A Systematic Review Of The Manangement Of Relapsed/Refractory Follicular Lymphoma
Keywords:
genetic diversity, targeted therapy, refractory indolent lymphoma, Follicular lymphomaAbstract
Refractory follicular lymphoma is an indolent malignancy of follicular center cells where a subgroup of disease presents with relapse and refractoriness to treatment or transformation to aggressive diffuse large B cell lymphoma. Improved knowledge of
the disease biology is expected to provide means of identifying refractory disease at diagnosis and new approach to their treatment. This systematic review of emerging treatment modalities was done with a view to identifying appropriate treatment of refractory or relapsed follicular lymphoma in resource poor settings.
A systematic search of the database of MEDLINE, COCHRANE and EMBASE was done using the following words: relapse/refractory follicular lymphoma, follicular lymphoma clinical trials, follicular lymphoma treatment guideline. Randomized controlled phase II/III trials were selected for review. National Comprehensive Cancer Network and European Society for Medical Oncology recent guidelines were also reviewed. The promising potentials of recently approved novel targeted therapy were dampened by toxicity and drug resistance.
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References
Groves FD, Linet MS, Travis LB, Devesa SS. Cancer surveillance series: non-Hodgkin’s lymphoma incidence by histologic subtype in the United States from 1978 through 1995. J Natl Cancer Inst. 2000; 92:1240–1251.
A clinical evaluation of the International Lymphoma Study Group classification of non Hodgkin’s lymphoma. The Non-Hodgkin’s Lymphoma Classification Project. Blood 1997; 89: 3909–3918.
Naresh KN, Raphael M, Ayers L, Hurwitz N, Calbi V, Rogena E, et al. Lymphomas in subSaharan Africa – what can we learn and how can we help in improving diagnosis, managing patients and fostering translational research? Br J Haematol. 2011; 154 (6): 696–703.
de Jong D. Molecular pathogenesis of follicular lymphoma: a cross talk of genetic and immunologic factors. J Clin Oncol. 2005; 23:6358–6363.
Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics. CA Cancer J Clin. 2014; 64:9–29.
Rummel MJ, Maschmeyer G, Ganser A, Heider A, von Gruenhagen U, Losem C, et al. Bendamustine plus rituximab (B-R) versus CHOP plus rituximab (CHOP-R) as first-line treatment in patients with indolent lymphomas: Nine-year updated results from the StiL NHL1 study. J Clin Oncol. 2017; 35(15): 7501-7501.
Flinn IW, van der Jagt R, Kahl BS, Wood P, Hawkins TE, Macdonald D, et al. Randomized trial of bendamustine-rituximab or R-CHOP/RCVP in first-line treatment of indolent NHL or MCL: the BRIGHT study. Blood 2014;123(19):2944-52.
Casulo C , Byrtek M , Dawson KL , Zhou X , Farber CM , Flowers CR, 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. Clin Oncol. 2015; 33(23): 2516-2522.
Dreyling M, Ghielmini M, Rule S, Salles G, Vitolo U, Ladetto M on behalf of the ESMO Guidelines Committee. Newly diagnosed and relapsed follicular lymphoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and followup. Ann Oncol. 2016; 27 (5): 83–9.
Ardeshna KM, Smith P, Norton A, Hankock BW, MacLennan KA, Marcus RE, et al. Long-term effect of a watch and wait policy versus immediate systemic treatment for asymptomatic advanced-stage non- Hodgkin lymphoma: a randomised controlled trial. Lancet 2003; 362: 516–522.
Solal-Ce´ligny P, Bellei M, Marcheselli L, Pesce EA, Pileri S, McLaughlin P, et al. Watchful Waiting in Low–Tumor Burden Follicular Lymphoma in the Rituximab Era: Results of an F2-Study Database. J Clin Oncol. 2012; 30(31): 3848-3853.
Andrea Gallamini,, Anna Borra. FDG-PET Scan: a new Paradigm for Follicular Lymphoma Management. Mediterr J Hematol Infect Dis. 2017; 9(1): 1-9
Bodet-Milin C, Eugène T, Gastinne T, Frampas E, Le Gouill S, Kraeber-Bodéré . FFDG-PET in Follicular Lymphoma Management. J Oncol. 2012; 370272:1-8
Zelenetz AD, Gordon LI, Abramson JS, Advany. B-Cell Lymphomas. NCCN Guideliness 2017; 15(3):293-311
Davis TA, Grillo-López AJ, White CA, McLaughlin P, Czuczman MS, Link BK, et al. Rituximab antiCD20 monoclonal antibody therapy in nonHodgkin's lymphoma: safety and efficacy of retreatment. J Clin Oncol. 2000; 18(17):3135.
Salles G, Seymour JF, Offner F, López-Guillermo A, Belada D, Xerri L, et al. Rituximab maintenance for 2 years in patients with high tumour burden follicular lymphoma responding to rituximab plus chemotherapy (PRIMA): a phase 3, randomised controlled trial Lancet 2011; 377 (9759): 2-51
Walker MS, Stepanski EJ, Reyes C, SatramHoang S, Houts AC, Schwartzberg LS. Symptom Burden and Quality of Life in Patients with Follicular Lymphoma undergoing Maintenance Treatment with Rituximab Compared with Observation.Ther Adv Hematol. 2011; 2(3):129-39.
Federico M, Barrigón MDC, Marcheselli L, Tarantino V, Manni M, Sarkozy C, et al. Rituximab and the risk of transformation of follicular lymphoma: a retrospective pooled analysis. Lancet haematol.2018;3026(18): 30090-30095
McLaughlin P, Estey E, Glassman A, Romaguera J, Samaniego F, Ayala A, et al. Myelodysplasia and acute myeloid leukemia following therapy for indolent lymphoma with fludarabine, mitoxantrone, and dexamethasone (FND) plus rituximab and interferon alpha. Blood 2005; 105(12): 4573–4575
Prusila R, Sorigue M, Tanhua T, TikkanenS, Jantunen E, Kuittinen O, et al. Risk of secondary hematological malignancy in patients with follicular lymphoma. Supplement: 14th International Conference on Malignant Lymphoma Palazzo deiCongressi, Lugano (Switzerland). Haem Oncol. 2017; 35(S2): 368369
Sehn LH, Goy A, Offner FC, Martinelli G, Caballero MD, Gadeberg O, et al. Randomized Phase II Trial Comparing Obinutuzumab (GA101) with Rituximab in Patients with Relapsed CD20 Indolent B-Cell Non-Hodgkin Lymphoma: Final Analysis of the GAUSS Study. J Clin Oncol. 2015; 33(30):3467-3474.
Salles GA, Morschhauser F, Solal-Ce´ligny P, Thieblemont C, Lamy T, Herve´ Tilly, 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): 2920-2926.
Edelmann J, Gribben JG. Obinutuzumab for the treatment of indolent lymphoma. Future Oncol. 2016; 12(15): 1769–1781
Sehn LH, Chua N , Mayer J, Dueck G, Trněný M, Bouabdallah K, et al. Obinutuzumab plus bendamustine versus bendamustine monotherapy in patients with rituximab-refractory indolent non-Hodgkin lymphoma (GADOLIN): a randomised, controlled, open-label, multicentre, phase 3 trial. Lancet Oncol. 2016; 17(8):10811093.
Radford J, Davies A, Cartron G, Morschhauser F, Salles G, Marcus R, et al. Obinutuzumab (GA101) plus CHOP or FC in relapsed/refractory follicular lymphoma: results of the GAUDI study (BO21000) Running head: GA101 plus CHOP or FC in refractory/relapsed FL. Blood 2013; 122(7):1137–43.
Cheson BD, Leoni L, Bendamustine : mechanism of action and clinical data. Clin Adv Hematol Oncol. 2011; 9(8-19): 1-11.
Wiseman GA, Kornmehl E, Leigh B, Erwin WD, Podoloff DA, Spies S, et al. Radiation dosimetry results and safety correlations from 90Y-ibritumomab tiuxetan radioimmunotherapy for relapsed or refractory non-Hodgkin's lymphoma: combined data from 4 clinical trials. J Nucl Med. 2003; 44(3):465-74.
Witzig TE , Gordon LI , Cabanillas F , Czuczman MS , Emmanouilides C , Robin J, et al. Randomized Controlled Trial of Yttrium-90– Labeled Ibritumomab Tiuxetan Radioimmunotherapy Versus Rituximab Immunotherapy for Patients With Relapsed or Refractory Low-Grade, Follicular, or Transformed B-Cell Non-Hodgkin’s Lymphoma. J Clinl Oncol. 2002; 20(10): 2453-2463.
Witzig TE, Flinn IW, Gordon LI, Emmanouilides C, Czuczman MS, Saleh MN, et al. Treatment with ibritumomab tiuxetan radioimmunotherapy in patients with rituximab-refractory follicular nonHodgkin's lymphoma. Clin Oncol. 2002; 20(15):3262-9.
Witzig TE, White CA , Gordon LI , Wiseman GA , Emmanouilides C , Murray JL, et al. Safety of Yttrium-90 Ibritumomab Tiuxetan Radioimmunotherapy for Relapsed Low-Grade, Follicular, or Transformed Non-Hodgkin’s Lymphoma. J Clin Oncol. 2003; 21(7):12631270.
Gordon LI, Witzig T, Molina A, Czuczman M, Emmanouilides C, Joyce R, et al. Yttrium 90labeled ibritumomab tiuxetan radioimmunotherapy produces high response rates and durable remissions in patients with previously treated B-cell lymphoma. Clin. Lymphoma 2004; 5(2):98-101.
Czuczman MS, Emmanouilides C, Darif M, Witzig TE, Gordon LI, Revell S, et al. Treatment-related myelodysplastic syndrome and acute myelogenous leukemia in patients treated with ibritumomab tiuxetan radioimmunotherapy. J Clin Oncol. 2007; 25(27):4285.
Ansell SM, Ristow KM, Habermann TM, Wiseman GA, Witzig TE. Subsequent chemotherapy regimens are well tolerated after radioimmunotherapy with yttrium-90 ibritumomab tiuxetan for non-Hodgkin's lymphoma. J Clin Oncol. 2002; 20(18):3885.
Pasquetto M, Vecchia L, Covini D, Digilio R, Scotti C. Targeted Drug Delivery Using Immunoconjugates: Principles and Applications. J. Immunotherapy 2011; 34(9):611–628.
Goy A, Forero A, Wagner-Johnston N, Ehmann CW, Tsai M, Hatake K, et al. A phase 2 study of inotuzumabozogamicin in patients with indolent B-cell non-Hodgkin lymphoma refractory to rituximab alone, rituximab and chemotherapy, or radioimmunotherapy. Br J Haematol. 2016; 174(4):571-81.
Dang NH, Smith MR, Offner F, Verhoef G, Johnson P, Rohatiner AZS, et al. Anti-CD22 Immunoconjugate InotuzumabOzogamicin (CMC544) + Rituximab: Clinical Activity Including Survival in Patients with Recurrent/Refractory Follicular or ‘Aggressive' Lymphoma. Blood 2009; 114:584.
Morschhauser F, Flinn I, Advani RH, Diefenbach CS, KolibabaK, Press OW, et al. Updated Results of a Phase II Randomized Study (ROMULUS) of PolatuzumabVedotin or PinatuzumabVedotin Plus Rituximab in Patients with Relapsed/Refractory NonHodgkin Lymphoma. Blood 2014; 124:4457.
Advani RH, Flinn I , Sharman JP , Diefenbach CSM , Kolibaba KS , Press OW. Two doses of polatuzumabvedotin (PoV, anti-CD79b antibodydrug conjugate) in patients (pts) with relapsed/refractory (RR) follicular lymphoma (FL): Durable responses at lower dose level. J Clin Oncol. 2015; 33(15): 8503-8513.
Herrera AF, Matasar M, Assouline S, Kamdar M, Mehta A, Fleury I, et al. Polatuzumab Vedotin combined with Bendamustine (B) and Rituximab (R) or Obinutuzumab (G) in Patients with Relapsed or Refractory (R/R) Follicular Lymphoma (FL) or Diffuse Large B-Cell Lymphoma (DLBCL): Preliminary Results of a Phase Ib/II Dose-Escalation Study. Blood 2016; 128:41
Eskian M, Khorasanizadeh M, Isidori A, Rezaei N. Radioimmunotherapy-based conditioning regimen prior to autologous stem cell transplantation in non-Hodgkin lymphoma. Int J Hematol Oncol. 2018; 7(1):IJH01. doi: 10.2217/ijh-2017-0025.
Jiménez-Ubieto A, Grande C, Caballero D, Yáñez L, Novelli S, Hernández-Garcia MT, et al. Autologous Stem Cell Transplantation for Follicular Lymphoma: Favorable Long-Term Survival Irrespective of Pretransplantation Rituximab Exposure. Biol Blood Marrow Transplant 2017; 23(10):1631-1640.
Maura F, Farina L, Corradini P. The Role of Autologous and Allogeneic Stem Cell Transplantation in Follicular Lymphoma in The New Drugs Era. Mediterr J Hematol Infect Dis. 2016; 8(1): 1-13.
Tarella C, Zanni M , Magni M , Benedetti F , Patti C , Barbui T, et al. Rituximab Improves the Efficacy of High-Dose Chemotherapy With Autograft for High-Risk Follicular and Diffuse Large B-Cell Lymphoma: A Multicenter Gruppo ItalianoTerapieInnnovativeneiLinfomi Survey. J Clin Oncol. 2008; 26:3166-317
Zinzani PL, Marchetti M, Billio A, Barosi G, Carella AM, Lazzarino M, et al. SIE, SIES, GITMO revised guidelines for the management of follicular lymphoma. Am J Hematol. 2013; 88:185–192.
Casulo C, Friedberg JW, Ahn KW, Flowers C, DiGilio A, Smith SM, et al. Autologous Transplantation in Follicular Lymphoma with Early Therapy Failure: A National LymphoCare Study and Center for International Blood and Marrow Transplant Research Analysis. Biol Blood Marrow Transpl. 2018; 24(6):1163-1171.
Jurinovic V, Metzner B, Pfreundschuh M, Schmitz N, Wandt H, Keller U, et al. Autologous stem cell transplantation for patients with early progression of follicular lymphoma: a follow-up study of 2 randomized trials from the German Low Grade Lymphoma Study Group. Biol Blood Marrow Transpl. 2018; 24(6):1172-1179.
Wang X, Riviere I. Clinical manufacturing of CAR T cells: foundation of a promising therapy. Mol Ther Oncolytics 2016; 3: 16015.
Chavez JC, Bachmeier C, Kharfan-Dabaja MA. CAR T-cell therapy for B-cell lymphomas: clinical trial results of available products. Ther Adv Hematol. 2019; 10: 1–20
Schuster SJ, Svoboda J, Chong EA, Nasta SD, Mato AR, Anak Ö, et al. Chimeric antigen receptor T cells in refractory B-cell lymphomas. N Engl J Med. 2017; 377: 2545-2554.
Rummel M, Kaiser U, Balser C, Stauch M, Brugger W, Welslau M, et al. on behalf of the Study Group Indolent Lymphomas. Bendamustine plus rituximab versus fludarabine plus rituximab for patients with relapsed indolent and mantle-cell lymphomas: a multicentre, randomised, open-label, non-inferiority phase 3 trial. Lancet Oncol. 2016; 17:57–66.
Evens AM, Vanderplas A, LaCasce AS, Crosby AL, Nademanee AP, Kaminski MS, Stem cell transplantation for follicular lymphoma relapsed/refractory after prior rituximab: a comprehensive analysis from the NCCN lymphoma outcomes project. Cancer. 2013; 119(20):3662-3671.
Klyuchnikov E,Bacher U,Kröger NM, Hari PN, Ahn KW,Carreras J, et al. Reduced-Intensity Allografting as First Transplantation Approach in Relapsed/Refractory Grades One and Two Follicular Lymphoma Provides Improved Outcomes in Long-Term Survivors. Biol Blood Marrow Transpl. 2015; 21(12):2091-2099.
Jiménez-Ubieto A, Grande C, Caballero D, Yáñez L, Novelli S, Hernández-Garcia MT, et al. on behalf of the GELTAMO (Grupo Español de Linfomas y TrasplantesdeMédulaÓsea) Cooperative Study Group Autologous Stem Cell Transplantation for Follicular Lymphoma: Favorable Long-Term Survival Irrespective of Pretransplantation Rituximab Exposure. Biol Blood Marrow Transpl 2017; 23:1631–1640.
Gopal AK, Kahl BS, Christopher R. Flowers CR, Martin P, Ansell SM, Abella-Dominicis E, et al. Idelalisib is effective in patients with high-risk follicular lymphoma and early relapse after initial chemoimmunotherapy. Blood 2017; 129:30373039.
Salles G, Schuster S, de Vos S, WagnerJohnston ND, Viardot A, Blum KA, et al. Efficacy and safety of idelalisib in patients with relapsed, rituximab- and alkylating agent-refractory follicular lymphoma: a subgroup analysis of a phase 2 study. Haematologica 2017; 102(4): 156–159.
Cuneo A , Barosi G , Danesi R , Fagiuo S, Ghia P, Marzano A, et al. Management of adverse events associated with idelalisib treatment in chronic lymphocytic leukemia and follicular lymphoma: A multidisciplinary position paper. Hemat Oncol. 2018;37:13-14.
Dreyling M, Morschhauser F, Bouabdallah K, Bron D, Cunningham D, Assouline SE, et al. Phase II study of copanlisib, a PI3K inhibitor, in relapsed or refractory, indolent or aggressive lymphoma. Ann Oncol. 2017; 28(9):2169-2178.
Dreyling MH, Santoro A, Leppa S, Demeter J. Follows G, Lenz G, et al. Copanlisib in patients with relapsed or refractory follicular lymphoma. J Clin Oncol. 2017; 35(15):7535-7535.
Kritharis A, Coyle M, Sharma J, Evens AM. Lenalidomide in non-Hodgkin lymphoma: biological opportunities. perspectives and therapeutic. Blood 2015; 125:2471-2476.
Andorsky DJ, Yacoub A, Bitran JD, Melear J, Brooks HD, Kenneth A, et al. MAGNIFY: Phase IIIb Randomized Study of Lenalidomide Plus Rituximab (R2) Followed by Lenalidomide Vs. Rituximab Maintenance in Subjects with Relapsed/Refractory Follicular, Marginal Zone, or Mantle Cell Lymphoma. Blood 2016; 128:1798.
Leonard JP, Trneny M, Izutsu K, Fowler NH, Hong X, Zhu J, et al. AUGMENT: A Phase III Study of Lenalidomide Plus Rituximab Versus Placebo Plus Rituximab in Relapsed or Refractory Indolent Lymphoma. Clin Oncol. 2019; 37(14): 1188-1199.
Cartron HR, Bijou G, de Guibert F, Salles SA, Fruchart G, Bouabdallah C. Obinutuzumab plus Lenalidomide (GALEN) for the treatment of relapse/refractory aggressive lymphoma: a phase II LYSA study. Leukemia 2018; 33 (10):1038.
Morschhauser F, Fowler NH, Feugier P, Bouabdallah R, Tilly H, Palomba ML, et al. for the RELEVANCE Trial Investigators Rituximab plus Lenalidomide in Advanced Untreated Follicular Lymphoma. N Engl J Med. 2018; 379:934-947.
Sven de voz, Shaker Dakhil S, Peter McLaughlin P, Mansoor Saleh M, Robert Belt R, Flowers C, et al. Bortezomib Plus Rituximab in Patients with Indolent Non-Hodgkin’s Lymphoma (NHL): A Phase 2 Study. Blood 2005; 106:17.
Zinzani PL, Khuageva NK, Wang H, Garicochea B, Walewski J, Van Hoof A, et al. Bortezomib plus rituximab versus rituximab in patients with high-risk, relapsed, rituximab-naïve or rituximabsensitive follicular lymphoma: subgroup analysis of a randomized phase 3 trial. J Hematol Oncol. 2012; 5:67
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