Combining blinatumomab and donor lymphocyte infusion in B-ALL patients relapsing after allogeneic hematopoietic cell transplantation: A study of the SFGM-TC
Chauvet, P.; Paviglianiti, A.; Labopin, M.et al.
2023 • In Bone Marrow Transplantation, 58, p. 72-79
Combining blinatumomab and donor lymphocyte infusion in B-ALL patients relapsing after allogeneic hematopoietic cell transplantation: A study of the SFGM-TC
Giebel S, Boumendil A, Labopin M, Seesaghur A, Baron F, Ciceri F, et al. Trends in the use of hematopoietic stem cell transplantation for adults with acute lymphoblastic leukemia in Europe: a report from the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation (EBMT). Ann Hematol. 2019;98:2389–98. DOI: 10.1007/s00277-019-03771-2
Roux C, Tifratene K, Socié G, Galambrun C, Bertrand Y, Rialland F, et al. Outcome after failure of allogeneic hematopoietic stem cell transplantation in children with acute leukemia: a study by the Société Francophone de Greffe de Moelle et de Thérapie Cellulaire (SFGM-TC). Bone Marrow Transplantation [Internet]. 2017 [cited 2020, 52. Available from: https://orbi.uliege.be/handle/2268/207119
Kuhlen M, Willasch AM, Dalle JH, Wachowiak J, Yaniv I, Ifversen M, et al. Outcome of relapse after allogeneic HSCT in children with ALL enrolled in the ALL-SCT 2003/2007 trial. Br J Haematol. 2018;180:82–9. DOI: 10.1111/bjh.14965
Desjonquères 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. DOI: 10.1038/bcj.2016.111
Spyridonidis A, Labopin M, Schmid C, Volin L, Yakoub-Agha I, Stadler M, et al. Outcomes and prognostic factors of adults with acute lymphoblastic leukemia who relapse after allogeneic hematopoietic cell transplantation. An analysis on behalf of the Acute Leukemia Working Party of EBMT. Leukemia 2012;26:1211–7. DOI: 10.1038/leu.2011.351
Poon LM, Hamdi A, Saliba R, Rondon G, Ledesma C, Kendrick M, et al. Outcomes of adults with acute lymphoblastic leukemia relapsing after allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transpl. 2013;19:1059–64. DOI: 10.1016/j.bbmt.2013.04.014
Liberio N, Robinson H, Nugent M, Simpson P, Margolis DA, Malarkannan S, et al. Single-center experience suggests donor lymphocyte infusion may promote long-term survival in children with high-risk acute lymphoblastic leukemia. Pediatr Blood Cancer. 2019;66:e27950. DOI: 10.1002/pbc.27950
Atra A, Millar B, Shepherd V, Shankar A, Wilson K, Treleaven J, et al. Donor lymphocyte infusion for childhood acute lymphoblastic leukaemia relapsing after bone marrow transplantation. Br J Haematol. 1997;97:165–8. DOI: 10.1046/j.1365-2141.1997.62650.x
Collins R Jr, Goldstein S, Giralt S, Levine J, Porter D, Drobyski W, et al. Donor leukocyte infusions in acute lymphocytic leukemia. Bone Marrow Transplant. 2000;26:511–6. DOI: 10.1038/sj.bmt.1702555
Choi SJ, Lee JH, Lee JH, Kim S, Lee YS, Seol M, et al. Treatment of relapsed acute lymphoblastic leukemia after allogeneic bone marrow transplantation with chemotherapy followed by G-CSF-primed donor leukocyte infusion: a prospective study. Bone Marrow Transpl. 2005;36:163–9. DOI: 10.1038/sj.bmt.1705024
El-Jurdi N, Reljic T, Kumar A, Pidala J, Bazarbachi A, Djulbegovic B, et al. Efficacy of adoptive immunotherapy with donor lymphocyte infusion in relapsed lymphoid malignancies. Immunotherapy 2013 ;5:457–66. DOI: 10.2217/imt.13.31
Scarisbrick JJ, Dignan FL, Tulpule S, Gupta ED, Kolade S, Shaw B, et al. A multicentre UK study of GVHD following DLI: Rates of GVHD are high but mortality from GVHD is infrequent. Bone Marrow Transpl. 2015;50:62–7. DOI: 10.1038/bmt.2014.227
Andreola G, Labopin M, Beelen D, Chevallier P, Tabrizi R, Bosi A, et al. Long-term outcome and prognostic factors of second allogeneic hematopoietic stem cell transplant for acute leukemia in patients with a median follow-up of ⩾10 years. Bone Marrow Transpl. 2015;50:1508–12. DOI: 10.1038/bmt.2015.193
Ortí G, Sanz J, García-Cadenas I, Sánchez-Ortega I, Alonso L, Jiménez MJ, et al. Analysis of relapse after transplantation in acute leukemia: A comparative on second allogeneic hematopoietic cell transplantation and donor lymphocyte infusions. Exp Hematol. 2018;62:24–32. DOI: 10.1016/j.exphem.2018.03.002
Kantarjian H, Stein A, Gökbuget 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. DOI: 10.1056/NEJMoa1609783
Stein AS, Kantarjian H, Gökbuget N, Bargou R, Litzow MR, Rambaldi A, et al. Blinatumomab for acute lymphoblastic leukemia relapse after allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transpl. 2019;25:1498–504. DOI: 10.1016/j.bbmt.2019.04.010
Ribera JM, Ferrer A, Ribera J, Genescà E. Profile of blinatumomab and its potential in the treatment of relapsed/refractory acute lymphoblastic leukemia. Onco Targets Ther. 2015;8:1567–74. DOI: 10.2147/OTT.S70524
Common Terminology Criteria for Adverse Events (CTCAE). 2017;155.
Przepiorka D, Weisdorf D, Martin P, Klingemann HG, Beatty P, Hows J, et al. 1994 Consensus Conference on Acute GVHD Grading. Bone Marrow Transpl. 1995;15:825–8.
Jagasia MH, Greinix HT, Arora M, Williams KM, Wolff D, Cowen EW, et al. National Institutes of Health Consensus Development Project on Criteria for Clinical Trials in Chronic Graft-versus-Host Disease: I. The 2014 Diagnosis and Staging Working Group Report. Biol Blood Marrow Transpl. 2015;21:389–401.e1. DOI: 10.1016/j.bbmt.2014.12.001
Locatelli F, Zugmaier G, Rizzari C, Morris JD, Gruhn B, Klingebiel T, et al. Effect of blinatumomab vs chemotherapy on event-free survival among children with high-risk first-relapse B-cell acute lymphoblastic leukemia: a randomized clinical trial. JAMA. 2021;325:843–54. DOI: 10.1001/jama.2021.0987
Dreier T, Lorenczewski G, Brandl C, Hoffmann P, Syring U, Hanakam F, et al. Extremely potent, rapid and costimulation-independent cytotoxic T-cell response against lymphoma cells catalyzed by a single-chain bispecific antibody. Int J Cancer. 2002;100:690–7. DOI: 10.1002/ijc.10557
Löffler A, Gruen M, Wuchter C, Schriever F, Kufer P, Dreier T, et al. Efficient elimination of chronic lymphocytic leukaemia B cells by autologous T cells with a bispecific anti-CD19/anti-CD3 single-chain antibody construct. Leukemia. 2003;17:900–9. DOI: 10.1038/sj.leu.2402890
Hoffmann P, Hofmeister R, Brischwein K, Brandl C, Crommer S, Bargou R, et al. Serial killing of tumor cells by cytotoxic T cells redirected with a CD19-/CD3-bispecific single-chain antibody construct. Int J Cancer. 2005;115:98–104. DOI: 10.1002/ijc.20908
Wei AH, Ribera JM, Larson RA, Ritchie D, Ghobadi A, Chen Y, et al. Biomarkers associated with blinatumomab outcomes in acute lymphoblastic leukemia. Leukemia. 2021;35:2220–31. DOI: 10.1038/s41375-020-01089-x
Parkman R, Cohen G, Carter SL, Weinberg KI, Masinsin B, Guinan E, et al. Successful immune reconstitution decreases leukemic relapse and improves survival in recipients of unrelated cord blood transplantation. Biol Blood Marrow Transpl. 2006;12:919–27. DOI: 10.1016/j.bbmt.2006.05.008
Minculescu L, Marquart HV, Ryder LP, Andersen NS, Schjoedt I, Friis LS, et al. Improved Overall Survival, Relapse-Free-Survival, and Less Graft-vs.-Host-Disease in Patients With High Immune Reconstitution of TCR Gamma Delta Cells 2 Months After Allogeneic Stem Cell Transplantation. Front Immunol [Internet]. 2019 [cited 2021 10. Available from: https://www.frontiersin.org/articles/10.3389/fimmu.2019.01997/full
Dekker L, de Koning C, Lindemans C, Nierkens S. Reconstitution of T Cell Subsets Following Allogeneic Hematopoietic Cell Transplantation. Cancers (Basel) [Internet]. 2020 Jul [cited 2021 Mar 2];12(7). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7409323/
Durer S, Durer C, Shafqat M, Comba IY, Malik S, Faridi W, et al. Concomitant use of blinatumomab and donor lymphocyte infusion for mixed-phenotype acute leukemia: a case report with literature review. Immunotherapy. 2019;11:373–8. DOI: 10.2217/imt-2018-0104
Ueda M, de Lima M, Caimi P, Tomlinson B, Little J, Creger R, et al. Concurrent blinatumomab and donor lymphocyte infusions for treatment of relapsed pre-B-cell ALL after allogeneic hematopoietic cell transplant. Bone Marrow Transpl. 2016;51:1253–5. DOI: 10.1038/bmt.2016.104
Papayannidis C, Sartor C, Dominietto A, Zappone E, Arpinati M, Marconi G, et al. Inotuzumab ozogamicin and donor lymphocyte infusion is a safe and promising combination in relapsed acute lymphoblastic leukemia after allogeneic stem cell transplant. Hematol Oncol. 2021;39:580–3. DOI: 10.1002/hon.2886
Portell CA, Wenzell CM, Advani AS. Clinical and pharmacologic aspects of blinatumomab in the treatment of B-cell acute lymphoblastic leukemia. Clin Pharmacol. 2013;5:5–11.
Topp MS, Kufer P, Gökbuget N, Goebeler M, Klinger M, Neumann S, et al. Targeted therapy with the T-cell-engaging antibody blinatumomab of chemotherapy-refractory minimal residual disease in B-lineage acute lymphoblastic leukemia patients results in high response rate and prolonged leukemia-free survival. J Clin Oncol. 2011;29:2493–8. DOI: 10.1200/JCO.2010.32.7270
Topp MS, Gökbuget N, Zugmaier G, Klappers P, Stelljes M, Neumann S, et al. Phase II trial of the anti-CD19 bispecific T cell-engager blinatumomab shows hematologic and molecular remissions in patients with relapsed or refractory B-precursor acute lymphoblastic leukemia. J Clin Oncol. 2014;32:4134–40. DOI: 10.1200/JCO.2014.56.3247
Topp MS, Gökbuget N, Stein AS, Zugmaier G, O’Brien S, Bargou RC, et al. Safety and activity of blinatumomab for adult patients with relapsed or refractory B-precursor acute lymphoblastic leukaemia: a multicentre, single-arm, phase 2 study. Lancet Oncol. 2015;16:57–66. DOI: 10.1016/S1470-2045(14)71170-2
Khan MW, Gul Z. Blinatumomab may induce graft versus host leukemia in patients with pre-B ALL relapsing after hematopoietic stem cell transplant. Clin Case Rep. 2016;4:743–6. DOI: 10.1002/ccr3.604
Maude SL, Frey N, Shaw PA, Aplenc R, Barrett DM, Bunin NJ, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N. Engl J Med. 2014;371:1507–17. DOI: 10.1056/NEJMoa1407222
Maude SL, Laetsch TW, Buechner J, Rives S, Boyer M, Bittencourt H, et al. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med. 2018;378:439–48. DOI: 10.1056/NEJMoa1709866
Shah BD, Ghobadi A, Oluwole OO, Logan AC, Boissel N, Cassaday RD, et al. KTE-X19 for relapsed or refractory adult B-cell acute lymphoblastic leukaemia: phase 2 results of the single-arm, open-label, multicentre ZUMA-3 study. Lancet. 2021;398:491–502. DOI: 10.1016/S0140-6736(21)01222-8
Neelapu SS, Tummala S, Kebriaei P, Wierda W, Gutierrez C, Locke FL, et al. Chimeric antigen receptor T-cell therapy—assessment and management of toxicities. Nat Rev Clin Oncol. 2018;15:47–62. DOI: 10.1038/nrclinonc.2017.148
Calmels B, Mfarrej B, Chabannon C. From clinical proof-of-concept to commercialization of CAR T cells. Drug Disco Today. 2018;23:758–62. DOI: 10.1016/j.drudis.2018.01.024
Assi R, Kantarjian H, Short NJ, Daver N, Takahashi K, Garcia-Manero G, et al. Safety and efficacy of blinatumomab in combination with a tyrosine kinase inhibitor for the treatment of relapsed Philadelphia chromosome-positive leukemia. Clin Lymphoma Myeloma Leuk. 2017;17:897–901. DOI: 10.1016/j.clml.2017.08.101
King AC, Pappacena JJ, Tallman MS, Park JH, Geyer MB. Blinatumomab administered concurrently with oral tyrosine kinase inhibitor therapy is a well-tolerated consolidation strategy and eradicates measurable residual disease in adults with Philadelphia chromosome positive acute lymphoblastic leukemia. Leuk Res. 2019;79:27–33. DOI: 10.1016/j.leukres.2019.02.009
Gaballa MR, Banerjee P, Milton DR, Jiang X, Ganesh C, Khazal S, et al. Blinatumomab maintenance after allogeneic hematopoietic cell transplantation for B-lineage acute lymphoblastic leukemia. Blood. 2022;139:1908–19. DOI: 10.1182/blood.2021013290
