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com

Digestive and Liver Disease 40 (2008) 650658

Mini-Symposium

OLGA staging for gastritis: A tutorial

M. Rugge a,b, , P. Correa c , F. Di Mario d , E. El-Omar e , R. Fiocca f ,
K. Geboes g , R.M. Genta h , D.Y. Graham i , T. Hattori j , P. Malfertheiner k ,
S. Nakajima l , P. Sipponen m , J. Sung n , W. Weinstein o , M. Vieth p
a

Department of Medical Diagnostic Sciences & Special Therapies (Pathology Section), University of Padova, Italy
b Veneto Institute of Oncology (IOV-IRCSS), Padova, Italy
c Division of Gastroenterology, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
d Department of Clinical Sciences, Section of Gastroenterology, University of Parma, Italy
e Department of Medicine & Therapeutics Institute of Medical Sciences, Aberdeen University, UK
f Department of Surgical, Morphological & Integrated Disciplines (Anatomic Pathology Section), University of Genova, Italy
g Department of Pathology, Catholic University of Leuven, Belgium
h Department of Pathology, University of Texas Southwestern Medical Center, Dallas, TX, USA
i Michael E. Debakey VA Medical Center & Baylor College of Medicine, Houston, TX, USA
j Department of Pathology Shiga University Medical Sciences, Shiga, Japan
k Department of Gastroenterology Hepatology And Infectious Diseases, Otto-Von-Guericke-University, Magdeburg, Germany
l Department of Medicine, Gastroenterology and Healthcare Social Insurance Shiga Hospital, Shiga, Japan
m Division of Pathology, HUSLAB, Helsinki University Hospital, Helsinki, Finland
n Department of Medicine & Therapeutics, Faculty of Medicine, The Chinese University of Hong Kong, China
o Department of Medicine Division of Digestive Diseases, UCLA Center for Health Sciences, USA
p Institute of Pathology Klinikum Bayreuth, Bayreuth, Germany
Received 1 February 2008; accepted 18 February 2008
Available online 17 April 2008

Abstract
Atrophic gastritis (resulting mainly from long-standing Helicobacter pylori infection) is a major risk factor for (intestinal-type) gastric
cancer development and the extent/topography of the atrophic changes significantly correlates with the degree of cancer risk.
The current format for histology reporting in cases of gastritis fails to establish an immediate link between gastritis phenotype and risk
of malignancy. The histology report consequently does not give clinical practitioners and gastroenterologists an explicit message of use in
orienting an individual patients clinical management.
Building on current knowledge of the biology of gastritis and incorporating experience gained worldwide by applying the Sydney System
for more than 15 years, an international group of pathologists (Operative Link for Gastritis Assessment) has proposed a system for reporting
gastritis in terms of stage (the OLGA staging system). Gastritis staging arranges the histological phenotypes of gastritis along a scale of
progressively increasing gastric cancer risk, from the lowest (stage 0) to the highest (stage IV).
This tutorial aims to provide unequivocal information on how to consistently apply the OLGA staging system in routine diagnostic histology
practice.
2008 Published by Elsevier Ltd on behalf of Editrice Gastroenterologica Italiana S.r.l.
Keywords: Atrophic gastritis; Gastritis staging; OLGA staging

1. Introduction

Corresponding author at: Chair, Anatomic Pathology, Universit`a degli

Studi di Padova, Istituto Oncologico del Veneto IOV-IRCCS, Via Aristide
Gabelli 61, 35121 Padova, Italy.
E-mail address: massimo.rugge@unipd.it (M. Rugge).

Chronic (Helicobacter-associated) gastritis is a crucial

step in the natural history of gastric oncogenesis and its epidemiological link with gastric carcinoma is well established
[1,2].

1590-8658/$30 2008 Published by Elsevier Ltd on behalf of Editrice Gastroenterologica Italiana S.r.l.
doi:10.1016/j.dld.2008.02.030

M. Rugge et al. / Digestive and Liver Disease 40 (2008) 650658

Upper gastrointestinal endoscopy with biopsy sampling is

the definitive diagnostic procedure whenever a gastric malignancy is suspected. Its use for the secondary prevention of
gastric cancer (GC) is generally limited because of its invasiveness and cost, but for selected high-risk patients it remains
the only available strategy [3,4].
While many aspects of the biology of gastritis remain
to be elucidated, a large body of information indicates that
gastric atrophy is the single most powerful predictor of the
onset of intestinal-type GC [59]. Intestinal metaplasia is
generally considered as the field cancerisation in the gastric mucosa and, at cell level, intestinalised glands provide
the cellular substrate on which gastric non-invasive neoplasia (NiN) develops [10,11]. There is some evidence to
show that intestinal metaplasia can be reversed (by clearing
H. pylori infection or applying chemoprevention strategies),
but the chances of aborting the progression of NiN to cancer are considerably lower, and that high-grade NiN will
evolve into invasive adenocarcinoma is a virtual certainty
[9].
In spite of the greater consistency brought about by
the Sydney System and its updated 1996 Houston version, the commonly-used nomenclature for gastritis remains
inconsistent and individual, non-standard styles of histology
reporting for gastritis are still widely used to the consternation of clinicians [1215]. Many practitioners are unable
to perceive the different cancer risk associated with multifocal atrophic gastritis, corpus predominant gastritis, or
antrum-predominant H. pylori chronic active gastritis, and
even well-informed specialists are often frustrated by a terminology that makes it difficult to identify candidates for
endoscopic surveillance [1,7,13,1518].
Building on current knowledge of the natural history of
gastritis and the associated cancer risk, an international group
of gastroenterologists and pathologists (the Operative Link
for Gastritis Assessment [OLGA]) has proposed a system
for reporting gastritis in terms of stage (the OLGA staging
system), which arranges the histological phenotypes of gastritis along a scale of progressively increasing GC risk, from
the lowest (OLGA stage 0) to the highest (OLGA stage IV)
[19,20]. The staging framework is borrowed from the oncology vocabulary and applies the histology reporting format
successfully employed for chronic hepatitis to the gastritis
setting too [21,22]. Just as fibrosis is the main lesion used
to weigh the risk of liver cirrhosis, gastric mucosal atrophy
is considered the marker of cancer risk. Additionally, just as
a given number of portal tracts are required for the accurate
staging of hepatitis, a well-defined biopsy sampling protocol (as recommended by the Sydney System) is considered a
minimum requirement for the reliable staging of gastritis
[13,2325].
The stage of gastritis results from the combination of the
extent of atrophy (scored histologically) with its topographical location (resulting from the mapping protocol) [26]. In
line with the Sydney recommendations, the OLGA staging
system also includes information on the likely aetiology of

651

the gastric inflammatory disease (e.g. H. pylori, autoimmune,

etc.).
This tutorial aims to expand on the available information
with a view to a consistent application of the OLGA staging system. The provided clues are founded basically on the
current definition of gastric atrophy and on the worldwide
experience accumulated by practicing the Houston-updated
Sydney System.

2. Denition of atrophy in the gastric mucosa

Normal gastric biopsy samples (from adolescents and
adults) feature different populations of glands (mucosecreting or oxyntic), appropriate for the functional compartment
(antrum or corpus) from which the specimen has been
obtained (i.e. appropriate glands) [27,28] (Fig. 1). Occasionally, minuscule foci metaplastic (goblet) cells may be
encountered, particularly in the foveolar epithelium, but
the overall density of appropriate glands is not affected.
In the gastric mucosa, atrophy is defined as the loss of
appropriate glands. Different phenotypes of atrophic transformation may be encountered, i.e.
(a) vanishing, or evident shrinkage of glandular units associated with (fibrotic) expansion of the surrounding lamina
propria. Such a situation results in a reduced glandular mass,
but does not imply any modification of the original epithelium
phenotype (Fig. 1);
(b) metaplastic replacement of the native glands by glands
featuring a new cellular commitment (= intestinal and/or
pseudopyloric metaplasia). The number of glands is not
necessarily lower, but the metaplastic replacement of the
original glandular units results in a smaller population of
the native glands (which are appropriate for the compartment considered). Such a condition is also consistent
with the general definition of loss of appropriate glands
(Fig. 1).
Sometimes (particularly in H. pylori-associated gastritis), severe inflammation makes it impossible to determine
whether glands that appear to be lost are merely obscured
by the inflammatory infiltrate or whether they have genuinely
vanished. In such cases, a temporary diagnosis of indefinite for atrophy can be made, deferring the final judgment
until the inflammation has resolved (e.g. after eradication of
the H. pylori infection). This indefinite category, borrowed
from the classification of intra-epithelial neoplasia (dysplasia) in the gastrointestinal tract, is not intended to represent
a biological entity [28].
In tune with the above-mentioned criteria, an International Group of Gastrointestinal Pathologists (Atrophy
club) arranged the histological spectrum of atrophic changes
into a formal classification (Table 1). After testing in real
cases, the interobserver consistency in recognizing/scoring
the atrophic lesions was considered more than adequate
[28].

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M. Rugge et al. / Digestive and Liver Disease 40 (2008) 650658

Fig. 1. Normal and atrophic glandular units in the stomach. 1: Normal mucosecreting gland. The glandular structure consists of mucosecreting cells (yellow
line). In this, as in all the other glandular structures, both the superficial layer and proliferative zone are represented as a pink line. 2: Non-metaplastic atrophy
in a mucosecreting gland: the number of glandular coils is decreased and the glands profile has become simpler (shrunk) and does not reach the bottom of
the mucosal layer. 3: Metaplastic atrophy (intestinal metaplasia): the glandular profile is simplified, looking like an intestinal crypt (intestinalized epithelia are
represented as bright blue line). 4: Normal oxyntic gland (green profile). 5: Non-metaplastic atrophy in an oxyntic gland: the glands profile is shorter (shrunk)
and the tubular structure does not reach the bottom of the mucosal layer. 6: Pseudopyloric metaplasia in oxyntic gland: the parietal and chief cells (green
line) are replaced by mucosecreting epithelia (yellow line, as in the antral glands). The intestinalization of a native oxyntic gland is similar to that shown for
mucosecreting glands (see 3).

3. Gastritis staging: the OLGA system

Gastritis can be interpreted on two different levels: (a) a
basic level represented by the elementary lesions; and (b) a
hierarchically higher level (as a stomach disease proper)
depending on the extent and topographic distribution of the
different elementary lesions.
In 1955 Basil Morson said that, the incidence and
the extent of intestinal metaplasia are greatest in stomachs
containing carcinomas and least in those with duodenal
ulcer, with cases of gastric ulcer taking an intermediate position. Correa later demonstrated that patchy areas
of atrophicmetaplastic changes in the antral and oxyntic

mucosa (i.e. multifocal atrophic gastritis) frequently coexist with gastric ulcer, creating the most frequent setting for
gastric carcinoma [16,29,30].
Based on the assumption that a different extent and
topographical distribution of atrophy expresses a different
clinico-biological situation (associated with a different cancer risk), the Houston-updated Sydney System established
that multiple biopsy samples should be obtained to explore
the different mucosa compartments [13]. Different biopsy
locations have been suggested in the international literature
to map the mucosa, all of them consistent with the general assumption that both the oxyntic and the antral mucosa
have to be explored, and also considering the incisura

Table 1
Atrophy in the gastric mucosa: histological classification and grading
Atrophy
0 Absent (= score 0)
1 Indefinite (no score is applicable)
Histological type
2 Present

2.1 Non-metaplastic

2.2 Metaplastic

Location and key lesions

Antrum
Glands: shirking/vanishing
Lamina propria: fibrosis
Intestinal metaplasia

Grading
Corpus
Glands: shirking/vanishing
Lamina propria: fibrosis
Intestinal metaplasia
Pseudopyloric metaplasia

2.1.1 Mild = G1 (130%)

2.1.2 Moderate = G2 (3160%)
2.1.3 Severe = G3 (>60%)
2.2.1 Mild = G1 (130%)
2.2.2 Moderate = G2 (3160%)
2.2.3 Severe = G3 (>60%)

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653

advances from the reversible inflammatory lesions (mostly

limited to the antrum) at one end to the atrophic changes
extensively involving both functional compartments (antrum
and corpus) and associated with a high risk of GC at the other
[23].

4. How to apply the OLGA staging system for

gastritis
The OLGA staging system integrates the above experiences in an internationally-agreed staging proposal. The
System uses gastric atrophy as the lesion marking disease progression. The stage of gastritis is obtained by combining the
extent of atrophy scored histologically with the topography
of atrophy identified by the multiple biopsies (Fig. 3). The
OLGA histology report also includes the etiological information obtainable from the tissue samples available (i.e. H.
pylori infection; autoimmune disease, etc.).
The following paragraphs are intended as a brief OLGA
staging system users manual. Visual Analogue Scales
(VAS) are used to give an example of how the histology
changes featured at single biopsy level can be pieced together
to stage a given patient (Figs. 49).

Fig. 2. Gastric biopsy sampling protocol.

angularis highly informative for the purpose of establishing the earliest onset of atrophicmetaplastic transformation
[24]. The OLGA proposal (basically consistent with the
Houston-updated biopsy protocol [13]) consists in recommending (at least) five biopsy samples from: (1) the greater
and lesser curvatures of the distal antrum (A1A2 = mucussecreting mucosa); (2) the lesser curvature at the incisura
angularis (A3), where the earliest atrophicmetaplastic
changes mostly occur; and (3) the anterior and posterior
walls of the proximal corpus (C1C2 = oxyntic mucosa)
(Fig. 2).
The information obtained enables to place patients at
approximate points along the path where chronic gastritis

4.1. Atrophy score

4.1.1. Scoring atrophy (loss of appropriate glands) at
single biopsy level
In each single biopsy, atrophy is scored as a percentage of atrophic glands. Ideally, the atrophy is assessed
on perpendicular (full thickness) mucosal sections. Nonmetaplastic and metaplastic subtypes are considered together.
For each biopsy sample (whatever the area it comes from),
atrophy is scored on a four-tiered scale (no atrophy = 0%,
score = 0; mild atrophy = 130%, score = 1; moderate atrophy = 3160%, score = 2; severe atrophy = > 60%, score = 3)
(Figs. 49).

Fig. 3. The OLGA staging frame.

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M. Rugge et al. / Digestive and Liver Disease 40 (2008) 650658

Fig. 4. All 5 biopsy samples (3 from the mucosecreting compartment and 2 from the oxyntic compartment) consist of normal glands. This figure shows a
normal gastric mucosa at both antral and corpus levels. Each strip (=1 biopsy sample) is labeled according to its site of origin (antral/angular = A, corpus = C)
and includes 10 glandular units. Any inflammation (lymphocytes, monocytes, plasmacytes, granulocytes) is disregarded. The percentages given on the left refer
to the percentage of atrophic glands at single biopsy level (in this VAS, the percentage of atrophy is 0 in all the available biopsies). The total (compartmental)
prevalence of atrophy is given on the right, distinguishing between antral and corpus compartments; the final compartment atrophy score is also shown. The
OLGA staging frame is provided in the bottom right-hand corner, where the OLGA-stage is reported (OLGA-stage 0).

4.1.2. Assessing atrophy in each compartment

(mucosecreting and oxyntic)
According to the Sydney protocol, three biopsy samples
should be taken from the mucosecreting area (two antral
samples + one from the incisura angularis), and two from
the oxyntic mucosa. It is important to note that the atrophic
transformation in samples of incisura angularis mucosa

is only assessed in terms of glandular shrinkage/vanishing

(with fibrosis of the lamina propria) or intestinal metaplasia (replacing original mucosecreting and/or oxyntic
glands).
In each of the two mucosal compartments (mucosecreting and oxyntic), an overall atrophy score expresses
the percentage of compartmental atrophic changes (con-

Fig. 5. Scoring atrophy at each single antral/angular biopsy level (atrophic glands are identified by a red marker): A1 = 20%, A2 = 20% and A3 = 40%. Assessing
atrophy at compartment level (antrum): dividing 80 (=20 + 20 + 40) by 3 (the number of antral biopsies considered), the final prevalence of antral atrophy is 27%
(<30%), which means a score of 1. Scoring atrophy at each single corpus biopsy level (atrophic glands are identified by a red marker): C1 = 20%; C2 = 30%.
Assessing atrophy at compartment level (corpus): dividing 50 (=20 + 30) by 2 (the number of corpus biopsies considered), the final prevalence of corpus atrophy
is 25% (<30%), which means a score of 1. Combining the atrophy scores for the antrum (Antral atrophy score [Aas] = 1) and corpus (Corpus atrophy score
[Cas] = 1) gives us the OLGA stage, as shown in the reference chart (bottom right-hand corner: OLGA-stage I). H. pylori-status (as histologically assessed by
special stain) has to be reported.

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655

Fig. 6. Scoring atrophy at each single antral/angular biopsy level (atrophic glands are identified by a red marker): A1 = 20%; A2 = 30%; A3 = 70%. Assessing
atrophy at compartment level (antrum): dividing 120 (=20 + 30 + 70) by 3 (the number of biopsies considered), the final prevalence of antral atrophy is 40%
(>30% < 60%), which means a score of 2. Scoring atrophy at each single corpus biopsy level (atrophic glands are identified by a red marker): C1 = 30%;
C2 = 20%. Assessing atrophy at compartment level (corpus): dividing 50 (=30 + 20) by 2 (the number of biopsies considered), the final prevalence of corpus
atrophy is 25%(<30%), which means a score of 1. Combining the atrophy scores for the antrum (Aas = 2) and corpus (Cas = 1) gives us the OLGA stage, as
shown in the reference chart (bottom right-hand corner: OLGA-stage II). H. pylori-status (as histologically assessed by special stain) has to be reported.

sidering all together the biopsies obtained from the same

functional compartment). The same cut-offs are used at
this hierarchically higher assessment level as for the single
biopsies (no atrophy = 0%, score = 0; mild atrophy = 130%,
score = 1; moderate atrophy = 3160%, score = 2; severe atrophy = > 60%, score = 3). Using this strategy, an overall

atrophy score is obtained that separately summarizes the

scores for the antrum ([Aas] Aas0, Aas1, Aas2, Aas3)
and the corpus mucosa ([Cas] Cas0, Cas1, Cas2, Cas3)
(Figs. 49).
The OLGA stage results from the combination of the overall antrum score with the overall corpus score (Fig. 3).

Fig. 7. Scoring atrophy at each single antral/angular biopsy level (atrophic glands are identified by a red marker): A1 = 40%; A2 = 40%; A3 = 40%. Assessing
atrophy at compartment level (antrum): dividing 120 (=40 + 40 + 40) by 3 (the number of biopsies considered), the final prevalence of antral atrophy is 40%
(>30% < 60%), which means a score of 2. Scoring atrophy at each single corpus biopsy level (atrophic glands are identified by a red marker): C1 = 30%;
C2 = 60%. Assessing atrophy at compartment level (corpus): dividing 90 (=30 + 60) by 2 (the number of biopsies considered), the final prevalence of corpus
atrophy is 45% (>30% < 60%), which means a score of 2. Combining the atrophy scores for the antrum (Aas = 2) and corpus (Cas = 2) gives us the OLGA stage,
as shown in the reference chart (bottom right-hand corner: OLGA-stage III). H. pylori-status (as histologically assessed by special stain) has to be reported.

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M. Rugge et al. / Digestive and Liver Disease 40 (2008) 650658

Fig. 8. Scoring atrophy at each single antral/angular biopsy level (atrophic glands are always identified by a red marker): A1 = 0%; A2 = 0%; A3 = 40%.
Assessing atrophy at compartment level (antrum): dividing 40 (=0 + 0 + 40) by 3 (the number of biopsies considered), the final prevalence of antral atrophy
is 13% (<30%), which means a score of 1. Scoring atrophy at each single corpus biopsy level (atrophic glands are identified by a red marker): C1 = 90%;
C2 = 90%. Assessing atrophy at compartment level (corpus): dividing 180 (=90 + 90) by 2 (the number of biopsies considered), the final prevalence of corpus
atrophy is 90% (>60%), which means a score of 3. Combining the atrophy scores for the antrum (Aas = 1) and corpus (Cas = 3) gives us the OLGA stage, as
shown in the reference chart (bottom right-hand corner: OLGA-stage III). H. pylori-status (as histologically assessed by special stain) has to be reported. In
this case, the pattern of atrophic gastritis (corpus predominant atrophy) should suggest an autoimmune etiology.

5. From atrophy score to OLGA stage

5.1. Stage 0 gastritis (i.e. non-atrophic mucosa) (Fig. 4)
When the overall score for atrophy is 0 in both the mucosecreting and the oxyntic compartments (which means that
none of the five standard biopsy samples show signs of

atrophy), the OLGA stage is obviously 0. The score for

inflammatory lesions is independent of said stage, except
in cases considered indefinite for atrophy because a florid
inflammatory infiltrate may prevent the proper assessment of
appropriate gland loss. To avoid confounding the issue, all
the VAS provided have been cleansed of any inflammatory
component and no mention is made of any grading of the

Fig. 9. Scoring atrophy at each single antral/angular biopsy level (atrophic glands are identified by a red marker): A1 = 70%; A2 = 90%; A3 = 70%. Assessing
atrophy at compartment level (antrum): dividing 230 (=70 + 90 + 70) by 3 (the number of biopsies considered), the final prevalence of antral atrophy is 77%
(>60%), which means a score of 3. Scoring atrophy at each single corpus biopsy level (atrophic glands are identified by a red marker): C1 = 40%; C2 = 70%.
Assessing atrophy at compartment level (corpus): dividing 110 (=40 + 70) by 2 (the number of biopsies considered), the final prevalence of corpus atrophy is
55% (>30% < 60%), which means a score of 2. Combining the atrophy scores for the antrum (Aas = 3) and corpus (Cas = 2) gives us the OLGA stage, as shown
in the reference chart (bottom right-hand corner: OLGA-stage IV). H. pylori-status (as histologically assessed by special stain) has to be reported.

M. Rugge et al. / Digestive and Liver Disease 40 (2008) 650658

657

inflammatory lesions. The VAS refer to non-atrophic (normal) mucosa and are given as a standard reference to enable
comparisons to be drawn with the pathological VAS.

and GC, so endoscopic surveillance programmes should

focus on stage IIIIV-patients.

5.2. Stage I gastritis (Fig. 5)

6. Conclusions

Stage I gastritis is the lowest atrophic stage. In most

cases (and especially in H. pylori-infected patients), atrophic
lesions are only detected in some of the biopsy samples.
H. pylori status (positive versus negative) must be reported
explicitly and is an essential part of the OLGA format. H.
pylori may be difficult (or even impossible) to identify histologically at either antral or corpus level (particularly in
patients on proton pomp inhibitors [PPI]), in which case
coexisting inflammatory lesions (polymorphs and lymphoid
infiltrate) may suggest the bacteriums presence even if it is
not confirmed histologically. A comment on the suspected
aetiology (suspicious for H. pylori infection) should be
added in such cases (whatever their stage).

Recent experience suggests that gastritis staging may

afford a reliable indication of the cancer risk of individual
patients. If this is confirmed, we may be able to add to the
pathologists diagnosis a brief but clinically relevant message to help the physician develop a clinical, serological
or endoscopic management plan tailored to each patients
disease.

5.3. Stage II gastritis (Fig. 6)

This may result from a combination of different scores
and locations of atrophic transformation. Atrophy can affect
mucosecreting and/or oxyntic mucosa, but in most cases the
atrophic lesions are detected in the biopsy samples obtained
from the mucosecreting area. H. pylori status (positive versus
negative) has to be reported (see above). From preliminary
experience of OLGA staging, stage II is the most represented
in the low GC risk epidemiological setting [31].
5.4. Stage III gastritis (Figs. 7 and 8)
Stage III gastritis results from at least moderate atrophy at
mucosecreting or oxyntic level. Atrophy is most frequently
identified in the incisura angularis sample and the most
prevalent histological subtype of atrophic transformation is
the metaplastic variant. Any presence of H. pylori needs to
be reported (see above). When stage III is found in patients
with no atrophy (score 0) in the biopsy samples of mucosecreting mucosa, the aetiological hypothesis of autoimmune
(corpus restricted) atrophic gastritis should be considered.
In most populations at low risk of GC, stage III is only
rarely encountered and may coexist with NiN or even more
advanced (invasive) neoplastic disease [32].

Practice points
The histological assessment of atrophic
changes within gastric mucosa needs welldened criteria. VAS may help in the
consistent assessment of the different phenotypes of atrophic transformation.
VAS are illustrated to provide an operative
support in the histological staging of gastritis
(OLGA staging).

Research agenda
To validate the OLGA staging system for gastritis in different epidemiological contexts.
To correlate the different OLGA stages of
gastritis with serological markers of gastric
atrophy.
To validate preliminary information which
associates the OLGA stages III and IV to a high
risk of gastric epithelial malignancy.

Conict of interest statement

None declared.

5.5. Stage IV gastritis (Fig. 9)

References
This means atrophy involving both antral and oxyntic
mucosa, a situation basically corresponding to the panatrophic gastritis phenotype. In patients with H. pylori
infection, extensive metaplastic transformation can interfere
with the histological detection of the bacterium. This stage is
rarely seen in areas with a low incidence of GC. Preliminary
data show a strong association between OLGA stages IIIIV

[1] Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S,

Yamakido M, et al. Helicobacter pylori infection and the development
of gastric cancer. N Engl J Med 2001;345:7849.
[2] Correa P. The biological model of gastric carcinogenesis. IARC Sci
Publ 2004:30110.
[3] Pasechnikov V, Chukov SZ, Kotelevets SM, Mostovov AN, Mernova VP, Polyakova MB. Invasive and non-invasive diagnosis of

658

[4]
[5]

[6]

[7]

[8]

[9]

[10]
[11]

[12]
[13]

[14]
[15]

[16]

M. Rugge et al. / Digestive and Liver Disease 40 (2008) 650658

Helicobacter pylori-associated atrophic gastritis: a comparative study.
Gastroenterology 2005;40:297301.
Rugge M. Secondary prevention of gastric cancer. A matter of definitions. Gut 2007;56:16467.
Filipe M, Munoz N, Matko I, Kato I, Pompe-Kirn V, Jutersek A, et al.
Intestinal metaplasia types and the risk of gastric cancer: a cohort study
in Slovenia. Int J Cancer 1994;57:3249.
Sipponen P, Riihela M, Hyvarinen H, Seppala K. Chronic nonatropic (superficial) gastritis increases the risk of gastric carcinoma.
A casecontrol study. Scand J Gastroenterol 1994:29.
Miehlke S, Hackelsberger A, Meining A, Hatz R, Lehn N, Malfertheiner P, et al. Severe expression of corpus gastritis is characteristic in
gastric cancer patients infected with Helicobacter pylori. Br J Cancer
1998;78:2636.
Cassaro M, Rugge M, Gutierrez O, Leandro G, Graham DY, Genta RM.
Topographic patterns of intestinal metaplasia and gastric cancer. Am J
Gastroenterol 2000;95:14318.
Rugge M, Cassaro M, Di Mario F, Leo G, Leandro G, Russo
VM, et al. Interdisciplinary Group on Gastric Epithelial Dysplasia
(IGGED). The long term outcome of gastric non-invasive neoplasia.
Gut 2003;52:11116.
Stemmermann G. Intestinal metaplasia of the stomach. A status report.
Cancer 1994;74:55664.
Garcia S, Park HS, Novelli M, Wright NA. Field cancerization, clonality, and epithelial stem cells: the spread of mutated clones in epithelial
sheets. J Pathol 1999;187:6181.
Price A. The Sydney System: histological division. J Gastroenterol
Hepatol 1991;6:20922.
Dixon M, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney System. International Workshop
on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol
1996;20:116181.
Genta R. Recognizing atrophy: another step toward a classification of
gastritits. Am J Surg Pathol 1996;20(Suppl. 1):S2330.
Dixon M, Genta RM, Yardley JH, Correa P. Histological classification of gastritits and Helicobacter pylori infection: an agreement at
last? The International Workshop on the Histopathology of Gastritis.
Helicobacter 1997;2(Suppl. 1):S1724.
Correa P. Chronic gastritis: a clinico-pathological classification. Am J
Gastroenterol 1988;83:5049.

[17] Whitehead R. The classification of chronic gastritis: current status. J

Clin Gastroenterol 1995;21(Suppl. 1):S1314.
[18] Meining A, Riedl B, Stolte M. Features of gastritits predisposing to
gastric adenoma and early gastric cancer. J Clin Pathol 2002;55:7703.
[19] Rugge M, Genta RM, OLGA-Group. Staging gastritis: an international
proposal. Gastroenterology 2005;129:18078.
[20] Rugge m, Genta RM. Staging and grading of chronic gastritis. Hum
Pathol 2005;36:22833.
[21] Desmet V, Gerber M, Hoofnagle JH, Manns M, Scheuer PJ. Classification of chronic hepatitis: diagnosis, grading and staging. Hepatology
1994;19:151320.
[22] UICC. TNM classification of malignant tumours. 2002.
[23] Sipponen P, Stolte M. Clinical impact of routine biopsies of the gastric
antrum and body. Endoscopy 1997;29:6718.
[24] Rugge M, Cassaro M, Pennelli G, Leandro G, Di Mario F, Farinati F.
Atrophic gastritis: pathology and endoscopy in the reversibility assessment. Gut 2003;52:13878.
[25] Guido M, Rugge M. Liver biopsy sampling in chronic viral hepatitis.
Semin Liver Dis 2004;24:8997.
[26] Genta R. Gastritis on the stage. Adv Anat Pathol 2007;14:233.
[27] Ruiz B, Garay J, Correa P, Fontham ET, Bravo JC, Bravo LE, et al.
Morphometric evaluation of gastric antral atrophy: improvement after
cure of Helicobacter pylori infection. Am J Gastroenterol 2001;96:
32817.
[28] Rugge M, Correa P, Dixon MF, Fiocca R, Hattori T, Lechago
J, et al. Gastric mucosal atrophy: interobserver consistency using
new criteria for classification and grading. Aliment Pharmacol Ther
2002;16:124959.
[29] Sipponen P, Seppala K, Aarynen M, Helske T, Kettunen P. Chronic gastritis and gastroduodenal ulcer: a case control study on risk of coexisting
duodenal or gastric ulcer in patients with gastritis. Gut 1989;30:9229.
[30] Graham D. Helicobacter pylori infection in the pathogenesis of
duodenal ulcer and gastric cancer: a model. Gastroenterology
1997;113:198391.
[31] Rugge M, Kim JG, Mahachai V, Miehlke S, Pennelli G, Russo VM, et
al. OLGA gastritis staging in young adults and country-specific gastric
cancer-risk. Int J Surg Pathol, [in press].
[32] Rugge M, Meggio A, Pennelli G, Piscioli F, Giacomelli L, De Pretis G,
et al. Gastritis staging in clinical practice: the OLGA staging system.
Gut 2007;56:6316.