Histologic transformation of t(11;18)-positive MALT lymphoma presented with aberrant T-cell marker expression

Abstract

Mucosa-associated lymphoid tissue (MALT) lymphoma with t(11;18)(q21;q21), resulting in an API2-MALT1 fusion transcript, is reported to rarely transform into aggressive lymphoma. Here, we report the clinical course of a patient who experienced histologic transformation after 20 years’ disease history of t(11;18)-positive MALT lymphoma. The patient suddenly developed a large intrapelvic mass and ascites with a rapid increase in lactate dehydrogenase. Cytology of the ascites detected large abnormal cells, and flow cytometric analysis revealed that the cells were positive for cytoplasmic CD3, CD4, and CD38, and partially positive for CD7, but negative for CD19 and CD20. Antigen receptor gene rearrangement analysis and in situ hybridization of the immunoglobulin light chains confirmed that the tumor cells were of B-cell lineage. Chromosomal analysis showed complex karyotypes with intraclonal variation, and in addition to t(11;18), t(8;14) and heterozygous loss of the TP53 were demonstrated. Although histological and phenotypic features were significantly altered from the original MALT lymphoma, the presence of t(11;18) led us to the diagnosis of histologic transformation of MALT lymphoma. Although transformation of t(11;18)-positive MALT lymphoma into aggressive lymphoma is extremely rare, it may occur, probably with additional genetic abnormalities such as cMYC rearrangement and/or the loss of TP53.

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Change history

  • 28 June 2020

    M. Nishikori receives honoraria from Eisai and funding from Eisai and Sumitomo Dainippon Pharmaceutical.

References

  1. 1.

    Cohen SM, Petryk M, Varma M, Kozuch PS, Ames ED, Grossbard ML. Non-Hodgkin’s lymphoma of mucosa-associated lymphoid tissue. Oncologist. 2006;11(10):1100–17.

    CAS  Article  Google Scholar 

  2. 2.

    Thieblemont C, Bertoni F, Copie-Bergman C, Ferreri AJ, Ponzoni M. Chronic inflammation and extra-nodal marginal-zone lymphomas of MALT-type. Semin Cancer Biol. 2014;24:33–42.

    CAS  Article  Google Scholar 

  3. 3.

    Thiede C, Wündisch T, Alpen B, Neubauer B, Morgner A, Schmitz M, et al. Long-term persistence of monoclonal B cells after cure of Helicobacter pylori infection and complete histologic remission in gastric mucosa-associated lymphoid tissue B-cell lymphoma. J Clin Oncol. 2001;19:1600–9.

    CAS  Article  Google Scholar 

  4. 4.

    Wündisch T, Thiede C, Morgner A, Dempfle A, Gunther A, Liu H, et al. Long-term follow-up of gastric MALT lymphoma after Helicobacter pylori eradication. J Clin Oncol. 2005;23:8018–24.

    Article  Google Scholar 

  5. 5.

    Asenjo LM, Gisbert JP. Prevalence of Helicobacter pylori infection in gastric MALT lymphoma: a systematic review. Rev Esp Enferm Dig. 2007;99:398–404.

    CAS  Article  Google Scholar 

  6. 6.

    Nakamura S, Matsumoto T, Ye H, Nakamura S, Suekane H, Matsumoto H, et al. Helicobacter pylori-negative gastric mucosa-associated lymphoid tissue lymphoma: a clinicopathologic and molecular study with reference to antibiotic treatment. Cancer. 2006;107:2770–8.

    Article  Google Scholar 

  7. 7.

    Thieblemont C. Clinical presentation and management of marginal zone lymphomas. Hematol Am Soc Hematol Educ Prog. 2005;2005:307–13.

    Article  Google Scholar 

  8. 8.

    Kobayashi Y. JSH practical guidelines for hematological malignancies, 2018: II. Lymphoma-2. Marginal zone lymphoma (MALT lymphoma/extranodal marginal zone lymphoma of mucosa-associated lymphoid tissue and splenic marginal zone lymphoma). Int J Hematol. 2019;110:393–405.

    Article  Google Scholar 

  9. 9.

    Starostik P, Patzner J, Greiner A, Schwarz S, Kalla J, Ott G, et al. Gastric marginal zone B-cell lymphomas of MALT type develop along 2 distinct pathogenetic pathways. Blood. 2002;99:3–9.

    CAS  Article  Google Scholar 

  10. 10.

    Ye H, Liu H, Raderer M, Chott A, Ruskone-Fourmestraux A, Wotherspoon A, et al. High incidence of t(11;18)(q21;q21) in Helicobacter pylori-negative gastric MALT lymphoma. Blood. 2003;101:2547–50.

    CAS  Article  Google Scholar 

  11. 11.

    Cobaleda C, Jochum W, Busslinger M. Conversion of mature B cells into T cells by dedifferentiation to uncommitted progenitors. Nature. 2007;449:473–7.

    CAS  Article  Google Scholar 

  12. 12.

    Coupland SE, Hellmich M, Auw-Haedrich C, Lee WR, Anagnostopoulos I, Stein H. Plasmacellular differentiation in extranodal marginal zone B cell lymphomas of the ocular adnexa: an analysis of the neoplastic plasma cell phenotype and its prognostic significance in 136 cases. Br J Ophthalmol. 2005;89:352–9.

    CAS  Article  Google Scholar 

  13. 13.

    Molina TJ, Lin P, Swerdlow SH, Cook JR. Marginal zone lymphomas with plasmacytic differentiation and related disorders. Am J Clin Pathol. 2011;136:211–25.

    Article  Google Scholar 

  14. 14.

    Chisholm KM, Bangs CD, Bacchi CE, Molina-Kirsch H, Cherry A, Natkunam Y. Expression profiles of MYC protein and MYC gene rearrangement in lymphomas. Am J Surg Pathol. 2015;39:294–303.

    Article  Google Scholar 

  15. 15.

    Toyoda K, Maeshima AM, Nomoto J, Suzuki T, Yuda S, Yamauchi N, et al. Mucosa-associated lymphoid tissue lymphoma with t(11;18)(q21;q21) translocation: long-term follow-up results. Ann Hematol. 2019;98:1675–87.

    CAS  Article  Google Scholar 

  16. 16.

    Chuang SS, Lee C, Hamoudi RA, Liu H, Lee PS, Ye H, et al. High frequency of t(11;18) in gastric mucosa-associated lymphoid tissue lymphomas in Taiwan, including one patient with high-grade transformation. Br J Haematol. 2003;120:97–100.

    Article  Google Scholar 

  17. 17.

    Ke X, Zhao L, Gao Z, Wang J, Dong F, Zhou X, et al. Higher rates of t(11;18) in Chinese patients with transformed type of MALT lymphoma suggest novel pathways for progression of the disease. Leuk Lymphoma. 2007;48:2157–66.

    CAS  Article  Google Scholar 

  18. 18.

    Suzuki Y, Yoshida T, Wang G, Aoki T, Katayama T, Miyamoto S, et al. Incidence and clinical significance of aberrant T-cell marker expression on diffuse large B-cell lymphoma cells. Acta Haematol. 2013;130:230–7.

    CAS  Article  Google Scholar 

  19. 19.

    Tsuyama N, Ennishi D, Yokoyama M, Baba S, Asaka R, Mishima Y, et al. Clinical and prognostic significance of aberrant T-cell marker expression in 225 cases of de novo diffuse large B-cell lymphoma and 276 cases of other B-cell lymphomas. Oncotarget. 2017;8:33487–500.

    Article  Google Scholar 

  20. 20.

    Carulli G, Stacchini A, Marini A, Ciriello MM, Zucca A, Cannizzo E, et al. Aberrant expression of CD8 in B-cell non-Hodgkin lymphoma: a multicenter study of 951 bone marrow samples with lymphomatous infiltration. Am J Clin Pathol. 2009;132:186–90.

    CAS  Article  Google Scholar 

  21. 21.

    Laurent C, Do C, Gascoyne RD, Lamant L, Ysebaert L, Laurent G, et al. Anaplastic lymphoma kinase-positive diffuse large B-cell lymphoma: a rare clinicopathologic entity with poor prognosis. J Clin Oncol. 2009;27:4211–6.

    Article  Google Scholar 

  22. 22.

    Oliveira JL, Grogg KL, Macon WR, Dogan A, Feldman AL. Clinicopathologic features of B-cell lineage neoplasms with aberrant expression of CD3: a study of 21 cases. Am J Surg Pathol. 2012;36:1364–70.

    Article  Google Scholar 

  23. 23.

    Pan Z, Chen M, Zhang Q, Wang E, Yin L, Xu Y, et al. CD3-positive plasmablastic B-cell neoplasms: a diagnostic pitfall. Mod Pathol. 2018;31:718–31.

    CAS  Article  Google Scholar 

  24. 24.

    Pan Z, Hu S, Li M, Zhou Y, Kim YS, Reddy V, et al. ALK-positive large B-cell lymphoma: a clinicopathologic study of 26 cases with review of additional 108 cases in the literature. Am J Surg Pathol. 2017;41:25–38.

    Article  Google Scholar 

  25. 25.

    Suzuki Y, Yoshida T, Nakamura N, Kamata H, Kotani S, Ohsaka M, et al. CD3- and CD4-positive plasmablastic lymphoma: a literature review of Japanese plasmablastic lymphoma cases. Intern Med. 2010;49:1801–5.

    Article  Google Scholar 

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Correspondence to Momoko Nishikori.

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Tamura, N., Maeda, H., Nishikori, M. et al. Histologic transformation of t(11;18)-positive MALT lymphoma presented with aberrant T-cell marker expression. Int J Hematol 111, 724–732 (2020). https://doi.org/10.1007/s12185-019-02810-y

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Keywords

  • MALT lymphoma
  • API2-MALT1 translocation
  • Histologic transformation