Graft-versus-host disease and impact on relapse in myelofibrosis undergoing hematopoietic stem cell transplantation.
Journal
Bone marrow transplantation
ISSN: 1476-5365
Titre abrégé: Bone Marrow Transplant
Pays: England
ID NLM: 8702459
Informations de publication
Date de publication:
06 Feb 2024
06 Feb 2024
Historique:
received:
19
11
2023
accepted:
19
01
2024
revised:
12
01
2024
medline:
7
2
2024
pubmed:
7
2
2024
entrez:
6
2
2024
Statut:
aheadofprint
Résumé
Allogeneic hematopoietic stem cell transplantation (alloHSCT) remains the only curative treatment for myelofibrosis (MF). Relapse occurs in 10-30% and remains a major factor for dismal outcomes. Previous work suggested that graft-versus-host disease (GVHD) might be associated with risk of relapse. This study included 341 patients undergoing their first (n = 308) or second (n = 33) alloHSCT. Anti-T-lymphocyte or antithymocyte globulin was used for GVHD prophylaxis in almost all patients. Median time to neutrophile and platelet engraftment was 13 days and 19 days, respectively. The cumulative incidence of acute GVHD grade II-IV was 41% (median, 31 days; range, 7-112). Grade III-IV acute GVHD was observed in 22%. The cumulative incidence of chronic GVHD was 61%. Liver was affected in 23% of acute GVHD cases and 46% of chronic GVHD cases. Severe acute GVHD was associated with high non-relapse mortality. The development of acute GVHD grade II and moderate GVHD was an independent factor for reduced risk for relapse after transplantation without increased risk for non-relapse mortality, while especially acute GVHD grade IV was associated with high non-relapse mortality. Last, we identified that ongoing response to ruxolitinib, accelerated-phase MF at time of transplantation and splenectomy prior to transplantation were independent predictors for relapse.
Identifiants
pubmed: 38321269
doi: 10.1038/s41409-024-02220-7
pii: 10.1038/s41409-024-02220-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
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
Mesa RA, Silverstein MN, Jacobsen SJ, Wollan PC, Tefferi A. Population-based incidence and survival figures in essential thrombocythemia and agnogenic myeloid metaplasia: an Olmsted county study, 1976-1995. Am J Hematol. 1999;61:10–5.
pubmed: 10331505
doi: 10.1002/(SICI)1096-8652(199905)61:1<10::AID-AJH3>3.0.CO;2-I
Rumi E, Cazzola M. Diagnosis, risk stratification, and response evaluation in classical myeloproliferative neoplasms. Blood. 2017;129:680–92.
pubmed: 28028026
pmcid: 5335805
doi: 10.1182/blood-2016-10-695957
Vannucchi AM, Lasho TL, Guglielmelli P, Biamonte F, Pardanani A, Pereira A, et al. Mutations and prognosis in primary myelofibrosis. Leukemia. 2013;27:1861–9.
pubmed: 23619563
doi: 10.1038/leu.2013.119
Tefferi A, Guglielmelli P, Lasho TL, Gangat N, Ketterling RP, Pardanani A, et al. MIPSS70+ version 2.0: mutation and karyotype-enhanced international prognostic scoring system for primary myelofibrosis. J Clin Oncol. 2018;36:1769–70.
pubmed: 29708808
doi: 10.1200/JCO.2018.78.9867
Kröger NM, Deeg JH, Olavarria E, Niederwieser D, Bacigalupo A, Barbui T, et al. Indication and management of allogeneic stem cell transplantation in primary myelofibrosis: a consensus process by an EBMT/ELN international working group. Leukemia. 2015;29:2126–33.
pubmed: 26293647
doi: 10.1038/leu.2015.233
Gagelmann N, Ditschkowski M, Bogdanov R, Bredin S, Robin M, Cassinat B, et al. Comprehensive clinical-molecular transplant scoring system for myelofibrosis undergoing stem cell transplantation. Blood. 2019;133:2233–42.
pubmed: 30760453
doi: 10.1182/blood-2018-12-890889
Stern, Wreede M, de LC, Brand R, van Biezen A, Dreger P, et al. Sensitivity of hematological malignancies to graft-versus-host effects: an EBMT megafile analysis. Leukemia. 2014;28:2235–40.
pubmed: 24781016
doi: 10.1038/leu.2014.145
McLornan DP, Szydlo R, Robin M, van Biezen A, Koster L, Blok HJP, et al. Outcome of patients with myelofibrosis relapsing after allogeneic stem cell transplant: a retrospective study by the chronic malignancies working party of EBMT. Br J Haematol. 2018;182:418–22.
pubmed: 29808926
doi: 10.1111/bjh.15407
Robin, Wreede M, de LC, Wolschke C, Schetelig J, Eikema DJ, et al. Long-term outcome after allogeneic hematopoietic cell transplantation for myelofibrosis. Haematologica. 2019;104:1782–8.
pubmed: 30733269
pmcid: 6717573
doi: 10.3324/haematol.2018.205211
Hernández-Boluda JC, Pereira A, Kröger N, Beelen D, Robin M, Bornhäuser M, et al. Determinants of survival in myelofibrosis patients undergoing allogeneic hematopoietic cell transplantation. Leukemia. 2021;35:215–24.
pubmed: 32286544
doi: 10.1038/s41375-020-0815-z
Atagunduz IK, Christopeit M, Ayuk F, Zeck G, Wolschke C, Kröger N. Incidence and outcome of late relapse after allogeneic stem cell transplantation for myelofibrosis. Biol Blood Marrow Transpl. 2020;26:2279–84.
doi: 10.1016/j.bbmt.2020.09.006
Kröger N, Holler E, Kobbe G, Bornhäuser M, Schwerdtfeger R, Baurmann H, et al. Allogeneic stem cell transplantation after reduced-intensity conditioning in patients with myelofibrosis: a prospective, multicenter study of the Chronic Leukemia Working Party of the European Group for Blood and Marrow Transplantation. Blood. 2009;114:5264–70.
pubmed: 19812383
doi: 10.1182/blood-2009-07-234880
Atagunduz IK, Klyuchnikov E, Wolschke C, Janson D, Heidenreich S, Christopeit M, et al. Treosulfan-based conditioning regimen for second allograft in patients with myelofibrosis. Cancers. 2020;12:3098.
pubmed: 33114179
pmcid: 7690833
doi: 10.3390/cancers12113098
Przepiorka D, Anderlini P, Saliba R, Cleary K, Mehra R, Khouri I, et al. Chronic graft-versus-host disease after allogeneic blood stem cell transplantation. Blood. 2001;98:1695–700.
pubmed: 11535499
doi: 10.1182/blood.V98.6.1695
Filipovich AH, Weisdorf D, Pavletic S, Socie G, Wingard JR, Lee SJ, et al. National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. Diagnosis and staging working group report. Biol Blood Marrow Transplant. 2005;11:945–56.
pubmed: 16338616
doi: 10.1016/j.bbmt.2005.09.004
Tefferi A, Barosi G, Mesa RA, Cervantes F, Deeg HJ, Reilly JT, et al. International Working Group (IWG) consensus criteria for treatment response in myelofibrosis with myeloid metaplasia, for the IWG for Myelofibrosis Research and Treatment (IWG-MRT). Blood. 2006;108:1497–503.
pubmed: 16675707
doi: 10.1182/blood-2006-03-009746
McLornan DP, Hernandez-Boluda JC, Czerw T, Cross N, Joachim Deeg H, Ditschkowski M, et al. Allogeneic haematopoietic cell transplantation for myelofibrosis: proposed definitions and management strategies for graft failure, poor graft function and relapse: best practice recommendations of the EBMT chronic malignancies working party. Leukemia. 2021;35:2445–59.
pubmed: 34040148
doi: 10.1038/s41375-021-01294-2
Gagelmann N, Wolschke C, Badbaran A, Janson D, Berger C, Klyuchnikov E, et al. donor lymphocyte infusion and molecular monitoring for relapsed myelofibrosis after hematopoietic cell transplantation. Hemasphere. 2023;7:e921.
pubmed: 37404772
pmcid: 10317484
doi: 10.1097/HS9.0000000000000921
Wolschke C, Badbaran A, Zabelina T, Christopeit M, Ayuk F, Triviai I, et al. Impact of molecular residual disease post allografting in myelofibrosis patients. Bone Marrow Transpl. 2017;52:1526–9.
doi: 10.1038/bmt.2017.157
Klyuchnikov E, Holler E, Bornhäuser M, Kobbe G, Nagler A, Shimoni A, et al. Donor lymphocyte infusions and second transplantation as salvage treatment for relapsed myelofibrosis after reduced-intensity allografting. Br J Haematol. 2012;159:172–81.
pubmed: 22909192
doi: 10.1111/bjh.12013
Park S-S, Jeon Y-W, Min GJ, Park S, Yahng SA, Yoon JH, et al. Graft-versus-host disease-free, relapse-free survival after allogeneic stem cell transplantation for myelodysplastic syndrome. Biol Blood Marrow Transpl. 2019;25:63–72.
doi: 10.1016/j.bbmt.2018.08.004
Battipaglia G, Ruggeri A, Labopin M, Volin L, Blaise D, Socié G, et al. Refined graft-versus-host disease/relapse-free survival in transplant from HLA-identical related or unrelated donors in acute myeloid leukemia. Bone Marrow Transpl. 2018;53:1295–303.
doi: 10.1038/s41409-018-0169-6
Gagelmann N, Badbaran A, Salit RB, Schroeder T, Gurnari C, Pagliuca S, et al. Impact of TP53 on outcome of patients with myelofibrosis undergoing hematopoietic stem cell transplantation. Blood. 2023;141:2901–11.
pubmed: 36940410
Gagelmann N, Wolschke C, Salit RB, Schroeder T, Ditschkowski M, Panagiota V, et al. Reduced intensity hematopoietic stem cell transplantation for accelerated-phase myelofibrosis. Blood Adv. 2022;6:1222–31.
pubmed: 35051996
pmcid: 8864646
doi: 10.1182/bloodadvances.2021006827
Ratanatharathorn V, Nash RA, Przepiorka D, Devine SM, Klein JL, Weisdorf D, et al. Phase III study comparing methotrexate and tacrolimus (prograf, FK506) with methotrexate and cyclosporine for graft-versus-host disease prophylaxis after HLA-identical sibling bone marrow transplantation. Blood. 1998;92:2303–14.
pubmed: 9746768
Penack O, Marchetti M, Ruutu T, Aljurf M, Bacigalupo A, Bonifazi F, et al. Prophylaxis and management of graft versus host disease after stem-cell transplantation for haematological malignancies: updated consensus recommendations of the European Society for Blood and Marrow Transplantation. Lancet Haematol. 2020;7:e157–e167.
pubmed: 32004485
doi: 10.1016/S2352-3026(19)30256-X
Robin M, Gras L, Gagelmann N, Koster L, Peffault de Latour R, Van Gorkom G, et al. Early hepatotoxicity in patients with myelofibrosis after allogeneic hematopoietic cell transplantation (Allo-HCT). Blood. 2022;140:7585–6.
doi: 10.1182/blood-2022-156076
Kröger N, Solano C, Wolschke C, Bandini G, Patriarca F, Pini M, et al. Antilymphocyte globulin for prevention of chronic graft-versus-host disease. N. Engl J Med. 2016;374:43–53.
pubmed: 26735993
doi: 10.1056/NEJMoa1506002
Rabischong B, Larraín D, Charpy C, Déchelotte PJ, Mage G. Extramedullary hematopoiesis and myeloid metaplasia of the ovaries and tubes in a patient with myelofibrosis: case report and concise review of the reported cases. J Clin Oncol. 2010;28:e511–2.
pubmed: 20697095
doi: 10.1200/JCO.2010.29.6442
Wanless IR, Peterson P, Das A, Boitnott JK, Moore GW, Bernier V. Hepatic vascular disease and portal hypertension in polycythemia vera and agnogenic myeloid metaplasia: a clinicopathological study of 145 patients examined at autopsy. Hepatology. 1990;12:1166–74.
pubmed: 2227815
doi: 10.1002/hep.1840120515
Gupta V, Malone AK, Hari PN, Ahn KW, Hu ZH, Gale RP, et al. Reduced-intensity hematopoietic cell transplantation for patients with primary myelofibrosis: a cohort analysis from the center for international blood and marrow transplant research. Biol Blood Marrow Transpl. 2014;20:89–97.
doi: 10.1016/j.bbmt.2013.10.018
Robin M, Chevret S, Koster L, Wolschke C, Yakoub-Agha I, Bourhis JH, et al. Antilymphocyte globulin for matched sibling donor transplantation in patients with myelofibrosis. Haematologica. 2019;104:1230–6.
pubmed: 30655365
pmcid: 6545844
doi: 10.3324/haematol.2018.201400
Finke J, Bethge WA, Schmoor C, Ottinger HD, Stelljes M, Zander AR, et al. Standard graft-versus-host disease prophylaxis with or without anti-T-cell globulin in haematopoietic cell transplantation from matched unrelated donors: a randomised, open-label, multicentre phase 3 trial. Lancet Oncol. 2009;10:855–64.
pubmed: 19695955
doi: 10.1016/S1470-2045(09)70225-6
Soiffer RJ, Kim HT, McGuirk J, Horwitz ME, Johnston L, Patnaik MM, et al. Prospective, randomized, double-blind, phase III clinical trial of anti-T-lymphocyte globulin to assess impact on chronic graft-versus-host disease-free survival in patients undergoing HLA-Matched unrelated myeloablative hematopoietic cell transplantation. J Clin Oncol. 2017;35:4003–11.
pubmed: 29040031
pmcid: 8462523
doi: 10.1200/JCO.2017.75.8177
Samuelson Bannow BT, Salit RB, Storer BE, Stevens EA, Wu D, Yeung C, et al. Hematopoietic cell transplantation for myelofibrosis: the dynamic international prognostic scoring system plus risk predicts post-transplant outcomes. Biol Blood Marrow Transpl. 2018;24:386–92.
doi: 10.1016/j.bbmt.2017.09.016
McLornan D, Eikema DJ, Czerw T, Kröger N, Koster L, Reinhardt HC, et al. Trends in allogeneic haematopoietic cell transplantation for myelofibrosis in Europe between 1995 and 2018: a CMWP of EBMT retrospective analysis. Bone Marrow Transpl. 2021;56:2160–72.
doi: 10.1038/s41409-021-01305-x
Kunte S, Rybicki L, Viswabandya A, Tamari R, Bashey A, Keyzner A, et al. Allogeneic blood or marrow transplantation with haploidentical donor and post-transplantation cyclophosphamide in patients with myelofibrosis: a multicenter study. Leukemia. 2022;36:856–64.
pubmed: 34663912
doi: 10.1038/s41375-021-01449-1
Gambella M, Bregante S, Raiola AM, Varaldo R, Ghiso A, Schiavetti I, et al. Haploidentical Hematopoietic Cell Transplantation for Myelofibrosis in the Ruxolitinib Era. Transpl Cell Ther. 2023;29:49.e1–49.e7.
doi: 10.1016/j.jtct.2022.10.015
Murthy GSG, Kim S, Estrada-Merly N, Abid MB, Aljurf M, Assal A, et al. Association between the choice of the conditioning regimen and outcomes of allogeneic hematopoietic cell transplantation for myelofibrosis. Haematologica. 2023;108:1900–8.
pubmed: 36779595
pmcid: 10316233
doi: 10.3324/haematol.2022.281958
McLornan D, Szydlo R, Koster L, Chalandon Y, Robin M, Wolschke C, et al. Myeloablative and reduced-intensity conditioned allogeneic hematopoietic stem cell transplantation in myelofibrosis: a retrospective study by the chronic malignancies working party of the European society for blood and marrow transplantation. Biol Blood Marrow Transpl. 2019;25:2167–71.
doi: 10.1016/j.bbmt.2019.06.034
Polverelli N, Mauff K, Kröger N, Robin M, Beelen D, Beauvais D, et al. Impact of spleen size and splenectomy on outcomes of allogeneic hematopoietic cell transplantation for myelofibrosis: a retrospective analysis by the chronic malignancies working party on behalf of European Society for Blood and Marrow Transplantation (EBMT). Am J Hematol 2021;96:69–79.
pubmed: 33064301
doi: 10.1002/ajh.26020
Bossard J-B, Beuscart J-B, Robin M, Mohty M, Barraco F, Chevallier P, et al. Splenectomy before allogeneic hematopoietic cell transplantation for myelofibrosis: A French nationwide study. Am J Hematol. 2021;96:80–8.
pubmed: 33108024
doi: 10.1002/ajh.26034
Gangat N, Guglielmelli P, Szuber N, Begna KH, Patnaik MM, Litzow MR, et al. Venetoclax with azacitidine or decitabine in blast-phase myeloproliferative neoplasm: A multicenter series of 32 consecutive cases. Am J Hematol. 2021;96:781–9.
pubmed: 33844862
pmcid: 8251544
doi: 10.1002/ajh.26186
Stübig T, Alchalby H, Ditschkowski M, Wolf D, Wulf G, Zabelina T, et al. JAK inhibition with ruxolitinib as pretreatment for allogeneic stem cell transplantation in primary or post-ET/PV myelofibrosis. Leukemia. 2014;28:1736–8.
pubmed: 24569777
doi: 10.1038/leu.2014.86
Gupta V, Kosiorek HE, Mead A, Klisovic RB, Galvin JP, Berenzon D, et al. Ruxolitinib therapy followed by reduced-intensity conditioning for hematopoietic cell transplantation for myelofibrosis: myeloproliferative disorders research consortium 114 Study. Biol Blood Marrow Transpl. 2019;25:256–64.
doi: 10.1016/j.bbmt.2018.09.001
Kröger N, Sbianchi G, Sirait T, Wolschke C, Beelen D, Passweg J, et al. Impact of prior JAK-inhibitor therapy with ruxolitinib on outcome after allogeneic hematopoietic stem cell transplantation for myelofibrosis: a study of the CMWP of EBMT. Leukemia. 2021;35:3551–60.
pubmed: 34023851
pmcid: 8632691
doi: 10.1038/s41375-021-01276-4
Maffioli M, Mora B, Ball S, Iurlo A, Elli EM, Finazzi MC, et al. A prognostic model to predict survival after 6 months of ruxolitinib in patients with myelofibrosis. Blood Adv. 2022;6:1855–64.
pubmed: 35130339
pmcid: 8941454
doi: 10.1182/bloodadvances.2021006889
Kröger N, Panagiota V, Badbaran A, Zabelina T, Triviai I, Araujo Cruz MM, et al. Impact of molecular genetics on outcome in myelofibrosis patients after allogeneic stem cell transplantation. Biol Blood Marrow Transpl. 2017;23:1095–101.
doi: 10.1016/j.bbmt.2017.03.034
Battipaglia G, Mauff K, Wendel L, Angelucci E, Mohty M, Arcese W, et al. Thiotepa-busulfan-fludarabine (TBF) conditioning regimen in patients undergoing allogeneic hematopoietic cell transplantation for myelofibrosis: an outcome analysis from the Chronic Malignancies working party of the EBMT. Bone Marrow Transpl. 2021;56:1593–602.
doi: 10.1038/s41409-021-01222-z
Iacobelli S, de Wreede LC. The EBMT handbook, Hematopoietic stem cell transplantation and cellular therapies. In Carreras E, Dufour C, Mohty M, Kröger N, editors. 7th ed. Leiden, Munich, Cham: Springer Open.; 2019. p 702.
Iwasaki M, Kanda J, Arai Y, Kondo T, Ishikawa T, Ueda Y, et al. Establishment of a predictive model for GVHD-free, relapse-free survival after allogeneic HSCT using ensemble learning. Blood Adv. 2022;6:2618–27.
pubmed: 34933327
pmcid: 9043925
doi: 10.1182/bloodadvances.2021005800