Original Article
Passive Smoking and the Risk of Coronary Heart Disease — A Meta-Analysis of Epidemiologic Studies
N Engl J Med 1999; 340:920-926March 25, 1999
- Abstract
Background
The effect of passive smoking on the risk of coronary heart disease is controversial. We conducted a meta-analysis of the risk of coronary heart disease associated with passive smoking among nonsmokers.
Methods
We searched the Medline and Dissertation Abstracts Online data bases and reviewed citations in relevant articles to identify 18 epidemiologic (10 cohort and 8 case–control) studies that met prestated inclusion criteria. Information on the designs of the studies, the characteristics of the study subjects, exposure and outcome measures, control for potential confounding factors, and risk estimates was abstracted independently by three investigators using a standardized protocol.
Results
Overall, nonsmokers exposed to environmental smoke had a relative risk of coronary heart disease of 1.25 (95 percent confidence interval, 1.17 to 1.32) as compared with nonsmokers not exposed to smoke. Passive smoking was consistently associated with an increased relative risk of coronary heart disease in cohort studies (relative risk, 1.21; 95 percent confidence interval, 1.14 to 1.30), in case–control studies (relative risk, 1.51; 95 percent confidence interval, 1.26 to 1.81), in men (relative risk, 1.22; 95 percent confidence interval, 1.10 to 1.35), in women (relative risk, 1.24; 95 percent confidence interval, 1.15 to 1.34), and in those exposed to smoking at home (relative risk, 1.17; 95 percent confidence interval, 1.11 to 1.24) or in the workplace (relative risk, 1.11; 95 percent confidence interval, 1.00 to 1.23). A significant dose–response relation was identified, with respective relative risks of 1.23 and 1.31 for nonsmokers who were exposed to the smoke of 1 to 19 cigarettes per day and those who were exposed to the smoke of 20 or more cigarettes per day, as compared with nonsmokers not exposed to smoke (P=0.006 for linear trend).
Conclusions
Passive smoking is associated with a small increase in the risk of coronary heart disease. Given the high prevalence of cigarette smoking, the public health consequences of passive smoking with regard to coronary heart disease may be important.
Media in This Article
Figure 2
Pooled Relative Risks of Coronary Heart Disease Associated with Various Levels of Exposure to Spouse's Smoking among Nonsmokers.Figure 3
Pooled Relative Risks of Coronary Heart Disease Associated with Various Durations of Exposure to Spouse's Smoking among Nonsmokers.Article Activity
- Article
Coronary heart disease is the leading cause of death in the United States and other industrialized countries. In 1995, an estimated 481,287 deaths in the United States resulted from coronary heart disease, representing more than 1 of every 5 deaths.1 In many developing countries, mortality from coronary heart disease has increased rapidly and the disease has become the leading cause of death.2
Active cigarette smoking is one of the most important modifiable risk factors for coronary heart disease.3-5 In the United States, active cigarette smoking results in approximately 100,000 deaths due to coronary heart disease each year.6 Many epidemiologic studies7-25 and reviews26-32 have pointed to the effect of passive smoking on the risk of coronary heart disease. Even so, the extent of the association between passive smoking and coronary heart disease is not fully known. Therefore, we assessed the relation between passive smoking and the risk of coronary heart disease among nonsmokers.
Methods
Selection of Studies
We searched the Medline data base (from January 1966 through June 1998) for literature with the medical subject headings “tobacco smoke pollution,” “coronary disease,” and “myocardial infarction” and the key words “passive smoking” and “environmental tobacco smoke.” The search was restricted to studies of passive smoking in humans. We also conducted a search of abstracts listed in Dissertation Abstracts Online using the key word “passive smoking,” and we performed a manual search of references cited in published original and review articles.26-32 All the potentially relevant manuscripts were independently reviewed by three investigators. Areas of disagreement or uncertainty were adjudicated by the other investigators. Inclusion was restricted to prospective cohort studies and case–control studies in which the relative risk (or relative odds) of coronary heart disease associated with passive smoking was reported.
Three potentially relevant studies were excluded from analysis.25,33,34 The first was a cross-sectional survey.25 The second did not provide valid data on passive smoking, and the case and control groups were not comparable.33 The results of the third study, an analysis of the data from the American Cancer Society Cancer Prevention studies I and II,34 conflicted with the findings of a more careful analysis of the same data conducted by Steenland and colleagues.15
Data Abstraction
All the data were independently abstracted in triplicate by means of a standardized protocol and data-collection form by three investigators, each of whom was unaware of the coding system used by the other two. Disagreements were resolved by discussion. Recorded characteristics of the studies were as follows: first author's name and year of publication, study design (prospective cohort study or case–control study), characteristics of the study subjects (sample size, sampling methods, and distribution according to age, sex, and race), measures of outcome and exposure, duration of follow-up (for prospective cohort studies), confounding factors that were controlled for by matching or adjustment, and the relative risk (or relative odds) of coronary heart disease associated with passive smoking and its standard error, overall and in each subgroup, according to sex and the site of exposure (home or workplace).
Statistical Analysis
Relative risk was used as a measure of the relation between passive smoking and the risk of coronary heart disease. For case–control studies, the relative odds were used as a surrogate measure of the corresponding relative risk. Because the absolute risk of coronary heart disease is low, the relative odds approximate the relative risk. Before data were pooled, relative risks from individual studies were transformed to their natural logarithms, or log (RRi), to stabilize the variances and to normalize the distributions.35 The overall log (RR) was estimated as
log (RR) = Σ wi × log (RRi) ÷ Σ wi
where wi is a weight that consists of the reciprocal of the variance of the log (RRi). The homogeneity of log (RRi) across the k studies was tested by using Woolf's ξ2 statistic36:
ξ2 = Σ wi [log (RRi) – log (RR)]2, with df = k – 1.
The variance of the natural logarithm was derived from the confidence interval provided in the study or was calculated by means of standard formulas.36 Ninety-five percent confidence intervals were approximated by natural-logarithm transformation and were expressed again by natural-antilogarithm transformation of the data. The z statistic was calculated, and a two-tailed P value of less than 0.05 was considered to indicate statistical significance. Linear regression analysis was used to test the dose–response relation between the degree of exposure to smoke (cigarettes per day) and the log relative risk and between the duration of exposure (years) and the log relative risk, with weighting by the reciprocal of its variance.
To estimate the robustness of our findings with respect to different assumptions, we conducted a sensitivity analysis. We used both a fixed-effects model and a random-effects model to calculate the pooled relative risk.37 Because these two approaches yielded virtually identical overall estimates, we present only the results obtained with the fixed-effects model. We also examined the influence of various exclusion criteria on the overall relative risk.
The potential for publication bias was examined by constructing a “funnel plot” in which variance was plotted against log relative risk.38 In addition, the association between variance and standardized log relative risk was analyzed by rank correlation with use of the Kendall tau method. If small studies with negative results were less likely to be published, the correlation between variance and log relative risk would be high; in the absence of publication bias, no significant correlation between variance and log relative risk would be evident.38
Results
We included 10 prospective cohort studies and 8 case–control studies in our meta-analysis. The characteristics of the study subjects and the designs of the cohort studies are presented in Table 1Table 1
Characteristics of 10 Cohort Studies of Passive Smoking and the Risk of Coronary Heart Disease among Nonsmokers.. Of the 10 cohort studies, 8 were conducted in the United States. The number of subjects ranged from 513 in the Evans County Study14 to 479,680 in the American Cancer Society Cancer Prevention Study II.15 Passive exposure to smoking at home was measured in all the cohort studies, but only four measured workplace exposure. In all the cohort studies, the outcome was myocardial infarction or death due to coronary heart disease. The mean follow-up period ranged from 6 to 20 years. The potentially confounding effects of age and sex were controlled for in all the cohort studies, whereas only six controlled for blood pressure or hypertension, body weight or body-mass index, and serum cholesterol level or hyperlipidemia.Most of the eight case–control studies were conducted outside the United States (Table 2Table 2
Characteristics of Eight Case–Control Studies of Passive Smoking and the Risk of Coronary Heart Disease among Nonsmokers.). The number of case subjects enrolled in these studies ranged from 34 to 343, and the corresponding number of control subjects ranged from 68 to 825. In four studies, passive smoking was assessed both at home and in the workplace; in the other four, it was assessed only at home. Matching or adjustment was performed for a variety of potential confounders.Figure 1Figure 1
Relative Risks of Coronary Heart Disease Associated with Passive Smoking among Nonsmokers in 18 Epidemiologic Studies. shows the relative risk (and 95 percent confidence intervals) of coronary heart disease associated with passive smoking in each study and overall. All the relative risks were greater than 1, but only 7 of the 18 were statistically significant. As compared with nonsmokers who were not exposed to smoke, nonsmokers exposed to passive smoking had an overall relative risk of coronary heart disease of 1.25 (95 percent confidence interval, 1.17 to 1.32) (Table 3Table 3
Overall Relative Risk of Coronary Heart Disease Associated with Passive Smoking among Nonsmokers in Studies That Used Different Exclusion Criteria.).This estimate changed very little after studies with different inclusion criteria had been excluded. For example, after the exclusion of an outlier study with an extremely large relative risk,9 the overall relative risk was reduced only slightly, to 1.24. After three studies that were available only as dissertations were excluded,11,19 the overall relative risk did not change. When the analysis was confined to the 14 studies that used myocardial infarction, death due to coronary heart disease, or both as end points, the overall relative risk was 1.24. When the analysis was confined to the 10 studies that adjusted for important risk factors for coronary heart disease, such as age, sex, blood pressure, body weight, and serum cholesterol, the overall relative risk was 1.26.
The relative risk of coronary heart disease increased significantly with exposure to a higher level or a longer duration of passive smoking (Figure 2Figure 2
Pooled Relative Risks of Coronary Heart Disease Associated with Various Levels of Exposure to Spouse's Smoking among Nonsmokers. and Figure 3Figure 3Pooled Relative Risks of Coronary Heart Disease Associated with Various Durations of Exposure to Spouse's Smoking among Nonsmokers.). For example, as compared with nonsmokers who were not exposed to smoke, nonsmokers who were exposed to 1 to 19 cigarettes per day and to 20 or more cigarettes per day had relative risks of coronary heart disease of 1.23 (95 percent confidence interval, 1.13 to 1.34) and 1.31 (95 percent confidence interval, 1.21 to 1.42), respectively (P=0.006 for linear trend). Likewise, as compared with nonsmokers who were not exposed to cigarette smoke, nonsmokers who were exposed to a spouse's smoke for 1 to 9 years, 10 to 19 years, and 20 or more years had relative risks of coronary heart disease of 1.18 (95 percent confidence interval, 0.98 to 1.42), 1.31 (95 percent confidence interval, 1.11 to 1.55), and 1.29 (95 percent confidence interval, 1.16 to 1.43), respectively (P=0.01 for linear trend).A significant increase in the relative risk of coronary heart disease associated with passive smoking was consistently found when the data were analyzed according to the type of study, sex, and place of exposure (Table 4Table 4
Overall Relative Risk of Coronary Heart Disease Associated with Passive Smoking among Nonsmokers, According to the Design of the Study and the Characteristics of the Participants.). The relative risks found in prospective cohort studies were slightly less than the corresponding relative odds found in case–control studies. The relative risks were not significantly different for men and women or for exposure at home and exposure in the workplace.There was no evidence of publication bias in our study. The Kendall tau correlation coefficient for the standard error and the standardized log relative risk was 0.24 (P=0.16) for all 18 studies. When a study with an extreme value was excluded,9 the Kendall tau correlation coefficient for the standard error and the standardized log relative risk was reduced to 0.19 (P=0.28).
Discussion
Passive cigarette smoking is associated with a smaller increase in the relative risk of coronary heart disease than is active cigarette smoking. For example, in the Cancer Prevention Study II, the risk of coronary heart disease was 1.7 times as high among men who smoked as among those who did not (95 percent confidence interval, 1.6 to 1.8); the corresponding increase in risk among women was by a factor of 1.6 (95 percent confidence interval, 1.4 to 1.7).39 In our analysis, the increase in the relative risk of coronary heart disease among passive smokers as compared with nonsmokers was 1.25 (95 percent confidence interval, 1.17 to 1.32). However, because of the high prevalence of passive cigarette smoking at home and in the workplace, a substantial number of coronary events occur, with implications for public health.40
Several studies have suggested that the increased risk of coronary heart disease associated with passive smoking may be due to confounding effects of lifestyle and diet.41,42 Passive smokers were more likely than nonsmokers to consume diets with fewer vegetables and fruits and more fat and were less likely to take antioxidant vitamin supplements.43-46 However, clinical trials have indicated that beta carotene and vitamin E supplementation does not reduce the risk of coronary heart disease in persons who do not have a history of myocardial infarction.47,48 In our analysis, the pooled relative risk of coronary heart disease associated with passive smoking for studies that adjusted for important confounding factors for coronary heart disease (such as age, sex, body weight, blood pressure, and serum cholesterol level) was virtually identical to the pooled relative risk for all the studies. In keeping with our findings, Law and colleagues have suggested that differences in diet between passive smokers and nonsmokers account for only 1 to 3 percent of the difference in their risk of coronary heart disease.31
Our findings are unlikely to be due to misclassification of outcomes. The pooled relative risk for studies in which the end points were myocardial infarction, death due to coronary heart disease, or both was similar to the pooled relative risk for all studies. Likewise, our findings are unlikely to result from publication bias, as was suggested in one report.34 The pooled relative risk for published studies is identical to that obtained by pooling relative-risk estimates for all the available studies, including dissertations. In addition, correlation analysis of the standard error and the log relative risk does not support the possibility of publication bias.
Several mechanisms may increase the risk of coronary heart disease in persons exposed to environmental tobacco smoke. The acute effects of passive smoking include increases in the heart rate at rest, blood pressure, and blood levels of carboxyhemoglobin and carbon monoxide.49,50 Other effects are an increase in the ratio of serum total cholesterol to high-density lipoprotein cholesterol, a decrease in the serum level of high-density lipoprotein cholesterol,50 an increase in platelet aggregation, and endothelial-cell damage.51 Abnormal platelet aggregation is an independent risk factor for coronary heart disease.26,28,29,52 There is also evidence that passive smoking may contribute to atherosclerosis by sensitizing neutrophils, causing their activation and subsequent oxidant-mediated tissue damage.53
According to the Third National Health and Nutrition Examination Survey, about 43 percent of nonsmoking children and 37 percent of nonsmoking adults are exposed to environmental tobacco smoke in the United States.40 The high prevalence of passive smoking in the general population has implications for public health. To achieve a meaningful reduction in the burden to society of coronary heart disease, both passive and active cigarette smoking must be targeted.
Many children are regularly exposed to cigarette smoke at home or in other environments, such as child-care facilities and schools.40 The only safe way to protect nonsmokers from exposure to cigarette smoke is to eliminate this health hazard from public places and workplaces, as well as from the home.
Supported by a Center Development grant (ES06435) from the National Institute of Environmental Health Sciences and by a grant (HL60300) from the National Heart, Lung, and Blood Institute.
Source Information
From the Department of Biostatistics and Epidemiology (J. He, S.V., K.A., M.R.P., J. Hughes, P.K.W.) and the Prevention Research Center (J. He, J. Hughes, P.K.W.), Tulane University School of Public Health and Tropical Medicine, New Orleans.
Address reprint requests to Dr. He at the Department of Biostatistics and Epidemiology, Tulane University School of Public Health and Tropical Medicine, 1430 Tulane Ave., SL18, New Orleans, LA 70112, or at jhe@mailhost.tcs.tulane.edu.
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