FROM AROUND THE WORLD: FOCUS ON CHINA
Combined Effects of Tobacco Smoke Exposure and Metabolic Syndrome on Cardiovascular Risk in Older Residents of China
Yao He, MD, PhD*,*,
Tai Hing Lam, MD||,
Bin Jiang, MD, PhD ,
Jie Wang, MD, PhD ,
Xiaoyong Sai, MD, PhD*,
Li Fan, MD ,
Xiaoying Li, MD,
Yinhe Qin, MD* and
Frank B. Hu, MD, PhD¶
* Institute of Geriatrics, Chinese PLA General Hospital, Beijing, China
Department of Acupuncture, Chinese PLA General Hospital, Beijing, China
Clinic of PLA Communication Department, Beijing, China
Department of Geriatric Cardiology, Chinese PLA General Hospital, Beijing, China
|| School of Public Health and Department of Community Medicine, The University of Hong Kong, Hong Kong, China
¶ Department of Nutrition, Harvard School of Public Health, Boston, Massachusetts
* Reprint requests and correspondence: Dr. Yao He, Institute of Geriatrics, Chinese PLA General Hospital, 28 Fuxing Road, Beijing 100853, China (Email: yhe301{at}x263.net).
Key Words: metabolic syndrome • smoking • second-hand smoke • cardiovascular risk
In the 1996 National Prevalence Survey of Smoking Pattern in mainland China, the prevalence of smoking was 66.9% in men and 4.2% in women; overall, 53.5% reported passive smoke exposure. More than 72% of all Chinese (>600 million people) are regularly exposed to either active smoking or secondhand smoke (SHS) (1). As the world's largest producer and consumer of tobacco products, China bears a substantial burden of smoking-related diseases and deaths (2). It is estimated that tobacco-related deaths will reach 7 million worldwide in 2025, with 2 million of these deaths predicted to occur in China (1,3). Tobacco smoking is a major risk factor for cardiovascular disease (CVD) (4–7) and type 2 diabetes (8,9). Moreover, there is strong evidence that passive smoking or SHS is causally associated with coronary heart disease (CHD) (10–13) and may be linked to stroke (14–16).
The metabolic syndrome (MetS) is characterized by a clustering of cardiovascular risk factors, including abdominal obesity, high blood pressure, increased glucose level, and dyslipidemia. The MetS is associated with the development of diabetes and CVD (17,18) as well as an increased risk of CVD and all-cause mortality (19,20). In China, it has become an important public health problem with the prevalence of MetS being 13.7% in the middle-aged (21) and 46.3% in the elderly (22) populations. There is also evidence that SHS is associated with both MetS and insulin resistance (8,23–28). Although SHS has been examined as a risk factor for individual CVD (CHD or stroke), it has not been investigated together with MetS in the Chinese population. In this study, we examined in detail the individual and combined effects of active smoking, SHS, and MetS on cardiovascular risk in a population-based survey of elderly Chinese in Beijing, China.
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Methods
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Study population.
We conducted a population-based cross-sectional survey of individuals age 60 years or older in the Wanshoulu Community within the Haidian District, a metropolitan area representative of the geographic and economic characteristics of Beijing, China. A 2-stage stratified sampling method was used. First, 9 residential communities (totaling approximately 300 to 600 households each) were selected randomly from a total of 94 residential communities in the Wanshoulu Area. Second, all individuals were chosen from selected streets within these communities, but only 1 participant from each household was invited to enroll in the study. From April 2001 to March 2002, 2,680 people 60 years of age or older were selected and invited for screening. A total of 2,334 subjects (943 men and 1,391 women) completed the survey, yielding a response rate of 87.1%, accounting for 11.4% of the older residents in the Wanshoulu Area. Details of data collection, physical examinations, and other tests have been reported elsewhere (22).
The Committee for Medical Ethics of the Chinese PLA General Hospital approved the study in 2001. Each participant signed an informed consent form before completing the questionnaire.
Active smoking and SHS exposure.
The categories of active smoking were: ever, former, and current smoker. An ever smoker was defined as one who had smoked at least 1 cigarette daily for 1 year or more. Current smokers were ever smokers who were still smoking at the time of the interview, and former smokers were those who had stopped for at least 2 years. Individuals with no history of tobacco smoking were considered never smokers. Pack-years of smoking were calculated by multiplying the average number of cigarettes smoked per day by the number of years of smoking and dividing by 20. SHS exposure was defined as being exposed to another person's tobacco smoke at home or in the workplace for at least 15 min daily more than 1 day per week in the past 10 years (1).
Definitions.
We defined MetS by using the International Diabetes Foundation (IDF) criteria of 2005 (29), which are similar to the modified U.S. National Cholesterol Education Program's Adult Treatment Panel III criteria (30). The IDF definition of MetS includes central obesity (waist circumference  90 cm in Chinese men and 80 cm in Chinese women) plus any 2 of the following 4 factors: 1) high blood pressure: systolic 130 mm Hg, diastolic 85 mm Hg, or known treatment for hypertension; 2) hypertriglyceridemia: fasting plasma triglycerides 1.7 mmol/l; 3) low high-density lipoprotein cholesterol (HDL-C): fasting HDL-C <1.0 mmol/l in men and <1.3 mmol/l in women; and 4) hyperglycemia: fasting glucose level of 5.6 mmol/l (100 mg/dl) or known treatment for diabetes.
Hypertension was defined as diastolic blood pressure of 90 mm Hg, systolic blood pressure of 140 mm Hg, or current medication for hypertension. Coronary heart disease and stroke were defined using the World Health Organization's MONICA (Multinational Monitoring of Trends and Determinants in Cardiovascular Disease) criteria (31). Myocardial infarction was defined by a representative set of electrocardiogram (ECG) changes, cardiac enzyme values, and typical symptoms. Angina was defined as use of nitroglycerin, experience of typical chest pain, or ECG changes compatible with ischemic heart disease. Strokes were defined as events requiring hospitalization and confirmed by local hospital records. CVD was defined by the presence of CHD and/or stroke.
Statistical analysis.
Data were entered (double entry) and managed by Access (Microsoft Corp., Redmond, Washington). The Wald chi-square analysis was used to determine the sex-specific prevalence of MetS by tobacco exposure status. Logistic regression was used to estimate the odds ratios (ORs) and 95% confidence interval (CI) of CVDs with adjustment for age, marital status, years of education, alcohol consumption, hours per day of physical exercise, total cholesterol, and family history of CHD or stroke. Both stratified analyses and multiple logistic regression analyses were used to examine the independent and combined effects of the tobacco exposure and MetS. Interaction between tobacco exposure groups and MetS status was investigated by adding interaction terms (tobacco exposure status multiplied by MetS status) to the logistic regression model using the likelihood ratio test. The statistical package used was SPSS (version 14.0, SPSS Inc., Chicago, Illinois).
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Results
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Among the study participants, there were 784 CHD patients, including 68 with myocardial infarction and 716 with stable angina. Among participants with CHD, 58% of the cases were confirmed by exercise test or B ultra-sound heart image. There were 378 cases of stroke (248 ischemic, 70 hemorrhagic, and 60 other types), and 83% of these events were confirmed by computed tomography and magnetic resonance imaging.
On the basis of the general characteristics of study participants, we found significant differences between men and women (Table 1). The prevalence of ever smoking was much greater in men (58.1%) than in women (13.1%), but SHS exposure was more likely in women (42.3% vs. 19.9%). On the basis of IDF criteria, MetS was present in 34.8% of men and 54.1% of women. Compared with never smokers without exposure to SHS, the prevalence of individual MetS components and MetS was greater in male active smokers as well as in female active and passive smokers, particularly, for low HDL-C and central obesity (Table 2).
Compared with never smokers without MetS, men with MetS had significantly greater risk of CVD among never (OR: 1.83; 95% CI: 1.17 to 2.86), former (OR: 2.24; 95% CI: 1.39 to 3.63), and current smokers (OR: 3.54; 95% CI: 2.03 to 6.18) (Table 3). Among the subjects with MetS, if current smokers were used as the reference, the ORs of CVD were 0.63 (95% CI: 0.34 to 0.99) for former smokers and 0.53 (95% CI: 0.28 to 0.94) for never smokers, suggesting that smoking cessation reduces CVD risk by approximately 37% in male smokers with MetS. The ORs of CHD and stroke in current smokers with MetS were the highest among the 6 groups and were 4.57 (95% CI: 2.57 to 8.12) for CHD and 2.41 (95% CI: 1.24 to 4.38) for stroke. Multivariate logistic models showed no significant interaction between active smoking (never/former/current) and MetS on CHD, stroke, and CVD (p = 0.69, p = 0.74, and p = 0.57, respectively). In contrast, no association between active smoking and CVD risk was found in women, probably the result of the small number of active smoking women.
There was a clear dose-response relationship between smoking consumption (pack-years) and the adjusted ORs of CHD and CVD in all 943 men with or without MetS (Table 4, Fig. 1). The test for trend was significant for CHD and CVD but not for stroke.
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Figure 1 Dose-Response Relation Between Smoking Consumption and Adjusted ORs of CHD, Stroke, and CVD in Men With or Without MetS
Blue diamonds = without metabolic syndrome (MetS); open squares = with MetS. CHD = coronary heart disease; CVD = cardiovascular disease; OR = odds ratio.
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Among never smokers (397 men and 1,209 women), the ORs of CHD, stroke, and CVD with SHS in men were not significantly different based on MetS status (Table 5). However, in women, SHS was associated with CHD, stroke, and CVD in subjects with or without MetS. Compared with those without passive smoke exposure and without MetS, the adjusted OR of CVD was 1.74 (95% CI: 1.27 to 2.38) in those with MetS only, 1.72 (95% CI: 1.20 to 2.47) in those exposed to SHS only, and 2.91 (95% CI: 2.03 to 4.16) for those with MetS and exposure to passive smoke. The interaction terms between SHS and MetS for CHD, stroke, and CVD were not statistically significant (p = 0.66, p = 0.99, and p = 0.66, respectively).
Odds ratios were determined for CHD, stroke, and CVD by tobacco exposure status (non-SHS in the never smokers, SHS in the never smokers, and active smoking regardless of SHS) and MetS status (Table 6). Compared with never smokers without MetS and SHS, the exposure to SHS in women, active smoking in men, and MetS in both men and women were associated with increased risk of CVD. Those with MetS and exposure to tobacco smoke (passive or active) had greater risks of CHD, stroke, and CVD than those exposed to tobacco smoke but without MetS. For example, the ORs of CHD were 2.94 in the female passive smokers with MetS versus 1.73 in females with exposure to tobacco smoke but without MetS. Among men, the OR of CHD was 3.18 for active smokers with MetS versus 1.57 for men exposed to SHS without MetS. Additionally, the ORs of CHD, stroke, and CVD in the active female smokers with MetS were 1.75 (95% CI: 1.07 to 2.88), 3.11 (95% CI: 1.78 to 5.32), and 2.12 (95% CI: 1.34 to 3.48), respectively.
The p values for the interaction analysis can be seen in Tables 3 and 5. There was no significant interaction between active smoking and MetS among the men or of passive smoking and MetS in men and women. However, there was a significant positive interaction between active smoking and MetS on CHD, stroke, and CVD among the women in this study (p = 0.005, p = 0.002, and p = 0.001, respectively) (Table 3).
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Discussion
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To the best of our knowledge, this is the first study to report the joint effects of tobacco smoke exposure and metabolic syndrome on cardiovascular risk in a population-based study in China. We focused on Chinese men and women age 60 years or older, a group at higher risk of developing CVD. The sample was randomly selected from a cluster sample of similar residential communities and the response fraction was relatively high, with only approximately 13% of eligible subjects having moved or otherwise failed to complete the interviews or examinations. However, there were no statistically significant differences in the characteristics between the responders and nonresponders. Hence, the prevalence of CVD and associated risk factors can be generalized to similar populations in urban Beijing.
In the present study, MetS was associated with CHD and stroke, which is consistent with previous findings (17–20,32). Furthermore, active smoking in men and exposure to SHS in women were strongly associated with increased CVD risk independent of MetS. There was a dose-response relationship between pack-years of active smoking and CVD among men and this difference was evident regardless of MetS status. Subjects with MetS exposed to tobacco smoke (active or passive) had greatly increased CVD risk by 48% to 193% compared with never smokers without MetS and without exposure to SHS. It is likely that smoking cessation could substantially reduce the risk of CVD in smokers with MetS.
We found no significant interaction between active smoking and MetS in relation to CVD in men and no significant interaction between passive smoking and MetS in men and women. Thus, the effects of tobacco smoke exposure and MetS on the risk of cardiovascular outcomes appear to be additive in the present study. The significant interaction between active smoking and MetS in relation to the risk of CVD in women suggests a synergistic effect, but this could be a chance finding due to a very low smoking prevalence and fewer CVD events among women.
Our results are consistent with several recent studies showing that smoking chronically induces insulin resistance, with a dose-response relationship between the number of cigarettes smoked and the degree of insulin resistance and metabolic abnormalities (28,33). There is evidence that smoking cessation improves insulin sensitivity (34) whereas passive smoking reduces insulin sensitivity (35) and increases risk of MetS (27). Because both tobacco smoke and MetS are independently associated with insulin resistance and because insulin resistance may contribute to accelerated atherosclerosis, these 2 risk factors may be linked through this common pathophysiology to increased risk of CVD.
In the past 30 years, the prevalence of traditional risk factors for CVD (i.e., cigarette smoking, dyslipidemia, and hypertension) has gradually declined in the U.S., with smoking prevalence decreasing from 50% in 1960 to about 23% in 2000. However, during this same period, the prevalence of obesity and MetS has increased dramatically in the U.S. (36). In China, smoking rates remain high (1) and cessation rates low (9.5% of all ever smokers have quit) (37), whereas being overweight and MetS are rapidly increasing with changes in lifestyle (e.g., excessive caloric intake and lack of physical activity) (21,22). It is likely that the growing double epidemics of smoking and MetS in China will greatly and rapidly increase the burden of CVD from traditional risk factors (such as smoking, SHS, hypertension) acting together with new risk factors (obesity, MetS, and diabetes).
Considering that both tobacco use and MetS are the 2 leading causes of preventable death in China, our findings have important public health implications. Our results emphasize that public health policies are needed to control smoking, SHS, and MetS. In terms of the implications for clinical practice, smokers or those exposed to passive smoke with MetS have very high CVD risk and should be targeted for intensive interventions.
Study limitations.
The present study has several limitations. The cross-sectional nature of the data limits causal inferences. The underreporting of smoking, including history of self-reported active and passive smoking, could also bias the association between smoking and CVD towards null. The data on smoking status should not have been affected by differential reporting bias in CVD cases versus noncases because they were collected before physical examination or the diseases defined by hospitalization.
The relatively low prevalence of SHS exposure (42.3%) in women could be attributable to 2 reasons. First, the prevalence of current smoking in elderly men in our study was much lower (24.7%) than that in the general population (1), thus reducing the exposure to SHS in women in close contact to elderly men. Second, exposure to SHS was restricted to passive smoking in the past 10 years to minimize recall error, but this means fewer opportunities to be exposed to SHS during this limited time period compared with women in the general population who may have had considerable exposure to SHS earlier than the 10-year period analyzed in this study.
To reduce the bias of "ill quitter effect," former smokers were defined as those who had stopped smoking for at least 2 years. Furthermore, the pattern of smoking cessation in our subjects is consistent with other Chinese data (37,38). Some subjects could have died young from smoking- or other CVD-related risk factors before the survey, making our participants the survivors. It is likely that the effects of smoking and MetS on CVD are stronger in younger people than in older individuals. Additionally, limiting SHS to a 10-year period might explain in part the lower prevalence (19.9%) of SHS in these older men; they are likely retired and have few opportunities for work-related SHS exposure. Similarly, because of the low prevalence of current smoking among women, the men in our study were less likely to be exposed to SHS in the home. This may explain why we didn't find a significant association of SHS and CVD in men. We observed no significant association between active smoking and risks of CVD in women probably due to their low prevalence of active smoking among women.
When considering all these factors as well as the potential for misclassification in ascertaining SHS exposure, the relationship between tobacco smoke exposure (especially SHS), MetS, and CVD is likely to be underestimated in our study. Finally, because of small numbers of former smokers and the lack of detailed information about the duration of SHS, a dose-response relationship of duration of quitting in men and the quantity of SHS exposure in women could not be analyzed.
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Conclusions
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Our study shows that cigarette smoking in men and SHS exposure in women are highly prevalent in elderly Chinese. Tobacco smoke exposure (including active and passive smoking) increased the prevalence of CHD, stroke, and CVD in the subjects with or without MetS after adjusting for other CVD risk factors. These findings collectively suggest that cigarette smoking and SHS, 2 modifiable risk factors, are strongly associated with increased CVD independent of MetS. The growing double epidemics of MetS and tobacco smoke exposure (both active smoking and SHS) will dramatically increase the risk of CVD in the Chinese population.
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Footnotes
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Please note: This study is supported by research grants from the National Natural Science Foundation of China (30671809, 30771859), Beijing Natural Science Foundation (7062063) and the Ministry of Health of China (06H050), Beijing Medical Scientific Development Foundation (2007-2039), and the Ministry of Science and Technology of China (2006BAI01A01). Dr. He was partly supported by the Cheng Yu Tung and Gordon Wu Exchange Professorship in the Faculty of Medicine at the University of Hong Kong.
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