164
Views
7
CrossRef citations to date
0
Altmetric
Review

Chemotherapy-Free Management of Follicular and Marginal Zone Lymphoma

& ORCID Icon
Pages 3935-3952 | Published online: 14 May 2021

References

  • Surveillance, Epidemiology, and End Results (SEER) Program. SEER*Stat Database: incidence - SEER research limited-field data, 21 registries, Nov 2019 sub (2000–2017) - linked to county attributes - time dependent (1990–2017) income/ rurality,1969–2018 counties, National cancer institute, DCCPS, surveillance research program, released April 2020, based on the November 2019 submission. 2020. Available from: www.seer.cancer.gov. Accessed 53, 2021.
  • Olszewski AJ, Shafqat H, Ali S. Disparate survival outcomes after front-line chemoimmunotherapy in older patients with follicular, nodal marginal zone and small lymphocytic lymphoma. Leuk Lymphoma. 2015;56(4):942–950. doi:10.3109/10428194.2014.93601324956144
  • Swerdlow SH. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. Revised 4th ed. Lyon: World Health Organization, International Agency for Research on Cancer; 2017.
  • Treon SP, Xu L, Guerrera ML, et al. Genomic landscape of waldenstrom macroglobulinemia and its impact on treatment strategies. J Clin Oncol. 2020;38(11):1198–1208. doi:10.1200/JCO.19.0231432083995
  • Kahl BS, Yang DT. Follicular lymphoma: evolving therapeutic strategies. Blood. 2016;127(17):2055–2063. doi:10.1182/blood-2015-11-62428826989204
  • Bertoni F, Zucca E. State-of-the-art therapeutics: marginal-zone lymphoma. J Clin Oncol. 2005;23(26):6415–6420. doi:10.1200/JCO.2005.05.01816155028
  • Brady JL, Binkley MS, Hajj C, et al. Definitive radiotherapy for localized follicular lymphoma staged by (18)F-FDG PET-CT: a collaborative study by ILROG. Blood. 2019;133(3):237–245. doi:10.1182/blood-2018-04-84354030446493
  • MacManus M, Fisher R, Roos D, et al. Randomized trial of systemic therapy after involved-field radiotherapy in patients with early-stage follicular lymphoma: TROG 99.03. J Clin Oncol. 2018;36(29):2918–2925. doi:10.1200/JCO.2018.77.989229975623
  • Iannitto E, Tripodo C. How I diagnose and treat splenic lymphomas. Blood. 2011;117(9):2585–2595. doi:10.1182/blood-2010-09-27143721119113
  • Zucca E, Bertoni F. The spectrum of MALT lymphoma at different sites: biological and therapeutic relevance. Blood. 2016;127(17):2082–2092. doi:10.1182/blood-2015-12-62430426989205
  • 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)70027-024602760
  • 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.2004.10.08615024027
  • 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)61763-223433739
  • Garcia Munoz R, Izquierdo-Gil A, Munoz A, Roldan-Galiacho V, Rabasa P, Panizo C. Lymphocyte recovery is impaired in patients with chronic lymphocytic leukemia and indolent non-Hodgkin lymphomas treated with bendamustine plus rituximab. Ann Hematol. 2014;93(11):1879–1887. doi:10.1007/s00277-014-2135-824951124
  • Olszewski AJ, Reagan JL, Castillo JJ. Late infections and secondary malignancies after bendamustine/rituximab or RCHOP/RCVP chemotherapy for B-cell lymphomas. Am J Hematol. 2018;93(1):E1–E3. doi:10.1002/ajh.2492128960532
  • Fung M, Jacobsen E, Freedman A, et al. Increased risk of infectious complications in older patients with indolent non-hodgkin lymphoma exposed to bendamustine. Clin Infect Dis. 2019;68(2):247–255. doi:10.1093/cid/ciy45829800121
  • Mohile SG, Dale W, Somerfield MR, et al. Practical assessment and management of vulnerabilities in older patients receiving chemotherapy: ASCO guideline for geriatric oncology. J Clin Oncol. 2018;36(22):2326–2347. doi:10.1200/JCO.2018.78.868729782209
  • Abel GA, Klepin HD. Frailty and the management of hematologic malignancies. Blood. 2018;131(5):515–524. doi:10.1182/blood-2017-09-74642029141942
  • Rosko AE, Olin RL, Artz A, Wildes TM, Stauder R, Klepin HD. A call to action in hematologic disorders: a report from the ASH scientific workshop on hematology and aging. J Geriatr Oncol. 2018;9(4):287–290. doi:10.1016/j.jgo.2018.04.00629759912
  • Brice P, Bastion Y, Lepage E, et al. Comparison in low-tumor-burden follicular lymphomas between an initial no-treatment policy, prednimustine, or interferon alfa: a randomized study from the Groupe d’Etude des Lymphomes Folliculaires. Groupe d’Etude des Lymphomes de l’Adulte. J Clin Oncol. 1997;15(3):1110–1117. doi:10.1200/JCO.1997.15.3.11109060552
  • 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)14110-412932382
  • Solal-Celigny P, Roy P, Colombat P, et al. Follicular lymphoma international prognostic index. Blood. 2004;104(5):1258–1265. doi:10.1182/blood-2003-12-443415126323
  • Thieblemont C, Cascione L, Conconi A, et al. A MALT lymphoma prognostic index. Blood. 2017;130(12):1409–1417. doi:10.1182/blood-2017-03-77191528720586
  • Bachy E, Maurer MJ, Habermann TM, et al. A simplified scoring system in de novo follicular lymphoma treated initially with immunochemotherapy. Blood. 2018;132(1):49–58. doi:10.1182/blood-2017-11-81640529666118
  • Merli F, Luminari S, Tucci A, et al. Simplified geriatric assessment in older patients with diffuse large B-cell lymphoma: the prospective elderly project of the Fondazione Italiana Linfomi. J Clin Oncol. 2021;39(11):1214–1222. doi:10.1200/JCO.20.0246533577377
  • Di M, Huntington SF, Olszewski AJ. Challenges and opportunities in the management of diffuse large B-cell lymphoma in older patients. Oncologist. 2021;26(2):120–132. doi:10.1002/onco.1361033230948
  • Scheepers ERM, Vondeling AM, Thielen N, van der Griend R, Stauder R, Hamaker ME. Geriatric assessment in older patients with a hematologic malignancy: a systematic review. Haematologica. 2020;105(6):1484–1493. doi:10.3324/haematol.2019.24580332381581
  • Boccomini C, Ladetto M, Rigacci L, et al. A brief rituximab, bendamustine, mitoxantrone (R-BM) induction followed by rituximab consolidation in elderly patients with advanced follicular lymphoma: a Phase II study by the Fondazione Italiana Linfomi (FIL). Br J Haematol. 2021;193(2):280–289. doi:10.1111/bjh.1728333476434
  • Liu MA, DuMontier C, Murillo A, et al. Gait speed, grip strength, and clinical outcomes in older patients with hematologic malignancies. Blood. 2019;134(4):374–382. doi:10.1182/blood.201900075831167800
  • Hantel A, DuMontier C, Odejide OO, et al. Gait speed, survival, and recommended treatment intensity in older adults with blood cancer requiring treatment. Cancer. 2021;127(6):875–883. doi:10.1002/cncr.3334433237587
  • Goede V, Bahlo J, Chataline V, et al. Evaluation of geriatric assessment in patients with chronic lymphocytic leukemia: results of the CLL9 trial of the German CLL study group. Leuk Lymphoma. 2016;57(4):789–796. doi:10.3109/10428194.2015.109193326377031
  • Colombat P, Salles G, Brousse N, et al. Rituximab (anti-CD20 monoclonal antibody) as single first-line therapy for patients with follicular lymphoma with a low tumor burden: clinical and molecular evaluation. Blood. 2001;97(1):101–106. doi:10.1182/blood.V97.1.10111133748
  • Colombat P, Brousse N, Salles G, et al. Rituximab induction immunotherapy for first-line low-tumor-burden follicular lymphoma: survival analyses with 7-year follow-up. Ann Oncol. 2012;23(9):2380–2385. doi:10.1093/annonc/mds17722782332
  • Lockmer S, Ostenstad B, Hagberg H, et al. Chemotherapy-free initial treatment of advanced indolent lymphoma has durable effect with low toxicity: results from two nordic lymphoma group trials with more than 10 years of follow-up. J Clin Oncol. 2018:JCO1800262. doi:10.1200/JCO.18.0026230285560
  • Kimby E, Ostenstad B, Brown P, et al. Two courses of four weekly infusions of rituximab with or without interferon-alpha2a: final results from a randomized Phase III study in symptomatic indolent B-cell lymphomas. Leuk Lymphoma. 2015;56(9):2598–2607. doi:10.3109/10428194.2015.101436325686644
  • Martinelli G, Schmitz SF, Utiger U, et al. Long-term follow-up of patients with follicular lymphoma receiving single-agent rituximab at two different schedules in trial SAKK 35/98. J Clin Oncol. 2010;28(29):4480–4484. doi:10.1200/JCO.2010.28.478620697092
  • Moccia AA, Taverna C, Schar S, et al. Prolonged rituximab maintenance in follicular lymphoma patients: long-term results of the SAKK 35/03 randomized trial. Blood Adv. 2020;4(23):5951–5957. doi:10.1182/bloodadvances.202000285833275769
  • Kahl BS, Hong F, Williams ME, et al. Rituximab extended schedule or re-treatment trial for low-tumor burden follicular lymphoma: eastern cooperative oncology group protocol e4402. J Clin Oncol. 2014;32(28):3096–3102. doi:10.1200/JCO.2014.56.585325154829
  • Williams ME, Hong F, Gascoyne RD, et al. Rituximab extended schedule or retreatment trial for low tumour burden non-follicular indolent B-cell non-Hodgkin lymphomas: Eastern cooperative oncology group protocol E4402. Br J Haematol. 2016;173(6):867–875. doi:10.1111/bjh.1400726970533
  • Wagner LI, Zhao F, Hong F, et al. Anxiety and health-related quality of life among patients with low-tumor burden non-Hodgkin lymphoma randomly assigned to two different rituximab dosing regimens: results from ECOG trial E4402 (RESORT). J Clin Oncol. 2015;33(7):740–748. doi:10.1200/JCO.2014.57.680125605841
  • Davies A, Merli F, Mihaljević B, et al. Efficacy and safety of subcutaneous rituximab versus intravenous rituximab for first-line treatment of follicular lymphoma (SABRINA): a randomised, open-label, phase 3 trial. Lancet Haematol. 2017;4(6):e272–e282. doi:10.1016/S2352-3026(17)30078-928476440
  • Ogura M, Sancho JM, Cho SG, et al. Efficacy, pharmacokinetics, and safety of the biosimilar CT-P10 in comparison with rituximab in patients with previously untreated low-tumour-burden follicular lymphoma: a randomised, double-blind, parallel-group, phase 3 trial. Lancet Haematol. 2018;5(11):e543–e553. doi:10.1016/S2352-3026(18)30157-130389036
  • Maloney DG, Ogura M, Fukuhara N, et al. A phase 3 randomized study (HOMER) of ofatumumab vs rituximab in iNHL relapsed after rituximab-containing therapy. Blood Adv. 2020;4(16):3886–3893. doi:10.1182/bloodadvances.202000194232810220
  • Rosenbaum CA, Jung SH, Pitcher B, et al. Phase 2 multicentre study of single-agent ofatumumab in previously untreated follicular lymphoma: CALGB 50901 (Alliance). Br J Haematol. 2019;185(1):53–64. doi:10.1111/bjh.1576830723894
  • Freeman CL, Sehn LH. A tale of two antibodies: obinutuzumab versus rituximab. Br J Haematol. 2018;182(1):29–45. doi:10.1111/bjh.1523229741753
  • Salles GA, Morschhauser F, Solal-Celigny 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):2920–2926. doi:10.1200/JCO.2012.46.971823835715
  • Sehn LH, Goy A, Offner FC, 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. doi:10.1200/JCO.2014.59.213926282650
  • 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/NEJMoa161459828976863
  • Sehn LH, Chua N, Mayer J, 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):1081–1093. doi:10.1016/S1470-2045(16)30097-327345636
  • Fowler NH, 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):1311–1318. doi:10.1016/S1470-2045(14)70455-325439689
  • Martin P, Jung SH, Pitcher B, et al. A phase II trial of lenalidomide plus rituximab in previously untreated follicular non-Hodgkin’s lymphoma (NHL): CALGB 50803 (Alliance). Ann Oncol. 2017;28(11):2806–2812. doi:10.1093/annonc/mdx49628945884
  • 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/NEJMoa180510430184451
  • Thanarajasingam G, Leonard JP, Witzig TE, et al. Longitudinal toxicity over time (ToxT) analysis to evaluate tolerability: a case study of lenalidomide in the CALGB 50401 (Alliance) trial. Lancet Haematol. 2020;7(6):e490–e497. doi:10.1016/S2352-3026(20)30067-332470440
  • Ujjani CS, Jung SH, Pitcher B, et al. Phase 1 trial of rituximab, lenalidomide, and ibrutinib in previously untreated follicular lymphoma: alliance A051103. Blood. 2016;128(21):2510–2516. doi:10.1182/blood-2016-06-71810627697771
  • Smith SM, Pitcher BN, Jung SH, et al. Safety and tolerability of idelalisib, lenalidomide, and rituximab in relapsed and refractory lymphoma: the alliance for clinical trials in oncology A051201 and A051202 phase 1 trials. Lancet Haematol. 2017;4(4):e176–e182. doi:10.1016/S2352-3026(17)30028-528314699
  • Becnel MR, Nastoupil LJ, Samaniego F, et al. Lenalidomide plus rituximab (R(2)) in previously untreated marginal zone lymphoma: subgroup analysis and long-term follow-up of an open-label phase 2 trial. Br J Haematol. 2019;185(5):874–882. doi:10.1111/bjh.1584330919940
  • Zucca E, Rondeau S, Vanazzi A, et al. Short regimen of rituximab plus lenalidomide in follicular lymphoma patients in need of first-line therapy. Blood. 2019;134(4):353–362. doi:10.1182/blood-2018-10-87964331101627
  • Morschhauser F, Radford J, Van Hoof A, et al. 90Yttrium-ibritumomab tiuxetan consolidation of first remission in advanced-stage follicular non-Hodgkin lymphoma: updated results after a median follow-up of 7.3 years from the international, randomized, phase III first-lineindolent trial. J Clin Oncol. 2013;31(16):1977–1983. doi:10.1200/JCO.2012.45.640023547079
  • Zinzani PL, Tani M, Pulsoni A, et al. Fludarabine and mitoxantrone followed by yttrium-90 ibritumomab tiuxetan in previously untreated patients with follicular non-Hodgkin lymphoma trial: a phase II non-randomised trial (FLUMIZ). Lancet Oncol. 2008;9(4):352–358. doi:10.1016/S1470-2045(08)70039-118342572
  • Ibatici A, Pica GM, Nati S, et al. Safety and efficacy of (90) yttrium-ibritumomab-tiuxetan for untreated follicular lymphoma patients. An Italian cooperative study. Br J Haematol. 2014;164(5):710–716. doi:10.1111/bjh.1269524344981
  • Samaniego F, Berkova Z, Romaguera JE, et al. 90Y-ibritumomab tiuxetan radiotherapy as first-line therapy for early stage low-grade B-cell lymphomas, including bulky disease. Br J Haematol. 2014;167(2):207–213. doi:10.1111/bjh.1302125040450
  • Scholz CW, Pinto A, Linkesch W, et al. (90)Yttrium-ibritumomab-tiuxetan as first-line treatment for follicular lymphoma: 30 months of follow-up data from an international multicenter phase II clinical trial. J Clin Oncol. 2013;31(3):308–313. doi:10.1200/JCO.2011.41.155323233718
  • Czuczman MS, Emmanouilides C, Darif M, et al. Treatment-related myelodysplastic syndrome and acute myelogenous leukemia in patients treated with ibritumomab tiuxetan radioimmunotherapy. J Clin Oncol. 2007;25(27):4285–4292. doi:10.1200/JCO.2006.09.288217709799
  • Epperla N, Pham AQ, Burnette BL, et al. Risk of histological transformation and therapy-related myelodysplasia/acute myeloid leukaemia in patients receiving radioimmunotherapy for follicular lymphoma. Br J Haematol. 2017;178(3):427–433. doi:10.1111/bjh.1468828466487
  • Di M, Ollila TA, Olszewski AJ. Exposure to ibritumomab tiuxetan and incidence of treatment-related myeloid neoplasms among older patients with B-cell lymphoma: a population-based study. Leukemia. 2020;34(10):2794–2797. doi:10.1038/s41375-020-0798-932203140
  • Illidge TM, Mayes S, Pettengell R, et al. Fractionated (9)(0)Y-ibritumomab tiuxetan radioimmunotherapy as an initial therapy of follicular lymphoma: an international phase II study in patients requiring treatment according to GELF/BNLI criteria. J Clin Oncol. 2014;32(3):212–218. doi:10.1200/JCO.2013.50.311024297953
  • Lossos IS, Fabregas JC, Koru-Sengul T, et al. Phase II study of (90)Y Ibritumomab tiuxetan (Zevalin) in patients with previously untreated marginal zone lymphoma. Leuk Lymphoma. 2015;56(6):1750–1755. doi:10.3109/10428194.2014.97580125315074
  • Dreyling M, Thieblemont C, Gallamini A, et al. ESMO Consensus conferences: guidelines on malignant lymphoma. part 2: marginal zone lymphoma, mantle cell lymphoma, peripheral T-cell lymphoma. Ann Oncol. 2013;24(4):857–877. doi:10.1093/annonc/mds64323425945
  • Zucca E, Conconi A, Martinelli G, et al. Final results of the IELSG-19 randomized trial of mucosa-associated lymphoid tissue lymphoma: improved event-free and progression-free survival with rituximab plus chlorambucil versus either chlorambucil or rituximab monotherapy. J Clin Oncol. 2017;35(17):1905–1912. doi:10.1200/JCO.2016.70.699428355112
  • Olszewski AJ, Ollila TA, Reagan JL. Bendamustine-rituximab does not improve survival over rituximab monotherapy for older patients with nodal or splenic marginal zone lymphoma. Blood. 2019;134(Supplement_1):2824. doi:10.1182/blood-2019-121841
  • Else M, Marin-Niebla A, de la Cruz F, et al. Rituximab, used alone or in combination, is superior to other treatment modalities in splenic marginal zone lymphoma. Br J Haematol. 2012;159(3):322–328. doi:10.1111/bjh.1203623016878
  • Hoskin P, Popova B, Schofield O, et al. 4 Gy versus 24 Gy radiotherapy for follicular and marginal zone lymphoma (FoRT): long-term follow-up of a multicentre, randomised, phase 3, non-inferiority trial. Lancet Oncol. 2021;22(3):332–340. doi:10.1016/S1470-2045(20)30686-033539729
  • 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. doi:10.1634/theoncologist.2012-025123345547
  • Olszewski AJ, Ali S. Comparative outcomes of rituximab-based systemic therapy and splenectomy in splenic marginal zone lymphoma. Ann Hematol. 2014;93(3):449–458. doi:10.1007/s00277-013-1900-424057925
  • Kalpadakis C, Pangalis GA, Sachanas S, et al. Rituximab monotherapy in splenic marginal zone lymphoma: prolonged responses and potential benefit from maintenance. Blood. 2018;132(6):666–670. doi:10.1182/blood-2018-02-83360829914978
  • 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. doi:10.1056/NEJMoa01337612110736
  • Xing KH, Kahlon A, Skinnider BF, et al. Outcomes in splenic marginal zone lymphoma: analysis of 107 patients treated in British Columbia. Br J Haematol. 2015;169(4):520–527. doi:10.1111/bjh.1332025854936
  • El Weshi A, Ribrag V, Girinski T, El Hajj M, Dhermain F, Bayle C. Low and medium dose spleen radiation therapy are able to induce long-term responses in splenic lymphoma with villous lymphocytes. Br J Haematol. 1998;103(4):1212–1213. doi:10.1046/j.1365-2141.1998.1161f.x9886348
  • 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.2014.59.753426124482
  • Moccia AA, Schar S, Hayoz S, et al. Prognostic value of POD24 validation in follicular lymphoma patients initially treated with chemotherapy-free regimens in a pooled analysis of three randomized trials of the Swiss group for clinical cancer research (SAKK). Br J Haematol. 2021;192(6):1031–1034. doi:10.1111/bjh.1704532805081
  • Leblond V, Johnson S, Chevret S, et al. Results of a randomized trial of chlorambucil versus fludarabine for patients with untreated Waldenstrom macroglobulinemia, marginal zone lymphoma, or lymphoplasmacytic lymphoma. J Clin Oncol. 2013;31(3):301–307. doi:10.1200/JCO.2012.44.792023233721
  • Zucca E, Conconi A, Laszlo D, et al. Addition of rituximab to chlorambucil produces superior event-free survival in the treatment of patients with extranodal marginal-zone B-cell lymphoma: 5-year analysis of the IELSG-19 randomized study. J Clin Oncol. 2013;31(5):565–572. doi:10.1200/JCO.2011.40.627223295789
  • Martinelli G, Laszlo D, Bertolini F, et al. Chlorambucil in combination with induction and maintenance rituximab is feasible and active in indolent non-Hodgkin’s lymphoma. Br J Haematol. 2003;123(2):271–277. doi:10.1046/j.1365-2141.2003.04586.x14531908
  • Davis TA, Grillo-López AJ, White CA, et al. Rituximab anti-CD20 monoclonal antibody therapy in non-Hodgkin’s lymphoma: safety and efficacy of re-treatment. J Clin Oncol. 2000;18(17):3135–3143. doi:10.1200/JCO.2000.18.17.313510963642
  • Vanazzi A, Grana C, Crosta C, et al. Efficacy of (9)(0)Yttrium-ibritumomab tiuxetan in relapsed/refractory extranodal marginal-zone lymphoma. Hematol Oncol. 2014;32(1):10–15. doi:10.1002/hon.207823696416
  • Gordon LI, Molina A, Witzig T, et al. Durable responses after ibritumomab tiuxetan radioimmunotherapy for CD20+ B-cell lymphoma: long-term follow-up of a phase 1/2 study. Blood. 2004;103(12):4429–4431. doi:10.1182/blood-2003-11-388315016644
  • Emmanouilides C, Witzig TE, Gordon LI, et al. Treatment with yttrium 90 ibritumomab tiuxetan at early relapse is safe and effective in patients with previously treated B-cell non-Hodgkin’s lymphoma. Leuk Lymphoma. 2006;47(4):629–636. doi:10.1080/1042819050037607616690521
  • Witzig TE, Flinn IW, Gordon LI, et al. Treatment with ibritumomab tiuxetan radioimmunotherapy in patients with rituximab-refractory follicular non-Hodgkin’s lymphoma. J Clin Oncol. 2002;20(15):3262–3269. doi:10.1200/JCO.2002.11.01712149300
  • Witzig TE, Gordon LI, Cabanillas F, 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 Clin Oncol. 2002;20(10):2453–2463. doi:10.1200/JCO.2002.11.07612011122
  • Lolli G, Argnani L, Broccoli A, et al. (90) Y-ibritumomab tiuxetan in patients with extra-nodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma) - The Zeno Study. Br J Haematol. 2020;189(1):e6–e9. doi:10.1111/bjh.1640431944265
  • 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.19.0001030897038
  • 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)30089-431296423
  • 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.2014.59.925826304886
  • 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):5404–5409. doi:10.1200/JCO.2008.21.116919805688
  • Witlox WJA, Grimm SE, Riemsma R, et al. Lenalidomide with rituximab for previously treated follicular lymphoma and marginal zone lymphoma: an evidence review group perspective of a NICE single technology appraisal. Pharmacoeconomics. 2021;39(2):171–180. doi:10.1007/s40273-020-00971-x33145711
  • von Keudell G, Moskowitz AJ. The role of PI3K inhibition in lymphoid malignancies. Curr Hematol Malig Rep. 2019;14(5):405–413. doi:10.1007/s11899-019-00540-w31359259
  • Cheah CY, Fowler NH. Idelalisib in the management of lymphoma. Blood. 2016;128(3):331–336. doi:10.1182/blood-2016-02-70276127252232
  • Gopal AK, Kahl BS, de Vos S, et al. PI3Kdelta inhibition by idelalisib in patients with relapsed indolent lymphoma. N Engl J Med. 2014;370(11):1008–1018. doi:10.1056/NEJMoa131458324450858
  • Bird ST, Tian F, Flowers N, et al. Idelalisib for treatment of relapsed follicular lymphoma and chronic lymphocytic leukemia: a comparison of treatment outcomes in clinical trial participants vs medicare beneficiaries. JAMA Oncol. 2020;6(2):248–254. doi:10.1001/jamaoncol.2019.399431855259
  • Coutre SE, Barrientos JC, Brown JR, et al. Management of adverse events associated with idelalisib treatment: expert panel opinion. Leuk Lymphoma. 2015;56(10):2779–2786. doi:10.3109/10428194.2015.102277025726955
  • Flinn IW, Miller CB, Ardeshna KM, et al. DYNAMO: a phase II study of duvelisib (IPI-145) in patients with refractory indolent non-Hodgkin lymphoma. J Clin Oncol. 2019;37(11):912–922. doi:10.1200/JCO.18.0091530742566
  • Burris HA, Flinn IW, Patel MR, et al. Umbralisib, a novel PI3Kdelta and casein kinase-1epsilon inhibitor, in relapsed or refractory chronic lymphocytic leukaemia and lymphoma: an open-label, phase 1, dose-escalation, first-in-human study. Lancet Oncol. 2018;19(4):486–496. doi:10.1016/S1470-2045(18)30082-229475723
  • Fowler NH, Samaniego F, Jurczak W, et al. Umbralisib, a dual PI3Kdelta/CK1epsilon Inhibitor in patients with relapsed or refractory indolent lymphoma. J Clin Oncol. 2021:JCO2003433. doi:10.1200/JCO.20.03433
  • Dreyling M, Santoro A, Mollica L, et al. Phosphatidylinositol 3-kinase inhibition by copanlisib in relapsed or refractory indolent lymphoma. J Clin Oncol. 2017;35(35):3898–3905. doi:10.1200/JCO.2017.75.464828976790
  • Panayiotidis P, Follows GA, Mollica L, et al. Efficacy and safety of copanlisib in patients with relapsed or refractory marginal zone lymphoma. Blood Adv. 2021;5(3):823–828. doi:10.1182/bloodadvances.202000291033560394
  • Gopal AK, Schuster SJ, Fowler NH, et al. Ibrutinib as treatment for patients with relapsed/refractory follicular lymphoma: results from the open-label, multicenter, phase II DAWN study. J Clin Oncol. 2018;36(23):2405–2412. doi:10.1200/JCO.2017.76.885329851546
  • Bartlett NL, Costello BA, LaPlant BR, et al. Single-agent ibrutinib in relapsed or refractory follicular lymphoma: a phase 2 consortium trial. Blood. 2018;131(2):182–190. doi:10.1182/blood-2017-09-80464129074501
  • Noy A, de Vos S, Thieblemont C, et al. Targeting Bruton tyrosine kinase with ibrutinib in relapsed/refractory marginal zone lymphoma. Blood. 2017;129(16):2224–2232. doi:10.1182/blood-2016-10-74734528167659
  • Noy A, de Vos S, Coleman M, et al. Durable ibrutinib responses in relapsed/refractory marginal zone lymphoma: long-term follow-up and biomarker analysis. Blood Adv. 2020;4(22):5773–5784. doi:10.1182/bloodadvances.202000312133227125
  • Pastore A, Jurinovic V, Kridel R, et al. Integration of gene mutations in risk prognostication for patients receiving first-line immunochemotherapy for follicular lymphoma: a retrospective analysis of a prospective clinical trial and validation in a population-based registry. Lancet Oncol. 2015;16(9):1111–1122. doi:10.1016/S1470-2045(15)00169-226256760
  • Morschhauser F, Tilly H, Chaidos A, et al. Tazemetostat for patients with relapsed or refractory follicular lymphoma: an open-label, single-arm, multicentre, phase 2 trial. Lancet Oncol. 2020;21(11):1433–1442. doi:10.1016/S1470-2045(20)30441-133035457
  • Dave SS, Wright G, Tan B, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med. 2004;351(21):2159–2169. doi:10.1056/NEJMoa04186915548776
  • Fowler NH, Cheah CY, Gascoyne RD, et al. Role of the tumor microenvironment in mature B-cell lymphoid malignancies. Haematologica. 2016;101(5):531–540. doi:10.3324/haematol.2015.13949327132279
  • Goy A, Forero A, Wagner-Johnston N, et al. A phase 2 study of inotuzumab ozogamicin in patients with indolent B-cell non-Hodgkin lymphoma refractory to rituximab alone, rituximab and chemotherapy, or radioimmunotherapy. Br J Haematol. 2016;174(4):571–581. doi:10.1111/bjh.1409427101934
  • Diefenbach C, Kahl BS, Banerjee L, et al. Polatuzumab vedotin plus obinutuzumab and lenalidomide in patients with relapsed/refractory follicular lymphoma: primary analysis of the full efficacy population in a phase Ib/II trial. Blood. 2019;134(Supplement_1):126. doi:10.1182/blood-2019-123669
  • Palanca-Wessels MC, Czuczman M, Salles G, et al. Safety and activity of the anti-CD79B antibody-drug conjugate polatuzumab vedotin in relapsed or refractory B-cell non-Hodgkin lymphoma and chronic lymphocytic leukaemia: a phase 1 study. Lancet Oncol. 2015;16(6):704–715. doi:10.1016/S1470-2045(15)70128-225925619
  • Morschhauser F, Flinn IW, Advani R, et al. Polatuzumab vedotin or pinatuzumab vedotin plus rituximab in patients with relapsed or refractory non-Hodgkin lymphoma: final results from a phase 2 randomised study (ROMULUS). Lancet Haematol. 2019;6(5):e254–e265. doi:10.1016/S2352-3026(19)30026-230935953
  • Hamadani M, Radford J, Carlo-Stella C, et al. Final results of a phase 1 study of loncastuximab tesirine in relapsed/refractory B-cell non-Hodgkin lymphoma. Blood. 2020. doi:10.1182/blood.2020007512
  • Jurczak W, Zinzani PL, Gaidano G, et al. Phase IIa study of the CD19 antibody MOR208 in patients with relapsed or refractory B-cell non-Hodgkin’s lymphoma. Ann Oncol. 2018;29(5):1266–1272. doi:10.1093/annonc/mdy05629444231
  • Salles G, Duell J, Gonzalez Barca E, et al. Tafasitamab plus lenalidomide in relapsed or refractory diffuse large B-cell lymphoma (L-MIND): a multicentre, prospective, single-arm, phase 2 study. Lancet Oncol. 2020;21(7):978–988. doi:10.1016/S1470-2045(20)30225-432511983
  • Jacobson CA, Maus MV. C(h)AR-ting a new course in incurable lymphomas: CAR T cells for mantle cell and follicular lymphomas. Blood Adv. 2020;4(22):5858–5862. doi:10.1182/bloodadvances.202000339133232481
  • Jacobson C, Chavez JC, Sehgal AR, et al. Primary analysis of Zuma-5: a phase 2 study of Axicabtagene Ciloleucel (Axi-Cel) in patients with relapsed/refractory (R/R) indolent non-Hodgkin lymphoma (iNHL). Blood. 2020;136(Supplement 1):40–41.
  • Neelapu SS, Jacobson CA, Oluwole OO, et al. Outcomes of older patients in ZUMA-1, a pivotal study of axicabtagene ciloleucel in refractory large B-cell lymphoma. Blood. 2020;135(23):2106–2109. doi:10.1182/blood.201900416232181801
  • Goebeler ME, Knop S, Viardot A, et al. Bispecific T-cell engager (BiTE) antibody construct blinatumomab for the treatment of patients with relapsed/refractory non-Hodgkin lymphoma: final results from a phase I study. J Clin Oncol. 2016;34(10):1104–1111. doi:10.1200/JCO.2014.59.158626884582
  • Sun LL, Ellerman D, Mathieu M, et al. Anti-CD20/CD3 T cell-dependent bispecific antibody for the treatment of B cell malignancies. Sci Transl Med. 2015;7(287):287ra270. doi:10.1126/scitranslmed.aaa4802
  • Budde LE, O’Hear C, Li CC, et al. Mosunetuzumab induces complete remissions in poor prognosis non-Hodgkin lymphoma patients, including those who are resistant to or relapsing after chimeric antigen receptor T-cell (CAR-T) therapies, and is active in treatment through multiple lines. Blood. 2019;134(Supplement_1):6. doi:10.1182/blood-2019-12374231273004
  • 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(Supplement 1):42–44. doi:10.1182/blood-2020-135839
  • Olszewski AJ, Avigdor A, Babu S, et al. Single-agent mosunetuzumab is a promising safe and efficacious chemotherapy-free regimen for elderly/unfit patients with previously untreated diffuse large B-cell lymphoma. Blood. 2020;136(Supplement 1):43–45. doi:10.1182/blood-2020-136255
  • Hutchings M, Mous R, Clausen MR, et al. Subcutaneous epcoritamab induces complete responses with an encouraging safety profile across relapsed/refractory B-cell non-Hodgkin lymphoma subtypes, including patients with prior CAR-T therapy: updated dose escalation data. Blood. 2020;136(Supplement 1):45–46. doi:10.1182/blood-2020-133820
  • Hutchings M, Morschhauser F, Iacoboni G, et al. Glofitamab, a novel, bivalent CD20-targeting T-cell-engaging bispecific antibody, induces durable complete remissions in relapsed or refractory B-cell lymphoma: a phase I trial. J Clin Oncol. 2021:JCO2003175. doi:10.1200/JCO.20.0317533739857
  • Bannerji R, Allan JN, Arnason JE, et al. Odronextamab (REGN1979), a human CD20 x CD3 bispecific antibody, induces durable, complete responses in patients with highly refractory B-cell non-Hodgkin lymphoma, including patients refractory to CAR T therapy. Blood. 2020;136(Supplement 1):42–43. doi:10.1182/blood-2020-136659
  • Lesokhin AM, Ansell SM, Armand P, et al. Nivolumab in patients with relapsed or refractory hematologic malignancy: preliminary results of a phase Ib study. J Clin Oncol. 2016;34(23):2698–2704. doi:10.1200/JCO.2015.65.978927269947
  • Armand P, Janssens A, Gritti G, et al. Efficacy and safety results from CheckMate 140, a phase 2 study of nivolumab for relapsed/refractory follicular lymphoma. Blood. 2021;137(5):637–645. doi:10.1182/blood.201900475332870269
  • Yang ZZ, Kim HJ, Wu H, et al. TIGIT expression is associated with T-cell suppression and exhaustion and predicts clinical outcome and anti-PD-1 response in follicular lymphoma. Clin Cancer Res. 2020;26(19):5217–5231. doi:10.1158/1078-0432.CCR-20-055832631956
  • Herrera AF, Goy A, Mehta A, et al. Safety and activity of ibrutinib in combination with durvalumab in patients with relapsed or refractory follicular lymphoma or diffuse large B-cell lymphoma. Am J Hematol. 2020;95(1):18–27. doi:10.1002/ajh.2565931621094
  • Miller PG, Sperling AS, Gibson CJ, et al. A deep molecular response of splenic marginal zone lymphoma to front-line checkpoint blockade. Haematologica. 2021;106(2):651–654. doi:10.3324/haematol.2020.25842633054119
  • Davids MS, Roberts AW, Seymour JF, et al. Phase I first-in-human study of venetoclax in patients with relapsed or refractory non-Hodgkin lymphoma. J Clin Oncol. 2017;35(8):826–833. doi:10.1200/JCO.2016.70.432028095146
  • Zinzani PL, Flinn IW, Yuen SLS, et al. Venetoclax-rituximab with or without bendamustine vs bendamustine-rituximab in relapsed/refractory follicular lymphoma. Blood. 2020;136(23):2628–2637. doi:10.1182/blood.202000558832785666
  • Seymour JF, Kipps TJ, Eichhorst B, et al. Venetoclax-rituximab in relapsed or refractory chronic lymphocytic leukemia. N Engl J Med. 2018;378(12):1107–1120. doi:10.1056/NEJMoa171397629562156
  • Michot JM, Bouabdallah R, Vitolo U, et al. Avadomide plus obinutuzumab in patients with relapsed or refractory B-cell non-Hodgkin lymphoma (CC-122-NHL-001): a multicentre, dose escalation and expansion phase 1 study. Lancet Haematol. 2020;7(9):e649–e659. doi:10.1016/S2352-3026(20)30208-832758434
  • Panayiotidis P, Tumyan G, Thieblemont C, et al. Primary Analysis of the Tegar Study: a Phase II Study Exploring the Safety and Efficacy of Atezolizumab in Combination with Obinutuzumab or Rituximab in Patients with Relapsed or Refractory (R/R) Mantle Cell Lymphoma (MCL), Marginal Zone Lymphoma (MZL), or Waldenstrom Macroglobulinemia (WM). Blood. 2020;136(Supplement 1):2–3.
  • Michot JM, Bouabdallah R, Doorduijn JK, et al. Long-term results from a phase 1b study of avadomide in combination with obinutuzumab in patients with relapsed and/or refractory B-cell non-Hodgkin lymphoma. Blood. 2020;136(Supplement 1):41–42. doi:10.1182/blood-2020-134949
  • Opat S, Tedeschi A, Linton K, et al. Efficacy and safety of zanubrutinib in patients with relapsed/refractory marginal zone lymphoma: initial results of the MAGNOLIA (BGB-3111-214) trial. Blood. 2020;136(Supplement 1):28–30. doi:10.1182/blood-2020-134611