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Review

Advances in the treatment of follicular lymphoma

, MD (Assistant Professor) & , MD FACP FAAAS (Professor of Medicine, Head of Hematology, Deputy Chief)

Bibliography

  • Solal-Céligny P, Roy P, Colombat P, et al. Follicular lymphoma international prognostic index. Blood 2004;104(5):1258-65
  • Federico M, Bellei M, Marcheselli L, et al. Follicular Lymphoma International Prognostic Index 2: a new prognostic index for follicular lymphoma developed by the international follicular lymphoma prognostic factor project. J Clin Oncol 2009;27(27):4555-62
  • Farinha P, Al-Tourah A, Gill K, et al. The architectural pattern of FOXP3-positive T cells in follicular lymphoma is an independent predictor of survival and histologic transformation. Blood 2010;115(2):289-95
  • Coiffier B, Li W, Henitz ED, et al. Prespecified candidate biomarkers identify follicular lymphoma patients who achieved longer progression-free survival with bortezomib-rituximab versus rituximab. Clin Cancer Res 2013;19(9):2551-61
  • Solal-Céligny P, Lepage E, Brousse N, et al. Doxorubicin-containing regimen with or without interferon alfa-2b for advanced follicular lymphomas: final analysis of survival and toxicity in the Groupe d’Etude des Lymphomes Folliculaires 86 Trial. J Clin Oncol 1998;16(7):2332-8
  • Tellier J, Menard C, Roulland S, et al. Human t(14;18)positive germinal center B cells: a new step in follicular lymphoma pathogenesis? Blood 2014;123(22):3462-5
  • Mamessier E, Song J, Eberle F, et al. Early lesions of follicular lymphoma: a genetic perspective. Haematologica 2014;99(3):481-8
  • Swerdlow SH, Campo E, Harris NL, et al. editors. World Health Organization classification of tumours of haematopoietic and lymphoid tissues. IARC Press, Lyon; 2008
  • Kridel R, Sehn L, Gascoyne R. Pathogenesis of follicular lymphoma. J Clin Invest 2012;122(10):3424-31
  • Friedberg J, Byrtek M, Link B, et al. Effectiveness of first-line management strategies for stage I follicular lymphoma: analysis of the National LymphoCare Study. J Clin Oncol 2012;30(27):3368-75
  • Federico M, Luminari S, Dondi A, et al. R-CVP versus R-CHOP versus R-FM for the initial treatment of patients with advanced-stage follicular lymphoma: results of the FOLL05 trial conducted by the Fondazione Italiana Linfomi. J Clin Oncol 2013;31(12):1506-13
  • Leoni LM, Bailey B, Reifert J, et al. Bendamustine (Treanda) displays a distinct pattern of cytotoxicity and unique mechanistic features compared with other alkylating agents. Clin Cancer Res 2008;14:309-17
  • Kahl B, Bartlett NL, Leonard JP, et al. Bendamustine is effective therapy in patients with rituximab-refractory, indolent B-cell NHL. Cancer 2010;116(1):106-14
  • Knauf WU, Lissichkov T, Aldaoud A, et al. Phase III randomized study of bendamustine compared with chlorambucil in previously untreated patients with CLL. J Clin Oncol 2009;27(26):4378-84
  • Rummel MJ, Al-Batran SE, Kim SZ, et al. Bendamustine plus rituximab is effective and has a favorable toxicity profile in the treatment of mantle cell and low-grade non-Hodgkin’s lymphoma. J Clin Oncol 2005;23(15):3383-9
  • Rummel M, Niederle N, Maschmeyer G, et al. Bendamustine plus rituximab versus CHOP plus rituximab as first-line treatment for patients with indolent and mantle-cell lymphomas: an open-label, multicentre, randomised, phase 3 non-inferiority trial. Lancet 2013;381(9873):1203-10
  • Rummel M, Maschmeyer G, Ganser A, et al. Bendamustine plus rituximab versus CHOP plus rituximab as first-line treatment in patients with indolent and mantle cell lymphomas – 7 year updated results from the StiL NHL1 study. Blood (ASH Annual Meeting Abstracts) 2014;124:abstract 4407
  • Flinn I, van der Jagt R, Kahl B, et al. Randomized trial of bendamustine-rituximab or R-CHOP/R-CVP in first-line treatment of indolent NHL or MCL: the BRIGHT study. Blood 2014;123(19):2944-52
  • Wierda W, Kipps T, Mayer J, et al. Ofatumumab as single-agent CD20 immunotherapy in fludarabine-refractory chronic lymphocytic leukemia. J Clin Oncol 2010;28(10):1749-55
  • Czuczman M, Fayad L, Delwail V, et al. Ofatumumab monotherapy in rituximab-refractory follicular lymphoma: results from a multicenter study. Blood 2012;119(16):3698-704
  • Fowler N, Kahanic S, Forero A, et al. Results of a phase II study with bendamustine and ofatumumab in untreated indolent B-cell non-hodgkin’s lymphoma. Blood (ASH Annual Meeting Abstracts) 2011;118:abstract 778
  • Czuczman M, Hess G, Gadeberg O, et al. Chemoimmunotherapy with ofatumumab in combination with CHOP in previously untreated follicular lymphoma. Br J Haematol 2012;157(4):438-45
  • Mossner E, Brunker P, Moser S, et al. Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 antibody with enhanced direct and immune effector cell-mediated B-cell cytotoxicity. Blood 2010;115(22):4393-402
  • Goede V, Fischer K, Busch R, et al. Obinutuzumab plus chlorambucil in patients with CLL and coexisting conditions. N Engl J Med 2014;370(12):1101-10
  • Salles G, Morschhauser F, Solal-Céligny P, et al. Obinutuzumab (GA101) in patients with relapsed/refractory indolent non-Hodgkin lymphoma: results from the phase II GAUGUIN study. J Clin Oncol 2013;31(23):2920-6
  • Sehn L, Goy A, Offner F, et al. Randomized phase II trial comparing GA101 (Obinutuzumab) with rituximab in patients with relapsed CD20 indolent B-cell non-hodgkin lymphoma: preliminary analysis of the GAUSS study. Blood (ASH Annual Meeting Abstracts) 2011;118:abstract 269
  • Dyer M, Grigg A, Gonzales M, et al. Obinutuzumab (GA101) in combination with cyclophosphamide, doxorubicin, vincristine and prednisone (CHOP) or bendamustine in patients with previously untreated follicular lymphoma (FL): results of the phase Ib GAUDI study (BO21000). Blood (ASH Annual Meeting) 2012;120:abstract 3686
  • Dyer M, Grigg A, Gonzales M, et al. Obinutuzumab (GA101) in combination with CHOP (Cyclophosphamide, doxorubicin, vincristine and prednisone) or bendamustine for the first-line treatment of follicular non-hodgkin lymphoma: final results from the maintenance phase of the phase Ib GAUDI study. Blood (ASH Annual Meetings) 2014;25:abstract 1743
  • O’Connor O, Schreeder M, Deng C, et al. Ublituximab (TG-1101), a novel anti-CD20 monoclonal antibody for rituximab relapsed/refractory B-cell malignancies. Eur Hematol Assoc (Annual Meetings) 2014;abstract 444
  • Czuczman MS, Thall A, Witzig TE, et al. Phase I/II study of galiximab, an anti-CD80 antibody, for relapsed or refractory follicular lymphoma. J Clin Oncol 2005;23:4390-8
  • Leonard J, Freidberg J, Younes A, et al. A phase I/II study of galiximab (an anti-CD80 antibody) in combination with rituximab for relapsed or refractory follicular lymphoma. Ann Oncol 2007;18:1216-23
  • Czuczman M, Leonard J, Jung S, et al. Phase II trial of galiximab (anti-CD80 monoclonal antibody) plus rituximab (CALGB 50402): follicular Lymphoma International Prognostic Index (FLIPI) score is predictive of upfront immunotherapy responsiveness. Ann Oncol 2012;23(9):2356-62
  • Leonard J, Coleman M, Ketas J, et al. Phase I/II trial of epratuzumab (humanized anti-CD22 antibody) in indolent non-Hodgkin’s lymphoma. J Clin Oncol 2003;21(16):3051-9
  • Grant B, Leonard J, Johnson J, et al. Combination biologic therapy as initial treatment for follicular lymphoma: initial results from CALGB 50701 - a Phase II trial of extended induction epratuzumab (anti-CD22) and rituximab (anti-CD20). Blood (ASH Annual Meeting Abstracts) 2010;116:abstract 427
  • Forero-Torres A, Hamadani M, Fanale M, et al. Safety profile and clinical response to MEDI-551, a humanized monoclonal anti-CD19, in a phase 1/2 study in adults with relapsed or refractory advanced B-Cell malignancies. Blood (ASH Annual Meeting Abstracts) 2013;122:abstract 1810
  • Ogura M, Ando K, Uike N, et al. A Multicenter Phase I Study of the humanized anti-CD19 monoclonal antibody, MEDI-551, in patients with relapsed or refractory B-cell lymphoma and multiple myeloma. Blood (ASH Annual Meeting Abstracts) 2014;abstract 1756
  • Witzig T, Linn I, Gordon L, et al. Treatment with ibritumomab tiuxetan radiotherapy in patients with rituximab-refractory follicular non-Hodgkin’s lymphoma. J Clin Oncol 2002;20(15):3262-9
  • Kaminski M, Zelenetz A, Press O, et al. Pivotal study of iodine-131 tositumomab for chemotherapy-refractory low-grade or transformed low-grade B-cell non-Hodgkin’s lymphoma. J Clin Oncol 2001;19(19):3918-28
  • Morschhauser F, Radford J, van Hoof A, et al. Phase III trial of consolidation therapy with yttrium-90-labeled ibritumomab tiuxetan compared with no additional therapy after first remission in advanced follicular lymphoma. J Clin Oncol 2008;26:5156-64
  • Press OW, Unger JM, Rimsza LM, et al. Phase III randomized intergroup trial of CHOP plus rituximab compared with CHOP chemotherapy plus 131Iodine-tositumomab for previously untreated follicular non-hodgkin lymphoma: SWOG S0016. J Clin Oncol 2013;31(3):314-20
  • Zevalin (Ibritumomab tiuxetan) prescribing information. Revised September 2009
  • Bennett J, Kaminski M, Leonard J, et al. Assessment of treatment-related myelodysplastic syndromes and acute myeloid leukemia in patients with non-Hodgkin lymphoma treated with tositumomab and iodine I131 tositumomab. Blood 2005;105(12):4576-82
  • Link B, Martin P, Kaminski M, et al. Cyclophosphamide, vincristine, and prednisone followed by tositumomab and iodine-131-tositumomab in patients with untreated low-grade follicular lymphoma: eight-year follow-up of a multicenter phase II study. J Clin Oncol 2010;28(18):3035-41
  • Martin P, Coleman M, Furman R, et al. Fludarabine Plus I-131 tositumomab as initial treatment for follicular lymphoma: half of patients in remission at over 10 years median follow up. Blood (ASH Annual Meeting Abstracts) 2010;116:abstract 1785
  • Goy A, Leach J, Ehmann W, et al. Inotuzumab ozogamicin (CMC-544) In patients with indolent B-Cell NHL that is refractory to rituximab alone, rituximab and chemotherapy, or radioimmunotherapy: preliminary safety and efficacy from a phase 2 trial. Blood (ASH Annual Meeting Abstracts) 2010;116:abstract 430
  • Fayad L, Offner F, Smith MR, et al. Safety and clinical activity of a combination therapy comprising two antibody-based targeting agents for the treatment of non-Hodgkin lymphoma: results of a phase I/II study evaluating the immunoconjugate inotuzumab ozogamicin with rituximab. J Clin Oncol 2013;31(5):573-83
  • Dang N, Ogura M, Castaigne S, et al. Randomized, phase 3 trial of inotuzumab ozogamicin plus rituximab versus chemotherapy for relapsed/refractory aggressive B-cell non-Hodgkin lymphoma. J Clin Oncol (ASCO Meeting Abstracts) 2014;32(15):abstract 8529
  • Advani R, Chen A, Lebovic D, et al. Final results of a phase I study of the anti-CD22 antibody-drug conjugate DCDT2980S with or without rituximab in patients with relapsed or refractory B-Cell non-hodgkin’s lymphoma. Blood (ASH Annual Meeting Abstracts) 2013;122:abstract 4399
  • Palanca-Wessels M, Salles G, Czuczman M, et al. Final results of a phase I. study of the anti-CD79b antibody-drug conjugate DCDS4501A in relapsed or refractory B-Cell non-hodgkin lymphoma. Blood (ASH Annual Meeting Abstracts) 2013;122:abstract 4400
  • Morschhauser F, Flinn I, Advani R, et al. Updated results of a phase II randomized study (ROMULUS) of polatuzumab vedotin or pinatuzumab vedotin plus rituximab in patients with relapsed/refractory non-hodgkin lymphoma. Blood (ASH Annual Meeting Abstracts) 2014;abstract 4457
  • Stathis A, Freedman A, Flinn I, et al. A phase I study of IMGN529, an antibody-drug conjugate targeting CD37, in adult patients with relapsed or refractory B-cell non-hodgkin’s lymphoma. Blood (ASH Annual Meeting Abstracts) 2014;abstract 1760
  • Chanan-Khan A, Cheson BD. Lenalidomide for the treatment of B-cell malignancies. J Clin Oncol 2008;26(9):1544-52
  • Smith S, Grinblatt D, Johnson J, et al. Thalidomide has limited single-agent activity in relapsed or refractory indolent non-Hodgkin lymphomas: a phase II trial of the Cancer and Leukemia Group B. Br J Haematol 2008;140(3):313-19
  • Witzig TE, Wiernik PH, Moore T, et al. Lenalidomide oral monotherapy produces durable responses in relapsed or refractory indolent non-Hodgkin’s Lymphoma. J Clin Oncol 2009;27(32):5404-9
  • Leonard J, Jung S, Johnson J, et al. CALGB 50401: A randomized trial of lenalidomide alone versus lenalidomide plus rituximab in patients with recurrent follicular lymphoma. J Clin Oncol (ASCO Meeting Abstracts) 2012;30(15):abstract 8000
  • Martin P, Jung S-H, Johnson J, et al. CALGB 50803 (Alliance): a phase II trial of lenalidomide plus rituximab in patients with previously untreated follicular lymphoma. J Clin Oncol (ASCO Meeting Abstracts) 2014;32(15):abstract 8521
  • Fowler N, Davis RE, Rawal S, et al. Safety and activity of lenalidomide and rituximab in untreated indolent lymphoma: an open-label, phase 2 trial. Lancet Oncol 2014;15(12):1311-18
  • Morschhauser F, Salles G, Le Gouill S, et al. A Phase Ib study of obinutuzumab combined with lenalidomide for relapsed/refractory follicular B-cell lymphoma. Blood (ASH Annual Meeting Abstracts) 2014;abstract 4458
  • Berger R, Rotem-Yehudar R, Slama G, et al. Phase I safety and pharmacokinetic study of CT-011, a humanized antibody interacting with PD-1, in patients with advanced hematologic malignancies. Clin Cancer Res 2008;14:3044-51
  • Westin J, Chu F, Fayad L, et al. Safety and activity of PD1 blockade by pidilizumab in combination with rituximab in patients with relapsed follicular lymphoma: a single group, open-label, phase 2 trial. Lancet Oncol 2014;15(1):69-77
  • Weber J, Minor D, D’Angelo S, et al. A phase 3 randomized, open-label study of nivolumab (anti-PD-1; BMS-936558; ONO-4538) versus investigator’s choice chemotherapy in patients with advanced melanoma with prior anti-CTLA-4 therapy [abstract: LBA3_PR]. European Society for Medical Oncology 2014 Congress, Madrid
  • Lesokhin A, Ansell S, Armand P, et al. Preliminary results of a phase I study of nivolumab (BMS-936558) in patients with relapsed or refractory lymphoid malignancies. Blood (ASH Annual Meeting Abstracts) 2014;abstract 291
  • Topp M, Gökbuget N, Stein A, et al. Safety and activity of blinatumomab for adult patients with relapsed or refractory B-precursor acute lymphoblastic leukaemia: a multicentre, single-arm, phase 2 study. Lancet Oncol 2015;16:57-66
  • Goebeler M, Viardot A, Noppeney R, et al. CD3/CD19 bispecific bite antibody blinatumomab treatment of NHL patients: 60 uG/m2/d by continuous infusion is tolerable and results in durable responses. Eur Hematol Assoc (Annual Meetings) 2010;21:abstract 0559
  • Schuster S, Svoboda J, Nasta SD, et al. Phase IIa trial of chimeric antigen receptor modified T cells directed against CD19 (CTL019) in patients with relapsed or refractory CD19+ lymphomas. Blood (ASH Annual Meeting Abstracts) 2014;abstract 3087
  • Kohrt H, Houot R, Goldstein M, et al. CD137 stimulation enhances the antilymphoma activity of anti-CD20 antibodies. Blood 2011;117(8):2423-32
  • Kohrt H, Godwin J, Lossos I, et al. A phase Ib, open-label, multicenter study of urelumab (BMS-663513) in combination with rituximab in subjects with relapsed/refractory B-cell malignancies. J Clin Oncol (ASCO Annual Meetings) 2013;31(Suppl):abstract TPS3108
  • Young R, Staudt L. Targeting pathological B cell receptor signalling in lymphoid malignancies. Nat Rev Drug Discov 2013;12(3):229-43
  • Friedberg JW, Sharman J, Sweetenham J, et al. Inhibition of Syk with fostamatinib disodium has significant clinical activity in non-Hodgkin lymphoma and chronic lymphocytic leukemia. Blood 2010;115(13):2578-85
  • Sharman J, Klein L, Boxer B, et al. Phase 2 trial of entospletinib (GS-9973), a selective SYK inhibitor, in follicular lymphoma. Blood (ASH Annual Meeting Abstracts) 2014;abstract 4419
  • Gopal A, Kahl B, de Vos S, et al. PI3Kdelta inhibition by idelalisib in patients with relapsed indolent lymphoma. N Engl J Med 2014;370(11):1008-18
  • Furman R, Sharman J, Coutre S, et al. Idelalisib and Rituximab in Relapsed Chronic Lymphocytic Leukemia. N Engl J Med 2014;370:997-1007
  • de Vos S, Wagner-Johnston N, Coutre S, et al. Durable responses following treatment with the PI3K-delta inhibitor idelalisib in combination with rituximab, bendamustine, or both, in recurrent indolent non-hodgkin lymphoma: phase I/II results. Blood (ASH Annual Meeting Abstracts) 2014;abstract 3063
  • Smith S, Pitcher B, Jung S-H, et al. Unexpected and serious toxicity observed with combined idelalisib, lenalidomide and rituximab in relapsed/refractory B cell lymphomas: Alliance A051201 and A051202. Blood (ASH Annual Meeting Abstracts) 2014;abstract 3091
  • Barr P, Saylors G, Spurgeon S, et al. Phase 2 trial of GS-9973, a selective syk inhibitor, and idelalisib in CLL and NHL. J Clin Oncol (ASCO Annual Meetings) 2014;32;abstract 7059
  • Flinn I, Oki Y, Patel M, et al. Phase 1 evaluation of duvelisib (IPI-145), a PI3K-delta,gamma inhibitor, in patients with relapsed/refractory iNHL. Blood (ASH Annual Meeting Abstracts) 2014;abstract 802
  • Byrd J, Furman R, Coutre S, et al. Targeting BTK with ibrutinib in relapsed CLL. N Engl J Med 2013;369:32-42
  • Wang M, Rule S, Martin P, et al. Targeting BTK with ibrutinib in relapsed or refractory mantle-cell lymphoma. N Engl J Med 2013;369:507-16
  • Advani R, Buggy J, Sharman J, et al. Bruton tyrosine kinase inhibitor ibrutinib (PCI-32765) has significant activity in patients with relapsed/refractory B-cell malignancies. J Clin Oncol 2013;31(1):88-94
  • Wilson W, Gerecitano J, Goy A, et al. The Bruton’s tyrosine kinase (BTK) inhibitor, ibrutinib (PCI-32765), has preferential activity in the ABC subtype of relapsed/refractory de novo diffuse large B-cell lymphoma: interim results of a multicenter, open-label, phase 2 study. Blood (ASH Annual Meeting) 2012;120:abstract 686
  • Bartlett N, LaPlant B, Qi J, et al. Ibrutinib monotherapy in relapsed/refractory follicular lymphoma: preliminary results of a phase 2 consortium trial. Blood (ASH Annual Meeting) 2014;abstract 800
  • Byrd JC, Brown JR, O’Brien S, et al. RESONATE Investigators. Ibrutinib versus ofatumumab in previously treated chronic lymphoid leukemia. N Engl J Med 2014;371(3):213-23
  • Blum K, Christian B, Flynn J, et al. A phase I trial of the bruton’s tyrosine kinase inhibitor, ibrutinib (PCI-32765), in combination with rituximab and bendamustine in patients with relapsed/refractory non-hodgkin’s lymphoma. Blood (ASH Annual Meeting Abstracts) 2012;120:abstract 1643
  • Ujjani C, Cheson BD, Jung S. A phase I study of rituximab, lenalidomide, and ibrutinib in previously untreated follicular lymphoma. Ann Oncol (International Conference on Malignant Lymphoma) 2013;31:abstract 562
  • Ng S, Davids M. Selective Bcl-2 inhibition to treat chronic lymphocytic leukemia and non-Hodgkin lymphoma. Clin Adv Hematol Oncol 2014;12(4):224-9
  • Davids M, Seymour J, Gerecitano J, et al. A phase I study of ABT-199 (GDC-0199) in patients with relapsed/refractory non-hodgkin lymphoma: responses observed in diffuse large B-cell and follicular lymphoma at higher cohort doses. J Clin Oncol (ASCO Annual Meeting Abstracts) 2014;32(15):abstract 8522
  • De Vos S, Flowers C, Wang D, et al. The BCL-2 inhibitor ABT-199 (GDC-0199) in combination with bendamustine and rituximab in patients with relapsed or refractory non-hodgkin’s lymphoma. Blood (ASH Annual Meeting) 2014;abstract 1722
  • Kuruvilla J, Byrd J, Flynn J, et al. The oral selective inhibitor of nuclear export (SINE) selinexor (KPT-330) demonstrates broad and durable clinical activity in relapsed/ refractory non hodgkin’s lymphoma. Blood (ASH Annual Meeting) 2014;abstract 3396
  • Oki Y, Fanale M, Romaguera J, et al. Phase II study of an AKT inhibitor MK2206 in patients with relapsed or refractory lymphoma. Blood (ASH Annual Meeting) 2014;abstract 3093
  • Maddocks K, Cohen J, Christian B, et al. A phase II study of MLN8237 (alisertib) alone and in combination with rituximab in patients with relapsed or refractory B-cell non-hodgkin lymphomas. Blood (ASH Annual Meeting) 2014;abstract 3082
  • Patel M, Hamlin P, Strickland D, et al. A phase I open-label, multi-dose escalation study of the dual Syk/Jak inhibitor PRT062070 (Cerdulatinib) in patients with relapsed/refractory B cell malignancies. Blood (ASH Annual Meeting) 2014;abstract 3103
  • Woyach J, Furman R, Liu T, et al. Resistance mechanisms for the Bruton’s tyrosine kinase inhibitor ibrutinib. N Engl J Med 2014;370:2286-94
  • Trotman J, Luminari S, Boussetta S, et al. Prognostic value of PET-CT after first-line therapy in patients with follicular lymphoma: a pooled analysis of central scan review in three multicentre studies. Lancet Haematol 2014;1(1):e17-27
  • Galimberti S, Luminari S, Ciabatti E, et al. Minimal residual disease after conventional treatment significantly impacts on progression-free survival of patients with follicular lymphoma: the FIL FOLL05 trial. Clin Cancer Res 2014;20(24):6398-405
  • Casulo C, Byrtek M, Dawson K, et al. Early relapse of follicular lymphoma after R-CHOP uniquely defines patients at high risk for death: an analysis from the National Lymphocare Study. Blood (ASH Annual Meeting) 2013;122:abstract 510

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