Affiliation of authors: Epidemiology and Surveillance Research, American Cancer Society, Atlanta, GA
Correspondence to: Jane Henley, MSPH, Epidemiology and Surveillance Research, American Cancer Society, 1599 Clifton Rd., NE, Atlanta, GA 30329 (e-mail: jane.henley{at}cancer.org)
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ABSTRACT |
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INTRODUCTION |
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The prevalence of pipe smoking among adult men in the United States has decreased from 14.1% in 1965 to 2.0% in 1991 (4), and pipe smoking remains rare among U.S. women (<0.1% in 1991) (4). The prevalence of pipe smoking is highest among men aged 45 or older and in the Midwest (4). Pipes are commonly used by some populations, including American Indians (male prevalence = 6.9% in 1991) (5) and by both men and women in parts of China (20% prevalence in 1996) (6). The National Youth Tobacco Survey has measured prevalence of pipe smoking among U.S. youth since 1999. The prevalence of current pipe smoking has increased from 2.4% to 3.5% of middle school students and from 2.8% to 3.2% of high school students from 1999 to 2002; prevalence was higher among boys than girls and varied by state and ethnicity (7,8).
Exclusive pipe smoking has been positively associated with tobacco-related diseases in prospective (912) and casecontrol studies (1323). The cohorts have contributed greatly to the epidemiologic evidence on tobacco and disease and include the HammondHorn nine-state study (9), the U.S. Veterans study (10), a sample of the Swedish population (11), and the Norwegian Cardiovascular Study (12). However, these studies have generally reported wide confidence intervals for the relative risk (RR) estimates associated with exclusive pipe smoking and have not been able to stratify by pipe smoking characteristics such as amount or duration because of small sample size. Casecontrol studies generally have not distinguished between current and former pipe smoking and present results for "ever" pipe smokers. Most published studies, especially prospective studies, have adjusted only for age and have not considered potentially important covariates such as socioeconomic status and alcohol use.
To provide a more precise estimate of the risks associated with pipe smoking, we analyzed data on a large number of exclusive pipe smokers (both current and former) from the Cancer Prevention Study II (CPS-II), an American Cancer Society prospective cohort study. We analyzed the risks of nine cancers known to be associated with tobacco as well as several other tobacco-related diseases, adjusting for potential confounding factors.
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SUBJECTS AND METHODS |
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Information on pipe smoking was based on questionnaire responses in 1982 and was not updated during the follow-up. Men were asked "Do you now or have you ever smoked cigarettes, cigars or pipes at least one a day for one years time?" Current and former pipe smoking habits were assessed by asking the number of pipes smoked a day, age at which pipe smoking began, total years of pipe smoking, and depth of inhalation of pipe smoking. Former pipe smokers were asked their age at smoking cessation. Men were also asked about the use of smokeless tobacco (chewing tobacco and snuff). Users of cigarettes, cigars, or smokeless tobacco were excluded from this analysis. Women could not be included in this analysis because they were not asked whether they smoked pipes.
The vital status and cause of death of participants in CPS-II have been ascertained biennially since the month of enrollment by two methods: until 1988, via personal inquiries from ACS volunteers in September 1984, 1986, and 1988, with reported deaths verified by death certificate; since 1988, through automated linkage with the National Death Index (NDI) (27). As of December 31, 2000, 34.6% of men had died, 65.2% were still living, and 0.2% had follow-up censored on September 1, 1988, because of insufficient data for linkage with the NDI. Death certificates or multiple cause-of-death codes were obtained for 98.9% of all deaths. The underlying cause of death was coded according to the International Classification of Diseases, Ninth Revision (ICD-9) (28).
Person-years at risk were accrued from month of enrollment through the end of follow-up (December 31, 2000), the date of death, or the date lost to follow-up (because of insufficient information for NDI linkage), whichever occurred first. Age-standardized death rates were directly standardized to the age distribution of person-years among CPS-II men during the 18 years of follow-up (29).
For the purpose of this study, we restricted the cohort to the 138 307 men who reported either exclusive use of pipes (n = 15 263) or never use of any tobacco product (n = 123 044). We examined both all-cause mortality and cause-specific mortality for diseases related to cigarette smoking (30,31). The causes of interest included several cancers (lung, oropharynx, esophagus, larynx, stomach, colorectal, pancreas, bladder, and kidney), cardiovascular disease (coronary heart disease and stroke), and chronic obstructive pulmonary disease. Men who reported prevalent disease at enrollment in 1982 were excluded as follows: analyses of cancer mortality excluded men who reported any prevalent cancer except nonmelanoma skin cancer; analysis of coronary heart disease mortality excluded men who reported prevalent heart disease or diabetes; analysis of cerebrovascular disease mortality excluded men who reported prevalent stroke; and analysis of chronic obstructive pulmonary disease mortality excluded men who reported prevalent chronic bronchitis or emphysema. The analysis of all-cause mortality excluded men who reported a history of any of these diseases at enrollment.
Statistical Analysis
We used Cox proportional hazards models to estimate hazard ratios and 95% confidence intervals for mortality associated with pipe smoking and to adjust for other potential risk factors reported at baseline (32). We assessed the appropriateness of the Cox proportional hazards model for each cause of death by plotting log(log) survival curves against survival time. The log(log) survival curves were essentially parallel, suggesting that the proportional hazards assumption was met. All statistical tests were two-sided; hazard ratios were considered statistically significantly elevated if the lower limit of the 95% confidence interval was greater than 1.0, and P values less than .05 were considered statistically significant. Indicator variables were used for all independent variables. All models were adjusted for single year of age by stratification. Multivariable Cox proportional hazards models were adjusted for current alcohol consumption (none, <1 drink daily, 1 drink daily, 23 drinks daily, 4 or more drinks daily, and unquantifiable use), educational level (less than high school graduate, high school graduate, some college or vocational school, college graduate, and graduate school), race (white and nonwhite), and body mass index (normal or below [<25 kg/m2], overweight [2529 kg/m2], and obese [30 kg/m2]). Men who left all alcohol questions blank ("missing" alcohol use) were combined with men who reported no current alcohol consumption based on a previous analysis of CPS-II (33) in which these two groups were shown to have similar mortality patterns. In models for coronary heart disease mortality, we assessed other potential confounding factors, including occupation, current employment, vegetable and fruit consumption, dietary fat consumption, and aspirin use; these factors had little effect on the risk estimates (data not shown) and were not included in final models.
Current pipe smokers were further characterized by number of pipes smoked per day, years of smoking, and depth of inhalation, and former pipe smokers were characterized by number of years since quitting smoking and age at quitting smoking. Causes of death with fewer than 15 deaths among current or former smokers are not shown by smoking characteristic. Linear trends of smoking characteristics, excluding lifelong nonusers, were tested using the likelihood ratio test (34).
Epidemiologic evidence suggests synergism between tobacco smoking and alcohol consumption for cancers of the upper aero-digestive tract, which includes the oropharynx, esophagus, and larynx (30). Therefore we examined the joint association of pipe smoking and alcohol consumption with cancers of the upper aero-digestive tract. Men with unquantifiable alcohol consumption were excluded from this analysis. A likelihood ratio test was used to test for multiplicative interaction between pipe smoking and alcohol consumption.
Analyses of cigarette smoking in CPS-II generally use only the first 6 years of follow-up to minimize the effects of misclassification among current smokers who quit smoking during more prolonged follow-up (35). We chose to use 18 years of follow-up to maximize the number of deaths available for analysis. To examine the effect of cessation of pipe smoking over the 18-year follow-up, we compared relative risks for current and former pipe smoking associated with all causes, lung cancer, coronary heart disease, cerebrovascular disease, and chronic obstructive pulmonary disease for three six-year periods: 19821988; 19891994; and 19952000. If bias due to misclassification of smoking status was substantial, we would expect to see the relative risks of current smoking decrease over time. Temporal trends were tested by including interaction terms between survival time and smoking in the Cox model (36); statistical significance of interaction terms was evaluated using the Wald chi-square test.
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RESULTS |
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DISCUSSION |
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The epidemiologic literature on tobacco use, including pipe and cigar smoking, has been reviewed recently (30). Many of the studies included in that review combined pipe and cigar smokers; however, the studies that examined exclusive pipe smoking showed results similar to ours. Of the prospective studies, ours is the largest and the only one to adjust for risk factors other than age. Men who smoke pipes exclusively have higher risk of lung cancer than men who have never smoked in most published prospective (912,41,42) and casecontrol (1317) studies. In our study, risk of lung cancer mortality in men was increased fivefold for current pipe smokers; this estimate is higher than that reported in two earlier U.S. cohorts (9,10) but is consistent with studies conducted in Europe (11,12,41,42). Like our study, two large European casecontrol studies (13,17) reported that lung cancer risk increased with years of pipe smoking, number of pipes smoked per day, and depth of inhalation and decreased with time since cessation of smoking.
Risk of death from laryngeal cancer was also strongly associated with current pipe smoking (RR = 13.1). To our knowledge, the association with laryngeal cancer has not previously been assessed among exclusive pipe smokers. Our estimates for death from cancers of the oropharynx (RR = 3.90) and esophagus (RR = 2.44) are consistent with those from other prospective studies, including HammondHorn (9), the U.S. Veterans Study (10), and a Swedish cohort (11). A hospital-based casecontrol study in Beijing observed a fivefold increased risk of oral cancer incidence among both male and female ever pipe smokers (18).
The risk estimate for stomach cancer mortality in this study is slightly lower than that reported in two prospective studies (10,12) or in a previous analysis in CPS-II men (RR = 1.3, 95% CI = 0.8 to 2.2), which was based on 14 years of follow-up (43). The risk of colorectal cancer mortality was highest for men who reported several decades of smoking or smoking 11 or more pipes per day, similar to results observed among cigarette smokers in CPS-II (44). Although no association was observed between current pipe smoking and colon or rectal cancer mortality in the Swedish study (11), Heineman et al. (45) observed an increasing risk of colon and rectal cancer death with increasing number of pipes smoked per day in a 26-year follow-up of U.S. veterans.
Risk of pancreatic cancer mortality associated with pipe smoking was increased in the Swedish prospective study (11) but not in two other prospective studiesthe U.S. Veterans study (10) or the Norwegian Cardiovascular Study (12). A hospital-based casecontrol study by Muscat et al. (19) observed an increased risk for pancreatic cancer incidence associated with ever pipe smoking.
Two previous studies in U.S. cohorts (9,10) reported an association between pipe smoking and bladder cancer mortality similar to that seen in CPS-II (RR = 1.50); a relative risk of 4.0 was reported in the Swedish study (11). The largest study of bladder cancer, a pooled analysis of European casecontrol studies (20), reported statistically significantly higher risk with longer duration of pipe smoking, as was also observed in CPS-II. We did not find an association between pipe smoking and kidney cancer mortality, similar to the results of two casecontrol studies of kidney cancer incidence (22,23).
Finally, our estimates of risk for cardiovascular and pulmonary disease are similar to those reported in the large Swedish study (11) and are within the range reported by other prospective A limitation of our study is that smoking habits were reported only at baseline. For diseases such as lung cancer, in which risk increases exponentially with duration of smoking (46), the relative risk estimate among continuing smokers would be expected to increase over time. However, we found that the association between lung cancer and current pipe smoking remained relatively constant over time (Table 6). The expected increase may have been obscured by misclassification of exposure due to cessation of smoking among current smokers during the 18-year follow-up period. The effect of this misclassification would be to underestimate the risks of continued smoking and to attenuate doseresponse gradients.
The main strength of our study was its size, which provided precise estimates of mortality risk associated with pipe smoking among men who smoked pipes exclusively and provided moderately stable estimates of risk for the more common endpoints in relation to the number of pipes smoked daily, duration of smoking, and depth of inhalation among current smokers, and age at quitting and years since quitting among former smokers.
Comprehensively documenting the deleterious health effects of pipe smoking is important in countering efforts by the tobacco industry to promote pipes as a desirable alternative to cigarettes or cigars. The tobacco industry has repeatedly demonstrated its ability to create new markets by reviving interest in tobacco products that had appeared to have become obsolete, especially among youth and young adults. Two complementary approaches used to rekindle demand for products such as moist snuff, premium cigars, bidis, and hookah pipes are to minimize the adverse health consequences of these products by presenting them as a less hazardous alternative to cigarette smoking and to glamorize use by creating positive associations with celebrity, athleticism, success, and/or internationalism (47).
Results from this large, prospective study strongly support a causal relationship between pipe smoking and mortality from cancers of the lung, larynx, esophagus, and oropharynx, and chronic obstructive pulmonary disease. Although the risk of dying from tobacco-associated diseases is lower for pipe smokers than for cigarette smokers, pipe smoking is as harmful as, and perhaps more harmful than, cigar smoking. All tobacco products cause excessive morbidity and mortality. Our findings may help deter efforts by the tobacco industry to imply, directly or indirectly, as it has with smokeless tobacco (48,49) and low-yield cigarettes (50), that any tobacco product has negligible adverse health effects.
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NOTES |
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Manuscript received October 31, 2003; revised March 31, 2004; accepted April 6, 2004.
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