Gastric Cancer: Descriptive Epidemiology, Risk Factors, Screening, and Prevention

Less than a century ago, gastric cancer was the most common cancer in the United States and perhaps throughout the world. Despite its worldwide decline in incidence over the past century, gastric cancer remains a major killer across the globe. This article reviews the epidemiology, screening, and prevention of gastric cancer. We first discuss the descriptive epidemiology of gastric cancer, including its incidence, survival, mortality, and trends over time. Next, we characterize the risk factors for gastric cancer, both environmental and genetic. Serologic markers and histological precursor lesions of gastric cancer and early detection of gastric cancer using these markers are reviewed. Finally, we discuss prevention strategies and provide suggestions for further research. Cancer Epidemiol Biomarkers Prev; 23(5); 700–13. ©2014 AACR.

[1]  C. la Vecchia,et al.  Cancer Mortality in Migrant Populations within Italy , 1988, Tumori.

[2]  C. Abnet,et al.  Serum pepsinogens and risk of gastric and oesophageal cancers in the General Population Nutrition Intervention Trial cohort , 2009, Gut.

[3]  Y. Loke,et al.  Reduced esophageal cancer incidence in statin users, particularly with cyclo-oxygenase inhibition. , 2013, World journal of gastrointestinal pharmacology and therapeutics.

[4]  P. Correa,et al.  Human gastric carcinogenesis: a multistep and multifactorial process--First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. , 1992, Cancer research.

[5]  Nomura Am,et al.  Multiethnic studies of diet, nutrition, and cancer in Hawaii. , 1985 .

[6]  Jennifer G. Robinson,et al.  2013 ACC/AHA Guideline on the Assessment of Cardiovascular Risk: A Report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines , 2014, Circulation.

[7]  D. Forman,et al.  Gastric cancer: global pattern of the disease and an overview of environmental risk factors. , 2006, Best practice & research. Clinical gastroenterology.

[8]  Tai-xiang Wu,et al.  Consumption of large amounts of Allium vegetables reduces risk for gastric cancer in a meta-analysis. , 2011, Gastroenterology.

[9]  D. Shibata,et al.  Elevated antibody titers to Epstein‐Barr virus prior to the diagnosis of Epstein‐Barr‐virus‐associated gastric adenocarcinoma , 1995, International journal of cancer.

[10]  D. Morgan,et al.  Sex Hormones, Hormonal Interventions, and Gastric Cancer Risk: A Meta-analysis , 2011, Cancer Epidemiology, Biomarkers & Prevention.

[11]  T. Byers.  Physical Activity and Gastric Cancer: So What? An Epidemiologist's Confession , 2013, Cancer Prevention Research.

[12]  K. Choi,et al.  Screening for Gastric Cancer in Korea: Population-Based Preferences for Endoscopy versus Upper Gastrointestinal Series , 2009, Cancer Epidemiology Biomarkers & Prevention.

[13]  D. Corley,et al.  Influence of site classification on cancer incidence rates: an analysis of gastric cardia carcinomas. , 2004, Journal of the National Cancer Institute.

[14]  R. Malekzadeh,et al.  Opium: An emerging risk factor for gastric adenocarcinoma , 2013, International journal of cancer.

[15]  R. Malekzadeh,et al.  Opium Use and Risk of Mortality from Digestive Diseases: A Prospective Cohort Study , 2013, The American Journal of Gastroenterology.

[16]  M. Blaser,et al.  Population attributable risks of esophageal and gastric cancers. , 2003, Journal of the National Cancer Institute.

[17]  R. Malekzadeh,et al.  Neglected role of hookah and opium in gastric carcinogenesis: A cohort study on risk factors and attributable fractions , 2014, International journal of cancer.

[18]  J. Paul,et al.  Oesophageal and gastric intestinal-type adenocarcinomas show the same male predominance due to a 17 year delayed development in females , 2008, Gut.

[19]  E. Feuer,et al.  SEER Cancer Statistics Review, 1975-2003 , 2006 .

[20]  A. Jemal,et al.  Annual Report to the Nation on the status of cancer, 1975‐2010, featuring prevalence of comorbidity and impact on survival among persons with lung, colorectal, breast, or prostate cancer , 2014, Cancer.

[21]  R. Hunt,et al.  Asia–Pacific consensus guidelines on gastric cancer prevention , 2008, Journal of gastroenterology and hepatology.

[22]  H. Brenner,et al.  Gastric Parietal Cell Antibodies, Helicobacter Pylori Infection, and Chronic Atrophic Gastritis: Evidence from a Large Population-based Study in Germany , 2013, Cancer Epidemiology, Biomarkers & Prevention.

[23]  P. Taylor,et al.  Nutritional interventions in cancer prevention. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[24]  Siddharth Singh,et al.  Statins are associated with reduced risk of gastric cancer: a systematic review and meta-analysis. , 2013, Annals of oncology : official journal of the European Society for Medical Oncology.

[25]  D. Huntsman,et al.  Gastric cancer: New genetic developments , 2005, Journal of surgical oncology.

[26]  P. Moayyedi,et al.  Gastric Cancer Consensus Conference Recommends Helicobacter pylori Screening and Treatment in Asymptomatic Persons From High-Risk Populations to Prevent Gastric Cancer , 2008, The American Journal of Gastroenterology.

[27]  C. Abnet,et al.  Prospective study of tooth loss and incident esophageal and gastric cancers in China , 2001, Cancer Causes and Control.

[28]  F. Bazzoli,et al.  Meta-analysis: Can Helicobacter pylori Eradication Treatment Reduce the Risk for Gastric Cancer? , 2009, Annals of Internal Medicine.

[29]  Scott M. Williams,et al.  Race, African Ancestry, and Helicobacter pylori Infection in a Low-Income United States Population , 2011, Cancer Epidemiology, Biomarkers & Prevention.

[30]  K. McColl,et al.  Gender, hiatus hernia and Barrett's oesophagus. , 2009, Gut.

[31]  F. Kamangar,et al.  The state of nutritional epidemiology: why we are still unsure of what we should eat? , 2013, Archives of Iranian medicine.

[32]  P. Laurén,et al.  THE TWO HISTOLOGICAL MAIN TYPES OF GASTRIC CARCINOMA: DIFFUSE AND SO-CALLED INTESTINAL-TYPE CARCINOMA. AN ATTEMPT AT A HISTO-CLINICAL CLASSIFICATION. , 1965, Acta pathologica et microbiologica Scandinavica.

[33]  Xiaolin Wang,et al.  Body Mass Index and Risk of Gastric Cancer: A Meta-analysis of a Population with More Than Ten Million from 24 Prospective Studies , 2013, Cancer Epidemiology, Biomarkers & Prevention.

[34]  S. Kato,et al.  A novel germline mutation of the LKB1 gene in a patient with Peutz-Jeghers syndrome with early-onset gastric cancer , 2004, Journal of Gastroenterology.

[35]  S. Tsugane,et al.  Salt and salted food intake and subsequent risk of gastric cancer among middle-aged Japanese men and women , 2004, British Journal of Cancer.

[36]  S. N. Thornton,et al.  Salt in health and disease--a delicate balance. , 2013, The New England journal of medicine.

[37]  Jeongseon Kim,et al.  Gastric cancer and salt preference: a population-based cohort study in Korea. , 2010, The American journal of clinical nutrition.

[38]  C. Abnet,et al.  Cigarette smoking and adenocarcinomas of the esophagus and esophagogastric junction: a pooled analysis from the international BEACON consortium. , 2010, Journal of the National Cancer Institute.

[39]  C. Abnet,et al.  Interleukin-1B Polymorphisms and Gastric Cancer Risk—A Meta-analysis , 2006, Cancer Epidemiology Biomarkers & Prevention.

[40]  M. Salgaller.  American Association for Cancer Research , 2000, Expert opinion on investigational drugs.

[41]  Yusuke Nakamura,et al.  Genetic variation in PSCA is associated with susceptibility to diffuse-type gastric cancer , 2008, Nature Genetics.

[42]  D. Gotley,et al.  Combined effects of obesity, acid reflux and smoking on the risk of adenocarcinomas of the oesophagus , 2007, Gut.

[43]  M. Dinis-Ribeiro,et al.  Screening for Gastric Cancer and Surveillance of Premalignant Lesions: a Systematic Review of Cost‐Effectiveness Studies , 2013, Helicobacter.

[44]  S. Chin,et al.  Germline CDH1 deletions in hereditary diffuse gastric cancer families , 2009, Human molecular genetics.

[45]  C. la Vecchia,et al.  Family history and the risk of stomach and colorectal cancer , 1992, Cancer.

[46]  Bin Liu,et al.  : Genome-wide association study of esophageal squamous cell carcinoma in Chinese subjects identifies susceptibility loci at PLCE1 and , 2010 .

[47]  Martin Wiseman,et al.  The Second World Cancer Research Fund/American Institute for Cancer Research Expert Report. Food, Nutrition, Physical Activity, and the Prevention of Cancer: A Global Perspective , 2008, Proceedings of the Nutrition Society.

[48]  R. Hunt,et al.  Second Asia–Pacific Consensus Guidelines for Helicobacter pylori infection , 2009, Journal of gastroenterology and hepatology.

[49]  David F Ransohoff,et al.  Principles of cancer screening: lessons from history and study design issues. , 2010, Seminars in oncology.

[50]  P. Hall,et al.  Stomach cancer risk after treatment for hodgkin lymphoma. , 2013, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[51]  Jack Coulehan,et al.  Family History , 2014, Annals of Internal Medicine.

[52]  K. Yao,et al.  White opaque substance within superficial elevated gastric neoplasia as visualized by magnification endoscopy with narrow-band imaging: a new optical sign for differentiating between adenoma and carcinoma. , 2008, Gastrointestinal endoscopy.

[53]  B. Marshall,et al.  UNIDENTIFIED CURVED BACILLI ON GASTRIC EPITHELIUM IN ACTIVE CHRONIC GASTRITIS , 1983, The Lancet.

[54]  N. Rothman,et al.  Plasma pepsinogens, antibodies against Helicobacter pylori, and risk of gastric cancer in the Shanghai Women's Health Study Cohort , 2011, British Journal of Cancer.

[55]  H. Adami,et al.  Early‐life risk indicators of gastric cancer. A population‐based case‐control study in sweden , 1994, International journal of cancer.

[56]  Jennifer G. Robinson,et al.  2013 ACC/AHA Guideline on the Treatment of Blood Cholesterol to Reduce Atherosclerotic Cardiovascular Risk in Adults: A Report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines , 2014, Journal of the American College of Cardiology.

[57]  F. Kamangar.  Socio-Economic Health Inequalities: Ever-Lasting Facts or Amenable to Change? , 2013, International journal of preventive medicine.

[58]  O. Uthman,et al.  Socioeconomic position and incidence of gastric cancer: a systematic review and meta-analysis , 2013, Journal of Epidemiology & Community Health.

[59]  S. McGuire.  Shields M., Carroll M.D., Ogden C.L. adult obesity prevalence in Canada and the United States. NCHS data brief no. 56, Hyattsville, MD: National Center for Health Statistics, 2011. , 2011, Advances in nutrition.

[60]  P. Bejarano.  Differential Trends in the Intestinal and Diffuse Types of Gastric Carcinoma in the United States, 1973-2000: Increase in the Signet Ring Cell Type , 2006 .

[61]  M. Blaser,et al.  Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. , 2009, The Journal of clinical investigation.

[62]  James G. Hanley.  Edwin Chadwick and the poverty of statistics. , 2002, Medical History.

[63]  H. El‐Serag,et al.  Epidemiological differences between adenocarcinoma of the oesophagus and adenocarcinoma of the gastric cardia in the USA , 2002, Gut.

[64]  Jennifer G. Robinson,et al.  2013 ACC/AHA guideline on the treatment of blood cholesterol to reduce atherosclerotic cardiovascular risk in adults: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. , 2014, Circulation.

[65]  N. Dubrawsky.  Cancer statistics , 1989, CA: a cancer journal for clinicians.

[66]  Farin Kamangar,et al.  Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. , 2006, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[67]  D. Corley,et al.  Abdominal Obesity and the Risk of Esophageal and Gastric Cardia Carcinomas , 2008, Cancer Epidemiology Biomarkers & Prevention.

[68]  A. Valleron,et al.  Louis-René Villermé (1782–1863), a pioneer in social epidemiology: re-analysis of his data on comparative mortality in Paris in the early 19th century , 2009, Journal of Epidemiology & Community Health.

[69]  Ji-hoon Jung,et al.  Effect of Helicobacter pylori Eradication on Metachronous Recurrence After Endoscopic Resection of Gastric Neoplasm , 2014, The American Journal of Gastroenterology.

[70]  A. Helicobacter,et al.  Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts , 2001, Gut.

[71]  J. Cuzick,et al.  Aspirin and cancer risk: a quantitative review to 2011. , 2012, Annals of oncology : official journal of the European Society for Medical Oncology.

[72]  A. Zuckerman,et al.  IARC Monographs on the Evaluation of Carcinogenic Risks to Humans , 1995, IARC monographs on the evaluation of carcinogenic risks to humans.

[73]  D. Graham,et al.  Age at acquisition of Helicobacter pylori infection: a follow-up study from infancy to adulthood , 2002, The Lancet.

[74]  N. Wong.  Faculty Opinions recommendation of 2013 ACC/AHA guideline on the treatment of blood cholesterol to reduce atherosclerotic cardiovascular risk in adults: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. , 2014 .

[75]  W. Chow,et al.  Risk of adenocarcinomas of the esophagus and gastric cardia in patients with gastroesophageal reflux diseases and after antireflux surgery. , 2001, Gastroenterology.

[76]  M. Stephens,et al.  Traces of Human Migrations in Helicobacter pylori Populations , 2003, Science.

[77]  D. Barker,et al.  Stomach cancer and migration within England and Wales. , 1990, British Journal of Cancer.

[78]  T. Shimosegawa,et al.  Two distinct types of cancer of different origin may be mixed in gastroesophageal junction adenocarcinomas in Japan: Evidence from direct evaluation of gastric acid secretion , 2011, Scandinavian journal of gastroenterology.

[79]  Kirsten Bibbins-Domingo,et al.  Projected effect of dietary salt reductions on future cardiovascular disease. , 2010, The New England journal of medicine.

[80]  R. Malekzadeh,et al.  Serum Ghrelin; A New Surrogate Marker of Gastric Mucosal Alterations in Upper Gastrointestinal Carcinogenesis , 2013, PloS one.

[81]  G. Maskarinec,et al.  The effect of migration on cancer incidence among Japanese in Hawaii. , 2004, Ethnicity & disease.

[82]  M. Gerretsen,et al.  A phase III randomised trial of cisplatinum, methotrextate, cisplatinum + methotrexate and cisplatinum + 5-FU in end stage squamous carcinoma of the head and neck. Liverpool Head and Neck Oncology Group. , 1990, British Journal of Cancer.

[83]  Jun Yu,et al.  Improved survival of gastric cancer with tumour Epstein–Barr virus positivity: an international pooled analysis , 2013, Gut.

[84]  B. Peleteiro,et al.  Helicobacter pylori infection and gastric cardia cancer: systematic review and meta-analysis , 2011, Cancer Causes & Control.

[85]  Yu Chen,et al.  Helicobacter pylori colonization is inversely associated with childhood asthma. , 2008, The Journal of infectious diseases.

[86]  C. la Vecchia,et al.  Cancer mortality in Europe, 2005-2009, and an overview of trends since 1980. , 2013, Annals of oncology : official journal of the European Society for Medical Oncology.

[87]  F. Kamangar,et al.  Vitamin and Mineral Supplements: Do We Really Need Them? , 2012, International Journal of Preventive Medicine.

[88]  M. Gnant,et al.  Efficacy and safety of more intensive lowering of LDL cholesterol: a meta-analysis of data from 170 000 participants in 26 randomised trials , 2010 .

[89]  A. Jemal,et al.  Cancer statistics, 2014 , 2014, CA: a cancer journal for clinicians.

[90]  M. Weiss.  Gastric cancer and Diet. , 1947 .

[91]  F. Mégraud,et al.  Helicobacter pylori infection assessed by ELISA and by immunoblot and noncardia gastric cancer risk in a prospective study: the Eurgast-EPIC project. , 2012, Annals of oncology : official journal of the European Society for Medical Oncology.

[92]  J. Rubenstein,et al.  Meta‐analysis: the association of oesophageal adenocarcinoma with symptoms of gastro‐oesophageal reflux , 2010, Alimentary pharmacology & therapeutics.

[93]  Robert A Smith,et al.  American Cancer Society Guidelines for the Early Detection of Cancer, 2006 , 2006, CA: a cancer journal for clinicians.

[94]  L. Bernstein,et al.  Hiatal hernia, reflux symptoms, body size, and risk of esophageal and gastric adenocarcinoma , 2003, Cancer.

[95]  S. Nagini,et al.  Carcinoma of the stomach: A review of epidemiology, pathogenesis, molecular genetics and chemoprevention. , 2012, World journal of gastrointestinal oncology.

[96]  D. Albanes,et al.  The relationship between serum ghrelin and the risk of gastric and esophagogastric junctional adenocarcinomas. , 2011, Journal of the National Cancer Institute.

[97]  Jennifer G. Robinson,et al.  2013 ACC/AHA Guideline on the Assessment of Cardiovascular Risk: A Report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines , 2014, Circulation.

[98]  S. Vollset,et al.  Two distinct aetiologies of cardia cancer; evidence from premorbid serological markers of gastric atrophy and Helicobacter pylori status , 2007, Gut.

[99]  D. Park,et al.  Acetic acid-indigo carmine chromoendoscopy for delineating early gastric cancers: its usefulness according to histological type , 2010, BMC gastroenterology.

[100]  L. Eusebi,et al.  Mechanisms of obesity-induced gastrointestinal neoplasia. , 2014, Gastroenterology.

[101]  Y. Yamaji,et al.  Predicting the development of gastric cancer from combining Helicobacter pylori antibodies and serum pepsinogen status: a prospective endoscopic cohort study , 2005, Gut.

[102]  R. Malekzadeh,et al.  Association of Tooth Loss and Oral Hygiene with Risk of Gastric Adenocarcinoma , 2013, Cancer Prevention Research.

[103]  M. Choti,et al.  Survival after gastric adenocarcinoma resection: Eighteen-year experience at a single institution , 2005, Journal of Gastrointestinal Surgery.

[104]  Hideo Tanaka,et al.  A functional single nucleotide polymorphism in mucin 1, at chromosome 1q22, determines susceptibility to diffuse-type gastric cancer. , 2011, Gastroenterology.

[105]  Hong Nguyen,et al.  Differential trends in the intestinal and diffuse types of gastric carcinoma in the United States, 1973-2000: increase in the signet ring cell type. , 2004, Archives of pathology & laboratory medicine.

[106]  H. Seno,et al.  Mechanism for gastric cancer development by Helicobacter pylori infection , 2008, Journal of gastroenterology and hepatology.

[107]  N. Adler,et al.  Socioeconomic Status and Health: What We Know and What We Don't , 1999, Annals of the New York Academy of Sciences.

[108]  C. McConkey,et al.  Increasing incidence of adenocarcinoma of the gastric cardia and adjacent sites. , 1990, British Journal of Cancer.

[109]  K. McPherson,et al.  Policy options to reduce population salt intake , 2011, BMJ : British Medical Journal.

[110]  D. Forman,et al.  The burden of stomach cancer in indigenous populations: a systematic review and global assessment , 2013, Gut.

[111]  C. Mathers,et al.  Global burden of cancer in 2008: a systematic analysis of disability-adjusted life-years in 12 world regions , 2012, The Lancet.

[112]  Y. Yamaoka,et al.  The significance of virulence factors in Helicobacter pylori , 2013, Journal of digestive diseases.

[113]  M. Gail,et al.  Fifteen-year effects of Helicobacter pylori, garlic, and vitamin treatments on gastric cancer incidence and mortality. , 2012, Journal of the National Cancer Institute.

[114]  C. Abnet,et al.  Fruit and vegetable intake and gastric cancer risk in a large United States prospective cohort study , 2007, Cancer Causes & Control.

[115]  J. R. Kelley,et al.  Gastric cancer epidemiology and risk factors. , 2003, Journal of clinical epidemiology.

[116]  T. Azuma,et al.  Meta-analysis of the relationship between CagA seropositivity and gastric cancer. , 2004, Gastroenterology.

[117]  Y. Kodera,et al.  Gastric cancer treatment in Japan: 2008 annual report of the JGCA nationwide registry , 2011, Gastric Cancer.

[118]  P. Rothwell,et al.  Effect of daily aspirin on long-term risk of death due to cancer: analysis of individual patient data from randomised trials , 2011, The Lancet.

[119]  A. Ochiai.  Gastric Cancer Treatment in Japan , 2010 .

[120]  A. McMichael,et al.  Patterns of gastro‐intestinal cancer in european migrants to Australia: The role of dietary change , 1980, International journal of cancer.

[121]  P. Malfertheiner,et al.  Management of precancerous conditions and lesions in the stomach (MAPS): guideline from the European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter Study Group (EHSG), European Society of Pathology (ESP), and the Sociedade Portuguesa de Endoscopia Digestiva (SPED) , 2012, Endoscopy.

[122]  Bin Liu,et al.  Genome-wide association study of esophageal squamous cell carcinoma in Chinese subjects identifies a susceptibility locus at PLCE1 , 2010, Nature Genetics.

[123]  D. Forman,et al.  Pickled Food and Risk of Gastric Cancer—a Systematic Review and Meta-analysis of English and Chinese Literature , 2012, Cancer Epidemiology, Biomarkers & Prevention.

[124]  K. Block,et al.  Nutritional Interventions in Cancer , 2014 .

[125]  P. Rosenberg,et al.  Age-specific trends in incidence of noncardia gastric cancer in US adults. , 2010, JAMA.

[126]  T. Key.  Fruit and vegetables and cancer risk , 2010, British Journal of Cancer.

[127]  Sheng Ge,et al.  Association between Habitual Dietary Salt Intake and Risk of Gastric Cancer: A Systematic Review of Observational Studies , 2012, Gastroenterology research and practice.

[128]  A. El-Sohemy,et al.  Statins and cancer. , 2007, Epidemiology.

[129]  F. Clavel-Chapelon,et al.  Dietary total antioxidant capacity and gastric cancer risk in the European prospective investigation into cancer and nutrition study , 2012, International journal of cancer.

[130]  N. Yoshimura,et al.  Gastric cancer screening of a high‐risk population in Japan using serum pepsinogen and barium digital radiography , 2005, Cancer science.

[131]  J. Stanford,et al.  Gastroesophageal reflux disease, use of H2 receptor antagonists, and risk of esophageal and gastric cancer , 2000, Cancer Causes & Control.

[132]  C. la Vecchia,et al.  Dietary patterns and gastric cancer risk: a systematic review and meta-analysis. , 2013, Annals of oncology : official journal of the European Society for Medical Oncology.

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

[134]  Gelin Xu,et al.  Dietary fiber intake reduces risk for gastric cancer: a meta-analysis. , 2013, Gastroenterology.

[135]  C. Abnet,et al.  A prospective study of tobacco, alcohol, and the risk of esophageal and gastric cancer subtypes. , 2007, American journal of epidemiology.

[136]  P. Brubaker,et al.  Ghrelin, the proglucagon-derived peptides and peptide YY in nutrient homeostasis , 2012, Nature Reviews Gastroenterology &Hepatology.

[137]  M. Solaymani-Dodaran,et al.  Risk of oesophageal cancer in Barrett’s oesophagus and gastro-oesophageal reflux , 2004, Gut.

[138]  Ping Yang,et al.  Aspirin Use and the Risk of Gastric Cancer: A Meta-Analysis , 2010, Digestive Diseases and Sciences.

[139]  M. Murad,et al.  Physical Activity Is Associated with Reduced Risk of Gastric Cancer: A Systematic Review and Meta-analysis , 2013, Cancer Prevention Research.

[140]  M. Blaser,et al.  What are the consequences of the disappearing human microbiota? , 2009, Nature Reviews Microbiology.

[141]  H. Tsukuma,et al.  Tobacco smoking and the risk of subsequent primary cancer among cancer survivors: a retrospective cohort study. , 2013, Annals of oncology : official journal of the European Society for Medical Oncology.

[142]  Khean Lee Goh,et al.  Screening for gastric cancer in Asia: current evidence and practice. , 2008, The Lancet. Oncology.

[143]  Jian-Min Yuan,et al.  Impact of Postdiagnosis Smoking on Long-term Survival of Cancer Patients: The Shanghai Cohort Study , 2013, Cancer Epidemiology, Biomarkers & Prevention.

[144]  A. Lindgren,et al.  Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. , 1999, The New England journal of medicine.

[145]  C. Abnet,et al.  Non-steroidal anti-inflammatory drugs and risk of gastric and oesophageal adenocarcinomas: results from a cohort study and a meta-analysis , 2009, British Journal of Cancer.

[146]  S. Narod,et al.  Family history and the risk of gastric cancer , 2009, British Journal of Cancer.

[147]  D. L. Preston,et al.  Solid Cancer Incidence in Atomic Bomb Survivors: 1958–1998 , 2007, Radiation research.

[148]  N. Freedman,et al.  Body mass index in relation to oesophageal and oesophagogastric junction adenocarcinomas: a pooled analysis from the International BEACON Consortium , 2012, International journal of epidemiology.

[149]  L. Brown,et al.  Epidemiologic trends in esophageal and gastric cancer in the United States. , 2002, Surgical oncology clinics of North America.

[150]  C. Mathers,et al.  Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008 , 2010, International journal of cancer.

[151]  N. Dungal,et al.  Gastric cancer and diet. A pilot study on dietary habits in two districts differing markedly in respect of mortality from gastric cancer. , 1967, British Journal of Cancer.

[152]  Wen Tan,et al.  A genome-wide association study identifies new susceptibility loci for non-cardia gastric cancer at 3q13.31 and 5p13.1 , 2011, Nature Genetics.

[153]  J. Hankin,et al.  Multiethnic studies of diet, nutrition, and cancer in Hawaii. , 1985, Princess Takamatsu symposia.

[154]  R. Malekzadeh,et al.  Combination of gastric atrophy, reflux symptoms and histological subtype indicates two distinct aetiologies of gastric cardia cancer , 2007, Gut.

[155]  I. Blanco,et al.  [Familial adenomatous polyposis]. , 2006, Gastroenterologia y hepatologia.

[156]  R. Collins,et al.  Efficacy and safety of more intensive lowering of LDL cholesterol: a meta-analysis of data from 170 000 participants in 26 randomised trials , 2010, The Lancet.

[157]  Tomotaka Sobue,et al.  The Japanese guidelines for gastric cancer screening. , 2008, Japanese journal of clinical oncology.

[158]  E. Lesaffre,et al.  Dietary salt, nitrate and stomach cancer mortality in 24 countries. European Cancer Prevention (ECP) and the INTERSALT Cooperative Research Group. , 1996, International journal of epidemiology.

[159]  N. Hu,et al.  A shared susceptibility locus in PLCE1 at 10q23 for gastric adenocarcinoma and esophageal squamous cell carcinoma , 2010, Nature Genetics.

[160]  K. Zeng,et al.  Statins are associated with reduced risk of gastric cancer: A meta-analysis , 2013, European Journal of Clinical Pharmacology.

[161]  Chiara Ricci,et al.  Diagnosis of Helicobacter pylori: invasive and non-invasive tests. , 2007, Best practice & research. Clinical gastroenterology.

[162]  B. Fernandez,et al.  Founder and recurrent CDH1 mutations in families with hereditary diffuse gastric cancer. , 2007, JAMA.

[163]  M. Drazner,et al.  2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. , 2013, Journal of the American College of Cardiology.

[164]  Hiroyuki Yoshikawa,et al.  Clinicopathological features of gastric cancer detected by endoscopy as part of annual health checkup , 2008, Journal of gastroenterology and hepatology.

[165]  Wenjing Tian,et al.  Meta-analysis on the relationship between nonsteroidal anti-inflammatory drug use and gastric cancer , 2010, European journal of cancer prevention : the official journal of the European Cancer Prevention Organisation.

[166]  J. Ferlay,et al.  Global estimates of cancer prevalence for 27 sites in the adult population in 2008 , 2013, International journal of cancer.

[167]  E. Bollschweiler,et al.  Is the prognosis for Japanese and German patients with gastric cancer really different? , 1993, Cancer.

[168]  M. Asaka.  A new approach for elimination of gastric cancer deaths in Japan , 2013, International journal of cancer.

[169]  F. Clavel-Chapelon,et al.  Fruit and vegetable intake and the risk of gastric adenocarcinoma: A reanalysis of the european prospective investigation into cancer and nutrition (EPIC‐EURGAST) study after a longer follow‐up , 2012, International journal of cancer.

[170]  P. Sipponen,et al.  Delayed rise in incidence of gastric cancer in females results in unique sex ratio (M/F) pattern: etiologic hypothesis , 2002, Gastric Cancer.

[171]  N. Dungal.  The special problem of stomach cancer in Iceland, with particular reference to dietary factors. , 1961, JAMA.

[172]  C. Abnet,et al.  Male predominance of upper gastrointestinal adenocarcinoma cannot be explained by differences in tobacco smoking in men versus women. , 2010, European journal of cancer.

[173]  S. Beghelli,et al.  Family history of gastric cancer: a correlation between epidemiologic findings and clinical data , 2005, Gastric Cancer.

[174]  R. Gilman,et al.  Variation in the prevalence of gastric cancer in Perú , 2008, International journal of cancer.

[175]  M. Gail,et al.  Total and cancer mortality after supplementation with vitamins and minerals: follow-up of the Linxian General Population Nutrition Intervention Trial. , 2009, Journal of the National Cancer Institute.

[176]  E. Riboli,et al.  The second expert report, Food, Nutrition, Physical Activity and the Prevention of Cancer: A Global Perspective , 2007 .

[177]  L. Loeb,et al.  Environmental and chemical carcinogenesis. , 2004, Seminars in cancer biology.

[178]  N. Lunet,et al.  Smoking and gastric cancer: systematic review and meta-analysis of cohort studies , 2008, Cancer Causes & Control.

[179]  J. Fraumeni,et al.  Cigarette smoking, body mass index, gastro-esophageal reflux disease, and non-steroidal anti-inflammatory drug use and risk of subtypes of esophageal and gastric cancers by P53 overexpression , 2009, Cancer Causes & Control.

[180]  P. Rothwell,et al.  Effects of regular aspirin on long-term cancer incidence and metastasis: a systematic comparison of evidence from observational studies versus randomised trials. , 2012, The Lancet. Oncology.

[181]  C. Abnet,et al.  Epstein–Barr virus serology and gastric cancer incidence and survival , 2007, British Journal of Cancer.

[182]  F. Kamangar,et al.  Helicobacter pylori and its effects on human health and disease. , 2011, Archives of Iranian medicine.

[183]  R. Taggart,et al.  Pepsinogens, pepsins, and peptic ulcer. , 1987, Clinical and investigative medicine. Medecine clinique et experimentale.

[184]  C. Bosetti,et al.  Adherence to the Mediterranean diet and gastric cancer risk in Italy , 2014, International journal of cancer.

[185]  C. Ogden,et al.  Adult obesity prevalence in Canada and the United States. , 2011, NCHS data brief.

[186]  N. Yamamichi,et al.  Cancer development based on chronic active gastritis and resulting gastric atrophy as assessed by serum levels of pepsinogen and Helicobacter pylori antibody titer , 2014, International journal of cancer.

[187]  M. Plummer,et al.  Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. , 2012, The Lancet. Oncology.

[188]  R. Malekzadeh,et al.  Opium use: an emerging risk factor for cancer? , 2014, The Lancet. Oncology.

[189]  Hongbing Shen,et al.  A genome-wide association study identifies new susceptibility loci for non-cardia gastric cancer at 3 q 13 . 31 and 5 p 13 . 1 , 2011 .

[190]  R. Fry,et al.  17β-Estradiol and Tamoxifen Prevent Gastric Cancer by Modulating Leukocyte Recruitment and Oncogenic Pathways in Helicobacter Pylori–Infected INS-GAS Male Mice , 2011, Cancer Prevention Research.

[191]  S. Nakaji,et al.  Confounding by dietary factors in case–control studies on the efficacy of cancer screening in Japan , 2004, European Journal of Epidemiology.

[192]  B. Levin,et al.  American Cancer Society Guidelines for the Early Detection of Cancer , 2002, CA: a cancer journal for clinicians.

[193]  A. Jemal,et al.  Global Patterns of Cancer Incidence and Mortality Rates and Trends , 2010, Cancer Epidemiology, Biomarkers & Prevention.

[194]  D. Albanes,et al.  Tooth loss is associated with increased risk of gastric non-cardia adenocarcinoma in a cohort of Finnish smokers , 2005, Scandinavian journal of gastroenterology.