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).


Journal

British journal of haematology
ISSN: 1365-2141
Titre abrégé: Br J Haematol
Pays: England
ID NLM: 0372544

Informations de publication

Date de publication:
04 2021
Historique:
received: 03 09 2020
accepted: 24 11 2020
pubmed: 22 1 2021
medline: 25 9 2021
entrez: 21 1 2021
Statut: ppublish

Résumé

Treatment for follicular lymphoma (FL) in the elderly is not well standardized. A phase II, multicentre, single arm trial was conducted in this setting with a brief chemoimmunotherapy regimen. Treatment consisted in four monthly courses of rituximab, bendamustine and mitoxantrone (R-BM) followed by 4 weekly rituximab as consolidation; rituximab maintenance was not applied because the drug was not licensed at the time of enrolment. The primary endpoint was the complete remission rate (CR). Seventy-six treatment-naive FL patients (aged 65-80 and a "FIT" score, according to the Comprehensive Geriatric Assessment) were enrolled. CR was documented in 59/76 patients (78%), partial remission in 12 (16%) and stable/progressive disease in five (6%) with an overall response rate in 71/76 (94%). Median follow-up was 44 months with 3-year progression-free-survival (PFS) and overall-survival of 67% and 92% respectively. Nine deaths occurred, three of progressive disease. The regimen was well tolerated and the most frequent severe toxicity was neutropenia (18% of the cycles). Bcl-2/IGH rearrangement was found in 40/75 (53%) of evaluated patients. R-BM was highly effective in clearing polymerase chain reaction-detectable disease: 29/31 (96%) evaluated patients converted to bcl-2/IGH negativity at the end of treatment. A brief R-BM regimen plus rituximab consolidation is effective and safe in "FIT" elderly, treatment-naïve, FL patients, inducing high CR and molecular remission rates with prolonged PFS.

Identifiants

pubmed: 33476434
doi: 10.1111/bjh.17283
doi:

Substances chimiques

Antineoplastic Agents, Alkylating 0
Antineoplastic Agents, Immunological 0
Topoisomerase II Inhibitors 0
Rituximab 4F4X42SYQ6
Bendamustine Hydrochloride 981Y8SX18M
Mitoxantrone BZ114NVM5P

Banques de données

ClinicalTrials.gov
['NCT01523860']

Types de publication

Clinical Trial, Phase II Journal Article Multicenter Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

280-289

Informations de copyright

© 2020 British Society for Haematology and John Wiley & Sons Ltd.

Références

Harris NL, Jaffe ES, Diebold J, Flandrin G, Muller-Hermelink HK, Vardiman J, et al. The World Health Organization classification of neoplastic diseases of the haematopoietic and lymphoid tissues: Report of the Clinical Advisory Committee Meeting, Airlie House, Virginia, November 1997. Histopathology. 2000;36:69-86.
Federico M, Luminari S, Dondi A, Tucci A, Vitolo U, Rigacci L, 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;31:1506-13.
Luminari S, Ferrari A, Manni M, Dondi A, Chiarenza A, Merli F, 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;36:689-96.
Forstpointner R, Unterhalt M, Dreyling M, Bock H-P, Repp R, Wandt H, et al. Maintenance therapy with rituximab leads to a significant prolongation of response duration after salvage therapy with a combination of rituximab, fludarabine, cyclophosphamide, and mitoxantrone (R-FCM) in patients with recurring and refractory follicular and mantle cell lymphomas: results of a prospective randomized study of the German Low Grade Lymphoma Study Group (GLSG). Blood. 2006;108:4003-8.
Magnano L, Montoto S, González-Barca E, Briones J, Sancho JM, Muntañola A, et al. Long-term safety and outcome of fludarabine, cyclophosphamide and mitoxantrone (FCM) regimen in previously untreated patients with advanced follicular lymphoma: 12 years follow-up of a phase 2 trial. Ann Hematol. 2017;96:639-46.
Vitolo U, Ladetto M, Boccomini C, Baldini L, De Angelis F, Tucci A, et al. Rituximab maintenance compared with observation after brief first-line R-FND chemoimmunotherapy with rituximab consolidation in patients age older than 60 years with advanced follicular lymphoma: a phase III randomized study by the Fondazione Italiana Linfomi. J Clin Oncol. 2013;31:3351-9.
Brice P, Bastion Y, Lepage E, Brousse N, Haïoun C, Moreau P, 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;15:1110-7.
Spina M, Balzarotti M, Uziel L, Ferreri AJM, Fratino L, Magagnoli M, et al. Modulated chemotherapy according to modified comprehensive geriatric assessment in 100 consecutive elderly patients with diffuse large B-cell lymphoma. Oncologist. 2012;17:838-46.
Ladetto M, Sametti S, Donovan JW, Ferrero D, Astolfi M, Mitterer M, et al. A validated real-time quantitative PCR approach shows a correlation between tumor burden and successful ex vivo purging in follicular lymphoma patients. Exp Hematol. 2001;29:183-93.
Ladetto M, Lobetti-Bodoni C, Mantoan B, Ceccarelli M, Boccomini C, Genuardi E, et al. Persistence of minimal residual disease in bone marrow predicts outcome in follicular lymphomas treated with a rituximab-intensive program. Blood. 2013;122:3759-66.
van der Velden VHJ, Cazzaniga G, Schrauder A, Hancock J, Bader P, Panzer-Grumayer ER, et al. Analysis of minimal residual disease by Ig/TCR gene rearrangements: guidelines for interpretation of real-time quantitative PCR data. Leukemia. 2007;21:604-11.
Marcus R, Imrie K, Belch A, Cunningham D, Flores E, Catalano J, et al. CVP chemotherapy plus rituximab compared with CVP as first-line treatment for advanced follicular lymphoma. Blood. 2005;105:1417-23.
Hiddemann W, Kneba M, Dreyling M, Schmitz N, Lengfelder E, Schmits R, 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: R. Blood. 2005;106:3725-32.
Schulz H, Bohlius J, Skoetz N, Trelle S, Kober T, Reiser M, et al. Chemotherapy plus Rituximab versus chemotherapy alone for B-cell non-Hodgkin's lymphoma. Cochrane Database Syst Rev. 2007; 17:1-71.
Forstpointner R, Dreyling M, Repp R, Hermann S, Hänel A, Metzner B, et al. The addition of rituximab to a combination of fludarabine, cyclophosphamide, mitoxantrone (FCM) significantly increases the response rate and prolongs survival as compared with FCM alone in patients with relapsed and refractory follicular and mantle cell lymphomas: Results of a prospective randomized study of the German Low-Grade Lymphoma Study Group. Blood. 2004;104:3064-71.
Salles G, Mounier N, De Guibert S, Morschhauser F, Doyen C, Rossi JF, et al. Rituximab combined with chemotherapy and interferon in follicular lymphoma patients: results of the GELA-GOELAMS FL2000 study. Blood. 2008;112:4824-31.
Herold M, Haas A, Srock S, Neser S, Al-Ali KH, Neubauer A, et al. Rituximab added to first-line mitoxantrone, chlorambucil, and prednisolone chemotherapy followed by interferon maintenance prolongs survival in patients with advanced follicular lymphoma: an East German study group hematology and oncology study. J Clin Oncol. 2007;25:1986-92.
Cheson BD, Pfistner B, Juweid ME, Gascoyne RD, Specht L, Horning SJ, et al. Revised response criteria for malignant lymphoma. J Clin Oncol. 2007;25:579-86.
Rummel MJ, Niederle N, Maschmeyer G, Banat GA, von Grünhagen U, Losem C, 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 (London, England). 2013;381:1203-10.
Flinn IW, van der Jagt R, Kahl BS, Wood P, Hawkins TE, MacDonald D, 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;123:2944-52.
Weide R, Hess G, Köppler H, Heymanns J, Thomalla J, Aldaoud A, et al. High anti-lymphoma activity of bendamustine/mitoxantrone/rituximab in rituximab pretreated relapsed or refractory indolent lymphomas and mantle cell lymphomas. A multicenter phase II study of the German Low Grade Lymphoma Study Group (GLSG). Leuk Lymphoma. 2007;48:1299-306.
Rummel MJ, Maschmeyer G, Ganser A, Heider A, von Grünhagen U, Losem C, et al. Bendamustine Plus Rituximab (B-R) versus CHOP Plus Rituximab (CHOP-R) As first-line treatment in patients with indolent and mantle cell lymphomas (MCL) - 7 year updated results from the StiL NHL1 Study. Blood. 2014;124:4407.
Rummel MJ, Heine K, Bodenstein H, Baldus M, Stauch M, von Gruenhagen U, et al. Efficacy and safety of bendamustine and rituximab in the treatment of indolent and mantle cell lymphomas in older patients. J Clin Oncol. 2008;26:8572.
Flowers C, Ou F-S, Shi Q, Hoster E, Peterson BA, Hochster HS, et al. Outcomes for Elderly Patients (pts) with Follicular Lymphoma (FL) Using Individual Patient Data (IPD) from 5922 Pts in 18 Randomized Controlled Trials (RCTs): a Follicular Lymphoma Analysis of Surrogate Hypothesis (FLASH) Group Study. Blood. 2016;128. http://www.bloodjournal.org/content/128/22/1102 (accessed 17 Jul 2019).
Dreyling M, Ghielmini M, Rule S, Salles G, Vitolo U, Ladetto M. Newly diagnosed and relapsed follicular lymphoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017;28:3109.
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;377:42-51.
Cheah CY, Nastoupil LJ, McLaughlin P, Fanale MA, Neelapu SS, Fayad LE, et al. Premature closure of a phase II study of bendamustine, mitoxantrone and rituximab for patients with untreated high-risk follicular lymphoma due to severe haematological and infectious toxicity. Br J Haematol. 2016;175:531-3.
Marcus R, Davies A, Ando K, Klapper W, Opat S, Owen C, et al. Obinutuzumab for the first-line treatment of follicular lymphoma. N Engl J Med. 2017;377:1331-44.
Gyan E, Sonet A, Brice P, Anglaret B, Laribi K, Fruchart C, et al. Bendamustine and rituximab in elderly patients with low-tumour burden follicular lymphoma. Results of the LYSA phase II BRIEF study. Br J Haematol. 2018;183:76-86.
Pott C, Belada D, Danesi N, Fingerle-Rowson G, Gribben J, Harbron C, et al. Analysis of minimal residual disease in follicular lymphoma patients in Gadolin, a phase III study of obinutuzumab plus bendamustine versus bendamustine in relapsed/refractory indolent non-Hodgkin lymphoma. Blood. 2015;126: 3978.
Pott C, Hoster E, Kehden B, Unterhalt M, Herold M, van der Jagt RH, et al. Minimal residual disease in patients with follicular lymphoma treated with obinutuzumab or rituximab as first-line induction immunochemotherapy and maintenance in the phase 3 GALLIUM study. Blood. 2016;128:613.
Zohren F, Bruns I, Pechtel S, Schroeder T, Fenk R, Czibere A, et al. Prognostic value of circulating Bcl-2/IgH levels in patients with follicular lymphoma receiving first-line immunochemotherapy. Blood. 2015;126:1407-14.
Morschhauser F, Fowler NH, Feugier P, Bouabdallah R, Tilly H, Palomba ML, et al. Rituximab plus lenalidomide in advanced untreated follicular lymphoma. N Engl J Med. 2018;379:934-47.

Auteurs

Carola Boccomini (C)

SC Ematologia AOU Città della Salute e della Scienza di Torino, Torino, Italy.

Marco Ladetto (M)

SC Ematologia Azienda Ospedaliera Santi Antonio e Biagio e Cesare Arrigo, Alessandria, Italy.

Luigi Rigacci (L)

UOC Ematologia e Trapianto Cellule Staminali, AO San Camillo Forlanini, Roma, Italy.
Hematology Department, Universisty of Florence and AOU Careggi, Firenze, Italy.

Benedetta Puccini (B)

Hematology Department, Universisty of Florence and AOU Careggi, Firenze, Italy.

Sara Rattotti (S)

Division of Hematology, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.

Stefano Volpetti (S)

Clinica Ematologia e Trapianto Midollo osseo, AOU Santa Maria della Misericordia, Udine, Italy.

Simone Ferrero (S)

Department of Molecular Biotechnologies and Health Sciences, Division of Hematology, University of Torino/Hematology 1, AOU "Città della Salute e della Scienza di Torino", Torino, Italy.

Annalisa Chiarenza (A)

Ematologia e Trapianto di Midollo Osseo, AOU Policlinico Vittorio Emanuele, PO Ferrarotto Alessi, Catania, Italy.

Roberto Freilone (R)

SSD Ematologia ASLTO4, Ivrea, Italy.

Mattia Novo (M)

Multidisciplinary Oncology Outpatient Clinic, Candiolo Cancer Institute, FPO-IRCCS, Candiolo (Torino), Italy.

Paolo Corradini (P)

Division of Hematology and Stem Cell Transplantation Fondazione, IRCCS Istituto Nazionale dei Tumori, Milano, Italy.

Luca Nassi (L)

Hematology, AOU Maggiore della Carità and University of Eastern Piedmont, Novara, Italy.

Chiara Rusconi (C)

Division of Hematology and Stem Cell Transplantation Fondazione, IRCCS Istituto Nazionale dei Tumori, Milano, Italy.
SC Ematologia, ASST Grande Ospedale Metropolitano Niguarda, Milano, Italy.

Caterina Stelitano (C)

UOC Ematologia, Grande Ospedale Metropolitano Bianchi-Melacrino-Morelli, Reggio Calabria, Italy.

Silvia Bolis (S)

SC Ematologia ASST-Monza, Monza, Italy.

Anna Marina Liberati (A)

Università del Studi di Perugia e Ospedale di Terni, Terni, Italy.

Alessandra Tucci (A)

SC Ematologia, ASST-Spedali Civili, Brescia, Italy.

Luca Baldini (L)

UOC Ematologia Fondazione IRCCS Cà Granda, Ospedale Maggiore Policlinico, Università degli Studi, Milano, Italy.

Monica Balzarotti (M)

UO Ematologia, Humanitas Clinical and Research Center - IRCCS, Rozzano (Milano), Italy.

Andrea Evangelista (A)

Unit of Clinical Epidemiology, CPO Piemonte, AOU Città della Salute e della Scienza di Torino, Torino, Italy.

Giovannino Ciccone (G)

Unit of Clinical Epidemiology, CPO Piemonte, AOU Città della Salute e della Scienza di Torino, Torino, Italy.

Umberto Vitolo (U)

SC Ematologia AOU Città della Salute e della Scienza di Torino, Torino, Italy.

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