Smoking and colorectal cancer: a meta-analysis.

CONTEXT Colorectal cancer is the third most common form of cancer and the fourth most frequent cause of cancer deaths worldwide. The association between cigarette smoking and colorectal cancer has been inconsistent among studies. OBJECTIVE To clarify the association of cigarette smoking and colorectal cancer, we performed a comprehensive literature search and a meta-analysis of observational studies considering both incidence and mortality. DATA SOURCES We performed a literature search using PubMed, ISI Web of Science (Science Citation Index Expanded), and EMBASE to May 2008, with no restrictions. We also reviewed references from all retrieved articles. STUDY SELECTION All articles that were independent and contained the minimum information necessary to estimate the colorectal cancer risk associated with cigarette smoking and a corresponding measure of uncertainty. DATA EXTRACTION Articles were reviewed and data were extracted and cross-checked independently by 3 investigators, and any disagreement was resolved by consensus among all 3. RESULTS One hundred six observational studies were included in the analysis of incidence. Twenty-six studies provided adjusted risk estimates for ever smokers vs never smokers, leading to a pooled relative risk of 1.18 (95% confidence interval [CI], 1.11-1.25). Smoking was associated with an absolute risk increase of 10.8 cases per 100,000 person-years (95% CI, 7.9-13.6). We found a statistically significant dose-relationship with an increasing number of pack-years and cigarettes per day. However, the association was statistically significant only after 30 years of smoking. Seventeen cohort studies were included in the analysis of mortality. The pooled risk estimate for ever vs never smokers was 1.25 (95% CI, 1.14-1.37). Smoking was associated with an absolute risk increase of 6.0 deaths per 100,000 person-years (95% CI, 4.2-7.6). For both incidence and mortality, the association was stronger for cancer of the rectum than of the colon. CONCLUSION Cigarette smoking is significantly associated with colorectal cancer incidence and mortality.

[1]  H. Kim,et al.  [Smoking and colorectal cancer risk in the Korean elderly]. , 2006, Journal of preventive medicine and public health = Yebang Uihakhoe chi.

[2]  Y. Yun,et al.  Cigarette smoking and cancer incidence risk in adult men: National Health Insurance Corporation Study. , 2005, Cancer detection and prevention.

[3]  P. Chyou,et al.  A prospective study of colon and rectal cancer among Hawaii Japanese men. , 1996, Annals of epidemiology.

[4]  M. Inoue,et al.  Alcohol consumption, smoking, and subsequent risk of colorectal cancer in middle-aged and elderly Japanese men and women: Japan Public Health Center-based prospective study. , 2003, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[5]  M. Woodward,et al.  The role of lifestyle risk factors on mortality from colorectal cancer in populations of the Asia-Pacific region. , 2007, Asian Pacific journal of cancer prevention : APJCP.

[6]  D. Schaid,et al.  The frequency of hereditary defective mismatch repair in a prospective series of unselected colorectal carcinomas. , 2001, American journal of human genetics.

[7]  R. Brand,et al.  Associations between the age at diagnosis and location of colorectal cancer and the use of alcohol and tobacco: implications for screening. , 2006, Archives of internal medicine.

[8]  P. Ghadirian,et al.  Dietary carotenoids and risk of colon cancer: Case‐control study , 2004, International journal of cancer.

[9]  T. Lam,et al.  Smoking, drinking and colorectal cancer in Hong Kong Chinese: A case‐control study , 2004, International journal of cancer.

[10]  M. Inoue,et al.  Subsite-specific risk factors for colorectal cancer: a hospital-based case-control study in Japan , 2004, Cancer Causes & Control.

[11]  L. Aaltonen,et al.  Incidence of hereditary nonpolyposis colorectal cancer and the feasibility of molecular screening for the disease. , 1998, The New England journal of medicine.

[12]  G. Smith,et al.  Bias in meta-analysis detected by a simple, graphical test , 1997, BMJ.

[13]  A. Tuyns,et al.  Cancers of the digestive tract, alcohol and tobacco , 1982, International journal of cancer.

[14]  S. Kuriyama,et al.  Alcohol consumption is associated with an increased risk of distal colon and rectal cancer in Japanese men: the Miyagi Cohort Study. , 2007, European journal of cancer.

[15]  J. Potter,et al.  Risk of microsatellite-unstable colorectal cancer is associated jointly with smoking and nonsteroidal anti-inflammatory drug use. , 2006, Cancer research.

[16]  D. Grobbee,et al.  Rapid N-acetyltransferase 2 imputed phenotype and smoking may increase risk of colorectal cancer in women (Netherlands) , 2003, Cancer Causes & Control.

[17]  M. Thun,et al.  Tobacco smoke and involuntary smoking. , 2004, IARC monographs on the evaluation of carcinogenic risks to humans.

[18]  W. Chow,et al.  Cigarette and alcohol consumption and the risk of colorectal cancer in Shanghai, China , 2002, European journal of cancer prevention : the official journal of the European Cancer Prevention Organisation.

[19]  S. Akiba Analysis of cancer risk related to longitudinal information on smoking habits. , 1994, Environmental health perspectives.

[20]  S. Neuhausen,et al.  CYP1A1, cigarette smoking, and colon and rectal cancer. , 2004, American journal of epidemiology.

[21]  N. Laird,et al.  Meta-analysis in clinical trials. , 1986, Controlled clinical trials.

[22]  A. Tamakoshi,et al.  Smoking and Colorectal Cancer in a Non-Western Population: a Prospective Cohort Study in Japan , 2003, Journal of epidemiology.

[23]  M. Leppert,et al.  The colon cancer burden of genetically defined hereditary nonpolyposis colon cancer. , 2001, Gastroenterology.

[24]  M. Mahoney,et al.  Colorectal cancer occurs earlier in those exposed to tobacco smoke: implications for screening , 2008, Journal of Cancer Research and Clinical Oncology.

[25]  P. Newcomb,et al.  Cigarette smoking in relation to risk of large bowel cancer in women. , 1995, Cancer research.

[26]  P. Knekt,et al.  Smoking and risk of colorectal cancer. , 1998, British Journal of Cancer.

[27]  J. Olsen,et al.  Coffee, tobacco and alcohol as risk factors for cancer and adenoma of the large intestine. , 1993, International journal of epidemiology.

[28]  H. A. Kahn The Dorn study of smoking and mortality among U.S. veterans: report on eight and one-half years of observation. , 1966, National Cancer Institute monograph.

[29]  A. Neugut,et al.  Cigarette smoking and microsatellite instability: causal pathway or marker-defined subset of colon tumors? , 2000, Journal of the National Cancer Institute.

[30]  C. Boland,et al.  A National Cancer Institute Workshop on Hereditary Nonpolyposis Colorectal Cancer Syndrome: meeting highlights and Bethesda guidelines. , 1997, Journal of the National Cancer Institute.

[31]  M. Leppert,et al.  Associations between cigarette smoking, lifestyle factors, and microsatellite instability in colon tumors. , 2000, Journal of the National Cancer Institute.

[32]  Y. T. van der Schouw,et al.  Age at menopause, body mass index, and the risk of colorectal cancer mortality in the Dutch Diagnostisch Onderzoek Mammacarcinoom (DOM) cohort. , 2000, Epidemiology.

[33]  K. Ozasa Smoking and mortality in the Japan Collaborative Cohort Study for Evaluation of Cancer (JACC). , 2007, Asian Pacific journal of cancer prevention : APJCP.

[34]  Chien-Jen Chen,et al.  The mortality risks of smokers in Taiwan: Part I: cause-specific mortality. , 2004, Preventive medicine.

[35]  R. Collins,et al.  Early health effects of the emerging tobacco epidemic in China. A 16-year prospective study. , 1997, JAMA.

[36]  Richard Doll,et al.  Mortality in relation to smoking: 22 years' observations on female British doctors. , 1980, British medical journal.

[37]  J. Siemiatycki,et al.  The Effects of Smoking on the Risk of Colorectal Cancer , 2002, Diseases of the colon and rectum.

[38]  R. Hiatt,et al.  The relations of alcoholic beverage use to colon and rectal cancer. , 1988, American journal of epidemiology.

[39]  F. Nagengast,et al.  Environmental factors and colorectal tumor risk in individuals with hereditary nonpolyposis colorectal cancer. , 2007, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[40]  G. Pershagen,et al.  Cancer incidence in female smokers: A 26‐year follow‐up , 1997, International journal of cancer.

[41]  J. Baron,et al.  Coffee, tea, tobacco, and cancer of the large bowel. , 1994, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[42]  N. Petrelli,et al.  The relationship between smoking exposure and p53 overexpression in colorectal cancer. , 1996, British Journal of Cancer.

[43]  A. Wolk,et al.  Long‐term tobacco smoking and colorectal cancer in a prospective cohort study , 2001, International journal of cancer.

[44]  S. Y. Choi,et al.  Effect of cigarette smoking and alcohol consumption in the aetiology of cancer of the oral cavity, pharynx and larynx. , 1991, International journal of epidemiology.

[45]  K. Steindorf,et al.  Combined risk assessment of physical activity and dietary habits on the development of colorectal cancer. A hospital-based case-control study in Poland. , 2000, European journal of cancer prevention : the official journal of the European Cancer Prevention Organisation.

[46]  R. Doll,et al.  Mortality in relation to smoking: 20 years' observations on male British doctors. , 1976, British medical journal.

[47]  A. Andersen,et al.  Smoking habits and risk of cancers other than lung cancer: 28 years' follow-up of 26,000 Norwegian men and women , 2004, Cancer Causes & Control.

[48]  C. la Vecchia,et al.  Cigarette smoking and risk of cancers of the colon and rectum: A case–control study from Italy , 1998, European Journal of Epidemiology.

[49]  P. Maisonneuve,et al.  Cigarette smoking and adenomatous polyps: a meta-analysis. , 2008, Gastroenterology.

[50]  K. Batts,et al.  Serrated polyps of the large intestine: a morphologic and molecular review of an evolving concept. , 2005, American journal of clinical pathology.

[51]  C. Fenoglio-Preiser,et al.  Mixed Hyperplastic Adenomatous Polyps/Serrated Adenomas: A Distinct Form of Colorectal Neoplasia , 1990, The American journal of surgical pathology.

[52]  A. Jemal,et al.  Cancer Statistics, 2008 , 2008, CA: a cancer journal for clinicians.

[53]  S. Berndt,et al.  Genetic Variation in the Nucleotide Excision Repair Pathway and Colorectal Cancer Risk , 2006, Cancer Epidemiology Biomarkers & Prevention.

[54]  A. Neugut,et al.  Cigarette smoking and the colorectal adenoma-carcinoma sequence: a hypothesis to explain the paradox. , 1998, American journal of epidemiology.

[55]  L. Tanoue Smoking and Smoking Cessation in Relation to Mortality in Women , 2009 .

[56]  G. Fraser,et al.  Dietary risk factors for colon cancer in a low-risk population. , 1998, American journal of epidemiology.

[57]  T Katoh,et al.  Glutathione S-transferase (GST) M1, T1, P1, N-acetyltransferase (NAT) 1 and 2 genetic polymorphisms and susceptibility to colorectal cancer. , 1999, Journal of UOEH.

[58]  Theo Stijnen,et al.  Advanced methods in meta‐analysis: multivariate approach and meta‐regression , 2002, Statistics in medicine.

[59]  Perry J Pickhardt,et al.  Screening and Surveillance for the Early Detection of Colorectal Cancer and Adenomatous Polyps, 2008: A Joint Guideline from the American Cancer Society, the US Multi‐Society Task Force on Colorectal Cancer, and the American College of Radiology * † , 2008, CA: a cancer journal for clinicians.

[60]  H. Brenner,et al.  Cigarette smoking and colorectal cancer risk in Germany: A population‐based case–control study , 2006, International journal of cancer.

[61]  L Nyström,et al.  Smoking and colorectal cancer: a 20-year follow-up study of Swedish construction workers. , 1996, Journal of the National Cancer Institute.

[62]  P. A. van den Brandt,et al.  Alcohol and the risk of colon and rectal cancer with mutations in the K-ras gene. , 2006, Alcohol.

[63]  C. Ulrich,et al.  TGFbeta1 polymorphism (L10P) and risk of colorectal adenomatous and hyperplastic polyps. , 2004, International journal of epidemiology.

[64]  W. Willett,et al.  A prospective study of body mass, height, and smoking on the risk of colorectal cancer in women , 1991, Cancer Causes & Control.

[65]  W. Koh,et al.  Cigarettes and alcohol in relation to colorectal cancer: the Singapore Chinese Health Study , 2007, British Journal of Cancer.

[66]  L. Kolonel,et al.  Smoking and Colorectal Cancer: Different Effects by Type of Cigarettes? , 2007, Cancer Epidemiology Biomarkers & Prevention.

[67]  Bondy,et al.  Cigarette smoking and risk of death from colorectal cancer in women , 2000, Colorectal disease : the official journal of the Association of Coloproctology of Great Britain and Ireland.

[68]  T. French,et al.  Tobacco, Alcohol, Coffee, and Caffeine as Risk Factors for Colon Cancer in a Low‐Risk Population , 1990, Epidemiology.

[69]  E. Riboli,et al.  Prospective study of diet and female colorectal cancer: the New York University Women's Health Study. , 1997, Nutrition and cancer.

[70]  H. Daniell,et al.  More advanced colonic cancer among smokers , 1986, Cancer.

[71]  S. Greenland,et al.  Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. , 1992, American journal of epidemiology.

[72]  T. Key,et al.  Nutrition, lifestyle and colorectal cancer incidence: a prospective investigation of 10 998 vegetarians and non-vegetarians in the United Kingdom , 2004, British Journal of Cancer.

[73]  C. la Vecchia,et al.  Cigarette smoking and colorectal cancer: a study of 1,584 cases and 2,879 controls. , 1995, Preventive medicine.

[74]  L. Tamer,et al.  Glutathione S-Transferase M1, T1, P1 Genotypes and Risk for Development of Colorectal Cancer , 2005, Biochemical Genetics.

[75]  K. Slim,et al.  Tobacco Smoking: A Factor of Early Onset of Colorectal Cancer , 2006, Diseases of the colon and rectum.

[76]  M. Marmot,et al.  Cigarette smoking and site-specific cancer mortality: testing uncertain associations using extended follow-up of the original Whitehall study. , 2008, Annals of oncology : official journal of the European Society for Medical Oncology.

[77]  J. Nasu,et al.  Relation of family history of cancer and environmental factors to the risk of colorectal cancer: a case-control study. , 1995, Japanese journal of clinical oncology.

[78]  M. Thun,et al.  Cigarette smoking and colorectal cancer mortality in the cancer prevention study II. , 2000, Journal of the National Cancer Institute.

[79]  J. Potter,et al.  Tobacco use and colon cancer , 1997, International journal of cancer.

[80]  A. Miller,et al.  Prospective cohort study of cigarette smoking and colorectal cancer risk in women , 2002, International journal of cancer.

[81]  H. Anton-Culver Smoking and other risk factors associated with the stage and age of diagnosis of colon and rectum cancers. , 1991, Cancer detection and prevention.

[82]  C. Begg,et al.  Operating characteristics of a rank correlation test for publication bias. , 1994, Biometrics.

[83]  T. Lesnick,et al.  Higher risk of mismatch repair-deficient colorectal cancer in alpha(1)-antitrypsin deficiency carriers and cigarette smokers. , 2000, Molecular genetics and metabolism.

[84]  R. Roetzheim,et al.  Predictors of advanced stage colorectal cancer diagnosis: results of a population-based study. , 2001, Cancer detection and prevention.

[85]  J. Cerhan,et al.  Cigarette smoking and risk of bladder, pancreas, kidney, and colorectal cancers in Iowa. , 2001, Annals of epidemiology.

[86]  S N Thibodeau,et al.  Microsatellite instability in cancer of the proximal colon. , 1993, Science.

[87]  A. Weston,et al.  Diminutive colonic polyps: histopathology, spatial distribution, concomitant significant lesions, and treatment complications. , 1995, The American journal of gastroenterology.

[88]  Qing Chen,et al.  The association of the DNA repair gene XRCC3 Thr241Met polymorphism with susceptibility to colorectal cancer in a Chinese population. , 2005, Cancer genetics and cytogenetics.

[89]  W. Bodmer,et al.  Genetic pathways in colorectal and other cancers. , 1999, European journal of cancer.

[90]  T. Rohan,et al.  Association between cigarette smoking and colorectal cancer in the Women's Health Initiative. , 2007, Journal of the National Cancer Institute.

[91]  J. Buring,et al.  Development of a risk score for colorectal cancer in men. , 2007, The American journal of medicine.

[92]  E. Rogot,et al.  Smoking and causes of death among U.S. veterans: 16 years of observation. , 1980, Public health reports.

[93]  Kahn Ha The Dorn Study of Smoking and Mortality Among U.S. Veterans: Report on Eight and One-Half Years of Observation , 1966 .

[94]  T. Mack,et al.  A case-control study of occupational and dietary factors in colorectal cancer in young men by subsite. , 1989, Cancer research.

[95]  J. Ferlay,et al.  Global Cancer Statistics, 2002 , 2005, CA: a cancer journal for clinicians.

[96]  W. Willett,et al.  A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in U.S. women. , 1994, Journal of the National Cancer Institute.

[97]  Chien-Jen Chen,et al.  Mortality attributable to cigarette smoking in Taiwan: a 12-year follow-up study , 1998, Tobacco control.

[98]  H. Morrison,et al.  Diet and vitamin or mineral supplementation and risk of colon cancer by subsite in Canada , 2007, European journal of cancer prevention : the official journal of the European Cancer Prevention Organisation.

[99]  R. Guéguen,et al.  [Alcohol, tobacco and colorectal adenomas and cancer. Case-control study in a population with positive fecal occult blood tests]. , 2007, Presse medicale.

[100]  R Doll,et al.  Mortality from cancer in relation to smoking: 50 years observations on British doctors , 2005, British Journal of Cancer.

[101]  H. Lynch,et al.  Tobacco use and increased colorectal cancer risk in patients with hereditary nonpolyposis colorectal cancer (Lynch syndrome). , 2004, Archives of internal medicine.

[102]  Jae-IlKim,et al.  hOGG1 Ser326Cys polymorphism modifies the significance of the environmental risk factor for colon cancer , 2003 .

[103]  H. Tajiri,et al.  High frequency of K-ras mutations in human colorectal hyperplastic polyps. , 1997, Gut.

[104]  W. Willett,et al.  Alcohol Intake and Colorectal Cancer: A Pooled Analysis of 8 Cohort Studies , 2004, Annals of Internal Medicine.

[105]  B. Henderson,et al.  A Prospective Study” , 2007 .

[106]  R. Glynn,et al.  Lifetime cigarette smoking and colorectal cancer incidence in the Physicians' Health Study I. , 2000, Journal of the National Cancer Institute.

[107]  Jian-Min Yuan,et al.  Morbidity and mortality in relation to smoking among women and men of Chinese ethnicity: the Singapore Chinese Health Study. , 2008, European journal of cancer.

[108]  P. Vihko,et al.  Colorectal carcinoma associated with serrated adenoma – prevalence, histological features, and prognosis , 2001, The Journal of pathology.

[109]  B. Levin,et al.  Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. , 2008, Gastroenterology.

[110]  E. Rimm,et al.  A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in U.S. men. , 1994, Journal of the National Cancer Institute.

[111]  S. Wacholder,et al.  Risk factors for colorectal cancer in a prospective study among U.S. white men , 1998, International journal of cancer.

[112]  L. Kolonel,et al.  Associations of sedentary lifestyle, obesity, smoking, alcohol use, and diabetes with the risk of colorectal cancer. , 1997, Cancer research.

[113]  Majid Ezzati,et al.  Estimates of global mortality attributable to smoking in 2000 , 2003, The Lancet.

[114]  E. Kampman,et al.  Role of EPHX genotype in the associations of smoking and diet with colorectal adenomas. , 2002, IARC scientific publications.

[115]  M. Longnecker,et al.  Associations between smoking status and stage of colorectal cancer at diagnosis in massachusetts between 1982 and 1987 , 1989, Cancer.

[116]  J P Vandenbroucke,et al.  Bias in meta-analysis detected by a simple, graphical test , 1998 .

[117]  Jia Cao,et al.  CYP2E1 Rsa I polymorphism impacts on risk of colorectal cancer association with smoking and alcohol drinking. , 2007, World journal of gastroenterology.

[118]  H. Dorn Tobacco consumption and mortality from cancer and other diseases. , 1959, Acta - Unio Internationalis Contra Cancrum.

[119]  D. Thelle,et al.  Mortality in relation to smoking history: 13 years' follow-up of 68,000 Norwegian men and women 35-49 years. , 1993, Journal of clinical epidemiology.

[120]  S. Thompson,et al.  Quantifying heterogeneity in a meta‐analysis , 2002, Statistics in medicine.

[121]  Y. Minami,et al.  Associations between cigarette smoking and the risk of four leading cancers in Miyagi Prefecture, Japan: A multi‐site case‐control study , 2003, Cancer science.

[122]  S. Tominaga,et al.  A Case‐Control Study of Male Colorectal Cancer in Aichi Prefecture, Japan: with Special Reference to Occupational Activity Level, Drinking Habits and Family History , 1990, Japanese journal of cancer research : Gann.

[123]  E. Kampman,et al.  Cigarette smoking and genetic alterations in sporadic colon carcinomas. , 2003, Carcinogenesis.

[124]  J. Cerhan,et al.  Cigarette smoking and colorectal cancer: long-term, subsite-specific risks in a cohort study of postmenopausal women. , 2003, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[125]  W. King,et al.  Health risk behaviors: examining social inequalities in bladder and colorectal cancers. , 2008, Annals of epidemiology.

[126]  S. Akiba,et al.  Cigarette smoking and cancer mortality risk in Japanese men and women--results from reanalysis of the six-prefecture cohort study data. , 1990, Environmental health perspectives.

[127]  P. Peltomäki Role of DNA mismatch repair defects in the pathogenesis of human cancer. , 2003, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[128]  Peter Boyle,et al.  Tobacco smoking and cancer: A meta‐analysis , 2008, International journal of cancer.

[129]  J. Jass Serrated route to colorectal cancer: back street or super highway? , 2001, The Journal of pathology.

[130]  J. Samet,et al.  Smoking and Cancer Risk in Korean Men and Women , 2004, Cancer Causes & Control.

[131]  R Doll,et al.  Mortality in relation to smoking: 40 years' observations on male British doctors , 1994, BMJ.

[132]  J. Mclaughlin,et al.  Increased risk of colorectal cancer among smokers: Results of a 26‐year follow‐up of us veterans and a review , 1994, International journal of cancer.

[133]  H. Kashihara,et al.  Case-control study of colorectal carcinoma in situ and cancer in relation to cigarette smoking and alcohol use (Japan) , 1997, Cancer Causes & Control.

[134]  L. Tryggvadottir,et al.  Risk factors for malignant diseases: a cohort study on a population of 22,946 Icelanders. , 1997, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[135]  R. Sandler,et al.  Cigarette smoking and the risk of colorectal cancer in women. , 1988, Journal of the National Cancer Institute.

[136]  R. Goldbohm,et al.  Cigarette smoking and colorectal cancer: APC mutations, hMLH1 expression, and GSTM1 and GSTT1 polymorphisms. , 2005, American Journal of Epidemiology.

[137]  M Schumacher,et al.  Modelling the effects of standard prognostic factors in node-positive breast cancer , 1999, British Journal of Cancer.

[138]  S Greenland,et al.  Quantitative methods in the review of epidemiologic literature. , 1987, Epidemiologic reviews.

[139]  A. LaCroix,et al.  Epidemiology of sociodemographic characteristics, lifestyle, medical history, and colon cancer: a case-control study among French Canadians in Montreal. , 1998, Cancer detection and prevention.

[140]  A. Dyer,et al.  Cigarette smoking and colorectal carcinoma mortality in a cohort with long‐term follow‐up , 2004, Cancer.

[141]  R. Guéguen,et al.  Le tabac et l'alcool augmentent le risque d'adénomes et de cancers colorectaux: Étude comparant 3 292 cas avec 5 456 témoins dans une population à risque moyen ayant eu un test de dépistage de sang dans les selles positif , 2007 .