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Overview of Current Concepts in Gastric Intestinal Metaplasia and Gastric Cancer

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Overview of Current Concepts in Gastric Intestinal Metaplasia and Gastric Cancer Overview of Current Concepts in Gastric Intestinal Metaplasia and Gastric Cancer David S. Jencks, MD, Jason D. Adam, MD, Marie L. Borum, MD, EdD, MPH, Joyce M. Koh, MD, Sindu Stephen, MD, and David B. Doman, MD Dr Jencks and Dr Adam are gastro- Abstract: Gastric intestinal metaplasia is a precancerous change of enterology fellows in the Division of the mucosa of the stomach with intestinal epithelium, and is asso- Gastroenterology and Liver Diseases ciated with an increased risk of dysplasia and cancer. The patho- at George Washington University genesis to gastric cancer is proposed by the Correa hypothesis as Medical Center and are affiliated with Medical Faculty Associates, the transition from normal gastric epithelium to invasive cancer both in Washington, DC. Dr Borum via inflammation followed by intramucosal cancer and invasion. is a professor of medicine at George Multiple risk factors have been associated with the development Washington University School of of gastric intestinal metaplasia interplay, including Helicobacter Medicine in Washington, DC; director pylori infection and associated genomics, host genetic factors, of the Division of Gastroenterology environmental milieu, rheumatologic disorders, diet, and intestinal and Liver Diseases at George Wash- ington University Medical Center; microbiota. Globally, screening guidelines have been established and is affiliated with Medical Faculty in countries with high incidence. In the United States, no such Associates. Dr Koh and Dr Stephen guidelines have been developed due to lower, albeit increasing, are in private practice in Silver Spring, incidence. The American Society for Gastrointestinal Endoscopy Maryland. Dr Doman is a clinical recommends a case-by-case patient assessment based upon epide- professor of medicine at George miology, genetics, and environmental risk factors. Studies have Washington University School of Medicine and is in private practice in examined the use of a serologic biopsy to stratify risk based upon Silver Spring, Maryland. factors such as H pylori status and virulence factors, along with serologic markers of chronic inflammation including pepsinogen I, pepsinogen II, and gastrin. High-risk patients may then be advised Address correspondence to: to undergo endoscopic evaluation with mapping biopsies from the Dr David B. Doman antrum (greater curvature, lesser curvature), incisura angularis, and 12012 Veirs Mill Road Silver Spring, MD 20906 corpus (greater curvature, lesser curvature). Surveillance guidelines Tel: 301-942-3550 have not been firmly established for patients with known gastric E-mail: drdbd1@gmail.com intestinal metaplasia, but include repeat endoscopy at intervals according to the histologic risk for malignant transformation. etaplastic changes in the esophagus and the stomach are both associated with an increased risk of cancer in their respective locations.1 Barrett esophagus, or the replace- Keywords Mment of stratified squamous epithelium by metaplastic columnar Gastric intestinal metaplasia, Helicobacter pylori, gastric cancer surveillance, intestinal-type gastric epithelium, is known to result in a 30-fold increased risk of esopha- 1 cancer, serologic biopsy, spasmolytic polypeptide- geal cancer above that of the general population. Although there is expressing metaplasia debate about the cost-effectiveness of Barrett esophagus screening and 92 Gastroenterology & Hepatology Volume 14, Issue 2 February 2018 GASTRIC INTESTINAL METAPLASIA AND GASTRIC CANCER A B Figure 1. Intestinal metaplasia is characterized by goblet cells similar to those seen in the small and large intestines. The goblet cells have blue-tinged to clear mucin vacuoles, which compress the nucleus to one side of the cell. Goblet cells may be focal (incomplete) or diffuse, and the gastric mucosa may even resemble small intestinal mucosa (complete). Paneth cells similar to those seen in the small and large intestines may also be seen (arrowhead). Figure 1A shows complete intestinal metaplasia, and Figure 1B shows incomplete intestinal metaplasia. Figures provided courtesy of Brian Theisen, MD. surveillance, guidelines are available for the management Pathogenesis of this condition.2 Despite the fact that the estimated Gastric adenocarcinoma is characterized into 2 subtypes: number of new cancer cases in the United States in 2017 intestinal and diffuse. The intestinal type is highly cor- was higher for gastric cancer at 28,000 than esophageal related with intestinal metaplasia, and the diffuse type is cancer at 16,940 (based upon Surveillance, Epidemiology, considered to be primarily genetically determined and less and End Results [SEER] data), no similar management associated with environmental factors and the inflamma- guidelines are available in the United States for gastric tory cascade.8 Intestinal-type adenocarcinoma accounts cancer.3 This article reviews the pathogenesis and risk for the vast majority of gastric cancer.9 factors, along with the current screening and surveillance GIM is a precancerous lesion defined as the replace- strategies, for gastric intestinal metaplasia. ment of surface, foveolar, and/or glandular epithelium in the oxyntic or antral mucosa by intestinal epithelium Background on Gastric Intestinal Metaplasia (Figure 1).10 GIM is categorized anatomically as limited and Gastric Cancer if it is confined to 1 region of the stomach or as extensive if 2 regions of the stomach are involved. Histologically, Epidemiology GIM is considered to be either complete or incomplete.10 Gastric cancer has seen a steady decline since the 1930s, Complete (type I) intestinal metaplasia is defined by which may be partially attributable to the advent of small intestinal-type mucosa with mature absorptive cells, widespread food refrigeration that has replaced smoking goblet cells, and a brush border. Incomplete (type II) meat as a means of preservation. The smoking process intestinal metaplasia secretes sialomucins and is similar to has been determined to promote carcinogens.4 However, colonic epithelium with columnar “intermediate” cells in despite global refrigeration, gastric cancer remains the various stages of differentiation, irregular mucin droplets, fifth most common malignancy and third leading cause and the absence of a brush border.11,12 The highest risk of cancer death worldwide with 723,000 deaths in 2012, of gastric cancer is associated with incomplete and/or according to the World Health Organization (WHO).5 extensive GIM.13 A systematic review that included 10 Although the prevalence of gastric intestinal metaplasia observational studies throughout Europe, Asia, and Latin (GIM) worldwide is largely unknown, a positive correla- America ranging from 10 months to 19 years of follow- tion, although not causation, has been associated with up showed the risk of gastric cancer to be 4- to 11-fold regional gastric cancer incidence.6 A large retrospective higher with incomplete metaplasia compared to without study performed by Sonnenberg and colleagues reviewed incomplete metaplasia.14 78,985 patients who underwent upper endoscopy in the The pathogenesis of the progression from precancer- United States, and found a 7% prevalence of GIM.7 ous lesions to intestinal-type gastric adenocarcinoma has Gastroenterology & Hepatology Volume 14, Issue 2 February 2018 93 JENCKS ET AL been proposed as the progression from normal gastric increase in the risk of gastric cancer.25 It is estimated that epithelium to inflammation, atrophy, intramucosal car- approximately 75% of the global gastric cancer burden is cinoma, and finally invasive carcinoma.15 A multifacto- attributed to H pylori–induced inflammation.26 rial interplay between Helicobacter pylori genomics, host The virulence effects of H pylori have been shown to genetic factors, environmental milieu, diet, and intestinal derive from bacterium factors causing alterations in gas- microbiota predispose the gastric mucosa to an inflamma- tric epithelial cells. Once the bacterial cell signaling pro- tory cascade with cancerous potential.16 tein cagA reaches the host cytosol, it is capable of altering The first histologic change in the cascade is active subsequent generations of progenitor cells, leading to the chronic inflammation with either nonatrophic chronic development of cancer through changes in mitotic activ- gastritis characterized by the presence of glands, or multi- ity, apoptosis, cellular assembly, and signaling.26 Although focal atrophic gastritis. The subsequent histologic changes it should be noted that while the presence of the cagA progress through complete metaplasia, incomplete meta- protein doubles the risk of gastric cancer, cagA-negative plasia, and low- and high-grade dysplasia, followed by strands also increase the risk of distal gastric cancer.27 carcinoma.14 A nationwide cohort study was performed Additional H pylori virulence factors include babA2, in the Netherlands to evaluate the risk of gastric cancer which encodes bacterial adhesion with gastric epithelial associated with the various premalignant gastric lesions. cells, and vacuolating cytotoxin A, which is encoded by Atrophic gastritis, intestinal metaplasia, mild-moderate the gene vacA.28,29 H pylori strains carrying some combi- dysplasia, and severe dysplasia were associated with annual nation of the babA2, cagA, and vacA genes were associated incidences of gastric cancer of 0.1%, 0.25%, 0.6%, and with the highest risk of developing intestinal metaplasia. 6.0%, respectively.17 The incidence of gastric cancer asso-
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