Journal of Pediatric Gastroenterology and Nutrition

36:217–222 © February 2003 Lippincott Williams & Wilkins, Inc., Philadelphia

Endoscopic Nodular Gastritis: An Endoscopic Indicator of

High-Grade Bacterial Colonization and Severe Gastritis in
Children With Helicobacter pylori
*Maria da Graça Soares Bahú, †Themis Reverbel da Silveira, ‡Ismael Maguilnick, and
§Jane Ulbrich-Kulczynski
*Pediatric Gastroenterology Unit, Hospital da Criança Conceição, Federal Department of Health, †Pediatric Gastroenterology
Unit and ‡Digestive Endoscopy Unit, Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, and
§Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, and Pathology Department, Hospital da
Criança Conceição, Federal Department of Health, Porto Alegre, Brazil

ABSTRACT positive predictive value (91.7%) for the diagnosis of H. pylori

Objective: To investigate the significance of endoscopic nodu-
lar gastritis associated with Helicobacter pylori infection.
Methods: This prospective study included 185 children (50.8%
boys) aged 1 to 12 years (mean, 6.9 ± 3.0 years) who underwent
upper intestinal endoscopy during evaluation of chronic ab-
dominal pain. The authors assessed the endoscopic appearance
of the stomach, noting those patients with endoscopic nodular
gastritis. Urease activity of gastric mucosal biopsies was mea-
sured. With histologic examination, the presence and density of
H. pylori organisms, the presence of follicular gastritis, the
nature of inflammation, and the gastritis activity grade and
overall gastritis score were assessed.
Results: H. pylori infection was identified in 50 children
(27%). Endoscopic nodular gastritis was significantly associ-
ated with active chronic gastritis and follicular gastritis. Nodu-
larity in the stomach showed a high specificity (98.5%) and
infection and was observed in 22 of 50 (44%) H. pylori-positive
patients and in 2 of 135 (1.5%) H. pylori-negative patients. A
significant association was observed between older age and the
prevalence of this finding (P < 0.001). There was a significant
increase in endoscopic nodular gastritis with increased H. py-
lori density and a positive correlation (Pearson coefficient ⳱
0.97) with increased gastritis score on histologic examination.
Increase in gastritis score was dependent on increased H. pylori
density in patients with gastric nodularity; this finding was
independent of age.
Conclusions: Endoscopic findings of antral nodularity in chil-
dren suggest the presence of H. pylori infection and follicular
gastritis and may identify cases of severe gastritis and marked
bacterial colonization. JPGN 36:217–222, 2003. Key Words:
Helicobacter pylori—Gastritis—Endoscopy—Abdominal
pain. © 2003 Lippincott Williams & Wilkins, Inc.

Helicobacter pylori infection is a common and uni-
versally distributed bacterial infection. It is predomi-
nantly acquired in childhood (1), and more than three
fourths of the population in developing countries is in-
fected during childhood. In developed countries, infec-
tion in children is less frequent (2). The major risk factor
for H. pylori infection is crowded living conditions (1,3–
5), but epidemiologic studies have shown that poor sani-
tation, lack of adequate water supply, and a low educa-
Received April 11, 2002; accepted September 30, 2002.
Supported in part by Coordenação de Aperfeiçoamento de Pessoal de
Ensino Superior (CAPES), Brazil.
Technical support was provided by the Graduate Program in Gas-
troenterology, Universidade Federal do Rio Grande do Sul, and the
Graduate Research Group, Hospital de Clínicas de Porto Alegre, Brazil.
Address correspondence and reprint requests to Maria da Graça
Soares Bahú, Ildefonso Simões Lopes, 201/02, 91330–180 Porto
Alegre, RS, Brazil (e-mail: mgbahu@uol.com.br).
tional level of the head of the family are also important
risk factors for infection (5,6).
H. pylori infection has fulfilled Koch postulates (7)
and met Hill criteria for being a cause of active chronic
gastritis (8). It is the most frequent cause of chronic
gastritis and peptic ulcer, and is directly associated with
gastric carcinoma and mucosa-associated lymphoid tis-
sue (MALT) lymphoma (1).
The inflammation that H. pylori causes in the gastric
mucosa is not always observed macroscopically with en-
doscopy, but it is identified on the histologic examination
of gastric biopsies (9–11). Endoscopic findings of nodu-
larity can be seen in the stomach of children much more
frequently than in adults. This nodularity, more often
observed in the gastric antrum, has been called antral
nodular gastritis (also, nodular antritis or gastric lympho-
nodular hyperplasia) (10,12–17). Some authors (12,13,

217
218 M. da GRAÇA SOARES BAHÚ ET AL.

18) believe that this macroscopic change may predict H.

pylori infection and histologic gastritis. Other authors,
however, still question the specificity of endoscopic
nodular gastritis for H. pylori infection (19).
We performed a cross-sectional study of children with
chronic abdominal pain to investigate the association of
H. pylori infection with endoscopic nodular gastritis and
histologic features of gastritis.

MATERIALS AND METHODS

Patients and Samples

One hundred eighty-five children (50.8% boys) aged 1 to 12

years (mean, 6.9 ± 3.0 years) were included in this prospective
study performed from 1997 to 1999 in two hospitals in Porto
Alegre, Brazil. All the children came from low-income fami-
lies, and the level of education of their parents was low. They
all presented with chronic abdominal pain and were referred for
upper intestinal endoscopy. Only the children whose parents
gave informed consent participated in the study. Exclusion cri-
teria were contraindication for endoscopy; use of antibiotics,
bismuth, H2 blockers, or proton pump inhibitors within 30 days FIG. 1. Nodularity seen in the gastric antrum during endoscopic
of the procedure; and use of antiinflammatory drugs or acetyl- examination.
salicylic acid (ASA) within 3 days of the procedure. Patients
taking immunosuppressive agents or chemotherapy drugs were
Histologic Examination
excluded, as were patients with immunodeficiency or suspected
celiac disease. Four age groups were established: 1 to 3 years
One of the authors (J.U.K.), blinded to the patients’ endo-
(35 patients), 4 to 6 years (58 patients), 7 to 9 years (48 pa-
scopic or clinical findings, examined the biopsies (stained with
tients), and 10 to 12 years (44 patients).
hematoxylin and eosin, and Giemsa) for H. pylori and gastritis.
Endoscopy was performed by one of the authors (M.G.S.B.).
H. pylori infection was characterized by bacteria found with
An Olympus GIF 130 videoendoscope (outer diameter ⳱ 9.5
mm; biopsy channel diameter ⳱ 2.8 mm) was used combined
with EVIS CV 100 video processor and FB-25K biopsy for-
ceps. Five gastric biopsy specimens were collected from each
patient for histologic analysis: two from the gastric antrum (one
from the distal lesser curvature and one from the distal greater
curvature), two from the corpus (one from the lesser curvature
and one from the greater curvature), and one from the area next
to the incisura angularis. Histologic examination followed the
Sydney System criteria as updated in Houston in 1994 (20).
Specimens were placed directly in 10% formalin without a
paper filter. A sixth specimen from the gastric antrum was
collected for the urease rapid test (21). This section was em-
bedded in GASTROtest gel (Santa Cruz do Sul, Brazil), which
consists of a small portion of modified Christensen urea agar
and a pH indicator.

Endoscopic Diagnosis

The diagnosis of endoscopic nodular gastritis was made

when the mucosa had an irregular appearance resembling a
cobblestone pavement. Micronodules measured 1 to 4 mm in
diameter, had a smooth surface, and were the same color as the
surrounding mucosa, as described by Hassal and Dimmick (22)
in 1991 (Fig. 1). These nodules, evident with introduction of
the endoscope, were better identified after biopsy collection
because the blood from the biopsy site surrounded and high- FIG. 2. Evident nodularity seen after collection of endoscopic
lighted them (Fig. 2). biopsies.

J Pediatr Gastroenterol Nutr, Vol. 36, No. 2, February 2003

 ENDOSCOPIC NODULAR GASTRITIS IN CHILDREN 219

histologic examination, and density of organisms was rated increased H. pylori density in the gastric mucosa (Spear-
low, moderate, or high. The diagnosis of gastritis was based on man correlation coefficient, 0.58).
the histopathologic findings of inflammation, activity, metapla- The diagnostic performance of the urease test for H.
sia, and atrophy. Each of these findings was scored as normal pylori infection in 176 patients was as follows: sensitiv-
(0), mild (1), moderate (2), or marked (3) following the updated ity, 60.4%; specificity, 94.5%; positive predictive value,
Sydney System and using visual analog scales (20). The final
gastritis score was the sum of the four histopathologic scores.
80.5%; and negative predictive value, 83%.
Finally, the diagnosis of follicular gastritis was based on the Active chronic gastritis was significantly more preva-
presence of lymphoid follicles with a germinative center and a lent in patients with H. pylori infection (24 of 50; 48.0%)
mononuclear infiltrate in the lamina propria of the gastric mu- than in patients not infected (6 of 135; 4.4%); ␹2 ⳱ 47.8
cosa. (P < 0.001); PR ⳱ 10.8 (95% CI, 4.7–24.9). Prevalence
increased significantly with the increase of bacterial den-
sity; ␹2 ⳱ 84.8 (P < 0.001). Spearman correlation coef-
Ethical Considerations and Variables Studied
ficient calculated to assess the association of H. pylori
The Scientific Committee and the Health Research Ethics density and severity of gastritis with increase in age was
Committees of the Department of Research and Graduate Stud- 0.17 and 0.07, respectively.
ies at Hospital de Clínicas de Porto Alegre and Hospital Con- Endoscopic nodular gastritis was seen in 24 of 185
ceição (Porto Alegre, Brazil) approved this research project. patients (13%; 95% CI, 8.5–18.7). Of these, 58.3% were
The variables studied were demographics, endoscopic nodu- boys. An association between older age groups and the
lar gastritis, urease test findings, H. pylori infection, follicular prevalence of this finding was observed (P < 0.001;
gastritis, inflammation (mononuclear cell infiltration) and gas- Table 1). Endoscopic nodular gastritis was found in 22 of
tritis activity (polymorphonuclear cell infiltration) grades, H.
the 50 (44%) patients with H. pylori infection and in only
pylori density found with histologic examination, and gastritis
score. 2 of the 135 (1.5%) who were H. pylori negative; ␹2 ⳱
54.72 (P < 0.001); PR ⳱ 29.7 (95% CI, 7.3–121.7).
Endoscopic nodular gastritis was significantly associ-
Statistical Analysis ated with active chronic gastritis identified during histo-
logic examination (15 of 30 [50%] vs. 9 of 155 [5.8%];
Results were expressed as number and percentage. Age was
Fisher exact test: P < 0.001; PR ⳱ 8.6; 95% CI, 4.2–
described as median and range. Percentage comparisons were
assessed using the ␹2 test or Fisher exact test when appropriate. 17.8) and with follicular gastritis (12 of 24 [50.0%] vs.
We also calculated prevalence ratio (PR) and 95% confidence 12 of 161 [7.5%]; ␹2 ⳱ 29.8 [P < 0.001]; PR ⳱ 6.7;
interval (CI). Correlation coefficients (Pearson and Spearman) 95% CI, 3.4–13.2).
were used for specific comparisons involving age, H. pylori The diagnostic performance of endoscopic nodular
density, and gastritis score. Combined effects were assessed gastritis for H. pylori infection was sensitivity, 44%;
using the logistic regression model to obtain adjusted odds ratio specificity, 98.5%; positive predictive value, 91.7%; and
for the association of age, H. pylori density, and gastritis score negative predictive value, 82.5%. Table 1 shows the sig-
with gastric nodularity. Significance was set at 0.05. Data were nificant increase in endoscopic nodular gastritis inci-
processed and analyzed with SPSS version 8.0 (SPSS Inc., dence with increased H. pylori density.
Chicago, IL, U.S.A.).
Endoscopic nodular gastritis was significantly associ-
ated with higher grades of gastritis severity observed
RESULTS
TABLE 1. Prevalence of endoscopic nodular gastritis
H. pylori infection was identified in 50 (27%) of the according to age and H. pylori density
185 children (95% CI, 20.8–34.0). There were 26 boys,
and age ranged from 1.7 to 12 years (median, 8.5 years). Endoscopic nodular gastritis
Bacterial density found with histologic examination was Variable Number Frequency Percent PR 95% CI
low in 23 (46%) of the 50 infected patients, moderate in
Age group*
12 patients (24%), and high in 15 (30%). There was a 1–3 y 35 0 0 — —
significant increase in H. pylori infection in association 4–6 y 58 4 6.9 5.5 0.3–99.0
with age: ␹2 ⳱ 5.35 (P ⳱ 0.021). All 50 children in- 7–9 y 48 8 16.7 12.5 0.7–209.5
fected with H. pylori had chronic gastritis (mononuclear 10–12 y 44 12 27.3 20.0 1.2–785.2
cell infiltration) found on histologic examination. Of Total 185
H. pylori density†
these, 24 had active chronic gastritis (polymorphonuclear Absent 135 2 1.5 — —
cell infiltration). Low 23 6 26.1 17.6 3.8–82.0
With regard to gastritis severity, 12 of 50 H. pylori- Moderate 12 6 50.0 33.8 7.6–149.4
positive children had a score of 1 (24%), 9 had a score of High 15 10 66.7 45.0 10.9–186.4
2 (18%), 11 had a score of 3 (22%), 9 had a score of 4 * PR ⳱ adjusted prevalence ratio based on Agresti’s correction: 0.5;
(18%), 7 had a score of 5 (14%), and 2 had a score of 6 ␹2 for linear trend ⳱ 15.4 (P < 0.001). †PR ⳱ prevalence ratio; ␹2 for
(4%). An increase in gastritis score was observed with linear trend ⳱ 71.5 (P < 0.001).

J Pediatr Gastroenterol Nutr, Vol. 36, No. 2, February 2003

220 M. da GRAÇA SOARES BAHÚ ET AL.
during histologic examination and determined according
to gastritis score. Pearson correlation coefficient was
0.97 (P < 0.001). Figure 3 shows, according to gastritis
score, the prevalence of nodularity in the gastric antrum
during endoscopy.
The odds ratio obtained with the logistic regression
model for the association of age, H. pylori density, and
gastritis score with gastric nodularity can be seen in
Table 2. Mutual adjustments of variables showed that
increased H. pylori density and age were independently
associated with presence of gastric nodularity. Increase
in gastritis score was dependent of increased H. pylori
density and significantly associated with gastric nodular-
ity.
DISCUSSION
The children included in this study had some of the
common risk factors for H. pylori infection, such as low
family income and parental education level. Of these
patients, 27% had H. pylori infection, and infection in-
creased with age. This result is the same found in reports
by several authors (3,4,15,23).
The urease test used in this study (GASTROtest, Santa
Cruz do Sul, Brazil) is a commercial test with high speci-
ficity (94.5%) but low sensitivity (60.4%). This feature is
somewhat different than the commercial CLOtest (Delta
West Bertley, Australia), whose sensitivity is reported to
be 70% to 85% (24–26). In accordance with the medical
position statement of the North American Society for
Pediatric Gastroenterology and Nutrition, we believe that
the accuracy of the test depends mainly on the H. pylori
FIG. 3. Correlation between gastritis score found on histologic
examination and endoscopic nodular gastritis.
J Pediatr Gastroenterol Nutr, Vol. 36, No. 2, February 2003
TABLE 2. Logistic regression model representing odds
ratio for the association of age, H. pylori density, and
gastritis score with gastric nodularity
Odds ratio 95% CI P
Age 1.03 1.01–1.05 0.004
H. pylori density 3.86 1.86–8.00 <0.001
Gastritis score 1.31 0.74–2.32 0.353
density in the gastric sample, which is usually lower in
children than in adolescents and adults (10,26,27). This
difference may be the reason for the low sensitivity of
our method.
In 1982, Warren and Marshal described H. pylori in
the gastric mucosa and reported the presence of endo-
scopic nodular gastritis in positive cases (28). Later,
Czinn et al. (29) and Cadranel et al. (30) reported the
same endoscopic finding in children. Nodularity was as-
sociated with lymphoid follicles seen with histologic ex-
amination in some of their patients. More recent studies
have also reported a significant association between en-
doscopic nodular gastritis and H. pylori infection (12–
15,18,31,32).
We also found a significant association between en-
doscopic nodular gastritis and H. pylori infection (as
seen in 44% of the patients with H. pylori infection and
in only 1.5% of the patients without infection). Our re-
sults are similar to those reported by Luzza et al. (45.3%
for H. pylori-positive patients and 1.5% for H. pylori-
negative patients) and by De Giacomo et al. (43% for H.
pylori-positive patients and 4% for H. pylori-negative
patients) (14,32).
Specificity (98.5%) and positive predictive value
(91.7%) of endoscopic nodular gastritis for H. pylori
infection were high, which confirms the findings of Pri-
eto Bozano et al. (18). The association between endo-
scopic nodular gastritis and follicular gastritis was ob-
served in our study and is supported by findings de-
scribed by other authors (12,14,18). Therefore, we can
say that positive findings for endoscopic nodular gastritis
point to a high probability of H. pylori infection because
the positive predictive value is high (27.0%) at low
prevalence rates of the disease. However, the absence of
nodularity in the gastric mucosa on histologic examina-
tion does not exclude the possibility of H. pylori infec-
tion.
Low bacterial density in the gastric mucosa and either
absent or moderate inflammatory response are common
histopathologic findings in children with H. pylori infec-
tion (10,33). In 70% of our children with H. pylori in-
fection, bacteria density ranged from low to moderate.
We noted, however, that a higher degree of bacterial
colonization in the gastric mucosa was associated with
endoscopic nodular gastritis. In 1993, Eidt and Stolte
(34) studied an adult sample and noted that a higher
number of lymphoid follicles were observed in the antral
mucosa with the increase in H. pylori colonization den-
 ENDOSCOPIC NODULAR GASTRITIS IN CHILDREN
sity. In our study, despite the low number of patients
with endoscopic nodular gastritis associated with differ-
ent degrees of H. pylori density, which determined high
CI in the statistical evaluation, our results still suggest
the presence of a strong association between both find-
ings. This finding was also recently demonstrated by
Luzza et al. (35).
Endoscopic nodular gastritis is not observed in all pa-
tients with H. pylori infection. Nodularity is probably
related to the density of H. pylori at the beginning of
infection, so that a large inoculum triggers an exagger-
ated immune response, as already suggested by Mitchell
et al. (13). The initial infection occurs more frequently
during childhood, and endoscopic nodular gastritis also
occurs more frequently in children than in adults.
H. pylori gastritis is usually less active and intense in
children than in adults (14). However, we demonstrated
that endoscopic nodular gastritis is not only associated
with active chronic gastritis but also shows a significant
correlation with gastritis severity (Pearson correlation
coefficient ⳱ 0.97). Studies with adult samples have
investigated the relation between follicular gastritis and
gastritis severity and have reported a significant correla-
tion between the presence of lymphoid follicles in the
gastric mucosa and the grade and severity of gastritis
(34,36,37).
Luzza et al. (32,35) also observed a higher gastritis
score in children with antral nodularity independent of
age. Those authors showed that gastritis score signifi-
cantly increased with age, but they did not find a signifi-
cant age-related increase in antral nodularity. Although
we observed a significant increase in endoscopic nodular
gastritis with increased age, we had few cases of nodu-
larity in younger children, which limited our statistical
conclusions. Therefore, this finding should be further
investigated. The correlation of H. pylori density and
gastritis severity with increasing age was insignificant or
very low. These results, in association with those of the
logistic regression model, suggest that the effects of H.
pylori density and increased gastritis score on gastric
nodularity are independent of age. In addition, our study
suggests that the increase in gastritis score with gastric
nodularity depends on the increase in H. pylori density in
the gastric mucosa.
Our study establishes the importance of antral nodu-
larity finding during endoscopic examination of children.
This finding is associated with H. pylori infection and
follicular gastritis, and it may identify patients in whom
gastritis is more severe and associated with marked bac-
terial colonization independent of age.
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