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AGA Technical Review on Gastric Intestinal Metaplasia—Natural History and Clinical Outcomes

2019; Elsevier BV; Volume: 158; Issue: 3 Linguagem: Inglês

10.1053/j.gastro.2019.12.001

1528-0012

Andrew J. Gawron, Shailja C. Shah, Osama Altayar, Perica Davitkov, Douglas R. Morgan, Kevin Turner, Reem A. Mustafa,

Gastrointestinal disorders and treatments

See editorial on page 473. See editorial on page 473. Gastric cancer is the third leading cause of cancer-related mortality and the fifth most common cancer globally. An estimated 1 million new cases and 750,000 related deaths are projected to occur annually, with the majority of cases in East Asia and developing or recently developed countries.1Bray 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: 394-424Crossref PubMed Scopus (50573) Google Scholar In the United States, which is considered a low-incidence country overall, 27,510 incident gastric cancer cases and 11,140 related deaths were estimated to occur in 2019, representing 1.6% and 1.8% of all new cancer diagnoses and deaths, respectively.2Siegel R.L. Miller K.D. Jemal A. Cancer statistics, 2017.CA Cancer J Clin. 2017; 67: 7-30Crossref PubMed Scopus (12753) Google Scholar While there is clear ethnic and geographic variation in disease burden worldwide with populations and regions of high and low incidence, in an era of expanding globalization it is equally important to recognize that early-generation immigrants from high- to low-incidence countries generally retain a higher risk of gastric cancer and related mortality.3Pabla B.S. Shah S.C. Corral J.E. et al.Increasing incidence and mortality of gastric cancer in immigrant populations from high to low regions of incidence—a systematic review and meta-analysis.Clin Gastroenterol Hepatol. 2019 May 30; ([Epub ahead of print])PubMed Google Scholar Indeed, recent estimates confirm that the incidence and mortality rates of gastric cancer are increasing in the United States among some groups, including minority populations.2Siegel R.L. Miller K.D. Jemal A. Cancer statistics, 2017.CA Cancer J Clin. 2017; 67: 7-30Crossref PubMed Scopus (12753) Google Scholar,4Merchant S.J. Kim J. Choi A.H. et al.A rising trend in the incidence of advanced gastric cancer in young Hispanic men.Gastric Cancer. 2017; 20: 226-234Crossref PubMed Scopus (73) Google Scholar,5Anderson W.F. Rabkin C.S. Turner N. et al.The changing face of noncardia gastric cancer incidence among US non-Hispanic whites.J Natl Cancer Inst. 2018; 110: 608-615Crossref PubMed Scopus (111) Google Scholar Gastric adenocarcinoma is classified by anatomic location as cardia and non-cardia and by the Lauren histologic classification as intestinal-type and diffuse-type.6Correa P. Schneider B.G. Etiology of gastric cancer: what is new?.Cancer Epidemiol Biomarkers Prev. 2005; 14: 1865-1868Crossref PubMed Scopus (49) Google Scholar Intestinal-type non-cardia gastric adenocarcinoma (NCGA) develops as a stepwise progression of discrete histopathologic stages from normal mucosa to chronic non-atrophic gastritis to chronic atrophic gastritis (AG) to gastric intestinal metaplasia (GIM) and dysplasia, before final malignant transformation (Figure 1). Infection with Helicobacter pylori is accepted to be the primary driver for this progression, termed the Correa cascade, although other triggers such as autoimmune gastritis are recognized.7Minalyan A. Benhammou J.N. Artashesyan A. et al.Autoimmune atrophic gastritis: current perspectives.Clin Exp Gastroenterol. 2017; 10: 19-27Crossref PubMed Scopus (75) Google Scholar, 8Jencks D.S. Adam J.D. Borum M.L. et al.Overview of current concepts in gastric intestinal metaplasia and gastric cancer.Gastroenterol Hepatol (NY). 2018; 14: 92-101PubMed Google Scholar, 9Correa P. Helicobacter pylori and gastric cancer: state of the art.Cancer Epidemiol Biomarkers Prev. 1996; 5: 477-481PubMed Google Scholar, 10Polk D.B. Peek R.M. Helicobacter pylori: gastric cancer and beyond.Nat Rev Cancer. 2010; 10: 403-414Crossref PubMed Scopus (740) Google Scholar Risk factors for advancement along the Correa cascade are incompletely understood, given that only a minority of individuals colonized with H pylori (approximately 1%–2%) will develop cancer.11Wroblewski L.E. Peek R.M. Wilson K.T. Helicobacter pylori and gastric cancer: factors that modulate disease risk.Clin Microbiol Rev. 2010; 23: 713-739Crossref PubMed Scopus (893) Google Scholar By contrast, no precursor lesions are definitively identified for diffuse-type gastric adenocarcinoma, although mixed intestinal–type and diffuse-type histology are noted in up to 10% of patients.11Wroblewski L.E. Peek R.M. Wilson K.T. Helicobacter pylori and gastric cancer: factors that modulate disease risk.Clin Microbiol Rev. 2010; 23: 713-739Crossref PubMed Scopus (893) Google Scholar The recent National Institutes Health-funded effort known as the “The Cancer Genome Atlas” (TCGA), delineated molecular subtypes of gastric cancer and confirmed both the intestinal and diffuse subtypes as distinct, as well as 2 lesser subtypes (Epstein-Barr virus–associated and microsatellite instability).12Bass A.J. Thorsson V. Shmulevich I. et al.Comprehensive molecular characterization of gastric adenocarcinoma.Nature. 2014; 513: 202-209Crossref PubMed Scopus (3908) Google Scholar AG and GIM are precancerous lesions that are associated with an increased risk of intestinal-type NCGA (hereafter referred to as “NCGA”) with GIM being the lesion more clearly discriminable on endoscopy and histology.13Correa P. Human gastric carcinogenesis: a multistep and multifactorial process—First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention.Cancer Res. 1992; 52: 6735-6740PubMed Google Scholar The combination of identifiable precancerous stages and stepwise neoplastic progression offers the potential opportunity for screening and surveillance, with the goal of early detection of neoplasia and opportunity for endoscopic resection to thereby reduce disease-related morbidity and mortality. Current US-based guidelines do not recommend endoscopic screening for NCGA nor do they recommend universal surveillance of gastric precancerous lesions for the purpose of early NCGA detection.14Evans J.A. Chandrasekhara V. et al.ASGE Standards of Practice CommitteeThe role of endoscopy in the management of premalignant and malignant conditions of the stomach.Gastrointest Endosc. 2015; 82: 1-8Abstract Full Text Full Text PDF PubMed Scopus (160) Google Scholar GIM is usually encountered incidentally in patients undergoing esophagogastroduodenoscopy (EGD) and biopsy for nonspecific symptoms (eg, dyspepsia). Limited awareness of risk factors for NCGA, uncertainty regarding the risk factors for neoplastic progression of GIM, and unadjudicated risk vs benefit of GIM surveillance, have resulted in wide clinical practice variability in the evaluation and management of patients with GIM.15Vance R.B. Kubiliun N. Dunbar K.B. How do we manage gastric intestinal metaplasia? A survey of clinical practice trends for gastrointestinal endoscopists in the United States.Dig Dis Sci. 2016; 61: 1870-1878Crossref PubMed Scopus (10) Google Scholar,16Shah S.C. Itzkowitz S.H. Jandorf L. Knowledge gaps among physicians caring for multiethnic populations at increased gastric cancer risk.Gut Liver. 2018; 12: 38-45Crossref PubMed Scopus (11) Google Scholar The American Society for Gastrointestinal Endoscopy (ASGE), the British Society of Gastroenterology (BSG),17Banks 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: 1545-1575Crossref PubMed Scopus (213) Google Scholar and the European Society for Gastrointestinal Endoscopy (ESGE) have position statements on the management of gastric precancerous lesions, with the updated 2019 European guidelines developed using an evidenced-based Delphi process and expert consensus vote.14Evans J.A. Chandrasekhara V. et al.ASGE Standards of Practice CommitteeThe role of endoscopy in the management of premalignant and malignant conditions of the stomach.Gastrointest Endosc. 2015; 82: 1-8Abstract Full Text Full Text PDF PubMed Scopus (160) Google Scholar,18Dinis-Ribeiro M. Areia M. De Vries 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: 74-94Crossref PubMed Scopus (538) Google Scholar,19Pimentel-Nunes P. Libânio 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: 365-388PubMed Google Scholar By contrast, the American Society for Gastrointestinal Endoscopy position statement is limited in its recommendations on GIM management without a formal systematic review of the available literature.14Evans J.A. Chandrasekhara V. et al.ASGE Standards of Practice CommitteeThe role of endoscopy in the management of premalignant and malignant conditions of the stomach.Gastrointest Endosc. 2015; 82: 1-8Abstract Full Text Full Text PDF PubMed Scopus (160) Google Scholar A 2015 global consensus statement provided guidance on diagnosis and treatment of H pylori gastritis20Sugano K. Tack J. Kuipers E.J. et al.Kyoto global consensus report on Helicobacter pylori gastritis.Gut. 2015; 64: 1353-1367Crossref PubMed Scopus (941) Google Scholar; however, incidental GIM management was not addressed specifically. There is an unmet need for updated comprehensive guidelines for GIM management that are practical and relevant for the US population, particularly given the racial/ethnic diversity of the inhabitants and their differential risk profiles for NCGA.21Hwang J.H. Understanding gastric cancer risk factors: we need to close the gap.Gut Liver. 2018; 12: 1-2Crossref PubMed Scopus (7) Google Scholar,22Kim G.H. Liang P.S. Bang S.J. et al.Screening and surveillance for gastric cancer in the United States: is it needed?.Gastrointest Endosc. 2016; 84: 18-28Abstract Full Text Full Text PDF PubMed Scopus (131) Google Scholar Our aim was to provide a systematic and comprehensive synthesis of the literature to inform the American Gastroenterological Association (AGA) guideline panel in formulating evidence-based recommendations on the management of GIM in the absence of concurrent neoplasia (dysplasia or cancer), with a focus on patient-important outcomes associated with H pylori eradication and endoscopic surveillance. The evidence used to inform the guideline is presented in 2 separate but related technical review (TR) reports. The present document represents “TR1” and is focused on the natural history and clinical outcomes of GIM, while TR2 is focused on the epidemiology of and risk factors for GIM.23Altayar O. Davitkov P. Shah S.C. et al.AGA technical review on gastric intestinal metaplasia—epidemiology and risk factors.Gastroenterology. 2020; 158: 732-744Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar The TR team systematically reviewed and synthesized the literature to inform predefined questions proposed by the AGA guideline panel using standard systematic review methodology. We used the Grading of Recommendations Assessment, Development and Evaluation (GRADE) framework to evaluate the certainty of evidence (also known as quality of evidence).24Guyatt G.H. Oxman A.D. Schünemann H.J. et al.GRADE guidelines: a new series of articles in the Journal of Clinical Epidemiology.J Clin Epidemiol. 2011; 64: 380-382Abstract Full Text Full Text PDF PubMed Scopus (1671) Google Scholar The TR team included a GRADE methodologist (R.M.) and 6 clinical domain experts (3 gastroenterologists, 1 pathologist, and 2 gastroenterology fellows with outcomes research expertise and guideline methodology training). The AGA guideline panel identified 4 clinically relevant questions and the TR team used the PICO format, which identifies a population, intervention, comparator, and outcomes to guide the evidence synthesis. Table 1 summarizes the PICO questions as well as direct and indirect evidence needed to inform the systematic review and the AGA guideline. The primary objective of the first question (PICO 1) was to synthesize the data assessing the need to empirically test for H pylori infection (and treat if positive) in patients with GIM. The primary objectives of PICO 2 and PICO 3 were to synthesize the data informing the need for surveillance upper endoscopy once GIM is diagnosed in groups at otherwise low vs high risk for NCGA, respectively, in the United States. The primary objective of PICO 4 was to synthesize the data informing the need for short-term endoscopic follow-up and histologic assessment in patients with GIM diagnosed incidentally on EGD.Table 1PICO Questions and Evidence Needed to Inform PICO QuestionsPICO questionPatient-important outcomesEvidence needed to inform PICO questions1.Among patients with GIM without neoplasia, does testing for H pylori and treating if positive vs no testing affect patient-important outcomes?2.Among patients with GIM without neoplasia, who are identified as low risk, does subsequent upper endoscopic surveillance vs no follow-up affect patient-important outcomes?3.Among patients with GIM without neoplasia, who are identified as high risk, does subsequent upper endoscopic surveillance vs no follow-up affect patient-important outcomes?4.Among patients with GIM without dysplasia, does short-term upper endoscopic follow-up (<1 year) to determine the extent (using biopsies) of GIM vs no short-term follow-up affect patient-important outcomes?Early gastric cancer detectionReduced gastric cancer morbidity/mortalityEndoscopy complicationsCostsPsychological harmsIncidence and prevalence of GIM in the US populationIncidence of gastric cancer in the general populationPrevalence of concurrent gastric cancer in patients with GIMIncidence of gastric cancer in patients with GIM after GIM diagnosisRisk of progression to gastric cancer in patients with GIMSubgroups: Family history of gastric cancer, race/ethnicity, smoking status, histologic features, extent of GIM, and biomarkersPotential adverse consequences of performing surveillance upper endoscopy for patients with GIMBenefits of performing surveillance upper endoscopy for patients with GIM Open table in a new tab After finalizing the PICO questions, the TR team and the guideline panel rated and prioritized outcomes critical for decision-making (Table 1). Patient-important outcomes of interest included both benefits and harms, such as early NCGA detection, reduced morbidity/mortality from NCGA, complications associated with endoscopy, psychological outcomes (eg, anxiety and stress related to endoscopic surveillance, coping with a precancerous condition), and resource implications (eg, “cost” of endoscopic and histologic surveillance). A comprehensive list of direct and indirect evidence needed to inform the questions was developed (Table 1). The desired evidence included incidence and prevalence data for GIM, incidence of NCGA among individuals with GIM, and risk factors associated with progression to NCGA in patients with GIM compared to individuals without GIM. This “wish list” of needed evidence guided the systematic literature search. Given the presumed paucity of robust direct data on GIM in the United States, evidence from all regions of the world was considered relevant in the evidence-gathering phase. Details related to the management and natural progression of dysplasia were considered outside the scope of this TR unless there were clear discernible data to inform clinical outcomes of GIM specifically. We reported the systematic review and the related meta-analyses results in concordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) and Meta-Analysis of Observational Studies in Epidemiology (MOOSE) statements.25Stroup D. Berlin J. Morton S. et al.Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group.JAMA. 2000; 283: 2008-2012Crossref PubMed Scopus (15336) Google Scholar,26Moher D. Liberati A. Tetzlaff J. et al.Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement.BMJ. 2009; 339 (b2535–b2535)Crossref Scopus (15071) Google Scholar The TR adhered to weekly meetings to conduct the systematic review and develop the GRADE evidence profiles for each PICO question.24Guyatt G.H. Oxman A.D. Schünemann H.J. et al.GRADE guidelines: a new series of articles in the Journal of Clinical Epidemiology.J Clin Epidemiol. 2011; 64: 380-382Abstract Full Text Full Text PDF PubMed Scopus (1671) Google Scholar The weekly meetings clarified and addressed issues that arose during the review process. Decisions were documented and input from the guideline panel was requested for key decisions. In collaboration with a medical librarian, we defined a systematic search strategy and searched 3 electronic databases, including Ovid MEDLINE Epub Ahead of Print, In-Process & Other Non-Indexed Citations, Ovid MEDLINE Daily and Ovid MEDLINE from 1946; Embase Classic+Embase from 1947; and Wiley’s Cochrane Library. The initial search was conducted in July 2017 and updated in September 2018. The primary search terms included stomach, precancerous conditions, neoplasms, gastric/stomach mucosa, and metaplasia. The full literature search strategy is provided in Supplementary Table 1. Additionally, we checked the references of prior systematic reviews and guidance documents to identify additional studies that met our inclusion criteria. We included randomized controlled trials (RCTs), prospective and retrospective cohort studies, case–control studies, and cross-sectional studies as long as they informed at least one PICO question. We included studies only where GIM was histologically confirmed. However, because we acknowledge that the noninvasive diagnosis of gastric preneoplasia by image-enhancing endoscopic techniques, such as magnifying endoscopy with narrow band imaging, is part of routine practice in East Asia and some other areas of the world where NCGA is endemic, we did not a priori exclude these studies if they otherwise met inclusion criteria and informed any of the PICO questions; that said, we did not identify any such studies. We excluded studies that included prevalent gastric cancer or history of gastric cancer to limit bias. We excluded studies on gastric cancer screening unless they included discernible data on histologically confirmed GIM. We excluded studies without data on GIM, studies that included GIM with concomitant neoplasia, and studies in which we were otherwise unable to separate the outcomes by GIM status. We excluded studies that were not performed in humans or those that did not include primary data, such as narrative reviews, opinion pieces, and letters. We excluded studies in pediatric-only populations, studies conducted to evaluate the diagnostic accuracy of H pylori tests, studies that compared different H pylori treatment regimens, and studies that focused solely on gastric dysplasia or cancer without data on GIM. For studies that informed the incidence or prevalence of GIM, we included studies with at least 100 patients. After the data-gathering phase, the threshold was modified to 250 patients, due to the large number of studies identified in our search; before this modification, we performed a sensitivity analysis calculation that confirmed the unlikelihood that the prevalence estimates would be affected if smaller studies were included. For studies that informed the risk or rate of progression from GIM to NCGA, we included studies with at least 20 patients with histologically confirmed GIM. We also obtained and searched the full texts of relevant abstracts. If the abstract was published before 2015 and no accompanying publication was identified, we excluded the reference. For abstracts published in or after 2015, we contacted the authors to inquire about publication status and additional data; we excluded the reference if we received no response. Two TR members independently screened the search results for articles based on titles and abstracts. The full-text article was retrieved for any citation considered potentially relevant by any investigator. Each of the investigators then independently assessed the eligibility of each article by using a pilot-tested, standardized form with written instructions generated and maintained on the Research Electronic Data Capture (REDCap) platform27Harris P.A. Taylor R. Thielke R. et al.Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support.J Biomed Inform. 2009; 42: 377-781Crossref PubMed Scopus (23133) Google Scholar hosted at The University of Kansas. If at least 1 of the prespecified inclusion criteria was not met, the article was excluded. Any disagreement was resolved by consensus or arbitration. Due to the vast amount of literature focused on gastric cancer and H pylori, but not specifically GIM, it was necessary to agree on definitions of certain concepts before data abstraction in order to limit confusion and disagreement. Box 1 summarizes the definition of different concepts that were used for this review.Box 1Definitions used throughout the process of the systematic reviews.Histologic progression: (a) progression of GIM to dysplasia and/or NCGA over time; (b) increase in histologic score or stage, ∗Includes Correa histology score, Operative Link on Gastritis Assessment (OLGA), and Operative Link on Gastric Intestinal Metaplasia Assessment (OLGIM)—see text for details only if there was transition to a higher discrete global histologic category (ie, incident dysplasia or NCGA)Histologic regression: (a) regression of GIM to normal gastric cancer, non-AG, or AG over time; (b) decrease in histologic score or stage, ∗Includes Correa histology score, Operative Link on Gastritis Assessment (OLGA), and Operative Link on Gastric Intestinal Metaplasia Assessment (OLGIM)—see text for details only if there was transition to a lower discrete histologic category (ie, normal mucosa or [non]-AG)Extensive GIM: GIM involving both the antrum and corpus or corpus aloneLimited GIM: GIM involving only the antrum or incisuraComplete GIM: (a) Resembles small intestinal epithelium phenotype on H&E staining; (b) type I GIM (see text)Incomplete GIM: (a) Resembles colonic epithelium phenotype on H&E staining; (b) type II and III GIM (see text)∗Includes Correa histology score, Operative Link on Gastritis Assessment (OLGA), and Operative Link on Gastric Intestinal Metaplasia Assessment (OLGIM)—see text for details Histologic progression: (a) progression of GIM to dysplasia and/or NCGA over time; (b) increase in histologic score or stage, ∗Includes Correa histology score, Operative Link on Gastritis Assessment (OLGA), and Operative Link on Gastric Intestinal Metaplasia Assessment (OLGIM)—see text for details only if there was transition to a higher discrete global histologic category (ie, incident dysplasia or NCGA) Histologic regression: (a) regression of GIM to normal gastric cancer, non-AG, or AG over time; (b) decrease in histologic score or stage, ∗Includes Correa histology score, Operative Link on Gastritis Assessment (OLGA), and Operative Link on Gastric Intestinal Metaplasia Assessment (OLGIM)—see text for details only if there was transition to a lower discrete histologic category (ie, normal mucosa or [non]-AG) Extensive GIM: GIM involving both the antrum and corpus or corpus alone Limited GIM: GIM involving only the antrum or incisura Complete GIM: (a) Resembles small intestinal epithelium phenotype on H&E staining; (b) type I GIM (see text) Incomplete GIM: (a) Resembles colonic epithelium phenotype on H&E staining; (b) type II and III GIM (see text)∗Includes Correa histology score, Operative Link on Gastritis Assessment (OLGA), and Operative Link on Gastric Intestinal Metaplasia Assessment (OLGIM)—see text for details Global histologic progression or regression of GIM were deemed to be the more clinically relevant outcome because scoring and staging systems are not used routinely in clinical practice and their implications are not well-defined. Similarly, we focused on incomplete vs complete as the most clinically relevant histologic classification for GIM.28Cassaro M. Rugge M. Gutierrez O. et al.Topographic patterns of intestinal metaplasia and gastric cancer.Am J Gastroenterol. 2000; 95: 1431-1438Crossref PubMed Google Scholar, 29Capelle L.G. De Vries A.C. 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: 1150-1158Abstract Full Text Full Text PDF PubMed Scopus (346) Google Scholar, 30Dixon M.F. Genta R.M. Yardley J.H. 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: 1161-1181Crossref PubMed Scopus (4429) Google Scholar We acknowledge another classification system utilized predominately for research that divides GIM into 3 types: type I GIM (non-secretory absorptive cells and sialomucin-secreting goblet cells), type 2 GIM (few or absent absorptive cells, columnar cells secreting neutral and acid sialomucins, and goblet cells secreting mainly sialomucins but some sulphomucins), and type 3 GIM (columnar cells secreting predominantly sulphomucins and goblet cells secreting sialomucins or sulphomucins).30Dixon M.F. Genta R.M. Yardley J.H. 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: 1161-1181Crossref PubMed Scopus (4429) Google Scholar,31Shah S.C. Gowron A.J. Mustafa R. et al.Histologic subtyping of gastric intestinal metaplasia: overview and considerations for clinical practice.Gastroenterology. 2020; 158: 745-750Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar In accordance with the literature, type I GIM was categorized as complete GIM, while type II and type III were categorized as incomplete GIM.30Dixon M.F. Genta R.M. Yardley J.H. 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: 1161-1181Crossref PubMed Scopus (4429) Google Scholar, 31Shah S.C. Gowron A.J. Mustafa R. et al.Histologic subtyping of gastric intestinal metaplasia: overview and considerations for clinical practice.Gastroenterology. 2020; 158: 745-750Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar, 32Correa P. Piazuelo M.B. Wilson K.T. Pathology of gastric intestinal metaplasia: clinical implications.Am J Gastroenterol. 2010; 105: 493-498Crossref PubMed Scopus (249) Google Scholar, 33El-Zimaity H.M. Ramchatesingh J. Saeed M.A. et al.Gastric intestinal metaplasia: subtypes and natural history.J Clin Pathol. 2001; 54: 679-683Crossref PubMed Scopus (127) Google Scholar Gastric histologic staging and scoring systems are used primarily in research settings because issues such as pathologist time investment, inter-observer variability in histopathologic grading (eg, differentiating moderate vs severe), and even familiarity limit routine clinical use, particularly in the United States.31Shah S.C. Gowron A.J. Mustafa R. et al.Histologic subtyping of gastric intestinal metaplasia: overview and considerations for clinical practice.Gastroenterology. 2020; 158: 745-750Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar Importantly, the systems require, at minimum, biopsies of both the antrum and corpus a priori. Two systems are prominent in the literature: Operative Link on Gastritis Assessment (OLGA)/Operative Link on Gastric Intestinal Metaplasia Assessment (OLGIM) and the Correa histopathology score. The OLGA and OLGIM are histopathologic staging standards that incorporate both the severity (mild, moderate, or severe) and extent (antrum/incisura or body) of AG and GIM, respectively, and range from stage I to IV.34Rugge M. Genta R.M. OLGA GroupStaging gastritis: an international proposal.Gastroenterology. 2005; 129: 1807-1808Abstract Full Text Full Text PDF PubMed Scopus (136) Google Scholar Stages III and IV, which necessitate both antrum and corpus involvement (with the exception of stage III, severe antral atrophy), are considered higher risk for neoplastic progression.29Capelle L.G. De Vries A.C. 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: 1150-1158Abstract Full Text Full Text PDF PubMed Scopus (346) Google Scholar,35Rugge M. Boni M De Pennelli G. et al.Gastritis OLGA-staging and gastric cancer risk: a twelve-year clinico-pathological follow-up study.Aliment Pharmacol Ther. 2010; 31: 1104-1111PubMed Google Scholar, 36Rugge M. Kim J.G. Mahachai V. et al.OLGA gastritis staging in young adults and country-specific gastric cancer risk.Int J Surg Pathol. 2008; 16: 150-154Crossref PubMed Scopus (30) Google Scholar, 37Yue 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: 579-587Crossref PubMed Scopus (66) Google Scholar These stages are derived from the semi-quantitative scoring of AG or GIM on an updated Sydney System–compliant set of 5 gastric biopsies, including biopsies fr