Alternative donors provide comparable results to matched unrelated donors in patients with acute lymphoblastic leukemia undergoing allogeneic stem cell transplantation in second complete remission: a report from the EBMT Acute Leukemia Working Party.


Journal

Bone marrow transplantation
ISSN: 1476-5365
Titre abrégé: Bone Marrow Transplant
Pays: England
ID NLM: 8702459

Informations de publication

Date de publication:
09 2020
Historique:
received: 13 12 2019
accepted: 25 02 2020
revised: 23 02 2020
pubmed: 24 3 2020
medline: 22 6 2021
entrez: 24 3 2020
Statut: ppublish

Résumé

Relapse of acute lymphoblastic leukemia (ALL) remains a major therapeutic challenge. Despite the consensus for proceeding to allogeneic stem cell transplantation (HSCT) in relapsing patients with ALL who achieve second complete remission (CR2) with salvage therapy, most patients lack a suitable matched-related histocompatible donor. The present multicenter retrospective study compared, for ALL patients in CR2, the HSCT outcome from all four possible alternative hematopoietic stem cell sources, namely matched unrelated 10/10 (n = 281), mismatched unrelated 9/10 (n = 125), haploidentical (n = 105), and cord blood (n = 104) donors. The 2-year outcomes were not statistically different between the four donor sources with respect to overall survival (38.3-47.2%), leukemia-free survival (30.5-39.6%), relapse incidence (32.6-37.6%), nonrelapse mortality (27.5-34.6%), and graft-versus-host disease-free relapse survival (21.4-33.1%). Donor choices for ALL patients achieving CR2 post first relapse are broad, ensuring that most patient in need secures a graft. Therefore, in practice, the donor choice should depend on timely availability and policy center.

Identifiants

pubmed: 32203261
doi: 10.1038/s41409-020-0849-x
pii: 10.1038/s41409-020-0849-x
doi:

Types de publication

Journal Article Multicenter Study

Langues

eng

Sous-ensembles de citation

IM

Pagination

1763-1772

Références

Huguet F, Chevret S, Leguay T, Thomas X, Boissel N, Escoffre-Barbe M, et al. Intensified therapy of acute lymphoblastic leukemia in adults: report of the randomized GRAALL-2005 clinical trial. J Clin Oncol. 2018;36:2514–23.
pubmed: 29863974 doi: 10.1200/JCO.2017.76.8192
Jabbour E, O’Brien S, Konopleva M, Kantarjian H. New insights into the pathophysiology and therapy of adult acute lymphoblastic leukemia. Cancer. 2015;121:2517–28.
pubmed: 25891003 doi: 10.1002/cncr.29383
Fielding AK, Richards SM, Chopra R, Lazarus HM, Litzow MR, Buck G, et al. Outcome of 609 adults after relapse of acute lymphoblastic leukemia (ALL); an MRC UKALL12/ECOG 2993 study. Blood. 2007;109:944–50.
pubmed: 17032921 doi: 10.1182/blood-2006-05-018192
Forman SJ, Rowe JM. The myth of the second remission of acute leukemia in the adult. Blood. 2013;121:1077–82.
pubmed: 23243288 pmcid: 3575753 doi: 10.1182/blood-2012-08-234492
Maffini E, Lanza F, Saraceni F. Treatment of adult patients with relapsed/refractory B-cell philadelphia-negative acute lymphoblastic leukemia. Clin Hematol Int. 2019;1:85–93.
pubmed: 34595415 pmcid: 8432388
Desjonqueres A, Chevallier P, Thomas X, Huguet F, Leguay T, Bernard M, et al. Acute lymphoblastic leukemia relapsing after first-line pediatric-inspired therapy: a retrospective GRAALL study. Blood Cancer J. 2016;6:e504.
pubmed: 27935576 pmcid: 5223147 doi: 10.1038/bcj.2016.111
Ruggeri A, Labopin M, Ciceri F, Mohty M, Nagler A. Definition of GvHD-free, relapse-free survival for registry-based studies: an ALWP-EBMT analysis on patients with AML in remission. Bone Marrow Transplant. 2016;51:610–1.
pubmed: 26657834 doi: 10.1038/bmt.2015.305
Przepiorka D, Weisdorf D, Martin P, Klingemann HG, Beatty P, Hows J, et al. 1994 consensus conference on acute GVHD grading. Bone Marrow Transplant. 1995;15:825–8.
pubmed: 7581076
Lee SJ, Vogelsang G, Flowers ME. Chronic graft-versus-host disease. Biol Blood Marrow Transplant. 2003;9:215–33.
pubmed: 12720215 doi: 10.1053/bbmt.2003.50026
Glucksberg H, Storb R, Fefer A, Buckner CD, Neiman PE, Clift RA, et al. Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation. 1974;18:295–304.
pubmed: 4153799 doi: 10.1097/00007890-197410000-00001
Terwey TH, Vega-Ruiz A, Hemmati PG, Martus P, Dietz E, le Coutre P, et al. NIH-defined graft-versus-host disease after reduced intensity or myeloablative conditioning in patients with acute myeloid leukemia. Leukemia. 2012;26:536–42.
pubmed: 21869841 doi: 10.1038/leu.2011.230
Grimwade D, Hills RK, Moorman AV, Walker H, Chatters S, Goldstone AH, et al. Refinement of cytogenetic classification in acute myeloid leukemia: determination of prognostic significance of rare recurring chromosomal abnormalities among 5876 younger adult patients treated in the United Kingdom Medical Research Council trials. Blood. 2010;116:354–65.
pubmed: 20385793 doi: 10.1182/blood-2009-11-254441
Marks DI, Aversa F, Lazarus HM. Alternative donor transplants for adult acute lymphoblastic leukaemia: a comparison of the three major options. Bone Marrow Transplant. 2006;38:467–75.
pubmed: 16892073 doi: 10.1038/sj.bmt.1705464
Terakura S, Atsuta Y, Tsukada N, Kobayashi T, Tanaka M, Kanda J, et al. Comparison of outcomes of 8/8 and 7/8 allele-matched unrelated bone marrow transplantation and single-unit cord blood transplantation in adults with acute leukemia. Biol Blood Marrow Transplant. 2016;22:330–8.
pubmed: 26476205 doi: 10.1016/j.bbmt.2015.10.006
Han LJ, Wang Y, Fan ZP, Huang F, Zhou J, Fu YW, et al. Haploidentical transplantation compared with matched sibling and unrelated donor transplantation for adults with standard-risk acute lymphoblastic leukaemia in first complete remission. Br J Haematol. 2017;179:120–30.
pubmed: 28737249 doi: 10.1111/bjh.14854
Srour SA, Milton DR, Bashey A, Karduss-Urueta A, Al Malki MM, Romee R, et al. Haploidentical transplantation with post-transplantation cyclophosphamide for high-risk acute lymphoblastic leukemia. Biol Blood Marrow Transplant. 2017;23:318–24.
pubmed: 27856368 doi: 10.1016/j.bbmt.2016.11.008
Santoro N, Ruggeri A, Labopin M, Bacigalupo A, Ciceri F, Gulbas Z, et al. Unmanipulated haploidentical stem cell transplantation in adults with acute lymphoblastic leukemia: a study on behalf of the Acute Leukemia Working Party of the EBMT. J Hematol Oncol. 2017;10:113.
pubmed: 28558762 pmcid: 5450162 doi: 10.1186/s13045-017-0480-5
Gokbuget N, Kneba M, Raff T, Trautmann H, Bartram CR, Arnold R, et al. Adult patients with acute lymphoblastic leukemia and molecular failure display a poor prognosis and are candidates for stem cell transplantation and targeted therapies. Blood. 2012;120:1868–76.
pubmed: 22442346 doi: 10.1182/blood-2011-09-377713
Gokbuget N, Dombret H, Ribera JM, Fielding AK, Advani A, Bassan R, et al. International reference analysis of outcomes in adults with B-precursor Ph-negative relapsed/refractory acute lymphoblastic leukemia. Haematologica. 2016;101:1524–33.
pubmed: 27587380 pmcid: 5479605 doi: 10.3324/haematol.2016.144311
Simon R, Makuch RW. A non-parametric graphical representation of the relationship between survival and the occurrence of an event: application to responder versus non-responder bias. Stat Med. 1984;3:35–44.
pubmed: 6729287 doi: 10.1002/sim.4780030106
Pavlu J, Labopin M, Zoellner AK, Sakellari I, Stelljes M, Finke J, et al. Allogeneic hematopoietic cell transplantation for primary refractory acute lymphoblastic leukemia: a report from the Acute Leukemia Working Party of the EBMT. Cancer. 2017;123:1965–70.
pubmed: 28211939 doi: 10.1002/cncr.30604
Davies SM, Ramsay NK, Klein JP, Weisdorf DJ, Bolwell B, Cahn JY, et al. Comparison of preparative regimens in transplants for children with acute lymphoblastic leukemia. J Clin Oncol. 2000;18:340–7.
pubmed: 10637248 doi: 10.1200/JCO.2000.18.2.340
Eroglu C, Pala C, Kaynar L, Yaray K, Aksozen MT, Bankir M, et al. Comparison of total body irradiation plus cyclophosphamide with busulfan plus cyclophosphamide as conditioning regimens in patients with acute lymphoblastic leukemia undergoing allogeneic hematopoietic stem cell transplant. Leuk Lymphoma. 2013;54:2474–9.
pubmed: 23442062 doi: 10.3109/10428194.2013.779691
Cahu X, Labopin M, Giebel S, Aljurf M, Kyrcz-Krzemien S, Socie G, et al. Impact of conditioning with TBI in adult patients with T-cell ALL who receive a myeloablative allogeneic stem cell transplantation: a report from the acute leukemia working party of EBMT. Bone Marrow Transplant. 2016;51:351–7.
pubmed: 26618548 doi: 10.1038/bmt.2015.278
Giebel S, Labopin M, Socie G, Beelen D, Browne P, Volin L, et al. Improving results of allogeneic hematopoietic cell transplantation for adults with acute lymphoblastic leukemia in first complete remission: an analysis from the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation. Haematologica. 2017;102:139–49.
pubmed: 27686376 pmcid: 5210244 doi: 10.3324/haematol.2016.145631
Zhang H, Chen J, Que W. A meta-analysis of unrelated donor umbilical cord blood transplantation versus unrelated donor bone marrow transplantation in acute leukemia patients. Biol Blood Marrow Transplant. 2012;18:1164–73.
pubmed: 22289799 doi: 10.1016/j.bbmt.2012.01.015
Rocha V, Labopin M, Sanz G, Arcese W, Schwerdtfeger R, Bosi A, et al. Transplants of umbilical-cord blood or bone marrow from unrelated donors in adults with acute leukemia. N. Engl J Med. 2004;351:2276–85.
pubmed: 15564544 doi: 10.1056/NEJMoa041469
Eapen M, Rocha V, Sanz G, Scaradavou A, Zhang MJ, Arcese W, et al. Effect of graft source on unrelated donor haemopoietic stem-cell transplantation in adults with acute leukaemia: a retrospective analysis. Lancet Oncol. 2010;11:653–60.
pubmed: 20558104 pmcid: 3163510 doi: 10.1016/S1470-2045(10)70127-3
Passweg JR, Baldomero H, Bader P, Bonini C, Duarte RF, Dufour C, et al. Use of haploidentical stem cell transplantation continues to increase: the 2015 European Society for Blood and Marrow Transplant activity survey report. Bone Marrow Transplant. 2017;52:811–7.
pubmed: 28287639 pmcid: 5467246 doi: 10.1038/bmt.2017.34
Gokbuget N, Stanze D, Beck J, Diedrich H, Horst HA, Huttmann A, et al. Outcome of relapsed adult lymphoblastic leukemia depends on response to salvage chemotherapy, prognostic factors, and performance of stem cell transplantation. Blood. 2012;120:2032–41.
pubmed: 22493293 doi: 10.1182/blood-2011-12-399287
O’Brien S, Thomas D, Ravandi F, Faderl S, Cortes J, Borthakur G, et al. Outcome of adults with acute lymphocytic leukemia after second salvage therapy. Cancer. 2008;113:3186–91.
pubmed: 18846563 doi: 10.1002/cncr.23919
Oriol A, Vives S, Hernandez-Rivas JM, Tormo M, Heras I, Rivas C, et al. Outcome after relapse of acute lymphoblastic leukemia in adult patients included in four consecutive risk-adapted trials by the PETHEMA Study Group. Haematologica. 2010;95:589–96.
pubmed: 20145276 pmcid: 2857188 doi: 10.3324/haematol.2009.014274
Kantarjian HM, Thomas D, Ravandi F, Faderl S, Jabbour E, Garcia-Manero G, et al. Defining the course and prognosis of adults with acute lymphocytic leukemia in first salvage after induction failure or short first remission duration. Cancer. 2010;116:5568–74.
pubmed: 20737576 doi: 10.1002/cncr.25354
Thomas DA, Kantarjian H, Smith TL, Koller C, Cortes J, O’Brien S, et al. Primary refractory and relapsed adult acute lymphoblastic leukemia: characteristics, treatment results, and prognosis with salvage therapy. Cancer. 1999;86:1216–30.
pubmed: 10506707 doi: 10.1002/(SICI)1097-0142(19991001)86:7<1216::AID-CNCR17>3.0.CO;2-O
Mullighan CG. The molecular genetic makeup of acute lymphoblastic leukemia. Hematol Am Soc Hematol Educ Program. 2012;2012:389–96.
doi: 10.1182/asheducation.V2012.1.389.3798360
Mullighan CG. Molecular genetics of B-precursor acute lymphoblastic leukemia. J Clin Investig. 2012;122:3407–15.
pubmed: 23023711 pmcid: 3461902 doi: 10.1172/JCI61203
Choi S, Henderson MJ, Kwan E, Beesley AH, Sutton R, Bahar AY, et al. Relapse in children with acute lymphoblastic leukemia involving selection of a preexisting drug-resistant subclone. Blood. 2007;110:632–9.
pubmed: 17371950 doi: 10.1182/blood-2007-01-067785
Kanakry CG, Fuchs EJ, Luznik L. Modern approaches to HLA-haploidentical blood or marrow transplantation. Nat Rev Clin Oncol. 2016;13:132.
pubmed: 26718103 doi: 10.1038/nrclinonc.2015.234
Kantarjian HM, DeAngelo DJ, Stelljes M, Martinelli G, Liedtke M, Stock W, et al. Inotuzumab ozogamicin versus standard therapy for acute lymphoblastic leukemia. N Engl J Med. 2016;375:740–53.
pubmed: 27292104 pmcid: 5594743 doi: 10.1056/NEJMoa1509277
Kantarjian H, Stein A, Gokbuget N, Fielding AK, Schuh AC, Ribera JM, et al. Blinatumomab versus chemotherapy for advanced acute lymphoblastic leukemia. N. Engl J Med. 2017;376:836–47.
pubmed: 28249141 pmcid: 5881572 doi: 10.1056/NEJMoa1609783
Kantarjian HM, DeAngelo DJ, Stelljes M, Liedtke M, Stock W, Gokbuget N, et al. Inotuzumab ozogamicin versus standard of care in relapsed or refractory acute lymphoblastic leukemia: final report and long-term survival follow-up from the randomized, phase 3 INO-VATE study. Cancer. 2019;125:2474–87.
pubmed: 30920645 doi: 10.1002/cncr.32116
Marks DI, Kebriaei P, Stelljes M, Gokbuget N, Kantarjian H, Advani AS, et al. Outcomes of allogeneic stem cell transplantation after inotuzumab ozogamicin treatment for relapsed or refractory acute lymphoblastic leukemia. Biol Blood Marrow Transplant. 2019;25:1720–9.
pubmed: 31039409 doi: 10.1016/j.bbmt.2019.04.020
Yeshurun M, Weisdorf D, Rowe JM, Tallman MS, Zhang MJ, Wang HL, et al. The impact of the graft-versus-leukemia effect on survival in acute lymphoblastic leukemia. Blood Adv. 2019;3:670–80.
pubmed: 30808685 pmcid: 6391668 doi: 10.1182/bloodadvances.2018027003

Auteurs

Eolia Brissot (E)

Sorbonne University, service d'Hématologie Clinique et de Thérapie Cellulaire, Hôpital Saint Antoine, APHP, INSERM U938 centre de Recherche Saint-Antoine, Paris, France. Eolia.brissot@gmail.com.
Acute Leukemia Working Party office, Hôpital Saint Antoine, APHP, Paris, France. Eolia.brissot@gmail.com.

Myriam Labopin (M)

Sorbonne University, service d'Hématologie Clinique et de Thérapie Cellulaire, Hôpital Saint Antoine, APHP, INSERM U938 centre de Recherche Saint-Antoine, Paris, France.
Acute Leukemia Working Party office, Hôpital Saint Antoine, APHP, Paris, France.

Domenico Russo (D)

Unit of Blood Disease and Stem Cell Transplantation, DPT of Medical and Experimental Sciences, Brescia University, ASST Spedali Civili di Brescia, Brescia, Italy.

Sonja Martin (S)

Robert-Bosch-Krankenhaus, Abt. Hämatologie/Onkologie, Stuttgart, Germany.

Christoph Schmid (C)

Universitaets-Klinikum Augsburg, II Medizinische Klinik, Augsburg, Germany.

Bertram Glass (B)

Department of Haematology, Asklepios Klinik St. Georg, Hamburg, Germany.

Ron Ram (R)

Tel Aviv Sourasky Medical Center, Blood and Bone Marrow Transplantation, Tel Aviv, Israel.

Zubeyde Nur Ozkurt (ZN)

Gazi University Faculty of Medicine, Hematology, Ankara, Turkey.

Jakob Passweg (J)

University Hospital, Hematology, Basel, Switzerland.

Joan Hendrik Veelken (JH)

Leiden University Hospital, BMT Centre Leiden, Leiden, The Netherlands.

Donald Bunjes (D)

Klinik fuer Innere Medizin III, Universtätklinikum, Ulm, Germany.

Jane Apperley (J)

Department of Haematology, Imperial College, Hammersmith Hospital, London, UK.

Sebastian Giebel (S)

Department of Bone Marrow Transplantation, Branch Gliwice, Comprehensive Cancer Center M. Sklodowska-Curie Memorial Institute, Gliwice, Poland.

Mohamad Mohty (M)

Sorbonne University, service d'Hématologie Clinique et de Thérapie Cellulaire, Hôpital Saint Antoine, APHP, INSERM U938 centre de Recherche Saint-Antoine, Paris, France.
Acute Leukemia Working Party office, Hôpital Saint Antoine, APHP, Paris, France.

Arnon Nagler (A)

Acute Leukemia Working Party office, Hôpital Saint Antoine, APHP, Paris, France.
Chaim Sheba Medical Center, Tel Hashomer, Ramat Gan, Israel.

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