The Role of Endoscopic Grading of Gastric Intestinal Metaplasia (EGGIM) in Assessing the Extent and Degree of Gastric Intestinal Metaplasia

Abstract

Objectives: We aimed to evaluate the consistency between endoscopic grading of gastric intestinal metaplasia (EGGIM) and the operative link on gastric intestinal metaplasia assessment (OLGIM) staging, as well as the value of endoscopic grading of gastric intestinal metaplasia (GIM) in early gastric cancer (EGC) risk.

Methods: The sample size was estimated to be at least 210 patients. To evaluate GIM, EGGIM staging was used during magnifying endoscopy with narrow-band imaging, while the OLGIM staging was carried out according to the updated Sydney system. The consistency between the two scoring systems and the accuracy of EGGIM in diagnosing OLGIM III/IV cases were evaluated. EGC risk was evaluated using the Kimura–Takemoto classification, the operative link on gastritis assessment (OLGA)/OLGIM, and EGGIM.

Results: Among the 210 patients, 68 (32.4%) had (previous) EGC and 142 (67.6%) had chronic atrophic gastritis (CAG). EGGIM and OLGIM staging showed good consistency (κ = 0.805, U = 12.620, p < 0.001) in diagnosing OLGIM III/IV GIM, with an area under the receiver operating characteristic curve for EGGIM of 0.95. Using a cut-off value of > 4, the sensitivity and specificity were 95.7% and 91.4%, respectively. The EGGIM score was higher in the EGC group than in the CAG group (4.93 vs. 3.92, p < 0.001).

Conclusions: EGGIM shows good diagnostic performance and consistency with OLGIM, which can simplify endoscopic surveillance by reducing the need for biopsy. The EGGIM score is associated with EGC risk, and endoscopic surveillance is recommended for patients with EGGIM score > 4.

Keywords

atrophic gastritis / early gastric cancer / endoscopic grading of gastric intestinal metaplasia / gastric intestinal metaplasia / operative link on gastric intestinal metaplasia assessment

References

[1] F. Bray, J. Ferlay, I. Soerjomataram, R. L. Siegel, L. A. Torre, and A. Jemal, “Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries,” CA: A Cancer Journal for Clinicians 68, no. 6 (2018): 394-424.

[2] H. Suzuki, I. Oda, S. Abe, et al., “High Rate of 5-Year Survival Among Patients With Early Gastric Cancer Undergoing Curative Endoscopic Submucosal Dissection,” Gastric Cancer 19, no. 1 (2016): 198-205.

[3] P. Correa, “Human Gastric Carcinogenesis: A Multistep and Multifactorial Process—First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention,” Cancer Research 52, no. 24 (1992): 6735-6740.

[4] P. Pimentel-Nunes, D. Libânio, R. Marcos-Pinto, 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 51, no. 4 (2019): 365-388.

[5] M. Rugge and R. M. Genta, “Staging Gastritis: An International Proposal,” Gastroenterology 129, no. 5 (2005): 1807-1808.

[6] L. G. Capelle, A. C. de Vries, J. Haringsma, et al., “The Staging of Gastritis With the OLGA System by Using Intestinal Metaplasia as an Accurate Alternative for Atrophic Gastritis,” Gastrointestinal Endoscopy 71, no. 7 (2010): 1150-1158.

[7] S. J. Cho, I. J. Choi, M. C. Kook, et al., “Staging of Intestinal- and Diffuse-Type Gastric Cancers With the OLGA and OLGIM Staging Systems,” Alimentary Pharmacology and Therapeutics 38, no. 10 (2013): 1292-1302.

[8] M. Rugge, A. Meggio, C. Pravadelli, 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 68, no. 1 (2019): 11-17.

[9] R. M. Mera, L. E. Bravo, M. C. Camargo, 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 67, no. 7 (2018): 1239-1246.

[10] Y. H. Song, L. D. Xu, M. X. Xing, et al., “Comparison of White-Light Endoscopy, Optical-Enhanced and Acetic-Acid Magnifying Endoscopy for Detecting Gastric Intestinal Metaplasia: A Randomized Trial,” World Journal of Clinical Cases 9, no. 16 (2021): 3895-3907.

[11] M. Dinis-Ribeiro, A. da Costa-Pereira, C. Lopes, et al., “Magnification Chromoendoscopy for the Diagnosis of Gastric Intestinal Metaplasia and Dysplasia,” Gastrointestinal Endoscopy 57, no. 4 (2003): 498-504.

[12] K. Tanaka, H. Toyoda, S. Kadowaki, et al., “Surface Pattern Classification by Enhanced-Magnification Endoscopy for Identifying Early Gastric Cancers,” Gastrointestinal Endoscopy 67, no. 3 (2008): 430-437.

[13] N. Uedo, R. Ishihara, H. Iishi, et al., “A New Method of Diagnosing Gastric Intestinal Metaplasia: Narrow-Band Imaging With Magnifying Endoscopy,” Endoscopy 38, no. 8 (2006): 819-824.

[14] P. Pimentel-Nunes, D. Libânio, J. Lage, 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 48, no. 8 (2016): 723-730.

[15] G. Esposito, P. Pimentel-Nunes, S. Angeletti, et al., “Endoscopic Grading of Gastric Intestinal Metaplasia (EGGIM): A Multicenter Validation Study,” Endoscopy 51, no. 6 (2019): 515-521.

[16] K. Kimura and T. Takemoto, “An Endoscopic Recognition of the Atrophic Border and Its Significance in Chronic Gastritis,” Endoscopy 1, no. 3 (1969): 87-97.

[17] M. F. Dixon, R. M. Genta, J. H. Yardley, and P. Correa, “Classification and Grading of Gastritis. The Updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994,” American Journal of Surgical Pathology 20, no. 10 (1996): 1161-1181.

[18] I. Tramacere, E. Negri, C. Pelucchi, et al., “A Meta-Analysis on Alcohol Drinking and Gastric Cancer Risk,” Annals of Oncology 23, no. 1 (2012): 28-36.

[19] Y. Huang, J. N. Chen, Y. X. Guo, et al., “Staging of Operative Link on Gastritis Assessment and Operative Link on Gastric Intestinal Metaplasia Systems for Risk Assessment of Early Gastric Cancer: A Case-Control Study,” Journal of Clinical Pathology 78, no. 2 (2025): 117-122.

[20] J. L. Buxbaum, D. Hormozdi, M. Dinis-Ribeiro, et al., “Narrow-Band Imaging Versus White Light Versus Mapping Biopsy for Gastric Intestinal Metaplasia: A Prospective Blinded Trial,” Gastrointestinal Endoscopy 86, no. 5 (2017): 857-865.

[21] T. Kanemitsu, K. Yao, T. Nagahama, et al., “Extending Magnifying NBI Diagnosis of Intestinal Metaplasia in the Stomach: The White Opaque Substance Marker,” Endoscopy 49, no. 6 (2017): 529-535.

[22] J. K. An, G. A. Song, G. H. Kim, et al., “Marginal Turbid Band and Light Blue Crest, Signs Observed in Magnifying Narrow-Band Imaging Endoscopy, Are Indicative of Gastric Intestinal Metaplasia,” BMC Gastroenterology 12 (2012): 169, https://doi.org/10.1186/1471-230X-12-169.

[23] T. Nakayoshi, H. Tajiri, K. Matsuda, M. Kaise, M. Ikegami, and H. Sasaki, “Magnifying Endoscopy Combined With Narrow Band Imaging System for Early Gastric Cancer: Correlation of Vascular Pattern With Histopathology (Including Video),” Endoscopy 36, no. 12 (2004): 1080-1084.

[24] M. Kaise, M. Kato, M. Urashima, et al., “Magnifying Endoscopy Combined With Narrow-Band Imaging for Differential Diagnosis of Superficial Depressed Gastric Lesions,” Endoscopy 41, no. 4 (2009): 310-315.

[25] E. Savarino, M. Corbo, P. Dulbecco, et al., “Narrow-Band Imaging With Magnifying Endoscopy Is Accurate for Detecting Gastric Intestinal Metaplasia,” World Journal of Gastroenterology 19, no. 17 (2013): 2668-2675.

[26] P. Marcos, G. Brito-Gonçalves, D. Libânio, et al., “Endoscopic Grading of Gastric Intestinal Metaplasia on Risk Assessment for Early Gastric Neoplasia: Can we Replace Histology Assessment Also in the West?,” Gut 69, no. 10 (2020): 1762-1768.

[27] T. M. DaFonte, E. Gleeson, T. Morson, K. L. Olshan, C. J. Moran, and M. M. Leonard, “No Increased Risk of Taking Additional Intestinal Mucosal Research Biopsies From the Duodenum During Pediatric Endoscopy,” Journal of Pediatric Gastroenterology and Nutrition 76, no. 4 (2023): 480-482.

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2025 The Author(s). Journal of Digestive Diseases published by Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and John Wiley & Sons Australia, Ltd.