Cigarette smoking, use of other tobacco products and stomach cancer mortality in US adults: The Cancer Prevention Study II

Cigarette smoking is associated with increased risk of stomach cancer in many studies but there are limited data on this relationship in women and on risk associated with use of tobacco products other than cigarettes. We examined stomach cancer death rates in relation to cigarette smoking in women and use of cigarette, cigar, pipe, or smokeless tobacco in men in a nationwide prospective mortality study in the United States (US). Cohort follow‐up from 1982–96 identified 996 and 509 stomach cancer deaths among 467,788 men and 588,053 women, respectively. Cox proportional hazards models were fitted to estimate rate ratios (RR) and 95% confidence intervals (CI) using non‐users of tobacco as the referent group. Multivariate‐adjusted RRs were the highest for men who currently smoked cigars (RR = 2.29, 95% CI = 1.49–3.51) or cigarettes (RR = 2.16, 95% CI = 1.75–2.67) and both increased with smoking duration. Women who currently (RR = 1.49, 95% CI = 1.18–1.88) or formerly (RR = 1.36, 95% CI = 1.08–1.71) smoked cigarettes were at significantly increased risk, as were men who formerly smoked cigarettes (RR = 1.55, 95% CI = 1.28–1.88), or currently (RR = 1.81, 95% CI = 1.40–2.35) or formerly (RR: 1.57, 95% CI = 1.22–2.03) used more than one type of tobacco. Men who reported a history of chronic indigestion or gastroduodenal ulcer had substantially higher mortality rates associated with current cigarette (RR = 3.45, 95% CI = 2.05–5.80) or cigar (RR = 8.93, 95% CI = 4.02–19.90) smoking, as did men who were current aspirin users. If causal, the estimated proportion of stomach cancer deaths attributable to tobacco use would be 28% in US men and 14% in women. We conclude that prolonged use of tobacco products is associated with increased stomach cancer mortality in men and women. The accumulated evidence from this and other studies support reconsidering stomach cancer as a tobacco‐related cancer. © 2002 Wiley‐Liss, Inc.

[1]  M. Plummer,et al.  International agency for research on cancer. , 2020, Archives of pathology.

[2]  J. Fraumeni,et al.  Smoking and cancer mortality among U.S. veterans: A 26‐year follow‐up , 2006, International journal of cancer.

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

[4]  M. Thun,et al.  A prospective study of diet and stomach cancer mortality in United States men and women. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[5]  M. McCullough,et al.  A prospective study of diet and stomach cancer mortality in US men and women , 2001 .

[6]  Leslie Bernstein,et al.  A multiethnic population-based study of smoking, alcohol and body size and risk of adenocarcinomas of the stomach and esophagus (United States) , 2001, Cancer Causes & Control.

[7]  V. Moreno,et al.  A case‐control study of gastric cancer in Venezuela , 2001, International journal of cancer.

[8]  S. Andreola,et al.  Effect of lifestyle, smoking, and diet on development of intestinal metaplasia in H. pylori-positive subjects , 2001, American Journal of Gastroenterology.

[9]  A. Axon,et al.  Influence of smoking and alcohol on gastric chemokine mRNA expression in patients with Helicobacter pylori infection , 2001, Journal of clinical pathology.

[10]  P. Simpson,et al.  Statistical methods in cancer research , 2001, Journal of surgical oncology.

[11]  G. Berglund,et al.  Tobacco smoking increases the risk for gastric adenocarcinoma among Helicobacter pylori-infected individuals. , 2001, Scandinavian journal of gastroenterology.

[12]  Ś. Ziemlański,et al.  Tobacco smoking and vitamin C concentration in gastric juice in healthy subjects and patients with Helicobacter pylori infection , 2000, European journal of cancer prevention : the official journal of the European Cancer Prevention Organisation.

[13]  M. Blaser,et al.  Gastric dysplasia and gastric cancer: Helicobacter pylori, serum vitamin C, and other risk factors. , 2000, Journal of the National Cancer Institute.

[14]  L J Schouten,et al.  Trends in incidence of adenocarcinoma of the oesophagus and gastric cardia in ten European countries. , 2000, International journal of epidemiology.

[15]  D. Zaridze,et al.  Alcohol Consumption, Smoking and Risk of Gastric Cancer: Case—Control Study from Moscow, Russia , 2000, Cancer Causes & Control.

[16]  T. Mizoue,et al.  Prospective study on the relation of cigarette smoking with cancer of the liver and stomach in an endemic region. , 2000, International journal of epidemiology.

[17]  A. Lindgren,et al.  The role of tobacco, snuff and alcohol use in the aetiology of cancer of the oesophagus and gastric cardia , 2000, International journal of cancer.

[18]  J. Ferlay,et al.  Erratum: Estimates of the worldwide mortality from 25 cancers in 1990. Int. J. Cancer, 83, 18–29 (1999). , 1999, International journal of cancer.

[19]  L. Hansson,et al.  Tobacco, alcohol and the risk of gastric cancer by sub‐site and histologic type , 1999, International journal of cancer.

[20]  J. Ferlay,et al.  Estimates of the worldwide mortality from 25 cancers in 1990 , 1999, International journal of cancer.

[21]  M. Blaser,et al.  Hypothesis: the changing relationships of Helicobacter pylori and humans: implications for health and disease. , 1999, The Journal of infectious diseases.

[22]  Frank J. Chaloupka,et al.  Curbing the epidemic: governments and the economics of tobacco control , 1999, Tobacco control.

[23]  Jacques Ferlay,et al.  Estimates of the worldwide incidence of 25 major cancers in 1990 , 1999, International journal of cancer.

[24]  S. Hecht,et al.  DNA adduct formation from tobacco-specific N-nitrosamines. , 1999, Mutation research.

[25]  J. Fraumeni,et al.  Changing patterns in the incidence of esophageal and gastric carcinoma in the United States , 1998, Cancer.

[26]  A. Price,et al.  Plasma free radical activity and antioxidant vitamin levels in dyspeptic patients: correlation with smoking and Helicobacter pylori infection , 1998, European journal of gastroenterology & hepatology.

[27]  M. Blaser Helicobacter pylori and gastric diseases , 1998, BMJ.

[28]  P. Boffetta,et al.  Tobacco Smoking and Alcohol Drinking as Risk Factors for Stomach Cancer: a Case-Control Study in Uruguay , 1998, Cancer Causes & Control.

[29]  J. Jang,et al.  Benzo[a]pyrene diol-epoxide-I-DNA and oxidative DNA adducts associated with gastric adenocarcinoma. , 1998, Cancer letters.

[30]  A B West,et al.  An inverse relation between cagA+ strains of Helicobacter pylori infection and risk of esophageal and gastric cardia adenocarcinoma. , 1998, Cancer research.

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

[32]  M. Gammon,et al.  Tobacco, alcohol, and socioeconomic status and adenocarcinomas of the esophagus and gastric cardia. , 1997, Journal of the National Cancer Institute.

[33]  Rodolfo Saracci,et al.  Tobacco smoking and gastric cancer: Review and meta‐analysis , 1997, International journal of cancer.

[34]  Alan D. Lopez,et al.  Alternative projections of mortality and disability by cause 1990–2020: Global Burden of Disease Study , 1997, The Lancet.

[35]  D Hoffmann,et al.  The changing cigarette, 1950-1995. , 1997, Journal of toxicology and environmental health.

[36]  V. Shanta,et al.  Lifestyle and risk of stomach cancer: a hospital-based case-control study. , 1996, International journal of epidemiology.

[37]  R. Kurtz,et al.  Adenocarcinomas of the esophagus and gastric cardia: medical conditions, tobacco, alcohol, and socioeconomic factors. , 1996, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[38]  J. Fraumeni,et al.  The influence of cigarette smoking, alcohol, and green tea consumption on the risk of carcinoma of the cardia and distal stomach in Shanghai, China , 1996, Cancer.

[39]  A. Kristal,et al.  Obesity, alcohol, and tobacco as risk factors for cancers of the esophagus and gastric cardia: adenocarcinoma versus squamous cell carcinoma. , 1995, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[40]  G. Giovino,et al.  Surveillance for selected tobacco-use behaviors--United States, 1900-1994. , 1994, MMWR. CDC surveillance summaries : Morbidity and mortality weekly report. CDC surveillance summaries.

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

[42]  F. Leung,et al.  Effects of smoking and nicotine on the gastric mucosa: a review of clinical and experimental evidence. , 1994, Gastroenterology.

[43]  P. Taylor,et al.  A nested case-control study of oesophageal and stomach cancers in the Linxian nutrition intervention trial. , 1994, International journal of epidemiology.

[44]  H. Adami,et al.  Tobacco, alcohol and the risk of gastric cancer. A population‐based case‐control study in Sweden , 1994, International journal of cancer.

[45]  M. Inoue,et al.  Life‐style and subsite of gastric cancer—joint effect of smoking and drinking habits , 1994, International journal of cancer.

[46]  H. Boeing,et al.  Vodka consumption, tobacco smoking and risk of gastric cancer in Poland. , 1993, International journal of epidemiology.

[47]  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.

[48]  E. Wynder,et al.  Tobacco, alcohol intake, and diet in relation to adenocarcinoma of the esophagus and gastric cardia , 1993, Cancer Causes & Control.

[49]  E. Calle,et al.  Utility of the National Death Index for ascertainment of mortality among cancer prevention study II participants. , 1993, American journal of epidemiology.

[50]  R. C. Garner,et al.  Smoking‐related dna adducts in human gastric cancers , 1992, International journal of cancer.

[51]  M. Blaser,et al.  Potentiation of Helicobacter pylori vacuolating toxin activity by nicotine and other weak bases. , 1992, The Journal of infectious diseases.

[52]  Y. Hoshiyama,et al.  A case-control study of stomach cancer and its relation to diet, cigarettes, and alcohol consumption in Saitama Prefecture, Japan , 1992, Cancer Causes & Control.

[53]  J. Fraumeni,et al.  Cigarette smoking and other risk factors for progression of precancerous stomach lesions. , 1992, Journal of the National Cancer Institute.

[54]  S. Tominaga,et al.  A Prospective Study of Stomach Cancer among a Rural Japanese Population: A 6‐Year Survey , 1992, Japanese journal of cancer research : Gann.

[55]  Alan D. Lopez,et al.  Mortality from tobacco in developed countries: indirect estimation from national vital statistics , 1992, The Lancet.

[56]  C. González,et al.  Consumption of alcohol, coffee, and tobacco, and gastric cancer in Spain , 1992, Cancer Causes & Control.

[57]  S. Bianchi,et al.  A case-control study of cancers of the gastric cardia in Italy. , 1992, British Journal of Cancer.

[58]  S. Wacholder,et al.  A cohort study of stomach cancer in a high‐risk american population , 1991, Cancer.

[59]  Sam Smoking-attributable mortality and years of potential life lost--United States, 1988. , 1991, MMWR. Morbidity and mortality weekly report.

[60]  C. Hsieh,et al.  Risk factors for stomach cancer: a population-based case-control study in Shanghai , 1991, Cancer Causes & Control.

[61]  S. Saha Smoking Habits and Carcinoma of the Stomach: A Case‐Control Study , 1991, Japanese journal of cancer research : Gann.

[62]  H. Boeing,et al.  Case‐control study on stomach cancer in Germany , 1991, International journal of cancer.

[63]  S. Tominaga,et al.  A comparative case-control analysis of stomach cancer and atrophic gastritis. , 1990, Cancer research.

[64]  T. Mack,et al.  Life-style, workplace, and stomach cancer by subsite in young men of Los Angeles County. , 1990, Cancer research.

[65]  R. Severson,et al.  A prospective study of stomach cancer and its relation to diet, cigarettes, and alcohol consumption. , 1990, Cancer research.

[66]  C. la Vecchia,et al.  Socioeconomic indicators, tobacco and alcohol in the aetiology of digestive tract neoplasms. , 1989, International journal of epidemiology.

[67]  R. Heidel,et al.  Reducing the Health Consequences of Smoking: 25 Years of Progress. A Report of the Surgeon General. , 1989 .

[68]  B. Henderson,et al.  Diet and high risk of stomach cancer in Shandong, China. , 1988, Cancer research.

[69]  S. Kono,et al.  Cigarette smoking, alcohol and cancer mortality: a cohort study of male Japanese physicians. , 1987, Japanese journal of cancer research : Gann.

[70]  G. Eklund,et al.  Mortality in relation to cigarette and pipe smoking: 16 years' observation of 25,000 Swedish men. , 1987, Journal of epidemiology and community health.

[71]  W. Jędrychowski,et al.  A case‐control study of dietary factors and stomach cancer risk in Poland , 1986, International journal of cancer.

[72]  S. Müller-lissner,et al.  Bile reflux is increased in cigarette smokers. , 1986, Gastroenterology.

[73]  L. Pickle,et al.  Dietary determinants of gastric cancer in south Louisiana inhabitants. , 1985, Journal of the National Cancer Institute.

[74]  N. Breslow,et al.  Statistical methods in cancer research: volume 1- The analysis of case-control studies , 1980 .

[75]  N. Breslow,et al.  Statistical methods in cancer research. Vol. 1. The analysis of case-control studies. , 1981 .

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

[77]  F. D. H. Hall St. Luke's Hostel , 1895 .

[78]  William Meade CHEMISTRY AND TOXICOLOGY. , 1834 .

[79]  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.

[80]  M. Thun,et al.  Vitamin C, vitamin E, and multivitamin supplement use and stomach cancer mortality in the Cancer Prevention Study II cohort. , 2002, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[81]  M. Corrao Tobacco control country profiles , 2000 .

[82]  S. Vollset,et al.  Helicobacter pylori infection and risk of cardia cancer and non-cardia gastric cancer. A nested case-control study. , 1999, Scandinavian journal of gastroenterology.

[83]  H. Ramroth,et al.  Effect of Helicobacter pylori infection, smoking and dietary habits on the occurrence of antrum intestinal metaplasia. Clinico-epidemiological study in Poland. , 1999, Polish journal of pathology : official journal of the Polish Society of Pathologists.

[84]  L. Sobin,et al.  Risk of stomach cancer in relation to consumption of cigarettes, alcohol, tea and coffee in Warsaw, Poland. , 1999, International journal of cancer.

[85]  Y. Kodera,et al.  Influence of habitual smoking on gastric cancer by histologic subtype. , 1999, International journal of cancer.

[86]  D. Burns,et al.  Cigar Smoking : Overview and Current State of the Science , 1998 .

[87]  Smoking-attributable mortality and years of potential life lost--United States, 1984. , 1997, MMWR. Morbidity and mortality weekly report.

[88]  R. Doll Cancers weakly related to smoking. , 1996, British medical bulletin.

[89]  S. Hecht,et al.  Carcinogen biomarkers related to smoking and upper aerodigestive tract cancer , 1993, Journal of cellular biochemistry. Supplement.

[90]  Á. Lanas,et al.  Influence of smoking on basal and on vagally and maximally stimulated gastric acid and pepsin secretion. , 1992, Scandinavian journal of gastroenterology.

[91]  J. Fraumeni,et al.  A cohort study of stomach cancer in a high‐risk American population , 2006 .

[92]  I S Anishchenko,et al.  [Stomach cancer]. , 1981, Fel'dsher i akusherka.

[93]  D. Cox Regression Models and Life-Tables , 1972 .

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

[95]  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.

[96]  Smoking and Tobacco Control Monograph No . 9 , 2022 .