Splenic marginal zone lymphoma: a review of the clinical presentation, pathology, molecular biology, and management

References

• Schmid C, Kirkham N, Diss T, Isaacson PG. Splenic marginal zone lymphoma. Am J Surg Pathol. 1992;16(5):455–466.
   PubMed Web of Science ®Google Scholar
• Isaacson PG, Piris MA, Berger F, et al. In: Swerdlow SH, Campos E, Harris NL, et al. WHO Classification of Tumours of the Haematopoietic and Lymphoid Tissues, 4th ed. Lyon, France: IARC Press, 2008. 289–291.
   Google Scholar
• Papadaki T, Stamatopoulos K, Belessi C, et al. Splenic marginal-zone lymphoma: one or more entities? A histologic, immunohistochemical, and molecular study of 42 cases. Am J Surg Pathol. 2007;31(3):438–446.
   PubMed Web of Science ®Google Scholar
• Arcaini L, Zibellini S, Passamonti F, et al. Splenic marginal zone lymphoma: Clinical clustering of immunoglobulin heavy chain repertoires. Blood Cells Mol Dis. 2009;42(3):286–291.
   Web of Science ®Google Scholar
• Franco V, Florena AM, Iannitto E. Splenic marginal zone lymphoma. Blood. 2003;101(7):2464–2472.
   PubMed Web of Science ®Google Scholar
• Murakami H, Irisawa H, Saitoh T, et al. Immunological abnormalities in splenic marginal zone cell lymphoma. Am J Hematol. 1997;56(3):173–178.
   Web of Science ®Google Scholar
• Satoh T, Yamada T, Nakano S, et al. The relationship between primary splenic malignant lymphoma and chronic liver disease associated with hepatitis C virus infection. Cancer. 1997;80(10):1981–1988.
   Web of Science ®Google Scholar
• Bates I, Bedu-Addo G, Rutherford TR, Bevan DH. Circulating villous lymphocytes – a link between hyperreactive malarial splenomegaly and splenic lymphoma. Trans R Soc Trop Med Hyg. 1997;91(2):171–174.
   Web of Science ®Google Scholar
• Matutes E. Splenic marginal zone lymphoma: disease features and management. Expert Rev Hematol. 2013;6(6):735–745.
   PubMed Web of Science ®Google Scholar
• Arcaini L, Bruno R. Hepatitis C virus infection and antiviral treatment in marginal zone lymphomas. Curr Clin Pharmacol. 2010;5(2):74–81.
   Google Scholar
• Kalpadakis C, Pangalis GA, Dimitriadou E, et al. Mutation analysis of IgVH genes in splenic marginal zone lymphomas: correlation with clinical characteristics and outcome. Anticancer Res. 2009;29(5):1811–1816.
   PubMed Web of Science ®Google Scholar
• Algara P, Mateo MS, Sanchez-Beato M, et al. Analysis of the IgVH somatic mutations in splenic marginal zone lymphoma defines a group of unmutated cases with frequent 7q deletion and adverse clinical course. Blood. 2002;99(4):1299–1304.
   Web of Science ®Google Scholar
• Wallace S, Bedu-Addo G, Rutherford TR, Bates I. Serological similarities between hyperreactive malarial splenomegaly and splenic lymphoma in west Africa. Trans R Soc Trop Med Hyg. 1998;92(4):463–467.
   Web of Science ®Google Scholar
• Xochelli A, Kalpadakis C, Gardiner A, et al. Clonal B-cell lymphocytosis exhibiting immunophenotypic features consistent with a marginal-zone origin: is this a distinct entity? Blood. 2014;123(8):1199–1206.
   PubMed Web of Science ®Google Scholar
• Thieblemont C, Felman P, Callet-Bauchu E, et al. Splenic marginal-zone lymphoma: a distinct clinical and pathological entity. Lancet Oncol. 2003;4(2):95–103.
   PubMed Web of Science ®Google Scholar
• Arcaini L, Lazzarino M, Colombo N, et al; Integruppo Italiano Linfomi. Splenic marginal zone lymphoma: a prognostic model for clinical use. Blood. 2006;107(12):4643–4649.
   PubMed Web of Science ®Google Scholar
• Troussard X, Valensi F, Duchayne E, et al. Splenic lymphoma with villous lymphocytes: clinical presentation, biology and prognostic factors in a series of 100 patients. Groupe Francais d’Hématologie Cellulaire (GFHC). Br J Haematol. 1996;93(3):731–736.
   PubMed Web of Science ®Google Scholar
• Chacón JI, Mollejo M, Muñoz E, et al. Splenic marginal zone lymphoma: clinical characteristics and prognostic factors in a series of 60 patients. Blood. 2002;100(5):1648–1654.
   PubMed Web of Science ®Google Scholar
• Matutes E, Oscier D, Montalban C, et al. Splenic marginal zone lymphoma proposals for a revision of diagnostic, staging and therapeutic criteria. Leukemia. 2008;22(3):487–495.
   PubMed Web of Science ®Google Scholar
• Hammer RD, Glick AD, Greer JP, Collins RD, Cousar JB. Splenic marginal zone lymphoma. A distinct B-cell neoplasm. Am J Surg Pathol. 1996;20(5):613–626.
   Web of Science ®Google Scholar
• Duong Van Huyen JP, Molina T, Delmer A, et al. Splenic marginal zone lymphoma with or without plasmacytic differentiation. Am J Surg Pathol. 2000;24(12):1581–1592.
   Web of Science ®Google Scholar
• Franco V, Florena AM, Stella M, et al. Splenectomy influences bone marrow infiltration in patients with splenic marginal zone cell lymphoma with or without villous lymphocytes. Cancer. 2001;91(2):294–301.
   Web of Science ®Google Scholar
• Wu CD, Jackson CL, Medeiros LJ. Splenic marginal zone lymphoma. An immunophenotypic and molecular study of five cases. Am J Clin Pathol. 1996;105(3):277–285.
   Web of Science ®Google Scholar
• Rosso R, Castello A, Colosini G, Astori C, Lazzarino M, Magrini U. Splenic marginal zone cell lymphoma involving liver and bone marrow. Report of a case with protracted follow-up, showing progressive disappearance of the lymphoma after splenectomy. Haematologica. 1996;81(1):44–46.
   Web of Science ®Google Scholar
• Mollejo M, Algara P, Mateo MS, et al. Splenic small B-cell lymphoma with predominant red pulp involvement: a diffuse variant of splenic marginal zone lymphoma? Histopathology. 2002;40(1):22–30.
   Web of Science ®Google Scholar
• Berger F, Felman P, Thieblemont C, et al. Non-MALT marginal zone B-cell lymphomas: a description of clinical presentation and outcome in 124 patients. Blood. 2000;95(6):1950–1956.
   PubMed Web of Science ®Google Scholar
• Orero MT, Miguel-Sosa A, Matutes E, et al. A soft tissue extranodal mass as an initial manifestation of splenic lymphoma with circulating villous lymphocytes. Br J Haematol. 1998;103(4):1213–1214.
   Web of Science ®Google Scholar
• Yamazaki K, Shimizu S, Negami T, et al. Leukemic meningitis in a patient with splenic lymphoma with villous lymphocytes (SLVL). Meningitis as a possible initial manifestation of SLVL. Cancer. 1994;74(1):61–65.
   Web of Science ®Google Scholar
• Gotlib V, Singareddy S, Gergis U, et al. Leptomeningeal involvement in a patient with splenic lymphoma with villous lymphocytes. Leuk Lymphoma. 2002;43(6):1337–1340.
   PubMed Web of Science ®Google Scholar
• Gruszka-Westwood AM, Hamoudi RA, Matutes E, Tuset E, Catovsky D. p53 abnormalities in splenic lymphoma with villous lymphocytes. Blood. 2001;97(11):3552–3558.
   Web of Science ®Google Scholar
• Zibellini S, Capello D, Forconi F, et al. Stereotyped patterns of B-cell receptor in splenic marginal zone lymphoma. Haematologica. 2010;95(10):1792–1796.
   PubMed Web of Science ®Google Scholar
• Bikos V, Darzentas N, Hadzidimitriou A, et al. Over 30% of patients with splenic marginal zone lymphoma express the same immunoglobulin heavy variable gene: ontogenetic implications. Leukemia. 2012;26(7):1638–1646.
   Web of Science ®Google Scholar
• Oscier D, Owen R, Johnson S. Splenic marginal zone lymphoma. Blood Rev. 2005;19(1):39–51.
   Web of Science ®Google Scholar
• Remstein ED, Law M, Mollejo M, Piris MA, Kurtin P, Dogan A. IGH translocation and 7 deletions are frequent genetic abnormalities in splenic marginal zone lymphoma and are present in mutually exclusive subjects [abstract]. XIII meeting of the European Association for Haematopathology, Vienna, Austria, 2006, LO8.
   Google Scholar
• Dierlamm J, Rosenberg C, Stul M, et al. Characteristic pattern of chromosomal gains and losses in marginal zone B cell lymphoma detected by comparative genomic hybridization. Leukemia. 1997;11(5):747–758.
   PubMed Web of Science ®Google Scholar
• Hernández JM, García JL, Gutiérrez NC, et al. Novel genomic imbalances in B-cell splenic marginal zone lymphomas revealed by comparative genomic hybridization and cytogenetics. Am J Pathol. 2001;158(5):1843–1850.
   Web of Science ®Google Scholar
• Andersen CL, Gruszka-Westwood A, Atkinson S, et al. Recurrent genomic imbalances in B-cell splenic marginal-zone lymphoma revealed by comparative genomic hybridization. Cancer Genet Cytogenet. 2005;156(2):122–128.
   Google Scholar
• Boonstra R, Bosga-Bouwer A, van Imhoff GW, et al. Splenic marginal zone lymphomas presenting with splenomegaly and typical immunophenotype are characterized by allelic loss in 7q31-32. Mod Pathol. 2003;16(12):1210–1217.
   Web of Science ®Google Scholar
• Watkins AJ, Huang Y, Ye H, et al. Splenic marginal zone lymphoma: characterization of 7q deletion and its value in diagnosis. J Pathol. 2010;220(4):461–474.
   Web of Science ®Google Scholar
• Fresquet V, Robles EF, Parker A, et al. High-throughput sequencing analysis of the chromosome 7q32 deletion reveals IRF5 as a potential tumour suppressor in splenic marginal-zone lymphoma. Br J Haematol. 2012;158(6):712–726.
   PubMed Web of Science ®Google Scholar
• Watkins AJ, Hamoudi RA, Zeng N, et al. An integrated genomic and expression analysis of 7q deletion in splenic marginal zone lymphoma. PLoS One. 2012;7(9):e44997.
   PubMed Web of Science ®Google Scholar
• Rossi D, Trifonov V, Fangazio M, et al. The coding genome of splenic marginal zone lymphoma: activation of NOTCH2 and other pathways regulating marginal zone development. J Exp Med. 2012;209(9):1537–1551.
   PubMed Web of Science ®Google Scholar
• Kiel MJ, Velusamy T, Betz BL, et al. Whole-genome sequencing identifies recurrent somatic NOTCH2 mutations in splenic marginal zone lymphoma. J Exp Med. 2012;209(9):1553–1565.
   PubMed Web of Science ®Google Scholar
• Martínez N, Almaraz C, Vaqué JP, et al. Whole-exome sequencing in splenic marginal zone lymphoma reveals mutations in genes involved in marginal zone differentiation. Leukemia. 2014;28(6):1334–1340.
   PubMed Web of Science ®Google Scholar
• Parry M, Rose-Zerilli MJ, Gibson J, et al. Whole exome sequencing identifies novel recurrently mutated genes in patients with splenic marginal zone lymphoma. PLoS One. 2013;8(12):e83244.
   Web of Science ®Google Scholar
• Radtke F, MacDonald HR, Tacchini-Cottier F. Regulation of innate and adaptive immunity by Notch. Nat Rev Immunol. 2013;13(6):427–437.
   PubMed Web of Science ®Google Scholar
• Kuroda K, Han H, Tani S, et al. Regulation of marginal zone B cell development by MINT, a suppressor of Notch/RBP-J signaling pathway. Immunity. 2003;18(2):301–312.
   PubMed Web of Science ®Google Scholar
• Saito T, Chiba S, Ichikawa M, et al. Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity. 2003;18(5):675–685.
   PubMed Web of Science ®Google Scholar
• Trøen G, Wlodarska I, Warsame A, Hernández Llodrà S, De Wolf-Peeters C, Delabie J. NOTCH2 mutations in marginal zone lymphoma. Haematologica. 2008;93(7):1107–1109.
   Web of Science ®Google Scholar
• Staudt LM. Oncogenic activation of NF-kappaB. Cold Spring Harb Perspect Biol. 2010;2(6):a000109.
   PubMed Web of Science ®Google Scholar
• Du MQ. MALT lymphoma: many roads lead to nuclear factor-κb activation. Histopathology. 2011;58(1):26–38.
   PubMed Web of Science ®Google Scholar
• Shaffer AL, Young RM, Staudt LM. Pathogenesis of human B cell lymphomas. Annu Rev Immunol. 2012;30:565–610.
   PubMed Web of Science ®Google Scholar
• Rossi D, Deaglio S, Dominguez-Sola D, et al. Alteration of BIRC3 and multiple other NF-κB pathway genes in splenic marginal zone lymphoma. Blood. 2011;118(18):4930–4934.
   Web of Science ®Google Scholar
• Yan Q, Huang Y, Watkins AJ, et al. BCR and TLR signaling pathways are recurrently targeted by genetic changes in splenic marginal zone lymphomas. Haematologica. 2012;97(4):595–598.
   PubMed Web of Science ®Google Scholar
• Tierens A, Delabie J, Michiels L, Vandenberghe P, De Wolf-Peeters C. Marginal-zone B cells in the human lymph node and spleen show somatic hypermutations and display clonal expansion. Blood. 1999;93(1):226–234.
   Web of Science ®Google Scholar
• Mulligan SP, Matutes E, Dearden C, Catovsky D. Splenic lymphoma with villous lymphocytes: natural history and response to therapy in 50 cases. Br J Haematol. 1991;78(2):206–209.
   Web of Science ®Google Scholar
• Hockley SL, Else M, Morilla A, et al. The prognostic impact of clinical and molecular features in hairy cell leukaemia variant and splenic marginal zone lymphoma. Br J Haematol. 2012;158(3):347–354.
   Web of Science ®Google Scholar
• Montalbán C, Abraira V, Arcaini L, et al; Splenic Marginal Zone Lymphoma Study Group. Risk stratification for Splenic Marginal Zone Lymphoma based on haemoglobin concentration, platelet count, high lactate dehydrogenase level and extrahilar lymphadenopathy: development and validation on 593 cases. Br J Haematol. 2012;159(2):164–171.
   PubMed Web of Science ®Google Scholar
• Montalban C, Abraira V, Arcaini L, et al; Splenic Marginal Zone Lymphoma Study Group (SMZLSG). Simplification of risk stratification for splenic marginal zone lymphoma: a point-based score for practical use. Leuk Lymphoma. 2014;55(4):929–931.
   PubMed Web of Science ®Google Scholar
• Salido M, Baró C, Oscier D, et al. Cytogenetic aberrations and their prognostic value in a series of 330 splenic marginal zone B-cell lymphomas: a multicenter study of the Splenic B-Cell Lymphoma Group. Blood. 2010;116(9):1479–1488.
   PubMed Web of Science ®Google Scholar
• Parry-Jones N, Matutes E, Gruszka-Westwood AM, Swansbury GJ, Wotherspoon AC, Catovsky D. Prognostic features of splenic lymphoma with villous lymphocytes: a report on 129 patients. Br J Haematol. 2003;120(5):759–764.
   PubMed Web of Science ®Google Scholar
• Iannito E, Ambrosetti A, Ammatuna E, et al. Splenic marginal zone lymphoma with or without villous lymphocytes. Hematologic findings and outcomes in a series of 57 patients. Cancer. 2004;101(9):2050–2057.
   Web of Science ®Google Scholar
• Tsimberidou AM, Catovsky D, Schlette E, et al. Outcomes in patients with splenic marginal zone lymphoma and marginal zone lymphoma treated with rituximab with or without chemotherapy or chemotherapy alone. Cancer. 2006;107(1):125–135.
   PubMed Web of Science ®Google Scholar
• Bennett M, Schechter GP. Treatment of splenic marginal zone lymphoma: splenectomy versus rituximab. Semin Hematol. 2010;47(2):143–147.
   PubMed Web of Science ®Google Scholar
• Arcaini L, Paulli M, Boveri E, et al. Splenic and nodal marginal zone lymphomas are indolent disorders at high hepatitis C virus seroprevalence with distinct presenting features but similar morphologic and phenotypic profiles. Cancer. 2004;100(1):107–115.
   PubMed Web of Science ®Google Scholar
• Hermine O, Lefrère F, Bronowicki JP, et al. Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. N Engl J Med. 2002;347(2):89–94.
   PubMed Web of Science ®Google Scholar
• Kelaidi C, Rollot F, Park S, et al. Response to antiviral treatment in hepatitis C virus-associated marginal zone lymphomas. Leukemia. 2004;18(10):1711–1716.
   PubMed Web of Science ®Google Scholar
• Bennett M, Yegena S, Dave HP, Schechter GP. Re: Rituximab monotherapy is highly effective in splenic marginal zone lymphoma. Hematol Oncol. 2008;26(2):114.
   Web of Science ®Google Scholar
• Kalpadakis C, Pangalis GA, Dimopoulou MN, et al. Rituximab monotherapy is highly effective in splenic marginal zone lymphoma. Hematol Oncol. 2007;25(3):127–131.
   Web of Science ®Google Scholar
• Kalpadakis C, Pangalis GA, Angelopoulou MK, et al. Treatment of splenic marginal zone lymphoma with rituximab monotherapy: progress report and comparison with splenectomy. Oncologist. 2013;18(2):190–197.
   PubMed Web of Science ®Google Scholar