Gastric cancer is the third leading cause of cancer-related deaths worldwide, with more than 1 million incident cases diagnosed globally.1Sung H. 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 Cancer J Clin. 2021; 71: 209-249Crossref PubMed Scopus (26505) Google Scholar Non-cardia intestinal-type gastric cancer, the most common subtype of gastric cancer, develops through the Correa cascade in which chronic inflammation of normal gastric mucosa leads to atrophic gastritis, followed by gastric intestinal metaplasia (GIM), dysplasia, and ultimately gastric cancer.2Correa P. Gastric cancer: overview.Gastroenterol Clin North Am. 2013; 42: 211-217Abstract Full Text Full Text PDF PubMed Scopus (348) Google Scholar GIM has an estimated prevalence of 4.8% in the United States based on an analysis of gastric biopsies from a large pathology database, but higher rates of GIM have been reported in certain racial and ethnic groups (14.8% in Asian Americans, 18.2% in Native Americans, 25.5% in African Americans, and 29.5% in Hispanic Americans).3Nguyen T.H. Tan M.C. Liu Y. et al.Prevalence of gastric intestinal metaplasia in a multiethnic US veterans population.Clin Gastroenterol Hepatol. 2021; 19: 269-276.e3Abstract Full Text Full Text PDF PubMed Scopus (7) Google Scholar,4Altayar O. Davitkov P. Shah S.C. et al.AGA technical review on gastric intestinal metaplasia-epidemiology and risk factors.Gastroenterology. 2020; 158: 732-744.e16Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar Additional risk factors for GIM include tobacco use, autoimmune gastritis, and living or immigrating from an endemic area. The annual risk of progression from GIM to non-cardia intestinal-type gastric cancer is 0.16%, and factors such as persistent Helicobacter pylori infection, family history, anatomic extent and location of GIM, and histologic subtypes may confer increased risk of progression to gastric cancer.5Gupta S. Li D. El Serag H.B. et al.AGA Clinical practice guidelines on management of gastric intestinal metaplasia.Gastroenterology. 2020; 158: 693-702Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar Studies of U.S. endoscopists show variation in the management of patients with GIM, including use and interval for endoscopic surveillance, prompting the development of guidelines for the management of GIM.6Vance 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,7Huang R.J. Ende A.R. Singla A. et al.Prevalence, risk factors, and surveillance patterns for gastric intestinal metaplasia among patients undergoing upper endoscopy with biopsy.Gastrointest Endosc. 2020; 91: 70-77.e1Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar Helicobacter pylori infection is one of the most common causes of atrophic gastritis and GIM and is a major driver of progression along the Correa cascade. The overall prevalence of H pylori in the U.S. is 35.6% but has been reported to be much higher in specific racial and ethnic groups: 74.8%, 61.6%, and 52.7% in Alaskan Native Americans, Hispanic Americans, and non-Hispanic African Americans, respectively, and disproportionately affecting vulnerable populations frequently affected by health care disparities.8Hooi J.K.Y. Lai W.Y. Ng W.K. et al.Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis.Gastroenterology. 2017; 153: 420-429Abstract Full Text Full Text PDF PubMed Scopus (1383) Google Scholar,9Everhart J.E. Kruszon-Moran D. Perez-Perez G.I. et al.Seroprevalence and ethnic differences in Helicobacter pylori infection among adults in the United States.J Infect Dis. 2000; 181: 1359-1363Crossref PubMed Scopus (271) Google Scholar Helicobacter pylori is readily treatable with a short course of antibiotics, and treatment is cost-effective in the prevention of gastric cancer.10Lansdorp-Vogelaar I. Meester R.G.S. Laszkowska M. et al.Cost-effectiveness of prevention and early detection of gastric cancer in Western countries.Best Pract Res Clin Gastroenterol. 2021; 50–51: 101735Crossref PubMed Scopus (13) Google Scholar However, rates of failed H pylori eradication are rising, so repeated testing to confirm eradication is recommended.11El-Serag H.B. Kao J.Y. Kanwal F. et al.Houston Consensus Conference on Testing for Helicobacter pylori Infection in the United States.Clin Gastroenterol Hepatol. 2018; 16: 992-1002.e6Abstract Full Text Full Text PDF PubMed Scopus (125) Google Scholar Despite the high prevalence of H pylori infection and release of evidence-based guidelines, quality gaps in testing and treatment exist in the management of H pylori.12Shah 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,13El-Zimaity H. Serra S. Szentgyorgyi E. et al.Gastric biopsies: the gap between evidence-based medicine and daily practice in the management of gastric Helicobacter pylori infection.Can J Gastroenterol. 2013; 27: e25-e30Crossref PubMed Scopus (26) Google Scholar The American Gastroenterological Association (AGA) recently published a clinical practice guideline on the management of GIM, highlighting best practices for treatment and eradication of coexistent H pylori.5Gupta S. Li D. El Serag H.B. et al.AGA Clinical practice guidelines on management of gastric intestinal metaplasia.Gastroenterology. 2020; 158: 693-702Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar Owing to the high incidence of gastric cancer, widespread prevalence of GIM and concomitant H pylori infection, and variation in practice patterns, development of quality measures for the management of GIM will provide meaningful aspirational care targets, promote adherence to evidence-based effective care, and allow benchmarking for quality practice to improve the care of patients with GIM. This document presents the official recommendations of the AGA regarding quality measures related to the diagnosis and management of GIM. The current report outlines the process by which the Quality Committee (QC) evaluates guidance statements published by the AGA’s Clinical Guidelines Committee (CGC) to inform measure development. The following recommendations were developed by the QC in consultation with the CGC. Their development was funded by the AGA Institute, with no additional outside funding. The recommendation statements from the AGA’s GIM guideline were evaluated for development as potential quality measures. A standardized process first implemented by the AGA in 2016 and outlined elsewhere14Adams M.A. Allen J.I. Saini S.D. Translating best practices to meaningful quality measures: from measure conceptualization to implementation.Clin Gastroenterol Hepatol. 2019; 17: 805-808Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar was used for this evaluation and concordant with previously used methods for measure development.15Mosko J.D. Leiman D.A. Ketwaroo G.A. et al.Development of quality measures for acute pancreatitis: a model for hospital-based measures in gastroenterology.Clin Gastroenterol Hepatol. 2020; 18: 272-275.e5Abstract Full Text Full Text PDF PubMed Scopus (8) Google Scholar Optimal understanding of this measure evaluation process can be enhanced by reading applicable portions of the topic guidelines. Briefly, the AGA QC follows a “guidelines to measures” protocol that has been used for the creation of other measures. This process relies on the evaluation of forthcoming guideline recommendations to be reviewed by the QC. Recommendation statements are evaluated as potential measure concepts along several axes, including the strength of the recommendation and quality of the evidence as specified with the use of GRADE (Grading of Recommendations Assessment, Development, and Evaluation) methodology. Only those statements with strong recommendations based on high or moderate quality evidence are considered for further measure development, which includes an assessment of their potential utility for practicing gastroenterologists. This assessment involves QC subcommittee analysis of measure importance and, when appropriate, is followed by the formal creation of a measure prioritization brief outlining the decision rationale whereby topics are rated on their meaningfulness, potential magnitude of effect, quality gaps, feasibility, and applicability to gastroenterologists. High-priority measure concepts subsequently undergo review and voting by all QC members ahead of a 30-day public comment period before testing and formal adoption. Finally, measures that receive 60% or more of the full QC vote are recommended for national implementation. The AGA Clinical Practice Guidelines on Management of GIM were reviewed and each recommendation statement independently evaluated by the AGA QC for the potential to develop into quality measures.5Gupta S. Li D. El Serag H.B. et al.AGA Clinical practice guidelines on management of gastric intestinal metaplasia.Gastroenterology. 2020; 158: 693-702Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar The assessment from that evaluation is outlined in Table 1.Table 1Summary of Recommendations and Rationale for Quality Measure Development in the Guideline on the Management of Gastric Intestinal Metaplasia (GIM)StatementGRADEDecisionRationaleIn patients with GIM, the AGA recommends testing for H pylori followed by eradication over no testing and eradication.Strong recommendation, moderate quality of evidenceProceed with measure concept developmentQuality gap in confirmation of H pylori eradicationIn patients with GIM, the AGA suggests against routine use of endoscopic surveillance.Conditional recommendation, very low quality of evidenceNo measure concept to developInsufficient strength of recommendation and certainty of evidenceIn patients with GIM, the AGA suggests against routine short-interval repeated endoscopy for the purpose of risk stratification.Conditional recommendation, very low quality of evidenceNo measure concept to developInsufficient strength of recommendation and certainty of evidenceAGA, American Gastroenterological Association. Open table in a new tab AGA, American Gastroenterological Association. Recommendations with low or very low quality of evidence were not considered for quality measure development because of the limited certainty of evidence; thus, new high-quality studies may change the clinical practice recommendations. Conditional recommendations also were not considered for measure development. As a result, the suggestions against the routine use of endoscopic surveillance or routine short-interval repeated endoscopy for the purpose of risk stratification in patients with GIM were not developed. Indeed, there are no prospective studies to support nor argue against the routine performance of endoscopic surveillance in patients with GIM in preventing gastric cancer, mortality, or other patient-related outcomes. There are patient-specific factors, such as family history of gastric cancer, race/ethnicity, smoking, autoimmune gastritis/pernicious anemia, anatomic extent of GIM, and histologic subtype of GIM within the stomach that may affect the risk of developing gastric cancer.4Altayar O. Davitkov P. Shah S.C. et al.AGA technical review on gastric intestinal metaplasia-epidemiology and risk factors.Gastroenterology. 2020; 158: 732-744.e16Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar Balancing this significantly increased risk of GIM progression in some groups (up to 4.5-fold higher) with the uncertain evidence in U.S. populations, AGA guidelines recommended against the routine surveillance of GIM (conditional recommendation, very low quality of evidence) but commented that there are populations at high risk for whom a shared discussion regarding the potential benefit of endoscopic surveillance at regular intervals should be considered.5Gupta S. Li D. El Serag H.B. et al.AGA Clinical practice guidelines on management of gastric intestinal metaplasia.Gastroenterology. 2020; 158: 693-702Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar However, because of the conditional recommendation provided against GIM surveillance among all patients diagnosed with GIM, regardless of additional risk factors, the AGA QC cannot generate a quality measure on routine endoscopic GIM surveillance. The data are also insufficient to indicate that routine short-interval repeated endoscopy for risk stratification in patients with GIM affects gastric cancer detection or treatment. In contrast, recommendations with moderate or strong quality of evidence were reviewed for suitability of quality measure development. In this case, the recommendation for patients with GIM to have testing for H pylori followed by eradication, over no testing and eradication, was assessed and developed as a fully specified measure. Helicobacter pylori, a class I carcinogen per the World Health Organization, is a major risk factor for GIM and non-cardia gastric cancer. Helicobacter pylori infection can be detected by stool antigen, breath testing, gastric biopsies, or serology. GIM may lower the sensitivity of H pylori detection in gastric biopsies, so repeated H pylori testing with either stool or breath testing—off proton pump inhibitor therapy for at least 2 weeks—is recommended. Helicobacter pylori eradication in individuals with or without GIM has been associated with a 32% pooled relative risk reduction for developing gastric cancer.16Gawron A.J. Shah S.C. Altayar O. et al.AGA technical review on gastric intestinal metaplasia—natural history and clinical outcomes.Gastroenterology. 2020; 158: 705-731.e5Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar However, H pylori antibiotic resistance is increasing, and post-treatment confirmation of eradication is recommended owing to rising rates of H pylori eradication failure.17Savoldi A. Carrara E. Graham D.Y. et al.Prevalence of antibiotic resistance in Helicobacter pylori: a systematic review and meta-analysis in World Health Organization regions.Gastroenterology. 2018; 155: 1372-1382.e17Abstract Full Text Full Text PDF PubMed Scopus (503) Google Scholar,18Chey W.D. Leontiadis G.I. Howden C.W. et al.ACG Clinical guideline: treatment of Helicobacter pylori infection.Am J Gastroenterol. 2017; 112: 212-239Crossref PubMed Scopus (768) Google Scholar Serology cannot reliably distinguish between active or previous infection, therefore methods other than serology are recommended to confirm H pylori eradication. Ensuring adequate assessment and eradication of H pylori in patients with GIM is of critical importance and addresses a significant quality gap because 1) gastric cancer incidence and mortality are high, 2) a strong association exists between H pylori, GIM, and gastric cancer, 3) H pylori eradication is associated with decreased gastric cancer incidence and mortality, 4) H pylori eradication failure rates are rising, resulting in the need for multiple courses of antibiotics that may further worsen antibiotic resistance, and 5) H pylori antibiotic resistance testing is difficult to obtain. We therefore proposed the development of a quality measure to ensure H pylori testing and confirmation of eradication in patients with GIM. The recent publication of International Classification of Diseases, 10th Revision, codes specific for GIM in October 2021 allowed the QC to proceed with development of a GIM quality measure (Figure 1). Following its development, the measure specification was posted for public comment in November 2021. Comments and suggestions that were received included the addition of Current Procedural Terminology (CPT) code descriptions into the measure specifications and revision of the measure specifications to emphasize testing for H pylori 4 weeks after completion of therapy. In response to these comments, we updated CPT codes with descriptions and emphasized the timing of repeated H pylori testing 4 weeks after completion of treatment. Comments in support of this measure were also received from the College of American Pathologists. The finalized measure reflects these comments. The AGA CGC systematically reviewed data and issued recommendations for the management of GIM based on the quality of available evidence. The AGA QC develops quality measures based on CGC guidelines with moderate or high quality of evidence and strong recommendations. Quality measure development entails a rigorous process of measure specification, testing, and submission to quality programs such as the Merit-Based Incentive Payment System. Data on long-term outcomes of GIM and endoscopy for risk stratification or surveillance in a U.S. population are lacking. Factors such as family history, histologic features, and anatomic extent of GIM all affect risk of progression of GIM to gastric cancer. International guidelines recommend endoscopic surveillance of GIM at varying intervals depending on anatomic extent of GIM and presence or absence of additional risk factors for gastric cancer.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,20Banks 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 (225) Google Scholar However, in the absence of high-quality data regarding the role of endoscopic surveillance of GIM and optimal surveillance intervals regarding patient-related outcomes, current evidence is not strong enough to support the development of quality measures for endoscopic surveillance of GIM. Until more evidence is available regarding endoscopic surveillance for GIM, ensuring eradication of H pylori is an attainable goal that would improve patient outcomes. Given the disparate impacts of gastric cancer, GIM, and H pylori on certain portions of the U.S. population, there may be a role for future measure development or measure stratification for populations at high risk when additional data are available. In the meantime, studies have shown nonadherence to H pylori testing guidelines and knowledge gaps in the management of patients at increased risk for gastric cancer.12Shah 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,13El-Zimaity H. Serra S. Szentgyorgyi E. et al.Gastric biopsies: the gap between evidence-based medicine and daily practice in the management of gastric Helicobacter pylori infection.Can J Gastroenterol. 2013; 27: e25-e30Crossref PubMed Scopus (26) Google Scholar Beyond GIM, H pylori assessment and eradication have been shown to improve outcomes in peptic ulcer disease–associated gastrointestinal bleeding and dyspepsia.21Hung K.W. Knotts R.M. Faye A.S. et al.Factors associated with adherence to Helicobacter pylori testing during hospitalization for bleeding peptic ulcer disease.Clin Gastroenterol Hepatol. 2020; 18: 1091-1098.e1Abstract Full Text Full Text PDF PubMed Scopus (14) Google Scholar, 22Guo C.G. Cheung K.S. Zhang F. et al.Delay in retreatment of Helicobacter pylori infection increases risk of upper gastrointestinal bleeding.Clin Gastroenterol Hepatol. 2021; 19: 314-322.e2Abstract Full Text Full Text PDF PubMed Scopus (14) Google Scholar, 23Chiba N. van Zanten S.J. Sinclair P. et al.Treating Helicobacter pylori infection in primary care patients with uninvestigated dyspepsia: the Canadian Adult Dyspepsia Empiric Treatment—Helicobacter pylori positive (CADET-Hp) randomised controlled trial.BMJ. 2002; 324: 1012-1016Crossref PubMed Scopus (201) Google Scholar Wide variations of care exist, so efforts to confirm eradication are important opportunities for improvement in the care of patients with GIM. Future quality improvement opportunities will include creating mechanisms to identify patients with H pylori and GIM, with a focus on tracking and increasing rates of H pylori eradication confirmation within a confined episode of care to reduce the risk of gastric cancer. Importantly, there are no other quality measures related to the management of H pylori. The current measure therefore represents an opportunity to improve the quality of care for patients with the most common bacterial infection worldwide, affecting more than half of the world’s population and disproportionately affecting vulnerable populations frequently affected by health care disparities.8Hooi J.K.Y. Lai W.Y. Ng W.K. et al.Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis.Gastroenterology. 2017; 153: 420-429Abstract Full Text Full Text PDF PubMed Scopus (1383) Google Scholar Because of the strong relationship between H pylori and atrophic gastritis, dyspepsia, and peptic ulcer disease, development of quality measures to promote H pylori testing, treatment, and confirmation of eradication in these conditions is a potential next step. The development of a broader quality measure for H pylori treatment and confirmation of eradication in all individuals who test positive for H pylori is another potential future direction in improving care of patients with H pylori in general. This will require thorough review and grading of the quality of available evidence regarding H pylori testing and treatment and patient-related outcomes, including benefits and harms, to determine the appropriateness and magnitude of the effect of a broader H pylori measure. Management of H pylori infection is beyond the scope of this document and has been discussed in numerous guidelines, consensus documents, and clinical practice updates.18Chey W.D. Leontiadis G.I. Howden C.W. et al.ACG Clinical guideline: treatment of Helicobacter pylori infection.Am J Gastroenterol. 2017; 112: 212-239Crossref PubMed Scopus (768) Google Scholar,24Shah S.C. Iyer P.G. Moss S.F. AGA Clinical practice update on the management of refractory Helicobacter pylori infection: expert review.Gastroenterology. 2021; 160: 1831-1841Abstract Full Text Full Text PDF PubMed Scopus (56) Google Scholar,25Fallone C.A. Chiba N. van Zanten S.V. et al.The Toronto Consensus for the Treatment of Helicobacter pylori Infection in Adults.Gastroenterology. 2016; 151: 51-69.e14Abstract Full Text Full Text PDF PubMed Scopus (508) Google Scholar Successful eradication on the initial treatment attempt is imperative owing to declining eradication rates with subsequent treatment regimens. A renewed focus on the treatment and eradication of H pylori has the potential to greatly improve global health, and emphasizing the need to confirm eradication will result in a greater understanding of current resistance patterns. This may have the potential to create a virtuous cycle whereby other best practices can be recognized, including tailoring treatment to local antimicrobial resistance and improving antibiotic stewardship.11El-Serag H.B. Kao J.Y. Kanwal F. et al.Houston Consensus Conference on Testing for Helicobacter pylori Infection in the United States.Clin Gastroenterol Hepatol. 2018; 16: 992-1002.e6Abstract Full Text Full Text PDF PubMed Scopus (125) Google Scholar,25Fallone C.A. Chiba N. van Zanten S.V. et al.The Toronto Consensus for the Treatment of Helicobacter pylori Infection in Adults.Gastroenterology. 2016; 151: 51-69.e14Abstract Full Text Full Text PDF PubMed Scopus (508) Google Scholar In conclusion, the AGA QC has created a novel quality measure for H pylori testing and eradication in patients with GIM. Future inclusion of this measure in a Quality Payment Program or endorsement by organizations such as the National Quality Forum will depend on real-world usage, testing, and refinement. In the meantime, the measure may be used for ongoing quality improvement interventions, and continued measurement will be essential to addressing the quality gap and improving the care of patients who are at risk for gastric cancer. We particularly acknowledge the work of David Godzina and members of the American Gastroenterological Association Quality Committee, who participated in generating and evaluating this measure.