Endoscopic classification systems for risk stratification of gastric precancerous lesions in Vietnam
Main Article Content
Abstract
Gastric cancer is a major health burden in Vietnam, with over 16,000 new cases annually, most diagnosed at advanced stages. Conventional gastric cancer risk stratification based on systematic five-site biopsy remains difficult to implement widely due to limited pathology resources. This narrative review synthesized evidence and proposed a sequential strategy for applying three endoscopic classification systems in stratifying the risk of gastric precancerous lesions among Vietnamese patients. The Kimura-Takemoto classification assesses mucosal atrophy with a 98% negative predictive value for excluding high-risk precancerous lesions and is applicable at all levels of healthcare. The Kyoto classification additionally provides predictive information on active Helicobacter pylori infection status. The Endoscopic Grading of Gastric Intestinal Metaplasia (EGGIM) score quantifies the extent of gastric intestinal metaplasia in real time using image-enhanced endoscopy and may replace systematic biopsy. A sequential risk stratification strategy enables selective biopsy, optimizing resource utilization, but requires standardization of endoscopic image quality and training of endoscopists.
Article Details
Keywords
Gastric cancer, gastric precancerous lesions, Kimura-Takemoto classification, endoscopic Kyoto classification, EGGIM, risk stratification
References
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11. Kimura K, Takemoto T. An Endoscopic Recognition of the Atrophic Border and its Significance in Chronic Gastritis. Endoscopy. 2008/12/08 1969; 1(03): 87-97. doi:10.1055/s-0028-1098086.
12. Toyoshima O, Nishizawa T, Koike K. Endoscopic Kyoto classification of Helicobacter pylori infection and gastric cancer risk diagnosis. World journal of gastroenterology. Feb 7 2020; 26(5): 466-477. doi:10.3748/wjg.v26.i5.466.
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14. Haruma K, Kato M, Inoue K. Kyoto classification of gastritis. 1st ed. Nihon Medical Center; 2017.
15. Quach DT, Aoki R, Iga A, et al. Diagnostic Accuracy of H. pylori Status by Conventional Endoscopy: Time-Trend Change After Eradication and Impact of Endoscopic Image Quality. Frontiers in medicine. 2021; 8:830730. doi:10.3389/fmed.2021.830730.
16. Trinh NA, Luu MN, Nguyen DTN, et al. The Predictive Value of the EGGIM Score for Extensive and Incomplete Gastric Intestinal Metaplasia: Implications for Biopsy Reduction in Endoscopic Practice. Digestive diseases and sciences. Jan 2 2026; doi:10.1007/s10620-025-09634-3.
17. Quach DT, Hiyama T. Assessment of Endoscopic Gastric Atrophy according to the Kimura-Takemoto Classification and Its Potential Application in Daily Practice. Clinical endoscopy. Jul 2019; 52(4): 321-327. doi:10.5946/ce.2019.072.
18. Xiao S, Fan Y, Yin Z, Zhou L. Endoscopic grading of gastric atrophy on risk assessment of gastric neoplasia: A systematic review and meta-analysis. Journal of gastroenterology and hepatology. Jan 2021; 36(1): 55-63. doi:10.1111/jgh.15177.
19. Miwata T, Quach DT, Hiyama T, et al. Interobserver and intraobserver agreement for gastric mucosa atrophy. BMC gastroenterology. Aug 4 2015; 15:95. doi:10.1186/s12876-015-0327-x.
20. Quach DT, Le HM, Hiyama T, Nguyen OT, Nguyen TS, Uemura N. Relationship between endoscopic and histologic gastric atrophy and intestinal metaplasia. Helicobacter. Apr 2013; 18(2): 151-7. doi:10.1111/hel.12027.
21. Toyoshima O, Nishizawa T. Kyoto classification of gastritis: Advances and future perspectives in endoscopic diagnosis of gastritis. World journal of gastroenterology. Nov 21 2022; 28(43): 6078-6089. doi:10.3748/wjg.v28.i43.6078.
22. Zhang H, Yang X, Zhang X, Huang X. The significance of endoscopic Kyoto classification of gastritis in the gastric cancer risk assessment: A systematic review and meta‑analysis. Medicine. Jun 2 2023; 102(22): e33942. doi:10.1097/md.0000000000033942.
23. Kawamura M, Uedo N, Koike T, et al. Kyoto classification risk scoring system and endoscopic grading of gastric intestinal metaplasia for gastric cancer: Multicenter observation study in Japan. Digestive endoscopy : official journal of the Japan Gastroenterological Endoscopy Society. Mar 2022; 34(3): 508-516. doi:10.1111/den.14114.
24. Esposito G, Pimentel-Nunes P, Angeletti S, et al. Endoscopic grading of gastric intestinal metaplasia (EGGIM): a multicenter validation study. Endoscopy. Jun 2019; 51(6): 515-521. doi:10.1055/a-0808-3186.
25. Rokkas T, Ekmektzoglou K. Current role of narrow band imaging in diagnosing gastric intestinal metaplasia: a systematic review and meta-analysis of its diagnostic accuracy. Annals of gastroenterology. Mar-Apr 2023; 36(2): 149-156. doi:10.20524/aog.2023.0784.
26. Cho JH, Jin SY, Park S. Carbon footprint and cost reduction by endoscopic grading of gastric intestinal metaplasia using narrow-band imaging. Journal of gastroenterology and hepatology. May 2024; 39(5): 942-948. doi:10.1111/jgh.16493.
27. Tiankanon K, Pittayanon R, Faknak N, et al. Diagnostic validity and learning curve of non-NBI expert endoscopists in gastric intestinal metaplasia diagnosis. Surgical endoscopy. Sep 2023; 37(9): 6771-6778. doi:10.1007/s00464-023-10123-9.
28. Quach DT, Mai BH, Tran MK, et al. Vietnam Association of Gastroenterology (VNAGE) consensus on the management of Helicobacter pylori infection. Frontiers in medicine. 2022; 9:1065045. doi:10.3389/fmed.2022.1065045.
2. Ferlay J, Ervik M, Lam F, et al. Global Cancer Observatory: Cancer Today - Viet Nam fact sheet 2022. Accessed May 02, 2026. https://gco.iarc.who.int/today
3. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process--First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer research. Dec 15 1992; 52(24): 6735-40.
4. Quach DT, Hiyama T, Gotoda T. Identifying high-risk individuals for gastric cancer surveillance from western and eastern perspectives: Lessons to learn and possibility to develop an integrated approach for daily practice. World journal of gastroenterology. Jul 21 2019; 25(27): 3546-3562. doi:10.3748/wjg.v25.i27.3546.
5. Dinis-Ribeiro M, Libânio D, Uchima H, et al. Management of epithelial precancerous conditions and early neoplasia of the stomach (MAPS III): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG) and European Society of Pathology (ESP) Guideline update 2025. Endoscopy. May 2025; 57(5): 504-554. doi:10.1055/a-2529-5025.
6. Gupta S, Li D, El Serag HB, et al. AGA Clinical Practice Guidelines on Management of Gastric Intestinal Metaplasia. Gastroenterology. Feb 2020; 158(3): 693-702. doi:10.1053/j.gastro.2019.12.003.
7. Morgan DR, Corral JE, Li D, et al. ACG Clinical Guideline: Diagnosis and Management of Gastric Premalignant Conditions. The American journal of gastroenterology. Apr 1 2025; 120(4): 709-737. doi:10.14309/ajg.0000000000003350.
8. Leung WK, Ang TL, Shah S, et al. Asian Pacific Association of Gastroenterology task force recommendations on surveillance for Helicobacter pylori associated gastric premalignant conditions. Gut. Mar 6 2026; 75(4): 685-704. doi:10.1136/gutjnl-2025-335823.
9. Quach DT, Hiyama T, Le HM, Nguyen TS, Gotoda T. Use of endoscopic assessment of gastric atrophy for gastric cancer risk stratification to reduce the need for gastric mapping. Scandinavian journal of gastroenterology. Apr 2020; 55(4): 402-407. doi:10.1080/00365521.2020.1740777.
10. Nguyen DTN, Quach DT, Le QD, et al. Endoscopic Kyoto and Kimura-Takemoto Classifications Are Comparable in Predicting High-Risk Gastric Precancerous Lesions. Digestion. 2024; 105(2): 140-148. doi:10.1159/000536048.
11. Kimura K, Takemoto T. An Endoscopic Recognition of the Atrophic Border and its Significance in Chronic Gastritis. Endoscopy. 2008/12/08 1969; 1(03): 87-97. doi:10.1055/s-0028-1098086.
12. Toyoshima O, Nishizawa T, Koike K. Endoscopic Kyoto classification of Helicobacter pylori infection and gastric cancer risk diagnosis. World journal of gastroenterology. Feb 7 2020; 26(5): 466-477. doi:10.3748/wjg.v26.i5.466.
13. Pimentel-Nunes P, Libânio 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. Aug 2016; 48(8): 723-30. doi:10.1055/s-0042-108435.
14. Haruma K, Kato M, Inoue K. Kyoto classification of gastritis. 1st ed. Nihon Medical Center; 2017.
15. Quach DT, Aoki R, Iga A, et al. Diagnostic Accuracy of H. pylori Status by Conventional Endoscopy: Time-Trend Change After Eradication and Impact of Endoscopic Image Quality. Frontiers in medicine. 2021; 8:830730. doi:10.3389/fmed.2021.830730.
16. Trinh NA, Luu MN, Nguyen DTN, et al. The Predictive Value of the EGGIM Score for Extensive and Incomplete Gastric Intestinal Metaplasia: Implications for Biopsy Reduction in Endoscopic Practice. Digestive diseases and sciences. Jan 2 2026; doi:10.1007/s10620-025-09634-3.
17. Quach DT, Hiyama T. Assessment of Endoscopic Gastric Atrophy according to the Kimura-Takemoto Classification and Its Potential Application in Daily Practice. Clinical endoscopy. Jul 2019; 52(4): 321-327. doi:10.5946/ce.2019.072.
18. Xiao S, Fan Y, Yin Z, Zhou L. Endoscopic grading of gastric atrophy on risk assessment of gastric neoplasia: A systematic review and meta-analysis. Journal of gastroenterology and hepatology. Jan 2021; 36(1): 55-63. doi:10.1111/jgh.15177.
19. Miwata T, Quach DT, Hiyama T, et al. Interobserver and intraobserver agreement for gastric mucosa atrophy. BMC gastroenterology. Aug 4 2015; 15:95. doi:10.1186/s12876-015-0327-x.
20. Quach DT, Le HM, Hiyama T, Nguyen OT, Nguyen TS, Uemura N. Relationship between endoscopic and histologic gastric atrophy and intestinal metaplasia. Helicobacter. Apr 2013; 18(2): 151-7. doi:10.1111/hel.12027.
21. Toyoshima O, Nishizawa T. Kyoto classification of gastritis: Advances and future perspectives in endoscopic diagnosis of gastritis. World journal of gastroenterology. Nov 21 2022; 28(43): 6078-6089. doi:10.3748/wjg.v28.i43.6078.
22. Zhang H, Yang X, Zhang X, Huang X. The significance of endoscopic Kyoto classification of gastritis in the gastric cancer risk assessment: A systematic review and meta‑analysis. Medicine. Jun 2 2023; 102(22): e33942. doi:10.1097/md.0000000000033942.
23. Kawamura M, Uedo N, Koike T, et al. Kyoto classification risk scoring system and endoscopic grading of gastric intestinal metaplasia for gastric cancer: Multicenter observation study in Japan. Digestive endoscopy : official journal of the Japan Gastroenterological Endoscopy Society. Mar 2022; 34(3): 508-516. doi:10.1111/den.14114.
24. Esposito G, Pimentel-Nunes P, Angeletti S, et al. Endoscopic grading of gastric intestinal metaplasia (EGGIM): a multicenter validation study. Endoscopy. Jun 2019; 51(6): 515-521. doi:10.1055/a-0808-3186.
25. Rokkas T, Ekmektzoglou K. Current role of narrow band imaging in diagnosing gastric intestinal metaplasia: a systematic review and meta-analysis of its diagnostic accuracy. Annals of gastroenterology. Mar-Apr 2023; 36(2): 149-156. doi:10.20524/aog.2023.0784.
26. Cho JH, Jin SY, Park S. Carbon footprint and cost reduction by endoscopic grading of gastric intestinal metaplasia using narrow-band imaging. Journal of gastroenterology and hepatology. May 2024; 39(5): 942-948. doi:10.1111/jgh.16493.
27. Tiankanon K, Pittayanon R, Faknak N, et al. Diagnostic validity and learning curve of non-NBI expert endoscopists in gastric intestinal metaplasia diagnosis. Surgical endoscopy. Sep 2023; 37(9): 6771-6778. doi:10.1007/s00464-023-10123-9.
28. Quach DT, Mai BH, Tran MK, et al. Vietnam Association of Gastroenterology (VNAGE) consensus on the management of Helicobacter pylori infection. Frontiers in medicine. 2022; 9:1065045. doi:10.3389/fmed.2022.1065045.