History of Classification of Gastritis.
The gastritis is an inflammatory condition of the gastric mucosa characterized by existence of elementary histological alternations. However these structural changes observed by the pioneer of gastric histology were noted more than a century ago, their etiology and proper interpretation for clinical practice required much longer time.
The ancient Egyptians wrote that the diseases of internal organs are difficult to detect even in well-preserved bodies, hence they were not able to comprehend outstanding discoveries on the stomach as they did on other organ diseases. The first major discovery in the field of gastric diseases was the description of gastric cancer by the Persian Avicenna around 1000 (quoted by Rugge et al, 2003). At the same time the discoveries of non-neoplastic gastric diseases, especially gastritis, was really elusive for quite a long time due to less macroscopic features and to post-mortem alternations. The inflammation of the inner lining of the stomach was first noted as “gastritis” by a German physician, Georg Ernst Stahl in 1728 (quoted by Bock, 1974). Italian anatomical pathologist Giovanni Battista Morgagni further described the signs of gastric inflammation. He gave the first classical description of an erosive or ulcerating gastritis. He stated that some of the erosions can become gangrenous, and described corrosive gastritis as it was the most well-known gastritis form of that time due high number of lye intoxication. French physician, François-Joseph-Victor Broussais gathering information by autopsy of dead French soldiers between 1808 and 1831, described common chronic gastritis as he called “Gastritides”, and sometimes got delusive conclusions as gastritis was the cause of ascites and other diseases, like typhoid fever and meningitis (Bock, 1974). Jones Handfield and Wilson Fox (1854) described microscopic changes of mucous membrane in gastric inflammation, which exists in diffuse and segmental forms. Not much later another British physician, William Brinton (1859) emphasized the symptomatic and microscopic differences of acut, subacute and chronic gastritis in his medical book entitled “Diseases of Stomach”, and described haemorrhagic erosion and follicular ulceration. Meanwhile Baron Carl von Rokitansky besides his major discoveries was the first to note hypertrophic gastritis in 1855. The next major footstep was done by Samuel Fenwick in 1870, who noted the presence of glandular atrophy due to gastric inflammation when classifying gastric lesions and anatomical alternations of the gastric mucosa (Fenwick, 1870). He also discovered that pernicious anaemia is associated with gastric mucosal atrophy. German surgeon, Georg Ernst Konjetzny using surgical specimens showed first that both gastric ulcer and gastric cancer are either secondary diseases or are associated in their pathogenesis to chronic gastric inflammation. Shields Warren and Willam A. Meissner described intestinal metaplasia of the stomach. They noted intestinal metaplasia as a feature of chronic gastritis, and found seldom extensive in duodenal ulcer patients, while it was extensive in stomachs removed due to carcinoma (Warren & Meissner, 1944; Rugge et al, 2003).
2. In vivodiagnosis of gastritis – Introduction of gastroscopy
Based on recent research data, Robert G. Strickland and Ian R. MacKay proposed the classification of gastritis based on additional factors just beside just histology and topography (Strickland & Mackay, 1973). They suggested that immunological and etiological data should be included along with pathomorphological and topographic parameters; gastric parietal cell antibody and serum level of gastrin have to be seen to get better classification of chronic gastritis. They used the term ‘Type A gastritis’ for gastric corporal inflammation mostly corresponding to pernicious anaemia, and ‘Type B’ for antral gastritis suspected to be induced by duodeno-gastric reflux according to some thoughts. In 1975 George B Jerzy Glass and Capecomorin S. Pitchumoni added the ‘Type AB’ to the classification. This term was aimed to be used for extended gastritis observed in corpus to pre-pyloric region (Glass & Pitchumoni, 1975). Those cases were named ‘AB-plus’ where antibody positivity was also founds against parietal cells. In 1980, the classification was further modified by Correa dividing chronic gastritis into autoimmune chronic gastritis with pernicious anaemia, ‘hypersecretory’ and ‘environmental’ forms. He described the gastritis accompanying ulcer to hypersecretory. All the rest of gastritis was called environmental, which are mostly due to diet and geographic localization (Correa, 1980). Later as more data were known from histological assessments, he changed his classification for ‘diffuse antral’, ‘diffuse corporal’ and ‘multifocal’ gastritis. By seeing his nomenclature, sometimes showing etiology, sometimes reflecting topography, we are able to see the controversy existed between pathologist and clinicians in the field of gastritis at that time. The extensiveness in topography along with histological and etiologic features were not to be combined in an uniformed nomenclature, even Correa in 1988 returned to his previous version of classification (Correa, 1988). Later, he went to different direction by dividing gastritis into two major categories of ‘atrophic’ and ‘non-atrophic’ gastritis.
The next major step was added by Judith I. Wyatt and Michael F. Dixon by the introduction of ‘type C’ gastritis for chemical (drug)-induced inflammation of gastric mucosa (Wyatt & Dixon, 1988). Two years later, examining 316 patients Sobala confirmed that most of reflux gastritis in intact (non-operated) stomach is not due to bile reflux but rather NSAID use. According to their proposition the term ‘type C’ or ‘chemical’ gastritis might be used for condition caused by both etiology (Sobala et al, 1990).
3. Modern time – Development of the Sydney system
Modern aspects of gastritis classification and knowledge of its biological course and consequences were relatively well-known at the time when
|1728||Stahl||‘Gastritis’ defined (quoted by Bock, 1974)|
|1771||Morgagni||’Erosive’ and ’ulcerating gastritis’’ described (Crawford et al, 1932)|
|1859||William Brinton||Acute, subacute and chronic gastritis differentiated □|
|1855||Rokitansky||Hypertrophic gastritis described (quoted by Vaugham, 1945).|
|1870||Fenwik||Gastric atrophy described □|
|1944||Warren & Meissner||Intestinal metaplasia described □|
|1947||Wood||First gastric biopsy, ‘Gastritis’ defined (Wood et al, 1949)|
|1956||Cheli & Dobero ¤||Superﬁcial, Interstitial and Atrophic gastritis □|
|1956||Eder-Palmer ∇||Introduction of ﬂexible ﬁbre optic endoscope (Palmer, 1956)|
|1972||Whitehead ¤||Superficial, Atrophic, both ‘Active’ or ‘In-active’. Type and Stage of activity. Presence and type of metaplasia □|
|1973||Strickland & MacKay ¤||A (autoimmune) PCA+ in 95% and IFA+ in 75%, B (nonautoimmune = environmental) □|
|1975||Pitchumoni ¤||A (autoimmune-corpus), B (antrum), AB (both antrum and corpus) PCA+ or - (Glass & Pitchumoni, 1975)|
|1980||Correa ¤||Autoimmune, Hypersecretory, Environmental □|
|1988||Correa ¤||Diffuse corporal (autoimmune), Chr. diffuse antral, Multifocal environmental, Chr. Superficial, Lymphocytic, Postgastrectomy □|
|1989||Owen ¤||Chr. non-specific type A, Chr. non-specific type B □|
|1990||Yardley ¤||H. pylori gastritis, Metaplastic atrophic (type A, autoimmune), Metaplastic atrophic (type B), Lymphocytic, Chemical □|
|1990||Dixon ¤||’Type C’ proposed to reactive gastric lesions □|
|1990||Sobala||Reflux gastritis defined as type C gastritis □|
|1990||Sydney ¤||Nonatrophic, Atrophic (Autoimmune, Multifocal), Special forms. Four-level scale, proper biopsy sampling & handling, standard reporting aiming etiology (Misiewicz et al, 1990)|
|1994||Appelman ¤||Acute or Chronic; Helicobacter type, Atrophic (type A, type B), Lymphocytic, Focal & miscellaneous, Chemical gastropathies □|
|1996||Up-dated Sydney ¤||Biopsy location changed from anterior and posterior wall to greater and lesser curvature (Dixon et al, 1996)|
|2000||Padova ¤||Classification of dysplasia and related lesions (Rugge et al, 2000)|
|2005||OLGA ¤||Classification of grading mucosal atrophy (Rugge et al, 2005b)|
The Sydney System which actually allowed statements to be made on etiology, topography and morphology of gastritis for the first time, was not accepted everywhere immediately, especially in the United States. The main criticism was that the some of the commonly used descriptive names were not enabled into the system, like the ‘multifocal atrophic gastritis’ or ‘diffuse antral gastritis’. Although, by that time it was already accepted that the Sydney System was not designed to be the textbook of gastric pathology, but to be a guide for standard methology of reporting. Correa and Yardley criticized the system for missing out certain types of the gastritis and well as it is not a ‘classification’ (Correa & Yardley, 1992). Consequently, a new system needed to gain wider acceptance.
In 1994, a two-day consensus meeting was held in Houston. After this another consensus report, “Up-dated Sydney System” was published in 1997 (Dixon et al, 1996). Original classification of gastritis dividing into acute, chronic and special forms, and grading of chronic inflammation, polymorph activity, atrophy, intestinal metaplasia and
4. Classification by Appleman
The clearest division of gastritis for clinicians was published by Appleman in 1994. He divided gastric inflammatory diseases to
According to Appelman’s classification the autoimmune gastritis used to be called as gastritis autoimmunogenes, gastritis chronic atrophica typus A, gastritis chronic typus A and gastritis chronic diffusa corporis, was called to a
Appelman’s classification of gastritis continues with the
Appelman seeing similarity of the histological changes of patients with gastroenteric anastomosis and taking nonsteroidal anti-inflammatory (NSAID) medications, called third division of gastritis caused by bile reflux or NSAIDs to
Appelman kept the name of
Appelman’s division of gastritis contained a miscellaneous group of gastritis. There are many gastritis forms that do not differ significantly from similar inflammations found other organs, including those that occur in syphilis, mycobacterial and cytomegalovirus, human immunodeficiency virus infections, histoplasmosis, candidiasis, cryptosporidiosis and other opportunistic fungi. There is a family of granulomatous reactions or
|Acute infectious gastritis (including Hp)|
|Erosive (caused mostly by NSAID or alcohol)|
|Necrotising and haemorrhagic (caused mostly by ischaemia)|
|Type A: autoimmune, diffuse|
|Type B: non-autoimmune, multifocal, enviromental|
|Including varioliform, ’sprue-like’ and Ménétrier-like|
|others (caused by other damaging agents and physical trauma)|
|Granulomatous (part of Crohn’s, Whipple’s, vasculitis, sarcoidosis or isolated granulomatous gastritis)|
|Specific infectious (HIV, mycobacterial, syphilis, Cytomegalovirus, histoplasmosis, cryptosporidiosis|
5. Precancerous lesions
Warren and Meissner describing intestinal metaplasia and recognising the clinical-pathological pattern of gastritis, described the bases of etiopathogenic relationship between gastric cancer and chronic gastritis (Warren & Meissner, 1944; Rugge et al, 2003). In 1980, Morson
|Negative for dysplasia||1.0 Normal|
|1.1 Reactive foveolar hyperplasia|
|1.2 Intestinal metaplasia||1.2.1 Complete type|
|1.2.2 Incomplete type|
|Indefinite for dysplasia||2.1 Foveolar hyperproliferation|
|2.2 Hyperproliferative intestinal metaplasia|
(flat or elevated)
|3.2 High-grade||3.2.1 Including suspicious for carcinoma without invasion (intraglandular)|
|3.2.2 Including carcinoma without invasion (intraglandular)|
|Suspicious for invasive carcinoma|
6. Evaluation of atrophy
The Sydney System and Up-dated Sydney System attempted to incorporate etiologic, topographic, and morphologic criteria into a clinically relevant scheme to reach a broad consensus in classification of gastritis. One of the most controversial issues at the Houston Workshop was the concept of atrophy. It was pointed out that "normal" was not precisely defined; the loss of appropriate glands occurs with distinct patterns and has different functional significance in antrum and corpus; the relationship between atrophy and intestinal metaplasia remained incompletely understood; and the topographic patterns of distribution and its evolution made the atrophic gastritis to the most controversial topic of gastritis (Genta, 1996). Later long-term follow-up studies have confirmed that the extent of gastric mucosal atrophy parallels gastric cancer risk (Meining et al, 2002; Sipponen et al, 1985, 1994, 1997; Stolte et al, 2000). At the same time Sydney System did not present a reporting terminology for chronic gastritis understandable and providing prognostic and therapeutic information for clinicians. Whereas, hepatitis staging had already improved useful, simple terminology for interdisciplinary communication representing disease progression and cancer risk.
Inspired by these facts, international group of gastroenterologists and pathologists named as Operative Link on Gastritis Assessment (OLGA) developed an improved histological staging system for gastric atrophy (Rugge & Genta, 2005a, 2005b). OLGA system uses the gastric biopsy sampling protocol defined by Sydney System and the visual analogue system recommended by the Up-dated Sydney System. The gastritis staging is defined from combined extent of atrophy scored histologically with the topography of atrophy identified through biopsy mapping (see Fig. 2). Long-term follow-up studies proved that gastritis OLGA staging conveys relevant information on clinic-pathological outcome of gastritis and therefore
Similar to the OLGA system another system, called the Baylor system was also introduced. The Baylor system follows the Baylor biopsy protocol (which uses Sydney System biopsy sites with two additional distal corporal biopsies) and scores the atrophy of antrum and corpus independently (Graham et al, 2006). Antral atrophy stage is an average score, but corpus atrophy stage is independent of antral atrophy, independent of individual reading in each biopsy but dependent on location. As corpus atrophy starts at the incisura and extends in continuity proximally and towards the greater curve, atrophy in a distal biopsy is early and atrophy in the most proximal location is advanced. The comparison of the two atrophy grading systems is still controversial. Although there were studies performed showing the superiority of Baylor system over OLGA in indentifying cancer risk (El-Zimaity et al, 2008), the evaluation of gastric atrophy by OLGA is more widely used, further developed and more studied.
Even though above precursor lesions were commonly known and found in everyday practice, there were no international recommendation to guide the clinicians in management of patients with such lesions. This resulted wide heterogeneity of surveillance practice and failure in diagnosing patients with early, curable stage cancer. The European Society of Gastrointestinal Endoscopy (ESGE), the European Helicobacter Study Group (EHSG), the European Society of Pathology (ESP) and the Sociedade Portuguesa de Endoscopia Digestiva (SPED) have therefore combined efforts to develop evidence-based guideline on the
The recommendations contain that conventional white light endoscopy cannot accurately differentiate between and diagnose pre-neoplastic gastric conditions/lesions. Thus, magnification chromoendoscopy or narrow-band imaging (NBI) endoscopy with or without magnification may be offered in these cases as it improves diagnosis of such lesions. In addition, at least four biopsies of the proximal and distal stomach, on the lesser and greater curvature, are needed for adequate assessment of premalignant gastric conditions. Systems for histopathological staging (e.g. OLGA or OLGIM assessment) may be useful for identifying subgroups of patients with different risks of progression to gastric cancer namely those with extensive lesions (i. e., atrophy and/or intestinal metaplasia in both antrum and corpus). Although only low potential applicability was reported by participants for this indicator, low serum pepsinogen levels can also predict this phenotype and, in such patients,
This review critically offers and emphasizes the necessity of an international consensus meeting, which will establish a more uniform classification of gastritis respecting the wider multidisciplinary aspects (morphology, clinical picture, endoscopic view, immunology, bacteriology, molecular pharmacology, general medicine, oncology and causative factors as well as social/environmental circumstances of the people) in this field.
During the about last 150 years the knowledge on “gastritides” has enlarged enormously. The discovered new forms of gastritis, the new etiopathogenic evidences have continuously modified our views on gastritis classification. Recently, good agreement has been established among pathologist and clinicians to standardise the methodology of biopsy sampling, histological assessment and reporting leading to reproducible and clinically useful diagnosis. Recent recommendations for the management of bleeding,
Appelman H.D. (1994). Gastritis: terminology, etiology, and clinicopathological correlations: another biased view. Hum Pathol, Vol.25, pp.1006-19.
Brinton W. (1857). On the Pathology, Symptoms and Treatment of Ulcer of the Stomach, London, J. Churchill.
Bock O.A. (1974). The relationship between chronic gastritis, gastric ulceration and carcinoma of the stomach. A historical review. S Afr Med J, Vol.48: pp.2063-6.
Capelle L.G., de Vries A.C., Haringsma J., et al. (2010). The staging of gastritis with the OLGA system by using intestinal metaplasia as an accurate alternative for atrophic gastritis. Gastrointest Endosc, Vol.71: pp.1150-8.
Cheli R., Dodero M. (1956). Sulle alterazioni ghiandolari fundiche nelle gastriti croniche. Ricerche bioetiche e correlazioni anatomo-secretorie. Min Gastroenterol, Vol.4: pp.1–6.
Correa P. (1980). The epidemiology and pathogenesis of chronic gastritis; three etiologic entities. Front Gastrointestinal Res, Vol. 6: pp.98-108.
Correa P. (1988). Chronic gastritis: a clinico-pathological classification. Am J Gastroenterol,Vol.83: pp.504-9.
Correa P., Yardley J.H. (1992). Grading and classification of chronic gastritis: one American response to the Sydney System. Gastroenterology, Vol.102, pp.355-9.
Crawford Q., Crawford A. (1832). Ulceration of the Brain. The Medico-Chirurgical Review, and Journal of Practical Medicine,Vol.16, pp.601.
Dinis-Ribeiro M., Areia M., de Vries A.C., et. al. (2012). European Society of Gastrointestinal Endoscopy; European Helicobacter Study Group; European Society of Pathology; Sociedade Portuguesa de Endoscopia Digestiva. 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, Vol.44: pp.74-94.
Dixon M.F. (1990). Progress in the pathology of gastritis and duodentitis. In: Gastrointestinal Pathology, Williams G.T. (Ed.), Springer-Verlag, Berlin, Germany, pp.1-27.
Dixon M.F., Genta R.M., Yardley J.H., Correa P, Participants on the International Workshop on the Histopathology of Gastritis. (1996). Classification and grading of gastritis. The updated Sydney System. Am J Surg Pathol, Vol.20, pp.1161-81.
Dixon M.F., Genta R.M., Yardley J.H., Correa P. (1997). Histological classification of gastritis and Helicobacter pyloriinfection: an agreement at last? The International Workshop on the Histopathology of Gastritis. Helicobacter, Vol.2 Suppl 1: pp.17-24.
El-Zimaity H.M., Graham D.Y., al-Assi M.T., et al. (1996). Interobserver variation in the histopathological assessment of Helicobacter pylorigastritis. Hum Pathol, Vol.27: pp.35-41.
El-Zimaity H. (2008). Gastritis and gastric atrophy. Curr Opin Gastroenterol, Vol.24: pp.682-6.
Fenwick S. (1870). On atrophy of the stomach. Lancet, Vol. ii: pp.78-80.
Genta R.M. (1996). Recognizing atrophy: another step toward a classification of gastritis. Am J Pathol, Vol.20 Suppl 1: pp.23-30.
Glass G.B.J., Pitchumoni C.S. (1975). Atrophic gastritis. Hum Pathol, Vol.6: pp.219-50.
Graham DY, Nurgalieva ZZ, El-Zimaity HM, et al.. (2006). Noninvasive versus histologic detection of gastric atrophy in a Hispanic population in North America. Clin Gastroenterol Hepatol, Vol.4: pp.306-14.
Haot J., Hamichi L., Wallez L., Mainguet P. (1988). Lymphocytic gastritis: a newly described entity: a retrospective endoscopic and histological study. Gut, Vol.29: pp.1258-64.
Haot J., Jouret A., Willette M., Gossuin A., Mainguet P. (1990). Lymphocytic gastritis--prospective study of its relationship with varioliform gastritis. Gut, Vol.31: pp.282-5.
Kozlowski W., Jochymski C, Markiewicz T. (2011). Chronic gastritis, In: Gastritis and Gastric Cancer – New Insights in Gastroprotection, Diagnosis and Treatments,Tonino P. (Ed.), 76-92, In-Tech, Rijeka, Croatia.
Marshall B.J., Warren J.R. (1984). Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet, Vol.1: pp.1311-5.
Meining A., Riedl B., Stolte M. (2002). Features of gastritis predisposing to gastric adenoma and early gastric cancer. J Clin Pathol, Vol.55: pp.770-3.
Misiewicz J.J., Tytgat G.N.J., Goodwin C.S., et al. (1990). The Sydney System: a new classification of gastritis. World Congresses of Gastroenterology,1990 August 26–31. Sydney, pp.1-10.
Morson B.C., Sobin L.H., Grundmann E., Johansen A., Nagayo T., Serck-Hanssen A. (1980). Precancerous conditions and epithelial dysplasia in the stomach. J Clin Pathol, Vol.33: pp.711–21.
Offerhaus GJ, Price AB, Haot J, et al. (1999). Observer agreement on the grading of gastric atrophy. Histopathology, Vol.34: pp.320-5.
Owen D.A: (1989). Stomach. In: Diagnostic surgical Pathology and Its Clinical Implications, Stenberg S.S. (Ed.), New York, NY, Raven Press, pp. 939-48.
Palmer E.D. (1956). Clinical benmefit of routine combined oesophagogastroscopy with the help of the two trabnsoesophagoscopic gastroscope. Bull Am Gastrosc Soc, Vol.4: pp.7-11.
Price A.B., Misiewicz J.J. (1991). Sydney classification for gastritis. Lancet, Vol.337:pp.174.
Price A.B. (1991). The Sydney System: Histological division. J Gastoenterol Hepatol, Vol.6, pp.209-22.
Rugge M., Di Mario F., Cassaro M., et al. (1993). Pathology of the gastric antrum and body associated with Helicobacter pyloriinfection in non-ulcerous patients: is the bacterium a promoter of intestinal metaplasia? Histopathology, Vol.22: pp.9-15.
Rugge M., Farinati F., Baffa R., Sonego F., Di Mario F., Leandro G., Valiante F. (1994). Gastric epithelial dysplasia in the natural history of gastric cancer: a multicenter prospective follow-up study. Interdisciplinary Group on Gastric Epithelial Dysplasia. Gastroenterology, Vol.107: pp.1288-96.
Rugge M., Cassaro M., Farinati F., Di Mario F. (1997). Diagnosis of gastric carcinoma in Japan and western countries. Lancet, Vol.350: pp.448.
Rugge M., Correa P., Dixon M.F., et al. (2000). Gastric dysplasia: the Padova international classification. Am J Surg Pathol, Vol.24: pp.167–76.
Rugge M., Russo V.M., Guido M. (2003). Review article: what have we learnt from gastric biopsy? Aliment Pharmacol Ther, Vol.17 Suppl 2: pp.68-74.
Rugge M., Genta R.M. (2005a). Staging and grading of chronic gastritis. Hum Pathol, Vol.36: pp.228-33.
Rugge M., Genta R.M., OLGA Group. (2005b). Staging gastritis: an international proposal. Gastroenterology, Vol.129: pp.1807-8.
Rugge M., Meggio A., Pennelli G., et al. (2007). Gastritis staging in clinical practice: the OLGA staging system. Gut,Vol.56: pp.631-6.
Rugge M., de Boni M., Pennelli G., et al. (2010). Gastritis OLGA-staging and gastric cancer risk: a twelve-year clinico-pathological follow-up study. Aliment Pharmacol Ther, Vol.31: pp.1104-11.
Rugge M., Fassan M., Pizzi M., et al. (2011). Operative link for gastritis assessment vs operative link on intestinal metaplasia assessment. World J Gastroenterol, Vol.17: pp.4596-601.
Schindler R. (1947). Gastritis. London: William Heinmann (Medical Books).
Sipponen P., Kekki M., Haapakoski J., Ihamäki T., Siurala M. (1985). Gastric cancer risk in chronic atrophic gastritis: statistical calculations of cross-sectional data. Int J Cancer, Vol.35: pp.173-7.
Sipponen P, Price A.B. (2011). The Sydney System for classification of gastritis 20 years ago. J Gastroenterol Hepatol, Vol.26 Suppl 1: pp.31-4.
Sipponen P., Riihelä M., Hyvärinen H., Seppälä K. (1994). Chronic nonatropic ('superficial') gastritis increases the risk of gastric carcinoma. A case-control study. Scand J Gastroenterol, Vol.29: pp.336-40.
Sipponen P., Stolte M. (1997). Clinical impact of routine biopsies of the gastric antrum and body. Endoscopy, Vol.29: pp.671-8.
Sobala G.M., King R.F., Axon A.T., Dixon M.F. (1990). Reflux gastritis in the intact stomach. J Clin Pathol, Vol.43: pp.303-6.
Stolte M., Meining A. (2000). Helicobacter pylorigastritis of the gastric carcinoma phenotype: is histology capable of identifying high-risk gastritis? J Gastroenterol, Vol.35 Suppl 12: pp.98-101.
Stolte M., Meining A. (2001). The updated Sydney system: classification and grading of gastritis as the basis of diagnosis and treatment. Can J Gastroenterol, Vol.15: pp.591-8.
Strickland R.G., Mackay I.R. (1973). A reappraisal of the nature and significance of chronic atrophic gastritis. Am J Dig Dis, Vol.18: pp.426-40.
Szabo I., Illes A., Godi S., et al. (2012). Gastritis staging in clinical practice by OLGA (Operative Link for Gastritis Assessment) system - Evaluation of gastric mucosal atrophy and metaplasia. Z Gastroenterol, Vol.50, A72.
Vaughan W. (1945). Antral Gastritis: Roentgenologic and Gastroscopic Findings. Radiology, Vol.44, pp. 531-42.
Warren J.R., Marshall B. (1983). Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet, Vol.321, pp.1273-4.
Warren S., Meissner W.A. (1944). Chronic Gastritis and Carcinoma of the Stomach. Gastroenterology, Vol.3: pp.251-6.
Whitehead R., Truelove S.C., Gear M.W. (1972). The histological diagnosis of chronic gastritis in fibreoptic gastroscope biopsy specimens. J Clin Pathol, Vol.25: pp.1–11.
Wood I.J., Doig R.K., Motteram R. et al. (1949). Gastric biopsy; report on 55 biopsies using a new flexible gastric biopsy tube. Lancet, Vol.1: pp.18-21.
Wyatt J.I., Dixon M.F. (1988). Chronic gastritis--a pathogenetic approach. J Pathol, Vol.154: pp.113-24.
Yadley J.H. (1990). Pathology of chronic gastritis and duodenitis. In: Gastrointestinal Pathology, Ch: 3, Goldman H., Appelman H.D., Kaufman N. (Eds.), Williams & Wilkins, Baltimore, MD, pp.69-121.