Russian consensus on prevention, diagnostics and treatment of gastric cancer. Issues of prevention, early diagnostics, and precancerous diseases

The Russian consensus on prevention, diagnostics and treatment of gastric cancer was prepared on the initiative of the Moscow clinical scientific center named after A. S. Loginov on the Delphi method. Its aim was to clarify and consolidate the opinions of specialists on the most relevant issues of prevention, diagnostics and treatment of gastric cancer. An interdisciplinary approach was provided by the participation of leading gastroen­terologists, oncologists and surgeons.

1. Pormohammad A., Mohtavinejad N., Gholizadeh P., et al. Global estimate of gastric cancer in Helicobacter pylori-in-fected population: A systematic review and meta-analysis. J Cell Physiol 2019;234(2):1208-1218. https://doi.org/10.1002/jcp.27114

2. Uemura N., Okamoto S., Yamamoto S., et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 2001;345(ll):784-9. https://doi.org/10.1056/NEJMoa001999

3. Hsu P.I., Lai K.H., Hsu P.N., et al. Helicobacter pylori infection and the risk of gastric malignancy. Am J Gastroenterol 2007;102(4):725-30. https://doi.Org/10.llll/j.1572-0241.2006.01109.x

4. Kamangar F., Qiao Y.L., Blaser M.J., et al. Helicobacter pylori and oesophageal and gastric cancers in a prospective study in China. BrJ Cancer 2007;96(l):172—6. https://doi.org/10.1038/sj.bjc.6603517

5. Matos J.I., de Sousa H.A., Marcos-Pinto R., Dinis-Ribeiro M. Helicobacter pylori CagA and VacA genotypes and gastric phenotype: a meta-analysis. Eur J Gastroenterol Hepatol 2013;25(12):1431—41. https://doi.org/10.1097/MEG.0b013e-328364b53e

6. Kpoghomou M.A., Wang J., Wang T., Jin G. Association of Helicobacter pylori babA2 gene and gastric cancer risk: ameta-analysis. BMC Cancer 2020;20(l):465. https://doi.org/10.1186/sl2885-020-06962-7

7. Malfertheiner P., Megraud F., O’Morain C.A., et al. Management of Helicobacter pylori infection-the Maastricht V/ Florence Consensus Report. Gut 2017;66(l):6-30. https://doi.org/10.1136/gutjnl-2016-312288

8. Sugano K., Tack J., Kuipers E.J., et al. Kyoto global consensus report on Helicobacter pylori gastritis. Gut 2015;64(9):1353— 67. https://doi.org/10.1136/gutjnl-2015-309252

9. Pimentel-Nunes Р., Libanio D., Marcos-Pinto R., et al. 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. Endoscopy 2019;51(4):365-388. https://doi.org/10.1055/a-0859-1883

10. Ivashkin V.T., Mayev I.V., Lapina T.L., et al. Diagnostics and treatment of Helicobacter pylori infection in adults: Clinical guidelines of the Russian gastroenterological association. Ross z gastroenterol gepatol koloproktol 2018;28(l):55-70 (In Russ.), https://doi.org/10.22416/1382-4376-2018-28-l-55-70

11. Ivashkin V.T., Mayev I.V., Kaprin A.D., et al. Early Detection of Oncological Diseases of the Digestive System (Guidelines of the Russian Gastroenterological Association and the Russian Association of Oncologists for Primary Care Physicians). Russian Journal of Gastroenterology, Hepatology, Coloproctology 2019;29(5):53-74 (In Russ.), https://doi.org/10.22416/1382-4376-2019-29-5-53-74

12. Chiang T.H., Chang W.J., Chen S.L., et al. Mass eradication of Helicobacter pylori to reduce gastric cancer incidence and mortality: a long-term cohort study on Matsu Islands. Gut 2021;70(2):243-250. https://doi.org/10.1136/gutjnl-2020-322200

13. Liou J.M., Malfertheiner P., Lee Y.C., et al; Asian Pacific Alliance on Helicobacter and Microbiota (АРАНАМ). Screening and eradication of Helicobacter pylori for gastric cancer prevention: the Taipei global consensus. Gut 2020;69(12):2093-2112. https://doi.org/10.1136/gutjnl-2020-322368

14. Pan K.F., Zhang L., Gerhard M., et al. A large randomised controlled intervention trial to prevent gastric cancer by eradication of Helicobacter pylori in Linqu County, China: baseline results and factors affecting the eradication. Gut 2016;65(1):9-18. https://doi.org/10.1136/gutjnl-2015-309197

15. Pimentel-Nunes P., Libanio D., Marcos-Pinto R., et al. 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. Endoscopy 2019;51(4):365-388. https://doi.org/10.1055/a-0859-1883

16. Sugano K. Effect of Helicobacter pylori eradication on the incidence of gastric cancer: a systematic review and meta-analysis. Gastric Cancer 2019;22(3):435-445. https://doi.org/10.1007/sl0120-018-0876-0

17. Bang C.S., Baik G.H., Shin I.S., et al. Helicobacter pylori Eradication for Prevention of Metachronous Recurrence after Endoscopic Resection of Early Gastric Cancer. J Korean Med Sci 2015;30(6):749-56. https://doi.org/10.3346/jkms.2015.30.6.749

18. Jung D.H., Kim J.H., Chung H.S., et al. Helicobacter pylori Eradication on the Prevention of Metachronous Lesions after Endoscopic Resection of Gastric Neoplasm: A Meta-Analysis. PLoS One 2015;10(4):e0124725. https://doi.org/10.1371/journal.pone.0124725

19. Yoon S.B., Park J.M., Lim С. H, et al. Effect of Helicobacter pylori eradication on metachronous gastric cancer after endoscopic resection of gastric tumors: a meta-analysis. Helicobacter 2014;19(4):243—8. https://doi.org/10.llll/hel.12146

20. Lee Y.C., Chiang T.H., Chou C.K., et al. Association Between Helicobacter pylori Eradication and Gastric Cancer Incidence: A Systematic Review and Meta-analysis. Gastroenterology 2016;150(5):1113-1124.e5. https://doi.org/10.1053/j.gastro.2016.01.028

21. Xiao S., Li S., Zhou L., et al. Helicobacter pylori status and risks of metachronous recurrence after endoscopic resection of early gastric cancer: a systematic review and meta-analysis. J Gastroenterol 2019;54(3):226—237. https://doi.org/10.1007/s00535-018-1513-8

22. Jung D.H., Lee Y.C., Kim J.H., et al. Postoperative Helicobacter pylori Infection as a Prognostic Factor for Gastric Cancer Patients after Curative Resection. Gut Liver 2017;ll(5):635—641. https://doi.org/10.5009/gnll6397

23. Kim Y.I., Cho S.J., Lee J.Y., et al. Effect of Helicobacter pylori Eradication on Long-Term Survival after Distal Gastrectomy for Gastric Cancer. Cancer Res Treat 2016;48(3):1020-9. https://doi.org/10.4143/crt.2015.264

24. Yoon K., Kim N., Kim J., et al. Dynamic Changes in Helicobacter pylori Status Following Gastric Cancer Surgery. Gut Liver 2017;ll(2):209-215. https://doi.org/10.5009/gnll6224

25. Miyashita T., Miwa K., Inokuchi M., et al. Spontaneous clearance of Helicobacter pylori after pylorus-preserving gastrectomy for gastric cancer. Oncol Rep 2013;30(l):299-303. https://doi.org/10.3892/or.2013.2472

26. Zullo A., Hassan C., Romiti A., et al. Follow-up of intestinal metaplasia in the stomach: When, how and why. World J Gastrointest Oncol 2012;4(3):30-6. https://doi.org/10.4251/wjgo.v4.i3.30

27. Park Y.H., Kim N. Review of atrophic gastritis and intestinal metaplasia as a premalignant lesion of gastric cancer. J Cancer Prev 2015;20(l):25-40. https://doi.Org/10.15430/JCP.2015.20.l.25

28. Gonzalez C.A., Sanz-Anquela J.M., 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(5):953-8. https://doi.org/10.llll/jgh.13249

29. Banks M., Graham D., Jansen M., et al. British Society of Gastroenterology guidelines on the diagnosis and management of patients at risk of gastric adenocarcinoma. Gut 2019;68(9):1545-1575. https://doi.org/10.1136/gutjnl-2018-318126

30. Dinis-Ribeiro M., Lopes C., da Costa-Pereira A., et al. A follow up model for patients with atrophic chronic gastritis and intestinal metaplasia. J Clin Pathol 2004;57(2):177-82. https://doi.org/10.1136/jcp.2003.11270

31. Mera R.M., Bravo L.E., Camargo M.C., 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(7):1239-1246. https://doi.org/10.1136/gutjnl-2016-311685

32. Pimentel-Nunes P., Libanio D., Marcos-Pinto R., et al. 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. Endoscopy 2019;51(4):365-388. https://doi.org/10.1055/a-0859-1883

33. 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(4):579-587. https://doi.org/10.1007/sl0120-018-0812-3

34. 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(4):618-24. https://doi.org/10.1016/j.gie.2016.03.791

35. Take S., Mizuno M., Ishiki K., et al. Risk of gastric cancer in the second decade of follow-up after Helicobacter pylori eradication. J Gastroenterol 2020;55(3):281-288. https://doi.org/10.1007/s00535-019-01639-w

36. Hamashima C. Systematic Review Group and Guideline Development Group for Gastric Cancer Screening Guidelines. Update version of the Japanese Guidelines for Gastric Cancer Screening. Jpn J Clin Oncol 2018;48(7):673-683. https://doi.org/10.1093/jjco/hyy077

37. Kim G.H., Liang P.S., Bang S.J., Hwang J.H. Screening and surveillance for gastric cancer in the United States: Is it needed? Gastrointest Endosc 2016;84(l):18-28. https://doi.Org/10.1016/j.gie.2016.02.028

38. Yao K., Uedo N., Kamada T., et al. Guidelines for endoscopic diagnosis of early gastric cancer. Dig Endosc 2020;32(5):663-698. https://doi.org/10.llll/den.13684

39. Eusebi L.H., Telese A., Marasco G., et al. Gastric cancer prevention strategies: A global perspective. J Gastroenterol Hepatol 2020;35(9):1495—1502. https://doi.org/10.llll/jgh.15037

40. Sugano K., Tack J., Kuipers E.J., et al; faculty members of Kyoto Global Consensus Conference. Kyoto global consensus report on Helicobacter pylori gastritis. Gut 2015;64(9):1353—67. https://doi.org/10.1136/gutjnl-2015-309252

41. Malfertheiner P., Megraud F., O’Morain C.A., et al; European Helicobacter and Microbiota Study Group and Consensus panel. Management of Helicobacter pylori infection-the Maastricht V/Florence Consensus Report. Gut 2017;66(l):6-30. https://doi.org/10.1136/gutjnl-2016-312288

42. Pimentel-Nunes P., Libanio D., Marcos-Pinto R., et al. 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. Endoscopy 2019;51(4):365-388. https://doi.org/10.1055/a-0859-1883

43. Yamaguchi Y., Nagata Y., Hiratsuka R., et al. Gastric Cancer Screening by Combined Assay for Serum Anti-Helicobacter pylori IgG Antibody and Serum Pepsinogen Levels—The ABC Method. Digestion 2016;93(l):13-8. https://doi.org/10.1159/000441742

44. Huang Y.K., Yu J.C., Kang W.M., 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(ll):e0142080. https://doi.org/10.1371/journal.pone.0142080

45. Sheu B.S., Wu M.S., Chiu C.T., et al. Consensus on the clinical management, screening-to-treat, and surveillance of Helicobacter pylori infection to improve gastric cancer control on a nationwide scale. Helicobacter 2017;22(3):el2368. https://doi.org/10.llll/hel.12368

46. Liou J.M., Malfertheiner P., Lee Y.C., et al; Asian Pacific Alliance on Helicobacter and Microbiota (АРАНАМ). Screening and eradication of Helicobacter pylori for gastric cancer prevention: the Taipei global consensus. Gut 2020;69(12):2093-2112. https://doi.org/10.1136/gutjnl-2020-322368

47. Zhang X., Li M., Chen S., et al. Endoscopic Screening in Asian Countries Is Associated With Reduced Gastric Cancer Mortality: A Meta-analysis and Systematic Review. Gastroenterology 2018;155(2):347-354.e9. https://doi.Org/10.1053/j.gastro.2018.04.026

48. Liu М., Не Z., Guo С., et al. Effectiveness of Intensive Endoscopic Screening for Esophageal Cancer in China: A Community-Based Study. AmJ Epidemiol 2019;188(4):776-784. https://doi.org/10.1093/aje/kwy291

49. Wei W.Q., Chen Z.F., He Y.T., et al. Long-Term Follow-Up of a Community Assignment, One-Time Endoscopic Screening Study of Esophageal Cancer in China. J Clin Oncol 2015;33(17):1951-7. https://doi.org/10.1200/JCO.2014.58.0423

50. Chen R., Liu Y., Song G., et al. Effectiveness of one-time endoscopic screening programme in prevention of upper gastrointestinal cancer in China: a multicentre population-based cohort study. Gut 2021;70(2):251-260. https://doi.org/10.1136/gutjnl-2019-320200

51. Kim H., Hwang Y., Sung H., et al. Effectiveness of Gastric Cancer Screening on Gastric Cancer Incidence and Mortality in a Community-Based Prospective Cohort. Cancer Res Treat 2018;50(2):582-589. https://doi.org/10.4143/crt.2017.048

52. Clinical Guidelines. Stomach cancer, 2020. Available at: https://oncology-association.ru/wp-content/uploads/2020/09/rak_zheludka.pdf (In Russ.)

53. Wu C., Han R., Yang S., et al. A case-control study of microRNA polymorphisms in gastric cancer screening by SNP chip combined with time of flight mass spectrometry. Biomark Med 2020;14(16):1563-1572. https://doi.org/10.2217/bmm-2020-0003

54. Huang H.L., Leung C.Y., Saito E., et al. Effect and cost-effectiveness of national gastric cancer screening in Japan: amicrosimulation modeling study. BMC Med 2020;18(1):257. https://doi.org/10.1186/sl2916-020-01729-0

55. Ge X., Zhang X., Ma Y., et al. Diagnostic value of macrophage inhibitory cytokine 1 as a novel prognostic biomarkers for early gastric cancer screening. J Clin Lab Anal 2021;35(l):e23568. https://doi.org/10.1002/jcla.23568

56. Kapoor R., So J.B.Y., Zhu F., et al. Evaluating the Use of microRNA Blood Tests for Gastric Cancer Screening in a Stratified Population-Level Screening Program: An Early Model-Based Cost-Effectiveness Analysis. Value Health 2020;23(9):1171-1179. https://doi.Org/10.1016/j.jval.2020.04.1829

57. Shah S.C., Canakis A., Peek R.M. Jr, Saumoy M. Endoscopy for Gastric Cancer Screening Is Cost Effective for Asian Americans in the United States. Clin Gastroenterol Hepatol 2020;18(13):3026-3039. https://doi.Org/10.1016/j.cgh.2020.07.031

58. Canakis A., Pani E., Saumoy M., Shah S.C. Decision model analyses of upper endoscopy for gastric cancer screening and preneoplasia surveillance: a systematic review. Therap Adv Gastroenterol 2020;13:1756284820941662. https://doi.org/10.1177/1756284820941662

59. Kim D.H., Shin N., Kim G.H., et al. Mucin expression in gastric cancer: reappraisal of its clinicopathologic and prognostic significance. Arch Pathol Lab Med 2013;137(8):1047—53. https://doi.org/10.5858/arpa.2012-0193-OA

60. Martin F.C., Chenevix-Trench G., Yeomans N.D. Systematic review with meta-analysis: fundic gland polyps and proton pump inhibitors. Aliment Pharmacol Ther 2016;44(9):915-925. https://doi.org/10.llll/apt.13800

61. Velazquez-Dohorn M., Lopez-Durand C.F., Candanedo-Gonzalez F., et al. Case-control analysis of fundic gland polyps and proton-pump inhibitors. A pathologist’s perspective. Rev Gastroenterol Mex (Engl Ed) 2020;85(l):42-47. https://doi.org/10.1016/j.rgmx.2019.02.007

62. Yao T., Kajiwara M., Kuroiwa S., et al. Malignant transformation of gastric hyperplastic polyps: alteration of phenotypes, proliferative activity, andp53 expression. Hum Pathol 2002;33(10):1016-22. https://doi.org/10.1053/hupa.2002.126874

63. Straub S.F., Drage M.G., Gonzalez R.S. Comparison of dysplastic fundic gland polyps in patients with and without familial adenomatous polyposis. Histopathology 2018;72(7):1172—1179. https://doi.org/10.llll/his.13485

64. Chen Z.M., Scudiere J.R., Abraham S.C., Montgomery E. Pyloric gland adenoma: an entity distinct from gastric foveolar type adenoma. AmJ Surg Pathol 2009;33(2):186-93. https://doi.org/10.1097/PAS.0b013e31817d7ff4

65. Park D.Y., Srivastava A., Kim G.H., et al. Adenomatous and foveolar gastric dysplasia: distinct patterns of mucin expression and background intestinal metaplasia. Am J Surg Pathol 2008;32(4):524-33. https://doi.org/10.1097/PAS.0b013e31815b890e

66. Ueyama H., Matsumoto K., Nagahara A., et al. Gastric adenocarcinoma of the fundic gland type (chief cell predominant type). Endoscopy 2014;46(2):153-7. https://doi.org/10.1055/s-0033-1359042

67. Choi W.T., Brown I., Ushiku T., et al. Gastric pyloric gland adenoma: a multicentre clinicopathological study of 67 cases. Histopathology 2018;72(6):1007—1014. https://doi.org/10.llll/his.13460

68. WHO Classification of Tumours Lyon, France: International Agency for Research on Cancer (2020) 5th. Available from: https://tumourclassification.iarc.who.int

69. Kushima R., Kim K.M. Interobserver Variation in the Diagnosis of Gastric Epithelial Dysplasia and Carcinoma between Two Pathologists in Japan and Korea. J Gastric Cancer 2011;ll(3):141-5. https://doi.Org/10.5230/jgc.2011.ll.3.141

70. Rugge M., Cassaro M., Di Mario F.,et al; Interdisciplinary Group on Gastric Epithelial Dysplasia (IGGED). The long term outcome of gastric non-invasive neoplasia. Gut 2003;52(8):llll-6. https://doi.Org/10.1136/gut.52.8.llll

71. Bray F., Laversanne M., Sung H., et al. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA CancerJ Clin 2024;74:229-263. https://doi.org/10.3322/caac.21834

72. Sung Н., Ferlay J., Siegel R.L., et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA CancerJ Clin 2021;71:209-249. https://doi.org/10.3322/caac.21660

73. Conti C.B., Agnesi S., Scaravaglio M., et al. Early Gastric Cancer: Update on Prevention, Diagnosis and Treatment. IntJ Environ Res Public Health 2023;20(3):2149. https://doi.org/10.3390/ijerph20032149.