Helicobacter pylori (HP) infection alone, but not HP-induced atrophic gastritis, increases the risk of gastric lymphoma: a case-control study in Japan

Ann Hematol. 2019 Aug;98(8):1981-1987. doi: 10.1007/s00277-019-03721-y. Epub 2019 Jun 8.

Abstract

Infection with Helicobacter pylori (H. pylori) is associated with an increased risk of gastric malignant lymphoma. The chronic inflammation of gastric mucosa by H. pylori infection induces lymphomagenesis. Although this chronic mucosal inflammation also results in atrophic gastritis, evidence supporting the possible significance of atrophic gastritis in gastric lymphomagenesis is scarce. Here, to evaluate the association between gastric mucosal atrophy and the risk of gastric lymphoma, we conducted a matched case-control study at Aichi Cancer Center focusing on the attribution of H. pylori infection status and pepsinogen (PG) serum levels. In total, 86 patients with gastric lymphoma (including 49 cases of extranodal marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma) and 24 cases of diffuse large B cell lymphoma (DLBCL)) and 1720 non-cancer controls were included. Odds ratios (ORs) and 95% confidence intervals (CIs) were assessed by conditional logistic regression analysis with adjustment for potential confounders. Results failed to show a statistically significant association between atrophic gastritis and the risk of gastric lymphoma. The adjusted ORs of positive atrophic gastritis relative to negative for overall gastric lymphoma, MALT lymphoma, DLBCL, and other lymphomas were 0.77 (95% CI 0.45-1.33), 0.65 (0.30-1.39), 1.03 (0.38-2.79), and 0.84 (0.22-3.29), respectively. In contrast, a positive association between overall gastric lymphoma and H. pylori infection was observed (OR = 2.14, 95% CI 1.30-3.54). A consistent association was observed for MALT lymphoma, DLBCL, and other lymphomas with ORs of 1.96 (1.00-3.86), 1.92 (0.74-4.95), and 5.80 (1.12-30.12), respectively. These findings suggest that H. pylori infection triggers gastric lymphoma but that epithelial changes due to atrophic gastritis do not inherently affect the development of gastric lymphoma.

Keywords: Atrophic gastritis; Case-control study; Gastric lymphoma; Helicobacter pylori; MALT lymphoma.

MeSH terms

  • Adult
  • Aged
  • Carcinogenesis / pathology
  • Case-Control Studies
  • Female
  • Gastric Mucosa / microbiology
  • Gastric Mucosa / pathology
  • Gastritis, Atrophic / complications
  • Gastritis, Atrophic / diagnosis
  • Gastritis, Atrophic / microbiology
  • Gastritis, Atrophic / pathology
  • Helicobacter Infections / complications
  • Helicobacter Infections / diagnosis*
  • Helicobacter Infections / microbiology
  • Helicobacter Infections / pathology
  • Helicobacter pylori / pathogenicity*
  • Helicobacter pylori / physiology
  • Humans
  • Japan
  • Logistic Models
  • Lymphoma, B-Cell, Marginal Zone / diagnosis*
  • Lymphoma, B-Cell, Marginal Zone / etiology
  • Lymphoma, B-Cell, Marginal Zone / microbiology
  • Lymphoma, B-Cell, Marginal Zone / pathology
  • Lymphoma, Large B-Cell, Diffuse / diagnosis*
  • Lymphoma, Large B-Cell, Diffuse / etiology
  • Lymphoma, Large B-Cell, Diffuse / microbiology
  • Lymphoma, Large B-Cell, Diffuse / pathology
  • Lymphoma, Non-Hodgkin / diagnosis*
  • Lymphoma, Non-Hodgkin / etiology
  • Lymphoma, Non-Hodgkin / microbiology
  • Lymphoma, Non-Hodgkin / pathology
  • Male
  • Middle Aged
  • Odds Ratio
  • Pepsinogen A / blood
  • Risk Factors
  • Stomach Neoplasms / diagnosis*
  • Stomach Neoplasms / etiology
  • Stomach Neoplasms / microbiology
  • Stomach Neoplasms / pathology

Substances

  • Pepsinogen A

Supplementary concepts

  • Familial primary gastric lymphoma