Ruxolitinib rechallenge in resistant or intolerant patients with myelofibrosis: Frequency, therapeutic effects, and impact on outcome.


Journal

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

Informations de publication

Date de publication:
01 08 2021
Historique:
revised: 24 02 2021
received: 18 01 2021
accepted: 01 03 2021
pubmed: 2 4 2021
medline: 9 3 2022
entrez: 1 4 2021
Statut: ppublish

Résumé

After ruxolitinib discontinuation, the outcome of patients with myelofibrosis (MF) is poor with scarce therapeutic possibilities. The authors performed a subanalysis of an observational, retrospective study (RUX-MF) that included 703 MF patients treated with ruxolitinib to investigate 1) the frequency and reasons for ruxolitinib rechallenge, 2) its therapeutic effects, and 3) its impact on overall survival. A total of 219 patients (31.2%) discontinued ruxolitinib for ≥14 days and survived for ≥30 days. In 60 patients (27.4%), ruxolitinib was rechallenged for ≥14 days (RUX-again patients), whereas 159 patients (72.6%) discontinued it permanently (RUX-stop patients). The baseline characteristics of the 2 cohorts were comparable, but discontinuation due to a lack/loss of spleen response was lower in RUX-again patients (P = .004). In comparison with the disease status at the first ruxolitinib stop, at its restart, there was a significant increase in patients with large splenomegaly (P < .001) and a high Total Symptom Score (TSS; P < .001). During the rechallenge, 44.6% and 48.3% of the patients had spleen and symptom improvements, respectively, with a significant increase in the number of patients with a TSS reduction (P = .01). Although the use of a ruxolitinib dose > 10 mg twice daily predicted better spleen (P = .05) and symptom improvements (P = .02), the reasons for/duration of ruxolitinib discontinuation and the use of other therapies before rechallenge were not associated with rechallenge efficacy. At 1 and 2 years, 33.3% and 48.3% of RUX-again patients, respectively, had permanently discontinued ruxolitinib. The median overall survival was 27.9 months, and it was significantly longer for RUX-again patients (P = .004). Ruxolitinib rechallenge was mainly used in intolerant patients; there were clinical improvements and a possible survival advantage in many cases, but there was a substantial rate of permanent discontinuation. Ruxolitinib rechallenge should be balanced against newer therapeutic possibilities.

Sections du résumé

BACKGROUND
After ruxolitinib discontinuation, the outcome of patients with myelofibrosis (MF) is poor with scarce therapeutic possibilities.
METHODS
The authors performed a subanalysis of an observational, retrospective study (RUX-MF) that included 703 MF patients treated with ruxolitinib to investigate 1) the frequency and reasons for ruxolitinib rechallenge, 2) its therapeutic effects, and 3) its impact on overall survival.
RESULTS
A total of 219 patients (31.2%) discontinued ruxolitinib for ≥14 days and survived for ≥30 days. In 60 patients (27.4%), ruxolitinib was rechallenged for ≥14 days (RUX-again patients), whereas 159 patients (72.6%) discontinued it permanently (RUX-stop patients). The baseline characteristics of the 2 cohorts were comparable, but discontinuation due to a lack/loss of spleen response was lower in RUX-again patients (P = .004). In comparison with the disease status at the first ruxolitinib stop, at its restart, there was a significant increase in patients with large splenomegaly (P < .001) and a high Total Symptom Score (TSS; P < .001). During the rechallenge, 44.6% and 48.3% of the patients had spleen and symptom improvements, respectively, with a significant increase in the number of patients with a TSS reduction (P = .01). Although the use of a ruxolitinib dose > 10 mg twice daily predicted better spleen (P = .05) and symptom improvements (P = .02), the reasons for/duration of ruxolitinib discontinuation and the use of other therapies before rechallenge were not associated with rechallenge efficacy. At 1 and 2 years, 33.3% and 48.3% of RUX-again patients, respectively, had permanently discontinued ruxolitinib. The median overall survival was 27.9 months, and it was significantly longer for RUX-again patients (P = .004).
CONCLUSIONS
Ruxolitinib rechallenge was mainly used in intolerant patients; there were clinical improvements and a possible survival advantage in many cases, but there was a substantial rate of permanent discontinuation. Ruxolitinib rechallenge should be balanced against newer therapeutic possibilities.

Identifiants

pubmed: 33794557
doi: 10.1002/cncr.33541
doi:

Substances chimiques

Nitriles 0
Pyrazoles 0
Pyrimidines 0
ruxolitinib 82S8X8XX8H

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2657-2665

Subventions

Organisme : AIL Bologna

Informations de copyright

© 2021 American Cancer Society.

Références

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;189:888-903.
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;10:156.
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;10:55.
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;126:1243-1252.
Newberry KJ, Patel K, Masarova L, et al. Clonal evolution and outcomes in myelofibrosis after ruxolitinib discontinuation. Blood. 2017;130:1125-1131.
Tefferi A. Primary myelofibrosis: 2021 update on diagnosis, risk-stratification and management. Am J Hematol. 2021;96:145-162.
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;122:1395-1398.
Gangat N, Tefferi A. Myelofibrosis biology and contemporary management. Br J Haematol. 2020;191:152-170.
Harrison CN, Schaap N, Vannucchi AM, et al. Fedratinib in patients with myelofibrosis previously treated with ruxolitinib: an updated analysis of the JAKARTA2 study using stringent criteria for ruxolitinib failure. Am J Hematol. 2020;95:594-603.
Bassiony S, Harrison CN, McLornan DP. Evaluating the safety, efficacy, and therapeutic potential of momelotinib in the treatment of intermediate/high-risk myelofibrosis: evidence to date. Ther Clin Risk Manag. 2020;16:889-901.
Gerds AT, Savona MR, Scott BL, et al. Determining the recommended dose of pacritinib: results from the PAC203 dose-finding trial in advanced myelofibrosis. Blood Adv. 2020;4:5825-5835.
Tefferi A, Lasho TL, Begna KH, et al. A pilot study of the telomerase inhibitor imetelstat for myelofibrosis. N Engl J Med. 2015;373:908-919.
Kremyanskaya M, Hoffman R, Mascarenhas J, et al. A phase II study of cpi-0610, a bromodomain and extraterminal protein inhibitor (BETi) alone or with ruxolitinib (RUX), in patients with myelofibrosis (MF). J Clin Oncol. 2019;37:7056.
Durrant ST, Nagler A, Guglielmelli P, et al. Results from HARMONY: an open-label, multicenter, 2-arm, phase 1b, dose-finding study assessing the safety and efficacy of the oral combination of ruxolitinib and buparlisib in patients with myelofibrosis. Haematologica. 2019;104:e551-e554.
Pettit K, Gerds AT, Yacoub A, et al. A phase 2a study of the LSD1 inhibitor Img-7289 (bomedemstat) for the treatment of myelofibrosis. Blood. 2019;134:556.
Harrison C, Garcia JS, Mesa R, et al. Navitoclax in combination with ruxolitinib in patients with primary or secondary myelofibrosis: a phase 2 study. Clin Lymphoma Myeloma Leuk. 2020;20(suppl 1):S325.
Gerds A, Su D, Martynova A, et al. Ruxolitinib rechallenge can improve constitutional symptoms and splenomegaly in patients with myelofibrosis: a case series. Clin Lymphoma Myeloma Leuk. 2018;18:e463-e468.
Barosi G, Mesa RA, Thiele J, et al. Proposed criteria for the diagnosis of post-polycythemia vera and post-essential thrombocythemia myelofibrosis: a consensus statement from the International Working Group for Myelofibrosis Research and Treatment. Leukemia. 2008;22:437-438.
Arber DA, Orazi A, Hasserjian R, et al. The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood. 2016;127:2391-2405.
Passamonti F, Cervantes F, Vannucchi AM, et al. Dynamic International Prognostic Scoring System (DIPSS) predicts progression to acute myeloid leukemia in primary myelofibrosis. Blood. 2010;116:2857-2858.
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;90:1128-1132.
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;29:392-397.
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;30:4098-4103.
McLornan DP, Harrison CN. Guidance on changing therapy choice in myelofibrosis. Blood Adv. 2020;4:607-610.
U.S. FDA approves INREBIC® (fedratinib) as first new treatment in nearly a decade for patients with myelofibrosis. Celgene Corporation. August 16, 2019. Accessed December 1, 2019. https://ir.celgene.com/press-releases-archive/press-release-details/2019/US-FDA-Approves-INREBIC-Fedratinib-as-First-New-Treatment-in-Nearly-a-Decade-for-Patients-With-Myelofibrosis/default.aspx
Palandri F, Palumbo GA, Elli E, et al. Ruxolitinib discontinuation syndrome: incidence, risk factors and management in 251 patients with myelofibrosis. Blood Cancer J. 2021;11:4.
Tefferi A, Pardanani A. Serious adverse events during ruxolitinib treatment discontinuation in patients with myelofibrosis. Mayo Clin Proc. 2011;86:1188-1191.
Dai T, Friedman EW, Barta SK. Ruxolitinib withdrawal syndrome leading to tumor lysis. J Clin Oncol. 2013;31:e430-e432.
Beauverd Y, Samii K. Acute respiratory distress syndrome in a patient with primary myelofibrosis after ruxolitinib treatment discontinuation. Int J Hematol. 2014;100:498-501.
Coltro G, Mannelli F, Guglielmelli P, Pacilli A, Bosi A, Vannucchi AM. A life-threatening ruxolitinib discontinuation syndrome. Am J Hematol. 2017;92:833-838.
Koppikar P, Bhagwat N, Kilpivaara O, et al. Heterodimeric JAK-STAT activation as a mechanism of persistence to JAK2 inhibitor therapy. Nature. 2012;489:155-159.
Jayavelu AK, Schnöder TM, Perner F, et al. Splicing factor YBX1 mediates persistence of JAK2-mutated neoplasms. Nature. 2020;588:157-163.
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;363:1117-1127.
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;8:79073-79086.
Venugopal S, Mascarenhas J. Novel therapeutics in myeloproliferative neoplasms. J Hematol Oncol. 2020;13:162.

Auteurs

Francesca Palandri (F)

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

Mario Tiribelli (M)

Division of Hematology and Bone Marrow Transplantation, Azienda Sanitaria Universitaria Integrata di Udine, Udine, Italy.

Massimo Breccia (M)

Division of Cellular Biotechnologies and Hematology, University Sapienza, Rome, Italy.

Daniela Bartoletti (D)

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

Elena M Elli (EM)

Hematology Division and Bone Marrow Unit, San Gerardo Hospital, Azienda Socio Sanitaria Territoriale Monza, Monza, Italy.

Giulia Benevolo (G)

Division of Hematology, Città della Salute e della Scienza Hospital, Turin, Italy.

Bruno Martino (B)

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

Francesco Cavazzini (F)

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

Alessia Tieghi (A)

Department of Hematology, Azienda Unità Sanitaria Locale-IRCCS di Reggio Emilia, Reggio Emilia, Italy.

Alessandra Iurlo (A)

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

Elisabetta Abruzzese (E)

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

Novella Pugliese (N)

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

Gianni Binotto (G)

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

Giovanni Caocci (G)

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

Giuseppe Auteri (G)

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

Daniele Cattaneo (D)

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

Malgorzata M Trawinska (MM)

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

Rossella Stella (R)

Division of Hematology and Bone Marrow Transplantation, Azienda Sanitaria Universitaria Integrata di Udine, Udine, Italy.

Luigi Scaffidi (L)

Section of Hematology, University of Verona, Verona, Italy.

Nicola Polverelli (N)

Unit of Blood Diseases and Stem Cell Transplantation, Azienda Socio Sanitaria Territoriale degli Spedali Civili di Brescia, Brescia, Italy.

Giorgia Micucci (G)

Hematology and Stem Cell Transplant Center, Azienda Ospedaliera Ospedali Riuniti Marche Nord, Pesaro, Italy.

Elena Masselli (E)

Department of Medicine and Surgery, University of Parma, Parma, Italy.

Monica Crugnola (M)

Department of Medicine and Surgery, University of Parma, Parma, Italy.

Costanza Bosi (C)

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

Florian H Heidel (FH)

Hematology and Oncology, Friedrich Schiller University Medical Center, Jena, Germany.

Roberto Latagliata (R)

Hematology Unit, Ospedale Belcolle, Viterbo, Italy.

Fabrizio Pane (F)

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

Antonio Cuneo (A)

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

Mauro Krampera (M)

Section of Hematology, University of Verona, Verona, Italy.

Gianpietro Semenzato (G)

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

Roberto M Lemoli (RM)

Clinic of Hematology, Department of Internal Medicine, University of Genoa, Genoa, Italy.
IRCCS Policlinico San Martino, Genova, Italy.

Michele Cavo (M)

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

Nicola Vianelli (N)

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

Massimiliano Bonifacio (M)

Section of Hematology, University of Verona, Verona, Italy.

Giuseppe A Palumbo (GA)

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

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH