Affiliations of authors: P. Boffetta, V. Gaborieau, International Agency for Research on Cancer, Lyon, France; G. Pershagen, F. Nyberg, Institute of Environmental Medicine, Karolinska Institute, Stockholm, Sweden; K.-H. Jöckel, Institute for Medical Informatics, Biometry and Epidemiology, Essen, Germany; F. Forastiere, Epidemiology Unit Latium Region, Rome, Italy; J. Heinrich, M. Kreuzer, National Research Center for Environment and Health (GSF) Institute for Epidemiology, Munich, Germany; I. Jahn, Bremen Institute for Prevention Research, Germany; F. Merletti, Unit of Cancer Epidemiology, University of Turin, Italy; F. Rösch, International Agency for Research on Cancer, Lyon, and GSF Institute for Epidemiology; L. Simonato, Venetian Cancer Registry, Padua, Italy.
Correspondence to: Paolo Boffetta, M.D., International Agency for Research on Cancer, 150 cours Albert-Thomas, 69372 Lyon cedex 08, France (e-mail: boffetta{at}iarc.fr).
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
We used data from seven case-control studies of lung cancer, including more than 5600 male case patients and 7200 male control subjects, for a detailed analysis of lung cancer risk following cigar and pipe smoking. These data were part of a pooled analysis of European case-control studies of lung cancer (7). We excluded women because of the very small number of cigar smokers and pipe smokers among them.
Cigars are products made of tobacco wrapped in tobacco leaves, as distinct from cigarettes, which are made of tobacco wrapped in paper (8). Most traditional cigars smoked in Europe weigh 2-8 g and are similar to American "small cigars." Cigarillos are smaller than cigars, weighing 1.5-3 g; they are called "little cigars" in the United States.
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
In Italy 3, control subjects were selected from hospital patients with diseases not related to tobacco smoking, while in the remaining centers, they were obtained from a random sample of the general male population. In the Swedish center, 51% of the study subjects were deceased at the time of the study, and proxies were interviewed. The response rate among case patients (or their proxies) was above 67% in all centers; that of control subjects was 63% or higher in all centers except Germany 2 (38%) and Germany 3 (45%).
A detailed interview concerning their lifetime history of tobacco smoking was obtained for each case patient and control subject: In particular, the dates at start and end and the detailed quantities (in the Swedish center: categories of tobacco used, without detailed amounts) were asked for each smoking period, defined by changes in either quantity or type of tobacco product. This enabled us to construct variables, such as total duration of smoking and average and cumulative consumption of cigarettes, cigars, cigarillos, and pipe tobacco. Information on inhalation was available for smokers from Germany and Italy.
For the purpose of comparing and combining data on cigarette, cigar, cigarillos, and pipe smoking, we equated one cigarette to 1 g of tobacco, one cigar to 4 g, and one cigarillo to 2 g [(8); Joeckel K-H: personal communication]; for pipe smoking, we requested the weight in grams of the pack of tobacco and the frequency of use. Subjects who reported a lifetime consumption of no more than 400 cigarettes (i.e., one cigarette a day during 1 year) or the equivalent amount of cigars, cigarillos, or pipe tobacco were classified as nonsmokers; "pure" smokers were considered those who smoked only one product. We classified as "mixed" smokers those who smoked cigarettes and cigars, cigarillos, or a pipe; among them, "predominant" smokers were those who smoked more than 80% of total tobacco as one product. Because of the relatively small number of pure smokers of cigars and cigarillos and the similarities between these two products in the traditional European market, we combined these two groups in most analyses.
We selected subjects aged up to 75 years, with a complete history of tobacco smoking. Nonsmokers of any tobacco product served as the reference category; the analysis was based on unconditional logistic regression, with terms for age and center, and was aimed to estimate odds ratios (ORs) and 95% confidence intervals (CIs) (9). In selected analyses, we adjusted for additional potential confounders, such as total amount of tobacco smoked, age at start of smoking, education level (in three categories), and occupational exposure to lung carcinogens. In the analysis of quantitative variables, such as duration of smoking and cumulative consumption, smokers were divided into quartiles based on the distribution of the variable among the control subjects. Ex-smokers were divided in two groups for duration of quitting, with a cut point at 15 years, corresponding to the median duration of quitting among control subjects. All P values are two-sided and are considered statistically significant for P<.05. We also conducted an analysis based on random-effects models (10), since the design of the study slightly differed among centers. Because the results of this analysis did not differ from those based on the pooled database, we present only results based on the latter approach.
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
A total of 117 case patients and 1750 control subjects were classified as nonsmokers: The
OR for ever smoking any tobacco product regularly was 14.2 (95% CI =
11.7-17.2). ORs of lung cancer in different groups of pure smokers and in mixed smokers are
shown in Table 1. Pure smokers of cigars and cigarillos include subjects
who smoked cigarillos only (21 case patients and 31 control subjects), cigars only (16 case
patients and 42 control subjects), or both cigars and cigarillos but not pipe tobacco or cigarettes
(six case patients and four control subjects). The risk was higher for cigarette smokers (OR
= 14.9; 95% CI = 12.3-18.1) than for smokers of other products. Among
control subjects, mixed smokers (excluding 60 control subjects who smoked cigars, cigarillos,
and pipe tobacco but not cigarettes) consumed 73.3% of their total tobacco as cigarettes,
4.7% as cigars, 5.2% as cigarillos, and 16.7% as pipe tobacco.
|
|
The OR for ever pipe smoking was 7.9 (95% CI = 5.3-11.8) (Table 1) and the results were similar when predominant smokers were considered
instead of pure smokers (OR = 8.7; 95% CI = 6.2-12.4, based on 89
exposed case patients and 172 control subjects). A clear dose-response relationship was shown
for duration of pipe smoking and cumulative consumption, while there was no clear pattern in
risk according to average consumption and age at start (Table 3).
Most
pure pipe smokers (51 case patients and 103 control subjects) were from Sweden. Because
information on inhalation was not available for these subjects, results for lung cancer risk by
pipe-smoke inhalation were limited by small numbers and are not presented in detail.
|
The lack of exact correspondence between the categories used in the dose-response analyses
for the different tobacco products limited the comparability of the results. We therefore
conducted an additional analysis on pure smokers of cigarettes, cigars or cigarillos, and pipes
based on continuous variables of consumption after restriction to smokers (Table 4). Although the risk estimates for cigar, cigarillo, and pipe smoking were less precise
than those for cigarette smoking, the results showed a comparable carcinogenic risk for all types
of tobacco products. Similar results were obtained when nonsmokers were retained in the
analysis and the ORs were estimated for the increase in one log-unit of pack-years: 3.3
(95% CI = 3.1-3.6) for cigarettes, 3.3 (95% CI = 1.8-6.0) for cigars
and cigarillos, and 2.4 (95% CI = 1.5-4.0) for pipe.
|
When we conducted the analysis by histologic type, we found a significant trend in the risk of squamous cell carcinoma according to cumulative consumption of either cigars and cigarillos or pipe. The OR for the highest exposure category was 54.6 (95% CI = 22.6-132) for cigars or cigarillos and 46.0 (95% CI = 19.0-111) for pipe. The results for small-cell carcinoma and adenocarcinoma were based on relatively small numbers of pure smokers, but they suggested a higher risk for the former (OR = 87.0 [95% CI = 26.2-289] for heavy cigar and cigarillo consumption and 48.0 [95% CI = 11.2-206] for heavy pipe consumption) than for the latter (OR = 2.1 [95% CI = 0.3-17.1] and 6.3 [95% CI = 2.0-19.8], respectively).
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Our comparative analysis was based on weights of 1 g for cigarettes, 4 g for cigars, and 2 g for cigarillos, which represent reasonable averages for traditional European products (Joeckel K-H: personal communication). The consumption of pipe tobacco, on the other hand, was based on the direct amount of pipe tobacco consumed by the smokers. To test the sensitivity of our results to the value for the average weight of cigars, we conducted additional analyses using different assumptions. With an average weight of 5 g, there was a small decrease in the risk estimate for 1 unit of average consumption (OR = 1.041; 95% CI = 1.005-1.078) and cumulative consumption (OR = 1.048; 95% CI = 1.022-1.075). The use of an average weight of 3 g, on the other hand, resulted in an increase in the risk estimates (OR = 1.079 [95% CI = 1.019-1.142] for average consumption and 1.076 [95% CI = 1.038-1.114] for cumulative consumption). Therefore, the risk estimates for pure cigar and cigarillo smoking seem to be comparable to those for cigarette smoking no matter which weight we choose for cigars.
We controlled for the potential confounding effect of education and exposure to occupational carcinogens: These factors did not change appreciably the results. We could not assess the impact of other potential confounders, such as diet and family predisposition to cancer. The participating centers adopted slightly different methods to recruit and interview case patients and control subjects. An additional limitation is the relatively low response rate among control subjects in two of the German centers. We addressed these issues by performing a meta-analysis based on random-effects models, which provided results similar to those of the analysis of the pooled dataset, owing to the lack of significant heterogeneity of the results among centers. In addition, we repeated the analysis after exclusion of one center at a time. The ORs for smoking 1 g/day x year of cigars or cigarillos varied from 1.053 (exclusion of Sweden) to 1.080 (exclusion of Germany 1), those for pipe smoking varied from 1.062 (exclusion of Germany 1) to 1.074 (exclusion of Sweden), and those for cigarette smoking varied from 1.035 (exclusion of Germany 2) to 1.042 (exclusion of Italy 1 or Italy 2). Therefore, the inclusion or exclusion of individual centers did not systematically affect our results.
Although a large number of studies have estimated the risk of lung cancer among cigar and pipe smokers, most reports do not present results for pure smokers of these products because of small numbers. In general, American studies [(1-14) and reviewed in (4)] and a study conducted in seven European regions (15) show a moderately increased risk for cigar and pipe smokers, while studies conducted in Scandinavia provide high-risk estimates, which are comparable to ours (16-19). Only a few studies have included a sufficiently large number of pure cigar and pipe smokers to allow a detailed quantitative analysis. In the Seven Area Study, the risk of lung cancer was higher for smokers of cigarettes alone for 40 years or more (OR = 11.6) than among the comparable groups of pure cigar (OR = 3.0) and pipe (OR = 4.4) smokers (15). In a Swedish cohort study (18), the increase in lung cancer risk was similar for smokers of cigarettes, cigars, and pipes. Results on cigar smokers from the American Cancer Society Cancer Prevention Study I have recently been reported (4): The relative risk among "primary" cigar smokers was 2.1 (95% CI = 1.6-2.7) and was 3.4 (95% CI = 2.3-4.8) among smokers of five or more cigars per day.
There are several possible explanations for these differences. Although we do not have direct information on the brand or weight of the cigars smoked by our study population, most cigars traditionally smoked in Europe are smaller than regular American cigars. In addition, smokers of cigarillos, corresponding to the American "little cigars," represent an important group in our study. We are not aware of data on the composition of the tobacco or the smoke of traditional European cigars. The available data on the composition of mainstream smoke of American cigarettes and cigars suggest higher levels of tobacco-specific nitrosamines and tar in smoke from both little and regular cigars than in smoke from cigarettes (20). Different inhalation patterns may also contribute to the differences in the results. The proportion of pure cigar and cigarillo smokers reporting inhalation among the control subjects in our study was lower than that of a previous European study (15) but higher than the proportion found in an American study (13). An additional possible explanation is misclassification of occasional and weak smokers as nonsmokers in some studies.
Only limited information is available on the histologic type of lung cancer among cigar and pipe smokers. In the study in seven European areas, lung cancers from smokers of cigars, pipes, and cigarettes alone had a similar histologic distribution (15) as did cancers from pipe and cigarette smokers in a Swedish study (17), while in an American study, there was a higher proportion of small-cell and squamous cell carcinomas in cigar and pipe smokers than in cigarette smokers (13). In our study, cigar and pipe smoking exerted a nonsignificantly stronger carcinogenic effect on squamous and small-cell carcinomas than on adenocarcinoma. To our knowledge, the effect of age at start and time since quitting smoking on lung cancer risk has not been previously investigated among Western smokers of cigars and pipes.
Consumption of cigars, cigarillos, and pipe tobacco has declined in most European countries during the last decades (21). This trend paralleled a similar decrease that occurred in North America until the 1980s (21). In recent years, this trend has reversed in the United States and cigar smoking is becoming increasingly popular (22,23), in particular among teenagers (23,24), and a similar pattern might be expected in Europe. The same pattern does not seem to take place for pipe smoking (25). The results of our study suggest that the lower risk of lung cancer among cigar and pipe smokers that has been reported in many studies might be explained by a lower cumulative consumption and a later age at start in the former group of smokers and not to a lower carcinogenic potency of cigar and pipe smoke as compared with cigarette smoke. With respect to cigars, our results reflect the experience of smoking traditional European products and might not reflect the current pattern of cigar smoking in the United States. Regardless, control of cigar and pipe smoking is as important as cigarette smoking control for the prevention of lung cancer.
![]() |
NOTES |
---|
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
1 Doll R, Hill AB. Smoking and carcinoma of the lung. Br Med J 1950;2:739-48.
2 US Department of Health and Human Services. Smoking and health. Other forms of tobacco use. Report of the Surgeon General. DHHS Publ No. (PHS) 79-50066, 1979.
3 Zaridze D, Peto R, editors. Tobacco: a major international health hazard (IARC Sci Publ 74). Lyon (France): International Agency for Research on Cancer; 1986.
4 Shanks TG, Burns DM. Disease consequence of cigar smoking. In: US Department of Health and Human Services. Cigars: health effects and trends (Smoking and Tobacco Control Monograph 9). DHHS Publ No. (NIH) 98-4302, 1998:105-58.
5 Peto R. Influence of dose and duration of smoking on lung cancer rates. In: Zaridze D, Peto R, editors. Tobacco: a major international health hazard (IARC Sci Publ 74). Lyon (France): International Agency for Research on Cancer; 1986.
6
Wald NJ, Watt HC. Prospective study of effect of switching from
cigarettes to pipes or cigars on mortality from three smoking related diseases. BMJ 1997;314:1860-3.
7 Simonato L, Boffetta P, Roesch F, Gaborieau V, Sartorel S. A multicentric case-control study of the major risk factors for lung cancer in Europe with particular emphasis on intercountry comparisonfinal scientific report. Padua (Italy): Venetian Tumour Registry; 1997.
8 IARC. Tobacco smoking. In: IARC monographs on the evaluation of carcinogenic risk of chemicals to humans, vol. 38. Lyon (France): International Agency for Research on Cancer; 1986. p. 55.
9 Breslow NE, Day NE. Statistical methods in cancer research, Vol I, The analysis of casecontrol studies (IARC Sci Publ 32). Lyon (France): International Agency for Research on Cancer; 1980.
10 DerSimonian R, Laird NM. Meta-analysis in clinical trials. Contr Clin Trials 1986;7:177-88.
11 Hammond EC. Smoking in relation to the death rates of one million men and women. Natl Cancer Inst Monogr 1966;19:127-204.[Medline]
12 Rogot E, Murray JL. Smoking and causes of death among U.S. veterans: 16 years of observation. Public Health Rep 1980;95:213-22.[Medline]
13 Higgins IT, Mahan CM, Wynder EL. Lung cancer among cigar and pipe smokers. Prev Med 1988;17:116-28.[Medline]
14 Tekawa IS, Friedman GD, Iribarren C, Sidney S. Cigar smoking and cancer incidence [abstract]. Am J Epidemiol 1998;147(Suppl 1):S26.
15 Lubin JH, Richter BS, Blot WJ. Lung cancer risk with cigar and pipe use. J Natl Cancer Inst 1984;73:377-81.[Medline]
16 Cederlof R, Friberg L, Hrubec Z, Lorich U. The relationship of smoking and some social covariables to mortality and cancer morbidity: a ten year follow-up in a probability sample of 55 000 subjects, age 18 to 69parts 1 and 2. Stockholm (Sweden): Department of Environmental Hygiene, Karolinska Institute; 1975.
17 Damber LA, Larsson LG. Smoking and lung cancer with special regard to type of smoking and type of cancer. A case-control study in north Sweden. Br J Cancer 1986;53: 673-81.[Medline]
18 Carstensen JM, Pershagen G, Eklund G. Mortality in relation to cigarette and pipe smoking: 16 years' observation of 25 000 Swedish men. J Epidemiol Community Health 1987;41:166-72.[Abstract]
19 Lange P, Nyboe J, Appleyard M, Jensen G, Schnohr P. Influence of tobacco type on mortality from lung cancer and chronic obstructive pulmonary disease. Ugeskr Laeger 1933;155:2333-7.
20 Hoffmann D, Hoffmann I. Chemistry and toxicology. In: US Department of Health and Human Services. Cigars: health effects and trends (Smoking and Tobacco Control Monograph 9). DHHS (Publ No. NIH 98-4302), 1998: 55-104.
21 Nicolaides-Bouman A, Wald N, Forey B, Lee P. International smoking statistics: a collection of historical data from 22 economically developed countries. Oxford (U.K.): Oxford Univ Press, 1993.
22 USDA. Tobacco situation and outlook report. Washington (DC): US Department of Agriculture, Commodity Economics Division, Economic Research Service (document No. TSB-238), April 1997.
23 Gerlach KK, Cummings KM, Hyland A, Gilpin EA, Johnson MD, Pierce JP. Trends in cigar consumption and smoking prevalence. In: US Department of Health and Human Services, Cigars: health effects and trends (Smoking and Tobacco Control Monograph 9). DHHS (Publ No. NIH 98-4302), 1998: 21-53.
24 Cigar smoking among teenagersUnited States, Massachusetts, and New York, 1996. MMWR Morb Mortal Wkly Rep 1997;46:433-40.[Medline]
25 Nelson DE, Davis RM, Chrismon JH, Giovino GA. Pipe smoking in the United States, 1965-1991: prevalence and attributable mortality. Prev Med 1996;25:91-9.[Medline]
Manuscript received September 11, 1998; revised January 19, 1999; accepted February 16, 1999.
This article has been cited by other articles in HighWire Press-hosted journals:
![]() |
||||
|
Oxford University Press Privacy Policy and Legal Statement |