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15 May 1995 | Volume 122 Issue 10 | Pages 767-769
Objective: To determine the effect of eradicating Helicobacter pylori infection on the course of low-grade gastric mucosa-associated lymphoid tissue (MALT) lymphoma.
Design: Prospective cohort study.
Setting: University internal medicine clinics, a referral oncology center in southern Switzerland, and a gastroenterology referral center in northern Italy.
Patients: 26 patients with localized primary low-grade gastric MALT lymphoma.
Intervention: Treatment for H. pylori infection (bismuth or omeprazole or both, amoxicillin, and metronidazole for 14 days).
Main Outcome Measures: Endoscopic biopsy specimens of the gastric mucosa were obtained every 3 to 6 months after treatment for H. pylori infection.
Results: Helicobacter pylori was completely eradicated in 25 of 26 patients, but 4 patients needed second-line antibiotic treatment to eradicate the microorganism. Disappearance or almost total regression of the lymphomatous tissue was observed in 15 of the 25 evaluable patients (60%; CI, 39% to 79%); however, disappearance or almost total regression was evident in the first biopsy specimen after treatment for H. pylori infection in only 8 of the 15 patients.
Conclusions: Our study confirms recent anecdotal reports of regression of gastric MALT lymphoma after eradication of H. pylori and indicates that the growth of these extranodal lymphomas may depend on H. pylori.
We analyzed the effects of antibiotic therapy for H. pylori infection in 26 patients with low-grade gastric MALT lymphoma. Our patients were from a geographic area (southern Switzerland and northern Italy) where the incidence of gastric tumors appears to be uncommonly high [4, 5]. Many patients with primary gastric lymphoma reside in northeastern Italy [6], a region geographically close and environmentally similar to the area in which our patients reside. Reasons for these disease clusters are not known.
Patients were treated for H. pylori infection for 2 weeks with amoxicillin (500 mg three times daily) plus metronidazole (400 mg three times daily) and colloidal bismuth (120 mg four times daily; 13 patients) or omeprazole (20 mg twice daily; 13 patients). Twenty patients were treated immediately after diagnosis of H. pylori infection, and 6 were treated after an observation period of several months (median, 5 months; range, 3 to 36 months) without endoscopic and histologic changes of the MALT lymphoma.
One patient had a brief response to first-line combination chemotherapy with cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP regimen), but the patient later had a local relapse. This patient still had histologic characteristics of low-grade gastric MALT lymphoma when treatment for H. pylori infection was given.
To reevaluate the condition of the patients after treatment for H. pylori infection, biopsy specimens were obtained from any abnormal area in the stomach and randomly obtained from the rest of the stomach. These multiple (range, 8 to 20 specimens), random biopsy specimens of the gastric mucosa were obtained within 6 months of treatment (3 months for 19 patients, 4 months for 4 patients, and 6 months for the remaining 3 patients); patients were reevaluated every 3 to 6 months thereafter. The patients with persistent H. pylori infection had additional treatment for 2 weeks with a different regimen: omeprazole (20 mg twice daily), metronidazole (400 mg three times daily), and azithromycin (500 mg daily for 3 consecutive days every week).
Restaging with chest radiographs and abdominal ultrasound was done again after 1 year. In 9 patients, a bone marrow biopsy specimen was obtained again after 6 months. Histologic responses were graded according to the histologic scoring system recently proposed for the diagnosis of gastric MALT lymphoma [2]. We considered a post-treatment score of 2 or less to be evidence of lymphoma regression. Binomial exact 95% CIs were calculated for outcome percentages.
All but one of the patients were symptomatic at presentation; the main symptoms were pain (60% of patients), dyspepsia (30% of patients), and nausea and vomiting (7% of patients). One patient presented with gastrointestinal hemorrhage. Symptoms disappeared in 77% of patients or markedly diminished after antibiotic treatment. At the endoscopic evaluation done before treatment, 11 patients had gastric ulcers, 9 had endoscopic evidence of gastritis, and the remaining 6 had abnormal, congestive (hyperemic) gastric mucosa. In all patients, these endoscopic features improved after eradication of H. pylori infection and all of the ulcers healed, but only one patient had a complete recovery of the gastric mucosa.
Histologic regression of the MALT lymphoma Table 1 was observed in 15 patients (60%; CI, 39% to 79%) after H. pylori eradication, including the 1 patient who relapsed after chemotherapy. Five patients had complete disappearance of any histologic evidence of lymphoma (histologic score, 0 to 1), and 10 patients had residual lymphoid follicles but no longer had lymphoepithelial lesions (histologic score, 2). Three patients showed persistent suspicious, probably reactive, lymphoid infiltrate in the lamina propria (histologic score, 3) and were considered to have not responded to treatment. The other patients showed no change or only partial improvement in the lymphoma histologic pattern in repeat gastric biopsy specimens. BRIEF COMMUNICATION
Eradication of Helicobacter pylori Infection in Primary Low-Grade Gastric Lymphoma of Mucosa-Associated Lymphoid Tissue
Low-grade gastric lymphoma of mucosa-associated lymphoid tissue (MALT) is an uncommon tumor with an indolent natural history and prolonged confinement to the site of origin. Its morphologic appearance is characterized by prominent and often multifocal lymphoepithelial lesions showing dense, diffuse infiltrates of centrocyte-like cells within the lamina propria [1]. B-cell monoclonality can often be shown by either immunocytochemical or molecular methods [2]. A close association has been suggested between gastric MALT lymphoma and the presence of certain strains of Helicobacter pylori, which are found in more than 90% of patients with gastric MALT lymphoma [3]. Regression of this lymphoma after eradication of H. pylori was reported in 5 of 6 patients who received antibiotic therapy [2].
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Twenty-six patients (14 women, 12 men; median age, 60 years [range, 21 to 76 years]) with histologic diagnoses of localized (stage IE), primary, B-cell, low-grade gastric MALT lymphoma and H. pylori infection (diagnosed using endoscopic biopsy specimens) were entered into our study. Almost all patients had a prolonged history (as long as 4 years) of gastric symptoms before diagnosis of H. pylori infection, and most of them had already been given antacid medication, motility stimulant agents, or both. Before patients received treatment for H. pylori infection, the following staging procedures were done: physical examination, routine laboratory tests, chest radiographs, abdominal ultrasound or computed tomographic scans, endoscopic gastric biopsy specimens, and bone marrow biopsy specimens.
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Complete eradication of H. pylori was initially achieved in 21 patients (81%; 95% CI, 61% to 93%); in the remaining 4 patients, second-line antibiotic treatment was needed to eradicate the microorganism. The overall eradication rate was therefore 96% (25 of 26 patients; 95% CI, 80% to 99%). After treatment for H. pylori infection, the median follow-up was 12 months (range, 3 to 36 months). One patient, treated after an observation period of 36 months without clinical or histologic change, showed persistent gastric infection and unchanged lymphoma features on biopsy specimens obtained 3 months after treatment. The patient received additional antibiotic treatment but has not been reevaluated with endoscopy.
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Our study suggests that regression of the lymphoma may require a prolonged period. Only 8 patients showed histologic regression on the first biopsy specimen after antibiotic treatment, but when endoscopic specimens were obtained again 3 or more months later, regression was clearly evident in 7 additional patients. At a median follow-up of 12 months, all patients were alive and 14 of 15 responders, including the 1 patient who relapsed after chemotherapy, were free of lymphoma. A bone marrow specimen from 1 patient showed evidence of relapse shortly thereafter, with a response duration of only 4 months; however, no evidence of MALT lymphoma was found in repeat gastric biopsy specimens (histologic score, 2).
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The case of low-grade gastric MALT lymphomas is not the only one in which a bacterial infection has been implicated in the pathogenesis of a lymphoma. Antibacterial therapy has already been reported to be useful in the treatment of 
-chain disease (a small-intestinal lymphoma) [11], providing indirect evidence that bacteria may have a pathogenetic role in lymphomas.
Only careful, prolonged follow-up will ascertain whether treatment for H. pylori can definitely cure gastric MALT lymphoma. Currently, this represents one of the many questions in the treatment of gastric lymphoma (others include those about the necessity for surgery and role of chemotherapy) [12]. Our data show that for low-grade MALT gastric lymphoma, an antibiotic treatment designed to eradicate H. pylori appears to be mandatory before further therapeutic options are considered. An international randomized trial will soon investigate whether it is beneficial to add cytotoxic chemotherapy to such an antibiotic treatment.
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1. Wotherspoon AC, Doglioni C, Isaacson PG. Low-grade gastric B-cell lymphoma of mucosa-associated lymphoid tissue (MALT): a multifocal disease. Histopathology. 1992; 20:29-34.
2. Wotherspoon AC, Doglioni C, Diss TC, Pan L, Moschini A, de Boni M, et al. Regression of primary low-grade B-cell gastric lymphoma of mucosa associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet. 1993; 342:575-7.
3. Wotherspoon AC, Ortiz-Hildago C, Falzon MF, Isaacson PG.Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet. 1991; 338:1175-6.
4. Spataro V, Pedrinis E, Muller W. Descriptive epidemiology of gastric tumors in southern Switzerland with special emphasis on time trends. Ann Oncol. 1994; 5:954-6.
5. Pinotti G, Novario R, Berrino F, Bianchi P, Comi MA, Gamba MC, et al. Primary gastric non-Hodgkin's lymphoma in a population based registry. Haematologica. 1992; 77:405-12.
6. Doglioni C, Wotherspoon AC, Moschini A, de Boni M, Isaacson PG. High incidence of primary gastric lymphoma in north-eastern Italy. Lancet. 1992; 339:834-5.
7. Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, et al.Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med. 1991; 325:1127-31.
8. Parsonnet J, Hansen S, Rodriguez L, Gelb AB, Warnke RA, Jellum E, et al.Helicobacter pylori infection and gastric lymphoma. N Engl J Med. 1994; 330:1267-71.
9. Hussel T, Isaacson PG, Cradtree 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.
10. Stolte M, Eidt S. Healing gastric MALT lymphomas by eradicating H. pylori? Lancet. 1993; 342:568.
11. Ben-Ayed F, Halphen M, Najjar T, Boussene H, Jaafoura H, Bouguerra A, et al. Treatment of -chain disease. Results of a prospective study in 21 Tunisian patients by the Tunisian-French Intestinal Lymphoma Study Group. Cancer. 1989; 63:1251-6.
12. Rohatiner A. Report on a workshop convened to discuss the pathological and staging classifications of gastrointestinal tract lymphoma. Ann Oncol. 1994; 5:397-400.
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