Clinical outcomes of ruxolitinib treatment in 595 intermediate-1 risk patients with myelofibrosis: The RUX-MF Real-World Study.

DIPSS score JAK2 mutation intermediate‐1 myelofibrosis ruxolitinib

Journal

Cancer
ISSN: 1097-0142
Titre abrégé: Cancer
Pays: United States
ID NLM: 0374236

Informations de publication

Date de publication:
30 Jul 2024
Historique:
revised: 24 05 2024
received: 19 04 2024
accepted: 14 06 2024
medline: 30 7 2024
pubmed: 30 7 2024
entrez: 30 7 2024
Statut: aheadofprint

Résumé

Ruxolitinib (RUX) is a JAK1/2 inhibitor approved for the therapy of myelofibrosis (MF) based on clinical trials including only intermediate2-high risk (INT2/HIGH) patients. However, RUX is commonly used in intermediate-1 (INT1) patients, with scarce information on responses and outcome. The authors investigated the benefit of RUX in 1055 MF patients, included in the "RUX-MF" retrospective study. At baseline (BL), 595 (56.2%) patients were at INT1-risk according to DIPSS (PMF) or MYSEC-PM (SMF). The spleen was palpable at <5 cm, between 5 and 10 cm, and >10 cm below costal margin in 5.9%, 47.4%, and 39.7% of patients, respectively; 300 (54.1%) were highly symptomatic (total symptom score ≥20). High-molecular-risk (HMR) mutations (IDH1/2, ASXL-1, SRSF2, EZH2, U2AF1 In INT1 patients, responses were more frequent and durable, whereas toxicity rates were lower compared to INT2/high-risk patients. Presence of HMR mutations, cytopenia, and peripheral blasts identified less-responsive INT1 patients, who may benefit for alternative therapeutic strategies.

Sections du résumé

BACKGROUND BACKGROUND
Ruxolitinib (RUX) is a JAK1/2 inhibitor approved for the therapy of myelofibrosis (MF) based on clinical trials including only intermediate2-high risk (INT2/HIGH) patients. However, RUX is commonly used in intermediate-1 (INT1) patients, with scarce information on responses and outcome.
METHODS METHODS
The authors investigated the benefit of RUX in 1055 MF patients, included in the "RUX-MF" retrospective study.
RESULTS RESULTS
At baseline (BL), 595 (56.2%) patients were at INT1-risk according to DIPSS (PMF) or MYSEC-PM (SMF). The spleen was palpable at <5 cm, between 5 and 10 cm, and >10 cm below costal margin in 5.9%, 47.4%, and 39.7% of patients, respectively; 300 (54.1%) were highly symptomatic (total symptom score ≥20). High-molecular-risk (HMR) mutations (IDH1/2, ASXL-1, SRSF2, EZH2, U2AF1
CONCLUSIONS CONCLUSIONS
In INT1 patients, responses were more frequent and durable, whereas toxicity rates were lower compared to INT2/high-risk patients. Presence of HMR mutations, cytopenia, and peripheral blasts identified less-responsive INT1 patients, who may benefit for alternative therapeutic strategies.

Identifiants

pubmed: 39078647
doi: 10.1002/cncr.35489
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Ministero della Salute
ID : RC-2024-2790083

Informations de copyright

© 2024 The Author(s). Cancer published by Wiley Periodicals LLC on behalf of American Cancer Society.

Références

Harrison CN, Kiladjian JJ, Koschmieder S, Passamonti F. Myelofibrosis: current unmet needs, emerging treatments, and future perspectives. Cancer. 2024;130(12):2091‐2097. doi:10.1002/cncr.35244
Passamonti F, Mora B. Myelofibrosis. Blood. 2023;141(16):1954‐1970. doi:10.1182/blood.2022017423
Guglielmelli P, Lasho TL, Rotunno G, et al. MIPSS70: Mutation‐Enhanced International Prognostic Score System for transplantation‐age patients with primary myelofibrosis. J Clin Oncol. 2018;36(4):310‐318. doi:10.1200/jco.2017.76.4886
Cervantes F, Dupriez B, Pereira A, et al. New prognostic scoring system for primary myelofibrosis based on a study of the International Working Group for Myelofibrosis Research and Treatment. Blood. 2009;113(13):2895‐2901. doi:10.1182/blood‐2008‐07‐170449
Passamonti F, Cervantes F, Vannucchi AM, et al. A dynamic prognostic model to predict survival in primary myelofibrosis: a study by the IWG‐MRT (International Working Group for Myeloproliferative Neoplasms Research and Treatment). Blood. 2010;115(9):1703‐1708. doi:10.1182/blood‐2009‐09‐245837
Passamonti F, Giorgino T, Mora B, et al. A clinical‐molecular prognostic model to predict survival in patients with post polycythemia vera and post essential thrombocythemia myelofibrosis. Leukemia. 2017;31(12):2726‐2731. 2017 31:12. doi:10.1038/leu.2017.169
Verstovsek S, Gotlib J, Mesa RA, et al. Long‐term survival in patients treated with ruxolitinib for myelofibrosis: COMFORT‐I and ‐II pooled analyses. J Hematol Oncol. 2017;10(1):156. doi:10.1186/s13045‐017‐0527‐7
Harrison CN, Vannucchi AM, Kiladjian JJ, et al. Long‐term findings from COMFORT‐II, a phase 3 study of ruxolitinib vs best available therapy for myelofibrosis. Leukemia. 2016;30(8):1701‐1707. doi:10.1038/leu.2016.148
Verstovsek S, Mesa RA, Gotlib J, et al. Long‐term treatment with ruxolitinib for patients with myelofibrosis: 5‐year update from the randomized, double‐blind, placebo‐controlled, phase 3 COMFORT‐I trial. J Hematol Oncol. 2017;10(1):1‐14. doi:10.1186/s13045‐017‐0417‐z
Passamonti F, Gupta V, Martino B, et al. Comparing the safety and efficacy of ruxolitinib in patients with Dynamic International Prognostic Scoring System low‐intermediate‐1‐intermediate‐2‐and high‐risk myelofibrosis in JUMP, a phase 3b, expanded‐access study. Hematol Oncol. 2021;39(4):558‐566. doi:10.1002/hon.2898
Gupta V, Griesshammer M, Martino B, et al. Analysis of predictors of response to ruxolitinib in patients with myelofibrosis in the phase 3b expanded‐access JUMP study. Leuk Lymphoma. 2021;62(4):918‐926. doi:10.1080/10428194.2020.1845334
Mead AJ, Milojkovic D, Knapper S, et al. Response to ruxolitinib in patients with intermediate‐1‐intermediate‐2‐and high‐risk myelofibrosis: results of the UK ROBUST Trial. Br J Haematol. 2015;170(1):29‐39. doi:10.1111/bjh.13379
Palandri F, Tiribelli M, Benevolo G, et al. Efficacy and safety of ruxolitinib in intermediate‐1 IPSS risk myelofibrosis patients: results from an independent study. Hematol Oncol. 2018;36(1):285‐290. doi:10.1002/hon.2429
Palandri F, Palumbo GA, Benevolo G, et al. Incidence of blast phase in myelofibrosis patients according to anemia severity at ruxolitinib start and during therapy. Cancer. 2024;130(8):1270‐1280. doi:10.1002/cncr.35156
Arber DA, Orazi A, Hasserjian RP, et al. International Consensus Classification of Myeloid Neoplasms and Acute Leukemias: integrating morphologic, clinical, and genomic data. Blood. 2022;140(11):1200‐1228. doi:10.1182/blood.2022015850
Tefferi A, Cervantes F, Mesa R, et al. Revised response criteria for myelofibrosis: International Working Group‐Myeloproliferative Neoplasms Research and Treatment (IWG‐MRT) and European LeukemiaNet (ELN) consensus report. Blood. 2013;122(8):1395‐1398. doi:10.1182/blood‐2013‐03‐488098
Gangat N, Caramazza D, Vaidya R, et al. DIPSS plus: a refined Dynamic International Prognostic Scoring System for primary myelofibrosis that incorporates prognostic information from karyotype, platelet count, and transfusion status. J Clin Oncol. 2011;29(4):392‐397. doi:10.1200/jco.2010.32.2446
Thiele J, Kvasnicka HM, Facchetti F, Franco V, van der Walt J, Orazi A. European consensus on grading bone marrow fibrosis and assessment of cellularity. Haematologica. 2005;90(8):1128‐1132.
Barbui T, Thiele J, Gisslinger H, et al. The 2016 WHO classification and diagnostic criteria for myeloproliferative neoplasms: document summary and in‐depth discussion. Blood Cancer J. 2018;8(2):15. doi:10.1038/s41408‐018‐0054‐y
Emanuel RM, Dueck AC, Geyer HL, et al. Myeloproliferative neoplasm (MPN) symptom assessment form total symptom score: prospective international assessment of an abbreviated symptom burden scoring system among patients with MPNs. J Clin Oncol. 2012;30(33):4098‐4103. doi:10.1200/jco.2012.42.3863
Tefferi A, Guglielmelli P, Lasho TL, et al. MIPSS70+ Version 2.0: Mutation and Karyotype‐Enhanced International Prognostic Scoring System for Primary Myelofibrosis. J Clin Oncol. 2018;36(17):1769‐1770. doi:10.1200/jco.2018.78.9867
National Cancer Institute. Common Terminology Criteria for Adverse Events (CTCAE) v5.0. 2017. Available from: https://www.meddra.org/
Tefferi A, Cervantes F, Mesa R, et al. Revised response criteria for myelofibrosis: International Working Group‐Myeloproliferative Neoplasms Research and Treatment (IWG‐MRT) and European LeukemiaNet (ELN) consensus report. Blood. 2013;122(8):1395‐1398. doi:10.1182/blood‐2013‐03‐488098
Verstovsek S, Mesa RA, Gotlib J, et al. A double‐blind, placebo‐controlled trial of ruxolitinib for myelofibrosis. N Engl J Med. 2012;366(9):799‐807. doi:10.1056/nejmoa1110557
Investigators On Behalf Of The Ci, Cervantes F, Vannucchi AM, Kiladjian JJ, et al. Three‐year efficacy, safety, and survival findings from COMFORT‐II, a phase 3 study comparing ruxolitinib with best available therapy for myelofibrosis. Blood. 2013;122(25):4047‐4053. doi:10.1182/blood‐2013‐02‐485888
Al‐Ali HK, Griesshammer M, Foltz L, et al. Primary analysis of JUMP, a phase 3b, expanded‐access study evaluating the safety and efficacy of ruxolitinib in patients with myelofibrosis, including those with low platelet counts. Br J Haematol. 2020;189(5):888‐903. doi:10.1111/bjh.16462
Davis KL, Côté I, Kaye JA, Mendelson E, Gao H, Perez RJ. Real‐world assessment of clinical outcomes in patients with lower‐risk myelofibrosis receiving treatment with ruxolitinib. Adv Hematol. Epub. 2015;2015:1‐9. doi:10.1155/2015/848473
Mazza P, Specchia G, Di Renzo N, et al. Ruxolitinib ‐ better prognostic impact in low‐intermediate 1 risk score: evaluation of the “rete ematologica pugliese” (REP) in primary and secondary myelofibrosis. Leuk Lymphoma. 2017;58(1):138‐144. doi:10.1080/10428194.2016.1189547
Palandri F, Palumbo GA, Bonifacio M, et al. Baseline factors associated with response to ruxolitinib: an independent study on 408 patients with myelofibrosis. Oncotarget. 2017;8(45):79073‐79086. doi:10.18632/oncotarget.18674
Mesa RA, Kiladjian JJ, Catalano JV, et al. SIMPLIFY‐1: a phase III randomized trial of momelotinib versus ruxolitinib in Janus kinase inhibitor‐naïve patients with myelofibrosis. J Clin Oncol. 2017;35(34):3844‐3850. doi:10.1200/jco.2017.73.4418
Harrison CN, Vannucchi AM, Platzbecker U, et al. Momelotinib versus best available therapy in patients with myelofibrosis previously treated with ruxolitinib (SIMPLIFY 2): a randomised, open‐label, phase 3 trial. Lancet Haematol. 2018;5(2):e73‐e81. doi:10.1016/s2352‐3026(17)30237‐5
Verstovsek S, Kantarjian H, Mesa RA, et al. Safety and efficacy of INCB018424, a JAK1 and JAK2 inhibitor, in myelofibrosis. N Engl J Med. 2010;363(12):1117‐1127. doi:10.1056/nejmoa1002028
Elli EM, Baratè C, Mendicino F, Palandri F, Palumbo GA. Mechanisms underlying the anti‐inflammatory and immunosuppressive activity of ruxolitinib. Front Oncol. 2019;9. doi:10.3389/fonc.2019.01186
Polverelli N, Palumbo GA, Binotto G, et al. Epidemiology, outcome, and risk factors for infectious complications in myelofibrosis patients receiving ruxolitinib: a multicenter study on 446 patients. Hematol Oncol. 2018;36(3):561‐569. doi:10.1002/hon.2509
Mora B, Maffioli M, Rumi E, et al. Incidence of blast phase in myelofibrosis according to anemia severity. EJHaem. 2023;4(3):679‐689. doi:10.1002/jha2.745
Palandri F, Breccia M, Bonifacio M, et al. Life after ruxolitinib: reasons for discontinuation, impact of disease phase, and outcomes in 218 patients with myelofibrosis. Cancer. 2020;126(6):1243‐1252. doi:10.1002/cncr.32664
Kuykendall AT, Shah S, Talati C, et al. Between a rux and a hard place: evaluating salvage treatment and outcomes in myelofibrosis after ruxolitinib discontinuation. Ann Hematol. 2018;97(3):435‐441. doi:10.1007/s00277‐017‐3194‐4
Newberry KJ, Patel K, Masarova L, et al. Clonal evolution and outcomes in myelofibrosis after ruxolitinib discontinuation. Blood. 2017;130(9):1125‐1131. doi:10.1182/blood‐2017‐05‐783225
Kröger N, Bacigalupo A, Barbui T, et al. Indication and management of allogeneic haematopoietic stem‐cell transplantation in myelofibrosis: updated recommendations by the EBMT/ELN International Working Group. Lancet Haematol. 2024;11(1):e62‐e74. doi:10.1016/s2352‐3026(23)00305‐8
Palandri F, Breccia M, Mazzoni C, et al. Ruxolitinib in cytopenic myelofibrosis: response, toxicity, drug discontinuation, and outcome. Cancer. 2023;129(11):1704‐1713. doi:10.1002/cncr.34722
Palandri F, Al‐Ali HK, Guglielmelli P, Zuurman MW, Sarkar R, Gupta V. Benefit of early ruxolitinib initiation regardless of fibrosis grade in patients with primary myelofibrosis: a post hoc analysis of the single‐arm phase 3b JUMP Study. Cancers. 2023;15(10):2859. doi:10.3390/cancers15102859

Auteurs

Francesca Palandri (F)

IRCCS Azienda Ospedaliero-Universitaria di Bologna, Istituto di Ematologia "Seràgnoli", Bologna, Italy.

Elena M Elli (EM)

Fondazione IRCCS San Gerardo dei Tintori, divisione di ematologia e unità trapianto di midollo, Monza, Italy.

Erika Morsia (E)

Hematology Unit, Department of Clinical and Molecular Sciences, DISCLIMO, Università Politecnica delle Marche, Ancona, Italy.

Giulia Benevolo (G)

University Hematology Division, Città della Salute e della Scienza Hospital, Torino, Italy.

Mario Tiribelli (M)

Division of Hematology and BMT, Department of Medicine, University of Udine, Udine, Italy.

Eloise Beggiato (E)

Unit of Hematology, Department of Oncology, University of Torino, Torino, Italy.

Massimiliano Bonifacio (M)

Department of Engineering for Innovation Medicine, Section of Innovation Biomedicine, Hematology Area, University of Verona, Verona, Italy.

Mirko Farina (M)

Unit of Blood Diseases and Stem Cells Transplantation, Department of Clinical and Experimental Sciences, University of Brescia, ASST Spedali Civili of Brescia, Brescia, Italy.

Bruno Martino (B)

Division of Hematology, Azienda Ospedaliera 'Bianchi Melacrino Morelli', Reggio Calabria, Italy.

Giovanni Caocci (G)

Ematologia, Ospedale Businco, Università degli studi di Cagliari, Cagliari, Italy.

Novella Pugliese (N)

Department of Clinical Medicine and Surgery, Federico II University Medical School, Naples, Italy.

Alessia Tieghi (A)

Department of Hematology, Azienda USL - IRCCS di Reggio Emilia, Reggio Emilia, Italy.

Monica Crugnola (M)

Haematology and BMT Centre, Azienda Ospedaliero-Universitaria di Parma, Parma, Italy.

Gianni Binotto (G)

Unit of Hematology and Clinical Immunology, University of Padova, Padova, Italy.

Francesco Cavazzini (F)

Division of Hematology, University of Ferrara, Ferrara, Italy.

Elisabetta Abruzzese (E)

Division of Hematology, Ospedale S. Eugenio, Roma, Italy.

Alessandra Iurlo (A)

Hematology Division, Foundation IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy.

Alessandro Isidori (A)

Hematology and Stem Cell Transplant Center, AORMN Hospital, Pesaro, Italy.

Costanza Bosi (C)

Division of Hematology, AUSL di Piacenza, Piacenza, Italy.

Veronica Guglielmana (V)

Fondazione IRCCS San Gerardo dei Tintori, divisione di ematologia e unità trapianto di midollo, Monza, Italy.

Marta Venturi (M)

Dipartimento di Medicina Specialistica, Diagnostica e Sperimentale, Università di Bologna, Bologna, Italy.

Alessandra Dedola (A)

Dipartimento di Medicina Specialistica, Diagnostica e Sperimentale, Università di Bologna, Bologna, Italy.

Michele Loffredo (M)

Dipartimento di Medicina Specialistica, Diagnostica e Sperimentale, Università di Bologna, Bologna, Italy.

Gabriele Fontana (G)

Dipartimento di Medicina Specialistica, Diagnostica e Sperimentale, Università di Bologna, Bologna, Italy.

Andrea Duminuco (A)

Postgraduate School of Hematology, University of Catania, Catania, Italy.

Alessia Moioli (A)

Department of Engineering for Innovation Medicine, Section of Innovation Biomedicine, Hematology Area, University of Verona, Verona, Italy.

Luca Tosoni (L)

Division of Hematology and BMT, Department of Medicine, University of Udine, Udine, Italy.

Emilia Scalzulli (E)

Hematology, Department of Translational and Precision Medicine, Az. Policlinico Umberto I-Sapienza University, Rome, Italy.

Daniele Cattaneo (D)

Hematology Division, Foundation IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy.

Roberto M Lemoli (RM)

IRCCS Ospedale Policlinico San Martino, Genoa, Italy.
Dipartimento di Medicina Interna e Specialità Mediche, Università di Genova, Genova, Italy.

Daniela Cilloni (D)

Department of Clinical and Biological Sciences, University of Turin, Turin, Italy.

Monica Bocchia (M)

Hematology Unit, Azienda Ospedaliera Universitaria Senese, University of Siena, Siena, Italy.

Fabrizio Pane (F)

Department of Clinical Medicine and Surgery, Federico II University Medical School, Naples, Italy.

Florian H Heidel (FH)

Hematology, Hemostasis, Oncology and Stem Cell Transplantation, Hannover Medical School (MHH), Hannover, Germany.

Nicola Vianelli (N)

IRCCS Azienda Ospedaliero-Universitaria di Bologna, Istituto di Ematologia "Seràgnoli", Bologna, Italy.

Michele Cavo (M)

IRCCS Azienda Ospedaliero-Universitaria di Bologna, Istituto di Ematologia "Seràgnoli", Bologna, Italy.
Dipartimento di Medicina Specialistica, Diagnostica e Sperimentale, Università di Bologna, Bologna, Italy.

Giuseppe A Palumbo (GA)

Department of Scienze Mediche, Chirurgiche e Tecnologie Avanzate "G.F. Ingrassia", University of Catania, Catania, Italy.

Filippo Branzanti (F)

Dipartimento di Medicina Specialistica, Diagnostica e Sperimentale, Università di Bologna, Bologna, Italy.

Massimo Breccia (M)

Hematology, Department of Translational and Precision Medicine, Az. Policlinico Umberto I-Sapienza University, Rome, Italy.

Classifications MeSH