Allogeneic Hematopoietic Cell Transplantation in Advanced Systemic Mastocytosis: A retrospective analysis of the DRST and GREM registries.
Journal
Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895
Informations de publication
Date de publication:
06 Mar 2024
06 Mar 2024
Historique:
received:
23
12
2023
accepted:
14
02
2024
medline:
7
3
2024
pubmed:
7
3
2024
entrez:
6
3
2024
Statut:
aheadofprint
Résumé
We identified 71 patients with AdvSM (aggressive SM [ASM], SM with an associated hematologic neoplasm [SM-AHN, e.g., acute myeloid leukemia, SM-AML], mast cell leukemia [MCL]) in two national registries (DRST/GREM) who received an allogeneic hematopoietic cell transplantation (alloHCT) performed in Germany from 1999-2021. Median overall survival (OS) of ASM/SM-AHN (n = 30, 45%), SM-AML (n = 28, 39%) and MCL ± AHN (n = 13, 19%) was 9.0, 3.3 and 0.9 years (P = 0.007). Improved median OS was associated with response of SM (17/41, 41%; HR 0.4 [0.2-0.9], P = 0.035) and/or of AHN (26/43, 60%, HR 0.3 [0.1-0.7], P = 0.004) prior to alloHCT. Adverse predictors for OS included absence of KIT D816V (10/61, 16%, HR 2.9 [1.2-6.5], P < 0.001) and a complex karyotype (9/60, 15%, HR 4.2 [1.8-10.0], P = 0.016). HLA-match, conditioning type or transplantation at centers reporting above-average alloHCTs (≥7) had no impact on OS. Taking into account competing events at years 1, 3 and 5, relapse-related mortality and non-relapse mortality rate were 15%/23%, 20%/30% and 23%/35%, respectively. Irrespective of subtype, subsequent treatment response was achieved in 13/30 (43%) patients and was highest on midostaurin/avapritinib (7/9, 78%). We conclude that outcome of alloHCT in AdvSM is more affected by disease phenotype and treatment response prior to transplant than by transplant characteristics.
Identifiants
pubmed: 38448757
doi: 10.1038/s41375-024-02186-x
pii: 10.1038/s41375-024-02186-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Valent P, Akin C, Hartmann K, Alvarez-Twose I, Brockow K, Hermine O, et al. Updated diagnostic criteria and classification of mast cell disorders: a consensus proposal. Hemasphere. 2021;5:e646.
pubmed: 34901755
pmcid: 8659997
doi: 10.1097/HS9.0000000000000646
Valent P, Horny HP, Escribano L, Longley BJ, Li CY, Schwartz LB, et al. Diagnostic criteria and classification of mastocytosis: a consensus proposal. Leuk Res. 2001;25:603–25.
pubmed: 11377686
doi: 10.1016/S0145-2126(01)00038-8
Khoury JD, Solary E, Abla O, Akkari Y, Alaggio R, Apperley JF, et al. The 5th edition of the World Health Organization classification of haematolymphoid tumours: myeloid and histiocytic/dendritic neoplasms. Leukemia. 2022;36:1703–19.
pubmed: 35732831
pmcid: 9252913
doi: 10.1038/s41375-022-01613-1
Arber DA, Orazi A, Hasserjian RP, Borowitz MJ, Calvo KR, Kvasnicka HM, et al. International consensus classification of myeloid neoplasms and acute leukemias: integrating morphologic, clinical, and genomic data. Blood. 2022;140:1200–28.
pubmed: 35767897
pmcid: 9479031
doi: 10.1182/blood.2022015850
Erben P, Schwaab J, Metzgeroth G, Horny HP, Jawhar M, Sotlar K, et al. The KIT D816V expressed allele burden for diagnosis and disease monitoring of systemic mastocytosis. Ann Hematol. 2014;93:81–8.
pubmed: 24281161
doi: 10.1007/s00277-013-1964-1
Naumann N, Lübke J, Baumann S, Schwaab J, Hoffmann O, Kreil S, et al. Adverse prognostic impact of the KIT D816V transcriptional activity in advanced systemic mastocytosis. Int J Mol Sci. 2021;22:2562.
pubmed: 33806359
pmcid: 7961551
doi: 10.3390/ijms22052562
Arock M, Sotlar K, Akin C, Broesby-Olsen S, Hoermann G, Escribano L, et al. KIT mutation analysis in mast cell neoplasms: recommendations of the European Competence Network on Mastocytosis. Leukemia. 2015;29:1223–32.
pubmed: 25650093
pmcid: 4522520
doi: 10.1038/leu.2015.24
Jawhar M, Schwaab J, Alvarez-Twose I, Shoumariyeh K, Naumann N, Lübke J, et al. MARS: mutation-adjusted risk score for advanced systemic mastocytosis. J Clin Oncol. 2019;37:2846–56.
pubmed: 31509472
pmcid: 6823885
doi: 10.1200/JCO.19.00640
Jawhar M, Schwaab J, Naumann N, Horny HP, Sotlar K, Haferlach T, et al. Response and progression on midostaurin in advanced systemic mastocytosis: KIT D816V and other molecular markers. Blood. 2017;130:137–45.
pubmed: 28424161
doi: 10.1182/blood-2017-01-764423
Jawhar M, Schwaab J, Schnittger S, Meggendorfer M, Pfirrmann M, Sotlar K, et al. Additional mutations in SRSF2, ASXL1 and/or RUNX1 identify a high-risk group of patients with KIT D816V(+) advanced systemic mastocytosis. Leukemia. 2016;30:136–43.
pubmed: 26464169
doi: 10.1038/leu.2015.284
Jawhar M, Schwaab J, Hausmann D, Clemens J, Naumann N, Henzler T, et al. Splenomegaly, elevated alkaline phosphatase and mutations in the SRSF2/ASXL1/RUNX1 gene panel are strong adverse prognostic markers in patients with systemic mastocytosis. Leukemia. 2016;30:2342–50.
pubmed: 27416984
doi: 10.1038/leu.2016.190
Schwaab J, Schnittger S, Sotlar K, Walz C, Fabarius A, Pfirrmann M, et al. Comprehensive mutational profiling in advanced systemic mastocytosis. Blood. 2013;122:2460–6.
pubmed: 23958953
doi: 10.1182/blood-2013-04-496448
Lübke J, Naumann N, Metzgeroth G, Kreil S, Brand T, Horny HP, et al. Response and resistance to cladribine in patients with advanced systemic mastocytosis: a registry-based analysis. Ann Hematol. 2023;102:2077–85.
pubmed: 37012462
pmcid: 10344834
doi: 10.1007/s00277-023-05180-y
Tefferi A, Kittur J, Farrukh F, Begna KH, Patnaik MM, Al-Kali A, et al. Cladribine therapy for advanced and indolent systemic mastocytosis: Mayo Clinic experience in 42 consecutive cases. Br J Haematol. 2022;196:975–83.
pubmed: 34729775
doi: 10.1111/bjh.17932
Kluin-Nelemans HC, Oldhoff JM, Van Doormaal JJ, Van ‘t Wout JW, Verhoef G, Gerrits WB, et al. Cladribine therapy for systemic mastocytosis. Blood. 2003;102:4270–6.
pubmed: 12933573
doi: 10.1182/blood-2003-05-1699
Barete S, Lortholary O, Damaj G, Hirsch I, Chandesris MO, Elie C, et al. Long-term efficacy and safety of cladribine (2-CdA) in adult patients with mastocytosis. Blood. 2015;126:1009–16.
pubmed: 26002962
doi: 10.1182/blood-2014-12-614743
Singh A, Al-Kali A, Begna KH, Litzow MR, Larsen JT, Sher T, et al. Midostaurin therapy for advanced systemic mastocytosis: Mayo Clinic experience in 33 consecutive cases. Am J Hematol. 2022;97:630–7.
pubmed: 35156231
doi: 10.1002/ajh.26498
Lübke J, Schwaab J, Naumann N, Horny HP, Weiß C, Metzgeroth G, et al. Superior efficacy of midostaurin over cladribine in advanced systemic mastocytosis: a registry-based analysis. J Clin Oncol. 2022;40:1783–94.
pubmed: 35235417
doi: 10.1200/JCO.21.01849
DeAngelo DJ, George TI, Linder A, Langford C, Perkins C, Ma J, et al. Efficacy and safety of midostaurin in patients with advanced systemic mastocytosis: 10-year median follow-up of a phase II trial. Leukemia. 2018;32:470–8.
pubmed: 28744009
doi: 10.1038/leu.2017.234
Gotlib J, Kluin-Nelemans HC, George TI, Akin C, Sotlar K, Hermine O, et al. Efficacy and safety of midostaurin in advanced systemic mastocytosis. N. Engl J Med. 2016;374:2530–41.
pubmed: 27355533
doi: 10.1056/NEJMoa1513098
Chandesris MO, Damaj G, Canioni D, Brouzes C, Lhermitte L, Hanssens K, et al. Midostaurin in advanced systemic mastocytosis. N Engl J Med. 2016;374:2605–7.
pubmed: 27355555
doi: 10.1056/NEJMc1515403
Reiter A, Gotlib J, Álvarez-Twose I, Radia DH, Lübke J, Bobbili PJ, et al. Efficacy of avapritinib versus best available therapy in the treatment of advanced systemic mastocytosis. Leukemia. 2022;36:2108–20.
pubmed: 35790816
pmcid: 9343245
doi: 10.1038/s41375-022-01615-z
Reiter A, Schwaab J, DeAngelo DJ, Gotlib J, Deininger MW, Pettit KM, et al. Efficacy and safety of avapritinib in previously treated patients with advanced systemic mastocytosis. Blood Adv. 2022;6:5750–62.
pubmed: 35640224
pmcid: 9647833
doi: 10.1182/bloodadvances.2022007539
DeAngelo DJ, Radia DH, George TI, Robinson WA, Quiery AT, Drummond MW, et al. Safety and efficacy of avapritinib in advanced systemic mastocytosis: the phase 1 EXPLORER trial. Nat Med. 2021;27:2183–91.
pubmed: 34873347
pmcid: 8674134
doi: 10.1038/s41591-021-01538-9
Gotlib J, Reiter A, Radia DH, Deininger MW, George TI, Panse J, et al. Efficacy and safety of avapritinib in advanced systemic mastocytosis: interim analysis of the phase 2 PATHFINDER trial. Nat Med. 2021;27:2192–9.
pubmed: 34873345
pmcid: 8674139
doi: 10.1038/s41591-021-01539-8
Ustun C, Reiter A, Scott BL, Nakamura R, Damaj G, Kreil S, et al. Hematopoietic stem-cell transplantation for advanced systemic mastocytosis. J Clin Oncol. 2014;32:3264–74.
pubmed: 25154823
pmcid: 4876356
doi: 10.1200/JCO.2014.55.2018
Slavin S, Nagler A, Naparstek E, Kapelushnik Y, Aker M, Cividalli G, et al. Nonmyeloablative stem cell transplantation and cell therapy as an alternative to conventional bone marrow transplantation with lethal cytoreduction for the treatment of malignant and nonmalignant hematologic diseases. Blood. 1998;91:756–63.
pubmed: 9446633
doi: 10.1182/blood.V91.3.756
Luznik L, O’Donnell PV, Fuchs EJ. Post-transplantation cyclophosphamide for tolerance induction in HLA-haploidentical bone marrow transplantation. Semin Oncol. 2012;39:683–93.
pubmed: 23206845
doi: 10.1053/j.seminoncol.2012.09.005
Shouval R, Fein JA, Labopin M, Kröger N, Duarte RF, Bader P, et al. Outcomes of allogeneic haematopoietic stem cell transplantation from HLA-matched and alternative donors: a European Society for Blood and Marrow Transplantation registry retrospective analysis. Lancet Haematol. 2019;6:e573–84.
pubmed: 31477550
doi: 10.1016/S2352-3026(19)30158-9
Bacigalupo A, Ballen K, Rizzo D, Giralt S, Lazarus H, Ho V, et al. Defining the intensity of conditioning regimens: working definitions. Biol Blood Marrow Transplant. 2009;15:1628–33.
pubmed: 19896087
pmcid: 2861656
doi: 10.1016/j.bbmt.2009.07.004
Gotlib J, Pardanani A, Akin C, Reiter A, George T, Hermine O, et al. International Working Group-Myeloproliferative Neoplasms Research and Treatment (IWG-MRT) & European Competence Network on Mastocytosis (ECNM) consensus response criteria in advanced systemic mastocytosis. Blood 2013;121:2393–401.
pubmed: 23325841
pmcid: 3612852
doi: 10.1182/blood-2012-09-458521
Gotlib J, Schwaab J, Shomali W, George TI, Radia DH, Castells M, et al. Proposed European Competence Network on Mastocytosis-American Initiative in Mast Cell Diseases (ECNM-AIM) response criteria in advanced systemic mastocytosis. J Allergy Clin Immunol Pr. 2022;10:2025–38.e1.
doi: 10.1016/j.jaip.2022.05.034
Shomali W, Gotlib J. Response criteria in advanced systemic mastocytosis: evolution in the Era of KIT inhibitors. Int J Mol Sci. 2021;22:2983.
Jawhar M, Schwaab J, Naumann N, Kluger S, Horny H-P, Sotlar K, et al. Impact of molecular markers on response and resistance in midostaurin-treated patients with advanced systemic mastocytosis. Blood. 2016;128:945.
doi: 10.1182/blood.V128.22.945.945
Lübke J, Naumann N, Kluger S, Schwaab J, Metzgeroth G, Evans E, et al. Inhibitory effects of midostaurin and avapritinib on myeloid progenitors derived from patients with KIT D816V positive advanced systemic mastocytosis. Leukemia. 2019;33:1195–205.
pubmed: 30911112
pmcid: 6756065
doi: 10.1038/s41375-019-0450-8
Buckley SA, Wood BL, Othus M, Hourigan CS, Ustun C, Linden MA, et al. Minimal residual disease prior to allogeneic hematopoietic cell transplantation in acute myeloid leukemia: a meta-analysis. Haematologica. 2017;102:865–73.
pubmed: 28126965
pmcid: 5477605
doi: 10.3324/haematol.2016.159343
Anthias C, Dignan FL, Morilla R, Morilla A, Ethell ME, Potter MN, et al. Pre-transplant MRD predicts outcome following reduced-intensity and myeloablative allogeneic hemopoietic SCT in AML. Bone Marrow Transpl. 2014;49:679–83.
doi: 10.1038/bmt.2014.9
Walter RB, Gyurkocza B, Storer BE, Godwin CD, Pagel JM, Buckley SA, et al. Comparison of minimal residual disease as outcome predictor for AML patients in first complete remission undergoing myeloablative or nonmyeloablative allogeneic hematopoietic cell transplantation. Leukemia. 2015;29:137–44.
pubmed: 24888275
doi: 10.1038/leu.2014.173
Woolfrey AE, Anasetti C, Storer B, Doney K, Milner LA, Sievers EL, et al. Factors associated with outcome after unrelated marrow transplantation for treatment of acute lymphoblastic leukemia in children. Blood. 2002;99:2002–8.
pubmed: 11877272
doi: 10.1182/blood.V99.6.2002
Sriskandarajah P, McLornan DP, Oni C, Wilson AJ, Woodley C, Ciesielska M, et al. Advanced systemic mastocytosis with associated haematological neoplasm: treatment with avapritinib can facilitate successful bridge to allogeneic haematopoietic cell transplant. Curr Res Transl Med. 2023;71:103398.
pubmed: 37331225
de Witte T, Bowen D, Robin M, Malcovati L, Niederwieser D, Yakoub-Agha I, et al. Allogeneic hematopoietic stem cell transplantation for MDS and CMML: recommendations from an international expert panel. Blood. 2017;129:1753–62.
pubmed: 28096091
pmcid: 5524528
doi: 10.1182/blood-2016-06-724500
Jentzsch M, Geus U, Grimm J, Vucinic V, Pönisch W, Franke GN, et al. Pretreatment CD34(+)/CD38(-) cell burden as prognostic factor in myelodysplastic syndrome patients receiving allogeneic stem cell transplantation. Biol Blood Marrow Transpl. 2019;25:1560–6.
doi: 10.1016/j.bbmt.2019.03.022
Ustun C, Gotlib J, Popat U, Artz A, Litzow M, Reiter A, et al. Consensus opinion on allogeneic hematopoietic cell transplantation in advanced systemic mastocytosis. Biol Blood Marrow Transpl. 2016;22:1348–56.
doi: 10.1016/j.bbmt.2016.04.018
Gyurkocza B, Sandmaier BM. Conditioning regimens for hematopoietic cell transplantation: one size does not fit all. Blood. 2014;124:344–53.
pubmed: 24914142
pmcid: 4102707
doi: 10.1182/blood-2014-02-514778
Kreidieh F, Abou Dalle I, Moukalled N, El-Cheikh J, Brissot E, Mohty M, et al. Relapse after allogeneic hematopoietic stem cell transplantation in acute myeloid leukemia: an overview of prevention and treatment. Int J Hematol. 2022;116:330–40.
pubmed: 35841458
doi: 10.1007/s12185-022-03416-7
Schwaab J, Cabral do OHN, Naumann N, Jawhar M, Weiß C, Metzgeroth G, et al. Importance of adequate diagnostic work-up for correct diagnosis of advanced systemic mastocytosis. J Allergy Clin Immunol Pract. 2020;8:3121–27.
Jawhar M, Schwaab J, Horny HP, Sotlar K, Naumann N, Fabarius A, et al. Impact of centralized evaluation of bone marrow histology in systemic mastocytosis. Eur J Clin Invest. 2016;46:392–7.
pubmed: 26914980
doi: 10.1111/eci.12607
DeAngelo DJ, Quiery AT, Radia D, Drummond MW, Gotlib JR, WA, Hexner E, et al. Clinical activity in a Phase 1 study of BLU-285, a potent, highly-selective inhibitor of KIT D816V in advanced systemic mastocytosis. American Society of Hematology Annual Meeting, Atlanta. 2017.
Gotlib J. World Health Organization-defined eosinophilic disorders: 2017 update on diagnosis, risk stratification, and management. Am J Hematol. 2017;92:1243–59.
pubmed: 29044676
doi: 10.1002/ajh.24880