B-cell lymphoma, unclassifiable, intermediate between diffuse large B-cell lymphoma and Burkitt’s lymphoma
- Authors: Baryakh EA1, Misyurina AE1, Kovrigina AM1, Misyurin VA1, Kravchenko SK1
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Affiliations:
- «Гематологический научный центр» Минздрава России
- Issue: Vol 87, No 4 (2015)
- Pages: 91-97
- Section: Editorial
- URL: https://journals.rcsi.science/0040-3660/article/view/31760
- ID: 31760
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Full Text
Abstract
B-cell lymphoma that is unclassifiable and intermediate between diffuse large B-cell lymphoma (DLBCL) and Burkitt’s lymphoma (BL) — (UBL) is an aggressive lymphoma that has simultaneously morphological, immunophenotypical, and cytogenetic signs of both DLBCL and LB. At the same time due to its biological characteristics and clinical manifestations, UBL cannot be referred to as one of the above nosological entities. UBL has been first identified as an individual nosological entity in the 2008 World Health Organization classification. The review details the epidemiology, clinical manifestations, morphological pattern, immunophenotypic and karyotypic features, as well as therapeutic approaches and prognostic factors.
About the authors
E A Baryakh
«Гематологический научный центр» Минздрава РоссииМосква, Россия
A E Misyurina
«Гематологический научный центр» Минздрава РоссииМосква, Россия
A M Kovrigina
«Гематологический научный центр» Минздрава РоссииМосква, Россия
V A Misyurin
«Гематологический научный центр» Минздрава РоссииМосква, Россия
S K Kravchenko
«Гематологический научный центр» Минздрава РоссииМосква, Россия
References
- Kluin P.M., Harris N.L., Stein H., Leoncini L., Raphael M., Campo E., Jaffe E.S. B-cell lymphoma, unclassifiable with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma in Who Classification of tumors of haematopoietic and lymphoid tissues, ed. by S.H. Swerdlow, E. Campo, N.L. Harris, E.S. Jaffe, S.A. Pileri, H. Stein, J. Thiele, J.W. Vardiman. Lyon: International Agency for Reaearch on Cancer 2008; 265—266.
- Jaffe E.S., Pittaluga S. Aggressive B-cell lymphomas: a review of new and old entities in the WHO classification. Hematology. Am Soc Hematol Educ Program 2011; 2011: 506—514.
- Hasserjian R.P., Ott G., Elenitoba-Johnson K.S., Balague-Ponz O., de Jong D., de Leval L. Commentary on the WHO classification of tumors of lymphoid tissues (2008): «Gray zone» lymphomas overlapping with Burkitt lymphoma or classical Hodgkin lymphoma. J Hematopathol 2009; 2: 89—95.
- Hummel M., Bentink S., Berger H., Klapper W., Wessendorf S., Barth T.F., Bernd H.W., Cogliatti S.B., Dierlamm J., Feller A.C., Hansmann M.L., Haralambieva E., Harder L., Hasenclever D., Kühn M., Lenze D., Lichter P., Martin-Subero JI., Möller P., Müller-Hermelink H.K., Ott G., Parwaresch R.M., Pott C., Rosenwald A., Rosolowski M., Schwaenen C., Stürzenhofecker B., Szczepanowski M., Trautmann H., Wacker H.H., Spang R., Loeffler M., Trümper L., Stein H., Siebert R. Molecular Mechanisms in Malignant Lymphomas Network Project of the Deutsche Krebshilfe. A Biologic Definition of Burkitt’s Lymphoma from Transcriptional and Genomic Profiling. N Engl J Med 2006; 354: 2419—2430.
- Motlló C., Grau J., Juncà J., Ruiz N., Mate J.L., Orna E., Navarro J.T., Vives S., Sancho J.M., Esteban D., Granada I., Feliu E., Ribera J.M., Millá F. Translocation (3;8)(q27;q24) in two cases of triple hit lymphoma. Cancer Genet Cytogenet 2010; 203(2): 328—332.
- Seegmiller A.C., Garcia R, Huang R., Huang R., Maleki A., Karandikar N.J., Chen W. Simple karyotype and bcl-6 expression predict a diagnosis of Burkitt lymphoma and better survival in IG-MYC rearranged high-grade B-cell lymphomas. Modern Pathol 2010; 23: 909—920.
- Yamamoto K., Matsuoka H., Yakushijin K., Miyata Y., Okamura A., Kawano S., Matsuoka H., Minami H. A novel five-way translocation, t(3;9;13;8;14)(q27;p13;q32;q24;q32), with concurrent MYC and BCL6 rearrangements in a primary bone marrow B-cell lymphoma. Cancer Genet 2011; 204: 501—506.
- Ahn J.Y., Seo Y.H., Park P.W., Kim K.H., Park M.J., Jeong J.H., Park S.H., Song Y.H. A case of B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma in a Korean child. Ann Lab Med 2012; 32 (2): 162—166.
- Lu B., Zhou C., Yang W., Huang H., Gao Z., He Y., Liu H., Zhou X., Gong L. Morphological, immunophenotypic and molecular characterization of mature aggressive B-cell lymphomas in Chinese pediatric patients. Leuk Lymphoma 2011; 52 (12): 2356—2364.
- Pervez S., Raza M.Q., Mirza A., Pal A. Strong BCL2 expression in Burkitt lymphoma is not uncommon in adults. Indian J Pathol Microbiol 2011; 54 (2): 290—293.
- Kanungo A., Medeiros L.J., Abruzzo L.V., Lin P. Lymphoid neoplasms associated with concurrent t(14;18) and 8q24/c-MYC translocation generally have a poor prognosis. Modern Pathol 2006; 19: 25—33.
- Le Gouill S., Talmant P., Touzeau C., Moreau A., Garand R., Juge-Morineau N., Gaillard F., Gastinne T., Milpied N., Moreau P., Harousseau J.L., Avet-Loiseau H. The clinical presentation and prognosis of diffuse large B-cell lymphoma with t(14;18) and 8q24/c-MYC rearrangement. Haematologica 2007; 92: 1335—1342.
- Tomita N., Tokunaka M., Nakamura N., Takeuchi K., Koike J., Motomura S., Miyamoto K., Kikuchi A., Hyo R., Yakushijin Y., Masaki Y., Fujii S., Hayashi T., Ishigatsubo Y., Miura I. Clinicopathological features of lymphoma/leukemia patients carrying both BCL2 and MYC translocations. Haematologica 2009; 94 (7): 935—943.
- Johnson N.A., Savage K.J., Ludkovski O., Ben-Neriah S., Woods R., Steidl C., Dyer M.J., Siebert R., Kuruvilla J., Klasa R., Connors J.M., Gascoyne R.D., Horsman D.E. Lymphomas with concurrent BCL2 and MYC translocations: the critical factors associated with survival. Blood 2009; 114: 2273—2279.
- Niitsu N., Okamoto M., Miura I., Hirano M. Clinical features and prognosis of de novo diffuse large B-cell lymphoma with t(14;18) and 8q24/c-MYC translocations. Leukemia 2009; 23: 777—783.
- Snuderl M., Kolman O.K., Chen Y.B., Hsu J.J., Ackerman A.M., Dal Cin P., Ferry J.A., Harris N.L., Hasserjian R.P., Zukerberg L.R., Abramson J.S., Hochberg E.P., Lee H., Lee A.I., Toomey C.E., Sohani A.R. B-cell lymphomas with concurrent IGH-BCL2 and MYC rearrangements are aggressive neoplasms with clinical and pathologic features distinct from Burkitt lymphoma and diffuse large B-cell lymphoma. Am J Surg Pathol 2010; 34 (3): 327—340.
- Greenwood M., Armytage T., Fay K., Coyle L., Kerrdge I., Arthur C., McIlroy K., MacKinlay N., Ward C., Stevenson W. Outcomes of allogeneic stem cell transplantation for non-Hodgkin lymphoma with concurrent MYC and BCL2 translocations: a single center retrospective analysis. Hematol Oncol 2013; 3 (Suppl. 1): 103.
- Oki Y., Noorani M., Davis R.E., Davis R.E., Neelapu S.S., Ma L., Ahmed M., Rodriguez M.A., Hagemeister F.B., Fowler N., Wang M., Fanale M.A., Nastoupil L., Samaniego F, Lee H.J., Dabaja B.S., Pinnix C.C., Medeiros L.J., Nieto Y., Khouri I., Kwak L.W., Turturro F., Romaguera J.E., Fayad L.E., Westin J.R. Double hit lymphoma: M.D. Anderson Experince. Blood 2013; 122 (21): 1776.
- Sun H., Savage K., Karsan A. Outcome of patients wits double-hit lymphomas treated with CODOX-M/IVAC + R followed by hematopoietic stem cell transplantation in British Columbia. Blood 2013; 122 (21): 1788.
- Petrich A.M., Gandhi M., Jovanovic B., Castillo J.J., Rajguru S., Yang D.T., Shah K.A., Whyman J.D., Lansigan F., Hernandez-Ilizaliturri F.J., Lee L.X., Barta S.K., Melinamani S., Karmali R., Adeimy C., Smith S., Dalal N., Nabhan C., Peace D., Vose J., Evens A.M., Shah N., Fenske T.S., Zelenetz A.D., Landsburg D.J., Howlett C., Mato A., Jaglal M., Chavez J.C., Tsai J.P., Reddy N., Li S., Handler C, Flowers C.R., Cohen J.B., Blum K.A., Song K., Sun H.L, Press O., Cassaday R., Jaso J., Medeiros L.J., Sohani A.R., Abramson J.S. Impact of induction regimen and stem cell transplantation on outcomes in double-hit lymphoma: a multicenter retrospective analysis. Blood 2014; 124 (15): 2354—2361.
- Aukema S.M., Siebert R., Schuuring E., van Imhoff G.W., Kluin-Nelemans H.C., Boerma E.J., Kluin P.M. Double-hit B-cell lymphomas. Blood 2011; 117 (8): 2319—2931.
- Aukema S.M., Kreuz M., Kohler C.W., Rosolowski M., Hasenclever D., Hummel M., Küppers R., Lenze D., Ott G., Pott C., Richter J., Rosenwald A., Szczepanowski M., Schwaenen C., Stein H., Trautmann H., Wessendorf S., Trümper L., Loeffler M., Spang R., Kluin P.M., Klapper W., Siebert R. Molecular Mechanisms in Malignant Lymphomas Network Project. Biological characterization of adult MYC-translocation-positive mature B-cell lymphomas other than molecular Burkitt lymphoma. Haematologica 2014; 99 (4): 726—735.
- Kobayashi T., Tsutsumi Y., Sakamoto N., Nagoshi H., Yamamoto-Sugitani M., Shimura Y., Mizutani S., Matsumoto Y., Nishida K., Horiike S., Asano N., Nakamura S., Kuroda J., Taniwaki M. Double-hit Lymphomas Constitute a Highly Aggressive Subgroup in Diffuse Large B-cell Lymphomas in the Era of Rituximab. Jpn J Clin Oncol 2012; 42 (11): 1035—1042.
- De Jong D., Voetdijk B.M., Beverstock G.C., van Ommen G.J., Willemze R., Kluin P.M. Activation of the c-myc oncogene in a precursor-B-cell blast crisis of follicular lymphoma, presenting as composite lymphoma. N Engl J Med 1988; 318: 1373—1378.
- Dunphy C.H., van Deventer H.W., Carder K.J., Rao K.W., Dent G.A. Mature B-cell acute lymphoblastic leukemia with associated translocations (14;18)(q32;q21) and (8;9)(q24;p13). A Burkitt variant? Arch Pathol Lab Med 2003; 127: 610—613.
- Fiedler W., Weh H.J., Zeller W., Fonatsch C., Hillion J., Larsen C., Wörmann B., Hossfeld D.K. Translocation (14;18) and (8;22) in three patients with acute leukemia/lymphoma following centrocytic/centroblastic non-Hodgkin’s lymphoma. Ann Hematol 1991; 63: 282—287.
- Galteland E., Sivertsen E.A., Svendsrud D.H., Smedshammer L., Kresse S.H., Meza-Zepeda L.A., Myklebost O., Suo Z., Mu D., Deangelis P.M., Stokke T. Translocation t(14;18) and gain of chromosome 18/BCL2: effects on BCL2 expression and apoptosis in B-cell non-Hodgkin’s lymphomas. Leukemia 2005; 19: 2313—2323.
- Kanagal-Shamanna R., Medeiros .LJ., Lu G., Lu G., Wang S.A., Manning J.T., Lin P., Penn G.M., Young K.H., You M.J., Vega F., Bassett R., Miranda R.N. High-grade B cell lymphoma, unclassifiable, with blastoid features: an unusual morphological subgroup associated frequently with BCL2 and/or MYC gene rearrangements and a poor prognosis. Histopathology 2012; 61 (5): 945—954.
- da Cunha Santos G., Ko H.M., Saieg M.A., Boerner S.L., Lai S.W., Bailey D., Geddie W.R. Cytomorphologic findings of B-cell lymphomas with concurrent IGH/BCL2 and MYC rearrangements (dual-translocation lymphomas). Cancer Cytopathol 2011; 119 (4): 254—262.
- Harrington A.M., Olteanu H., Kroft S.H., Eshoa C. The unique immunophenotype of double-hit lymphomas. Am J Clin Pathol 2011; 135 (4): 649—650.
- Wu D., Wood B.L., Dorer R., Fromm J.R. «Double-Hit» mature B-cell lymphomas show a common immunophenotype by flow cytometry that includes decreased CD20 expression. Am J Clin Pathol 2010; 134 (2): 258—265.
- Yamazaki T., Ohno H. Double-hit lymphoma with t(8;14)(q24;q32) and t(12;14)(q24;q32) chromosomal translocations. Intern Med 2011; 50 (21): 2659—2662.
- Bloomfield C.D., Arthur D.C., Frizzera G., Levine E.G., Peterson B.A., Gajl-Peczalska K.J. Nonrandom chromosome abnormalities in lymphoma. Cancer Res 1983; 43 (6): 2975—2984.
- Yunis J.J., Oken M.M., Theologides A., Howe R.B., Kaplan M.E. Recurrent chromosomal defects arefound in most patients with non-Hodgkin’s-lymphoma. Cancer Genet Cytogenet 1984; 13 (1): 17—28.
- Offit K., Jhanwar S.C., Ladanyi M., Filippa D.A., Chaganti R.S. Cytogenetic analysis of 434 consecutively ascertained specimens of non-Hodgkin’s lymphoma: correlations between recurrent aberrations, histology, and exposure to cytotoxic treatment. Genes Chromosomes Cancer 1991; 3 (3): 189—201.
- Siebert R. Mature B- and T-cell neoplasms and Hodgkin lymphomas. In: Heim S., Mitelman F. Cancer Cytogenetics. New York, NY: Wiley-Blackwell 2009.
- Siebert R., Rosenwald A., Staudt L.M., Morris S.W. Molecular features of B-cell lymphoma. Curr Opin Oncol 2001; 13 (5): 316—324.
- Carè A., Cianetti L., Giampaolo A., Sposi N.M., Zappavigna V., Mavilio F., Alimena G., Amadori S., Mandelli F., Peschle C. Translocation of c-myc into the immunoglobulin heavy-chain locus in human acute B-cell leukemia. A molecular analysis. EMBO J 1986; 5 (5): 905—911.
- Marcu K.B., Harris L.J., Stanton L.W., Erikson J., Watt R., Croce C.M. Transcriptionally active c-myc oncogene is contained within NIARD, a DNA sequence associated with chro- mosome translocations in B-cell neoplasia. Proc Natl Acad Sci USA 1983; 80: 519—523.
- Horn H., Schmelter C., Leich E., Salaverria I., Katzenberger T., Ott M.M., Kalla J., Romero M., Siebert R., Rosenwald A., Ott G. Follicular lymphoma grade 3b is a distinct neoplasm according to cytogenetic and immunohistochemical profiles. Haematologica 2011; 96 (9): 1327—1348.
- Li S., Lin P., Fayad L.E., Lennon P.A., Lennon P.A., Miranda R.N., Yin C.C., Lin E., Medeiros L.J. B-cell lymphomas with MYC/8q24 rearrangements and IGH@BCL2/t(14;18)(q32;q21): an aggressive disease with heterogeneous histology, germinal center B-cell immunophenotype and poor outcome. Mod Pathol 2012; 25 (1): 145—156.
- Nagel I., Akasaka T., Klapper W., Gesk S., Böttcher S., Ritgen M., Harder L., Kneba M., Dyer M.J., Siebert R. Identification of the gene encoding cyclin E1 (CCNE1) as a novel IGH translocation partner in t(14;19)(q32;q12) in diffuse large B-cell lymphoma. Haematologica 2009; 94 (7): 1020—1023.
- Au W.Y., Horsman D.E., Ohno H., Klasa R.J., Gascoyne R.D. Bcl-3/IgH translocation (14;19)(q32;q13) in non-Hodgkin’s lymphomas. Leuk Lymphoma 2002; 43(4): 813—816.
- De Jong D., Voetdijk B.M., Beverstock G.C., van Ommen G.J., Willemze R., Kluin P.M. Activation of the c-myc oncogene in a precursor-B-cell blast crisis of follicular lymphoma, presenting as composite lymphoma. N Engl J Med 1988; 318 (21): 1373—1378.
- Tsai A.G., Lu H., Raghavan S.C., Muschen M., Hsieh C.L., Lieber M.R. Human chromosomal translocations at CpG sites and a theoretical basis for their lineage and stage specificity. Cell 2008; 135 (6): 1130—1142.
- Xu Z., Zan H., Pone E.J., Mai T., Casali P. Immunoglobulin class-switch DNA recombination: induction, targeting and beyond. Nat Rev Immunol 2012; 12 (7): 517—531.
- Boerma E.G., Siebert R., Kluin P.M., Baudis M. Translocations involving 8q24 in Burkitt lymphoma and other malignant lymphomas: a historical review of cytogenetics in the light of today’s knowledge. Leukemia 2009; 23 (2): 225—234.
- Jankovic M., Robbiani D.F., Dorsett Y., Eisenreich T., Xu Y., Tarakhovsky A., Nussenzweig A., Nussenzweig M.C. Role of the translocation partner in protection against AID-dependent chromosomal translocations. Proc Natl Acad Sci USA 2010; 107 (1): 187—192.
- Ramiro A.R., Jankovic M., Eisenreich T., Difilippantonio S., Chen-Kiang S., Muramatsu M., Honjo T., Nussenzweig A., Nussenzweig M.C. AID is required for c-myc/IgH chromosome translocations in vivo. Cell 2004; 118 (4): 431—438.
- Slack G.W., Gascoyne R.D. MYC and aggressive B-cell lymphoma. Adv Anat Pathol 2011; 18: 219—228.
- Korac P. «Double hit» lymphoma or secondary MYC translocation lymphoma? Periodicum biologorum 2012; 114 (4), 527—537.
- Gebauer N., Bernard V., Gebauer W., Thorns C., Feller A.C., Merz H. TP53 mutations are frequent events in double-hit B-cell lymphomas with MYC and BCL2 but not MYC and BCL6 translocations. Leuk Lymphoma 2014, May 7 [epub ahead of print]
- Vaque J.P., Martenez N., Batlle-Lopez A., Pérez C., Montes-Moreno S., Sánchez-Beato M., Piris M.A. B-cell lymphoma mutations: improving diagnostics and enabling targeted therapies. Haematologica 2014; 99 (2): 222—231.
- Pedersen M.Ø., Gang A.O., Poulsen T.S., Knudsen H., Lauritzen A.F., Nielsen S.L., Gang U.O., Nørgaard P. Double-hit BCL2/MYC translocations in a consecutive cohort of patients with large B-cell lymphoma — a single centre’s experience Eur J Haematol 2012; 89 (1): 63—71.
- Valera A., López-Guillermo A., Cardesa-Salzmann T., Climent F., González-Barca E., Mercadal S., Espinosa I., Novelli S., Briones J., Mate J.L., Salamero O., Sancho J.M., Arenillas L., Serrano S., Erill N., Martínez D., Castillo P., Rovira J., Martínez A., Campo E., Colomo L., Grup per l’Estudi dels Limfomes de Catalunya i Balears (GELCAB). MYC Protein Expression And Genetic Alterations Have Prognostic Impact In Patients With Diffuse Large B-Cell Lymphoma Treated With Immunochemotherapy. Haematologica 2013; 98 (10): 1554—1562.
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