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BCL10 nuclear expression and t(11;18)(q21;q21) indicate nonresponsiveness to Helicobacter pylori eradication of Chinese primary gastric MALT lymphoma

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Abstract

The eradication of Helicobacter pylori (H. pylori) with antibiotics induces complete remission in 75% of patients with gastric MALT lymphoma. We investigated the efficacy of H. pylori eradication and assessed the predictive value of BCL10 nuclear expression and t(11;18)(q21;q21) regarding resistance to H. pylori eradication in primary gastric mucosa-associated lymphoid tissue lymphoma (MALT lymphoma) patients from mainland China. Twenty-two gastric MALT cases (Stage IE) underwent H. pylori eradication with antibiotics, and sequential endoscopic-bioptic follow-ups were performed and assessed with regular morphologic and immunohistochemical examinations. BCL10 nuclear expression and interphase fluorescence in situ hybridization (FISH) for MALT1 and API2/MALT1 were tested. Thirteen out of the 22 cases (59.1%) achieved complete regression (CR) after the eradication of H. pylori. The longest follow-up period in the 22 patients was 68 months, with 12 patients longer than 24 months. For the 13 CR patients, the longest follow-up period after H. pylori eradication was 53 months, with 6 patients longer than 24 months. BCL10 nuclear expression was detected by immunohistochemical staining in 9 cases, including 7 (77.8%) of 9 cases who showed no response (NR) and 2 (15.4%) of 13 patients who achieved CR following eradication therapy (P < 0.05). t(11;18)(q21;q21) was evaluated by interphase FISH in 18 cases including 11 CR and 7 NR patients after H. pylori eradication. t(11;18)(q21;q21) was found in 4 (57.1%) of 7 patients who showed NR following H. pylori eradication, but one in 11 CR patients (P < 0.05). A total of 59.1% of patients with early gastric MALT lymphoma recruited in this study achieved CR after H. pylori eradication. BCL10 nuclear expression and t(11;18)(q21;q21)-positive gastric MALT lymphomas are likely to be related to a failure to respond to H. pylori eradication in Chinese patients.

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References

  1. Isaacson P, Müller-Hermelink HK, Piris MA, et al. Extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma). In: Jaffe ES, Harris NL, Stein H, Vardiman JW, editors. Tumours of haematopoietic and lymphoid tissues. Lyon: IARC Press; 2001. p. 157–60.

    Google Scholar 

  2. Isaacson P, Wright DH. Malignant lymphoma of mucosa-associated lymphoid tissue. A distinctive type of B-cell lymphoma. Cancer. 1983;52:1410–6. doi:10.1002/1097-0142(19831015)52:8<1410::AID-CNCR2820520813>3.0.CO;2-3.

    Article  CAS  PubMed  Google Scholar 

  3. Wotherspoon AC, Doglioni C, Diss TC, 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. doi:10.1016/0140-6736(93)91409-F.

    Article  CAS  PubMed  Google Scholar 

  4. Kaneko Y, Sakurai S, Hironaka M, et al. Distinct methylated profiles in Helicobacter pylori dependent and independent gastric MALT lymphomas. Gut. 2003;52:641–6. doi:10.1136/gut.52.5.641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Liu H, Ruskone-Fourmestraux A, Lavergne-Slove A, et al. Gastric MALT Lymphoma with t(11;18)(q21;q21) fails to respond to Helicobacter pylori eradication therapy. Lancet. 2001;357:39–40. doi:10.1016/S0140-6736(00)03571-6.

    Article  CAS  PubMed  Google Scholar 

  6. Sackmann M, Morgner A, Rudolph B, et al. Regression of gastric MALT lymphoma after eradication of Helicobacter pylori is predicted by endosonographic staging. MALT Lymphoma Study Group. Gastroenterology. 1997;113:1087–90. doi:10.1053/gast.1997.v113.pm9322502.

    Article  CAS  PubMed  Google Scholar 

  7. Nakamura S, Matsumoto T, Suekane H, et al. Predictive value of endoscopic ultrasonography for regression of gastric low grade and high grade MALT lymphomas after eradication of Helicobacter pylori. Gut. 2001;48:454–60. doi:10.1136/gut.48.4.454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ye H, Dogan A, Karran L, et al. BCL10 expression in normal and neoplastic lymphoid tissue. Nuclear localization in MALT lymphoma. Am J Pathol. 2000;157:1147–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Liu H, Ye H, Dogan A, et al. T(11;18)(q21;q21) is associated with advanced mucosa-associated lymphoid tissue lymphoma that expresses nuclear BCL 10. Blood. 2001;98:1182–7. doi:10.1182/blood.V98.4.1182.

    Article  CAS  PubMed  Google Scholar 

  10. Streubel B, Simonitsch-Klupp I, Mu llauer L, et al. Variable frequencies of MALT lymphoma-associated genetic aberrations in MALT lymphomas of different sites. Leukemia. 2004;18:1722–6. doi:10.1038/sj.leu.2403501.

    Article  CAS  PubMed  Google Scholar 

  11. Ye H, Gong L, Liu H, et al. MALT lymphoma with t(14;18)(q32;q21)/IGH-MALT1 is characterized by strong cytoplasmic MALT1 and BCL10 expression. J Pathol. 2005;205:293–301. doi:10.1002/path.1715.

    Article  CAS  PubMed  Google Scholar 

  12. Wu¨ndisch T, Thiede C, Morgner A, et al. Long-term follow-up of gastric MALT lymphoma after Helicobacter pylori eradication. J Clin Oncol. 2005;23:8018–24. doi:10.1200/JCO.2005.02.3903.

    Article  Google Scholar 

  13. Remstein ED, Dogan A, Einerson RR, et al. The incidence and anatomic site specificity of chromosomal translocations in primary extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma) in North America. Am J Surg Pathol. 2006;30:1546–53. doi:10.1097/01.pas.0000213275.60962.2a.

    Article  PubMed  Google Scholar 

  14. Nakamura S, Ye H, Bacon CM, et al. Clinical impact of genetic aberrations in gastric MALT lymphoma: a comprehensive analysis using interphase fluorescence in situ hybridization. Gut. 2007;56:1358–63. doi:10.1136/gut.2007.123729.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Willis TG, Jadayel DM, Du MQ, et al. Bcl 10 is involved in t(1;14)(p22;q32) of MALT B-cell lymphoma and mutated in multiple tumor types. Cell. 1999;96:35–45. doi:10.1016/S0092-8674(00)80957-5.

    Article  CAS  PubMed  Google Scholar 

  16. Ruland J, Duncan GS, Elia A, et al. Bcl 10 is a positive regulator of antigen receptor-induced activation of NF-kappa B and neural tube closure. Cell. 2001;104:33–42. doi:10.1016/S0092-8674(01)00189-1.

    Article  CAS  PubMed  Google Scholar 

  17. Wotherspoon AC, Ortiz-Hidalgo C, Falzon MR, et al. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet. 1991;338:1175–6. doi:10.1016/0140-6736(91)92035-Z.

    Article  CAS  PubMed  Google Scholar 

  18. Chen LT, Lin JT, Chen GH, et al. Long-term results of anti-Helicobacter pylori therapy in early-stage gastric high-grade transformed MALT lymphoma. J Natl Cancer Inst. 2005;97:1345–53.

    Article  CAS  PubMed  Google Scholar 

  19. Pinotti G, Zucca E, Roggero E, et al. Clinical features, treatment and outcome in a series of 93 patients with low-grade gastric MALT lymphoma. Leuk Lymphoma. 1997;26:527–37.

    Article  CAS  PubMed  Google Scholar 

  20. Raderer M, Streubel B, Wöhrer S, et al. Successful antibiotic treatment of Helicobacter pylori negative gastric mucosa associated lymphoid tissue lymphomas. Gut. 2006;55(5):616–8. doi:10.1136/gut.2005.083022.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fox JG. The non-H. pylori helicobacters: their expanding role in gastrointestinal and systemic diseases. Gut. 2002;50:273–83. doi:10.1136/gut.50.2.273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Cavalli F, Isaacson PG, Gascoyne RD, et al. MALT lymphomas. Hematology Am Soc Hematol Educ Program. 2001;2001:241–58. doi:10.1182/asheducation-2001.1.241.

  23. Neubauer A, Thiede C, Morgner A, et al. Cure of Helicobacter pylori infection and duration of remission of lowgrade gastric mucosa-associated lymphoid tissue lymphoma. J Natl Cancer Inst. 1997;89:1350–5. doi:10.1093/jnci/89.18.1350.

    Article  CAS  PubMed  Google Scholar 

  24. Bayerdorffer E, Neubauer A, Rudolph B, et al. Regression of primary gastric lymphoma of mucosa associated lymphoid tissue type after cure of Helicobacter pylori infection. MALT Lymphoma Study Group. Lancet. 1995;345:1591–4. doi:10.1016/S0140-6736(95)90113-2.

    Article  CAS  PubMed  Google Scholar 

  25. Cavanna L, Pagani R, Seghini P, et al. High grade B-cell gastric lymphoma with complete pathologic remission after eradication of Helicobacter pylori infection: Report of a case and review of the literature. World J Surg Oncol. 2008;6:35–41. doi:10.1186/1477-7819-6-35.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Soweid AM, El Sayed A. Predictive value of endoscopic ultrasonography for regression of gastric low grade and high grade MALT lymphomas after eradication of Helicobacter pylori. Gastrointest Endosc. 2002;55:449–51.

    PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Natural Science Fundation of China (30428018) and Natural Science Fundation of Guangxi Zhuang Autonomous Region (0499015). We thank Professor Ming-Qing Du, Division of Molecular Histopathology, Department of Pathology, University of Cambridge, UK, for his technical assistance.

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Correspondence to Zifen Gao.

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Both G. Dong and C. Liu are treated as co-first authors.

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Dong, G., Liu, C., Ye, H. et al. BCL10 nuclear expression and t(11;18)(q21;q21) indicate nonresponsiveness to Helicobacter pylori eradication of Chinese primary gastric MALT lymphoma. Int J Hematol 88, 516–523 (2008). https://doi.org/10.1007/s12185-008-0187-z

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  • DOI: https://doi.org/10.1007/s12185-008-0187-z

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