Affiliations of authors: J. A. Shapiro, Division of Cancer Prevention and Control, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, GA; E. J. Jacobs, M. J. Thun, Department of Epidemiology and Surveillance Research, American Cancer Society, Atlanta.
Correspondence to: Jean A. Shapiro, Ph.D., Centers for Disease Control and Prevention, NCCDPHP, DCPC, Mailstop K-55, 4770 Buford Hwy, N.E., Atlanta, GA 30341-3717.
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ABSTRACT |
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INTRODUCTION |
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METHODS |
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Men in this analysis were a subset of the 508 353 male participants in Cancer Prevention Study II (CPS-II), a prospective mortality study of 1.2 million men and women enrolled in 1982 by American Cancer Society volunteers in all 50 U.S. states, the District of Columbia, and Puerto Rico (6). Participants completed a baseline self-administered questionnaire in 1982 that included information on demographic characteristics and various behavioral, environmental, occupational, and dietary factors. Women could not be included in this analysis because they were not asked if they smoked cigars. The median age of male participants in 1982 was 57 years; none were younger than 30 years of age.
The vital status of study participants was determined for 12 years, through December 31, 1994. Two approaches were used to ascertain vital status. Volunteers made personal inquiries in September 1984, 1986, and 1988 to determine whether the participants whom they had enrolled were alive or dead and to record the date and place of all deaths. Automated linkage to the National Death Index extended follow-up through December 31, 1994, and identified deaths among the 8485 men lost to follow-up between 1982 and 1988 (7). At the completion of follow-up in December 1994, 400 290 men (78.7%) were alive, 107 248 (21.1%) had died, and 815 (0.2%) had follow-up truncated in September 1988 because of insufficient data for National Death Index linkage. Death certificates were obtained for 98.5% of all men known to have died. The underlying cause of death was coded from death certificates according to the International Classification of Disease, 9th Revision (ICD-9) (8). The ICD-9 codes used to define the tobacco-related cancer outcomes were as follows: lung (162.0-162.9), larynx (161.0-161.9), oral cavity/pharynx (140.0-141.9 and 143.0-149.9, which excludes salivary gland cancer), esophagus (150.0-150.9), bladder (188.0-188.9), and pancreas (157.0-157.9).
Information on cigar smoking was based entirely on the smoking history reported in 1982. Men who reported ever smoking "cigarettes, cigars, or pipes, at least one a day for 1 year's time" were instructed to complete more detailed questions about smoking status (current or former), duration (in years), amount (number smoked per day), and depth of inhalation (none, slight, moderate, or deep). Each of these questions was asked separately for cigarettes, cigars, and pipes. Men who reported that they were current cigar smokers on the baseline questionnaire are considered "current" cigar smokers, although no information was available about smoking status later during follow-up. Men who reported they had never "smoked cigarettes, cigars, or pipes, at least one a day for 1 year's time" were considered to be "never smokers."
Analyses excluded men who reported a history of cancer other than nonmelanoma skin cancer (n = 6119), who reported that they had ever regularly smoked cigarettes or pipes (n = 364 561), or who had unclear or contradictory responses to smoking questions (n = 118). A total of 137 555 men remained for analysis.
Statistical Analysis
We used Cox proportional hazards modeling to examine the association of cigar smoking and cancer mortality while adjusting for other potential risk factors (9). We adjusted all rate ratio (RR) estimates for age, alcohol use, and use of snuff or chewing tobacco. The time axis used was follow-up time since enrollment in 1982. Age adjustment was accomplished by stratifying on exact year of age at enrollment within each Cox model. All Cox models were also adjusted for alcohol use (no regular use, less than one drink per day, one to two drinks per day, three drinks per day, four or more drinks per day) and use of snuff or chewing tobacco (never, former, or current). A small number of men whose level of alcohol consumption could not be determined (n = 312) were not included in the models. Race, educational level, body mass index, diabetes, vitamin supplement use, exercise level, and vegetable/citrus fruit intake were also examined as potential confounders. However, adjustment for these factors had little effect on the risk estimates. Vegetable and citrus fruit intake was estimated from the frequency of consumption of 28 common foods reported on the 1982 questionnaire, as has been described previously (10).
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RESULTS |
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DISCUSSION |
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In our study, risk of lung cancer mortality was increased approximately fivefold for men who
were current cigar-only smokers at the start of the 12-year follow-up as compared with men who
had never smoked (RR = 5.1; 95% CI = 4.0-6.6; 88 deaths among cigar
smokers). Results from previous cohort studies are summarized in Table 4. The increased risk of lung cancer in our study was substantially larger than the
twofold increased risk reported in the three earlier U.S. cohort studies that compared cigar-only
smokers with never smokers (11,13,14). In contrast, a small Swedish
cohort study found an RR of 7.6 for lung cancer mortality (11 deaths among cigar smokers, no CI
reported) (15), and a recent large, case-control study of incident lung
cancer from Germany, Italy, and Sweden found an odds ratio for current cigar or cigarillo
smokers of 10.6 (95% CI = 5.9-19.1) (16). In our study,
risk was particularly increased for men who smoked three or more cigars per day, who reported
inhaling, or who had smoked for 25 or more years. However, even cigar smokers who reported
that they did not inhale were considerably more likely than never smokers to die from lung
cancer (RR = 3.3; 95% CI = 2.3-4.7).
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One possible explanation for the greater increase in risk of lung cancer mortality observed in CPS-II is that there have been changes over time in the type of cigars smoked. Changes in the pH of cigars may be particularly important with respect to lung cancer because of the potential effect of pH on inhalation patterns. While the pH of cigars is higher than cigarettes, pH varies greatly between cigar types, with some brands having low pH levels close to those of cigarettes (19). Low pH cigars may be particularly hazardous, since, like cigarettes, they may require some degree of inhalation to achieve substantial nicotine absorption (19), and their smoke may contain less free ammonia and, therefore, be easier to inhale than the smoke from high pH cigars (20). The role of changes in cigar pH or other cigar characteristics is, however, difficult to investigate because, to our knowledge, such historic data are not available. Chance variation may also have contributed to the differing results between our study and earlier studies.
Our results regarding increased risk of fatal cancers of the oral cavity/pharynx, larynx, and
esophagus are generally similar to those from the limited number of prospective studies that have
examined risk among current cigar-only smokers (see Table 4).
The approximately
twofold increased risk of mortality from esophageal cancer in our study is lower than the
approximately fourfold to fivefold increased risk of mortality observed in CPS-I (11) and in the U.S. Veterans Study (12), possibly as a result of
chance. For all three of these cancers (oral cavity/pharynx, larynx, and esophagus), the increase
in risk appeared strongest for men who had smoked for 25 or more years at the start of the
12-year follow-up. Conclusions about the precise risks of shorter-duration cigar smoking are
limited by the small numbers of such short-duration smokers in this analysis. Risk also appeared
to increase with the number of cigars smoked per day and inhalation for cancers of the oral
cavity/pharynx and larynx but not for esophageal cancer. It is possible that variations in cigar
consumption behavior that determine the amount of tobacco carcinogens swallowed (such as
whether or not cigars are chewed or held in the mouth for long periods) may be more important
for esophageal cancer than inhalation patterns or the number of cigars smoked per day.
While we found no clear overall increased risk of fatal pancreatic or bladder cancer, risk of
mortality from both cancers was increased for cigar smokers who reported inhalation of cigar
smoke. Inhalation of cigar smoke may be particularly relevant for these organs because (unlike
the oral cavity/pharynx, larynx, and esophagus) they may have limited exposure to tobacco
carcinogens except through inhalation into the lungs and subsequent absorption into the
bloodstream. Results from previous cohort studies are summarized in Table 4. Risk of pancreatic cancer mortality was increased in CPS-I (11) and in the U.S. Veterans Study (12), but incidence of
pancreatic cancer was not clearly increased in the smaller Kaiser Permanente study (14). Mortality from bladder cancer was increased in CPS-I (11)
but not in the U.S. Veterans Study (12), while there was no
evidence of increased bladder cancer incidence in the Kaiser Permanente Study (14).
Strengths of this study include its large size and prospective design. The size of this study allowed us to examine risk among men who had never smoked cigarettes or pipes, isolating the effect of cigar smoking. In addition, we were able to examine the importance of number of cigars smoked per day, duration of cigar smoking, and self-reported inhalation, although small numbers for the less common cancers limited these analyses. We also were able to adjust (or determine that adjustment was unnecessary) for potential confounding factors, including alcohol and smokeless tobacco use.
A limitation of this study is that no information was available on smoking habits after completion of the baseline questionnaire. A considerable proportion of men classified as "current" cigar smokers at baseline may have quit smoking during the 12 years of follow-up. While the exact proportion of cigar smokers who quit during the 12 years of follow-up (1982 through 1994) is unknown, information on cigar smoking cessation in this cohort before baseline in 1982 suggests that the quit rate may have been quite high. We estimate that approximately 34% of cigar-only smokers in this cohort 12 years before baseline (1970) had quit by baseline (1982). To the extent that the risk of tobacco-related cancer decreases after quitting, we will have underestimated the effect of current cigar smoking. A second limitation is that we had no information on cigar size or type, which may be important determinants of cancer risk.
Current cigar smokers in this analysis had never regularly smoked cigarettes and had smoked cigars at least daily. Therefore, our results may not be generalizable to cigar smokers who have previously smoked cigarettes or who smoke cigars only occasionally.
The importance of cigar smoking as a potential emerging public health hazard is illustrated by data from the 1997 Youth Risk Behavior Survey showing that 31% of U.S. high school boys and 11% of U.S. high school girls had reported smoking a cigar within the past 30 days (21). Our results, together with those from previous studies, indicate that, if these young people become regular cigar smokers, a sizable number will develop a smoking-related cancer later in life.
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Manuscript received July 19, 1999; revised November 18, 1999; accepted December 9, 1999.
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