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O RI G I N A L A RT I CL E

In French Children, Primary Gastritis Is More FrequentThan Helicobacter pylori Gastritis

N. Kalach S. Papadopoulos E. Asmar C. SpyckerelleP. Gosset J. Raymond E. Dehecq A. Decoster C. Creusy C. Dupont

Received: 14 May 2008 / Accepted: 16 September 2008 / Published online: 12 November 2008

Springer Science+Business Media, LLC 2008

Abstract The aim of this study was to analyze the his-

tological characteristics according to the updated Sydneyclassification (intensity of gastritis, degree of activity,

gastric atrophy, intestinal metaplasia, and Helicobacter

pylori) in symptomatic children referred for upper gastro-

intestinal endoscopy. A 4-year retrospective descriptive

study was carried out in 619 children (282 females and 337

males), median age 3.75 years (15 days to 17.3 years)

referred for endoscopy. Six gastric biopsies were done

(three antrum and three corpus) for histological analysis

(n = 4), direct examination and H. pylori culture (n = 2).

H. pyloristatus was considered positive if at least two out

of three tests were positive and negative if all three tests

were negative. The results showed that only 66 children

(10.66%) were H. pylori positive. Histological antral and

corpus gastritis was detected in, respectively, 53.95% and59.12% of all cases, most of them of mild grade 1. Antral

and corpus activity was grade 1 in 18.57% and 20.03% of

cases.H. pylori-positive versusH. pylori-negative children

did differ in terms of moderate and marked histological

gastritis and grade 2 or 3 activities. One girl had moderate

gastric atrophy and another one moderate intestinal meta-

plasia, both being H. pylori negative. The findings indicate

that primary antrum and corpus gastritis is 5.3 and 6.9

times, respectively, more frequent than H. pylori gastritis

in French children, with usually mild histological gastritis

and activity. Gastric atrophy and intestinal metaplasia are

rare.

Keywords Helicobacter pylori Children Gastritis

Activity Primary Gastric atrophy Intestinal metaplasia

Sydney classification

Introduction

The updated Sydney classification is now well established

as the most appropriate for the precise description of his-

tological gastric biopsy specimens [1]. In children,

prevalence of histological chronic gastric inflammation

varies from 75% to 100% [25]. The majority of authors of

pediatric studies reported histological gastritis in all cases

of Helicobacter pylori infection [3, 68]. However, some

cases of infection without microscopic lesions were also

reported [4, 9]. H. pylori infection is found in most prim-

itive gastritis in adults, whereas it was observed in only

60% of pediatric gastritis [7,9]. This difference, potentially

linked to lower infection prevalence in children, also

reflects the probable existence of other causes of gastritis,

N. Kalach (&) E. Asmar C. Spyckerelle

Department of Pediatrics, Saint Antoine Paediatric Clinic,

Saint Vincent de Paul Hospital, Catholic University of Lille,

P.O. Box 387, Bd de Belfort, 59020 Lille Cedex, France

e-mail: [email protected]

N. Kalach C. Dupont

Department of Pediatrics, Neonatalogy Cochin-Saint Vincent de

Paul Hospital, University Paris Descartes, Paris, France

S. Papadopoulos P. Gosset C. Creusy

Department of Pathology, Saint Vincent de Paul Hospital,

Catholic University of Lille, Lille Cedex, France

J. Raymond

Department of Microbiology, Cochin-Saint Vincent de Paul

Hospital, University Paris Descartes, Paris, France

E. Dehecq A. Decoster

Department of Microbiology, Saint Philibert Hospital,

Catholic University of Lille, Lille Cedex, France

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Dig Dis Sci (2009) 54:19581965

DOI 10.1007/s10620-008-0553-y


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which could be masked in adults by the strong incidence of

subjects carryingH. pylori. The detection of primary antral

gastritis (PAG) in about 20% of children with recurrent

abdominal pain (RAP) [10], and the discovery of other

types of germs in the mucous membrane of some subjects

with gastritis, could support this assumption [11]. The low

concentration of germs on the surface of the mucous

membrane related to the recent character of the infection inthe child could also explain the high histological rate of

gastric inflammation without H. pylori isolation [9].

Mucosal atrophy and intestinal metaplasia of the stom-

ach are frequently found in gastric biopsy specimens of

adults infected with H. pylori [12]. However, ifH. pylori

infection is frequently acquired during childhood, its role in

gastric atrophy and intestinal metaplasia has not been

extensively searched for and described [13].

The purpose of this study was to analyze the charac-

teristics and parallelism of clinical, endoscopic, and

histological features according to the updated Sydney

classification [1] in symptomatic children referred to apediatric gastroenterology clinic with clinical symptoms

leading to upper gastrointestinal (GI) endoscopy and

biopsy.

Patients and Methods

Patients

A retrospective descriptive study was carried out in the

pediatric department of Saint Vincent de Paul Hospital,

Lille, France. This study enrolled all children: (1) referred

for upper GI endoscopy between January 2001 and

December 2004 in the course of diagnostic and etiologic

assessment of clinical gastritis, i.e., the association of one

or more symptom or sign of those digestive manifestations:

RAP (at least three episodes of abdominal pain per week

during the last 3 months), gastro-oesophageal reflux

(GER), vomiting, occult or macroscopic digestive hemor-

rhages, failure to thrive, or other digestive demonstrations

of gastritis, anorexia, malaise, dysphasia; (2) whose

endoscopy included gastric biopsy specimens. Children

were excluded from analysis if they had received antibi-

otics, anti-H2, or proton pump inhibitors (PPIs),

nonsteroidal anti-inflammatory drugs (NSAID) 4 weeks

before endoscopy or if there was presence of chronic

organic diseases, i.e., cystic fibrosis, metabolic diseases,

inflammatory bowel diseases, celiac disease, diabetes

mellitus, etc. Ethnic origin of children was identified by

mothers country of birth, i.e., Caucasian for Europe, or

non-Caucasian for Middle East or Africa. In accordance

with good clinical practice, written consent was obtained

from all parents before endoscopy.

Endoscopy, Gastric Biopsy, and Histological Analysis

Endoscopic lesions were recorded as follows: for esopha-

gus, normal, inflammatory esophagitis (grade I), ulcerative

esophagitis (grade II), mycotic esophagitis, endobrachy-

esophagus, and esophageal varices; for gastric lesions,

normal, gastritis (congestive, nodular, and erosive) and

ulcer; for bulbar lesions, normal, bulbitis (congestive,nodular, atrophic), and bulbar ulcer; for duodenal lesions,

normal, duodenitis (congestive, nodular, atrophic), and

duodenal ulcer.

Biopsies were performed in both gastric antrum (n = 3)

and corpus (n = 3). Two antral and two corpus specimens

were formalin fixed and paraffin embedded, and hema-

toxylin and eosin stains were used for histopathologic

analysis according to updated Sydney classification [1].

The amounts of inflammation, activity, atrophy, meta-

plasia, and H. pylori were established by the visual analog

scale given in the updated Sydney classification [1].

Inflammation

Intensity of histological gastric inflammation, i.e., histo-

logical gastritis, was estimated according to mononuclear

cells and lymphocytes, i.e., absent (grade 0), few (1, mild),

moderate number (2, moderate), or high number (3,

marked).

Activity

Degree of activity, i.e., histological active gastritis, was

estimated according to neutrophils infiltration, i.e., absent

(grade 0), few (1, mild), moderate number (2, moderate), or

high number (3, marked).

Gastric Glandular Atrophy and Intestinal Metaplasia

Gastric glandular atrophy and intestinal metaplasia were

assessed as absent (grade 0), mild (1), moderate (2), or

marked (3).

Helicobacter pylori

Intensity of infection with H. pylori was classified as

Gram-negative bacillus absent (grade 0), mild or rare (1),

moderate (2), or marked (3).

Further histological analysis was done by recording

presence or absence of follicular gastritis.

H. pylori Status: Direct Examination and Culture

One antral and one corpus gastric biopsy specimens were

placed in a tube of sterile physiological saline solution,

Dig Dis Sci (2009) 54:19581965 1959

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transported to the laboratory of bacteriology, maintained at

4C, then quickly dealt with. The bacteriological exami-

nation included direct examination of the totality of a first

biopsy specimen with the use of Gram staining at 1% in a

concentrate of carbolfuschin (RAI, Paris, France). The

biopsies were put thereafter in culture in 0.5 ml meat-liver

suspension (Pasteur, Paris, France), homogenized by

Griffith tube and cultivated on chocolate gelose (Bio-Merieux, Paris, France) then incubated with 37C in

microaerophilic conditions (5% O2, 10% CO2, 85% N2)

during 7 days. The presence of small, round, convex col-

onies with strong urease activity, oxidasic, catalasic,

gamma glutamyl transferasic, and alkaline phosphatasic

with a negative nitrate reductase reaction (API, Bio-Mer-

ieux, Paris, France) enabled confirmation of diagnosis of

H. pylori infection.

The results of the histological analysis, bacterial culture,

and direct examination of the gastric biopsy specimens

were carried out in a blind way, without knowing the

results of any other examination. A positive result ofH. pyloriinfection was recorded when culture was positive

or when at least two out of three tests were positive. A

negative result was recorded when all three tests were

concomitantly negative.

Statistical Treatment

This is a descriptive study; StatView software (Abacus,

CA, USA) was used for calculation of quantitative

parameters: mean, median, standard deviation (SD), and

range. Difference between the qualitative parameters was

calculated by using v2 test. Analysis of variance (ANOVA)

was also used for the crossing of qualitative and quantita-

tive parameters. P values \0.05 were considered

significant.

Results

Population and Endoscopic Findings

During the study period, only 619 children met the inclu-

sion criteria: 282 girls and 337 boys, with mean age

5.29 5.12 years (median 3.75 years, range 1 month to

17.75 years), with the age distribution displayed in Fig. 1.

The clinical purpose of endoscopy was RAP (51.3%)

children, GER (23.9%), vomiting (10.1%), failure to thrive

(6.7%), digestive hemorrhage (4.3%), and miscellaneous

(4.3%) (Table1).

Endoscopic aspects were: normal (62.6%), congestion

(28.2%), nodular (6.9%) or erosive gastritis (1.6%). Only

three children had gastric ulcer and two bulbar ulcers

(Table2).

Histological Analysis (Table3)

Inflammation

Histological gastritis was detected in 53.95% antrum and in

59.12% corpus samples, mostly mild (grade 1). Children

with moderate (grade 2) histological gastritis were signif-

icantly older than those with grade 1 (P\ 0.02).

Activity

Histological active gastritis of grade 1 was detected in

18.57% antrum and corpus 20.03%. Children with an

active histological antro-corpus gastritis were significantly

older than those without active histological gastritis

(P\ 0.007).

Follicular Gastritis

Follicular gastritis was found in only 25 children (1.4%).

Gastric atrophy occurred in only one 13-year-old girl

who had suffered from GER since infancy. Following

persistence of recurrent epigastric pain and pyrosis, upper

digestive endoscopy highlighted presence of severe con-

gestive gastro-bulbitis. Antro-corpus biopsy specimens

evidenced H. pylori-negative moderate histological active

gastritis, associated with antral gastric atrophy. Following

3-month PPI treatment, she became completely asymp-

tomatic, and control endoscopic within 3 months showed

complete cure of all lesions.

Intestinal metaplasia occurred in a 15-year-old girl who

had suffered from GER since infancy. Also, following

Fig. 1 Distribution of the age scales and antral and corpus histologic

inflammation of enrolled children

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persistence of recurrent epigastric pain and pyrosis, upper

digestive endoscopy showed severe congestive gastro-

bulbitis with erosive prepyloric lesions. Antro-corpus

biopsy specimens evidenced H. pylori-negative moderate

histological active gastritis, and low-grade intestinal

metaplasia located inside the cryptic antral epithelium.

Following 3-month PPI treatment, she became completely

asymptomatic and control endoscopic also showed disap-pearance of all lesions.

H. pylori Status

Only 66 out of 619 children (10.66%) were H. pylori

positive (Table4). All grade 2 and 3 H. pylori biopsy

specimens were concomitantly positive for bacterial cul-

ture and direct examination. In patients with grade 1

H. pylori, positive bacterial culture and direct examination

were seen in only one child in the antrum and two children

in the corpus (Table 4). H. pylori-positive children (antro-

corpus) were significantly older than H. pylori-negative

ones (7.4 4.75 years versus 5 5.1 years, P 0.0003).

Similarly, grade 3 H. pylori children were significantly

older than those with grades 2 and 1 (P\ 0.05).

Correlations of Histological, Clinical Manifestations,

Endoscopic Findings, and H. pylori Status

Caucasians (516, 83.3%) were significantly less infected

than non-Caucasians (Table1).

Most clinical manifestations were significantly associ-

ated with H. pylori-negative status, but RAP was

significantly more frequent with H. pylori (Table1). The

318 children with RAP exhibited significant antral and

corpus gastric inflammation [190 (59.75%) and 184

(57.86%), respectively; P\ 0.005 versus those without

histological antral and corpus inflammation] (Table1).

However, children with RAP had a mild prevalence ofhistological antral and corpus gastric activity: 94/318

children with RAP (29.55%) versus 224/318 (70.45%)

children without gastric activity (P\ 0.0001). The other

clinical manifestations were not associated with any spe-

cific histological features.

Antral histological gastritis and activity were signifi-

cantly higher in H. pylori-positive versus H. pylori-

negative children: 80.3 versus 50.8% and 71.2 versus

19.8% (P\ 0.001).

At endoscopy, H. pylori-negative children exhibited

significantly higher levels of normal esophageal, gastric,

and bulbo-duodenal mucosa than H. pylori-positive chil-

dren. Grade I and II oesophagitis, congestive, and erosive

gastritis were significantly more frequently detected in

H. pylori-negative children. Surprisingly, nodular gastritis

was detected in 60.46% of H. pylori-positive versus in

39.54% H. pylori-negative children (not significant, ns).

On the other hand, nodular gastritis was only detected in

17/553 H. pylori-negative children (3%) versus 26/66 of

H. pylori-positive children (39.3%) (P\ 0.0001). Gastric

ulcers were seen in only three H. pylori-negative children,

Table 1 Clinical features, histological inflammation, and ethnic origin according toH. pylori status

Clinical features H. pylori

positive

H. pylori

negative

H. pylori

positive

H. pylori

positive

H. pylori

negative

H. pylori

negative

66 (10.66)

n (%)

553 (89.34)

n (%)

Antral

inflammation

n (%)

Corpus

inflammation

n (%)

Antral

inflammation

n (%)

Corpus

inflammation

n (%)

RAP, n = 318 46 (14.46) 272 (85.63)* 38 (82.6)** 33 (71.7)** 152 (55.8) 151 (55.3)

GER, n = 148 6 (4.05) 142 (95.95)* 5 (83.3) 5 (83.3) 61 (42.9) 86 (60.5)

Vomiting,n = 63 6 (9.52) 57 (90.48)* 5 (83.3) 6 (100) 28 (49.1) 28 (49.1)

Failure to thrive,n = 42 3 (7.69) 39 (92.31)* 3 (100) 1 (33.3) 22 (56.4) 24 (61.5)

Digestive hemorrhages,n = 27 4 (14.81) 23 (85.79)* 3 (75) 2 (50) 10 (43.4) 15 (65.2)

Miscellaneous,n = 21 1 (4.77) 20 (95.23)** 0 0 9 (45) 17 (85%)

Ethnic origins

Caucasian,n = 516 42 (8.14) 474 (91.86)*

Non-Caucasian (Middle east

or Africa), n = 103

24 (23.31)* 79 (76.69)

* P \ 0.0001 according to the v2-test

** P 0.01 according to the v2-test

P 0.01 according to the v2

-test, in children with RAP,H. pylori positive (46/66, 69.69%) versusH. pylori negative (272/553, 49.18%) P 0.01 according to thev2-test, in children from the Middle east and Africa,H. pyloripositive (24/66, 36.36%) versusH. pylorinegative (79/

553, 14.28%)

Dig Dis Sci (2009) 54:19581965 1961

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and bulbar ulcers in one H. pylori-positive child and one

H. pylori-negative child (Table2). Antro-corpus histolog-

ical inflammation was seen in 68.57% of children with

congestive gastritis and in 86.4% of those with nodular

gastritis. Comparatively, antro-corpus histological activity

was detected in only 31.15% and 43.49%, respectively.

Finally, none of the other endoscopic aspects exhibited

any significant difference of histological gastritis or

activity.

Low grades (mild) of gastric inflammation and activity

were both associated with H. pylori-negative status. Fol-

licular gastritis in antrum and corpus was significantly

associated with H. pylori positivity (Table3). Children

with antro-corpus histological follicular gastritis were sig-

nificantly older (9.75 4.5 years versus 5.1 4.9 years,

P\ 0.0001).

Discussion

This study suggests that, in children referred with symp-

toms of clinical gastritis, endoscopy reveals that primary

mild-grade histological gastritis is frequent, amounting to

53% in the antrum and 59% in the corpus, that H. pylori

infection is infrequent, detected in only 10.6% of cases,and that histological gastritis appears largely unrelated to

H. pylori infection. In addition, both gastric atrophy and

intestinal metaplasia are rare.

The population evaluated in this study was characterized

by symptoms of clinical gastritis represented mainly by

RAP, GER, and vomiting, usually leading to upper GI

endoscopy according to the recommendation of the North

American Society of Pediatric Gastroenterology, Hepatol-

ogy, and Nutrition (NASPGHAN) [5,14, 15], so that it is

Table 2 Endoscopical lesions according toH. pylori status

H. pylori

positive

H. pylori

negative

66 (10.66)

n (%)

553 (89.34)

n (%)

Esophagus

Normal esophagus,n=

414 53 (12.8) 361 (87.2)*Inflammatory oesophagitis

(grade I),n = 180

10 (5.55) 170 (94.45)*

Ulcerative oesophagitis

(grade II),n = 23

2 (8.7) 21 (91.3)**

Mycotic oesophagitis,n = 2 1 (50) 1 (50)

Endobrachy-esophagus,n = 1 0 1 (100)

Oesophageal varices,n = 1 0 1 (100)

Stomach

Normal stomach,n = 388 22 (5.68) 366 (94.32)*

Congestive gastritis,n = 175 17 (9.72) 158 (90.28)*

Nodular gastritis,n = 43 26 (60.46) 17 (39.54)

Erosive gastritis,n = 10 1 (10) 9 (90)

Gastric ulcer, n = 3 0 3 (100)

Bulb

Normal bulb,n = 557 54 (9.69) 503 (90.31)*

Congestive bulbitis,n = 26 3 (11.53) 23 (88.47)*

Nodular bulbitis,n = 22 6 (27.27) 16 (72.73)

Atrophic bulbitis,n = 12 2 (16.66) 10 (83.34)

Bulbar ulcer,n = 2 1 (50) 1 (50)

Duodenum

Normal duodenum,n = 614 65 (10.58) 549 (89.42)*

Congestive duodenitis,n = 3 1 (33.33) 2 (66.67)

Nodular duodenitis,n = 2 0 2 (100)


** P 0.002 according to the v2-test P 0.04 according to the v2-test P 0.05 according to the v2-test

Table 3 Gastric histological features according toH. pylori status

H. pylori

positive

H. pylori

negative

66 (10.66)

n (%)

553 (89.34)

n (%)

Antrum

InflammationAbsence of inflammation,

n = 285

13 (4.57) 272 (95.43)*

Grade 1,n = 278 18 (6.48) 260 (93.52)*

Grade 2,n = 47 28 (59.57) 19 (40.43)

Grade 3,n = 9 7 (77.77) 2 (22.23)

Activity

Absence of activity,n = 462 19 (4.12) 443 (95.88)*

Grade 1,n = 115 24 (20.87) 91 (79.13)*

Grade 2,n = 42 23 (54.76) 19 (45.24)

Corpus

Inflammation

Absence of inflammation,n = 253 20 (7.91) 233 (92.09)*Grade 1,n = 309 16 (5.18) 293 (94.82)*

Grade 2,n = 55 28 (50.9) 27 (49.1)

Grade 3,n = 2 2 (100) 0

Activity

Absence of activity,n = 454 26 (5.73) 428 (94.27)*

Grade 1,n = 124 21 (17) 103 (83)*

Grade 2,n = 41 19 (46.34) 22 (53.66)

Antrum and corpus

Follicular gastritis

Absence of follicular

gastritis,n = 596

43 (7.22) 553 (92.78)*

Presence of folliculargastritis,n = 25

23 (92)* 2 (8)

Note: One girl presented withH. pylori-negative mild gastric atrophy

and another one withH. pylori-negative mild intestinal metaplasia


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likely to encompass any type of disease affecting the upper

digestive tract, especially gastritis in its different aspects.

Endoscopy showed normality or congestion in more than

90% of cases. Nodular gastritis, the aspect most clearly

related to H. pylori infection, found in up to 53% of cases

[3,16,17], was seen in only 60.46%. Nodular gastritis is not

absolutely specific ofH. pylori infection and nodular gas-

tritis cases withoutH. pylorihave already been reported [3,

17,18].Helicobacter heilmanniiinfection may be involved;

it is usually large and very distinctive when seen in histo-

pathologic sections, and thus should have been reported by

the pathologists reviewing these cases [19]. However,

probably in a considerable number of cases, nonspecific

antibiotic treatments for other nonspecific infections used

previous to endoscopy could decrease the concentration of

the bacteria on mucous membrane surfaces, hence leading

to false-negative results. In our study, surprisingly, nodular

gastritis was not significantly associated with H. pylori

even though all enrolled children had been free of any

antibiotics, anti-H2 or PPI use for at least the preceding

4 weeks, and the search forH. heilmanniiinfection was also

negative. Furthermore, this nodular endoscopic aspect

could have been related to former H. pyloriinfection, since

this endoscopic feature persists a long time after proper

eradication of the bug and the only way to decide would

have been by using an immunoblot H. pylori diagnostic

tool. Interestingly, expressing the endoscopic features in

relation to the 66 H. pylori-positive or 553 H. pylori-neg-

ative children shows that nodular gastritis is not as frequent

in our population: 39.3% versus 3% of cases, respectively.

Besides, also that normal stomach feature is present in 33%

of H. pylori-positive and in 66% of H. pylori-negative

children. Furthermore, H. pylori-negative children exhib-

ited significantly higher levels of normal esophageal,gastric, and bulbo-duodenal mucosa thanH. pylori-positive

children. These endoscopic findings could probably be due

to a certain patient selection bias.

Peptic ulcer in childhood is exceptional and H. pylori

gastritis without peptic ulcer is frequent in children. In a

previous study, one gastric and two duodenal ulcers were

found in 47 children with H. pylori infection [3]. Further-

more, in a recent prospective European multicenter pilot

study on the incidence in children of gastric and duodenal

ulcer disease or erosions, ulcers occurred in 10.6% of

cases, withH. pyloriinfection in only 26.7% of these [20].

In agreement with these previous data, only 1 out of 66H. pylori-positive children exhibited bulbar ulcer.

Antral and corpus histological gastritis were found in

53.95% and 59.12% of cases and most were H. pylori

negative. In previous pediatric studies, prevalence of his-

tological chronic gastric inflammation varied from 75% to

100% [25]. The lowest prevalence of chronic gastritis was

reported by American pediatric series: 32% for Elitsur

et al. [21] and 26.31% for Mahony et al. [22]. Chronic

gastritis occurs in boys as well as in girls [ 4, 10]. Fur-

thermore, the frequency of gastritis increases in correlation

with age [5, 14, 21], in agreement with our results. The

classical aspect of chronic active gastritis commonly

observed in adults, characterized by prevalence of poly-

nuclear neutrophils in the inflammatory infiltrate, is rarer in

children [7, 23,24], also in agreement with our study.

Chronic follicular gastritis was suggested to be specific

toH. pylori infection [1,2,10]. Chronic follicular gastritis

corresponds to a diffuse and polymorphic inflammatory

infiltrate comprising a very high number of lymphoid fol-

licles in a gastric mucosa [1]. Those data are in agreement

with our study since follicular gastritis was significantly

more frequent in the antrum and corpus of H. pylori-

positive children.

In adults, gastric glandular atrophy and/or intestinal

metaplasia are frequently associated with H. pylori infec-

tion and both are considered preneoplastic lesions [12,13].

This relationship is still controversial in the pediatric

population and the incidence of gastric atrophy and/or

intestinal metaplasia is not consistent among published

studies [2, 13, 2430]. The absence of consistence rela-

tionship between H. pylori infection and gastric glandular

atrophy and/or intestinal metaplasia in the reported pedi-

atric studies is might be due to the fact that H. pylori

Table 4 The results of histology, bacterial culture, and direct

examination according toH. pylori status

H. pylori

positive

H. pylori

negative

66 (10.66)

n (%)

553 (89.34)

n (%)

Histology

H. pylori (antrum)

Absence ofH. pylori, n = 511 4 (0.78) 507 (99.22)*

Grade 1,n = 47 1 (2.12) 46 (97.88)*

Grade 2,n = 30 30 (100) 0

Grade 3,n = 31 31 (100) 0

H. pylori (corpus)

Absence ofH. pylori, n = 507 14 (2.76) 493 (97.24)*

Grade 1,n = 56 2 (3.57) 54 (96.43)*

Grade 2,n = 30 30 (100) 0

Grade 3,n = 26 26 (100) 0

Bacterial culture

Negative,n = 553 0 553 (100)Positive,n = 66 66 (100) 0

Direct examination

Negative,n = 553 0 553 (100)

Positive,n = 66 66 (100) 0

* P \ 0.0001 according to v2-test

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serology was not performed to define if there was past

infection [2, 13, 2430]. In fact, diagnosis of gastric

glandular atrophy as well as intestinal metaplasia in chil-

dren is very difficult because it requires an adequate

number of properly oriented gastric biopsy specimens;

furthermore, those lesions have a patchy gastric distribu-

tion. Finally, interobserver agreement is poor, especially in

the assessment of atrophy. At present gastric glandularatrophy and intestinal metaplasia criteria in children are not

established and are urgently needed [27,30].

In Tunisia, Maherzi et al. [2] reported a frequency of

gastric atrophy in 25.38% of children, always associated

with H. pylori. In the USA, Guarner et al. [13] reported

gastric atrophy and/or intestinal metaplasia in 12 of 19

(63%) children infected with H. pylori, gastric atrophy

alone being observed in eight, intestinal metaplasia alone

in two, and both in two. In Turkey, Usta et al. [27] reported

gastric atrophy and/or intestinal metaplasia in only 5/175

H. pylori-positive children (2.8%), atrophy alone in three,

intestinal metaplasia in one, and both lesions in one. Thoseresults contrast with those of another Turkish study

showing glandular atrophy and/or intestinal metaplasia in

14 of 18 (77.7%) H. pylori-positive children [28]. Other

researchers did not observe any atrophic gastritis in chil-

dren [2426]. Finally in France, Blain-Stregloff et al. [29]

reported a frequency of gastric atrophy in 5% of cases and

Trinh et al. [31] in only one case, in close agreement with

our data.

Intestinal metaplasia is rare in children. It is the conse-

quence of prolonged H. pylori infection and its prevalence

increases with time [32]. Shabib et al. [33], comparing two

groups of children with H. pylori-positive gastritis versus

H. pylori-negative gastritis, reported a frequency of intes-

tinal metaplasia, respectively, in 42% and 6% of cases. On

the other hand, Blain-Stregloff et al. [29] reported only one

case (0.3%) of intestinal metaplasia, whereas Ilboudo et al.

[25] and Chong et al. [26] did not observe any cases.

This study shows only 10.66% of children with

H. pylori infection, in good agreement with the study

carried out by Wizla-Derambure et al. [34] with the pur-

pose of identifying familial and community environmental

risk factors associated with H. pylori infection in a pedi-

atric population requiring diagnostic upper endoscopy

during a 2-year period. The authors included 436 patients

(242 boys), aged 2 days to 17.9 years (median 2.7 years),

and H. pylori was present in 7.3% [34].

The low incidence ofH. pylori infection in our popu-

lation contrasts with a high level of H. pylori-negative

histological gastritis, up to almost two out of three cases.

For Hessey et al. [35], absence ofH. pyloriduring gastritis

could be related to the local inflammatory answer itself,

which in certain cases would lead to elimination of the

germ in contact with the mucous membrane, hence

transient persisting histological gastritis. According to

another hypothesis, histologic gastritis could be related to

infection by other H. pylori species not detected by con-

ventional methods, i.e., histology and culture. Further

molecular analysis of the gastric biopsy specimens could

be helpful [36].

The exact relationship between H. pylori infection and

macroscopic and histologic gastritis still remains uneluci-dated. In a previous study [37], we found an extremely high

prevalence of macroscopic and histologic gastritis (71.7%)

in noninfected children [37]. This highly selected popula-

tion of children with epigastric pain was actually close to

that depicted by Snyder et al. [10], where PAG was found

in about 20% of the four different age groups of 408

children, with only 4/39 children\10 years old with PAG

having evidence of H. pylori infection. Trinh et al. [31]

compared prospectively two groups of children, one with a

histological gastritis and the other one with a normal his-

tology, with no significant difference between the two

groups with regard to existence of digestive symptoms. Inour study, RAP was significantly but only slightly higher in

H. pylori-positive children. Furthermore, children with

RAP were significantly associated with H. pylori-negative

nonactive antro-corpus histological gastritis.

Conclusion

H. pylori infection was rare in this systematic analysis of

endoscopic features in children with clinical gastritis, but

associated with (1) a high level of mild-grade histological

antro-corpus primary gastritis and activity and (2) a sig-

nificantly higher rate of follicular in gastric antrum and

corpus. Intensity and activity of histological gastritis both

increased with age. Nodular and congestive gastritis were

associated with nonactive histological gastritis. Gastric

atrophy and intestinal metaplasia seem rare in children.

RAP were more frequent in case of H. pylori infection.

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