Evaluation of six different types of sequential conditioning regimens for allogeneic stem cell transplantation in relapsed/refractory acute myelogenous leukemia – a study of the Acute Leukemia Working Party of the EBMT

References

• Thol F, Schlenk RF, Heuser M, et al. How I treat refractory and early relapsed acute myeloid leukemia. Blood. 2015;126:319–327.
   PubMed Web of Science ®Google Scholar
• Duval M, Klein JP, He W, et al. Hematopoietic stem-cell transplantation for acute leukemia in relapse or primary induction failure. J Clin Oncol. 2010;28:3730–3738.
   PubMed Web of Science ®Google Scholar
• Nagler A, Savani BN, Labopin M, et al. Outcomes after use of two standard ablative regimens in patients with refractory acute myeloid leukaemia: a retrospective, multicentre, registry analysis. Lancet Haematol. 2015;2:e384–e392.
   PubMed Web of Science ®Google Scholar
• Gyurkocza B, Lazarus HM, Giralt S. Allogeneic hematopoietic cell transplantation in patients with AML not achieving remission: potentially curative therapy. Bone Marrow Transplant. 2017;52:1083–1090.
   PubMedGoogle Scholar
• Shimoni A, Hardan I, Shem-Tov N, et al. Allogeneic hematopoietic stem-cell transplantation in AML and MDS using myeloablative versus reduced-intensity conditioning: the role of dose intensity. Leukemia. 2006;20(2):322–328.
   PubMed Web of Science ®Google Scholar
• Gyurkocza B, Storb R, Storer BE, et al. Nonmyeloablative allogeneic hematopoietic cell transplantation in patients with acute myeloid leukemia. J Clin Oncol. 2010;28:2859–2867.
   PubMed Web of Science ®Google Scholar
• Schmid C, Schleuning M, Ledderose G, et al. Sequential regimen of chemotherapy, reduced-intensity conditioning for allogeneic stem-cell transplantation, and prophylactic donor lymphocyte transfusion in high-risk acute myeloid leukemia and myelodysplastic syndrome. J Clin Oncol. 2005;23:5675–5687.
   PubMed Web of Science ®Google Scholar
• Schmid C, Schleuning M, Schwerdtfeger R, et al. Long-term survival in refractory acute myeloid leukemia after sequential treatment with chemotherapy and reduced-intensity conditioning for allogeneic stem cell transplantation. Blood. 2006;108:1092–1099.
   PubMed Web of Science ®Google Scholar
• Ringdén O, Labopin M, Schmid C, et al. Sequential chemotherapy followed by reduced-intensity conditioning and allogeneic haematopoietic stem cell transplantation in adult patients with relapse or refractory acute myeloid leukaemia: a survey from the Acute Leukaemia Working Party of EBMT. Br J Haematol. 2017;176:431–439.
   PubMed Web of Science ®Google Scholar
• Schmid C, Schleuning M, Hentrich M, et al. High antileukemic efficacy of an intermediate intensity conditioning regimen for allogeneic stem cell transplantation in patients with high-risk acute myeloid leukemia in first complete remission. Bone Marrow Transplant. 2008;41(8):721–727.
   PubMed Web of Science ®Google Scholar
• Malard F, Labopin M, Stuhler G, et al. Sequential intensified conditioning regimen allogeneic hematopoietic stem cell transplantation in adult patients with intermediate- or high-risk acute myeloid leukemia in complete remission: a study from the Acute Leukemia Working Party of the European Group for Blood and Marrow Transplantation. Biol Blood Marrow Transplant. 2017;23:278–284.
   PubMedGoogle Scholar
• Heinicke T, Labopin M, Schmid C, et al. Reduced relapse incidence with FLAMSA-RIC compared with busulfan/fludarabine for acute myelogenous leukemia patients in first or second complete remission: a study from the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation. Biol Blood Marrow Transplant. 2018;24(11):2224–2232.
   PubMed Web of Science ®Google Scholar
• Sheth V, Labopin M, Canaani J, et al. Comparison of FLAMSA-based reduced intensity conditioning with treosulfan/fludarabine conditioning for patients with acute myeloid leukemia: an ALWP/EBMT analysis. Bone Marrow Transplant. 2019;54(4):531–539.
   PubMed Web of Science ®Google Scholar
• Buchholz S, Dammann E, Stadler M, et al. Cytoreductive treatment with clofarabine/ara-C combined with reduced-intensity conditioning and allogeneic stem cell transplantation in patients with high-risk, relapsed, or refractory acute myeloid leukemia and advanced myelodysplastic syndrome. Eur J Haematol. 2012;88:52–60.
   PubMed Web of Science ®Google Scholar
• Chemnitz JM, von Lilienfeld-Toal M, Holtick U, et al. Intermediate intensity conditioning regimen containing FLAMSA, treosulfan, cyclophosphamide, and ATG for allogeneic stem cell transplantation in elderly patients with relapsed or high-risk acute myeloid leukemia. Ann Hematol. 2012;91:47–55.
   PubMed Web of Science ®Google Scholar
• Tischer J, Stemmler HJ, Engel N, et al. Feasibility of clofarabine cytoreduction followed by haploidentical hematopoietic stem cell transplantation in patients with relapsed or refractory advanced acute leukemia. Ann Hematol. 2013;92(10):1379–1388.
   PubMed Web of Science ®Google Scholar
• Tang W, Fan X, Wang L, et al. Busulfan and fludarabine conditioning regimen given at hematological nadir of cytoreduction fludarabine, cytarabine, and idarubicin chemotherapy in patients with refractory acute myeloid leukemia undergoing allogeneic stem cell transplantation: a single arm pilot consort study. Medicine (Baltimore). 2015;94:e706.
   PubMed Web of Science ®Google Scholar
• Xuan L, Fan Z, Zhang Y, et al. Sequential intensified conditioning followed by prophylactic DLI could reduce relapse of refractory acute leukemia after allo-HSCT. Oncotarget. 2016;7(22):32579–32591.
   PubMedGoogle Scholar
• Mohty M, Malard F, Blaise D, et al. Sequential regimen of clofarabine, cytosine arabinoside and reduced-intensity conditioned transplantation for primary refractory acute myeloid leukemia. Haematologica. 2017;102(1):184–191.
   PubMed Web of Science ®Google Scholar
• Davies JK, Hassan S, Sarker S-J, et al. Durable graft-versus-leukaemia effects without donor lymphocyte infusions – results of a phase II study of sequential T-replete allogeneic transplantation for high-risk acute myeloid leukaemia and myelodysplasia. Br J Haematol. 2018;180(3):346–355.
   PubMed Web of Science ®Google Scholar
• Fraccaroli A, Prevalsek D, Fritsch S, et al. Sequential HLA-haploidentical transplantation utilizing post-transplantation cyclophosphamide for GvHD prophylaxis in high-risk and relapsed/refractory AML/MDS. Am J Hematol. 2018;93(12):1524–1531.
   PubMed Web of Science ®Google Scholar
• Wang L, Devillier R, Wan M, et al. Clinical outcome of FLAG-IDA chemotherapy sequential with Flu–Bu3 conditioning regimen in patients with refractory AML: a parallel study from Shanghai Institute of Hematology and Institut Paoli-Calmettes. Bone Marrow Transplant. 2019;54(3):458–464.
   PubMed Web of Science ®Google Scholar
• Steckel NK, Groth C, Mikesch J-H, et al. High-dose melphalan-based sequential conditioning chemotherapy followed by allogeneic haematopoietic stem cell transplantation in adult patients with relapsed or refractory acute myeloid leukaemia. Br J Haematol. 2018;180(6):840–853.
   PubMed Web of Science ®Google Scholar
• Duléry R, Ménard A-L, Chantepie S, et al. Sequential conditioning with thiotepa in T cell-replete hematopoietic stem cell transplantation for the treatment of refractory hematologic malignancies: comparison with matched related, haplo-mismatched, and unrelated donors. Biol. Blood Marrow Transplant. 2018;24(5):1013–1021.
   PubMed Web of Science ®Google Scholar
• Xiao H, Li L, Pang Y, et al. Sequential treatment combining cladribine-based re-induction, myeloablative allogeneic HSCT, and prophylactic donor lymphocyte infusion: a promising treatment for refractory acute myeloid leukemia. Ann Hematol. 2018;97:2479–2490.
   PubMed Web of Science ®Google Scholar
• Spyridonidis A, Labopin M, Savani BN, et al. Redefining and measuring transplant conditioning intensity in current era: a study in acute myeloid leukemia patients. Bone Marrow Transplant. 2020;55(6):1114–1112.
   PubMed Web of Science ®Google Scholar
• 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. Blood. 1998;92(7):2322–2333.
   PubMed Web of Science ®Google Scholar
• Glucksberg H, Storb R, Fefer A, et al. Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation. 1974;18(4):295–304.
   PubMed Web of Science ®Google Scholar
• Filipovich A, Weisdorf D, Pavletic S, 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(12):945–956.
   PubMed Web of Science ®Google Scholar
• Ruggeri A, Labopin M, Ciceri F, et al. 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(4):610–611.
   PubMed Web of Science ®Google Scholar
• Kanate AS, Nagler A, Savani B. Summary of scientific and statistical methods, study endpoints and definitions for observational and registry-based studies in hematopoietic cell transplantation. Clin Hematol Int. 2019;2:2–4.
   Google Scholar
• Bertz H, Potthoff K, Finke J. Allogeneic stem-cell transplantation from related and unrelated donors in older patients with myeloid leukemia. J Clin Oncol. 2003;21(8):1480–1484.
   PubMed Web of Science ®Google Scholar
• Bug G, Atta J, Klein SA, et al. High-dose melphalan is an effective salvage therapy in acute myeloid leukaemia patients with refractory relapse and relapse after autologous stem cell transplantation. Ann Hematol. 2005;84(11):748–754.
   PubMed Web of Science ®Google Scholar
• Shimoni A, Hardan I, Shem-Tov N, et al. Comparison between two fludarabine-based reduced-intensity conditioning regimens before allogeneic hematopoietic stem-cell transplantation: fludarabine/melphalan is associated with higher incidence of acute graft-versus-host disease and non-relapse mortality and lower incidence of relapse than fludarabine/busulfan. Leukemia. 2007;21(10):2109–2116.
   PubMed Web of Science ®Google Scholar
• Baron F, Labopin M, Peniket A, et al. Reduced-intensity conditioning with fludarabine and busulfan versus fludarabine and melphalan for patients with acute myeloid leukemia: a report from the Acute Leukemia Working Party of the European Group for Blood and Marrow Transplantation. Cancer. 2015;121:1048–1055.
   PubMed Web of Science ®Google Scholar
• Holtick U, Herling M, Pflug N, et al. Similar outcome after allogeneic stem cell transplantation with a modified FLAMSA conditioning protocol substituting 4 Gy TBI with treosulfan in an elderly population with high-risk AML. Ann Hematol. 2017;96(3):479–487.
   PubMed Web of Science ®Google Scholar
• Faderl S, Ferrajoli A, Wierda W, et al. Clofarabine combinations as acute myeloid leukemia salvage therapy. Cancer. 2008;113(8):2090–2096.
   PubMed Web of Science ®Google Scholar
• Middeke JM, Herbst R, Parmentier S, et al. Clofarabine salvage therapy before allogeneic hematopoietic stem cell transplantation in patients with relapsed or refractory AML: results of the BRIDGE trial. Leukemia. 2016;30:261–267.
   PubMed Web of Science ®Google Scholar
• Saraceni F, Labopin M, Brecht A, et al. Fludarabine-treosulfan compared to thiotepa-busulfan-fludarabine or FLAMSA as conditioning regimen for patients with primary refractory or relapsed acute myeloid leukemia: a study from the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation (EBMT). J Hematol Oncol. 2019;12:44.
   PubMed Web of Science ®Google Scholar
• Decroocq J, Itzykson R, Vigouroux S, et al. Similar outcome of allogeneic stem cell transplantation after myeloablative and sequential conditioning regimen in patients with refractory or relapsed acute myeloid leukemia: a study from the Société Francophone de Greffe de Moelle et de Thérapie Cellula. Am J Hematol. 2018;93(3):416–423.
   PubMed Web of Science ®Google Scholar
• Burchert A, Bug G, Finke J, et al. Sorafenib as maintenance therapy post allogeneic stem cell transplantation for FLT3-ITD positive AML: results from the Randomized, Double-Blind, Placebo-Controlled Multicentre Sormain Trial. Blood. 2018;132(Suppl. 1):661–661.
   Google Scholar
• Bazarbachi A, Labopin M, Battipaglia G, et al. Allogeneic stem cell transplantation for FLT3-mutated acute myeloid leukemia: in vivo T-cell depletion and posttransplant sorafenib maintenance improve survival. A Retrospective Acute Leukemia Working Party-European Society for Blood and Marrow Transplant Study. Clin Hematol Int. 2019;1(1):58.
   Google Scholar
• Bug G, Burchert A, Wagner E-M, et al. Phase I/II study of the deacetylase inhibitor panobinostat after allogeneic stem cell transplantation in patients with high-risk MDS or AML (PANOBEST trial). Leukemia. 2017;31:2523–2525.
   PubMed Web of Science ®Google Scholar