187
Views
2
CrossRef citations to date
0
Altmetric
Review

How can we assess and measure prognosis for MALT lymphoma? A review of current findings and strategies

&
Pages 391-399 | Received 30 Dec 2020, Accepted 23 Mar 2021, Published online: 02 Apr 2021

References

  • Raderer M, Kiesewetter B, Ferreri AJM. Clinicopathologic characteristics and treatment of marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma). CA Cancer J Clin. 2016;66(2):152–171.
  • Cook JR, Chott A, Nakamura S, et al. Extranodal marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma). In: Swerdlow SHCE, Harris NL, Jaffe ES, et al., editors. WHO classification of tumours of Haematopoetic and lymphoid tissues, 4th, 259–262. Lyon, France: IARC; 2017, Revised.
  • Bacon CM, Du MQ, Dogan A. Mucosa-associated lymphoid tissue (MALT) lymphoma: a practical guide for pathologists. J Clin Pathol. 2007 Apr;60(4):361–372.
  • Hussell T, Isaacson PG, Crabtree JE, et al. The response of cells from low-grade B-cell gastric lymphomas of mucosa-associated lymphoid tissue to helicobacter pylori. Lancet. 1993 Sep 4;342(8871):571–574.
  • Isaacson PG, Du MQ. MALT lymphoma: from morphology to molecules. Nat Rev Cancer. 2004 Aug;4(8):644–653.
  • Sagaert X, De Wolf-Peeters C, Noels H, et al. The pathogenesis of MALT lymphomas: where do we stand? Leukemia. 2007;21(3):389–396.
  • Kiesewetter B, Lamm W, Dolak W, et al. Transformed mucosa-associated lymphoid tissue lymphomas: a single institution retrospective study including polymerase chain reaction-based clonality analysis. Br J Haematol. 2019;186(3):448–459.
  • Conconi A, Franceschetti S, Aprile Von Hohenstaufen K, et al. Histologic transformation in marginal zone lymphomas†. Ann Oncol. 2015 Nov;26(11):2329–2335.
  • Maeshima AM, Taniguchi H, Toyoda K, et al. Clinicopathological features of histological transformation from extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue to diffuse large B-cell lymphoma: an analysis of 467 patients. Br J Haematol. 2016 Sep;174(6):923–931.
  • Starr AG, Caimi PF, Fu P, et al. Dual institution experience of extranodal marginal zone lymphoma reveals excellent long-term outcomes. Br J Haematol. 2016 May;173(3):404–412.
  • Zucca E, Arcaini L, Buske C, et al. Marginal zone lymphomas: ESMO clinical practice guidelines for diagnosis, treatment and follow-up✰. Ann Oncol. 2020;31(1):17–29.
  • Kiesewetter B, Ferreri AJM, Raderer M. Chemoimmunotherapy for Mucosa-Associated lymphoid tissue-type lymphoma: a review of the literature. Oncologist. 2015;20(8):915–925.
  • Zucca E, Conconi A, Martinelli G, et al. Final results of the IELSG-19 randomized trial of Mucosa-Associated Lymphoid Tissue Lymphoma: Improved Event-Free And Progression-Free Survival With Rituximab plus chlorambucil versus either chlorambucil or rituximab monotherapy. J Clin Oncol. 2017 Jun 10;35(17):1905–1912.
  • Salar A, Domingo-Domenech E, Panizo C, et al. Long-term results of a phase 2 study of rituximab and bendamustine for mucosa-associated lymphoid tissue lymphoma. Blood. 2017 Oct 12;130(15):1772–1774.
  • Kiesewetter B, Raderer M. Immunomodulatory treatment for mucosa-associated lymphoid tissue lymphoma (MALT lymphoma). Hematol Oncol. 2020 Oct;38(4):417–424.
  • Jan Paul De B, Reinier FH, Markus R, et al. Dissemination patterns in non-gastric MALT lymphoma. Haematologica. 2008;93(2):201–206.
  • Raderer M, Wöhrer S, Streubel B, et al. Assessment of disease dissemination in gastric compared with extragastric mucosa-associated lymphoid tissue lymphoma using extensive staging: a single-center experience. J Clin Oncol. 2006 Jul 1;24(19):3136–3141.
  • Thieblemont C, Berger F, Dumontet C, et al. Mucosa-associated lymphoid tissue lymphoma is a disseminated disease in one third of 158 patients analyzed. Blood. 2000 Feb 1;95(3):802–806.
  • Ruskoné-Fourmestraux A, Fischbach W, Aleman BM, et al. EGILS consensus report. Gastric extranodal marginal zone B-cell lymphoma of MALT. Gut 2011 Jun;60(6):747–758.
  • Mayerhoefer ME, Karanikas G, Kletter K, et al. Evaluation of diffusion-weighted MRI for pretherapeutic assessment and staging of lymphoma: results of a prospective study in 140 patients. Clin Cancer Res. 2014 Jun 1;20(11):2984–2993.
  • Qi S, Huang MY, Yang Y, et al. Uptake of [(18)F]fluorodeoxyglucose in initial positron-emission tomography predicts survival in MALT lymphoma. Blood Adv. 2018 Mar 27;2(6):649–655.
  • Treglia G, Zucca E, Sadeghi R, et al. Detection rate of fluorine-18-fluorodeoxyglucose positron emission tomography in patients with marginal zone lymphoma of MALT type: a meta-analysis. Hematol Oncol. 2015 Sep;33(3):113–124.
  • Albano D, Bertoli M, Ferro P, et al. 18F-FDG PET/CT in gastric MALT lymphoma: a bicentric experience. Eur J Nucl Med Mol Imaging. 2017 Apr;44(4):589–597.
  • Albano D, Bosio G, Giubbini R, et al. 18F-FDG PET/CT and extragastric MALT lymphoma: role of Ki-67 score and plasmacytic differentiation. Leuk Lymphoma. 2017 Oct;58(10):2328–2334.
  • Mayerhoefer ME, Staudenherz A, Kiesewetter B, et al. Pre-therapeutic total lesion glycolysis on [(18)F]FDG-PET enables prognostication of 2-year progression-free survival in MALT lymphoma patients treated with CD20-antibody-based immunotherapy. Mol Imaging Biol. 2019 Dec;21(6):1192–1199.
  • Haug AR, Leisser A, Wadsak W, et al. Prospective non-invasive evaluation of CXCR4 expression for the diagnosis of MALT lymphoma using [(68)Ga]Ga-Pentixafor-PET/MRI. Theranostics. 2019;9(12):3653–3658.
  • Berzaczy D, Staudenherz A, Raderer M, et al. DWI-MRI vs CT in gastric MALT lymphoma-preliminary results in 19 patients. Br J Radiol. 2018;92(1093):20180263.
  • Mayerhoefer ME, Archibald SJ, Messiou C, et al. MRI and PET/MRI in hematologic malignancies. J Magn Reson Imaging. 2020 May;51(5):1325–1335.
  • Choi SI, Kook MC, Hwang S, et al. Prevalence and implications of bone marrow involvement in patients with Gastric Mucosa-Associated lymphoid tissue lymphoma. Gut Liver. 2018 May 15;12(3):278–287.
  • Zucca E, Conconi A, Pedrinis E, et al. Nongastric marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue. Blood. 2003;101(7):2489–2495.
  • Wöhrer S, Kiesewetter B, Fischbach J, et al. Retrospective comparison of the effectiveness of various treatment modalities of extragastric MALT lymphoma: a single-center analysis. Ann Hematol. 2014 Aug;93(8):1287–1295.
  • Teckie S, Qi S, Lovie S, et al. Long-term outcomes and patterns of relapse of early-stage extranodal marginal zone lymphoma treated with radiation therapy with curative intent. Int J Radiat Oncol Biol Phys. 2015 May 1;92(1):130–137.
  • Wöhrer S, Streubel B, Bartsch R, et al. Monoclonal immunoglobulin production is a frequent event in patients with mucosa-associated lymphoid tissue lymphoma. Clin Cancer Res. 2004 Nov 1;10(21):7179–7181.
  • Yoo C, Yoon DH, Yoon S, et al. Prognostic impact of β2-microglobulin in patients with non-gastric mucosa-associated lymphoid tissue lymphoma. Leuk Lymphoma. 2015;56(3):688–693.
  • Zucca E, Bertoni F. The spectrum of MALT lymphoma at different sites: biological and therapeutic relevance. Blood. 2016 Apr 28;127(17):2082–2092.
  • Wöhrer S, Troch M, Streubel B, et al. MALT lymphoma in patients with autoimmune diseases: a comparative analysis of characteristics and clinical course. Leukemia. 2007;21(8):1812–1818.
  • Thieblemont C, Cascione L, Conconi A, et al. A MALT lymphoma prognostic index. Blood. 2017 Sep 21;130(12):1409–1417.
  • Bertoni F, Rossi D, Zucca E. Recent advances in understanding the biology of marginal zone lymphoma. F1000Res. 2018;7:406.
  • 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.
  • Farinha P, Gascoyne RD. Helicobacter pylori and MALT lymphoma. Gastroenterology. 2005 May;128(6):1579–1605.
  • Sagaert X, Van Cutsem E, De Hertogh G, et al. Gastric MALT lymphoma: a model of chronic inflammation-induced tumor development. Nat Clin Pract Gastroenterol Hepatol. 2010;7(6):336–346. .
  • García M, Bellosillo B, Sánchez-González B, et al. Study of regulatory T-cells in patients with gastric MALT lymphoma: influence on treatment response and outcome. Plos One. 2012;7(12):e51681.
  • Du MQ. MALT lymphoma: a paradigm of NF-κB dysregulation. Semin Cancer Biol. 2016 Aug;39:49–60.
  • Thieblemont C, Bertoni F, Copie-Bergman C, et al. Chronic inflammation and extra-nodal marginal-zone lymphomas of MALT-type. Semin Cancer Biol. 2014 Feb;24:33–42.
  • Streubel B, Seitz G, Stolte M, et al. MALT lymphoma associated genetic aberrations occur at different frequencies in primary and secondary intestinal MALT lymphomas. Gut. 2006 Nov;55(11):1581–1585.
  • Ye H, Liu H, Attygalle A, et al. Variable frequencies of t(11;18)(q21;q21) in MALT lymphomas of different sites: significant association with CagA strains of H pylori in gastric MALT lymphoma. Blood. 2003 Aug 1;102(3):1012–1018.
  • Liu H, Ye H, Ruskone-Fourmestraux A, et al. T(11;18) is a marker for all stage gastric MALT lymphomas that will not respond to H. pylori eradication. Gastroenterology 2002 May;122(5):1286–1294.
  • Huang X, Zhang Z, Liu H, et al. T(11;18)(q21;q21) in gastric MALT lymphoma and diffuse large B-cell lymphoma of Chinese patients. Hematol J. 2003;4(5):342–345.
  • Toyoda K, Maeshima AM, Nomoto J, et al. Mucosa-associated lymphoid tissue lymphoma with t(11;18)(q21;q21) translocation: long-term follow-up results. Ann Hematol. 2019 Jul;98(7):1675–1687.
  • Lévy M, Copie-Bergman C, Gameiro C, et al. Prognostic value of translocation t(11;18) in Tumoral response of low-grade gastric lymphoma of mucosa-associated lymphoid tissue type to oral chemotherapy. J Clin Oncol. 2005;23(22):5061–5066.
  • Streubel B, Ye H, Du MQ, et al. Translocation t(11;18)(q21;q21) is not predictive of response to chemotherapy with 2CdA in patients with gastric MALT lymphoma. Oncology. 2004;66(6):476–480.
  • Salar A, Domingo-Domenech E, Panizo C, et al. First-line response-adapted treatment with the combination of bendamustine and rituximab in patients with mucosa-associated lymphoid tissue lymphoma (MALT2008-01): a multicentre, single-arm, phase 2 trial. Lancet Haematol. 2014 Dec;1(3):e104–11.
  • Ye H, Gong L, Liu H, et al. Strong BCL10 nuclear expression identifies gastric MALT lymphomas that do not respond to H pylori eradication. Gut. 2006;55(1):137.
  • Franco R, Camacho FI, Caleo A, et al. Nuclear bcl10 expression characterizes a group of ocular adnexa MALT lymphomas with shorter failure-free survival. Mod Pathol. 2006;19(8):1055–1067.
  • Streubel B, Vinatzer U, Lamprecht A, et al. T(3;14)(p14.1;q32) involving IGH and FOXP1 is a novel recurrent chromosomal aberration in MALT lymphoma. Leukemia. 2005 Apr;19(4):652–658.
  • Sagaert X, De Paepe P, Libbrecht L, et al. Forkhead box protein P1 Expression in mucosa-associated lymphoid tissue lymphomas predicts poor prognosis and transformation to diffuse large B-cell lymphoma. J Clin Oncol. 2006;24(16):2490–2497.
  • Huang W, Guo L, Liu H, et al. C-MYC overexpression predicts aggressive transformation and a poor outcome in mucosa-associated lymphoid tissue lymphomas. Int J Clin Exp Pathol. 2014;7(9):5634–5644.
  • Kiesewetter B, Simonitsch-Klupp I, Kornauth C, et al. Immunohistochemical expression of cereblon and MUM1 as potential predictive markers of response to lenalidomide in extranodal marginal zone B-cell lymphoma of the mucosa-associated lymphoid tissue (MALT lymphoma). Hematol Oncol. 2018 Feb;36(1):62–67.
  • Peng H, Chen G, Du M, et al. Replication error phenotype and p53 gene mutation in lymphomas of mucosa-associated lymphoid tissue. Am J Pathol. 1996 Feb;148(2):643–648.
  • Du M, Peng H, Singh N, et al. The accumulation of p53 abnormalities is associated with progression of mucosa-associated lymphoid tissue lymphoma. Blood. 1995 Dec 15;86(12):4587–4593.
  • Cascione L, Rinaldi A, Bruscaggin A, et al. Novel insights into the genetics and epigenetics of MALT lymphoma unveiled by next generation sequencing analyses. Haematologica. 2019 Dec;104(12):e558–e561.
  • Huh SJ, Oh SY, Lee S, et al. Mutational analysis of extranodal marginal zone lymphoma using next generation sequencing. Oncol Lett. 2020;20(5):205.
  • Moody S, Thompson JS, Chuang SS, et al. Novel GPR34 and CCR6 mutation and distinct genetic profiles in MALT lymphomas of different sites. Haematologica. 2018 Aug;103(8):1329–1336.
  • Schreuder MI, Van Den Brand M, Hebeda KM, et al. Novel developments in the pathogenesis and diagnosis of extranodal marginal zone lymphoma. J Hematopathol. 2017;10(3):91–107
  • Hyeon J, Lee B, Shin S-H, et al. Targeted deep sequencing of gastric marginal zone lymphoma identified alterations of TRAF3 and TNFAIP3 that were mutually exclusive for MALT1 rearrangement. Mod Pathol. 2018;31(9):1418–1428.
  • Kuo SH, Wu MS, Yeh KH, et al. Novel insights of lymphomagenesis of helicobacter pylori-dependent gastric mucosa-associated lymphoid tissue lymphoma. Cancers (Basel). 2019 Apr 17;11(4):547.
  • Ziepert M, Hasenclever D, Kuhnt E, et al. Standard international prognostic index remains a valid predictor of outcome for patients with aggressive CD20+ B-cell lymphoma in the rituximab era. J Clin Oncol. 2010 May 10;28(14):2373–2380.
  • Troch M, Wöhrer S, Raderer M. Assessment of the prognostic indices IPI and FLIPI in patients with mucosa-associated lymphoid tissue lymphoma. Anticancer Res. 2010 Feb;30(2):635–639.
  • Heilgeist A, McClanahan F, Ho AD, et al. Prognostic value of the follicular lymphoma international prognostic index score in marginal zone lymphoma. Cancer. 2013;119(1):99–106.
  • Casulo C, Byrtek M, Dawson KL, et al. Early relapse of follicular lymphoma after rituximab plus cyclophosphamide, doxorubicin, vincristine, and prednisone defines patients at high risk for death: an analysis from the national lymphocare study. J Clin Oncol. 2015;33(23):2516–2522.
  • Conconi A, Thieblemont C, Cascione L, et al. Early progression of disease predicts shorter survival in MALT lymphoma patients receiving systemic treatment. Haematologica. 2020;105(11): 237990. .
  • Raderer M, How KB. I treat MALT lymphoma: ‘a subjective interpretation of the gospel according to Isaacson. ESMO Open. 2020;5(4):e000812.
  • Kiesewetter B, Lamm W, Neuper O, et al. Prolonged follow-up on lenalidomide-based treatment for mucosa-associated lymphoid tissue lymphoma (MALT lymphoma)-Real-world data from the Medical University of Vienna. Hematol Oncol. 2019 Oct;37(4):345–351.
  • Ladetto M, Dreyling M. on behalf of the EHA GC. EHA endorsement of ESMO clinical practice guidelines for marginal zone lymphomas. HemaSphere 2020;4(2):2.
  • Fischbach W, Goebeler ME, Ruskone-Fourmestraux A, et al. Most patients with minimal histological residuals of gastric MALT lymphoma after successful eradication of Helicobacter pylori can be managed safely by a watch and wait strategy: experience from a large international series. Gut. 2007 Dec;56(12):1685–1687.
  • Kiesewetter B, Troch M, Mayerhoefer ME, et al. Delayed efficacy after treatment with lenalidomide or thalidomide in patients with mucosa-associated lymphoid tissue lymphoma. Oncologist. 2016;21(1):72–75.
  • Kiesewetter B, Simonitsch-Klupp I, Dolak W, et al. Depth of remission following first-line treatment is an independent prognostic marker for progression-free survival in gastric Mucosa-Associated Lymphoid Tissue (MALT) lymphoma. Cancers (Basel). 2020 Feb 20;12(2):492.
  • Hancock BW, Qian W, Linch D, et al. Chlorambucil versus observation after anti-Helicobacter therapy in gastric MALT lymphomas: results of the international randomised LY03 trial. Br J Haematol. 2009;144(3):367–375.
  • Tanimoto K, Kaneko A, Suzuki S, et al. Long-term follow-up results of no initial therapy for ocular adnexal MALT lymphoma. Ann Oncol. 2006 Jan;17(1):135–140.
  • Troch M, Streubel B, Petkov V, et al. Does MALT lymphoma of the lung require immediate treatment? An analysis of 11 untreated cases with long-term follow-up. Anticancer Res. 2007 Sep-Oct;27(5b):3633–3637.
  • Kiesewetter B, Willenbacher E, Willenbacher W, et al. A phase 2 study of rituximab plus lenalidomide for mucosa-associated lymphoid tissue lymphoma. Blood. 2017 Jan 19;129(3):383–385.
  • Ferreri AJM, Cecchetti C, Kiesewetter B, et al. Clarithromycin as a “repurposing drug” against MALT lymphoma. Br J Haematol. 2018 Sep;182(6):913–915.
  • Ferreri AJ, Sassone M, Kiesewetter B, et al. High-dose clarithromycin is an active monotherapy for patients with relapsed/refractory extranodal marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT): the HD-K phase II trial. Ann Oncol. 2015 Aug;26(8):1760–1765.
  • Kiesewetter B, Neuper O, Mayerhoefer ME, et al. A pilot phase II study of ofatumumab monotherapy for extranodal marginal zone B-cell lymphoma of the mucosa-associated lymphoid tissue (MALT) lymphoma. Hematol Oncol. 2018 Feb;36(1):49–55.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.