Screening and surveillance for gastric cancer in the United States: Is it needed?

BACKGROUND AND AIMS Although the incidence of gastric cancer in the United States is relatively low, the incidence of gastric cancer is higher than for esophageal cancer, for which clear guidelines for screening and surveillance exist. With the increasing availability of endoscopic therapy, such as endoscopic submucosal dissection, for treating advanced dysplasia and early gastric cancer, establishing guidelines for screening and surveillance of patients who are at high risk of developing gastric cancer has the potential to diagnose and treat gastric cancer at an earlier stage and improve mortality from gastric cancer. The aims of this article were to review the data regarding the risk factors for developing gastric cancer, methods for gastric cancer screening, and results of national screening programs. METHODS A review of the existing literature related to the aims was performed. RESULTS Risk factors for gastric cancer that were identified include race/ethnicity (East Asian, Russian, or South American), first-degree relative diagnosed with gastric cancer, positive Helicobacter pylori status, and presence of atrophic gastritis or intestinal metaplasia. Endoscopy has the highest rate of detecting gastric cancer compared with other gastric cancer screening methods. The national screening program in Japan has demonstrated a mortality reduction from gastric cancer based on cohort data. CONCLUSIONS Gastric cancer screening with endoscopy should be considered in individuals who are immigrants from regions associated with a high risk of gastric cancer (East Asia, Russia, or South America) or who have a family history of gastric cancer. Those with findings of atrophic gastritis or intestinal metaplasia on screening endoscopy should undergo surveillance endoscopy every 1 to 2 years. Large prospective multicenter studies are needed to further identify additional risk factors for developing gastric cancer and to assess whether gastric cancer screening programs for high-risk populations in the United States would result in improved mortality.

[1]  Inaba Shizuyo,et al.  Evaluation of a screening program on reduction of gastric cancer mortality in Japan: preliminary results from a cohort study. , 1999 .

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

[3]  A. Oshima,et al.  Fundal atrophic gastritis as a risk factor for gastric cancer , 1993, International journal of cancer.

[4]  Y. Sugisaki,et al.  Helicobacter pylori infection‐negative gastric cancer in Japanese hospital patients: Incidence and pathological characteristics , 2007, Cancer science.

[5]  C. Mathers,et al.  Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012 , 2015, International journal of cancer.

[6]  J. Guarner,et al.  Diagnostic yield of gastric biopsy specimens when screening for preneoplastic lesions. , 2003, Human pathology.

[7]  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.

[8]  C. Lopes,et al.  Validity of serum pepsinogen I/II ratio for the diagnosis of gastric epithelial dysplasia and intestinal metaplasia during the follow-up of patients at risk for intestinal-type gastric adenocarcinoma. , 2004, Neoplasia.

[9]  M. Rugge,et al.  Gastric dysplasia: the Padova international classification. , 2000, The American journal of surgical pathology.

[10]  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.

[11]  Manami Inoue,et al.  Gastric cancer screening and subsequent risk of gastric cancer: A large‐scale population‐based cohort study, with a 13‐year follow‐up in Japan , 2006, International journal of cancer.

[12]  J. Gisbert,et al.  Utility of subtyping intestinal metaplasia as marker of gastric cancer risk. A review of the evidence , 2013, International journal of cancer.

[13]  S. Kudo,et al.  Acetic acid spray enhances accuracy of narrow-band imaging magnifying endoscopy for endoscopic tissue characterization of early gastric cancer. , 2014, Gastrointestinal endoscopy.

[14]  E. Kuipers,et al.  Narrow Band Imaging for the Detection of Gastric Intestinal Metaplasia and Dysplasia During Surveillance Endoscopy , 2010, Digestive Diseases and Sciences.

[15]  S. Hisamichi,et al.  Mass screening for gastric cancer by X-ray examination. , 1984, Japanese journal of clinical oncology.

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

[17]  N. Sasaki,et al.  Helicobacter pylori infection and the development of gastric cancer. , 2001, The New England journal of medicine.

[18]  K. Haruma,et al.  Reduction in gastric cancer mortality by screening based on serum pepsinogen concentration: A case-control study , 2007, Scandinavian journal of gastroenterology.

[19]  Masakazu Hattori,et al.  Decreased death from gastric cancer by endoscopic screening: Association with a population-based cancer registry , 2008, Scandinavian journal of gastroenterology.

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

[21]  A. Sigurdsson,et al.  The long term results of endoscopic surveillance of premalignant gastric lesions , 2002, Gut.

[22]  A. Yoshizawa,et al.  Conventional Narrow-Band Imaging Has Good Correlation with Histopathological Severity of Helicobacter pylori Gastritis , 2011, Digestive Diseases and Sciences.

[23]  E. Kuipers,et al.  Epidemiology of Premalignant Gastric Lesions: Implications for the Development of Screening and Surveillance Strategies , 2007, Helicobacter.

[24]  Angelo Zullo,et al.  Follow-up of intestinal metaplasia in the stomach: When, how and why. , 2012, World journal of gastrointestinal oncology.

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

[26]  F. Roviello,et al.  Familial gastric cancer and germline mutations of E-cadherin. , 2012, Annali italiani di chirurgia.

[27]  John A. Evans,et al.  The role of endoscopy in the management of premalignant and malignant conditions of the stomach. , 2015, Gastrointestinal endoscopy.

[28]  T. Rokkas,et al.  Helicobacter pylori infection and gastric histology in first-degree relatives of gastric cancer patients: a meta-analysis , 2010, European journal of gastroenterology & hepatology.

[29]  C. Mathers,et al.  GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. Lyon, France: International Agency for Research on Cancer , 2013 .

[30]  L. Aaltonen,et al.  Features of gastric cancer in hereditary non‐polyposis colorectal cancer syndrome , 1997, International journal of cancer.

[31]  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.

[32]  Bo Chen,et al.  Overweight, obesity and gastric cancer risk: results from a meta-analysis of cohort studies. , 2009, European journal of cancer.

[33]  M. Kubo,et al.  The serum pepsinogen test as a predictor of gastric cancer: the Hisayama study. , 2006, American journal of epidemiology.

[34]  M. Asaka,et al.  Relationship between Helicobacter pylori infection, atrophic gastritis and gastric carcinoma in a Japanese population. , 1995, European journal of gastroenterology & hepatology.

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

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

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

[38]  Z. Ge,et al.  Application of magnifying endoscopy with narrow-band imaging in diagnosing gastric lesions: a prospective study. , 2012, Gastrointestinal endoscopy.

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

[40]  A. Rastogi,et al.  Endoscopy for upper GI cancer screening in the general population: a cost-utility analysis. , 2011, Gastrointestinal endoscopy.

[41]  M. Gail,et al.  No impact of repeated endoscopic screens on gastric cancer mortality in a prospectively followed Chinese population at high risk. , 2002, Preventive medicine.

[42]  B. Hankey,et al.  Cancer incidence and mortality patterns among specific Asian and Pacific Islander populations in the U.S. , 2008, Cancer Causes & Control.

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

[44]  J. Ford,et al.  Genetic Testing by Cancer Site: Stomach , 2012, Cancer journal.

[45]  T. Ledin,et al.  The ratio of pepsinogen A to pepsinogen C: a sensitive test for atrophic gastritis. , 1989, Scandinavian journal of gastroenterology.

[46]  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.

[47]  N. Yoshimura,et al.  Cancer High-Risk Subjects Identified by Serum Pepsinogen Tests: Outcomes after 10-Year Follow-up in Asymptomatic Middle-Aged Males , 2008, Cancer Epidemiology Biomarkers & Prevention.

[48]  A. Jemal,et al.  Cancer statistics, 2015 , 2015, CA: a cancer journal for clinicians.

[49]  K. Sugano,et al.  Screening of gastric cancer in Asia. , 2015, Best practice & research. Clinical gastroenterology.

[50]  Nayoung Kim,et al.  Diagnosis and Management of High Risk Group for Gastric Cancer , 2015, Gut and liver.

[51]  J Pohl,et al.  Computed virtual chromoendoscopy: a new tool for enhancing tissue surface structures , 2007, Endoscopy.

[52]  J. Fraumeni,et al.  Family history and risk of stomach cancer in Italy. , 1994, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[53]  H. Gouveia,et al.  External validation of a classification for methylene blue magnification chromoendoscopy in premalignant gastric lesions. , 2008, Gastrointestinal endoscopy.

[54]  N. Samadder,et al.  Hereditary and Common Familial Colorectal Cancer: Evidence for Colorectal Screening , 2015, Digestive Diseases and Sciences.

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

[56]  Andrew Y. Wang,et al.  Gastric intestinal metaplasia and early gastric cancer in the west: a changing paradigm. , 2014, Gastroenterology & hepatology.

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

[58]  Nayoung Kim,et al.  Stomach Cancer Risk in Gastric Cancer Relatives: Interaction Between Helicobacter pylori Infection and Family History of Gastric Cancer for the Risk of Stomach Cancer , 2010, Journal of clinical gastroenterology.

[59]  X. Zuo,et al.  Magnified and enhanced computed virtual chromoendoscopy in gastric neoplasia: a feasibility study. , 2013, World journal of gastroenterology.

[60]  N. Lunet,et al.  Fruit and vegetable consumption and gastric cancer by location and histological type: case–control and meta-analysis , 2007, European journal of cancer prevention : the official journal of the European Cancer Prevention Organisation.

[61]  R. Busuttil,et al.  Intestinal metaplasia: A premalignant lesion involved in gastric carcinogenesis , 2009, Journal of gastroenterology and hepatology.

[62]  A. Tashiro,et al.  Comparing mass screening techniques for gastric cancer in Japan. , 2006, World journal of gastroenterology.

[63]  K. Sugano,et al.  Guidelines for the Management of Helicobacter pylori Infection in Japan: 2009 Revised Edition , 2010, Helicobacter.

[64]  H. Yatsuya,et al.  Prospective study of screening for stomach cancer in Japan , 2003, International journal of cancer.

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

[66]  Takanori Yoshida,et al.  Effect of periodic endoscopy for gastric cancer on early detection and improvement of survival , 2001, Gastric Cancer.

[67]  R. Wong,et al.  Ethnic Disparities in Gastric Cancer Incidence and Survival in the USA: An Updated Analysis of 1992–2009 SEER Data , 2014, Digestive Diseases and Sciences.

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

[69]  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.

[70]  I. Choi.  [Gastric cancer screening and diagnosis]. , 2009, The Korean journal of gastroenterology = Taehan Sohwagi Hakhoe chi.

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

[72]  Jaw-Town Lin.  Screening of gastric cancer: who, when, and how. , 2014, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[73]  M. Kaise.  Advanced endoscopic imaging for early gastric cancer. , 2015, Best practice & research. Clinical gastroenterology.

[74]  Samloff Im.  Cellular localization of group I pepsinogens in human gastric mucosa by immunofluorescence. , 1971 .

[75]  T. Yoshikawa,et al.  Is gastric carcinoma different between Japan and the United States? , 2000, Cancer.

[76]  W. Liebman,et al.  Cellular localization of the group II pepsinogens in human stomach and duodenum by immunofluorescence. , 1973, Gastroenterology.

[77]  Sharmila Anandasabapathy,et al.  Gastric Cancer: Descriptive Epidemiology, Risk Factors, Screening, and Prevention , 2014, Cancer Epidemiology, Biomarkers & Prevention.

[78]  J. Guarner,et al.  Screening markers for chronic atrophic gastritis in Chiapas, Mexico. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

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

[80]  M F Dixon,et al.  Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. , 1996, The American journal of surgical pathology.

[81]  C. la Vecchia,et al.  A meta-analysis on alcohol drinking and gastric cancer risk. , 2012, Annals of oncology : official journal of the European Society for Medical Oncology.

[82]  K. Choi,et al.  Cost-effectiveness outcomes of the national gastric cancer screening program in South Korea. , 2013, Asian Pacific journal of cancer prevention : APJCP.

[83]  I. Choi,et al.  Effect of repeated endoscopic screening on the incidence and treatment of gastric cancer in health screenees , 2009, European journal of gastroenterology & hepatology.

[84]  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.

[85]  Jae Seong Jang,et al.  Differences in the Survival of Gastric Cancer Patients after Gastrectomy according to the Medical Insurance Status , 2013, Journal of gastric cancer.

[86]  M. Ghigna,et al.  Type or extension of intestinal metaplasia and immature/atypical "indefinite-for-dysplasia" lesions as predictors of gastric neoplasia. , 2006, Human pathology.

[87]  M. Piazuelo,et al.  Pathology of Gastric Intestinal Metaplasia: Clinical Implications , 2010, The American Journal of Gastroenterology.

[88]  M. Asaka,et al.  Recent development of gastric cancer prevention. , 2012, Japanese journal of clinical oncology.

[89]  C. Hamashima,et al.  A Community-Based, Case-Control Study Evaluating Mortality Reduction from Gastric Cancer by Endoscopic Screening in Japan , 2013, PloS one.

[90]  E. Kuipers,et al.  Gastric cancer risk in patients with premalignant gastric lesions: a nationwide cohort study in the Netherlands. , 2008, Gastroenterology.

[91]  R. Pounder,et al.  The prevalence of Helicobacter pylori infection in different countries. , 1995, Alimentary pharmacology & therapeutics.

[92]  M. Gail,et al.  Randomized double-blind factorial trial of three treatments to reduce the prevalence of precancerous gastric lesions. , 2006, Journal of the National Cancer Institute.

[93]  I. Tsuji,et al.  The evaluation of screening for gastric cancer in miyagi prefecture, Japan: A population‐based case‐control study , 1995, International journal of cancer.

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

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