R-CHOP treatment for patients with advanced follicular lymphoma: Over 15-year follow-up of JCOG0203.
R-CHOP
follicular lymphoma
histological transformation
long term
secondary malignancies
Journal
British journal of haematology
ISSN: 1365-2141
Titre abrégé: Br J Haematol
Pays: England
ID NLM: 0372544
Informations de publication
Date de publication:
23 Nov 2023
23 Nov 2023
Historique:
revised:
07
11
2023
received:
01
09
2023
accepted:
08
11
2023
medline:
24
11
2023
pubmed:
24
11
2023
entrez:
24
11
2023
Statut:
aheadofprint
Résumé
Anti-CD20 antibody in combination with chemotherapy extends overall survival (OS) in untreated advanced-stage follicular lymphoma (FL), yet the optimal associated therapy is unclear. Data on the cumulative incidence of secondary malignancies postrelapse after conventional immunochemotherapy are scarce. A long-term analysis of rituximab combined with cyclophosphamide, doxorubicin, vincristine and prednisone (R-CHOP) as first-line treatment was conducted in a randomised clinical trial. A six-cycle R-CHOP regimen was administered every 2 or 3 weeks without rituximab maintenance. A prespecified evaluation was conducted 15 years after the completion of enrolment, following initial analysis results that showed no significant differences in outcomes at the 3-year mark. In-depth analyses were performed on the cohort of 248 patients with FL who were allocated to the two treatment arms. With a median follow-up period of 15.9 years, the 15-year OS was 76.2%. There were no protocol treatment-related deaths, nor were there any fatal infections attributable to subsequent lymphoma treatment. At 15 years, the cumulative incidence of non-haematological and haematological malignancies was 12.8% and 3.7% respectively. Histological transformation appeared after a median of 8 years. R-CHOP maintains safety and efficacy in patients with advanced FL over extended follow-up, making it a viable first-line option for patients with advanced-stage FL.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Clinical Cancer Research
ID : 2000-6
Organisme : Grants-In-Aid for Cancer Research from the Ministry of Health, Labour and Welfare of Japan
ID : 11S-1
Organisme : Grants-In-Aid for Cancer Research from the Ministry of Health, Labour and Welfare of Japan
ID : 11S-4
Organisme : Grants-In-Aid for Cancer Research from the Ministry of Health, Labour and Welfare of Japan
ID : 14S-1
Organisme : Grants-In-Aid for Cancer Research from the Ministry of Health, Labour and Welfare of Japan
ID : 14S-4
Organisme : Grants-In-Aid for Cancer Research from the Ministry of Health, Labour and Welfare of Japan
ID : 17S-1
Organisme : Grants-In-Aid for Cancer Research from the Ministry of Health, Labour and Welfare of Japan
ID : 17S-5
Organisme : Grants-In-Aid for Cancer Research from the Ministry of Health, Labour and Welfare of Japan
ID : 20S-1
Organisme : Grants-In-Aid for Cancer Research from the Ministry of Health, Labour and Welfare of Japan
ID : 20S-6
Organisme : National Cancer Center Research and Development Fund
ID : 23-A-17
Organisme : National Cancer Center Research and Development Fund
ID : 26-A-4
Organisme : National Cancer Center Research and Development Fund
ID : 2020-J-3
Organisme : National Cancer Center Research and Development Fund
ID : 23-A-16
Organisme : National Cancer Center Research and Development Fund
ID : 29-A-3
Informations de copyright
© 2023 The Authors. British Journal of Haematology published by British Society for Haematology and John Wiley & Sons Ltd.
Références
Ekstrom-Smedby K. Epidemiology and etiology of non-Hodgkin lymphoma-a review. Acta Oncol. 2006;45(3):258-271.
Teras LR, DeSantis CE, Cerhan JR, Morton LM, Jemal A, Flowers CR. 2016 US lymphoid malignancy statistics by World Health Organization subtypes. CA Cancer J Clin. 2016;66(6):443-459.
Ardeshna KM, Smith P, Norton A, Hancock BW, Hoskin PJ, MacLennan KA, 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.
Ardeshna KM, Qian W, Smith P, Braganca N, Lowry L, Patrick 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.
Nastoupil LJ, Sinha R, Byrtek M, Ziemiecki R, Zhou X, Taylor M, et al. Outcomes following watchful waiting for stage II-IV follicular lymphoma patients in the modern era. Br J Haematol. 2016;172(5):724-734.
Friedberg JW. Potential long-term toxicities should influence the choice of therapy for indolent non-Hodgkin's lymphoma. Haematologica. 2006;91(11):1453-1455.
Friedberg JW. Secondary malignancies after therapy of indolent non-Hodgkin's lymphoma. Haematologica. 2008;93(3):336-338.
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: results of a prospective randomized study of the German Low-Grade Lymphoma Study Group. Blood. 2005;106(12):3725-3732.
Marcus R, Imrie K, Solal-Céligny P, Catalano JV, Dmoszynska A, Raposo JC, 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.
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(12):1506-1513.
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(7):689-696.
Sorigue M, Sancho JM. Recent landmark studies in follicular lymphoma. Blood Rev. 2019;35:68-80.
Freedman A, Jacobsen E. Follicular lymphoma: 2020 update on diagnosis and management. Am J Hematol. 2020;95(3):316-327.
McNamara C, Montoto S, Eyre TA, Ardeshna K, Burton C, Illidge T, et al. The investigation and management of follicular lymphoma. Br J Haematol. 2020;191(3):363-381.
Batlevi CL, Sha F, Alperovich A, Ni A, Smith K, Ying Z, et al. Follicular lymphoma in the modern era: survival, treatment outcomes, and identification of high-risk subgroups. Blood Cancer J. 2020;10(7):74.
Rummel MJ, Niederle N, Maschmeyer G, Banat GA, von Grunhagen 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. 2013;381(9873):1203-1210.
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):42-51.
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(27):3351-3359.
Nastoupil LJ, Sinha R, Byrtek M, Zhou X, Taylor MD, Friedberg JW, et al. The use and effectiveness of rituximab maintenance in patients with follicular lymphoma diagnosed between 2004 and 2007 in the United States. Cancer. 2014;120(12):1830-1837.
Bachy E, Seymour JF, Feugier P, Offner F, López-Guillermo A, Belada D, et al. Sustained progression-free survival benefit of rituximab maintenance in patients with follicular lymphoma: long-term results of the PRIMA study. J Clin Oncol. 2019;37(31):2815-2824.
Hirt C, Hoster E, Unterhalt M, Hanel M, Prange-Krex G, Forstpointner R, et al. Rituximab maintenance versus observation after immunochemotherapy (R-CHOP, R-MCP, and R-FCM) in untreated follicular lymphoma patients: a randomized trial of the Ostdeutsche Studiengruppe Hamatologie und Onkologie and the German Low-Grade Lymphoma Study Group. HemaSphere. 2021;5(7):e600.
Vidal L, Gafter-Gvili A, Leibovici L, Dreyling M, Ghielmini M, Hsu Schmitz SF, et al. Rituximab maintenance for the treatment of patients with follicular lymphoma: systematic review and meta-analysis of randomized trials. J Natl Cancer Inst. 2009;101(4):248-255.
Hiddemann W, Barbui AM, Canales MA, Cannell PK, Collins GP, Durig J, et al. Immunochemotherapy with obinutuzumab or rituximab for previously untreated follicular lymphoma in the GALLIUM study: influence of chemotherapy on efficacy and safety. J Clin Oncol. 2018;36(23):2395-2404.
Montoto S, Davies AJ, Matthews J, Calaminici M, Norton AJ, Amess J, et al. Risk and clinical implications of transformation of follicular lymphoma to diffuse large B-cell lymphoma. J Clin Oncol. 2007;25(17):2426-2433.
Al-Tourah AJ, Gill KK, Chhanabhai M, Hoskins PJ, Klasa RJ, Savage KJ, et al. Population-based analysis of incidence and outcome of transformed non-Hodgkin's lymphoma. J Clin Oncol. 2008;26(32):5165-5169.
Link BK, Maurer MJ, Nowakowski GS, Ansell SM, Macon WR, Syrbu SI, et al. Rates and outcomes of follicular lymphoma transformation in the immunochemotherapy era: a report from the University of Iowa/MayoClinic Specialized Program of Research Excellence Molecular Epidemiology Resource. J Clin Oncol. 2013;31(26):3272-3278.
Wagner-Johnston ND, Link BK, Byrtek M, Dawson KL, Hainsworth J, Flowers CR, et al. Outcomes of transformed follicular lymphoma in the modern era: a report from the National LymphoCare Study (NLCS). Blood. 2015;126(7):851-857.
Federico M, Caballero Barrigón MD, Marcheselli L, Tarantino V, Manni M, Sarcozy C, et al. Rituximab and the risk of transformation of follicular lymphoma: a retrospective pooled analysis. Lancet Haematol. 2018;5(8):e359-e367.
Alonso-Alvarez S, Magnano L, Alcoceba M, Andrade-Campos M, Espinosa-Lara N, Rodriguez G, et al. Risk of, and survival following, histological transformation in follicular lymphoma in the rituximab era. A retrospective multicentre study by the Spanish GELTAMO Group. Br J Haematol. 2017;178(5):699-708.
Conconi A, Ponzio C, Lobetti-Bodoni C, Motta M, Rancoita PM, Stathis A, et al. Incidence, risk factors and outcome of histological transformation in follicular lymphoma. Br J Haematol. 2012;157(2):188-196.
Sarkozy C, Trneny M, Xerri L, Wickham N, Feugier P, Leppa S, et al. Risk factors and outcomes for patients with follicular lymphoma who had histologic transformation after response to first-line immunochemotherapy in the PRIMA trial. J Clin Oncol. 2016;34(22):2575-2582.
Janikova A, Bortlicek Z, Campr V, Kopalova N, Benesova K, Hamouzova M, et al. The incidence of biopsy-proven transformation in follicular lymphoma in the rituximab era. A retrospective analysis from the Czech Lymphoma Study Group (CLSG) database. Ann Hematol. 2018;97(4):669-678.
Schöder H, Noy A, Gönen M, Weng L, Green D, Erdi YE, et al. Intensity of 18fluoro-deoxyglucose uptake in positron emission tomography distinguishes between indolent and aggressive non-Hodgkin lymphoma. J Clin Oncol. 2005;23(21):4643-4651.
Noy A, Schoder H, Gonen M, Weissler M, Ertelt K, Cohler C, et al. The majority of transformed lymphomas have high standardized uptake values (SUVs) on positron emission tomography (PET) scanning similar to diffuse large B-cell lymphoma (DLBCL). Ann Oncol. 2009;20(3):508-512.
Casulo C, Burack WR, Friedberg JW. Transformed follicular non-Hodgkin lymphoma. Blood. 2015;125(1):40-47.
Papajík T, Mysliveček M, Sedová Z, Buriánoková E, Procházke V, Koranda P, et al. Standardised uptake value of 18F-FDG on staging PET/CT in newly diagnosed patients with different sutypes of non-Hodgkin's lymphoma. Eur J Haematol. 2011;86(1):32-37.
Alobthani G, Romanov V, Isohashi K, Matsunaga K, Watabe T, Kato H, et al. Value of 18F-FDG PET/CT in discrimination between indolent and aggressive non-Hodgkin's lymphoma: a study of 328 patuients. Hell J Nucl Med. 2018;21(1):7-14.
Watanabe T, Tobinai K, Shibata T, Tsukasaki K, Morishima Y, Maseki N, et al. Phase II/III study of R-CHOP-21 versus R-CHOP-14 for untreated indolent B-cell non-Hodgkin's lymphoma: JCOG 0203 trial. J Clin Oncol. 2011;29(30):3990-3998.
Hernandez-Ilizaliturri FJ, Jupudy V, Ostberg J, Oflazoglu E, Huberman A, Repasky E, et al. Neutrophils contribute to the biological antitumor activity of rituximab in a non-Hodgkin's lymphoma severe combined immunodeficiency mouse model. Clin Cancer Res. 2003;9:5866-5873.
Cartron G, Zhao-Yang L, Baudard M, Kanouni T, Rouille V, Quittet P, et al. Granulocyte-macrophage colony-stimulating factor potentiates rituximab in patients with relapsed follicular lymphoma: results of a phase II study. J Clin Oncol. 2008;26(16):2725-2731.
Watanabe T, Tobinai K, Wakabayashi M, Morishima Y, Kobayashi H, Kinoshita T, et al. Outcomes after R-CHOP in patients with newly diagnosed advanced follicular lymphoma: a 10-year follow-up analysis of the JCOG0203 trial. Lancet Haematol. 2018;5(11):e520-e531.
Méndez M, Torrente M, Sánchez-Beato M, González-Rincón J, Royuela A, Gómez-Codina J, et al. Transformed follicular lymphoma in the rituximab era: a report from the Spanish Lymphoma Oncology Group. Hematol Oncol. 2019;37(2):143-150.
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. J Clin Oncol. 2015;33(23):2516-2522.
Jurinovic V, Kridel R, Staiger AM, Szczepanowski M, Horn H, Dreyling MH, et al. Clinicogenetic risk models predict early progression of follicular lymphoma after first-line immunochemotherapy. Blood. 2016;128(8):1112-1120.
Freeman CL, Kridel R, Moccia AA, Savage KJ, Villa DR, Scott DW, et al. Early progression after bendamustine-rituximab is associated with high risk of transformation in advanced stage follicular lymphoma. Blood. 2019;134(9):761-764.
Jaffe ES, World Health Organization. Pathology and genetics of tumours of haematopoietic and lymphoid tissues. 3rd ed. Lyon, Oxford: IARC Press, Oxford University Press (distributor); 2001. p. 351.
Pirani M, Marcheselli R, Marcheselli L, Bari M, Federico M, Sacchi S. Risk for second malignancies in non-Hodgkin's lymphoma survivors: a meta-analysis. Ann Oncol. 2011;22(8):1845-1858.
Sorigue M, Prusila REI, Jauhiainen J, Mercadal S, Postila A, Salmi P, et al. Incidence of solid cancer in patients with follicular lymphoma. Acta Oncol. 2019;58(11):1564-1569.
Flinn IW, van der Jagt R, Kahl B, Wood P, Hawkins T, MacDonald D, et al. First-line treatment of patients with indolent non-Hodgkin lymphoma or mantle-cell lymphoma with bendamustine plus rituximab versus R-CHOP or R-CVP: results of the BRIGHT 5-year follow-up study. J Clin Oncol. 2019;37(12):984-991.
Magnano L, Montoto S, González-Barca E, Briones J, Sancho JM, Muntanola 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(4):639-646.
Lyman GH, Yau L, Nakov R, Krendyukov A. Overall survival and risk of second malignancies with cancer chemotherapy and G-CSF support. Ann Oncol. 2018;29(9):1903-1910.
Mozas P, Nadeu F, Rivas-Delgado A, Rivero A, Garrote M, Balahue O, et al. Patterns of change in treatment, response, and outcome in patients with follicular lymphoma over the last four decades: a single-center experience. Blood Cancer J. 2020;10(3):31.
Leonard RCF, Hayward RL, Prescott RJ, Wang J-X. The identification of discrete prognostic groups in low-grade non-Hodgkin's lymphoma: the Scotland and Newcastle Lymphoma Group Therapy Working Party. Ann Oncol. 1991;2:655-662.
Romaguera JE, McLaughlin P, North L, Dixon D, Silvermintz KB, Garnsey LA, et al. Multivariate analysis of prognostic factors in stage IV follicular low-grade lymphoma: a risk model. J Clin Oncol. 1991;9(5):762-769.
Dana BW, Dahlberg S, Nathwani B, Chase E, Coltman C, Miller TP, et al. Long-term follow-up of patients with low-grade malignant lymphomas treated with doxorubicin-based chemothrapy or chemoimmunothrapy. J Clin Oncol. 1993;11(4):644-651.
Federico M, Vitolo U, Zinzani PL, Chisesi T, Cló V, Bellesi G, et al. Prognosis of follicular lymphoma: a predictive model based on a retrospective analysis of 987 cases. Blood. 2000;95:783-789.
Nabhan C, Aschebrook-Kilfoy B, Chiu BC-H, Kruczek K, Smith SM, Evens AM. The impact of race, age, and sex in follicular lymphoma: a comprehensive SEER analysis across consecutive treatment eras. Am J Haematol. 2014;89(6):633-638.
Nabhan C, Byrtek M, Rai A, Dawson K, Zhou X, Link BK, et al. Disease characteristics, treatment patterns, prognosis, outcomes and lymphoma-related mortality in elderly follicular lymphoma in the United States. Br J Haematol. 2015;170:85-95.
Decaudin D, Lepage E, Brousse N, Brice P, Harousseau JL, Belhadj K, et al. Low-grade stage III-IV follicular lymphoma: multivariable analysis of prognostic factors in 484 patients: a study of the Groupe d'Etude des Lymphomes de l'Adulte. J Clin Oncol. 1999;17:2499-2505.
Mozas P, Rivero A, Rivas-Delgado A, Nadeu F, Correa JG, Castillo C, et al. Age and comorbidity are determinig factors in the overall and relative survival of patients with follicular lymphma. Ann Hematol. 2021;100:1231-1239.
Solal-Céligny P, Roy P, Colombat P, White J, Armitage JO, Arranz-Saez R, et al. Follicular lymphoma international prognostic index. Blood. 2004;104(5):1258-1265.