoked might have some degree of frailty. Although the exclusion of early death that occurred within 5 years did not alter the interaction, some residual confounding might have remained. For example, some might have had respiratory conditions before starting to smoke, such as tuberculosis or childhood asthma. Participants with poor nutrition, irrespective of symptoms, might have a higher CVD risk. Since information on history of respiratory diseases was unavailable, we could not determine the validity of this speculation. Unknown confounding factors might also exist that could explain the higher mortality in never smoked with lower TC. Further studies are required to understand the relationship between TC and CVD among Japanese who have never smoked. Regardless, both biological mechanisms and personal characteristics in men with lower TC who had never smoked might explain the interaction.
Our findings are consistent with recent changes in the relationship between smoking and CVD in Japan.2,13 In the two Japanese cohorts (Tanushimaru and Ushibuka) in the Seven Countries Study, which collected baseline data between 1957 and 1964 and followed participants for 25 years, excess CHD or stroke-associated mortality8 did not significantly differ among smokers and non-smokers. Although most prospective studies have found a significant relationship between smoking and CHD,10,13,14 older studies did not find a significantly increased multiple-adjusted risk of stroke among smokers.9–11 However, recent studies, in which TC levels are higher, have established a significant and closer relationship between cigarette smoking and stroke, especially ischaemic stroke.12-15 Thus, our findings appear to be relevant and are also supported by several other epidemiological studies. The Hisayama study found that the relative risk of smoking for CHD was obviously greater among those with high, than low, TC.10 However, they did not formally test the effect-modification. A recent finding from the ARIC study also revealed a modest but significant interaction between smoking and LDL-C for CHD incidence.21 However, two large Korean studies (with shorter follow-ups) and a US study found that lower serum TC levels did not modify the risk relationship between smoking and CVD.5,22,23
One of the limitations of this study is the use of mortality data. Lower-quality nutrition might determine early death after CVD events. Thus, the risk of TC might have been underestimated. Another limitation is the low mortality rate, especially among men who had never smoked and among women who current smoked. Our findings should be substantiated by longer studies of larger cohorts using CVD incidence data.
Mean levels of TC in Japan are rapidly increasing in Japan.2 The National Nutrition Survey in Japan conducted in 2000 reported that the mean level of TC in Japan is 5.16 mmol/l (199.7 mg/dl) for men and 5.36 mmol/l (207.5 mg/dl) for women.24 The prevalence of cholesterol values of 6.22 mmol/l (240 mg/dl) in the 2000 survey (12.0% for men and 17.4% for women) was double that found in an identical national survey in 1980, which was the source of our cohort data (6.1% for men and 8.5% for women).24 In the same report in 2000, although the prevalence of current cigarette smoking was <50% overall (45.6% for men and 10.5% for women), it was higher among younger populations (56.8% and 55.0% in men aged 30–39 and 40–49 years, respectively; 18.5 and 13.7% in women aged 30–39 and 40–49 years).22 Thus, the impact and contribution of smoking or TC to CVD mortality, especially ischaemic CVD in Japan could increase.
In conclusion, we found that powerful effect modifications between smoking and TC for CVD mortality among Japanese men. This pattern was also observed for CHD mortality and ischaemic CVD in men and for ischaemic CVD mortality in women. Thus, the weak association of cigarette smoking with CVD mortality in Japan may be partly explained by a lower TC level. Since TC is increasing among Japanese, especially among younger men who often smoke,25 greater efforts to reduce smoking are warranted in Japan and in other Asian countries.
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Appendix |
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List of the NIPPON DATA 80 Research Group.
NIPPON DATA80: "National Integrated Project for Prospective Observation of Non-communicable Disease And its Trends in the Aged."
Chairman: Hirotsugu Ueshima (Department of Health Science, Shiga University of Medical Science, Otsu, Shiga).
Consultant: Osamu Iimura (Hokkaido JR Sapporo Hospital, Sapporo, Hokkaido), Teruo Omae (Health C&C Center, Hisayama, Kasuya, Fukuoka), Kazuo Ueda (Murakami Memorial Hospital, Nakatsu, Oita), Hiroshi Yanagawa (Saitama Prefectural University, Koshigaya, Saitama), Hiroshi Horibe (Aichi Medical University, Nagakute, Aichi).
Participating Researchers: Akira Okayama (The First Institute of Health Service, Japan Anti-Tuberculosis Association, Chyioda-ku, Tokyo), Kazunori Kodama, Fumiyoshi Kasagi (Department of Epidemiology, Radiation Effects Research Foundation, Hiroshima, Hiroshima), Tomonori Okamura, Yoshikuni Kita (Department of Health Science, Shiga University of Medical Science, Otsu, Shiga), Takehito Hayakawa (Department of Hygiene and Preventive Medicine, Fukushima Medical University, Fukushima, Fukushima), Shinichi Tanihara (Department of Hygiene and Preventive Medicine, Fukuoka University School of Medicine, Fukuoka, Fukuoka), Shigeyuki Saito (Second Department of Internal Medicine, Sapporo Medical University School of Medicine, Sapporo, Hokkaido), Kiyomi Sakata (Department of Hygiene and Preventive Medicine, Iwate Medical University School of Medicine, Morioka, Iwate), Yosikazu Nakamura (Department of Public Health, Jichi Medical University School of Medicine, Shimotsuke, Tochigi), Fumihiko Kakuno (Higashiomi Public Health Center, Higashiomi, Shiga).
Participating Research Associates: Toshihiro Takeuchi, Mitsuru Hasebe, Fumitsugu Kusano, Takahisa Kawamoto and members of 300 Public Health Centers in Japan, Masumi Minowa (Faculty of Humanities, Seitoku University, Matsudo, Chiba), Minoru Iida (Kansai University of Welfare Sciences, Kashiwara, Osaka), Tsutomu Hashimoto (Kinugasa General Hospital, Yokosuka, Kanagawa), Shigemichi Tanaka (Department of Cardiology, Cardiovascular Center, Teine Keijinkai, Sapporo, Hokkaido), Atsushi Terao (Health Promotion Division, Department of Public Health and Welfare, Shiga Prefecture, Otsu, Shiga), Katsuhiko Kawaminami (Department of Public Health Policy, National Institute of Public Health, Wako, Saitama), Koryo Sawai (The Japanese Association for Cerebro-cardiovascular Disease Control, Tokyo), Shigeo Shibata (Clinical Nutrition, Kagawa Nutrition University, Sakado, Saitama).
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Acknowledgements |
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This study was supported by a Grant-in-Aid from the Ministry of Health and Welfare, under the auspices of the Japanese Association for Cerebro-cardiovascular Disease Control, a Research Grant for Cardiovascular Diseases (7A-2) from the Ministry of Health, Labour and Welfare and a Health and Labour Sciences Research Grant, Japan (Comprehensive Research on Aging and Health: H11-chouju-046, H14-chouju-003, and H17,18-chouju-012). The authors thank all members of Japanese Association of Public Health Center, Directors and all staffs of the public health centres that cooperated with our study. The authors also would like to thank Professor Aaron R Folsom for his valuable comments on this article.
Conflict of interest: None declared.
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Notes |
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Members of the NIPPON DATA Research Group are listed in the Appendix. 
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References |
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