Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019

Main Recommendations

Patients with chronic atrophic gastritis or intestinal metaplasia (IM) are at risk for gastric adenocarcinoma. This underscores the importance of diagnosis and risk stratification for these patients. High definition endoscopy with chromoendoscopy (CE) is better than high definition white-light endoscopy alone for this purpose. Virtual CE can guide biopsies for staging atrophic and metaplastic changes and can target neoplastic lesions. Biopsies should be taken from at least two topographic sites (antrum and corpus) and labelled in two separate vials. For patients with mild to moderate atrophy restricted to the antrum there is no evidence to recommend surveillance. In patients with IM at a single location but with a family history of gastric cancer, incomplete IM, or persistent Helicobacter pylori gastritis, endoscopic surveillance with CE and guided biopsies may be considered in 3 years. Patients with advanced stages of atrophic gastritis should be followed up with a high quality endoscopy every 3 years. In patients with dysplasia, in the absence of an endoscopically defined lesion, immediate high quality endoscopic reassessment with CE is recommended. Patients with an endoscopically visible lesion harboring low or high grade dysplasia or carcinoma should undergo staging and treatment. H. pylori eradication heals nonatrophic chronic gastritis, may lead to regression of atrophic gastritis, and reduces the risk of gastric cancer in patients with these conditions, and it is recommended. H. pylori eradication is also recommended for patients with neoplasia after endoscopic therapy. In intermediate to high risk regions, identification and surveillance of patients with precancerous gastric conditions is cost-effective.

• References

• 1 Bray F, Ferlay J, Soerjomataram I. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68: 393-424
• 2 Pimentel-Nunes P, Dinis-Ribeiro M. Endoscopic submucosal dissection in the treatment of gastrointestinal superficial lesions: Follow the guidelines!. GE Port J Gastroenterol 2015; 22: 184-186
• 3 Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T. et al. Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2015; 47: 829-854
• 4 Dinis-Ribeiro M, Areia M, de Vries AC. 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). Endoscopy 2012; 44: 74-94
• 5 Dinis-Ribeiro M, Areia M, de Vries AC. 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). Virchows Arch 2012; 460: 19-46
• 6 Bisschops R, Areia M, Coron E. et al. Performance measures for upper gastrointestinal endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative. Endoscopy 2016; 48: 843-864
• 7 AGREE Collaboration. Development and validation of an international appraisal instrument for assessing the quality of clinical practice guidelines: the AGREE project. Qual Saf Health Care 2003; 12: 18-23
• 8 Atkins D, Eccles M, Flottorp S. et al. Systems for grading the quality of evidence and the strength of recommendations I: critical appraisal of existing approaches The GRADE Working Group. BMC Health Serv Res 2004; 4: 38
• 9 Guyatt GH, Oxman AD, Vist GE. et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008; 336: 924-926
• 10 Correa P. Human gastric carcinogenesis: a multistep and multifactorial process – First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992; 52: 6735-6740
• 11 Kapadia CR. Gastric atrophy, metaplasia and dysplasia: a clinical perspective. J Clin Gastroenterol 2003; 36 : S29-36
• 12 Carneiro F, Machado JC, David L. et al. Current thoughts on the histopathogenesis of gastric cancer. Eur J Cancer Prev 2001; 10: 101-102
• 13 Ihamaki T, Sankkonen M, Siurala M. Long-term observation of subjects with normal mucosa and with superficial gastritis: results of 23 – 27 years’ follow-up examinations. Scand J Gastroenterol 1978; 13: 771-775
• 14 Ormiston MC, Gear MW, Codling BW. Five year follow-up study of gastritis. J Clin Pathol 1982; 35: 757-760
• 15 Laurèn P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. Acta Pathol Microbiol Scand 1965; 64: 31-49
• 16 Fukao A, Hisamichi S, Ohsato N. et al. Correlation between the prevalence of gastritis and gastric cancer in Japan. Cancer Causes Control 1993; 4: 17.20
• 17 Genta RM. Gastric atrophy and atrophic gastritis – nebulous concepts in search of a definition. Aliment Pharmacol Ther 1998; 12: 17-23
• 18 Yue H, Shan L, Bin L. The significance of OLGA and OLGIM staging systems in the risk assessment of gastric cancer: a systematic review and meta-analysis. Gastric Cancer 2018; 21: 579-587 , Epub 2018 Feb 19
• 19 Mera RM, Bravo LE, Camargo MC. et al. Dynamics of Helicobacter pylori infection as a determinant of progression of gastric precancerous lesions: 16-year follow-up of an eradication trial. Gut 2018; 67: 1239-1246 , Epub 2017 Jun 24
• 20 Dixon MF, Genta RM, Yardley JH. et al. Classification and grading of gastritis. The updated Sydney System. International workshop on the histopathology of gastritis, Houston 1994. Am J Surg Pathol 1996; 20: 1161-1181
• 21 Misiewicz JJ. The Sydney System: a new classification of gastritis. Introduction. J Gastroenterol Hepatol 1991; 6: 207-208
• 22 Plummer M, Buiatti E, Lopez G. et al. Histological diagnosis of precancerous lesions of the stomach: a reliability study. Int J Epidemiol 1997; 26: 716-720
• 23 Cotruta B, Gheorghe C, Iacob R. et al. The orientation of gastric biopsy samples improves the inter-observer agreement of the OLGA staging system. J Gastrointestin Liver Dis 2017; 26: 351-356
• 24 Isajevs S, Liepniece-Karele I, Janciauskas D. et al. Gastritis staging: interobserver agreement by applying OLGA and OLGIM systems. Virchows Arch 2014; 464: 403-407
• 25 Correa P. Clinical implications of recent developments in gastric cancer pathology and epidemiology. Semin Oncol 1985; 12: 2-10
• 26 Lauwers G, Carneiro F, Graham D. et al. Gastric carcinoma. In: Theise N. , ed. WHO Classification of tumours of the digestive system. Lyon: IARC Press; 2010: 48-58
• 27 Lim H, Jung HY, Park YS. et al. Discrepancy between endoscopic forceps biopsy and endoscopic resection in gastric epithelial neoplasia. Surg Endosc 2014; 28: 1256-1262
• 28 Pimentel-Nunes P, Mourao F, Veloso N. et al. Long-term follow-up after endoscopic resection of gastric superficial neoplastic lesions in Portugal. Endoscopy 2014; 46: 933-940
• 29 Zhao G, Xue M, Hu Y. et al. How commonly is the diagnosis of gastric low grade dysplasia upgraded following endoscopic resection? A meta-analysis. PLoS One 2015; 10: e0132699
• 30 Atkins L, Benedict EB. Correlation of gross gastroscopic findings with gastroscopic biopsy in gastritis. N Engl J Med 1956; 254: 641-644
• 31 Carpenter HA, Talley NJ. Gastroscopy is incomplete without biopsy: clinical relevance of distinguishing gastropathy from gastritis. Gastroenterology 1995; 108: 917-924
• 32 Eshmuratov A, Nah JC, Kim N. et al. The correlation of endoscopic and histological diagnosis of gastric atrophy. Dig Dis Sci 2010; 55: 1364-1375
• 33 Redéen S, Petersson F, Jönsson KA. et al. Relationship of gastroscopic features to histological findings in gastritis and Helicobacter pylori infection in a general population sample. Endoscopy 2003; 35: 946-950
• 34 Stathopoulos G, Goldberg RD, Blackstone MO. Endoscopic diagnosis of intestinal metaplasia. Gastrointest Endosc 1990; 36: 544-545
• 35 Panteris V, Nikolopoulou S, Lountou A. et al. Diagnostic capabilities of high-definition white light endoscopy for the diagnosis of gastric intestinal metaplasia and correlation with histologic and clinical data. Eur J Gastroenterol Hepatol 2014; 26: 594-601
• 36 Pimentel-Nunes P, Libanio D, Lage J. et al. A multicenter prospective study of the real-time use of narrow-band imaging in the diagnosis of premalignant gastric conditions and lesions. Endoscopy 2016; 48: 723-730
• 37 Ang TL, Pittayanon R, Lau JY. et al. A multicenter randomized comparison between high-definition white light endoscopy and narrow band imaging for detection of gastric lesions. Eur J Gastroenterol Hepatol 2015; 27: 1473-1478
• 38 Anagnostopoulos GK, Yao K, Kaye P. et al. High-resolution magnification endoscopy can reliably identify normal gastric mucosa, Helicobacter pylori-associated gastritis, and gastric atrophy. Endoscopy 2007; 39: 202-207
• 39 Gonen C, Simsek I, Sarioglu S. et al. Comparison of high resolution magnifying endoscopy and standard videoendoscopy for the diagnosis of Helicobacter pylori gastritis in routine clinical practice: a prospective study. Helicobacter 2009; 14: 12-21
• 40 Tahara T, Shibata T, Nakamura M. et al. Gastric mucosal pattern by using magnifying narrow-band imaging endoscopy clearly distinguishes histological and serological severity of chronic gastritis. Gastrointest Endosc 2009; 70: 246-253
• 41 Areia M, Amaro P, Dinis-Ribeiro M. et al. External validation of a classification for methylene blue magnification chromoendoscopy in premalignant gastric lesions. Gastrointest Endosc 2008; 67: 1011-1018
• 42 Dinis-Ribeiro M, da Costa-Pereira A, Lopes C. et al. Magnification chromoendoscopy for the diagnosis of gastric intestinal metaplasia and dysplasia. Gastrointest Endosc 2003; 57: 498-504
• 43 Kono Y, Takenaka R, Kawahara Y. et al. Chromoendoscopy of gastric adenoma using an acetic acid indigocarmine mixture. World J Gastroenterol 2014; 20: 5092-5097
• 44 Mouzyka S, Fedoseeva A. Chromoendoscopy with hematoxylin in the classification of gastric lesions. Gastric Cancer 2008; 11: 15-21 ; discussion 21–12
• 45 Tanaka K, Toyoda H, Kadowaki S. et al. Surface pattern classification by enhanced-magnification endoscopy for identifying early gastric cancers. Gastrointest Endosc 2008; 67: 430-437
• 46 Zhao Z, Yin Z, Wang S. et al. Meta-analysis: The diagnostic efficacy of chromoendoscopy for early gastric cancer and premalignant gastric lesions. J Gastroenterol Hepatol 2016; 31: 1539-1545
• 47 Kikuste I, Marques-Pereira R, Monteiro-Soares M. et al. Systematic review of the diagnosis of gastric premalignant conditions and neoplasia with high-resolution endoscopic technologies. Scand J Gastroenterol 2013; 48: 1108-1117
• 48 Pimentel-Nunes P, Dinis-Ribeiro M, Soares JB. et al. A multicenter validation of an endoscopic classification with narrow band imaging for gastric precancerous and cancerous lesions. Endoscopy 2012; 44: 236-246
• 49 Dias-Silva D, Pimentel-Nunes P, Magalhaes J. et al. The learning curve for narrow-band imaging in the diagnosis of precancerous gastric lesions by using web-based video. Gastrointest Endosc 2014; 79: 910-920 ; quiz 983-e911, 983 e914
• 50 East JE, Vleugels JL, Roelandt P. et al. Advanced endoscopic imaging: European Society of Gastrointestinal Endoscopy (ESGE) Technology Review. Endoscopy 2016; 48: 1029-1045
• 51 Dutta AK, Sajith KG, Pulimood AB. et al. Narrow band imaging versus white light gastroscopy in detecting potentially premalignant gastric lesions: a randomized prospective crossover study. Indian J Gastroenterol 2013; 32: 37-42
• 52 Xirouchakis E, Laoudi F, Tsartsali L. et al. Screening for gastric premalignant lesions with narrow band imaging, white light and updated Sydney protocol or both?. Dig Dis Sci 2013; 58: 1084-1090
• 53 Buxbaum JL, Hormozdi D, Dinis-Ribeiro M. et al. Narrow-band imaging versus white light versus mapping biopsy for gastric intestinal metaplasia: a prospective blinded trial. Gastrointest Endosc 2017; 86: 857-865
• 54 Lage J, Pimentel-Nunes P, Figueiredo PC. et al. Light-NBI to identify high-risk phenotypes for gastric adenocarcinoma: do we still need biopsies?. Scand J Gastroenterol 2016; 51: 501-506
• 55 Ezoe Y, Muto M, Uedo N. et al. Magnifying narrowband imaging is more accurate than conventional white-light imaging in diagnosis of gastric mucosal cancer. Gastroenterology 2011; 141: 2017-2025 e2013
• 56 Zhang Q, Wang F, Chen ZY. et al. Comparison of the diagnostic efficacy of white light endoscopy and magnifying endoscopy with narrow band imaging for early gastric cancer: a meta-analysis. Gastric Cancer 2016; 19: 543-552
• 57 Pimenta-Melo AR, Monteiro-Soares M, Libanio D. et al. Missing rate for gastric cancer during upper gastrointestinal endoscopy: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol 2016; 28: 1041-1049
• 58 Pimentel-Nunes P, Libanio D, Dinis-Ribeiro M. Evaluation and management of gastric superficial neoplastic lesions. GE Port J Gastroenterol 2017; 24: 8-21
• 59 Lee JW, Lim LG, Yeoh KG. Advanced endoscopic imaging in gastric neoplasia and preneoplasia. BMJ Open Gastroenterol 2017; 4: e000105
• 60 Dohi O, Yagi N, Majima A. et al. Diagnostic ability of magnifying endoscopy with blue laser imaging for early gastric cancer: a prospective study. Gastric Cancer 2017; 20: 297-303
• 61 Dohi O, Yagi N, Yoshida S. et al. Magnifying blue laser imaging versus magnifying narrow-band imaging for the diagnosis of early gastric cancer: a prospective, multicenter, comparative study. Digestion 2017; 96: 127-134
• 62 Kaneko K, Oono Y, Yano T. et al. Effect of novel bright image enhanced endoscopy using blue laser imaging (BLI). Endosc Int Open 2014; 2: E212-219
• 63 Mao XY, Xu SF, Liu Q. et al. Anatomical predilection of intestinal metaplasia based on 78,335 endoscopic cases. Saudi J Gastroenterol 2016; 22: 154-160
• 64 Kim YI, Kook MC, Cho SJ. et al. Effect of biopsy site on detection of gastric cancer high-risk groups by OLGA and OLGIM stages. Helicobacter 2017;
• 65 Isajevs S, Liepniece-Karele I, Janciauskas D. et al. The effect of incisura angularis biopsy sampling on the assessment of gastritis stage. Eur J Gastroenterol Hepatol 2014; 26: 510-513
• 66 Lash JG, Genta RM. Adherence to the Sydney System guidelines increases the detection of Helicobacter gastritis and intestinal metaplasia in 400738 sets of gastric biopsies. Aliment Pharmacol Ther 2013; 38: 424-431
• 67 Varbanova M, Wex T, Jechorek D. et al. Impact of the angulus biopsy for the detection of gastric preneoplastic conditions and gastric cancer risk assessment. J Clin Pathol 2016; 69: 19-25
• 68 Marcos-Pinto R, Carneiro F, Dinis-Ribeiro M. et al. First-degree relatives of patients with early-onset gastric carcinoma show even at young ages a high prevalence of advanced OLGA/OLGIM stages and dysplasia. Aliment Pharmacol Ther 2012; 35: 1451-1459
• 69 Rugge M, Meggio A, Pennelli G. et al. Gastritis staging in clinical practice: the OLGA staging system. Gut 2007; 56: 631-636
• 70 Rugge M, de Boni M, Pennelli G. et al. Gastritis OLGA-staging and gastric cancer risk: a twelve-year clinico-pathological follow-up study. Aliment Pharmacol Ther 2010; 31: 1104-1111
• 71 Capelle LG, de Vries AC, Haringsma J. et al. The staging of gastritis with the OLGA system by using intestinal metaplasia as an accurate alternative for atrophic gastritis. Gastrointest Endosc 2010; 71: 1150-1158
• 72 Dinis-Ribeiro M, Yamaki G, Miki K. et al. Meta-analysis on the validity of pepsinogen test for gastric carcinoma, dysplasia or chronic atrophic gastritis screening. J Med Screen 2004; 11: 141-147
• 73 Cho JH, Jeon SR, Kim HG. et al. The serum pepsinogen levels for risk assessment of gastric neoplasms: New proposal from a case-control study in Korea. Medicine (Baltimore) 2017; 96: e7603
• 74 Tong Y, Wu Y, Song Z. et al. The potential value of serum pepsinogen for the diagnosis of atrophic gastritis among the health check-up populations in China: a diagnostic clinical research. BMC Gastroenterol 2017; 17: 88
• 75 Huang YK, Yu JC, Kang WM. et al. Significance of serum pepsinogens as a biomarker for gastric cancer and atrophic gastritis screening: a systematic review and meta-analysis. PLoS One 2015; 10: e0142080
• 76 Kitahara F, Kobayashi K, Sato T. et al. Accuracy of screening for gastric cancer using serum pepsinogen concentrations. Gut 1999; 44: 693-697
• 77 Leja M, Camargo MC, Polaka I. et al. Detection of gastric atrophy by circulating pepsinogens: A comparison of three assays. Helicobacter 2017;
• 78 Zagari RM, Rabitti S, Greenwood DC. et al. Systematic review with meta-analysis: diagnostic performance of the combination of pepsinogen, gastrin-17 and anti-Helicobacter pylori antibodies serum assays for the diagnosis of atrophic gastritis. Aliment Pharmacol Ther 2017; 46: 657-667
• 79 Leja M, Kupcinskas L, Funka K. et al. Value of gastrin-17 in detecting antral atrophy. Adv Med Sci 2011; 56: 145-150
• 80 Watabe H, Mitsushima T, Yamaji Y. et al. Predicting the development of gastric cancer from combining Helicobacter pylori antibodies and serum pepsinogen status: a prospective endoscopic cohort study. Gut 2005; 54: 764-768
• 81 Yoshida T, Kato J, Inoue I. 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. Int J Cancer 2014; 134: 1445-1457
• 82 Kawashima J, Ohno S, Sakurada T. et al. Circulating acylated ghrelin level decreases in accordance with the extent of atrophic gastritis. J Gastroenterol 2009; 44: 1046-1054
• 83 Eun Bae S, Hoon Lee J, Soo Park Y. et al. Decrease of serum total ghrelin in extensive atrophic gastritis: comparison with pepsinogens in histological reference. Scand J Gastroenterol 2016; 51: 137-144
• 84 Kasai C, Sugimoto K, Moritani I. et al. Changes in plasma ghrelin and leptin levels in patients with peptic ulcer and gastritis following eradication of Helicobacter pylori infection. BMC Gastroenterol 2016; 16: 119
• 85 Shi SQ, Cai JT, Yang JM. Expression of trefoil factors 1 and 2 in precancerous condition and gastric cancer. World J Gastroenterol 2006; 12: 3119-3122
• 86 Link A, Schirrmeister W, Langner C. et al. Differential expression of microRNAs in preneoplastic gastric mucosa. Scientific reports 2015; 5: 8270
• 87 Amal H, Leja M, Funka K. et al. Detection of precancerous gastric lesions and gastric cancer through exhaled breath. Gut 2016; 65: 400-407
• 88 [Anonymous] Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the evaluation of carcinogenic risks to humans. Lyon, 7–14 June 1994. IARC Monogr Eval Carcinog Risks Hum 1994; 61: 1-241
• 89 Figueiredo C, Machado JC, Pharoah P. et al. Helicobacter pylori and interleukin 1 genotyping: an opportunity to identify high-risk individuals for gastric carcinoma. J Natl Cancer Inst 2002; 94: 1680-1687
• 90 Amieva MR, El-Omar EM. Host-bacterial interactions in Helicobacter pylori infection. Gastroenterology 2008; 134: 306-323
• 91 Machado JC, Figueiredo C, Canedo P. et al. A proinflammatory genetic profile increases the risk for chronic atrophic gastritis and gastric carcinoma. Gastroenterology 2003; 125: 364-371
• 92 Huang JQ, Zheng GF, Sumanac K. et al. Meta-analysis of the relationship between cagA seropositivity and gastric cancer. Gastroenterology 2003; 125: 1636-1644
• 93 Basso D, Zambon CF, Letley DP. et al. Clinical relevance of Helicobacter pylori cagA and vacA gene polymorphisms. Gastroenterology 2008; 135: 91-99
• 94 Rizzato C, Kato I, Plummer M. et al. Risk of advanced gastric precancerous lesions in Helicobacter pylori infected subjects is influenced by ABO blood group and cagA status. Int J Cancer 2013; 133: 315-322
• 95 Palli D, Masala G, Del Giudice G. et al. CagA+ Helicobacter pylori infection and gastric cancer risk in the EPIC-EURGAST study. Int J Cancer 2007; 120: 859-867
• 96 Winter JA, Letley DP, Cook KW. et al. A role for the vacuolating cytotoxin, VacA, in colonization and Helicobacter pylori-induced metaplasia in the stomach. J Infect Dis 2014; 210: 954-963
• 97 Cover TL. Helicobacter pylori diversity and gastric cancer risk. MBio 2016; 7: e01869-01815
• 98 El-Omar EM, Carrington M, Chow WH. et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 2000; 404: 398-402
• 99 Persson C, Canedo P, Machado JC. et al. Polymorphisms in inflammatory response genes and their association with gastric cancer: a huge systematic review and meta-analyses. Am J Epidemiol 2011; 173: 259-270
• 100 Wang P, Xia HH-X, Zhang J-Y. et al. Association of interleukin-1 gene polymorphisms with gastric cancer: A meta-analysis. Int J Cancer 2007; 120: 552-562
• 101 Camargo MC, Mera R, Correa P. et al. Interleukin-1beta and interleukin-1 receptor antagonist gene polymorphisms and gastric cancer: a meta-analysis. Cancer Epidemiol Biomarkers Prev 2006; 15: 1674-1687
• 102 Xue H, Lin B, Ni P. et al. Interleukin-1B and interleukin-1 RN polymorphisms and gastric carcinoma risk: a meta-analysis. J Gastroenterol Hepatol 2010; 25: 1604-1617
• 103 Loh M, Koh KX, Yeo BH. et al. Meta-analysis of genetic polymorphisms and gastric cancer risk: variability in associations according to race. Eur J Cancer 2009; 45: 2562-2568
• 104 Hnatyszyn A, Wielgus K, Kaczmarek-Rys M. et al. Interleukin-1 gene polymorphisms in chronic gastritis patients infected with Helicobacter pylori as risk factors of gastric cancer development. Arch Immunol Ther Exp (Warsz) 2013; 61: 503-512
• 105 Simone A, Casadei A, De Vergori E. et al. Rescue endoscopy to identify site of gastric dysplasia or carcinoma found at random biopsies. Dig Liver Dis 2011; 43: 721-725
• 106 Yep-Gamarra V, Diaz-Velez C, Araujo I. et al. [Usefulness of systematic chromoendoscopy with a double dye staining technique for the detection of dysplasia in patients with premalignant gastric lesions]. Gastroenterol Hepatol 2016; 39: 49-54
• 107 Gong EJ, Lee JH, Jung K. et al. Characteristics of missed simultaneous gastric lesions based on double-check analysis of the endoscopic image. Clin Endosc 2017; 50: 261-269
• 108 Teh JL, Tan JR, Lau LJ. et al. Longer examination time improves detection of gastric cancer during diagnostic upper gastrointestinal endoscopy. Clin Gastroenterol Hepatol 2015; 13: 480-487.e2
• 109 de Vries AC, van Grieken NC, Looman CW. et al. Gastric cancer risk in patients with premalignant gastric lesions: a nationwide cohort study in the Netherlands. Gastroenterology 2008; 134: 945-952
• 110 Song H, Ekheden IG, Zheng Z. et al. Incidence of gastric cancer among patients with gastric precancerous lesions: observational cohort study in a low risk Western population. BMJ 2015; 351: h3867
• 111 Goo JJ, Choi CW, Kang DH. et al. Risk factors associated with diagnostic discrepancy of gastric indefinite neoplasia: Who need en bloc resection?. Surg Endosc 2015; 29: 3761-3767
• 112 Raftopoulos SC, Kumarasinghe P, de Boer B. et al. Gastric intraepithelial neoplasia in a Western population. Eur J Gastroenterol Hepatol 2012; 24: 48-54
• 113 Fassan M, Pizzi M, Farinati F. et al. Lesions indefinite for intraepithelial neoplasia and OLGA staging for gastric atrophy. Am J Clin Pathol 2012; 137: 727-732
• 114 Lahner E, Esposito G, Pilozzi E. et al. Occurrence of gastric cancer and carcinoids in atrophic gastritis during prospective long-term follow up. Scand J Gastroenterol 2015; 50: 856-865
• 115 Shichijo S, Hirata Y, Niikura R. et al. Histologic intestinal metaplasia and endoscopic atrophy are predictors of gastric cancer development after Helicobacter pylori eradication. Gastrointest Endosc 2016; 84: 618-624
• 116 Reddy KM, Chang JI, Shi JM. et al. Risk of gastric cancer among patients with intestinal metaplasia of the stomach in a US integrated health care system. Clin Gastroenterol Hepatol 2016; 14: 1420-1425
• 117 Tsai YC, Hsiao WH, Yang HB. et al. The corpus-predominant gastritis index may serve as an early marker of Helicobacter pylori-infected patients at risk of gastric cancer. Aliment Pharmacol Ther 2013; 37: 969-978
• 118 Zhou Y, Li HY, Zhang JJ. et al. Operative link on gastritis assessment stage is an appropriate predictor of early gastric cancer. World J Gastroenterol 2016; 22: 3670-3678
• 119 Masuyama H, Yoshitake N, Sasai T. et al. Relationship between the degree of endoscopic atrophy of the gastric mucosa and carcinogenic risk. Digestion 2015; 91: 30-36
• 120 Cho SJ, Choi IJ, Kook MC. et al. Staging of intestinal- and diffuse-type gastric cancers with the OLGA and OLGIM staging systems. Aliment Pharmacol Ther 2013; 38: 1292-1302
• 121 Kodama M, Murakami K, Okimoto T. et al. Histological characteristics of gastric mucosa prior to Helicobacter pylori eradication may predict gastric cancer. Scand J Gastroenterol 2013; 48: 1249-1256
• 122 Marques-Silva L, Areia M, Elvas L. et al. Prevalence of gastric precancerous conditions: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol 2014; 26: 378-387
• 123 Gonzalez CA, Sanz-Anquela JM, Companioni O. et al. Incomplete type of intestinal metaplasia has the highest risk to progress to gastric cancer: results of the Spanish follow-up multicenter study. J Gastroenterol Hepatol 2016; 31: 953-958
• 124 Gonzalez CA, Sanz-Anquela JM, Gisbert JP. et al. Utility of subtyping intestinal metaplasia as marker of gastric cancer risk. A review of the evidence. Int J Cancer 2013; 133: 1023-1032
• 125 Conchillo JM, Houben G, de Bruine A. et al. Is type III intestinal metaplasia an obligatory precancerous lesion in intestinal-type gastric carcinoma?. Eur J Cancer Prev 2001; 10: 307-312
• 126 Matsukura N, Onda M, Tokunaga A. et al. Mucosal IgA antibody against Helicobacter pylori in chronic gastritis and intestinal metaplasia detected by the Tes-Tape method in resection specimens after gastrectomy for gastric cancer. Cancer 1995; 75: 1472-1477
• 127 Silva S, Filipe MI. Intestinal metaplasia and its variants in the gastric mucosa of Portuguese subjects: a comparative analysis of biopsy and gastrectomy material. Hum Pathol 1986; 17: 988-995
• 128 Oliveira C, Pinheiro H, Figueiredo J. et al. Familial gastric cancer: genetic susceptibility, pathology, and implications for management. Lancet Oncol 2015; 16: e60-e70
• 129 Yaghoobi M, Bijarchi R, Narod SA. Family history and the risk of gastric cancer. Br J Cancer 2010; 102: 237-242
• 130 Safaee A, Moghimi-Dehkordi B, Fatemi SR. et al. Family history of cancer and risk of gastric cancer in Iran. Asian Pac J Cancer Prev 2011; 12: 3117-3120
• 131 Rokkas T, Sechopoulos P, Pistiolas D. et al. Helicobacter pylori infection and gastric histology in first-degree relatives of gastric cancer patients: a meta-analysis. Eur J Gastroenterol Hepatol 2010; 22: 1128-1133
• 132 Marcos-Pinto R, Dinis-Ribeiro M, Carneiro F. et al. First-degree relatives of early-onset gastric cancer patients show a high risk for gastric cancer: phenotype and genotype profile. Virchows Arch 2013; 463: 391-399
• 133 Rugge M, Meggio A, Pravadelli C. et al. Gastritis staging in the endoscopic follow-up for the secondary prevention of gastric cancer: a 5-year prospective study of 1755 patients. Gut 2019; 68: 11-17
• 134 van der Post RS, Vogelaar IP, Carneiro F. et al. Hereditary diffuse gastric cancer: updated clinical guidelines with an emphasis on germline CDH1 mutation carriers. J Med Genet 2015; 52: 361-374
• 135 Murphy G, Dawsey SM, Engels EA. et al. Cancer risk after pernicious anemia in the US elderly population. Clin Gastroenterol Hepatol 2015; 13: 2282-2289 , e2281–2284
• 136 Landgren AM, Landgren O, Gridley G. et al. Autoimmune disease and subsequent risk of developing alimentary tract cancers among 4.5 million US male veterans. Cancer 2011; 117: 1163-1171
• 137 Hemminki K, Liu X, Ji J. et al. Autoimmune disease and subsequent digestive tract cancer by histology. Ann Oncol 2012; 23: 927-933
• 138 Ye W, Nyren O. Risk of cancers of the oesophagus and stomach by histology or subsite in patients hospitalised for pernicious anaemia. Gut 2003; 52: 938-941
• 139 Kokkola A, Sjoblom SM, Haapiainen R. et al. The risk of gastric carcinoma and carcinoid tumours in patients with pernicious anaemia. A prospective follow-up study. Scand J Gastroenterol 1998; 33: 88-92
• 140 Mellemkjoer L, Gridley G, Moller H. et al. [Pernicious anemia and risk of cancer in Denmark]. Ugeskr Laeger 1997; 159: 4850-4853
• 141 Hsing AW, Hansson LE, McLaughlin JK. et al. Pernicious anemia and subsequent cancer. A population-based cohort study. Cancer 1993; 71: 745-750
• 142 Armbrecht U, Stockbrugger RW, Rode J. et al. Development of gastric dysplasia in pernicious anaemia: a clinical and endoscopic follow up study of 80 patients. Gut 1990; 31: 1105-1109
• 143 Brinton LA, Gridley G, Hrubec Z. et al. Cancer risk following pernicious anaemia. Br J Cancer 1989; 59: 810-813
• 144 Svendsen JH, Dahl C, Svendsen LB. et al. Gastric cancer risk in achlorhydric patients. A long-term follow-up study. Scand J Gastroenterol 1986; 21: 16-20
• 145 Kuipers EJ. Pernicious anemia, atrophic gastritis, and the risk of cancer. Clin Gastroenterol Hepatol 2015; 13: 2290-2292
• 146 Vannella L, Lahner E, Osborn J. et al. Systematic review: gastric cancer incidence in pernicious anaemia. Aliment Pharmacol Ther 2013; 37: 375-382
• 147 Sjoblom SM, Sipponen P, Jarvinen H. Gastroscopic follow up of pernicious anaemia patients. Gut 1993; 34: 28-32
• 148 Lahner E, Caruana P, D'Ambra G. et al. First endoscopic-histologic follow-up in patients with body-predominant atrophic gastritis: when should it be done?. Gastrointest Endosc 2001; 53: 443-448
• 149 Sjoblom SM, Sipponen P, Miettinen M. et al. Gastroscopic screening for gastric carcinoids and carcinoma in pernicious anemia. Endoscopy 1988; 20: 52-56
• 150 Chen HN, Wang Z, Li X. et al. Helicobacter pylori eradication cannot reduce the risk of gastric cancer in patients with intestinal metaplasia and dysplasia: evidence from a meta-analysis. Gastric Cancer 2016; 19: 166-175
• 151 Kong YJ, Yi HG, Dai JC. et al. Histological changes of gastric mucosa after Helicobacter pylori eradication: a systematic review and meta-analysis. World J Gastroenterol 2014; 20: 5903-5911
• 152 Rokkas T, Rokka A, Portincasa P. A systematic review and meta-analysis of the role of Helicobacter pylori eradication in preventing gastric cancer. Ann Gastroenterol 2017; 30: 414-423
• 153 Hwang YJ, Kim N, Lee HS. et al. Reversibility of atrophic gastritis and intestinal metaplasia after Helicobacter pylori eradication – a prospective study for up to 10 years. Aliment Pharmacol Ther 2018; 47: 380-390
• 154 Kodama M, Murakami K, Okimoto T. et al. Helicobacter pylori eradication improves gastric atrophy and intestinal metaplasia in long-term observation. Digestion 2012; 85: 126-130
• 155 Kodama M, Murakami K, Okimoto T. et al. Ten-year prospective follow-up of histological changes at five points on the gastric mucosa as recommended by the updated Sydney system after Helicobacter pylori eradication. J Gastroenterol 2012; 47: 394-403
• 156 Malfertheiner P, Megraud F, O'Morain CA. et al. Management of Helicobacter pylori infection – the Maastricht V/Florence Consensus Report. Gut 2017; 66: 6-30
• 157 Maehata Y, Nakamura S, Fujisawa K. et al. Long-term effect of Helicobacter pylori eradication on the development of metachronous gastric cancer after endoscopic resection of early gastric cancer. Gastrointest Endosc 2012; 75: 39-46
• 158 Choi J, Kim SG, Yoon H. et al. Eradication of Helicobacter pylori after endoscopic resection of gastric tumors does not reduce incidence of metachronous gastric carcinoma. Clin Gastroenterol Hepatol 2014; 12: 793-800 e791
• 159 Fukase K, Kato M, Kikuchi S. et al. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet 2008; 372: 392-397
• 160 Bae SE, Jung HY, Kang J. et al. Effect of Helicobacter pylori eradication on metachronous recurrence after endoscopic resection of gastric neoplasm. Am J Gastroenterol 2014; 109: 60-67
• 161 Bang CS, Baik GH, Shin IS. et al. Helicobacter pylori eradication for prevention of metachronous recurrence after endoscopic resection of early gastric cancer. J Korean Med Sci 2015; 30: 749-756
• 162 Jung DH, Kim JH, Chung HS. et al. Helicobacter pylori eradication on the prevention of metachronous lesions after endoscopic resection of gastric neoplasm: a meta-analysis. PLoS One 2015; 10: e0124725
• 163 Choi IJ, Kook MC, Kim YI. et al. Helicobacter pylori therapy for the prevention of metachronous gastric cancer. N Engl J Med 2018; 378: 1085-1095
• 164 Tian W, Zhao Y, Liu S. et al. Meta-analysis on the relationship between nonsteroidal anti-inflammatory drug use and gastric cancer. Eur J Cancer Prev 2010; 19: 288-298
• 165 Wang WH, Huang JQ, Zheng GF. et al. Non-steroidal anti-inflammatory drug use and the risk of gastric cancer: a systematic review and meta-analysis. J Natl Cancer Inst 2003; 95: 1784-1791
• 166 Sheu BS, Tsai YC, Wu CT. et al. Long‐term celecoxib can prevent the progression of persistent gastric intestinal metaplasia after H. pylori eradication. Helicobacter 2013; 18: 117-123
• 167 Wong BC, Zhang L, Ma JL. et al. Effects of selective COX-2 inhibitor and Helicobacter pylori eradication on precancerous gastric lesions. Gut 2012; 61: 812-818
• 168 Huang X-Z, Chen Y, Wu J. et al. Aspirin and non-steroidal anti-inflammatory drugs use reduce gastric cancer risk: A dose-response meta-analysis. Oncotarget 2017; 8: 4781-4795
• 169 Kong P, Wu R, Liu X. et al. The effects of anti-inflammatory drug treatment in gastric cancer prevention: an update of a meta-analysis. J Cancer 2016; 7: 2247-2257
• 170 Ye X, Fu J, Yang Y. et al. Frequency-risk and duration-risk relationships between aspirin use and gastric cancer: a systematic review and meta-analysis. PLoS ONE 2013; 8: e71522
• 171 Bosetti C, Rosato V, Gallus S. et al. Aspirin and cancer risk: a quantitative review to 2011. Ann Oncol 2012; 23: 1403-1415
• 172 Tian W, Zhao Y, Liu S. et al. Meta-analysis on the relationship between nonsteroidal anti-inflammatory drug use and gastric cancer. Eur J Cancer Prev 2010; 19: 288-298
• 173 Abnet CC, Freedman ND, Kamangar F. et al. Non-steroidal anti-inflammatory drugs and risk of gastric and oesophageal adenocarcinomas: results from a cohort study and a meta-analysis. Br J Cancer 2009; 100: 551-557
• 174 Han X, Jiang K, Wang B. et al. Effect of rebamipide on the premalignant progression of chronic gastritis: a randomized controlled study. Clin Drug Investig 2015; 35: 665-673
• 175 Kamada T, Sato M, Tokutomi T. et al. Rebamipide improves chronic inflammation in the lesser curvature of the corpus after Helicobacter pylori eradication: a multicenter study. Biomed Res Int 2015; 2015: 865146-865148
• 176 Tang XD, Zhou LY, Zhang ST. et al. Randomized double-blind clinical trial of Moluodan () for the treatment of chronic atrophic gastritis with dysplasia. Chin J Integr Med 2016; 22: 9-18
• 177 Kong P, Cai Q, Geng Q. et al. Vitamin intake reduce the risk of gastric cancer: meta-analysis and systematic review of randomized and observational studies. PLoS One 2014; 9: e116060
• 178 Taylor PR. Prevention of gastric cancer: a miss. J Natl Cancer Inst 2007; 99: 101-103
• 179 Bjelakovic G, Nikolova D, Gluud C. Meta-regression analyses, meta-analyses, and trial sequential analyses of the effects of supplementation with beta-carotene, vitamin A, and vitamin E singly or in different combinations on all-cause mortality: do we have evidence for lack of harm?. PLoS One 2013; 8: e74558
• 180 Zhou Y, Zhuang W, Hu W. et al. Consumption of large amounts of allium vegetables reduces risk for gastric cancer in a meta-analysis. Gastroenterology 2011; 141: 80-89
• 181 Bertuccio P, Rosato V, Andreano A. et al. Dietary patterns and gastric cancer risk: a systematic review and meta-analysis. Ann Oncol 2013; 24: 1450-1458
• 182 Areia M, Dinis-Ribeiro M, Rocha Goncalves F. Cost-utility analysis of endoscopic surveillance of patients with gastric premalignant conditions. Helicobacter 2014; 19: 425-436
• 183 Zhou HJ, Dan YY, Naidoo N. et al. A cost-effectiveness analysis evaluating endoscopic surveillance for gastric cancer for populations with low to intermediate risk. PLoS One 2013; 8: e83959
• 184 Wu JT, Zhou J, Naidoo N. et al. Determining the cost-effectiveness of endoscopic surveillance for gastric cancer in patients with precancerous lesions. Asia Pac J Clin Oncol 2016; 12: 359-368
• 185 Areia M, Carvalho R, Cadime AT. et al. Screening for gastric cancer and surveillance of premalignant lesions: a systematic review of cost-effectiveness studies. Helicobacter 2013; 18: 325-337
• 186 Chang HS, Park EC, Chung W. et al. Comparing endoscopy and upper gastrointestinal X-ray for gastric cancer screening in South Korea: a cost-utility analysis. Asian Pac J Cancer Prev 2012; 13: 2721-2728
• 187 Cho E, Kang MH, Choi KS. et al. Cost-effectiveness outcomes of the national gastric cancer screening program in South Korea. Asian Pac J Cancer Prev 2013; 14: 2533-2540
• 188 Yeh JM, Hur C, Ward Z. et al. Gastric adenocarcinoma screening and prevention in the era of new biomarker and endoscopic technologies: a cost-effectiveness analysis. Gut 2016; 65: 563-574
• 189 Gupta N, Bansal A, Wani SB. et al. Endoscopy for upper GI cancer screening in the general population: a cost-utility analysis. Gastrointest Endosc 2011; 74: 610-624 e612
• 190 Areia M, Spaander MC, Kuipers EJ. et al. Endoscopic screening for gastric cancer: A cost-utility analysis for countries with an intermediate gastric cancer risk. United European Gastroenterol J 2018; 6: 192-202
• 191 Dumonceau JM, Hassan C, Riphaus A. et al. European Society of Gastrointestinal Endoscopy (ESGE) Guideline Development Policy. Endoscopy 2012; 44: 626-629