Management of follicular lymphoma at first relapse

Authors

  • Roopesh Kansara, MD, FRCPC

DOI:

https://doi.org/10.58931/cht.2022.116

Abstract

Follicular lymphoma (FL) is the most common subtype of indolent B-cell non-Hodgkin’s lymphoma (NHL). Histologically, it is subcategorized as grade 1, 2, 3A or 3B. FL, grade 3B is considered an aggressive form of the disease and is managed similar to diffuse large B-cell lymphoma (DLBCL). The intent of this article is to discuss the management of FL at first relapse. However, the knowledge of upfront management strategy is crucial in planning treatment in the event of a relapse.

Author Biography

Roopesh Kansara, MD, FRCPC

Dr. Roopesh Kansara is a staff Hematologist within the Department of Internal medicine, University of Manitoba. He is appointed as an assistant professor and is also the Program Director for Adult Hematology subspecialty program at the University of Manitoba. He pursued his Medicine and Hematology subspecialty training at the University of Manitoba followed by further training in Lymphoproliferative disorders at the British Columbia Cancer Agency (Vancouver). He treats both malignant and benign hematologic disorders but with special focus on Lymphoproliferative neoplasms especially CNS B-cell lymphomas.

References

Swerdlow SH, Campo E, Harris NL. WHO Classification of Tumors. Vol 2. WHO Press.

Brady JL, Binkley MS, Hajj C, et al. Definitive radiotherapy for localized follicular lymphoma staged by 18F-FDG PET-CT: a collaborative study by ILROG. Blood. 2019;133(3):237-245. doi:10.1182/blood-2018-04-843540 DOI: https://doi.org/10.1182/blood-2018-04-843540

El-Galaly TC, Bilgrau AE, de Nully Brown P, et al. A population-based study of prognosis in advanced stage follicular lymphoma managed by watch and wait. Br J Haematol. 2015;169(3):435-444. doi:10.1111/bjh.13316 DOI: https://doi.org/10.1111/bjh.13316

Solal-Céligny P, Bellei M, Marcheselli L, 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. doi:10.1200/JCO.2010.33.4474 DOI: https://doi.org/10.1200/JCO.2010.33.4474

Ardeshna KM, Smith P, Norton A, 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(9383):516-522. doi:10.1016/s0140-6736(03)14110-4 DOI: https://doi.org/10.1016/S0140-6736(03)14110-4

Advani R, Rosenberg SA, Horning SJ. Stage I and II follicular non-Hodgkin’s lymphoma: long-term follow-up of no initial therapy. J Clin Oncol. 2004;22(8):1454- 1459. doi:10.1200/JCO.2004.10.086 DOI: https://doi.org/10.1200/JCO.2004.10.086

Ardeshna KM, Qian W, Smith P, et al. Rituximab versus a watch-and-wait approach in patients with advanced-stage, asymptomatic, non-bulky follicular lymphoma: an open-label randomised phase 3 trial. Lancet Oncol. 2014;15(4):424-435. doi:10.1016/S1470-2045(14)70027-0 DOI: https://doi.org/10.1016/S1470-2045(14)70027-0

Hiddemann W, Kneba M, Dreyling M, et al. Frontline therapy with rituximab added to the combination of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) significantly improves the outcome for patients with advanced-stage follicular lymphoma compared with therapy with CHOP alone: results of a prospective randomized study of the German Low-Grade Lymphoma Study Group. Blood. 2005;106(12):3725-3732. doi:10.1182/blood-2005-01-0016 DOI: https://doi.org/10.1182/blood-2005-01-0016

Marcus R, Imrie K, Solal-Celigny P, et al. Phase III study of R-CVP compared with cyclophosphamide, vincristine, and prednisone alone in patients with previously untreated advanced follicular lymphoma. J Clin Oncol. 2008;26(28):4579-4586. doi:10.1200/JCO.2007.13.5376 DOI: https://doi.org/10.1200/JCO.2007.13.5376

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):1506-1513. doi:10.1200/JCO.2012.45.0866 DOI: https://doi.org/10.1200/JCO.2012.45.0866

Luminari S, Ferrari A, Manni M, et al. Long-Term Results of the FOLL05 Trial Comparing R-CVP Versus R-CHOP Versus R-FM for the Initial Treatment of Patients With Advanced-Stage Symptomatic Follicular Lymphoma. J Clin Oncol. 2018;36(7):689-696. doi:10.1200/JCO.2017.74.1652 DOI: https://doi.org/10.1200/JCO.2017.74.1652

Flinn IW, van der Jagt R, Kahl BS, 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):2944-2952. doi:10.1182/blood-2013-11-531327 DOI: https://doi.org/10.1182/blood-2013-11-531327

Rummel MJ, 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):1203-1210. doi:10.1016/S0140- 6736(12)61763-2 DOI: https://doi.org/10.1016/S0140-6736(12)61763-2

Bruna R, Benedetti F, Boccomini C, et al. Prolonged survival in the absence of disease-recurrence in advanced-stage follicular lymphoma following chemo-immunotherapy: 13-year update of the prospective, multicenter randomized GITMO-IIL trial. Haematologica. 2019;104(11):2241-2248. doi:10.3324/haematol.2018.20993 DOI: https://doi.org/10.3324/haematol.2018.209932

Vidal L, Gafter-Gvili A, Salles G, et al. Rituximab maintenance improves overall survival of patients with follicular lymphoma-Individual patient data meta- analysis. Eur J Cancer. 2017;76:216-225. doi:10.1016/j.ejca.2017.01.02 DOI: https://doi.org/10.1016/j.ejca.2017.01.021

Roschewski M, Hill BT. One Size Does Not Fit All: Who Benefits From Maintenance After Frontline Therapy for Follicular Lymphoma? Am Soc Clin Oncol Educ Book. 2019;39:467-476. doi:10.1200/EDBK_23906 DOI: https://doi.org/10.1200/EDBK_239065

Morschhauser F, Fowler NH, Feugier P, et al. Rituximab plus Lenalidomide in Advanced Untreated Follicular Lymphoma. N Engl J Med. 2018;379(10):934-947. doi:10.1056/NEJMoa180510 DOI: https://doi.org/10.1056/NEJMoa1805104

Marcus R, Davies A, Ando K, et al. Obinutuzumab for the First-Line Treatment of Follicular Lymphoma. N Engl J Med. 2017;377(14):1331-1344. doi:10.1056/NEJMoa161459 DOI: https://doi.org/10.1056/NEJMoa1614598

Bachy E, Houot R, Feugier P, et al. Obinutuzumab plus lenalidomide (GALEN) in advanced, previously untreated follicular lymphoma in need of systemic therapy. Blood. Published online December 22, 2021:blood.2021013526. doi:10.1182/blood.202101352

Maurer MJ, Bachy E, Ghesquières H, et al. Early event status informs subsequent outcome in newly diagnosed follicular lymphoma. Am J Hematol. 2016;91(11):1096-1101. doi:10.1002/ajh.2449 DOI: https://doi.org/10.1002/ajh.24492

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. doi:10.1200/JCO.2014.59.753 DOI: https://doi.org/10.1200/JCO.2014.59.7534

Cheson BD, Friedberg JW, Kahl BS, Van der Jagt RH, Tremmel L. Bendamustine produces durable responses with an acceptable safety profile in patients with rituximab-refractory indolent non-Hodgkin lymphoma. Clin Lymphoma Myeloma Leuk. 2010;10(6):452-457. doi:10.3816/CLML.2010.n.07 DOI: https://doi.org/10.3816/CLML.2010.n.079

Rummel M, Kaiser U, Balser C, et al. 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(1):57-66. doi:10.1016/S1470-2045(15)00447-7 DOI: https://doi.org/10.1016/S1470-2045(15)00447-7

Cheson BD, Chua N, Mayer J, et al. Overall Survival Benefit in Patients With Rituximab-Refractory Indolent Non-Hodgkin Lymphoma Who Received Obinutuzumab Plus Bendamustine Induction and Obinutuzumab Maintenance in the GADOLIN Study. J Clin Oncol. 2018;36(22):2259-2266. doi:10.1200/JCO.2017.76.3656 DOI: https://doi.org/10.1200/JCO.2017.76.3656

Rummel MJ, Janssens A, MacDonald D, et al. A phase 3, randomized study of ofatumumab combined with bendamustine in rituximab-refractory iNHL (COMPLEMENT A + B study). Br J Haematol. 2021;193(6):1123-1133. doi:10.1111/bjh.1742 DOI: https://doi.org/10.1111/bjh.17420

Czuczman MS, Weaver R, Alkuzweny B, Berlfein J, Grillo-López AJ. Prolonged clinical and molecular remission in patients with low-grade or follicular non-Hodgkin’s lymphoma treated with rituximab plus CHOP chemotherapy: 9-year follow-up. J Clin Oncol. 2004;22(23):4711-4716. doi:10.1200/JCO.2004.04.02 DOI: https://doi.org/10.1200/JCO.2004.04.020

Leonard JP, Jung SH, Johnson J, et al. Randomized Trial of Lenalidomide Alone Versus Lenalidomide Plus Rituximab in Patients With Recurrent Follicular Lymphoma: CALGB 50401 (Alliance). J Clin Oncol. 2015;33(31):3635-3640. doi:10.1200/JCO.2014.59.925 DOI: https://doi.org/10.1200/JCO.2014.59.9258

Leonard JP, Trneny M, Izutsu K, et al. AUGMENT: A Phase III Study of Lenalidomide Plus Rituximab Versus Placebo Plus Rituximab in Relapsed or Refractory Indolent Lymphoma. J Clin Oncol. 2019;37(14):1188-1199. doi:10.1200/JCO.19.00010 DOI: https://doi.org/10.1200/JCO.19.00010

Morschhauser F, Le Gouill S, Feugier P, et al. Obinutuzumab combined with lenalidomide for relapsed or refractory follicular B-cell lymphoma (GALEN): a multicentre, single-arm, phase 2 study. Lancet Haematol. 2019;6(8):e429-e437. doi:10.1016/S2352-3026(19)30089-4 DOI: https://doi.org/10.1016/S2352-3026(19)30089-4

Pfreundschuh M, Kuhnt E, Trümper L, et al. CHOP-like chemotherapy with or without rituximab in young patients with good-prognosis diffuse large-B-cell lymphoma: 6-year results of an open-label randomised study of the MabThera International Trial (MInT) Group. Lancet Oncol. 2011;12(11):1013-1022. doi:10.1016/S1470-2045(11)70235-2 DOI: https://doi.org/10.1016/S1470-2045(11)70235-2

Pfreundschuh M, Schubert J, Ziepert M, et al. Six versus eight cycles of bi-weekly CHOP-14 with or without rituximab in elderly patients with aggressive CD20+ B-cell lymphomas: a randomised controlled trial (RICOVER-60). Lancet Oncol. 2008;9(2):105-116. doi:10.1016/S1470-2045(08)70002-0 DOI: https://doi.org/10.1016/S1470-2045(08)70002-0

Habermann TM, Weller EA, Morrison VA, et al. Rituximab-CHOP versus CHOP alone or with maintenance rituximab in older patients with diffuse large B-cell lymphoma. J Clin Oncol. 2006;24(19):3121-3127. doi:10.1200/JCO.2005.05.100 DOI: https://doi.org/10.1200/JCO.2005.05.1003

Dunleavy K, Fanale MA, Abramson JS, et al. Dose-adjusted EPOCH-R (etoposide, prednisone, vincristine, cyclophosphamide, doxorubicin, and rituximab) in untreated aggressive diffuse large B-cell lymphoma with MYC rearrangement: a prospective, multicentre, single-arm phase 2 study. Lancet Haematol. 2018;5(12):e609-e617. doi:10.1016/S2352-3026(18)30177-7 DOI: https://doi.org/10.1016/S2352-3026(18)30177-7

Crump M, Kuruvilla J, Couban S, et al. Randomized comparison of gemcitabine, dexamethasone, and cisplatin versus dexamethasone, cytarabine, and cisplatin chemotherapy before autologous stem-cell transplantation for relapsed and refractory aggressive lymphomas: NCIC-CTG LY.12. J Clin Oncol. 2014;32(31):3490-3496. doi:10.1200/JCO.2013.53.9593 DOI: https://doi.org/10.1200/JCO.2013.53.9593

Hagberg H, Gisselbrecht C, CORAL study group. Randomised phase III study of R-ICE versus R-DHAP in relapsed patients with CD20 diffuse large B-cell lymphoma (DLBCL) followed by high-dose therapy and a second randomisation to maintenance treatment with rituximab or not: an update of the CORAL study. Ann Oncol. 2006;17 Suppl 4:iv31-32. doi:10.1093/annonc/mdj996 DOI: https://doi.org/10.1093/annonc/mdj996

Schouten HC, Kvaloy S, Sydes M, Qian W, Fayers PM. The CUP trial: a randomized study analyzing the efficacy of high dose therapy and purging in low-grade non-Hodgkin’s lymphoma (NHL). Ann Oncol. 2000;11 Suppl 1:91-94. DOI: https://doi.org/10.1093/annonc/11.suppl_1.S91

Le Gouill S, De Guibert S, Planche L, et al. Impact of the use of autologous stem cell transplantation at first relapse both in naive and previously rituximab exposed follicular lymphoma patients treated in the GELA/GOELAMS FL2000 study. Haematologica. 2011;96(8):1128-1135. doi:10.3324/haematol.2010.030320 DOI: https://doi.org/10.3324/haematol.2010.030320

Manna M, Lee-Ying R, Davies G, et al. Autologous transplantation improves survival rates for follicular lymphoma patients who relapse within two years of chemoimmunotherapy: a multi-center retrospective analysis of consecutively treated patients in the real world. Leuk Lymphoma. 2019;60(1):133-141. doi:10.108 0/10428194.2018.1473576 DOI: https://doi.org/10.1080/10428194.2018.1473576

Casulo C, Friedberg JW, Ahn KW, 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 Transplant. 2018;24(6):1163-1171. doi:10.1016/j.bbmt.2017.12.771 DOI: https://doi.org/10.1016/j.bbmt.2017.12.771

Jurinovic V, Metzner B, Pfreundschuh M, 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 Transplant. 2018;24(6):1172-1179. doi:10.1016/j.bbmt.2018.03.022 DOI: https://doi.org/10.1016/j.bbmt.2018.03.022

Khouri IF, Milton DR, Gulbis AM, et al. Nine-Year Follow-up of Patients with Relapsed Follicular Lymphoma after Nonmyeloablative Allogeneic Stem Cell Transplant and Autologous Transplant. Clin Cancer Res. 2021;27(21):5847-5856. doi:10.1158/1078-0432.CCR-21-1377 DOI: https://doi.org/10.1158/1078-0432.CCR-21-1377

Hosing C, Saliba RM, McLaughlin P, et al. Long-term results favor allogeneic over autologous hematopoietic stem cell transplantation in patients with refractory or recurrent indolent non-Hodgkin’s lymphoma. Ann Oncol. 2003;14(5):737-744. doi:10.1093/annonc/mdg200 DOI: https://doi.org/10.1093/annonc/mdg200

van Besien K, Loberiza FR, Bajorunaite R, et al. Comparison of autologous and allogeneic hematopoietic stem cell transplantation for follicular lymphoma. Blood. 2003;102(10):3521-3529. doi:10.1182/blood-2003-04-1205 DOI: https://doi.org/10.1182/blood-2003-04-1205

Smith SM, Godfrey J, Ahn KW, et al. Autologous transplantation versus allogeneic transplantation in patients with follicular lymphoma experiencing early treatment failure. Cancer. 2018;124(12):2541-2551. doi:10.1002/cncr.31374 DOI: https://doi.org/10.1002/cncr.31374

Kanate AS, Kumar A, Dreger P, et al. Maintenance Therapies for Hodgkin and Non-Hodgkin Lymphomas After Autologous Transplantation: A Consensus Project of ASBMT, CIBMTR, and the Lymphoma Working Party of EBMT. JAMA Oncol. 2019;5(5):715-722. doi:10.1001/jamaoncol.2018.6278 DOI: https://doi.org/10.1001/jamaoncol.2018.6278

Hirayama AV, Gauthier J, Hay KA, et al. High rate of durable complete remission in follicular lymphoma after CD19 CAR-T cell immunotherapy. Blood. 2019;134(7):636-640. doi:10.1182/blood.2019000905 DOI: https://doi.org/10.1182/blood.2019000905

Assouline SE, Kim WS, Sehn LH, et al. Mosunetuzumab Shows Promising Efficacy in Patients with Multiply Relapsed Follicular Lymphoma: Updated Clinical Experience from a Phase I Dose-Escalation Trial. Blood. 2020;136:42-4. DOI: https://doi.org/10.1182/blood-2020-135839

Downloads

Published

2022-03-01

How to Cite

1.
Kansara R. Management of follicular lymphoma at first relapse. Can Hematol Today [Internet]. 2022 Mar. 1 [cited 2024 Apr. 20];1(1):16–21. Available from: https://canadianhematologytoday.com/article/view/1-1-2-kansara

Issue

Volume 1, Issue 1, March 2022

Section

Articles

Most read articles by the same author(s)