Saudi Journal of Gastroenterology

: 1999  |  Volume : 5  |  Issue : 3  |  Page : 129--133

The association between Helicobacter pylori infection and lymphoid reaction in patients suffering from dyspepsia in Bahrain

Abdul Rahman E Fakhro1, Bahaa El Din A Fateha2, Iman M Amin Farid2, Huda M Jamsheer2,  
1 Department of Surgery, Salmaniya Medical Complex and Ministry of Health, Bahrain
2 Department of Pathology, Salmaniya Medical Complex and Ministry of Health, Bahrain

Correspondence Address:
Abdul Rahman E Fakhro
Department of Surgery, Salmaniya Medical Complex, P.O. Box 12


Lymphoid reaction to Helicobacter pylori (H. pylori ) infection varies from simple aggregates to primary gastric lymphoma. This study analyzes various lymphoid reaction to H. pylori infection among 102 patients with dyspepsia in Bahrain during 1994-1995. Cases underwent gastroscopy for gastrointestinal complaints and at least four biopsies were taken from each patient. The prevalence of H. pylori among the study group was 79.4%. Males constituted 63.7%. Lymphoid reaction in the form of lymphoid follicles and lymphoid aggregates were found in 31.4% and 24.5% respectively. The Odds Ratio (OR) of developing lymphoid reaction among H. pylori infected cases, compared to non- H. pylori subjects was 20.1:1, and the relative risk (RR) was 7.13. The OR of developing lymphoid follicles among H. pylori cases compared to non-H. pylon subjects was 11:1 and the RR was 5.63.

How to cite this article:
Fakhro AE, Fateha BA, Amin Farid IM, Jamsheer HM. The association between Helicobacter pylori infection and lymphoid reaction in patients suffering from dyspepsia in Bahrain.Saudi J Gastroenterol 1999;5:129-133

How to cite this URL:
Fakhro AE, Fateha BA, Amin Farid IM, Jamsheer HM. The association between Helicobacter pylori infection and lymphoid reaction in patients suffering from dyspepsia in Bahrain. Saudi J Gastroenterol [serial online] 1999 [cited 2019 Dec 12 ];5:129-133
Available from:

Full Text

Infection with Helicobacter pylori (H, pylori) is a world-wide chronic infection with the highest incidence in developing countries. It is associated with duodenal ulcer, chronic active gastritis, gastric cancer and gastric lymphoma [1] . It can be easily identified on biopsy specimens taken at endoscopy. Eradication of the organism may have a role in the treatment of low-grade lymphoma [2] The normal gastric mucosa does not contain Mucosa-Associated Lymphoid Tissue (MALT). In 1993, a study has revealed lymphoid follicles in gastric mucosa of all patients with H. pylori infection [3],[4] . These follicles have also been found in stomachs with chronic active antral gastritis [5]

In Finland, a retrospective study has suggested that lymphocytic gastritis could be a precursor of gastric lymphoma. In their study, patients with gastric lymphoma have had a significantly increased prevalence of lymphocytic gastritis [6] . In addition, a group of scientists in Australia, have found that long-term infection of mice with H. pylori resulted in the development of low-grade B-cell gastric lymphoma [7] . On the other hand, Wotherspoon et al, have reported regression of early primary low grade B-cell gastric lymphoma of MALT type in humans after eradication of H. pylori [8] . However, another group of researchers have reported that eradication of H. pylori resulted in a slow decrease, but not disappearance, of lymphoid follicles in all patients [4] .

This study aims to identify the prevalence of H. pylori infection among dyspeptic patients attending Salmaniya Medical Complex in Bahrain and the association between H. pylori infection and MALT in the gastric mucosa.

 Patients and Methods

All 102 patients who attended the surgical clinic at Salmaniya Medical Complex in Bahrain with the diagnosis of dyspepsia and underwent gastroscopy between February 1994 and June 1995 were included in the study. Patients were clinically diagnosed as suffering from dyspepsia based on the following symptoms: nausea, vomiting, anorexia, fullness and bloating in addition to pain or discomfort [9] . At least four biopsies from the stomach antrum were taken from each patient. Two biopsies were sent for histo-pathological examination and two for bacteriological examination to detect the presence of H. pylori. For histopathology, biopsy specimens were fixed in 10% Buffered formalin and processed, embedded in paraffin and cut in sequential 5 µm sections.

The mean size of the biopsy specimen (measured on the glass slide) was 3 mm in diameter and contained between 7-14 serial sections. All sections were stained by hematoxylin-eosin. All biopsies were examined for the presence of H. pylori. An increase in lymphocytes and plasma cells in lamina propria categorizes the gastritis as chronic and the activity in the context of chronic gastritis refers to the density of neutrophil polymorphs in the lamina propria. As an arbitrary guideline infiltration involving upto 1/3 of the gastric pits and surface is designated mild; between 1/3 and 2/3 moderate and more than this as severe [10] . Lymphoid follicles were defined as an aggregate of lymphocytes with an unequivocal germinal centers [4],[11] . Lymphoid aggregates were defined as accumulation of lymphocytes without evidence of germinal centers [3],[12] . Any lymphoid aggregates seen were followed by examining all the serial sections for the presence or absence of germinal centers.

For bacteriological examination, the biopsies were put in 5 ml sterile saline and sent immediately to the microbiology lab for culture. The biopsy was divided into two pieces under sterile conditions: One piece was used for direct film and the other for culture.

Direct film: Tissues from the biopsy was rubbed over a microscopic slide. The smear was heat-fixed and stained by Gram's stain and examined for small gram-negative curved bacilli.

Culture: The biopsy was introduced into a glass grinder containing 0.5 ml of sterile normal saline, crushed, then inoculated on blood agar plates. The plates were then placed in ajar for micro-aerophilic condition using special gas envelops (Oxoid) and incubated at 37°C. Plates were later examined after 48 hours upto 5 days. Suspected colonies were examined microscopically using Gram stained films. Gram negative small curved rods were tested biochemically. Oxidase positive, urease positive, catalase positive and Hippurate hydrolysis-negative organisms were identified as H. pylori [13],[14] . A case is considered positive if histopathological and/or bacteriological examination is found positive.

The odds Ratio and Relative Risk concepts were utilized for the analysis of the risk of developing lymphoid reaction and lymphoid aggregates among H. pylori-infected patients compared to non infected subjects. Data was sorted in a 2x2 tables, where exposure to H. pylori versus development of lymphoid reaction constituted the main variables [15] . A ratio over one is considered significant.


Among the 102 cases in our series, 93 patients (91.2%) were Bahrainis and 9 (8.8%) were non Bahrainis. The age of patients in our series ranged between band 78 years. The mean age for Bahrainis was 41.1 years and for non Bahrainis 41.0 years and this predominance of males was found in all age groups except under the age of ten years. There were 81 positive H. pylori cases in the study group (79.4%) and 21 negative subjects (20.6%). 83.1% of males and 74% of the females in the study group were positive for H. pylori.

Histopathologically, 66 cases out of 102 patients (64.7%) showed evidence of chronic active gastritis, of which 65 cases (98.5%) were H. pylori positive. Mild gastritis was evidenced in 15 cases (14.7%), of which 9 cases (60%) were H. pylori positive. Three cases of duodenal ulcer were detected, all were H. pylori positive. Two cases of gastric ulcer (2.0%), one of them was H. pylori positive and 16 cases were normal, of which 3 cases (18.8%) were H. pylori positive [Table 1]. The relationship between Lymphoid Reaction and H. pylori infection is shown in [Table 2], which illustrates that 32 cases (31.4%) had lymphoid follicles in histopathology. Twenty­five cases (24.5%) had lymphoid aggregates only, while 45 cases (44.1%) had no evidence of lymphoid reaction. With regard to H. pylori-positive cases (N=81), lymphoid follicles were found in 30 cases (37.0%), lymphoid aggregates in 25 cases (30.9%), while 26 H. pylori-positive cases were negative for lymphoid reaction (32.1 %) [Figure 1] & [Figure 2].

Computation to estimate the Odds Ratio (OR) and Relative Risk (RR) illustrated that the OR of developing lymphoid reaction among H. pylori infected patients compared to non infected ones was 20.1 and the RR was 7.13:1 [Table 3]. On the other hand, the OR of developing lymphoid follicles among H. pylori-infected persons compared to non infected subjects was 11.0 and the RR was 5.63:1 [Table 4].


In the present study, the prevalence of H. pylori infection was found to be 79.4%. This composes with two previous studies from Bahrain reporting H. pylori prevalence of 75% [16] and 51% [17] among dyspeptic patients. In the present study, lymphoid follicles were present in 37% of patients with H. pylori-positive gastritis. Two previous studies demonstrated lymphoid follicles in 27.4% and 54% respectively of patients with H. pylori-positive gastritis [18],[19] . These investigators presented the hypothesis that lymphoid follicles may result from the chronic antigenic stimulation exerted by the organisms on the gastric mucosa and therefore represent the expression of a specific immune response directed against H. pylori.

Recently, a link was made between the lymphatic tissue in the gastric mucosa acquired through chronic H. pylori infection and the development of primary low-grade MALT lymphoma. In a study involving 33 patients with primary gastric low-grade MALT lymphoma associated with H. pylori gastritis, 70% of the patients showed complete regression and 12% partial regression of lymphoma, while 18% had no change after eradication of H. pylori infection [20] . Regression of MALT type lymphoma following eradication of H. pylori is suggested to be due to the recognition of H. pylori by tumor infiltrating T-cells, which in turn provides help for tumor cell proliferation [21] . This observation was previously reported in another in-vitro study which concluded that the response of tumor cells to stimulating strains of H. pylori is dependent of H. pylori specific T-cells and their products rather than the bacteria themselves [12] . Origin and evolution of lymphoid tissue in the gastric mucosa are issues of considerable interest with regard to the histogenesis of gastric lymphoma [3] When there is dense lymphoid cell infiltration of the gastric mucosa but no evidence of lymphoepithelial destruction, the differential diagnosis between reactive infiltrates due to H. pylori gastritis and early gastric low-grade lymphoma is difficult [22],[23]


1Cover TL, Blascr MJ. Helicobacter pylori infection, a paradigm for chronic mucosal inflammation: pathogenesis and implications for eradication and prevention. Adv Intern Med 1996;41:85-117.
2Curless D, Hennigan TW. Surgical aspects of Helicobacter pylori infection. Postgraduate Doctor Middle East 1994;17:214-8.
3Owen DA. Normal histology of the stomach. Am J Surg Pathol 1986;10:48-61.
4Genta RM, Hammer W, Graham DY. Gastric Lmphoid Follicles in Helicobacter pylori infection. Human Pathology 1993;24:577-83.
5Correa P. Chronic gastritis: A clinico-pathological classification. Am J Gastroenterol 1988;83:504-9.
6Miettinen A, Karttunen TJ, Alavaikko M. Lymphocytic gastritis and Helicobacter pylori infection in gastric lymphoma. Gut 19995;37(Suppl 4):471-6.
7Lee A. Helicobacter infections in laboratory animals: A model for gastric neoplasias? Ann Med 1995;27(Suppl 5):575-82.
8Wotherspoon AC, Doglioni C, Diss TC, et al. Regression of primary low-grade B cell gastric lymphoma of mucosa­associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet 1993;342:575-7.
9Schiller LR. Peptic ulcer, epidemiology, clinical manifestations and diagnosis. In Wyngaarden and Smith (Eds). Cecil Textbook of Medicine. W. B. Saunders Co. 1988;18th edition, PP696-7.
10Price AB. The Sydney system: 1-listological division. J Gastroenterol and Hepatol 1991;6:209-22.
11Edit S, Stolte M. Prevalence of lymphoid follicles and aggregates in Helicobacter pylori gastritis in antral and body mucosa.J Clin Pathol 1993;46:832-5.
12Hussell T, Isaacson PG, Crabtree JE, Spencer J. The response of cells from low grade B cell gastric lymphomas of mucosa associated lymphoid tissue to Helicobacter pylori. Lancet 1993;342:571-4.
13Cheesbrough M. Medical Laboratory Manual for Tropical Countries. Butterworth-Heinemann Ltd., Oxford. 1989:Vol II:PP42-4.
14Colle JG, Duguid JP, Frasar AG and Marnion BP. Practical Medical Microbiology-Churchill Livingstone I989;PP21-59.
15Meier P, Beach M. Biostatistics for the clinicians. In. Data Analysis for Clinical Medicine. The quantiative Approach to Patient Care in Gastroenterology, Thomas C, Chalmers, (Eds). International University Press 1988;PPI 1-13.
16Kamath R, Al Qamish J, Yousif A, Fakhro R, Johns S. Prevalence of Helicobacter pylori among dyspeptic patients in Bahrain, Bahrain Medical Bulletin 1995;17:50-52.
17Abdul Wahab AM, Bin Dayna KM, Patil DC. Helicobacter pylori association with upper gastrointestinal disease in Bahrain. Bahrain Medical Bulletin 1994;16:78-81.
18Wyatt JI. Rathbone BJ. Immune response of the gastric mucosa to compylobacter pylori. Scand J Gastroenterol 1988;23(Suppl 142):44-9.
19Stolte M, Eidt S. Lymphoid follicles in the antral mucosa: Immune response to compylobacter pylori. J Clin Pathol 1989;42:1269-71.
20Bayerdorffer E, Neubauer A, Rudolph B, et al. Regression of primary gastric lymphoma of mucosa-associated lymphoid tissue type after cure of Helicobacter pylori infection. Lancet 1995;345:1591-94.
21Hussell T, Isaacson PG, Crabtree JE, Spencer J. Helicobacter pylori specific tumor-infiltrating T-cells provide contract dependent help for the growth of malignant B cells in low grade gastric lymphoma of mucosa associated lymphoid tissue. J Pathol 1996;178(Suppl 2):122-7.
22Stole M, Eidt S. The diagnosis of early gastric lymphoma. J Gastroenterol 1992;29:6-10.
23Stolte M. Helicobacter pylori and gastric MALT - lymphoma. Lancet 1992;339:745-6.