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Chronic Gastritis Associated with

Helicobacter pylori in Mexican Children:
Histopathological Patterns

Article in Pediatric and Developmental Pathology · January 2010

DOI: 10.2350/09-12-0754-OA.1 · Source: PubMed

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Pediatric and Developmental Pathology 14, 93–98, 2011
DOI: 10.2350/09-12-0754-OA.1
ª 2011 Society for Pediatric Pathology

Chronic Gastritis Associated with Helicobacter

pylori in Mexican Children: Histopathological
Patterns
YOLANDA JARAMILLO-RODRÍGUEZ,1* JESÚS NARES-CISNEROS,2 VERÓNICA ARACELI MARTÍNEZ-ORDAZ,3
VÍCTOR MANUEL VELASCO-RODRÍGUEZ,3 FRANCISCO CARLOS LÓPEZ MÁRQUEZ,4
1
AND LUIS ENRIQUE MANRÍQUEZ-COVARRUBIAS
1
Department of General Pathology, General Hospital No. 16, Mexican Institute of Social Security (IMSS), Torreon, Coahuila, Mexico
2
Department of Pediatric Gastroenterology and Nutrition, Medical High Specialty Unit (UMAE) No. 71, IMSS, Torreon, Coahuila, Mexico
3
Clinical Epidemiology Research Unit, Medical High Specialty Unit (UMAE) No. 71, IMSS, Torreon, Coahuila, Mexico
4
Biomedic Research Center, School of Medicine, Universidad Autonoma de Coahuila, Torreon, Coahuila, Mexico

Received December 15, 2009; accepted July 21, 2010; published online July 26, 2010.

ABSTRACT children in diverse study populations to provide localized

The objective of this study was to analyze the
histopathological patterns of inflammation, distribution,
severity, and degree of gastric mucosa of Helicobacter
pylori (Hp)–infected children in Northern Mexico, as well
as the correlation between colonization density and
inflammation intensity. We carried out a cross-sectional
study of gastric biopsies performed on children ranging
from 2 to 17 years of age who underwent upper
gastrointestinal endoscopy for diverse gastroduodenal
disorders. This study includes only children who were
found to be Hp carriers, with positive results for tests of
Hp antigens in feces and in gastric biopsy studies. We
studied 107 patients (age 8.2 6 3.7 years). In 47.7% of
patients, the density of Hp colonization was low; only
21.5% had a marked density. Mononuclear leukocyte
infiltration showed a similar distribution. Thirty-seven
percent of patients had follicular gastritis. An acute
inflammatory response was absent in 65% and mild in
20.6% of patients. When inflammation was present, it was
primarily located in the antrum (79%). There were no
cases of intestinal metaplasia or atrophy. A link was
found between Hp density and age, infiltration by
mononuclear cells, the presence of follicular gastritis,
and the level of neutrophil infiltration (P 5 0.001).
Despite the high rates of Hp infection in the region, the
histopathological findings in these children were mild and
were limited primarily to the antral mucosa. These data
indicate the need to study the behavior of this disease in
This work was performed at the Department of General Pathology, General
Hospital No. 16 and at the Department of Pediatric Gastroenterology and
Nutrition of UMAE No. 71, Mexican Institute of Social Security (IMSS)
Torreon, Coahuila, Mexico.
*Corresponding author, e-mail: yolandaj@prodigy.net.mx
prevention and treatment strategies.
Key words: children, gastritis, Helicobacter pylori,
histopathological patterns, Mexico
INTRODUCTION
Helicobacter pylori is the main microbial agent
responsible for gastritis, peptic ulcer, gastric adenocar-
cinoma, and MALT lymphomas. Helicobacter pylori
infection tends to be acquired during the 1st 5 years of
life, and the bacteria are present in the gastric mucosa
of 50% of the world’s population [1,2]. In developed
countries, less than 10% of children are infected, while
in developing countries, such as Mexico, the rate of
infection is directly proportional to age: 20% are
already infected at 1 year of age, 24.5% by the age of
4 years, and 65% when they reach adolescence [3]. This
statistic is relevant because early H. pylori infection is
associated with a high risk for the development of
gastric cancer [4,5]. Helicobacter pylori colonization of
the gastric mucosa induces a variable inflammatory
response according to the virulence of the germ, the
immunological response of the host, and the age of the
patient. The histopathological changes secondary to the
infectious process of H. pylori are well defined in
adults, but the findings are less conclusive in children.
In adults, the presence of the bacteria in the gastric
mucosa produces acute and chronic inflammatory
responses of variable intensity. In a small proportion
of cases, more severe lesions, such as metaplasia and
intestinal atrophy, considered factors for gastric neopla-
sia, develop. In general, children experience less
inflammation than adults, and they tend to display an
inflammatory process the intensity and type of which
vary depending on the child’s geographic location [4,6–
12]. This fact generates questions that emphasize the
need for studying the behavior of this disease in
children of different populations, which will help in
the development of local prevention and treatment
strategies.
The aim of this study was to evaluate the histopath-
ological patterns of inflammation in the gastric mucosa in
H. pylori–infected children from northern Mexico. The
distribution, severity, and degree of inflammation, as well
as the correlation between the intensity of the inflamma-
tory process and the density of H. pylori, were also
assessed.
MATERIALS AND METHODS
Gastric mucosa biopsies were collected from H. pylori–
infected children living in the north-central region of
Mexico who receive health care from the Mexican
Institute of Social Security in Torreon, Coahuila, Mexico.
Patients
The study population comprised 107 children, ranging in
age from 2 to 17 years, who underwent upper gastroin-
testinal endoscopy and biopsy of the gastric mucosa for
diverse gastroduodenal disorders, such as recurrent
chronic abdominal pain, dyspepsia, recurrent vomiting,
and gastritis. Patients’ parents or legal guardians con-
sented to their children’s participation in the study, which
was previously approved by the ethics and research
committees of the participating medical units. Gastric
mucosal biopsies were collected, and H. pylori–antigen
determination studies of fecal matter were conducted with
immunochromatography using monoclonal antibodies
(ImmunoCard STAT HpSA, Meridian Diagnostics, Cin-
cinnati, OH, USA). The inclusion criteria sought out
children with a positive test for H. pylori–antigen
detection in fecal matter (HpSA) and for whom the
presence of H. pylori had been confirmed in the gastric
biopsy by special stains.
Patients who received treatment with amoxicillin,
ampicillin, clarithromycin, H2 receptor antagonists,
proton-pump inhibitors, bismuth, antiparasitics, anti-
inflammatory drugs, or steroids in the 4 weeks before
the study as well as carriers of any other gastrointestinal
diseases were not included.
Endoscopy and biopsies
Endoscopies were performed using an 8-mm Olympus GIF
XPE endoscope (Los Angeles, CA, USA). Biopsies were
collected from areas determined by a standardized
protocol, which consisted of a sample from the incisura
angularis, 2 antral samples taken 2 cm away from the
pylorus (one from the distal portion of the minor curvature
and the other from the distal portion of the major
curvature), and 2 gastric body samples. The samples were
identified separately and placed in diluted formaldehyde.
94 Y. JARAMILLO-RODRÍGUEZ ET AL.
Histological study
The biopsy samples were embedded in paraffin, and serial
5-mm-thick sections were obtained for histological
examination. Sections were stained with hematoxylin
and eosin and Giemsa and also with Alcian Blue (pH 2.5)–
periodic acid–Schiff to determine the presence of
intestinal metaplasia. The analysis was carried out in
duplicate. In each of the samples (5 per patient) the
following variables were analyzed: chronic inflammation
(the presence of mononuclear cells), activity and severity
of gastritis (infiltration by neutrophils), lesion localiza-
tion, glandular atrophy, intestinal metaplasia, and number
of H. pylori bacteria. The ordinal variables were graded
from absent to marked, following the visual analog scale
of the Sydney system. The severity of these lesions was
classified according to the degree of infiltration and the
density of H. pylori colonization in a sample of the most
severe lesion in each patient.
Statistical analysis
A Kappa test was done to analyze the concordance
coefficient between the 2 pathologists who participated in
the study. We used chi-square test and the Fisher test for
nominal variables and the Mann-Whitney U-test for the
comparison of ordinal variables. The Student t-test and
the Wilcoxon test were used to determine differences of
means, and Spearman’s r and Pearson’s r were used for
the correlation of variables. We considered a P value of
,0.05 to be meaningful (using SPSS version 15.0, SPSS,
Chicago, IL, USA).
RESULTS
We studied 107 patients, aged 2 to 17 (8.2 6 3.7) years,
with a slight predominance of males (58%). Approxi-
mately half of the patients had mild H. pylori colonization
density, and only 21.5% (n 5 23) displayed abundant
density and showed a correlation between this density and
the intensity of mononuclear leukocyte infiltration
(Spearman’s r 5 0.977, P , 0.0001; Table 1).
The neutrophil inflammatory infiltrate was present in
34.6% (n 5 37) of the cases and showed less correlation
with the density of H. pylori colonization than with the
mononuclear leukocyte infiltration (Spearman’s r 5
0.387, P , 0.0001; Table 2). The proportion of cases
with acute inflammatory activity increased with age,
exhibiting a statistically significant correlation (Spear-
man’s r 5 0.947, P , 0.001; not shown in tables).
Seventy percent (n 5 75) of the subjects were 6 to
13 years of age. Both H. pylori colonization density and
mononuclear leukocyte infiltrates increased according to
age (Spearman’s r 5 0.723 and 0.739, respectively, P ,
0.001; Table 3).
Follicular gastritis was present in 37% (n 5 40) of
the patients. Out of all the cases in the study, these
patients showed the greatest H. pylori colonization
density (P , 0.001) and were the oldest (P , 0.001):
83% (n 5 15) of subjects fell between the ages of 14 to
Table 1. Correlation between Helicobacter pylori (Hp) colonization density and mononuclear infiltration severity
Hp colonization density
Sydney classification Mild Moderate Abundant Total %
Mononuclear infiltration
Mild 50 0 0 50 46.7
Moderate 1 32 1 34 31.8
Abundant 0 1 22 23 21.5
Total 51 33 23 107
% 47.6 30.8 20.6

Spearman’s r 5 .977; P , 0.0001.

Table 2. Correlation between Helicobacter pylori (Hp) colonization density and neutrophil infiltration severity
Hp colonization density
Sydney classification Absent Mild Moderate Abundant Total %
Neutrophil infiltration
Absent 0 44 13 13 70 65.4
Mild 0 7 12 3 22 20.6
Moderate 0 0 8 7 15 14.0
Abundant 0 0 0 0 0 0
Total 0 51 33 22 107
% 0 47.6 30.8 20.6

Spearman’s r 5 .387; P , 0.0001.

17 years and only 7.1% (n 5 1) between the ages of 2 to
5 years (Table 4).
In patients with follicular gastritis, there was a
stronger correlation between H. pylori colonization
density and higher levels of mononuclear infiltrate than
between H. pylori colonization density and neutrophil
infiltrates (Fig. 1).
With regard to the inflammatory process, both the
follicular and the nonfollicular infiltrates were more
frequently found in the antrum (among 79% of patients, n
5 85). Pangastritis was found in 19 subjects, mostly
children over 14 years of age (P , 0.001) (Table 5).
There were no cases of intestinal metaplasia or atrophy.
DISCUSSION
Helicobacter pylori infection affects children worldwide.
In developing countries, the rates of infection in children
by this bacterium are greater than those observed in
children of industrialized countries [6,11,13–15]. Helico-
bacter pylori infection prevalence rates in Mexican
children and adults have been published previously
[3,16]. An earlier study [9]—which included the same
patients as the present study—reported a prevalence rate
of 71.3% in symptomatic children. Similar rates has been
reported by other Mexican authors [3,5]. They found H.
pylori–associated infection in 66% of an asymptomatic
population of all ages. Among children, the infection rate
increases directly with age, from 24.5% in children
younger than 4 years of age to 65% in adolescents [3].
Differences in prevalence rates between our study and
other Mexican studies are partially due to the age of the
patients selected and the techniques used for diagnosis of
H. pylori.
The presence of H. pylori in the gastric mucosa
produces an inflammatory response of variable intensity;
while a predominance of cells respond with chronic
inflammation, in some cases, no inflammation is found
[4,5,8,12,17–22].
There is a consensus in the literature with respect to
the intensity of the inflammatory response. As in our
population, most reports confirm that children show
smaller degrees of inflammatory intensity compared with
adults, and this pattern is associated with the density of
colonization by H. pylori. Children who come from
populations with a high risk of gastric cancer show
greater degrees of gastric mucosal damage, a smaller
capacity to regenerate damaged epithelium, and a greater
density of H. pylori [4]. However, children such as the
ones in this study, who come from populations with a low
risk for gastric cancer, show mild mononuclear and
neutrophil infiltration, despite high rates of H. pylori
infection (greater than 50%) [5]. The intensity of the
inflammatory response caused by neutrophil leukocytes
and H. pylori density was mostly mild and was limited to
the antrum. The presence of neutrophil infiltration has
been associated with a person’s recent acquisition of H.
pylori infection. The intensity of the inflammatory

HELICOBACTER PYLORI IN MEXICAN CHILDREN 95

Table 3. Comparison of Helicobacter pylori (Hp)
colonization density and degree of mononuclear
infiltration among age groups
Colonization Mononuclear
Sydney density of Hp infiltration
classification n % n %
2–5 years
Absent 0 0
Mild 12 12
Moderate 2 2
Abundant 0 0 0 0
Total 14 14
6–9 years Figure 1. Relationship between Helicobacter pylori (Hp)
Absent 0 0 colonization density and the percentage of patients with
follicular gastritis and higher levels of mononuclear and
Mild 33 32
neutrophil leukocyte.
Moderate 8 10
Abundant 1 2.4 0 0
Total 42 42 This study and that of Munoz and colleagues [5]
found that the quantity of infiltration increased with age.
10–13 years
Both studies found a correlation between age and the
Absent 0 0
Mild 6 6
presence of chronic and acute inflammatory responses to
Moderate 18 18 infection. Teenagers had a statistically significant greater
Abundant 9 27.3 9 27.3 frequency of both acute and chronic inflammation and
Total 33 33 follicular gastritis. As Kato and colleagues [20] and Luzza
14–17 years and colleagues [21] point out, follicular gastritis is
Absent 0 0
associated with the intensity of the chronic inflammatory
Mild 0 0 response and likely with the time of exposure to the
Moderate 5 4 bacteria.
Abundant 13 72.2a 14 77.7a With regard to the complications of H. pylori
Total 18 18 infection, findings of intestinal metaplasia and atrophy
in children may be regarded as controversial. The criteria
a
Patient percentage in the abundant category by age group. for detecting these complications are not clearly defined,
which explains why the reported rates of gastric atrophy
in children vary greatly, between 0% and 72%, according
response has been associated with cag A+, but this to several studies [6–8,10,11,13,21,23–30]. Dimitrov and
association has not been found consistently [13,14]. With Gottrand [29] reported that atrophic gastritis and
the exception of studies from Colombia and Japan [4,15], intestinal metaplasia affect all histological degrees of
other publications—those by Gottrand and colleagues inflammatory activity.
[16], Elitsur and colleagues [17], Whitney and colleagues Kato and colleagues [30] reported the presence of
[18], and Campbell and colleagues [19], in their atrophy in the antrum in 10.7% of cases and in the gastric
respective study populations—have reported that the body in 4.3% of cases in a population of Japanese
presence of H. pylori in the gastric mucosa is accompa- children. Kato and colleagues [20] analyzed 131 children;
nied by either acute and chronic inflammatory processes of these, 15 showed grade 2 or 3 atrophic gastritis, most
of mild to moderate intensity or no response at all. of whom were girls and among whom the average age
However, the aforementioned populations possessed was 12.1 years. Concerning atrophic gastritis, we did not
lower infection rates (20% and 50%) than the one in this find any cases with this disease, and our findings were
study. The mild intensity of the inflammatory response similar to those obtained in other parts of the world. In
occurs despite variations in the prevalence of H. pylori France, Kalach and colleagues [7] studied 619 gastric
infection among different ethnic groups and geographic biopsies in children, finding atrophy in one patient and
regions. intestinal metaplasia in another. Both cases were negative
In Columbia, Bedoya and colleagues [4] found a high for H. pylori. Usta and colleagues [31] analyzed 175
H. pylori infection prevalence linked to an intense patients with H. pylori and reported atrophy in 2.8% of
inflammatory response. The current study showed a the cases.
significant difference between its study populations and Intestinal metaplasia is infrequent in children. Only
the one in Colombia. The inflammatory response reported Ricuarte and colleagues [15], in his comparative work of
in Colombia was greater than that reported in Mexico, children in Colombia and Korea, found intestinal
perhaps as a result of more virulent H. pylori strains. metaplasia in 4 of the 173 children studied (0.04%), with

96 Y. JARAMILLO-RODRÍGUEZ ET AL.
Table 4. Follicular gastritis in relation to age and Helicobacter pylori (Hp) colonization density
Follicular gastritis Nonfollicular gastritis
Hp colonization density Hp colonization density
Age (years) Mild Moderate Abundant Total % Mild Moderate Abundant Total
2–5 0 1 0 1 7.14 12 1 0 13
6–9 3 2 0 5 11.9 30 6 1 37
10–13 1 11 7 19 57.57 5 7 2 14
14–17 0 2 13 15 83.3a 0 3 0 3
Total 4 16 20 40 47 17 3
% 7.8 46.5 86.9b

a
Follicular gastritis. Patient percentage according age group. P , 0.001.
b
Follicular gastritis. Patient percentage according to Hp density colonization. P , 0.001.

Table 5. Comparison between acute inflammatory response and distribution in gastric mucosa among age
groups
Acute inflammatory response
Present Absent Gastric mucosa distribution
Age (years) n % n % Body Antrum Pan-gastritis
2–5 1 7.1 13 92.85 0 14 0
6–9 4 9.5 38 90.5 0 38 4
10–13 19 57.6 14 42.4 1 27 5
14–17 13 72.2a 5 27.8 2 6 10
Total 37 34.6 70 65.4 3 85 19b

a
Proportion of subjects with acute inflammatory response according to age groups. Chi-square P , 0.001.
b
Subjects with pan-gastritis according to age group chi-square P , 0.001.

an average age of 15 years. Kato and colleagues [20] did
not find any differences in the incidence of intestinal
metaplasia in the body and antrum among children with
and without H. pylori. We did not find any cases with this
complication.
We selected the study population by detecting H.
pylori antigen in the patients’ fecal matter through
immunochromatography using monoclonal antibodies
and determination of H. pylori in gastric biopsies. Both
tests offer high sensitivity, specificity, positive predictive
value, and negative predictive value (96%, 97%, 96%, and
97%, respectively) [32–34]. These tests allow us to
robustly determine the presence of H. pylori infection.
The low intensity of inflammatory response, low density of
colonization by H. pylori, and low acute inflammatory
response indicate that the gastric mucosa of our population
contains H. pylori with factors of a mildly virulent strain of
H. pylori. It is necessary to continue the study of these
bacteria with respect to its virulence factors.
CONCLUSIONS
Despite the high prevalence of H. pylori infection in our
study population, the intensity of the inflammatory
response was low, and no complications, such as atrophy
or intestinal metaplasia, were found. There was a
correlation between the density of H. pylori and the
intensity of the mononuclear inflammatory response. The
inflammatory response spectrum of adolescents was
similar to that of adults.
Criteria to enable the diagnosis of atrophic gastritis in
children are necessary, and further studies analyzing the
characteristics of H. pylori strains and the inflammatory
response in diverse stages of childhood must be carried
out. It is advisable that researchers continue to study the
virulence factors of the strains of H. pylori in the
population used for this study.
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