Dismal outcome of refractory or relapsing patients with myelodysplasia-related acute myeloid leukemia partially alleviated by intensive chemotherapy.

acute myeloid leukemia azacitidine intensive chemotherapy myelodysplasia-related changes primary induction failure refractoriness relapse

Journal

Cancer medicine
ISSN: 2045-7634
Titre abrégé: Cancer Med
Pays: United States
ID NLM: 101595310

Informations de publication

Date de publication:
Feb 2024
Historique:
revised: 08 01 2024
received: 15 05 2023
accepted: 31 01 2024
medline: 24 2 2024
pubmed: 24 2 2024
entrez: 24 2 2024
Statut: ppublish

Résumé

Acute myeloid leukemia (AML) with myelodysplasia-related characteristics is a heterogeneous subset of AML that has been challenged throughout the history of myeloid malignancies classifications, considered to have similar outcomes as intermediate- or adverse-risk AML depending on the subgroup. However, little is known about the fate of these patients in refractory or relapsed situation (R/R) after first line therapy. A large series of R/R AML patients, recorded in the French DATAML registry, have received either intensive chemotherapy (ICT), azacitidine (AZA) as single agent, or best supportive care (BSC). A cohort of 183 patients (median age 63-year-old) with what was called at the time AML-MRC has been explored, and data are reported here. Patient status was refractory for 93, while 90 had relapsed. Respectively, 88, 34, and 61 were included in the three treatment arms. The median OS of the whole cohort was 4.2 months (95%CI: 3.1-5.6) with a mean 1-year overall survival of 24% ± 3.2%. There was no significant survival difference between refractory and relapsed patients. The BSC group had overall a significantly worse outcome (p = 0.0001), and this remained true in both refractory (p = 0.01) and relapsed (p = 0.002) patients. Similar survivals were observed in both groups comparing ICT and AZA. These data, reporting about an ill-explored population, indicate the poor prognosis of this condition where both ICT and AZA can be proposed. The latter, which was demonstrated here to be a feasible option, should be added to new targeted therapies.

Sections du résumé

BACKGROUND BACKGROUND
Acute myeloid leukemia (AML) with myelodysplasia-related characteristics is a heterogeneous subset of AML that has been challenged throughout the history of myeloid malignancies classifications, considered to have similar outcomes as intermediate- or adverse-risk AML depending on the subgroup. However, little is known about the fate of these patients in refractory or relapsed situation (R/R) after first line therapy.
METHODS METHODS
A large series of R/R AML patients, recorded in the French DATAML registry, have received either intensive chemotherapy (ICT), azacitidine (AZA) as single agent, or best supportive care (BSC). A cohort of 183 patients (median age 63-year-old) with what was called at the time AML-MRC has been explored, and data are reported here.
RESULTS RESULTS
Patient status was refractory for 93, while 90 had relapsed. Respectively, 88, 34, and 61 were included in the three treatment arms. The median OS of the whole cohort was 4.2 months (95%CI: 3.1-5.6) with a mean 1-year overall survival of 24% ± 3.2%. There was no significant survival difference between refractory and relapsed patients. The BSC group had overall a significantly worse outcome (p = 0.0001), and this remained true in both refractory (p = 0.01) and relapsed (p = 0.002) patients. Similar survivals were observed in both groups comparing ICT and AZA.
CONCLUSIONS CONCLUSIONS
These data, reporting about an ill-explored population, indicate the poor prognosis of this condition where both ICT and AZA can be proposed. The latter, which was demonstrated here to be a feasible option, should be added to new targeted therapies.

Identifiants

pubmed: 38400682
doi: 10.1002/cam4.7003
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e7003

Informations de copyright

© 2024 The Authors. Cancer Medicine published by John Wiley & Sons Ltd.

Références

Jaffe ES, Harris NL, Stein H, Wardiman JW. Tumors of Haematopoietic and Lymphoid Tissues. IARCPress; 2001.
Vardiman JW, Thiele J, Arber DA, et al. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood. 2009:114-951.
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.
Khoury JD, Solary E, Abla O, et al. The 5th edition of the World Health Organization classification of haematolymphoid tumours: myeloid and histiocytic/dendritic neoplasms. Leukemia. 2022;36:1703-1719.
Miesner M, Haferlach C, Bacher U, et al. Multilineage dysplasia (MLD) in acute myeloid leukemia (AML) correlates with MDS-related cytogenetic abnormalities and a prior history of MDS or MDS/MPN but has no independent prognostic relevance: a comparison of 408 cases classified as “AML not otherwise specified” (AML-NOS) or “AML with myelodysplasia-related changes” (AML-MRC). Blood. 2010;116:2742-2751.
Montalban-Bravo G, Kanagal-Shamanna R, Class CA, et al. Outcomes of acute myeloid leukemia with myelodysplasia related changes depend on diagnostic criteria and therapy. Am J Hematol. 2020;95:612-622.
Fenaux P, Mufti GJ, Hellstrom-Lindberg E, et al. Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: a randomised, open-label, phase III study. Lancet Oncol. 2009;10:223-232.
Fenaux P, Mufti GJ, Hellström-Lindberg E, et al. Azacitidine prolongs overall survival compared with conventional care regimens in elderly patients with low bone marrow blast count acute myeloid leukemia. J Clin Oncol. 2010;28:562-569.
Dombret H, Seymour JF, Butrym A, et al. International phase 3 study of azacitidine vs conventional care regimens in older patients with newly diagnosed AML with >30% blasts. Blood. 2015;126:291-299.
Seymour JF, Döhner H, Butrym A, et al. Azacitidine improves clinical outcomes in older patients with acute myeloid leukaemia with myelodysplasia-related changes compared with conventional care regimens. BMC Cancer. 2017;17:852.
Lancet JE, Cortes JE, Hogge DE, et al. Phase 2 trial of CPX-351, a fixed 5:1 molar ratio of cytarabine/daunorubicin, vs cytarabine/daunorubicin in older adults with untreated AML. Blood. 2014;123:3239-3246.
Lancet JE, Uy GL, Cortes JE, et al. CPX-351 (cytarabine and daunorubicin) liposome for injection versus conventional cytarabine plus daunorubicin in older patients with newly diagnosed secondary acute myeloid leukemia. J Clin Oncol. 2018;36:2684-2692.
Perl AE, Martinelli G, Cortes JE, et al. Gilteritinib or chemotherapy for relapsed or refractory FLT3-mutated AML. N Engl J Med. 2019;381:1728-1740.
Koenig K, Mims A. Relapsed or primary refractory AML: moving past MEC and FLAG-ida. Curr Opin Hematol. 2020;27:108-114.
Jonas BA, Potter LA, Galkin M, Tuscano JM. A phase II trial of decitabine, bortezomib and pegylated liposomal doxorubicin for the treatment of relapsed or refractory AML. Leuk Res Rep. 2023;8(19):100374.
Jonas BA, Hou JZ, Roboz GJ, et al. A phase 1b study of venetoclax and alvocidib in patients with relapsed/refractory acute myeloid leukemia. Hematol Oncol. 2023;41:743-752.
Grimwade D, Walker H, Oliver F, et al. The importance of diagnostic cytogenetics on outcome in AML: analysis of 1,612 patients entered into the MRC AML 10 trial. The Medical Research Council Adult and Children's Leukaemia Working Parties. Blood. 1998;92:2322-2333.
Döhner H, Estey E, Grimwade D, et al. Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel. Blood. 2017;129:424-447.
Adès L, Duployez N, Guerci-Bresler A, et al. A randomised phase II study of azacitidine (AZA) alone or with lenalidomide (LEN), valproic acid (VPA) or idarubicin (IDA) in higher-risk MDS or low blast AML: GFM's “pick a winner” trial, with the impact of somatic mutations. Br J Haematol. 2022;198:535-544.
Cheson BD, Greenberg PL, Bennett JM, et al. Clinical application and proposal for modification of the International Working Group (IWG) response criteria in myelodysplasia. Blood. 2006;108:419-425.
Gadaud N, Leroy H, Bérard E, et al. Azacitidine, intensive chemotherapy or best supportive care in relapsed or refractory acute myeloid leukemia, a DATAML registry study. Leuk Lymphoma. 2022;63:1398-1406.
Kaivers J, Peters J, Rautenberg C, et al. The WHO 2016 diagnostic criteria for acute myeloid leukemia with myelodysplasia related changes (AML-MRC) produce a very heterogeneous entity: a retrospective analysis of the FAB subtype RAEB-T. Leuk Res. 2022;112:106757.
Kern W, Haferlach T, Schnittger S, Ludwig WD, Hiddemann W, Schoch C. Karyotype instability between diagnosis and relapse in 117 patients with acute myeloid leukemia: implications for resistance against therapy. Leukemia. 2002;16:2084-2091.
Lindsley RC, Mar BG, Mazzola E, et al. Acute myeloid leukemia ontogeny is defined by distinct somatic mutations. Blood. 2015;125:1367-1376.
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;140:1200-1228.
Döhner H, Wei AH, Appelbaum FR, et al. Diagnosis and management of AML in adults: 2022 recommendations from an international expert panel on behalf of the ELN. Blood. 2022;140:1345-1377.
Xu XQ, Wang JM, Gao L, et al. Characteristics of acute myeloid leukemia with myelodysplasia-related changes: a retrospective analysis in a cohort of Chinese patients. Am J Hematol. 2014;8:874-881.
Stahl M, DeVeaux M, Montesinos P, et al. Hypomethylating agents in relapsed and refractory AML: outcomes and their predictors in a large international patient cohort. Blood Adv. 2018;2:923-932.
DiNardo CD, Jonas BA, Pullarkat V, et al. Azacitidine and venetoclax in previously untreated acute myeloid leukemia. N Engl J Med. 2020;383(7):617-629.
Wei AH, Panayiotidis P, Montesinos P, et al. 6-month follow-up of VIALE-C demonstrates improved and durable efficacy in patients with untreated AML ineligible for intensive chemotherapy (141/150). Blood Cancer J. 2021;11:163.

Auteurs

Harmony Leroy (H)

CHU Bordeaux, Service d'Hématologie Clinique et de Thérapie Cellulaire, Bordeaux, France.

Noémie Gadaud (N)

Service d'Hématologie, Centre Hospitalier Universitaire de Toulouse, Institut Universitaire du Cancer de Toulouse-Oncopole, Toulouse, France.

Emilie Bérard (E)

Centre Hospitalier Universitaire de Toulouse, Service d'Epidémiologie, CERPOP, Inserm, Université Toulouse III Paul Sabatier, Toulouse, France.

Emilie Klein (E)

CHU Bordeaux, Laboratoire d'Hématologie Biologique, Bordeaux, France.

Isabelle Luquet (I)

Laboratoire d'Hématologie, Centre Hospitalier Universitaire de Toulouse, Institut Universitaire du Cancer de Toulouse-Oncopole, Toulouse, France.

Jean-Philippe Vial (JP)

CHU Bordeaux, Laboratoire d'Hématologie Biologique, Bordeaux, France.

Jean-Baptiste Rieu (JB)

Laboratoire d'Hématologie, Centre Hospitalier Universitaire de Toulouse, Institut Universitaire du Cancer de Toulouse-Oncopole, Toulouse, France.

Nicolas Lechevalier (N)

CHU Bordeaux, Laboratoire d'Hématologie Biologique, Bordeaux, France.

Suzanne Tavitian (S)

Service d'Hématologie, Centre Hospitalier Universitaire de Toulouse, Institut Universitaire du Cancer de Toulouse-Oncopole, Toulouse, France.

Thibaut Leguay (T)

CHU Bordeaux, Service d'Hématologie Clinique et de Thérapie Cellulaire, Bordeaux, France.

Laetitia Largeaud (L)

Laboratoire d'Hématologie, Centre Hospitalier Universitaire de Toulouse, Institut Universitaire du Cancer de Toulouse-Oncopole, Toulouse, France.

Audrey Bidet (A)

CHU Bordeaux, Laboratoire d'Hématologie Biologique, Bordeaux, France.

Eric Delabesse (E)

Laboratoire d'Hématologie, Centre Hospitalier Universitaire de Toulouse, Institut Universitaire du Cancer de Toulouse-Oncopole, Toulouse, France.

Audrey Sarry (A)

Service d'Hématologie, Centre Hospitalier Universitaire de Toulouse, Institut Universitaire du Cancer de Toulouse-Oncopole, Toulouse, France.

Anne-Charlotte de Grande (AC)

CHU Bordeaux, Service d'Hématologie Clinique et de Thérapie Cellulaire, Bordeaux, France.

Christian Récher (C)

Service d'Hématologie, Centre Hospitalier Universitaire de Toulouse, Institut Universitaire du Cancer de Toulouse-Oncopole, Toulouse, France.

Arnaud Pigneux (A)

CHU Bordeaux, Service d'Hématologie Clinique et de Thérapie Cellulaire, Bordeaux, France.
Université de Bordeaux, Bordeaux, Institut National de la Santé et de la Recherche Médicale, Bordeaux, France.

Sarah Bertoli (S)

Service d'Hématologie, Centre Hospitalier Universitaire de Toulouse, Institut Universitaire du Cancer de Toulouse-Oncopole, Toulouse, France.

Pierre-Yves Dumas (PY)

CHU Bordeaux, Service d'Hématologie Clinique et de Thérapie Cellulaire, Bordeaux, France.
Université de Bordeaux, Bordeaux, Institut National de la Santé et de la Recherche Médicale, Bordeaux, France.

Classifications MeSH