Japanese Journal of Clinical Oncology Advance Access originally published online on January 19, 2006
Japanese Journal of Clinical Oncology 2006 36(1):25-39; doi:10.1093/jjco/hyi207
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© 2006 Foundation for Promotion of Cancer Research
Tobacco Smoking and Colorectal Cancer Risk: An Evaluation Based on a Systematic Review of Epidemiologic Evidence among the Japanese Population
1 Department of Preventive Medicine, Graduate School of Medical Sciences, Kyushu University, Fukuoka, 2 Epidemiology and Prevention Division, Research Center for Cancer Prevention and Screening, National Cancer Center, Tokyo, 3 Department of Preventive Medicine, Saga Medical School, Faculty of Medicine, Saga University, Saga, 4 Division of Epidemiology, Department of Public Health and Forensic Medicine, Tohoku University Graduate School of Medicine, Sendai, 5 Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, Nagoya and 6 Department of Epidemiology and Preventive Medicine, Gifu University School of Medicine, Gifu, Japan
For reprints and all correspondence: Tetsuya Mizoue, Department of Preventive Medicine, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashiku, Fukuoka 812-8582, Japan. E-mail: mizoue{at}phealth.med.kyushu-u.ac.jp
Received August 28, 2005; accepted October 12, 2005
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Abstract |
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 TOP Abstract INTRODUCTIONMETHODSMAIN FEATURES AND COMMENTSEVALUATION OF THE EVIDENCE...References |
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Background: It is unclear whether tobacco smoking is related to colorectal cancer risk in Japan. We evaluated the association among the Japanese population based on a systematic review of epidemiologic evidence.
Methods: Original data were obtained from searches of MEDLINE using PubMed, complemented with manual searches. The evaluation of associations was based on the strength of evidence and the magnitude of association, together with biological plausibility as previously evaluated by the International Agency for Research on Cancer.
Results: A total of six cohort studies and 15 case–control studies were thus identified. A substantial degree of heterogeneity was observed in the association between smoking and colon cancer; most case–control studies published before 1994 reported an inverse association, whereas studies conducted over the last decade did not find any significant association. Recent cohort studies have shown a non-significant 20–40% increase in colon cancer risk associated with current smoking. Several recent case–control studies and some cohort studies have identified a weak to strong positive association between smoking and rectal cancer.
Conclusion: We conclude that tobacco smoking possibly increases the risk of colorectal cancer among the Japanese population. More specifically, tobacco smoking may possibly increase the risk of rectal cancer; however, epidemiologic evidence is still insufficient to demonstrate any clear association with colon cancer.
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INTRODUCTION |
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TOPAbstractINTRODUCTIONMETHODSMAIN FEATURES AND COMMENTSEVALUATION OF THE EVIDENCE...References |
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In Japan, colorectal cancer has markedly increased over the last several decades (1) and it is now among the highest levels in the world (2). The increase in mortality has been linked to dietary changes including a decreased consumption dietary fibers (3) or grains (4). However, the increasing male-to-female mortality ratio from colorectal cancer since 1970 in Japan (1) may have been a result of sex differences in health-related lifestyles including tobacco smoking.
Tobacco smoke contains numerous chemicals that are potentially carcinogenic to humans. The range of cancer sites associated with tobacco smoking has been expanded and the International Agency for Research on Cancer (IARC) (5) recently admitted cancers of several sites including stomach and liver as smoke-related. Although colorectal cancer has not formally been recognized as a smoke-related cancer, a review identified emerging evidence showing an increased risk of colorectal cancer associated with smoking, especially long-term smoking (6). However, such an association has been reported mainly from the United States, whereas the findings from other populations remain conflicting.
The objective of the present study was to review the epidemiological findings regarding the association between smoking and colorectal cancer among Japanese population. The study results were summarized and the magnitude of the association was assessed. This work was conducted as part of a project of systematic evaluation of the epidemiological evidence regarding lifestyles and cancers in Japanese (7).
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METHODS |
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TOPAbstractINTRODUCTIONMETHODSMAIN FEATURES AND COMMENTSEVALUATION OF THE EVIDENCE...References |
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The original data for this review were identified by searches of MEDLINE using PubMed, complemented by manual searches of references from relevant articles where necessary. All epidemiologic studies on the association between tobacco smoking and colorectal cancer incidence or mortality among Japanese from 1963 to 2004, including papers in press if available, were identified using the search terms ‘tobacco smoking’, ‘colorectal cancer’, ‘colon cancer’, ‘rectal cancer’, ‘cohort studies’, ‘case–control studies’, ‘Japan’ and ‘Japanese’ as keywords found in the abstract. Papers written in either English or Japanese were reviewed, and only studies on Japanese population living in Japan were included. The individual results were summarized in the tables separately by a study design as cohort or case–control studies and, if available, by cancer site as colon, rectum or colorectum.
An evaluation was made based on the magnitude of association and the strength of evidence. First, the relative risks in each epidemiologic study were grouped by the magnitude of association, while considering statistical significance (SS) or no statistical significance (NS), as strong, <0.5 or >2.0 (SS); moderate, either (i) <0.5 or >2.0 (NS), (ii) >1.5 to 2 (SS) or (iii) 0.5 to <0.67 (SS); weak, either (i) >1.5 to 2 (NS), (ii) 0.5 to <0.67 (NS) or (iii) 0.67 to 1.5 (SS); or no association, 0.67 to 1.5 (NS). In the case of multiple publications of analyses of the same or overlapping datasets, only data from the largest or most updated results were included, and the incidence was given priority over mortality as an outcome measure. The incidence was also given priority in a single publication describing both incidence and mortality. After this process, the strength of evidence was evaluated in a similar manner to that used in the WHO/FAO Expert Consultation Report (8), in which evidence was classified as ‘convincing’, ‘probable’, ‘possible’ and ‘insufficient’. We assumed that biological plausibility corresponded to the judgment of the most recent evaluation from IARC (5). Notwithstanding the use of this quantitative assessment rule, an arbitrary assessment cannot be avoided when considerable variation exists in the magnitude of association between the results of each study. The final judgment, therefore, was made based on a consensus of the research group members, and it was therefore not necessarily objective. When we reach a conclusion that there is ‘convincing’ or ‘probable’ evidence of an association, we conduct a meta-analysis to obtain summary estimates for the overall magnitude of association.
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MAIN FEATURES AND COMMENTS |
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TOPAbstractINTRODUCTIONMETHODSMAIN FEATURES AND COMMENTSEVALUATION OF THE EVIDENCE...References |
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A total of six cohort studies and 15 case–controls studies were identified (Table 1 and Table 2, respectively). Among the cohort studies, four presented results by gender (10,12–14), one for men only (9), and one only for men and women combined (11). The respective numbers for the case–control studies are three, four and eight. Two case–control studies that did not indicate a point estimate and confidence interval, or P-value, were excluded (15,27), and a summary of the magnitude of association for the remaining studies is shown in Tables 3 and 4 for the cohort studies and case–control studies, respectively.
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Among the five cohort studies showing relative risks separately for the colon and rectum, no study found a significant association with colon cancer, although recent cohort studies (12–14) reported a non-significant 20–40% increased risk for colon cancer associated with smoking. For rectal cancer, one study (10) found a weak positive association in both men and women, whereas another study (12) reported a strong positive association in men. Of the two cohort studies showing relative risk for colon and rectum combined, a nation-wide study (13) reported a weak positive association in men. This study also found marginally significant associations in a separate analysis for the colon and rectum; the respective relative risks (95% confidence intervals) of current smoking compared with never-smoking were 1.4 (0.99–1.9) and 1.4 (0.9–2.3).
Of the 13 case–control studies evaluated, 11 studies provided odds ratios for the colon and rectum separately. Among these studies, five (17–20,22) of six studies published before 1994 have identified a reduced risk of colon cancer associated with smoking, whereas no study published after 1994 showed either a positive or inverse association with colon cancer. For rectal cancer, of five relevant studies published after 1994, four (23–25,29) have shown a weak or moderate positive association and the remaining study (28) reported a significant trend association with smoking index (P for trend = 0.04), whereas studies published before 1994 did not find any significant association. Of the four case–control studies reporting odds ratio for the colon and rectum combined (16,21,26,28), one study (26) found a significantly increased risk associated with smoking, especially with smoking in the distant past.
Four cohort studies (9,12–14) and two case–control studies (26,29) adjusted for alcohol consumption, but few studies controlled for other dietary (14) and non-dietary factors including sports activities (13,14) and obesity (12–14,26). Three case-control studies were performed on a community basis for recruiting control subjects (20–22), whereas the remaining studies were conducted using either hospital-based, health center-based or screening-based design.
Numerous studies including Japanese one (30) have identified smoking as a risk factor for colorectal adenomas, a precursor of colorectal cancer. Among the Japanese studies reviewed; however, we found a substantial heterogeneity in the risk estimates for an association between smoking and colon cancer, including marginally significant positive association in a nation-wide cohort study (13) and an inverse association in several case–control studies (17–20,22). Interestingly, all case–controls studies that reported an inverse association with colon cancer were published before 1994. Giovannucci (6) proposed a hypothesis that smoking is involved in cancer initiation and long induction period is needed before the appearance of the carcinogenic effects of smoking, which may be detected by recent studies including a sufficient number of long-term smokers. In line with the hypothesis, recent cohort studies in Japan (12–14) reported a 20–40% increased risk of colon cancer associated with current smoking in men. These studies probably include many long-term smokers, because most Japanese smokers started smoking around 20 years of age and participants in these studies were relatively old: 35 years or older (12), 40–69 years (13) and 40–79 years (14).
We identified a significant, or marginally significant, increased risk of rectal cancer associated with smoking in all case–control studies published after 1994 (23–29) and in some cohort studies (10,12,13). No study in this review reported a significant inverse association between smoking and rectal cancer. A clearer association of smoking with rectal cancer than with colon cancer has also been noted in several studies outside Japan (6). Furthermore, a Japanese study indicated that smoking is more strongly associated with rectal adenomas than with colon adenomas (30).
We should mention methodological issues. Several Japanese studies (9,12–14,26,29) controlled for alcohol drinking, a probable risk factor for colorectal cancer (8) and closely correlated with smoking behavior. However, few controlled for other dietary factors (14). According to a Japanese national survey on nutrition (31), there is a substantial difference between smokers and non-smokers in diet including the intake of calcium and folate, which are potentially associated with reduced risk of colorectal cancer (32,33). As a result, such confounding cannot be excluded from the results of Japanese studies.
In summary, epidemiological evidence for the association with smoking among Japanese population appears to be stronger for rectal cancer than for colon cancer. A consistent positive association between smoking and rectal cancer was observed among several recent case–control studies. However, since earlier case–controls studies and several cohort studies did not show a significant association between smoking and rectal cancer, it would therefore be appropriate to classify their association as ‘possible’. For colon cancer, epidemiological studies have provided mixed results; namely, several earlier case–control studies reported a decreased risk with smoking, whereas recent cohort studies showed a non-significant increased risk with smoking. Therefore, evidence among Japanese population is insufficient to establish any clear association between smoking and colon cancer.
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EVALUATION OF THE EVIDENCE ON TOBACCO SMOKING AND COLORECTAL CANCER RISK IN JAPANESE |
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TOPAbstractINTRODUCTIONMETHODSMAIN FEATURES AND COMMENTSEVALUATION OF THE EVIDENCE...References |
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From these results and based on assumed biological plausibility, we conclude that tobacco smoking may possibly increase the risk of colorectal cancer among the Japanese population. More specifically, tobacco smoking may possibly increase the risk of rectal cancer; however, the epidemiologic evidence remains insufficient to demonstrate any clear association with colon cancer.
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Acknowledgments |
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The authors gratefully acknowledge the assistance of Ms Tamami Hatano. 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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References |
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TOPAbstractINTRODUCTIONMETHODSMAIN FEATURES AND COMMENTSEVALUATION OF THE EVIDENCE...References |
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