Gastritis and gastric atrophy Hala El-Zimaity a,b
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1 Gastritis and gastric Hala El-Zimaity a,b a Department of Pathology, McMaster University, Hamilton, Ontario, Canada and b Department of Medicine, Michael E. DeBakey Veterans Affairs Medical Center, Baylor College of Medicine, Houston, Texas, USA Correspondence to Hala El-Zimaity, MD, Hamilton Health Sciences, McMaster Division, 1200 Main Street West, Anatomical Pathology, RM 2N31, Hamilton, ON L8S 3Z5, Canada Tel: x76637; fax: ; zimaity@mcmaster.ca Current Opinion in Gastroenterology 2008, 24: Purpose of review The majority of problems in interpreting gastritis remain Helicobacter related, but their nature has changed. The present review covers gastritis historically through cancer risk staging systems. Recent findings Key points to remember are: Helicobacter is associated with several forms of gastritis; in the present review, I am focusing on the two ends of the disease, Helicobacter pylori infection, that starts with antral predominant gastritis but can continue to oxyntic predominant disease with ; the role Helicobacter pylori plays in autoimmune gastritis with pernicious anemia remains unresolved; gastritis staging systems for cancer risk, namely Baylor and Operative Link on Gastritis Assessment, are currently available. Summary As most gastric carcinomas arise on a background of atrophic gastritis, and the risk increases with the extent of, an index of location and extent could be useful in predicting patients at greatest risk for carcinoma. It is now possible to stage patients for cancer risk. Nonetheless, in a field such as gastritis in which many issues remain unresolved, a classification or staging system that is more descriptive will likely prove more useful. Keywords, gastritis, staging Curr Opin Gastroenterol 24: ß 2008 Wolters Kluwer Health Lippincott Williams & Wilkins Introduction As the development of gastric carcinoma is an unpredictable process, recognizing the presence and extent of gastritis with associated can help identify patients with different gastric cancer risk. The present review is an overview of our approach to gastritis, including the most recently described histology-based gastritis staging systems, the Baylor System [1] and Operative Link on Gastritis Assessment (OLGA) System [2,3 ]. Our past understanding of gastritis patterns Before the rediscovery of Helicobacter pylori, it was known that different patterns of gastritis were associated with different diseases [4,5]: (1) antral predominant gastritis with little or no gastric in duodenal ulcer disease with normal or increased acid secretion [6 9], (2) extensive gastritis with corpus (and invariably antral) in gastric ulcer disease, which tends to progress through intestinal metaplasia to intestinal type gastric cancer with hypochlorhydria or achlorhydria [6,10 13], and (3) corpus predominant gastritis in autoimmune gastritis. It was suggested that in the intestinal form of gastric carcinoma begins at the antrum corpus junction, specifically at the incisura angularis, with subsequent spread of foci up and down the lesser curvature and the anterior and posterior wall. Although Western countries concept of gastric was heavily influenced by Correa s proposal [14] of multifocal independent foci of (at the time equated with intestinal metaplasia) throughout the stomach [14,15], Eastern countries recognized the presence of an advancing atrophic border endoscopically in 1969 [16], a change they attributed to aging. Fueled by a need to group patients by cancer risk, Filipe et al. [17] suggested subtyping intestinal metaplasia using high iron diamine; intestinal metaplasia subtyped III (incomplete) was considered to be the most precancerous. Other forms of gastric such as pseudopyloric metaplasia have been observed particularly in gastric remnants following distal gastrectomy with gastroenteric anastomosis [18], but many considered it a sequel of autoimmune gastritis ß 2008 Wolters Kluwer Health Lippincott Williams & Wilkins DOI: /MOG.0b013e328311d1cc
2 Gastritis and gastric El-Zimaity 683 [14,19,20]. In practice, it likely is a sequel of longstanding chronic inflammation of any cause. Our present understanding of gastritis patterns It is now recognized that a person s acid secretory status affects both the distribution and severity of H. pylorirelated gastritis and, therefore, indirectly determines whether they develop duodenal or gastric ulcer disease and, thus, their risk for gastric cancer [21 23]. In the early stages in which H. pylori-associated gastritis is antral predominant, the acid secretion of the oxyntic mucosa shows an exaggerated gastrin response to H. pylori, an increase enough to cause duodenal ulcer disease in some patients [7]. With continued inflammation, the development of hypochlorhydria and achlorhydria facilitates the proximal migration of the bacteria that allows the development of corpus gastritis and, eventually, corpus [24 26]. The natural history of H. pylori-related gastritis is for the inflammation to progress from the antrum into the adjacent corpus resulting in an advancing atrophic front of corpus injury (metaplastic and nonmetaplastic [14,27]), which incrementally destroys parietal cells causing further reduction in acid secretion and, thus, further proximal advancement of inflammation with associated injury with the eventual development of extensive corpus [21,27,28]. This situation is accelerated in clinical scenarios associated with low acid secretion such as chronic therapy with proton pump inhibitors, which is widely used in gastroesophageal reflux disease [29 31]. Thus, antral predominant gastritis may, in some instances, represent an earlier stage of atrophic pangastritis such that these patterns actually represent two ends of the spectrum of H. pylori infection rather than mutually exclusive diseases [21,32,33]. Interestingly, several investigators implicated H. pylori in modulating the host s immune response through molecular mimicry or cross-reactivity between H. pylori and the human stomach [14,34 37]. Recognizing that chronic autoimmune gastritis is significantly more common in H. pylori-infected patients with anti H þ K þ -ATPase antibodies [37 39] challenged our previous perception of autoimmune gastritis and H. pylori-related gastritis as two separate diseases. As studies on autoimmune gastritis preceded the rediscovery of H. pylori, many believed that simultaneous infection with H. pylori masked the pathology seen in autoimmune gastritis. For example, extensive pseudopyloric metaplasia with focal intestinal metaplasia, previously thought to be more common in later stages of autoimmune gastritis [14,19,20], is increasingly recognized in H. pylori-associated gastritis [27,40 42]. Some suggested that pernicious anemia (autoimmune gastritis) could be a long-term consequence of H. pylori infection [43]. Yet, contrary to classical autoimmune gastritis, patients with H. pylori-associated chronic gastritis exhibit a gradual decrease in acid secretion but seldom develop enterochromaffin-like cell (ECL) hyperplasia or megaloblastic anemia [44]. In addition, countries with a high incidence of gastric carcinoma do not have a high incidence of pernicious anemia. H. pylori may be responsible for initiating the process; nonetheless, only patients with a genetic predisposition will develop early destruction of corpus glandular components precipitating relatively rapid and profound achlorhydria and secondary hypergastrinaemia with the eventual development of ECL hyperplasia and gastric carcinoids. Classifications systems of gastritis As the progression from chronic gastritis to severe gastric mucosal is not inevitable and disease progression varies considerably from person to person [28], the recognition of a person s gastritis pattern is paramount. Several classifications systems have been introduced with the goal of understanding the status of the gastric mucosa [14,45,46]; the present classification of chronic gastritis the updated Sydney System takes into account the topography and morphology of gastric mucosal changes in addition to the microbiological aspects of the disease [14] (Table 1). Corpus, the precursor for intestinal-type gastric carcinoma, is currently defined as the loss of normal glands with and without its replacement with fibrosis, intestinal metaplasia or pseudopyloric metaplasia, also called pyloric metaplasia or mucus metaplasia and ulcerassociated cell lineage (Nick Wright, personal communication), or all [14,27,42]. Although incomplete intestinal metaplasia has been linked to gastric carcinoma, subtyp- Table 1 Gastritis classification systems (time period, ) Year Classification system Comments 1972 Whitehead Mucosa type Type and stage of activity Presence and type of metaplasia 1973 Strickland-Mackay A (autoimmune) and B (nonautoimmune) 1975 Glass and Pitchumoni modification of Strickland-Mackay A (autoimmune), B (antrum), and AB 1990 Sydney Nonatrophic Atrophic Autoimmune Multifocal Special forms 1996 Updated Sydney Same as above, biopsy location changed from anterior and posterior wall to greater and lesser curve
3 684 Stomach and duodenum Table 2 The current gastritis staging systems for gastric (Baylor [1] and Operative Link on Gastritis Assessment [3 ]) have different biopsy site(s) protocols and different staging system criteria Biopsy System OLGA Baylor Those recommended by updated Sydney System (Fig. 1) Additional biopsy sites were taken (Fig. 1) OLGA, Operative Link on Gastritis Assessment. Gastritis stage is obtained by combining antral with oxyntic scores (Fig. 2) An average reading is given for antrum. Corpus stage is independent of antral and independent of individual reading in each biopsy but dependent on location. Assuming that the atrophic border is circumferential, and the more proximal the extends, the greater the amount of present, at a distal location is graded mild and at a proximal location is graded severe ing intestinal metaplasia failed as a marker of disease severity, as areas of intestinal metaplasia (or a certain subtype) are generally small and can easily be missed in biopsy [27,47]; subtyping intestinal metaplasia is confined to research setting [14]. Nonetheless, recognizing the presence of does not equate with cancer, although, at least with the intestinal variant of carcinoma, the risk increases with the degree of and metaplasia. Aware of these impediments, two gastritis staging systems for (Baylor [1] and OLGA [3 ]) with different biopsy site(s) protocols and different staging system criteria have been introduced (Table 2, Figs 1 and 2). The two systems have had variable success. Whereas the Baylor gastritis staging system matched noninvasive testing of gastric with serum concentrations of pepsinogens and gastrin-17 levels used as indirect measure of gastric mucosal functional integrity [1], the OLGA system was successful in subgrouping patients by cancer risk [3 ]. On comparing both systems, the Baylor system was, not surprisingly, more sensitive in identifying, particular in early cases (unpublished data). Summary Our understanding of gastritis has seen many strides. In the early 1970s, gastritis was classified into autoimmune (type A) and nonautoimmune (type B: antral predominant). At that time, duodenal ulcer, gastric ulcer, and gastric cancer represented three primary diseases that affected the stomach. Today, H. pylori takes center stage, and we suspect that duodenal ulcer and gastric cancer are two ends of one disease, namely, H. pylori infection [21 23]. The prevalence of H. pylori is decreasing as a result of children not becoming infected in addition to treatment Figure 1 Recommended biopsy site(s) for the Sydney System include two from the antrum (A 1 and A 2 ), one from the incisura (1A) and two from the corpus (B 1 and B 2 ) The Baylor System uses the same biopsy sites as the Sydney System with additional distal biopsies from the corpus and antrum (Baylor).
4 Gastritis and gastric El-Zimaity 685 Figure 2 The Operative Link on Gastritis Assessment System Corpus Antrum Atrophy score No (score 0) Mild (score 1) Moderate (score 2) Severe (score 3) No (score 0) Mild (score 1) Stage 0 Stage I Stage II Stage II Stage I Stage I Stage II Stage III Moderate (score 2) Stage II Stage II Stage III Stage IV Severe (score 3) Stage III Stage III Stage IV Stage IV of H. pylori in both duodenal ulcer patients and asymptomatic patients [48,49]; gastric cancer secondary to H. pylori gastritis may not be tomorrow s challenge particularly in Western countries. As most gastric carcinomas arise on a background of atrophic gastritis, and the risk increases with the extent of, an index of location and extent could be useful in predicting patients at greatest risk for carcinoma. The OLGA system, although useful for categorizing patients by cancer risk [50], lacks an index of location in addition to requiring a degree of memorization (or constant referral to the chart) for criteria used for each stage. Further, it is not intuitive, as severe in the antrum and severe in the corpus both receive the same score. In the changing field of gastritis, a classification that is more descriptive will likely prove more useful. This extends to other gastritides such as those accompanying inflammatory bowel disease or autoimmune gastritis or both, in which disease presentation and progression are not yet well defined. References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as: of special interest of outstanding interest Additional references related to this topic can also be found in the Current World Literature section in this issue (p. 751). 1 Graham DY, Nurgalieva ZZ, El-Zimaity HM, et al. Noninvasive versus histologic detection of gastric in a Hispanic population in North America. Clin Gastroenterol Hepatol 2006; 4: Rugge M, Meggio A, Pennelli G, et al. Gastritis staging in clinical practice: the OLGA staging system. Gut 2007; 56: Rugge M, Kim JG, Mahachai V, et al. OLGA gastritis staging in young adults and country-specific gastric cancer risk. Int J Surg Pathol 2008; 16: In this study, gastritis score matched gastric cancer risk in different populations. 4 Stemmermann GN, Hayashi T. Intestinal metaplasia of the gastric mucosa: a gross and microscopic study of its distribution in various disease states. J Natl Cancer Inst 1968; 41: Lambert R. Chronic gastritis. A critical study of the progressive of the gastric mucosa. Digestion 1972; 7: Faber K. Chronic gastritis: its relation to achlorhydria and ulcer. Lancet 1927; 2: Graham DY, Opekun A, Lew GM, et al. Helicobacter pylori-associated exaggerated gastrin release in duodenal ulcer patients. The effect of bombesin infusion and urea ingestion. Gastroenterology 1991; 100: Dixon MF. Helicobacter pylori and peptic ulceration: histopathological aspects. J Gastroenterol Hepatol 1991; 6: Graham DY. Campylobacter pylori and peptic ulcer disease. Gastroenterology 1989; 96 (Pt 2 Suppl 2): Burstein M, Monge E, Leon-Barua R, et al. Low peptic ulcer and high gastric cancer prevalence in a developing country with a high prevalence of infection by Helicobacter pylori. J Clin Gastroenterol 1991; 13: Meining A, Stolte M, Hatz R, et al. Differing degree and distribution of gastritis in Helicobacter pylori-associated diseases. Virchows Arch 1997; 431: Malaty HM, Kim JG, El-Zimaity HM, et al. High prevalence of duodenal ulcer and gastric cancer in dyspeptic patients in Korea. Scand J Gastroenterol 1997; 32: El-Zimaity HMT. Recent advances in histopathology of gastritis. Curr Diagn Pathol 2007; 13: Dixon MF, Genta RM, Yardley JH, et al. Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston Am J Surg Pathol 1996; 20: Correa P, Cuello C, Duque E. Carcinoma and intestinal metaplasia of the stomach in Colombian migrants. J Natl Cancer Inst 1970; 44: Kimura K, Takemoto T. An endoscopic recognition of the atrophic border and its significance in chronic gastritis. Endoscopy 1969; 1: Filipe MI, Munoz N, Matko I, et al. Intestinal metaplasia types and the risk of gastric cancer: a cohort study in Slovenia. Int J Cancer 1994; 57: Savage A, Jones S. Histological appearances of the gastric mucosa years after partial gastrectomy. J Clin Pathol 1979; 32: Lewin KJ, Dowling F, Wright JP, et al. Gastric morphology and serum gastrin levels in pernicious anaemia. Gut 1976; 17: Rubio CA. My approach to reporting a gastric biopsy. J Clin Pathol 2007; 60: El-Zimaity HMT, Gutierrez O, Kim JG, et al. Geographic differences in the distribution of intestinal metaplasia in duodenal ulcer patients. Am J Gastroenterol 2001; 96:
5 686 Stomach and duodenum 22 Recavarren-Arce S, Leon-Barua R, Cok J, et al. Helicobacter pylori and progressive gastric pathology that predisposes to gastric cancer. Scand J Gastroenterol Suppl 1991; 181: Sipponen P. Gastric cancer: a long-term consequence of Helicobacter pylori infection? Scand J Gastroenterol Suppl 1994; 201: Sipponen P. Atrophic gastritis as a premalignant condition. Ann Med 1989; 21: Vaananen H, Vauhkonen M, Helske T, et al. Nonendoscopic diagnosis of atrophic gastritis with a blood test. Correlation between gastric histology and serum levels of gastrin-17 and pepsinogen I: a multicentre study. Eur J Gastroenterol Hepatol 2003; 15: Sipponen P, Ranta P, Helske T, et al. Serum levels of amidated gastrin-17 and pepsinogen I in atrophic gastritis: an observational case-control study. Scand J Gastroenterol 2002; 37: El-Zimaity HM, Ota H, Graham DY, et al. Patterns of gastric in intestinal type gastric carcinoma. Cancer 2002; 94: Siurala M, Sipponen P, Kekki M. Chronic gastritis: dynamic and clinical aspects. Scand J Gastroenterol Suppl 1985; 109: Lamberts R, Creutzfeldt W, Struber HG, et al. Long-term omeprazole therapy in peptic ulcer disease: gastrin, endocrine cell growth, and gastritis. Gastroenterology 1993; 104: Kuipers EJ, Uyterlinde AM, Pena AS, et al. Increase of Helicobacter pyloriassociated corpus gastritis during acid suppressive therapy: implications for long-term safety. Am J Gastroenterol 1995; 90: Moayyedi P, Wason C, Peacock R, et al. Changing patterns of Helicobacter pylori gastritis in long-standing acid suppression. Helicobacter 2000; 5: Kim HY, Kim YB, Park CK, et al. Co-existing gastric cancer and duodenal ulcer disease: role of Helicobacter pylori infection. Helicobacter 1997; 2: Kirk RM, Jeffery PJ. Development of surgery for peptic ulcer: a review. J R Soc Med 1981; 74: Faller G, Steininger H, Kranzlein J, et al. Antigastric autoantibodies in Helicobacter pylori infection: implications of histological and clinical parameters of gastritis. Gut 1997; 41: Negrini R, Savio A, Poiesi C, et al. Antigenic mimicry between Helicobacter pylori and gastric mucosa in the pathogenesis of body atrophic gastritis. Gastroenterology 1996; 111: Alkout AM, Blackwell CC, Weir DM, et al. Isolation of a cell surface component of Helicobacter pylori that binds H type 2, Lewis(a), and Lewis(b) antigens. Gastroenterology 1997; 112: Wirth HP, Yang M, Peek RM Jr, et al. Helicobacter pylori Lewis expression is related to the host Lewis phenotype. Gastroenterology 1997; 113: Ma JY, Borch K, Mardh S. Human gastric H,K-adenosine triphosphatase betasubunit is a major autoantigen in atrophic corpus gastritis. Expression of the recombinant human glycoprotein in insect cells. Scand J Gastroenterol 1994; 29: Claeys D, Faller G, Appelmelk BJ, et al. The gastric Hþ,Kþ-ATPase is a major autoantigen in chronic Helicobacter pylori gastritis with body mucosa. Gastroenterology 1998; 115: Sakai H, Eishi Y, Li XL, et al. PDX1 homeobox protein expression in pseudopyloric glands and gastric carcinomas. Gut 2004; 53: Tatematsu M, Ichinose M, Miki K, et al. Gastric and intestinal phenotypic expression of human stomach cancers as revealed by pepsinogen immunohistochemistry and mucin histochemistry. Acta Pathol Jpn 1990; 40: Ricuarte O, Gutierrez O, Cardona H, et al. Atrophic gastritis in young children and adolescents. J Clin Pathol 2005; 58: DeLuca VA Jr. Helicobacter pylori gastric and pernicious anemia. Gastroenterology 1992; 102: Chlumska A, Boudova L, Benes Z, et al. Autoimmune gastritis. A clinicopathologic study of 25 cases. Cesk Patol 2005; 41: Whitehead R, Truelove SC, Gear MW. The histological diagnosis of chronic gastritis in fibreoptic gastroscope biopsy specimens. J Clin Pathol 1972; 25: Price AB. The Sydney System: histological division. J Gastroenterol Hepatol 1991; 6: El-Zimaity HM, Ramchatesingh J, Saeed MA, et al. Gastric intestinal metaplasia: subtypes and natural history. J Clin Pathol 2001; 54: Fock KM, Talley NJ, Fass R, et al. Asia-Pacific consensus guidelines on gastric cancer prevention. J Gastroenterol Hepatol 2008; 23: In this manuscript, consensus guidelines for H. pylori screening and eradication were established. 49 Talley NJ, Fock KM, Moayyedi P. Gastric Cancer Consensus conference recommends Helicobacter pylori screening and treatment in asymptomatic persons from high-risk populations to prevent gastric cancer. Am J Gastroenterol 2008; 103: Satoh K, Osawa H, Yoshizawa M, et al. Assessment of atrophic gastritis using the OLGA system. Helicobacter 2008; 13:
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