Japanese Journal of Clinical Oncology Advance Access originally published online on May 30, 2006
Japanese Journal of Clinical Oncology 2006 36(5):309-324; doi:10.1093/jjco/hyl025
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© 2006 Foundation for Promotion of Cancer Research
Tobacco Smoking and Lung Cancer Risk: An Evaluation Based on a Systematic Review of Epidemiological Evidence Among the Japanese Population
1 Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, 2 Epidemiology and Prevention Division, Research Center for Cancer Prevention and Screening, National Cancer Center, Tokyo, 3 Department of Preventive Medicine, Graduate School of Medical Sciences, Kyushu University, Fukuoka, 4 Department of Preventive Medicine, Saga Medical School, Faculty of Medicine, Saga University, Saga, 5 Division of Epidemiology, Department of Public Health and Forensic Medicine, Tohoku University Graduate School of Medicine, Sendai, 6 Department of Epidemiology and Preventive Medicine, Gifu University School of Medicine, Gifu, Japan
For reprints and all correspondence: Kenji Wakai, Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya, 1-1 Kanokoden, Chikusa-ku, Nagoya 464-8681, Japan. Tel: +81 052-764-2988; Fax: +81 052-763-5233; E-mail: wakai{at}aichi-cc.jp
Received December 19, 2005; accepted March 12, 2006
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Abstract |
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 TOP Abstract INTRODUCTIONMETHODSMAIN FEATURES AND COMMENTSEVALUATION OF EVIDENCE ON...References |
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Background: Although tobacco smoking is the best established risk factor for lung cancer, the association is not as strong among Japanese as among Western populations. It would be of value, therefore, to quantify that association in Japan based on a systematic review of epidemiological evidence for the primary prevention of lung cancer.
Methods: Original data were obtained from MEDLINE searches using PubMed, supplemented with manual searches. The evaluation of associations was based on the strength of evidence and the magnitude of the association, together with biological plausibility as previously evaluated by the International Agency for Research on Cancer. A meta-analysis was also conducted to estimate the summary measure of those associations.
Results: A total of 8 cohort studies and 14 case–control studies were identified, almost all of which consistently showed a strong association of current smoking with the risk of lung cancer. The summary relative risk for current smokers versus never smokers was estimated as 4.39 (95% confidence interval 3.92–4.92) for men and 2.79 (95% confidence interval 2.44–3.20) for women. Cohort studies and case–control studies gave reasonably consistent summary measures. The summary relative risks were 11.7 and 2.30 for squamous cell carcinoma and adenocarcinoma, respectively, in men, and were 11.3 and 1.37 correspondingly in women.
Conclusion: There is convincing evidence that tobacco smoking strongly increases the risk of lung cancer in the Japanese population, with the relative risk for current smokers compared with never smokers measuring around 4.4 for men and 2.8 for women.
Key Words: systematic review • epidemiology • smoking • lung neoplasms • Japanese
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INTRODUCTION |
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TOPAbstractINTRODUCTIONMETHODSMAIN FEATURES AND COMMENTSEVALUATION OF EVIDENCE ON...References |
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Although tobacco smoking is the best established risk factor for lung cancer, the association between smoking and that risk is not as strong among Japanese as among Western populations. The relative risk (RR) of current smokers is much smaller in Japan than in Western countries, where the RR reaches more than 10 in men (1). This may mean that the epidemiological information on smoking and lung cancer from Western countries is not directly applicable to Japanese.
It will therefore be of importance to quantify the impact of smoking on the development of lung cancer using data from Japanese populations in order for us to estimate how much of a decrease in the incidence or mortality of lung cancer can be expected by reducing the smoking prevalence in this country. Fortunately, large prospective studies have recently provided highly reliable evidence for the association between smoking and lung cancer risk, thus making a more accurate assessment possible. Such studies include the Three-Prefecture Cohort Study (2), the Japan Collaborative Cohort Study (3) and the Japan Public Health Center-based Prospective Study (1).
In the present study, we evaluated the magnitude of the association between tobacco smoking and the risk of lung cancer among Japanese by conducting a systematic review of epidemiological evidence to provide the basic data for the primary prevention of lung cancer in Japan. This report is one among a series of articles by our research group, which is investigating the association between health-related lifestyles (e.g. tobacco smoking, alcohol consumption and diet) and the risk of total cancers and major cancer sites (i.e. the stomach, colon and rectum, liver, lung and breast) in Japan (4,5).
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METHODS |
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TOPAbstractINTRODUCTIONMETHODSMAIN FEATURES AND COMMENTSEVALUATION OF EVIDENCE ON...References |
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The original data for this review were identified by searches of MEDLINE using PubMed, supplemented with manual searches of references from relevant articles where necessary. All epidemiological studies on the association between tobacco smoking and lung cancer incidence or mortality among Japanese from 1968 to 2005 were identified using the search terms ‘smoking’, ‘lung cancer’, ‘cohort studies’, ‘case–control studies’ and ‘Japan’ as keywords found in the abstract. Papers published in either English or Japanese were reviewed, and only studies on Japanese populations residing in Japan were included. In the case of multiple publication of the same or overlapping datasets, only data from the latest or most comprehensive results were included. The individual results were summarized separately in the tables by a study design as cohort or case–control studies.
We evaluated the results based on the magnitude of association and the strength of evidence. First, the RRs by gender in each epidemiological study were grouped by magnitude of association, with consideration for statistical significance (SS) or no statistical significance (NS), as strong (symbol 
or 
), <0.5 or >2 (SS); moderate (symbol or ), (1) <0.5 or >2 (NS), (2) >1.5 to 2 (SS) or (3) 0.5 to <0.67 (SS); weak (symbol or ), (1) >1.5 to 2 (NS), (2) 0.5 to <0.67 (NS) or (3) 0.67 to 1.5 (SS); or no association (symbol —), 0.67 to 1.5 (NS). The RR was approximated by the odds ratio in case–control studies. When the amount smoked was grouped into several levels or subgroup analyses by cell type were made, we considered the highest RR or odds ratio among all the exposure levels or subgroups.
After this process, the strength of evidence was evaluated in a similar manner to that used in the WHO/FAO Expert Consultation Report (6), in which evidence was classified as ‘convincing’, ‘probable’, ‘possible’ or ‘insufficient’, based on a consensus of the research group members. We assumed that biological plausibility corresponded to the judgment of the most recent evaluation from the International Agency for Research on Cancer (IARC) (7). The details underlying those judgments have been described elsewhere (4,5).
In addition, when we reached a conclusion that there was ‘convincing’ or ‘probable’ evidence of an association, a meta-analysis was conducted to obtain summary estimates for the overall magnitude of association. In principle, studies that reported RRs or odds ratios and their confidence intervals (CIs) by comparing current smokers with never smokers were included in the meta-analysis. For those that categorized risk values separately according to the smoking amount, such as the number of cigarettes smoked per day or the pack-year index, we first conducted a meta-analysis to estimate summary risk values for current smokers and then used these values for further meta-analysis. Studies without information on CIs of risk estimates or those with a reference group other than a group of never smokers were excluded from the meta-analysis. General variance-based methods were used to estimate summary statistics and their 95% CIs. Heterogeneity among studies was tested using the Q statistic together with a model to determine the summary RR and its 95% CI, i.e. a random- or fixed-effect model, selected according to the statistical significance in the Q statistic. The meta-analysis was performed using the meta command of the STATA statistical package (Stata Corporation, College Station, TX, USA), version 8 (8).
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MAIN FEATURES AND COMMENTS |
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A total of 8 cohort studies (1–3,9–13) and 14 case–control studies (14–27) were identified (Tables 1 and 2, respectively). Of the eight cohort studies, three (1,2,10) were population-based, in which subjects were recruited from general populations in geographically defined areas with a high response rate (>80%). The endpoint was defined as incidence of lung cancer in three studies (1,12,13) and death due to cancer in other cohort studies (2,3,9–11). The follow-up rate exceeded 90% in all the studies reporting the follow-up status of participants (1,3,9–11), except for one study in which 15.6% of the subjects migrated from the study areas (2).
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All the identified case–control studies were hospital-based, that is cases were enrolled in arbitrarily selected hospitals. In all (14,16–22,25–27) but three investigations (15,23,24) control subjects were also selected from patients in the hospitals where cases arose (hospital controls). Two studies (15,23) included controls randomly sampled from general populations (population or community controls). Stellman et al. (24) adopted both hospital and community controls. The diagnosis of cases was microscopically confirmed in most of the studies (14–16,18,19,21–25,27), and the response rate was reasonably high (at least 70%) in studies reporting the relevant figures among cases (14,15,18,21,23,24) and/or controls (15,18,21,24).
Among the cohort studies, four reported results by gender (1–3,10), three for men only (9,11,12) and one for men and women combined (13). The respective numbers for case–control studies were eight (14–16,21–23,26,27), three (18,20,24) and two (19,25). One study presented results for men only along with those for both genders combined (17).
The magnitude of association for these studies is summarized in Tables 3 and 4 for cohort and case–control studies, respectively. All cohort studies (1–3,9,10,12,13) except one (11) showed a strong positive association () between current smoking and the risk of lung cancer. The case–control studies (15,17–24,26,27) also consistently reported a similarly strong association except for two investigations in the analysis for women (14,16) and one in the analysis for men and women combined (25). Most of the studies demonstrated clear dose–response relationships between the risk of lung cancer and the number of cigarettes smoked per day (Tables 1 and 2), years of smoking, the pack-year index and/or years since stopped smoking (data not shown in tables). The RRs or odds ratios were generally lower in women than in men, probably due to the female smaller amount of smoking, so that we estimated the summary measure of association by gender (Fig. 1). Therefore, the three studies (13,19,25) that presented findings only for men and women combined were excluded from the meta-analysis.
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The summary RR for current smokers versus never smokers was estimated to be 4.39 (95% CI 3.92–4.92) for men and 2.79 (95% CI 2.44–3.20) for women by the meta-analysis using fixed-effect models (test for heterogeneity: P = 0.17 for men and P = 0.14 for women). We adopted fixed-effect models because the heterogeneity among studies was not statistically significant. Cohort studies and case–control studies gave a reasonably consistent summary measure (Fig. 1). In men, no apparent difference in the RR was found between recent investigations and an earlier cohort study (the follow-up started in 1966) by Akiba and Hirayama (10), while the RR was higher in recent cohort studies (1–3) than in the earlier one (10) in women. To clarify whether women have a smaller risk of lung cancer at the same exposure to tobacco smoking, we attempted to estimate the summary RRs according to the level of exposure by sex. Unfortunately, such summary RRs could not be calculated because only five studies (2,10,14,26,27) reported the RRs or odds ratios by both sex and the amount of cigarette smoking, and they used various cutoffs to categorize subjects according to the consumption level of cigarettes. To address the question, a pooled analysis of original data may be warranted.
The summary RRs comparing current and never smokers derived from the present meta-analysis are much lower than the corresponding RRs in Western countries (1). This discrepancy in the relative risk has been extensively discussed by Sobue et al. (1) and Marugame et al. (2) and may be attributable to both the lower risk of lung cancer in current smokers and the higher risk in non-smokers. The lower lifetime consumption of cigarettes in Japanese, due partly to the later initiation of smoking habits, the lower consumption per day, or the shortage of cigarettes during and immediately after World War II in Japan, may be one explanation for the lower risk of lung cancer in Japanese smokers. However, the differences in other factors, including ingredients and filters of cigarettes, lifestyle factors other than smoking and genetic susceptibility to lung cancer between Japanese and Western populations, should also be considered when explaining the lower risk among Japanese (1,2).
In addition to the summary measures for all lung cancer, we estimated the summary RRs (current smokers versus never smokers) by histological type by using the meta-analysis method mentioned above. In men, the resultant summary RRs were 11.7 (95% CI 8.31–16.6) for squamous cell carcinoma, 2.30 (95% CI 1.89–2.79) for adenocarcinoma and 14.0 (95% CI 6.64–29.4) for small cell carcinoma. In women, they were 11.3 (95% CI 7.15–17.9) for squamous cell carcinoma and 1.37 (95% CI 1.08–1.76) for adenocarcinoma. [The RRs for large cell carcinoma and female small cell carcinoma were not estimated due to the small number of studies (one or two) reporting required data].
In the IARC evaluation (7), it was concluded that the major cause of human lung cancer is tobacco smoking. The evaluation also noted that exposure to tobacco smoke led to modest increases in the occurrence of malignant and/or benign lung tumors in rats and mice and that smoking-related DNA adducts were detected in the respiratory tract. We therefore assumed that the association of tobacco smoking with lung cancer risk held biological plausibility.
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EVALUATION OF EVIDENCE ON TOBACCO SMOKING AND LUNG CANCER RISK IN JAPANESE |
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TOPAbstractINTRODUCTIONMETHODSMAIN FEATURES AND COMMENTSEVALUATION OF EVIDENCE ON...References |
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Based on these results and assumed biological plausibility, we conclude that there is convincing evidence that tobacco smoking strongly increases the risk of lung cancer in the Japanese population. The RR for Japanese current smokers compared with never smokers was estimated to be around 4.4 for men and 2.8 for women. These figures can be used to plan programs for the primary prevention of lung cancer by the reduction of tobacco smoking in Japan.
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Acknowledgments |
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The authors gratefully acknowledge the assistance of Ms Izumi Suenaga and Mr Tomohiro Shintani in this review. This work was supported by the Third-Term Comprehensive 10-year Strategy for Cancer Control from the Ministry of Health, Labour and Welfare, Japan.
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Notes |
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* Research group members: Shoichiro Tsugane (principal investigator), Manami Inoue, Shizuka Sasazuki, Motoki Iwasaki, Tetsuya Otani, National Cancer Center, Tokyo; Kenji Wakai, Aichi Cancer Center, Nagoya; Tetsuya Mizoue, Kyushu University, Fukuoka; Keitaro Tanaka, Saga University, Saga; Ichiro Tsuji (2004–), Yoshitaka Tsubono (2003), Taichi Shimazu, Tohoku University, Sendai; and Chisato Nagata, Gifu University, Gifu.
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