GASTROENTEROLOGY 1992;102:355-359
Grading and Classification of Chronic
Gastritis: One American Response to the
Sydney System
PELAYO CORREA and JOHN H. YARDLEY
Department of Pathology, Louisiana State University Medical Center, New Orleans, Louisiana; and
Department of Pathology, The Johns Hopkins University School of Medicine, Baltimore, Maryland
A new classification of chronic gastritis coined the
Sydney system has been proposed as a “flexible
matrix of rules.“‘* The system claims that “the recog-
nition that Helicobacter pylori is the major cause of
chronic inflammation of the human gastric mucosa
has in part solved this problem”. As is often the case,
the enthusiasm over new medical findings may have
led to overinterpretation. Chronic gastritis is a multi-
factorial disease, and its biological characteristics are
stil1 poorly understood. H. pylori is undoubtedly an
important etiologic factor but not the only one.
The purpose of this article is to give the reader our
reasons for believing that the Sydney system has ma-
jor flaws in regard to both its underlying premises
about the nature of chronic gastritis and in its ap-
proach to classifying these disorders. Furthermore,
we believe that those flaws are so serious that they
could have a detrimental effect on progress in under-
standing chronic gastritis if the Sydney system be-
comes widely accepted. We have necessarily given
our contrasting views about gastritis by reference to
terminology and approaches previously reported by
one of US,~but our primary purpose is not mere advo-
cacy of one particular system. We fee1 strongly that
understanding of chronic gastritis, spurred by recent
exciting discoveries, continues to evolve and that its
evolution should not be impeded by accepting ques-
tionable inferences on etiopathogenesis and by pre-
mature attempts to establish a universal system of
classification.
The Sydney System
The Sydney system recommends that the
diagnosis of gastritis be made by integration of infor-
mation on its etiology, histopathology, and endos-
copy, as shown in Figure 1. It further recommends
that the same grading categories (mild, moderate,
and severe) be used for histological and endoscopic
variables without considering the poor record of in-
terobserver reproducibility of such exercises. The
system assumes that al1 forms of chronic gastritis are
one nosologic entity, with the exception of forms
with a specific etiology. It further assumes that it is a
progressive disease in which al1 types of advanced
lesions, regardless of topography or morphology, are
sequentia1 events of common precursors and sug-
gests H. pylori (apparently in isolation from other eti-
ologic factors) as the cause of the condition.
The Sydney system proposes that “the micro-
scopic details of the gastritis are documented in the
main body of the pathologist’s report by a series of
SUFFIX phrases, the major variables being graded
using a common uniform scale. In the conclusion,
the topographic summary phrase is PREFIXED, if
sufficient data are available, by the etiology or by the
most likely etiologic association.“’ This amounts to a
grading scheme for each main area of the mucosa
(antrum and corpus) prefixed by an etiologic opin-
ion. A system of grading histological parameters by
topography could indeed be the basis for a classifica-
tion but is not in itself a classification, defined as a
categorization of nosologic entities. The Sydney sys-
tem recommends “a minimum of two biopsies from
the anterior and posterior walls of the antrum and
corpus” (ignoring the incisura). It thus ignores that in
the multifocal atrophic gastritis (MAG) nosologic
complex, the earliest and most advanced lesions are
usually found in and around the incisura. The sys-
tem creates new problems for the pathologists by un-
wisely stating that “attempts to orient biopsies are
unnecessary.”
The endoscopic component proposes that edema,
erythema, friability, exudate, erosions, hyperrugos-
ity, fold atrophy, visibility of vascular pattern, bleed-
ing spots, and granularity be graded and used to clas-
sify the gastritis. The present critique addresses
mostly the etiology and pathological aspects of the
Sydney system, but we cannot avoid expressing dis-
agreement with implying a correlation between
pathological and endoscopic findings in chronic gas-
tritis. The limited potential of endoscopy in classify-
ing gastritis has been noted by many authors.
The Sydney system is accompanied by a summary
0 1992 by the American Gastroenterological Association
0016-5085/92/$3.00
356 CORREA AND YARDLEY GASTROENTEROLOGY Vol. 102. No. 1

ETIOLOGY TOPOGRAPHY MORPHOLOGY

(prefix) (core) (suffix)

TOPOGRAPHY
Pangastritis
Gastritis Gastritis
ACUTE GASTRITIS
- Inflammation of antrum of corpus
CHRONIC GASTRITIS
SPECIAL FORMS
- Activity
ETIOLOGY
+
- Atrophy Descriptive terms
GRADED
Pangastritis
VARIABLES
Intestinal
PATHOGENIC
metaplasia Edema
ASSOCIATIONS Rugal hyperplasia
Erythema Rugal atrophy
Helicobacter Friability Visibility of vascular
pylori Exudate pattern
Flat erosion Intramural bleeding
Raised erosion spots
Nodularity

NONGRADED
Gastritis Gastritis
of antrum of corpus
VARIABLES
I I Categories of endoscopic gastritis
I

P Specific

Figure 1. The Sydney system. Severity grading: none, mild, moderate, and severe.

review of some of the classifications available and Two Types ofAtrophic Gastritis
some comments on the epidemiology and natura1 his-
Al1 major publications recognize the exis-
tory of gastritis. The latter is mostly based in the Fin-
tence of two types of atrophic gastritis characterized
nish system of grading (not classifying) gastritis.4 To
by gland loss and intestinal metaplasia. First recog-
provide a perspective of the developments that have
nized was the type associated with the pernicieus
led to the present state of confusion, a different view
anemia syndrome, limited to the oxyntic mucosa,
of such developments is hereby offered, followed by
and not usually associated with gastric ulcer but
comments on how they conflict with the Sydney
linked to a higher risk of gastric carcinoma originat-
system.
ing in the previously metaplastic corpus mucosa. It
Scope of Classification Problems has received a variety of names: gastric atrophy,g
body atrophy,” type A,” diffuse atrophic gastritis,”
The present dilemma concerns only the most
and diffuse corpora1 atrophic gastritis (DCG).3 It is
common types of chronic gastritis, sometimes called
also referred to as autoimmune gastritis.13,14 Table 1
nonspecific. There is no important controversy
about the specific forms of gastritis. These refer to
well-defined entities such as sarcoidosis, tuberculo-
sis, and eosinophilic gastritis. Recently, two new spe- Table 1. Morphological Classification of Chronic Gastritis
cific forms of gastritis have been recognized: lympho- Not atrophic
cytic gastritis, which may be related to intestinal Superficial (SG)
malabsorption syndromes,5*6 and reflux gastritis, orig- Diffuse antral [DAG)
inally described in postgastrectomy specimens and Atrophic
Diffuse corpora1 (DCG)
recently linked to nonsteroidal antiinflammatory
Multifocal (MAG)
drugs and other “chemical” injuries.“’
January 1992 GRADING AND CLASSIFICATION OF CHRONIC GASTRITIS 357

summarizes the classification previously proposed
by one of usa3 Classic DCG, as the pernicieus anemia
syndrome, is characteristic of populations of Scan-
dinavian and northern European extraction and is
either absent or extremely rare in other groups.
The second type of atrophic gastritis has histori-
cally created much confusion. It was called multifo-
cal atrophic by Lambert in 197Z1’ and type B by
Strickland and Mackay in 197X*’ The choice of the
name type B turned out to be unfortunate because it
has been frequently misused to describe gastritis
without atrophy (not considered in the Strickland
and Mackay article confined to atrophic types of gas-
tritis) or gastritis of bacterial (B) etiology.14 Its topo-
graphic distribution has been extensively studied in
its “pure” form in populations in which pernicieus
anemia is not present. Its multifocal pattern has been
excellently illustrated by Stemmermann and Haya-
shi15 who used special stains to locate the foei of in-
testinal metaplasia in gastrectomy specimens from
Japanese patients. Its multifocal nature and its age-
dependency was shown in a study of over 1500 au-
topsy specimens of Colombian patients,16 as seen in
Table 2 which includes topographic distribution of
1113 foei of metaplasia found in 435 specimens. It is
clear that the focal lesions in which metaplasia is
accompanied by chronic inflammatory infiltrate are
more prevalent and appear earlier in the middle and
lower lesser curvature (around the incisura) and
spread to other areas with age.
The classification problems have arisen mostly in
studies of populations in which both the pernicieus
anemia syndrome and MAG are frequent. There is
no reason why a subject with a genotype associated
with the pernicieus anemia syndrome, exposed to
the environment that leads to MAG, should not de-
velop both types of atrophic gastritis. Detailed stud-
ies of the dynamics of the gastritis have been pub-
lished, especially by the Finnish group of Siurala et
al. and Kekki et a1.4,‘7Their grading system clearly
describes the dynamics of progression of atrophy of
the corpus (a feature shared by DCG and MAG) and
atrophy of the antrum (an exclusive feature of MAG).
The problem arises when such a grading system is
adopted as a classification, which the Sydney system
does, thereby melding two diseases into one. Siurala
et a1.4present their contribution as a system for grad-
ing, not for classifying atrophic gastritis. They refer
to DCG as pernicieus anemia type and to MAG as the
genera1 population type. However, they present a
controversial speculation implying that the two dis-
eases are one and the same when they state that “it is
possible that the only essential differente between
the pernicieus anemia type and the gastritis prevail-
ing in the genera1 population is the dynamics, i.e., in
the speed of progression of the body gastritis. . . .”
Had they had experience with populations free of
pernicieus anemia, they would probably have come
to a different conclusion. Glass and Pitchumoni” rec-
ognized the coincidence of the two types of atrophic
gastritis. They proposed the name type AB- (with
negative parietal cel1 antibodies) corresponding to
MAG. The type they cal1 AB+ (with parietal cel1 anti-
bodies) probably corresponds to subjects with the
two diseases, i.e., DCG responsible for the parietal
cel1 antibodies and MAG, the only disease known to
lead to atrophy of the antrum.
Two Types of Peptic Ulcers
The second major source of confusion comes
from the fact that for many years gastric and duo-
denal peptic ulcers were considered as one nosologic
entity. This led to the notion that the gastritis asso-
ciated with each localization was part of the same
disease complex. It seems clear now that the two
peptic ulcers are different disease entities. Gastric
ulcer is accompanied by MAG, whereas duodenal
ulcer is accompanied by diffuse antral (not atrophic)
gastritis (DAG). Ulcers of the pyloric Channel behave
as duodenal ulcers in this regard.‘g~20 The existente
of DAG has been recognized by many investigators,
although different names or descriptions have been
used. Diffuse antral gastritis involves diffusely the
full thickness of the mucosa exclusively in the an-
trum and is characterized by a dense lymphoplas-

Table 2. Distribution of Independent Foei ofïntestinal Metaplasia in Stomachs of Colombian Subjects

Location of lesions

No. of Lesser curvature Greater curvature

specimens No. of
Age (yrl with lesions lesions Cardia Upper Medium Lower Medium Fundus

0-14 9 15 2 (2.2) 1 (1.1) 2 (2.2) 8 (88.9) 1 (1.1) 1 (1.1)

15-34 100 171 13 (13.0) 20 (20.0) 41 (41.0) 76 (76.0) 16 (16.0) 5 (5.0)
35-54 125 313 31 (24.8) 52 (41.6) 78 (62.4) 94 (75.2) 40 (32.0) 18 (14.4)
55+ 201 614 71 (35.3) 101 (50.2) 148 (73.6) 165 (82.1) 94 (46.7) 35 (17.4)
Total 435 1113 117 174 269 343 151 59

NOTE. Parentheses show percentage positive for each site.

358 CORREA AND YARDLEY
mocytic infiltrate. Gland loss (atrophy) and intestinal
metaplasia are not part of DAG. However, as in the
previous example, occasionally DAG and MAG coin-
cide in the same patient.
The evidente for DAG as an independent noso-
logie entity is mostly epidemiological; it is the pre-
dominant form of chronic gastritis in children and
young adults, it predominates in affluent urbanized
populations, it is specifically associated with duo-
denal or pyloric ulcers, and it does not lead to atro-
phy (gland loss), intestinal metaplasia, dysplasia, or
gastric carcinoma. Present evidente strongly sug-
gests that infection with H. pylori may be the chief
cause of DAG, probably triggered by precipitating
factors so far poorly understood.
Gastric ulcer, on the other hand, is part of the
MAG disease complex, multifocal in the antrum and
corpus and associated with atrophy and intestinal
metaplasia.lg It is associated with an increased risk of
gastric carcinoma.” Schindler” recognized the dif-
ferences in the gastritis of the two types of ulcer
when he stated: “In gastric ulcer often atrophic
changes are found. These are almost always missing
in duodenal ulcer, in which hypertrophic gastric
mucosal thickness predominates.” He notes that
these findings were previously reported by Stempien
et al. in 1953. The endoscopic “hypertrophy” of the
antrum of duodenal ulcer patients led to the endo-
scopic classification of DAG as hypertrophic gastritis,
which has been subsequently abandoned.” A totally
different entity, hypertrophy of the oxyntic mucosa
(without inflammation) is seen in the Zollinger-Elli-
son and related syndromes. H. pylori is frequently
found in MAG, but its prevalente varies markedly
between populations from approximately 100% in
populations at high gastric cancer risk to somewhere
between 50% and 70% in populations at lower gas-
tric cancer risk.23
Superficial Gastritis
A final point of confusion relates to the term
superficial gastritis, described as an inflammatory
infiltrate localized to the superficial portions of the
gastric mucosa.3~‘2~21~24 Superficial is therefore a term
to describe the topographic distribution of the infil-
trate. The problem arose when some investigators
stated that when the infiltrate penetrated to the full
thickness of the mucosa, the gastritis became “atro-
phic.” Atrophy of course has nothing to do with the
depth of the infiltrate. It has been used to imply
gland loss since the times of Magnus.” The trend to
confuse topography of infiltrate with loss of glands
apparently began as a result of attempts to correlate
endoscopic and histopathologie findings21*25but has
been unfortunately adopted in more recent publica-
GASTROENTEROLOGY Vol. 102, No. 1
tions. There is no scientific evidente that infiltrate
of the full thickness of the mucosa is a cause or a
consequente of gland 10ss.~~*~’ The confusion might
have been an attempt to fill the vacuum created by
the lack of a name for DAG, which was frequently
observed by many pathologists but not recognized as
a disease entity. Attempts to fill the vacuum led to a
proposal to cal1 preatrophic gastritis those cases with
“reduction of the parenchyma and extension of the
inflammatory infiltrate into the deepest areas.”
Pseudoatrophic would be a more appropriate term
for this morphological expression of DAG, because
the apparent reduction of the parenchyma does not
represent gland loss but separation of glands to ac-
commodate the dense infiltrate in the lamina pro-
pria.
Problems of the Sydney System
As described above, the main misconceptions
and misunderstandings about chronic gastritis have
been identified and are slowly being clarified. This
trend, however, may be reversed by the Sydney sys-
tem for the following reasons: (a) it confuses the need
for a system of grading and reporting (useful to assess
the degree and topography of specific histological
changes) with the need for a classification (a system-
atic arrangement of nosologic entities); (b) it pre-
serves unproven assumptions of past attempts to
classify the disease entities, especially the notion
that al1 forms of chronic gastritis are part of a contin-
uum of progressive changes, from leucocytic infil-
trate to gland loss and metaplasia; and (c) it ignores
the wel1 known interpopulation variations in the
distribution of the types of gastritis and tries to im-
pose the present-day European experience on the
rest of the world.
Conclusion
1. To clarify the present confusion, grading systems
have to be recognized as different from classifica-
tions.
2. There is abundant evidente that there are two
separate entities associated with gastric atrophy
(gland loss frequently associated with intestinal
metaplasia). One is diffuse, localized to the oxyn-
tic mucosa, and part of the pernicieus anemia
syndrome; the other is multifocal in the antrum
and corpus and is the predominant type in non-
Scandinavian populations at high gastric cancer
risk. Both types cover more extensive area of the
mucosa with age.
3. There is abundant evidente that the duodenal
and pyloric peptic ulcers are accompanied by a
chronic gastritis limited to the antrum, character-
ized by a diffuse, dense, and deep lymphoplasmo-
January 1992 GRADING
cytic infiltrate, and almost universally associated
with severe infection by H. pylori. There is no
scientific evidente that it leads to atrophy, meta-
plasia, or carcinoma. Diffuse antral gastritis is
completely reversible after treatment; such re-
versibility has not been shown for MAG.
4. In some individuals, two types of gastritis may
coexist. This is especially the case with MAG,
which may coexist with corpora1 atrophic gastri-
tis of the pernicieus anemia type or with the DAG
of the type seen in duodenal ulcers.
5. The disease entities have been wel1 recognized,
but the names given to them by different investi-
gators are multiple and confusing.
6. Much is known about the biology of chronic gas-
tritis, and the chief problems are those of nomen-
clature (semantics) and classification. In our opin-
ion, the Sydney system has conceptual flaws that
may perpetuate outmoded views and fail to help
in the clarification of the present state of confu-
sion. Further joint efforts among pathologists and
other specialists wil1 be needed before a satisfac-
tory and generally accepted system for classifying
chronic gastritis can be achieved.
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Received November 2, 1990. Accepted March 15, 1991.
Address requests for reprints to: Pelayo Correa, M.D., Depart-
ment of Pathology, Louisiana State University Medical Center,
1901 Perdido Street, New Orleans, Louisiana 70112.