• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of amjpatholAmerican Journal of Pathology For AuthorsAmerican Journal of Pathology SubscribeAmerican Journal of Pathology SearchAmerican Journal of Pathology Current IssueAmerican Journal of Pathology About the JournalAmerican Journal of Pathology
Am J Pathol. Jul 1997; 151(1): 273–280.
PMCID: PMC1857920

Helicobacter mustelae-associated gastric MALT lymphoma in ferrets.


Gastric lymphoma resembling gastric mucosa-associated lymphoid tissue (MALT) lymphoma linked with Helicobacter pylori infection in humans was observed in ferrets infected with H. mustelae. Four ferrets with ante- or postmortem evidence of primary gastric lymphoma were described. Lymphoma was diagnosed in the wall of the lesser curvature of the pyloric antrum, corresponding to the predominant focus of H. mustelae induced gastritis in ferrets. Two ferrets had low-grade small-cell lymphoma and two ferrets had high-grade large-cell lymphoma. Gastric lymphomas demonstrated characteristic lymphoepithelial lesions, and the lymphoid cells were IgG+ in all ferrets. Lymphoma was confirmed by light chain restriction, which contrasted with the 1.2:1 kappa lambda ratio observed in H. mustelae-associated chronic gastritis. H. mustelae infection in ferrets has been used as a model for gastritis, ulcerogenesis, and carcinogenesis. The ferret may provide an attractive model to study pathogenesis and treatment of gastric MALT lymphoma in humans.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.6M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Severson RK, Davis S. Increasing incidence of primary gastric lymphoma. Cancer. 1990 Sep 15;66(6):1283–1287. [PubMed]
  • Parsonnet J, Hansen S, Rodriguez L, Gelb AB, Warnke RA, Jellum E, Orentreich N, Vogelman JH, Friedman GD. Helicobacter pylori infection and gastric lymphoma. N Engl J Med. 1994 May 5;330(18):1267–1271. [PubMed]
  • Genta RM, Hamner HW, Graham DY. Gastric lymphoid follicles in Helicobacter pylori infection: frequency, distribution, and response to triple therapy. Hum Pathol. 1993 Jun;24(6):577–583. [PubMed]
  • Genta RM, Hamner HW. The significance of lymphoid follicles in the interpretation of gastric biopsy specimens. Arch Pathol Lab Med. 1994 Jul;118(7):740–743. [PubMed]
  • Isaacson P, Wright DH. Malignant lymphoma of mucosa-associated lymphoid tissue. A distinctive type of B-cell lymphoma. Cancer. 1983 Oct 15;52(8):1410–1416. [PubMed]
  • Isaacson PG, Spencer J, Wright DH. Classifying primary gut lymphomas. Lancet. 1988 Nov 12;2(8620):1148–1149. [PubMed]
  • Wotherspoon AC, Doglioni C, Diss TC, Pan L, Moschini A, de Boni M, Isaacson PG. Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet. 1993 Sep 4;342(8871):575–577. [PubMed]
  • Isaacson PG, Spencer J. The biology of low grade MALT lymphoma. J Clin Pathol. 1995 May;48(5):395–397. [PMC free article] [PubMed]
  • Roggero E, Zucca E, Pinotti G, Pascarella A, Capella C, Savio A, Pedrinis E, Paterlini A, Venco A, Cavalli F. Eradication of Helicobacter pylori infection in primary low-grade gastric lymphoma of mucosa-associated lymphoid tissue. Ann Intern Med. 1995 May 15;122(10):767–769. [PubMed]
  • Savio A, Franzin G, Wotherspoon AC, Zamboni G, Negrini R, Buffoli F, Diss TC, Pan L, Isaacson PG. Diagnosis and posttreatment follow-up of Helicobacter pylori-positive gastric lymphoma of mucosa-associated lymphoid tissue: histology, polymerase chain reaction, or both? Blood. 1996 Feb 15;87(4):1255–1260. [PubMed]
  • Enno A, O'Rourke JL, Howlett CR, Jack A, Dixon MF, Lee A. MALToma-like lesions in the murine gastric mucosa after long-term infection with Helicobacter felis. A mouse model of Helicobacter pylori-induced gastric lymphoma. Am J Pathol. 1995 Jul;147(1):217–222. [PMC free article] [PubMed]
  • Nakamura S, Akazawa K, Yao T, Tsuneyoshi M. A clinicopathologic study of 233 cases with special reference to evaluation with the MIB-1 index. Cancer. 1995 Oct 15;76(8):1313–1324. [PubMed]
  • Chan JK, Ng CS, Isaacson PG. Relationship between high-grade lymphoma and low-grade B-cell mucosa-associated lymphoid tissue lymphoma (MALToma) of the stomach. Am J Pathol. 1990 May;136(5):1153–1164. [PMC free article] [PubMed]
  • Tosi P, Leoncini L, Del Vecchio MT, Cevenini G, Stramignoni A, Valente G, Palestro G, Novero D, Cottier H. Heterogeneous subgroups among malignant diffuse small B cell lymphomas. A combined nucleometric and immunocytologic study. Lab Invest. 1990 Feb;62(2):202–212. [PubMed]
  • Montalbán C, Manzanal A, Castrillo JM, Escribano L, Bellas C. Low grade gastric B-cell MALT lymphoma progressing into high grade lymphoma. Clonal identity of the two stages of the tumour, unusual bone involvement and leukemic dissemination. Histopathology. 1995 Jul;27(1):89–91. [PubMed]
  • Fox JG, Edrise BM, Cabot EB, Beaucage C, Murphy JC, Prostak KS. Campylobacter-like organisms isolated from gastric mucosa of ferrets. Am J Vet Res. 1986 Feb;47(2):236–239. [PubMed]
  • Fox JG, Correa P, Taylor NS, Lee A, Otto G, Murphy JC, Rose R. Helicobacter mustelae-associated gastritis in ferrets. An animal model of Helicobacter pylori gastritis in humans. Gastroenterology. 1990 Aug;99(2):352–361. [PubMed]
  • Fox JG, Otto G, Murphy JC, Taylor NS, Lee A. Gastric colonization of the ferret with Helicobacter species: natural and experimental infections. Rev Infect Dis. 1991 Jul-Aug;13 (Suppl 8):S671–S680. [PubMed]
  • Saifuddin M, Fox JG. Identification of a DNA segment in ferret Aleutian disease virus similar to a hypervariable capsid region of mink Aleutian disease parvovirus. Arch Virol. 1996;141(7):1329–1336. [PubMed]
  • Erdman SE, Kanki PJ, Moore FM, Brown SA, Kawasaki TA, Mikule KW, Travers KU, Badylak SF, Fox JG. Clusters of lymphoma in ferrets. Cancer Invest. 1996;14(3):225–230. [PubMed]
  • Erdman SE, Moore FM, Rose R, Fox JG. Malignant lymphoma in ferrets: clinical and pathological findings in 19 cases. J Comp Pathol. 1992 Jan;106(1):37–47. [PubMed]
  • Erdman SE, Brown SA, Kawasaki TA, Moore FM, Li X, Fox JG. Clinical and pathologic findings in ferrets with lymphoma: 60 cases (1982-1994). J Am Vet Med Assoc. 1996 Apr 15;208(8):1285–1289. [PubMed]
  • Segal GH, Edinger MG, Owen M, McNealis M, Lopez P, Perkins A, Linden MD, Fishleder AJ, Stoler MH, Tubbs RR. Concomitant delineation of surface Ig, B-cell differentiation antigens, and HLADR on lymphoid proliferations using three-color immunocytometry. Cytometry. 1991;12(4):350–359. [PubMed]
  • Fox JG, Wishnok JS, Murphy JC, Tannenbaum SR, Correa P. MNNG-induced gastric carcinoma in ferrets infected with Helicobacter mustelae. Carcinogenesis. 1993 Sep;14(9):1957–1961. [PubMed]
  • Yu J, Russell RM, Salomon RN, Murphy JC, Palley LS, Fox JG. Effect of Helicobacter mustelae infection on ferret gastric epithelial cell proliferation. Carcinogenesis. 1995 Aug;16(8):1927–1931. [PubMed]
  • Eidt S, Stolte M, Fischer R. Factors influencing lymph node infiltration in primary gastric malignant lymphoma of the mucosa-associated lymphoid tissue. Pathol Res Pract. 1994 Nov;190(11):1077–1081. [PubMed]
  • Du M, Diss TC, Xu C, Peng H, Isaacson PG, Pan L. Ongoing mutation in MALT lymphoma immunoglobulin gene suggests that antigen stimulation plays a role in the clonal expansion. Leukemia. 1996 Jul;10(7):1190–1197. [PubMed]
  • Otto G, Fox JG, Wu PY, Taylor NS. Eradication of Helicobacter mustelae from the ferret stomach: an animal model of Helicobacter (Campylobacter) pylori chemotherapy. Antimicrob Agents Chemother. 1990 Jun;34(6):1232–1236. [PMC free article] [PubMed]
  • Calvert RJ, Evans PA, Randerson JA, Jack AS, Morgan GJ, Dixon MF. The significance of B-cell clonality in gastric lymphoid infiltrates. J Pathol. 1996 Sep;180(1):26–32. [PubMed]
  • Hockey MS, Powell J, Crocker J, Fielding JW. Primary gastric lymphoma. Br J Surg. 1987 Jun;74(6):483–487. [PubMed]
  • Muller AF, Maloney A, Jenkins D, Dowling F, Smith P, Bessell EM, Toghill PJ. Primary gastric lymphoma in clinical practice 1973-1992. Gut. 1995 May;36(5):679–683. [PMC free article] [PubMed]
  • Palley LS, Corning BF, Fox JG, Murphy JC, Gould DH. Parvovirus-associated syndrome (Aleutian disease) in two ferrets. J Am Vet Med Assoc. 1992 Jul 1;201(1):100–106. [PubMed]
  • Erdman SE, Reimann KA, Moore FM, Kanki PJ, Yu QC, Fox JG. Transmission of a chronic lymphoproliferative syndrome in ferrets. Lab Invest. 1995 May;72(5):539–546. [PubMed]

Articles from The American Journal of Pathology are provided here courtesy of American Society for Investigative Pathology