Differences in the detection of gastric premalignant conditions and its correlation with gastric cancer after a negative esophagogastroduodenoscopy in a low-risk gastric cancer country
DOI:
https://doi.org/10.47892/rgp.2025.452.1909Keywords:
Cancer, Gastric, Misdiagnosis, Quality Indicators, Health CareAbstract
Introduction: Gastric cancer (GC), with nearly 90% being sporadic adenocarcinomas, is preceded by gastric premalignant conditions (GPC). Accurate detection of GPC during esophagogastroduodenoscopy (EGD) can enhance the identification of high-risk patients and improve early GC diagnosis. However, GPC detection rates during EGD vary among endoscopists, potentially leading to differences in GC rates after a negative EGD (GC postEGD). Objective: This study aimed to assess the correlation between the GPC detection rate and the rate of GC post-EGD among endoscopists. Materials and methods: We conducted an observational study of EGDs at a community hospital between 2010 and 2019. GPC were defined as glandular atrophy, intestinal metaplasia, and dysplasia. EGDs were categorized into three groups: (i) benign, (ii) GPC, and (iii) malignant findings. GC post-EGD was defined as a diagnosis of gastric adenocarcinoma within three years of an EGD negative for malignancy. GPC detection rates and GC post-EGD were calculated for each endoscopist. Results: A total of 18,635 EGDs were performed by nine endoscopists. Gastric biopsies were obtained in 2,415 (13%) EGDs, identifying 533 GPCs (2.9%). The GC post-EGD rate was 1.26 per 1,000 EGDs. The detection rate of GPC varied between 1.8% and 5.8%, while GC post-EGD rates ranged from 0 to 3.36 per 1,000 EGDs. A negative correlation trend was observed between GC post-EGD and GPC detection rate (rs=-0.65, p=0.057), which was statistically significant for dysplasia (rs=-0.69, p=0.037). Conclusion: The detection rate of GPC—particularly dysplasia—showed a negative correlation with GC post-EGD in a community hospital within a low-risk setting during the period from 2010 to 2019.
Downloads
Metrics
References
Correa P, Piazuelo MB. The gastric precancerous cascade. J Dig Dis. 2012;13(1):2-9. doi: 10.1111/j.1751-2980.2011.00550.x.
Delgado-Guillena PG, Morales-Alvarado VJ, Elosua-González A, Murcia Pomares O, Pérez-Aisa A, Córdova H, et al. Gastroenterologists’ attitudes on the detection and management of gastric premalignant conditions: results of a nationwide survey in Spain. Eur J Cancer Prev. 2021;30(6):431-436. doi: 10.1097/CEJ.0000000000000648.
Yip HC, Uedo N, Chan SM, Teoh AYB, Wong SKH, Chiu PW, et al. An international survey on recognition and characterization of atrophic gastritis and intestinal metaplasia. Endosc Int Open. 2020;8(10):E1365-E1370. doi: 10.1055/a-1230-3586.
Dinis-Ribeiro M, Areia M, de Vries AC, Marcos-Pinto R, Monteiro-Soares M, O’Connor A, 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(1):74-94. doi: 10.1055/s-0031-1291491.
Pimentel-Nunes P, Libânio D, Marcos-Pinto R, Areia M, Leja M, Esposito G, 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. doi: 10.1055/a-0859-1883.
Bisschops R, Areia M, Coron E, Dobru D, Kaskas B, Kuvaev R, et al. Performance measures for upper gastrointestinal endoscopy: A European Society of Gastrointestinal Endoscopy quality improvement initiative. United European Gastroenterol J. 2016;4(5):629-656. doi: 10.1177/2050640616664843.
Dinis-Ribeiro M, Libânio D, Uchima H, Spaander MCW, Bornschein J, Matysiak-Budnik T, 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. 2025;57(5):504-554. doi: 10.1055/a2529-5025.
Morgan DR, Corral JE, Li D, Montgomery EA, Riquelme A, Kim JJ, et al. ACG Clinical Guideline: Diagnosis and Management of Gastric Premalignant Conditions. Am J Gastroenterol. 2025;120(4):709-737. doi: 10.14309/ajg.0000000000003350.
Areia M, Dinis-Ribeiro M, Rocha Gonçalves F. Cost-utility analysis of endoscopic surveillance of patients with gastric premalignant conditions. Helicobacter. 2014;19(6):425-36. doi: 10.1111/hel.12150.
Pimenta-Melo AR, Monteiro-Soares M, Libânio D, Dinis-Ribeiro M. Missing rate for gastric cancer during upper gastrointestinal endoscopy: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol. 2016;28(9):1041-9. doi: 10.1097/ MEG.0000000000000657.
Menon S, Trudgill N. How commonly is upper gastrointestinal cancer missed at endoscopy? A meta-analysis. Endosc Int Open. 2014;2(2):E46-50. doi: 10.1055/s-0034-1365524.
Alexandre L, Tsilegeridis-Legeris T, Lam S. Clinical and Endoscopic Characteristics Associated With Post-Endoscopy Upper Gastrointestinal Cancers: A Systematic Review and Meta-analysis. Gastroenterology. 2022;162(4):1123-1135. doi: 10.1053/j.gastro.2021.12.270.
Delgado-Guillena P, Morales-Alvarado V, Ramírez Salazar C, Jimeno Ramiro M, Llibre Nieto G, Galvez-Olortegui J, et al. Frequency and clinical characteristics of early gastric cancer in comparison to advanced gastric cancer in a health area of Spain. Gastroenterol Hepatol. 2020;43(9):506-514. English, Spanish. doi: 10.1016/j.gastrohep.2020.01.015.
Chapelle N, Bouvier A-M, Manfredi S, Drouillard A, Lepage C, Faivre J, et al. Early Gastric Cancer: Trends in Incidence, Management, and Survival in a Well-Defined French Population. Ann Surg Oncol. 2016;23(11):3677-3683. doi: 10.1245/s10434- 016-5279-z.
Dassen AE, Dikken JL, Bosscha K, Wouters MW, Cats A, van de Velde CJ, et al. Gastric cancer: decreasing incidence but stable survival in the Netherlands. Acta Oncol. 2014;53(1):138-42. doi: 10.3109/0284186X.2013.789139.
Bornschein J, Tran-Nguyen T, Fernandez-Esparrach G, Ash S, Balaguer F, Bird-Lieberman E, et al. Biopsy Sampling in Upper Gastrointestinal Endoscopy: A Survey from 10 Tertiary Referral Centres Across Europe. Dig Dis. 2021;39(3):179-189. doi: 10.1159/000511867.
Delgado Guillena PG, Morales Alvarado VJ, Jimeno Ramiro M, Rigau Cañardo J, Ramírez Salazar C, García Rodríguez A, et al. Gastric cancer missed at esophagogastroduodenoscopy in a well-defined Spanish population. Dig Liver Dis. 2019;51(8):1123-1129. doi: 10.1016/j.dld.2019.03.005.
Hernanz N, Rodríguez de Santiago E, Marcos Prieto HM, Jorge Turrión MÁ, Barreiro Alonso E, Rodríguez Escaja C, et al. Characteristics and consequences of missed gastric cancer: A multicentric cohort study. Dig Liver Dis. 2019;51(6):894-900. doi: 10.1016/j.dld.2019.02.006.
Voutilainen ME, Juhola MT. Evaluation of the diagnostic accuracy of gastroscopy to detect gastric tumours: clinicopathological features and prognosis of patients with gastric cancer missed on endoscopy. Eur J Gastroenterol Hepatol. 2005;17(12):1345-9. doi: 10.1097/00042737-200512000- 00013.
Teh JL, Tan JR, Lau LJF, Saxena N, Salim A, Tay A, et al. Longer examination time improves detection of gastric cancer during diagnostic upper gastrointestinal endoscopy. Clin Gastroenterol Hepatol. 2015;13(3):480-487.e2. doi: 10.1016/j. cgh.2014.07.059.
Park JM, Huo SM, Lee HH, Lee BI, Song HJ, Choi MG. Longer Observation Time Increases Proportion of Neoplasms Detected by Esophagogastroduodenoscopy. Gastroenterology. 2017;153(2):460-469.e1. doi: 10.1053/j.gastro.2017.05.009.
Buxbaum JL, Hormozdi D, Dinis-Ribeiro M, Lane C, Dias-Silva D, Sahakian A, et al. Narrow-band imaging versus white light versus mapping biopsy for gastric intestinal metaplasia: a prospective blinded trial. Gastrointest Endosc. 2017;86(5):857- 865. doi: 10.1016/j.gie.2017.03.1528.
Januszewicz W, Wieszczy P, Bialek A, Karpinska K, Szlak J, Szymonik J, et al. Endoscopist biopsy rate as a quality indicator for outpatient gastroscopy: a multicenter cohort study with validation. Gastrointest Endosc. 2019;89(6):1141–9. doi: 10.1016/j.gie.2019.01.008.
Zhou J, Li Z, Ji R, Wang P, Zhang A, Wu K, et al. Influence of Sedation on the Detection Rate of Early Cancer and Precancerous Lesions During Diagnostic Upper Gastrointestinal Endoscopies: A Multicenter Retrospective Study. Am J Gastroenterol. 2021;116(6):1230-1237. doi: 10.14309/ajg.0000000000001201.
Fujita S. Biology of early gastric carcinoma. Pathol Res Pract. 1978;163(4):297-309. doi: 10.1016/S0344-0338(78)80028-4.
Hosokawa O, Tsuda S, Kidani E, Watanabe K, Tanigawa Y, Shirasaki S, et al. Diagnosis of gastric cancer up to three years after negative upper gastrointestinal endoscopy. Endoscopy. 1998;30(8):669-74. doi: 10.1055/s-2007-1001386.
Kamran U, King D, Abbasi A, Coupland B, Umar N, Chapman WC, et al. A root cause analysis system to establish the most plausible explanation for post-endoscopy upper gastrointestinal cancer. Endoscopy. 2023;55(2):109-118. doi: 10.1055/a-1917-0192.
Kaminski MF, Wieszczy P, Rupinski M, Wojciechowska U, Didkowska J, Kraszewska E, et al. Increased Rate of Adenoma Detection Associates With Reduced Risk of Colorectal Cancer and Death. Gastroenterology. 2017;153(1):98-105. doi: 10.1053/j.gastro.2017.04.006.
Park CH, Kim B, Chung H, Lee H, Park JC, Shin SK, et al. Endoscopic quality indicators for esophagogastroduodenoscopy in gastric cancer screening. Dig Dis Sci. 2015;60(1):38-46. doi: 10.1007/ s10620-014-3288-y.
Beg S, Ragunath K, Wyman A, Banks M, Trudgill N, Mark Pritchard D, et al. Quality standards in upper gastrointestinal endoscopy: a position statement of the British Society of Gastroenterology (BSG) and Association of Upper Gastrointestinal Surgeons of Great Britain and Ireland (AUGIS). Gut. 2017;66(11):1886-1899. doi: 10.1136/gutjnl-2017-314109.
Chapelle N, Péron M, Mosnier J-F, Quénéhervé L, Coron E, Bourget A, et al. Prevalence, Characteristics and Endoscopic Management of Gastric Premalignant Lesions in France. Dig Dis. 2020;38(4):286-292. doi: 10.1159/000503748.
Raftopoulos SC, Segarajasingam DS, Burke V, Ee HC, Yusoff IF. A cohort study of missed and new cancers after esophagogastroduodenoscopy. Am J Gastroenterol. 2010;105(6):1292-7. doi: 10.1038/ajg.2009.736.
Lassen A, Hallas J, de Muckadell OB. The risk of missed gastroesophageal cancer diagnoses in users and nonusers of antisecretory medication. Gastroenterology. 2005;129(4):1179- 86. doi: 10.1053/j.gastro.2005.07.028.
Hosokawa O, Tsuda S, Kidani E, Watanabe K, Tanigawa Y, Shirasaki S, et al. Diagnosis of gastric cancer up to three years after negative upper gastrointestinal endoscopy. Endoscopy. 1998;30(8):669-74. doi: 10.1055/s-2007-1001386.
Rugge M, Genta RM, Malfertheiner P, Dinis-Ribeiro M, ElSerag H, Graham DY, et al. RE.GA.IN.: the Real-world Gastritis Initiative-updating the updates. Gut. 2024;73(3):407-441. doi: 10.1136/gutjnl-2023-331164.
Latorre G, Vargas JI, Shah SC, Ivanovic-Zuvic D, Achurra P, Fritzsche M, et al. Implementation of the updated Sydney system biopsy protocol improves the diagnostic yield of gastric preneoplastic conditions: Results from a real-world study. Gastroenterol Hepatol. 2024;47(8):793-803. doi: 10.1016/j.gastrohep.2023.08.005.
Shen Y, Gao X-J, Zhang X-X, Zhao J-M, Hu F-F, Han J-L, et al. Endoscopists and endoscopic assistants’ qualifications, but not their biopsy rates, improve gastric precancerous lesions detection rate. World J Gastrointest Endosc. 2025;17(4):104097. doi: 10.4253/wjge.v17.i4.104097.
Delgado-Guillena P, Jimeno M, López-Nuñez A, Córdova H, Fernández-Esparrach G. The endoscopic model for gastric carcinogenesis and Helicobacter pylori infection: a potential visual mind-map during gastroscopy examination. Gastroenterol Hepatol. 2024 Dec;47(10):502214. doi: 10.1016/j.gastrohep.2024.502214.
Nasseri-Moghaddam S, Mousavian A-H, Kasaeian A, Kanno T, Yuan Y, Ford AC, et al. What is the Prevalence of Clinically Significant Endoscopic Findings in Subjects With Dyspepsia? Updated Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol. 2023;21(7):1739-1749.e2. doi: 10.1016/j.cgh.2022.05.041.
Gavric A, Hanzel J, Zagar T, Zadnik V, Plut S, Stabuc B. Survival outcomes and rate of missed upper gastrointestinal cancers at routine endoscopy: a single centre retrospective cohort study. Eur J Gastroenterol Hepatol. 2020;32(10):1312-1321. doi: 10.1097/MEG.0000000000001863.
Córdova H, Sánchez-Montes C, Delgado-Guillena PG, Morales VJ, Sendino O, González-Suárez B, et al. Quality indicators for esophagogastroduodenoscopy: A comparative study of outcomes after an improvement programme in a tertiary hospital. Gastroenterol Hepatol. 2017;40(9):587-594. English, Spanish. doi: 10.1016/j.gastrohep.2017.05.007.
Alcaraz Serrat JA, Córdova H, Moreira L, Pocurrull A, Ureña R, Delgado-Guillena PG, et al. Evaluation of long-term adherence to oesophagogastroduodenoscopy quality indicators. Gastroenterol Hepatol. 2020 Dec;43(10):589-597. doi: 10.1016/j.gastrohep.2020.01.017.
Dekker E, Houwen BBSL, Puig I, Bustamante-Balén M, Coron E, Dobru DE, et al. Curriculum for optical diagnosis training in Europe: European Society of Gastrointestinal Endoscopy (ESGE) Position Statement. Endoscopy. 2020;52(10):899-923. doi: 10.1055/a-1231-5123.
Cubiella J, Pérez Aisa Á, Cuatrecasas M, Díez Redondo P, Fernández Esparrach G, Marín-Gabriel JC, et al. Gastric cancer screening in low incidence populations: Position statement of AEG, SEED and SEAP. Gastroenterol Hepatol. 2021;44(1):67-86. English, Spanish. doi: 10.1016/j.gastrohep.2020.08.004.
Fernández-Esparrach G, Marín-Gabriel JC, Díez Redondo P, Núñez H, Rodríguez de Santiago E, Rosón P, et al. Quality in diagnostic upper gastrointestinal endoscopy for the detection and surveillance of gastric cancer precursor lesions: Position paper of AEG, SEED and SEAP. Gastroenterol Hepatol. 2021;44(6):448-464. English, Spanish. doi: 10.1016/j. gastrohep.2021.01.002.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2025 Pedro Genaro Delgado-Guillena, Víctor Jair Morales-Alvarado, Beatriz De-Riba-Soler, Gemma Llibre-Nieto, Indira Armas-Ramírez, Terry Guillena-Castañeda, Ivana Levy-Ríos, Mireya Jimeno-Ramiro, Joaquim Rigau-Cañardo, Albert García-Rodríguez, Esteve Llargués Rocabruna, Henry Córdova, Gloria Fernández-Esparrach

This work is licensed under a Creative Commons Attribution 4.0 International License.
Revista de Gastroenterología del Perú by Sociedad Peruana de Gastroenterología del Perú is licensed under a Licencia Creative Commons Atribución 4.0 Internacional..
Aquellos autores/as que tengan publicaciones con esta revista, aceptan los términos siguientes:
- Los autores/as conservarán sus derechos de autor y garantizarán a la revista el derecho de primera publicación de su obra, el cuál estará simultáneamente sujeto a la Licencia de reconocimiento de Creative Commons que permite a terceros compartir la obra siempre que se indique su autor y su primera publicación esta revista.
- Los autores/as podrán adoptar otros acuerdos de licencia no exclusiva de distribución de la versión de la obra publicada (p. ej.: depositarla en un archivo telemático institucional o publicarla en un volumen monográfico) siempre que se indique la publicación inicial en esta revista.
- Se permite y recomienda a los autores/as difundir su obra a través de Internet (p. ej.: en archivos telemáticos institucionales o en su página web) antes y durante el proceso de envío, lo cual puede producir intercambios interesantes y aumentar las citas de la obra publicada. (Véase El efecto del acceso abierto).








2022