Outcome of T-cell-replete haploidentical stem cell transplantation improves with time in adults with acute lymphoblastic leukemia: A study from the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation.


Journal

Cancer
ISSN: 1097-0142
Titre abrégé: Cancer
Pays: United States
ID NLM: 0374236

Informations de publication

Date de publication:
15 07 2021
Historique:
revised: 31 01 2021
received: 15 10 2020
accepted: 11 02 2021
pubmed: 20 3 2021
medline: 8 3 2022
entrez: 19 3 2021
Statut: ppublish

Résumé

The use of haploidentical hematopoietic cell transplantation (haplo-HCT) with posttransplantation cyclophosphamide prophylaxis is gaining traction in patients with acute lymphoblastic leukemia (ALL). The Acute Leukemia Working Party/European Society for Blood and Marrow Transplantation registry was used to evaluate the outcomes of adult patients with ALL who underwent haplo-HCT during 2011 through 2015 and compared them with the outcomes of those who underwent transplantation during 2016 through 2018. The analysis consisted of 195 patients, including 79 who underwent transplantation during 2011 through 2015 and 116 who underwent transplantation during 2016 through 2018. Overall, the 2-year leukemia-free survival and relapse incidence rates were 56.5% and 21%, respectively. The 100-day incidence of grade 2 through 4 acute graft-vs-host disease (GVHD) was 34.5%. The rates of nonrelapse mortality (NRM) and overall survival (OS) were 22.5% and 64.7%, respectively. Patients who underwent transplantation during 2016 through 2018 experienced improved rates of leukemia-free survival (64.9% vs 47.3%; P = .019) and OS (75.5% vs 53.5%; P = .006). Patients who underwent transplantation during 2016 through 2018 developed more grade 2 through 4 acute GVHD (42% vs 26.4%; P = .047). The incidence of relapse, GVHD-free/relapse-free survival, grade 3 and 4 acute GVHD, chronic GVHD, and extensive chronic GVHD did not differ significantly between groups. In multivariate analysis, more recently transplanted patients had a significantly reduced risk of NRM (hazard ratio, 0.44; 95% CI, 0.22-0.89; P = .022) and improved OS (hazard ratio, 0.47; 95% CI, 0.26-0.86; P = .014). A comparable analysis of patients who had acute myeloid leukemia during the same timeframes did not reveal any statistically significant differences in any outcomes. The outcome of adult patients with ALL who receive posttransplant cyclophosphamide has improved over time, with an impressive 2-year OS of 75% and, most recently, an NRM rate of only 17%.

Sections du résumé

BACKGROUND
The use of haploidentical hematopoietic cell transplantation (haplo-HCT) with posttransplantation cyclophosphamide prophylaxis is gaining traction in patients with acute lymphoblastic leukemia (ALL).
METHODS
The Acute Leukemia Working Party/European Society for Blood and Marrow Transplantation registry was used to evaluate the outcomes of adult patients with ALL who underwent haplo-HCT during 2011 through 2015 and compared them with the outcomes of those who underwent transplantation during 2016 through 2018.
RESULTS
The analysis consisted of 195 patients, including 79 who underwent transplantation during 2011 through 2015 and 116 who underwent transplantation during 2016 through 2018. Overall, the 2-year leukemia-free survival and relapse incidence rates were 56.5% and 21%, respectively. The 100-day incidence of grade 2 through 4 acute graft-vs-host disease (GVHD) was 34.5%. The rates of nonrelapse mortality (NRM) and overall survival (OS) were 22.5% and 64.7%, respectively. Patients who underwent transplantation during 2016 through 2018 experienced improved rates of leukemia-free survival (64.9% vs 47.3%; P = .019) and OS (75.5% vs 53.5%; P = .006). Patients who underwent transplantation during 2016 through 2018 developed more grade 2 through 4 acute GVHD (42% vs 26.4%; P = .047). The incidence of relapse, GVHD-free/relapse-free survival, grade 3 and 4 acute GVHD, chronic GVHD, and extensive chronic GVHD did not differ significantly between groups. In multivariate analysis, more recently transplanted patients had a significantly reduced risk of NRM (hazard ratio, 0.44; 95% CI, 0.22-0.89; P = .022) and improved OS (hazard ratio, 0.47; 95% CI, 0.26-0.86; P = .014). A comparable analysis of patients who had acute myeloid leukemia during the same timeframes did not reveal any statistically significant differences in any outcomes.
CONCLUSIONS
The outcome of adult patients with ALL who receive posttransplant cyclophosphamide has improved over time, with an impressive 2-year OS of 75% and, most recently, an NRM rate of only 17%.

Identifiants

pubmed: 33739471
doi: 10.1002/cncr.33522
doi:

Substances chimiques

Cyclophosphamide 8N3DW7272P

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2507-2514

Informations de copyright

© 2021 American Cancer Society.

Références

Passweg JR, Baldomero H, Bader P, 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;52:811-817.
Shouval R, Fein JA, Labopin M, 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-e584.
Gragert L, Eapen M, Williams E, et al. HLA match likelihoods for hematopoietic stem-cell grafts in the U.S. registry. N Engl J Med. 2014;371:339-348.
Bashey A, Zhang X, Sizemore CA, et al. T-cell-replete HLA-haploidentical hematopoietic transplantation for hematologic malignancies using post-transplantation cyclophosphamide results in outcomes equivalent to those of contemporaneous HLA-matched related and unrelated donor transplantation. J Clin Oncol. 2013;31:1310-1316.
Ciurea SO, Zhang MJ, Bacigalupo AA, et al. Haploidentical transplant with posttransplant cyclophosphamide vs matched unrelated donor transplant for acute myeloid leukemia. Blood. 2015;126:1033-1040.
Bittencourt MCB, Ciurea SO. Recent advances in allogeneic hematopoietic stem cell transplantation for acute myeloid leukemia. Biol Blood Marrow Transplant. 2020;26:e215-e221.
Shem-Tov N, Peczynski C, Labopin M, et al. Haploidentical vs. unrelated allogeneic stem cell transplantation for acute lymphoblastic leukemia in first complete remission: on behalf of the ALWP of the EBMT. Leukemia. 2020;34:283-292.
Al Malki MM, Yang D, Labopin M, et al. Comparing transplant outcomes in ALL patients after haploidentical with PTCy or matched unrelated donor transplantation. Blood Adv. 2020;4:2073-2083.
Nagler A, Dholaria B, Labopin M, et al. Bone marrow versus mobilized peripheral blood stem cell graft in T-cell-replete haploidentical transplantation in acute lymphoblastic leukemia. Leukemia. 2020;34:2766-2775.
Wang Y, Liu DH, Liu KY, et al. Long-term follow-up of haploidentical hematopoietic stem cell transplantation without in vitro T cell depletion for the treatment of leukemia: nine years of experience at a single center. Cancer. 2013;119:978-985.
Wang Y, Liu QF, Xu LP, et al. Haploidentical versus matched-sibling transplant in adults with Philadelphia-negative high-risk acute lymphoblastic leukemia: a biologically phase III randomized study. Clin Cancer Res. 2016;22:3467-3476.
Gooley TA, Chien JW, Pergam SA, et al. Reduced mortality after allogeneic hematopoietic-cell transplantation. N Engl J Med. 2010;363:2091-2101.
Wood WA, Lee SJ, Brazauskas R, et al. Survival improvements in adolescents and young adults after myeloablative allogeneic transplantation for acute lymphoblastic leukemia. Biol Blood Marrow Transplant. 2014;20:829-836.
Brissot E, Labopin M, Beckers MM, et al. Tyrosine kinase inhibitors improve long-term outcome of allogeneic hematopoietic stem cell transplantation for adult patients with Philadelphia chromosome positive acute lymphoblastic leukemia. Haematologica. 2015;100:392-399.
Giebel S, Labopin M, Socie G, 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;102:139-149.
D'Souza A, Fretham C, Lee SJ, et al. Current use of and trends in hematopoietic cell transplantation in the United States. Biol Blood Marrow Transplant. 2020;26:e177-e182.
Srour SA, Milton DR, Bashey A, et al. Haploidentical transplantation with post-transplantation cyclophosphamide for high-risk acute lymphoblastic leukemia. Biol Blood Marrow Transplant. 2017;23:318-324.
Santoro N, Ruggeri A, Labopin M, 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.
Nagler A, Kanate AS, Labopin M, et al. Post-transplant cyclophosphamide versus anti-thymocyte globulin for graft-versus-host disease prevention in haploidentical transplantation for adult acute lymphoblastic leukemia. Haematologica. Published online April 30, 2020. doi:10.3324/haematol.2020.247296
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;51:610-611.
Aoudjhane M, Labopin M, Gorin NC, et al. Comparative outcome of reduced intensity and myeloablative conditioning regimen in HLA identical sibling allogeneic haematopoietic stem cell transplantation for patients older than 50 years of age with acute myeloblastic leukaemia: a retrospective survey from the Acute Leukemia Working Party (ALWP) of the European Group for Blood and Marrow Transplantation (EBMT). Leukemia. 2005;19:2304-2312.
Ciurea SO, Mulanovich V, Saliba RM, et al. Improved early outcomes using a T cell replete graft compared with T cell depleted haploidentical hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2012;18:1835-1844.
Aversa F, Tabilio A, Velardi A, et al. Treatment of high-risk acute leukemia with T-cell-depleted stem cells from related donors with one fully mismatched HLA haplotype. N Engl J Med. 1998;339:1186-1193.
Al Malki MM, Gendzekhadze K, Yang D, et al. Long-term outcome of allogeneic hematopoietic stem cell transplantation from unrelated donor using tacrolimus/sirolimus-based GvHD prophylaxis: impact of HLA mismatch. Transplantation. 2020;104:1070-1080.
Luznik L, Jalla S, Engstrom LW, Iannone R, Fuchs EJ. Durable engraftment of major histocompatibility complex-incompatible cells after nonmyeloablative conditioning with fludarabine, low-dose total body irradiation, and posttransplantation cyclophosphamide. Blood. 2001;98:3456-3464.
Luznik L, O'Donnell PV, Symons HJ, et al. HLA-haploidentical bone marrow transplantation for hematologic malignancies using nonmyeloablative conditioning and high-dose, posttransplantation cyclophosphamide. Biol Blood Marrow Transplant. 2008;14:641-650.
Brunstein CG, Fuchs EJ, Carter SL, et al. Alternative donor transplantation after reduced intensity conditioning: results of parallel phase 2 trials using partially HLA-mismatched related bone marrow or unrelated double umbilical cord blood grafts. Blood. 2011;118:282-288.
Solomon SR, Sizemore CA, Sanacore M, et al. Haploidentical transplantation using T cell replete peripheral blood stem cells and myeloablative conditioning in patients with high-risk hematologic malignancies who lack conventional donors is well tolerated and produces excellent relapse-free survival: results of a prospective phase II trial. Biol Blood Marrow Transplant. 2012;18:1859-1866.
Gaballa S, Ge I, El Fakih R, et al. Results of a 2-arm, phase 2 clinical trial using post-transplantation cyclophosphamide for the prevention of graft-versus-host disease in haploidentical donor and mismatched unrelated donor hematopoietic stem cell transplantation. Cancer. 2016;122:3316-3326.
O'Donnell PV, Eapen M, Horowitz MM, et al. Comparable outcomes with marrow or peripheral blood as stem cell sources for hematopoietic cell transplantation from haploidentical donors after non-ablative conditioning: a matched-pair analysis. Bone Marrow Transplant. 2016;51:1599-1601.
Bashey A, Zhang MJ, McCurdy SR, et al. Mobilized peripheral blood stem cells versus unstimulated bone marrow as a graft source for T-cell-replete haploidentical donor transplantation using post-transplant cyclophosphamide. J Clin Oncol. 2017;35:3002-3009.
Im A, Rashidi A, Wang T, et al. Risk factors for graft-versus-host disease in haploidentical hematopoietic cell transplantation using post-transplant cyclophosphamide. Biol Blood Marrow Transplant. 2020;26:1459-1468.
Canaani J, Beohou E, Labopin M, et al. Trends in patient outcome over the past two decades following allogeneic stem cell transplantation for acute myeloid leukaemia: an ALWP/EBMT analysis. J Intern Med. 2019;285:407-418.
Horan JT, Logan BR, Agovi-Johnson MA, et al. Reducing the risk for transplantation-related mortality after allogeneic hematopoietic cell transplantation: how much progress has been made? J Clin Oncol. 2011;29:805-813.
Bazarbachi A, Labopin M, Angelucci E, et al. Haploidentical transplantation with post-transplantation cyclophosphamide for T cell acute lymphoblastic leukemia: a report from the European Society for Blood and Marrow Transplantation Acute Leukemia Working Party. Biol Blood Marrow Transplant. 2020;26:936-942.
Fielding AK. Curing Ph+ ALL: assessing the relative contributions of chemotherapy, TKIs, and allogeneic stem cell transplant. Hematology Am Soc Hematol Educ Program. 2019;2019:24-29.
Duarte RF, Labopin M, Bader P, et al. Indications for haematopoietic stem cell transplantation for haematological diseases, solid tumours and immune disorders: current practice in Europe, 2019. Bone Marrow Transplant. 2019;54:1525-1552.
DeFilipp Z, Advani AS, Bachanova V, et al. Hematopoietic cell transplantation in the treatment of adult acute lymphoblastic leukemia: updated 2019 evidence-based review from the American Society for Transplantation and Cellular Therapy. Biol Blood Marrow Transplant. 2019;25:2113-2123.

Auteurs

Arnon Nagler (A)

Hematology Division, Sheba Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Ramat-Gan, Israel.
European Society for Blood and Marrow Transplantation Acute Leukemia Working Party, St Anthony Hospital, Paris, France.

Myriam Labopin (M)

European Society for Blood and Marrow Transplantation Acute Leukemia Working Party, St Anthony Hospital, Paris, France.

Yener Koc (Y)

Bone Marrow Transplant Unit, Medicana International, Istanbul, Turkey.

Emanuele Angelucci (E)

Hematology and Transplant Unit, IRCCS San Martino Hospital Polyclinic, Genoa, Italy.

Johanna Tischer (J)

Medical Clinic III, Grosshadern Clinic, Munich, Germany.

Mutlu Arat (M)

Hematopoietic Stem Cell Transplant Unit, Florence Nightingale Sisli Hospital, Istanbul, Turkey.

Pietro Pioltelli (P)

Hematological Clinic of the University of Milano-Bicocca, San Gerardo Hospital, Monza, Italy.

Paolo Bernasconi (P)

Bone Marrow Transplant Unit, Hematology Clinic, IRCCS Foundation San Matteo Polyclinic, Pavia, Italy.

Patrizia Chiusolo (P)

Section of Hematology, Department of Radiological and Hematological Sciences, Catholic University of the Sacred Heart, Rome, Italy.

J L Diez-Martin (JL)

Bone Marrow Transplant Section, Gregorio Maranon Hospital, Madrid, Spain.

Jamie Sanz (J)

Hematology Department, University Hospital LaFe, Valencia, Spain.

Fabio Ciceri (F)

Hematology and Bone Marrow Transplantation, San Raffaele Hospital, Milan, Italy.

Zinaida Peric (Z)

Bone Marrow Transplant Unit, University Hospital Center Zagreb and School of Medicine, University of Zagreb, Zagreb, Croatia.

Sebastian Giebel (S)

Institute of Oncology, Maria Sklodowska-Curie Memorial Cancer Center, Gliwice, Poland.

Jonathan Canaani (J)

Hematology Division, Sheba Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Ramat-Gan, Israel.

Mohamad Mohty (M)

European Society for Blood and Marrow Transplantation Acute Leukemia Working Party, St Anthony Hospital, Paris, France.

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