Allogeneic Hematopoietic Stem Cell Transplantation for Elderly Acute Lymphoblastic Leukemia Patients: A Registry Study From the Société Francophone de Greffe de Moelle et Thérapie Cellulaire (SFGM-TC)
Corresponding Author
Yves Chalandon
University Hospital Geneva, Hematology Service and Faculty of Medicine, University of Geneva, Geneva, Switzerland
Correspondence:
Yves Chalandon ([email protected])
Search for more papers by this authorStephanie Nguyen
Hôpital de la Pitié Salpêtrière, Paris, France
Search for more papers by this authorEolia Brissot
Sorbonne Université, INSERM UMRs938, Paris, France, Service d'Hématologie Clinique et de Thérapie Cellulaire, Paris, France
Search for more papers by this authorXavier Poiré
Cliniques Universitaires Saint-Luc, Brussels, Belgium
Search for more papers by this authorCristina Castilla-Llorente
Department of Haematology, Gustave Roussy Cancer Campus, Villejuif, France
Search for more papers by this authorJacques-Olivier Bay
CHU de Clermont-Ferrand, Clermont-Ferrand, France
Search for more papers by this authorPascal Turlure
Clinical Hematology, Limoges University Hospital, Limoges, France
Search for more papers by this authorAli Bazarbachi
BMT Program, Department of Internal Medicine, American University of Beirut, Beirut, Lebanon
Search for more papers by this authorPhilippe Lewalle
Hematology Department, Hôpital Universitaire de Bruxelles (HUB), Institut Jules Bordet, Brussels, Belgium
Search for more papers by this authorPaul Chauvet
CHU de Lille, Maladies du Sang, Université de Lille, Lille, France
Search for more papers by this authorEdouard Forcade
Service d'Hématologie Clinique et Thérapie Cellulaire, CHU Bordeaux, Bordeaux, France
Search for more papers by this authorMarie Robin
Hôpital Saint-Louis, APHP, Université de Paris Cité, Paris, France
Search for more papers by this authorStavroula Masouridi-Levrat
University Hospital Geneva, Hematology Service and Faculty of Medicine, University of Geneva, Geneva, Switzerland
Search for more papers by this authorCorresponding Author
Yves Chalandon
University Hospital Geneva, Hematology Service and Faculty of Medicine, University of Geneva, Geneva, Switzerland
Correspondence:
Yves Chalandon ([email protected])
Search for more papers by this authorStephanie Nguyen
Hôpital de la Pitié Salpêtrière, Paris, France
Search for more papers by this authorEolia Brissot
Sorbonne Université, INSERM UMRs938, Paris, France, Service d'Hématologie Clinique et de Thérapie Cellulaire, Paris, France
Search for more papers by this authorXavier Poiré
Cliniques Universitaires Saint-Luc, Brussels, Belgium
Search for more papers by this authorCristina Castilla-Llorente
Department of Haematology, Gustave Roussy Cancer Campus, Villejuif, France
Search for more papers by this authorJacques-Olivier Bay
CHU de Clermont-Ferrand, Clermont-Ferrand, France
Search for more papers by this authorPascal Turlure
Clinical Hematology, Limoges University Hospital, Limoges, France
Search for more papers by this authorAli Bazarbachi
BMT Program, Department of Internal Medicine, American University of Beirut, Beirut, Lebanon
Search for more papers by this authorPhilippe Lewalle
Hematology Department, Hôpital Universitaire de Bruxelles (HUB), Institut Jules Bordet, Brussels, Belgium
Search for more papers by this authorPaul Chauvet
CHU de Lille, Maladies du Sang, Université de Lille, Lille, France
Search for more papers by this authorEdouard Forcade
Service d'Hématologie Clinique et Thérapie Cellulaire, CHU Bordeaux, Bordeaux, France
Search for more papers by this authorMarie Robin
Hôpital Saint-Louis, APHP, Université de Paris Cité, Paris, France
Search for more papers by this authorStavroula Masouridi-Levrat
University Hospital Geneva, Hematology Service and Faculty of Medicine, University of Geneva, Geneva, Switzerland
Search for more papers by this authorFunding: The authors received no specific funding for this work.
Marie Robin and Stavroula Masouridi-Levrat contributed equally to this study.
ABSTRACT
There are very limited data regarding the outcomes of elderly patients with acute lymphoblastic leukemia (ALL) who undergo allogeneic hematopoietic stem cell transplantation (alloHSCT). A total of 316 ALL patients aged ≥ 60 years who underwent alloHSCT between 2010 to 2022 were identified in the SFGM-TC registry. The primary objective was to evaluate progression-free survival (PFS), non-relapse mortality (NRM), relapse incidence (RI), and graft-versus-host disease (GvHD)-free relapse-free survival (GRFS), as well as their risk factors. The median age was 63.8 years (range 60–75.8), 49.8% of patients had Philadelphia-positive B-ALL (Ph + ALL), and 70.9% were in first complete remission (CR1) at transplantation. The donor was an unrelated donor in 52.1%, a matched related donor (MRD) in 26.3%, and a haplo-identical donor in 17.7%. Reduced-intensity conditioning (RIC) was administered to 64.6% of patients, while total body irradiation (TBI) was used in 35.8%. The 3-year overall survival (OS) was 46% (95% CI 40%–53%). The 3-year PFS, NRM, RI, and GRFS were 41% (95% CI 35%–48%), 23% (95% CI 18%–28%), 36% (95% CI 31%–42%), and 30% (95% CI 25%–37%), respectively. Multivariable analyses confirmed poorer OS and PFS in patients with advanced disease, with an HR of 1.79 (95% CI 1.22–2.64), p = 0.0032. Additionally, the ALL subtype significantly impacted outcomes, with an HR of 1.99 (95% CI 1.42–2.79) for non-Ph + ALL. This study suggests that alloHSCT is a viable option for elderly ALL patients, as age itself did not impact outcomes. However, advanced disease and non-Ph + ALL were associated with significantly worse survival.
Conflicts of Interest
Y.C. has received consulting fees for advisory board from MSD, Novartis, Incyte, BMS, Pfizer, Abbvie, Roche, Jazz, Gilead, Amgen, Astra-Zeneca, Servier, Takeda, Pierre Fabre, Medac; travel support from MSD, Roche, Novartis, Pfizer, BMS, Gilead, Amgen, Incyte, Abbvie, Janssen, Astra-Zeneca, Jazz, Pierre Fabre, Sanofi all via the institution. E.F. received funding for congress participation from Alexion, Gilead, Jazz, MSD, Novartis; and honoraria for boards and speaker bureau participation from Alexion, GSK, Novartis, Gilead, Astellas. E.B. received research funding, honorarium, speaker's fees and travel expenses from Novartis, Astellas, Alexion, Jazz Pharmaceuticals, Gilead, MSD, Keocyt, Amgen, Beigen, Pierre Fabre, Pfizer, Celgene/BMS, Sanofi. M.L. received funding for honoraria: Alexion, Astra Zeneca, BMS Celgene, Gilead, GSK, Jazz, Kartos, Medac, MSD, Novartis, Pfizer, Sanofi, Sobi, Telios. T.M. has received consulting fees from Servier, Jazz Pharmaceutical, Sobi, Astellas. Travel support from Servier, Jazz Pharmaceutical. A.H. has received consulting fees advisory board from Jazz, Pfizer, Servier, Novartis, Astellas; Travel support from Medac, Jazz, Neovii all via the Institution. M.R. support for research from Neovii, Medac, Abbvie, Novartis. S.M.-L. received funding for congress participation from Gilead, Jazz, BeiGene, Sanofi all via institution.
Open Research
Data Availability Statement
As for SFGM-TC Policy, data cannot be shared but are available on reasonable request to: [email protected].
Supporting Information
Filename | Description |
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ajh27701-sup-0001-supinfo.docxWord 2007 document , 41 KB |
Table S1. Univariable analysis for acute GvHD at 180 days, chronic GvHD and GRFS at 36 months. Table S2. Univariable analysis for OS, PFS, RI and NRM at 36 months post-transplantation. All centers that participated to the study are cited in the Supporting Information (Appendix: SFGM-TC centers). |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1R. Pieters, C. G. Mullighan, and S. P. Hunger, “Advancing Diagnostics and Therapy to Reach Universal Cure in Childhood ALL,” Journal of Clinical Oncology 41, no. 36 (2023): 5579–5591.
- 2F. Huguet, S. Chevret, T. Leguay, et al., “Intensified Therapy of Acute Lymphoblastic Leukemia in Adults: Report of the Randomized GRAALL-2005 Clinical Trial,” Journal of Clinical Oncology 36, no. 24 (2018): 2514–2523.
- 3D. J. DeAngelo, K. E. Stevenson, S. E. Dahlberg, et al., “Long-Term Outcome of a Pediatric-Inspired Regimen Used for Adults Aged 18-50 Years With Newly Diagnosed Acute Lymphoblastic Leukemia,” Leukemia 29, no. 3 (2015): 526–534, https://doi.org/10.1038/leu.2014.229.
- 4S. E. Siegel, W. Stock, R. H. Johnson, et al., “Pediatric-Inspired Treatment Regimens for Adolescents and Young Adults With Philadelphia Chromosome-Negative Acute Lymphoblastic Leukemia: A Review,” JAMA Oncology 4, no. 5 (2018): 725–734, https://doi.org/10.1001/jamaoncol.2017.5305.
- 5S. Chiaretti, A. Vitale, G. Cazzaniga, et al., “Clinico-Biological Features of 5202 Patients With Acute Lymphoblastic Leukemia Enrolled in the Italian AIEOP and GIMEMA Protocols and Stratified in Age Cohorts,” Haematologica 98, no. 11 (2013): 1702–1710.
- 6R. Foà and S. Chiaretti, “Philadelphia Chromosome-Positive Acute Lymphoblastic Leukemia,” New England Journal of Medicine 386, no. 25 (2022): 2399–2411.
- 7P. Rousselot, M. M. Coudé, N. Gokbuget, et al., “Dasatinib and Low-Intensity Chemotherapy in Elderly Patients With Philadelphia Chromosome–Positive ALL,” Blood 128, no. 6 (2016): 774–782.
- 8Z. DeFilipp, A. S. Advani, V. Bachanova, 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,” Biology of Blood and Marrow Transplantation 25, no. 11 (2019): 2113–2123.
- 9S. Giebel, D. I. Marks, N. Boissel, et al., “Hematopoietic Stem Cell Transplantation for Adults With Philadelphia Chromosome-Negative Acute Lymphoblastic Leukemia in First Remission: A Position Statement of the European Working Group for Adult Acute Lymphoblastic Leukemia (EWALL) and the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation (EBMT),” Bone Marrow Transplantation 54, no. 6 (2019): 798–809.
- 10A. H. Goldstone, S. M. Richards, H. M. Lazarus, et al., “In Adults With Standard-Risk Acute Lymphoblastic Leukemia, the Greatest Benefit Is Achieved From a Matched Sibling Allogeneic Transplantation in First Complete Remission, and an Autologous Transplantation Is Less Effective Than Conventional Consolidation/Maintenance Chemotherapy in all Patients: Final Results of the International ALL Trial (MRC UKALL XII/ECOG E2993),” Blood 111, no. 4 (2008): 1827–1833.
- 11D. I. Marks, T. Wang, W. S. Pérez, et al., “The Outcome of Full-Intensity and Reduced-Intensity Conditioning Matched Sibling or Unrelated Donor Transplantation in Adults With Philadelphia Chromosome-Negative Acute Lymphoblastic Leukemia in First and Second Complete Remission,” Blood 116, no. 3 (2010): 366–374.
- 12M. Mohty, M. Labopin, L. Volin, et al., “Reduced-Intensity Versus Conventional Myeloablative Conditioning Allogeneic Stem Cell Transplantation for Patients With Acute Lymphoblastic Leukemia: A Retrospective Study From the European Group for Blood and Marrow Transplantation,” Blood 116, no. 22 (2010): 4439–4443.
- 13A. Rosko, H.-L. Wang, M. de Lima, et al., “Reduced Intensity Conditioned Allograft Yields Favorable Survival for Older Adults With B-Cell Acute Lymphoblastic Leukemia,” American Journal of Hematology 92, no. 1 (2017): 42–49, https://doi.org/10.1002/ajh.24575.
- 14A. Sijs-Szabo, A. G. Dinmohamed, J. Versluis, et al., “Allogeneic Stem Cell Transplantation in Patients > 40 Years of Age With Acute Lymphoblastic Leukemia: Reduced Intensity Versus Myeloablative Conditioning,” Transplantation 107, no. 12 (2023): 2561–2567.
- 15L. K. Gjærde, C. U. Rank, M. K. Andersen, et al., “Improved Survival After Allogeneic Transplantation for Acute Lymphoblastic Leukemia in Adults: A Danish Population-Based Study,” Leukemia & Lymphoma 63, no. 2 (2022): 416–425.
- 16P. Kebriaei, C. Anasetti, M.-J. Zhang, et al., “Intravenous Busulfan Compared With Total Body Irradiation Pretransplant Conditioning for Adults With Acute Lymphoblastic Leukemia,” Biology of Blood and Marrow Transplantation 24, no. 4 (2018): 726–733.
- 17A. Czyz, M. Labopin, S. Giebel, et al., “Cyclophosphamide Versus Etoposide in Combination With Total Body Irradiation as Conditioning Regimen for Adult Patients With Ph-Negative Acute Lymphoblastic Leukemia Undergoing Allogeneic Stem Cell Transplant: On Behalf of the ALWP of the European Society for Blood and Marrow Transplantation,” American Journal of Hematology 93, no. 6 (2018): 778–785.
- 18J. Pavlů, M. Labopin, R. Niittyvuopio, et al., “Measurable Residual Disease at Myeloablative Allogeneic Transplantation in Adults With Acute Lymphoblastic Leukemia: A Retrospective Registry Study on 2780 Patients From the Acute Leukemia Working Party of the EBMT,” Journal of Hematology & Oncology 12, no. 1 (2019): 108.
- 19H. Zhang, Z. Fan, F. Huang, et al., “Busulfan Plus Cyclophosphamide Versus Total Body Irradiation Plus Cyclophosphamide for Adults Acute B Lymphoblastic Leukemia: An Open-Label, Multicenter, Phase III Trial,” Journal of Clinical Oncology 41, no. 2 (2023): 343–353, https://doi.org/10.1200/JCO.22.00767.
- 20K. Hirschbühl, M. Labopin, E. Polge, et al., “Total Body Irradiation Versus Busulfan Based Intermediate Intensity Conditioning for Stem Cell Transplantation in ALL Patients >45 Years-a Registry-Based Study by the Acute Leukemia Working Party of the EBMT,” Bone Marrow Transplantation 58, no. 8 (2023): 874–880.
- 21Z. Peric, M. Labopin, C. Peczynski, et al., “Comparison of Reduced-Intensity Conditioning Regimens in Patients With Acute Lymphoblastic Leukemia >45 Years Undergoing Allogeneic Stem Cell Transplantation-a Retrospective Study by the Acute Leukemia Working Party of EBMT,” Bone Marrow Transplantation 55, no. 8 (2020): 1560–1569.
- 22G. Roth-Guepin, J. Canaani, A. Ruggeri, et al., “Allogeneic Stem Cell Transplantation in Acute Lymphoblastic Leukemia Patients Older Than 60 Years: A Survey From the Acute Leukemia Working Party of EBMT,” Oncotarget 8, no. 68 (2017): 112972–112979.
- 23D. J. Weisdorf, D. Hurd, S. Carter, et al., “Prospective Grading of Graft-Versus-Host Disease After Unrelated Donor Marrow Transplantation: A Grading Algorithm Versus Blinded Expert Panel Review,” Biology of Blood and Marrow Transplantation 9, no. 8 (2003): 512–518.
- 24A. C. Harris, R. Young, S. Devine, et al., “International, Multicenter Standardization of Acute Graft-Versus-Host Disease Clinical Data Collection: A Report From the Mount Sinai Acute GVHD International Consortium,” Biology of Blood and Marrow Transplantation 22, no. 1 (2016): 4–10.
- 25S. Z. Pavletic, P. Martin, S. J. Lee, et al., “Measuring Therapeutic Response in Chronic Graft-Versus-Host Disease: National Institutes of Health Consensus Development Project on Criteria for Clinical Trials in Chronic Graft-Versus-Host Disease: IV. Response Criteria Working Group Report,” Biology of Blood and Marrow Transplantation 12, no. 3 (2006): 252–266.
- 26S. J. Lee, D. Wolff, C. Kitko, et al., “Measuring Therapeutic Response in Chronic Graft-Versus-Host Disease. National Institutes of Health Consensus Development Project on Criteria for Clinical Trials in Chronic Graft-Versus-Host Disease: IV. The 2014 Response Criteria Working Group Report,” Biology of Blood and Marrow Transplantation 21, no. 6 (2015): 984–999.
- 27A. Ruggeri, M. Labopin, F. Ciceri, M. Mohty, and A. Nagler, “Definition of GvHD-Free, Relapse-Free Survival for Registry-Based Studies: An ALWP-EBMT Analysis on Patients With AML in Remission,” Bone Marrow Transplantation 51, no. 4 (2016): 610–611.
- 28A. S. Kanate, A. Nagler, and B. Savani, “Summary of Scientific and Statistical Methods, Study Endpoints and Definitions for Observational and Registry-Based Studies in Hematopoietic Cell Transplantation,” Clinical Hematology 2, no. 1 (2020): 2–4.
10.2991/chi.d.191207.001 Google Scholar
- 29P. K. Andersen, J. P. Klein, and M. J. Zhang, “Testing for Centre Effects in Multi-Centre Survival Studies: A Monte Carlo Comparison of Fixed and Random Effects Tests,” Statistics in Medicine 18, no. 12 (1999): 1489–1500.
10.1002/(SICI)1097-0258(19990630)18:12<1489::AID-SIM140>3.0.CO;2-# CAS PubMed Web of Science® Google Scholar
- 30P. Armand, H. T. Kim, B. R. Logan, et al., “Validation and Refinement of the Disease Risk Index for Allogeneic Stem Cell Transplantation,” Blood 123, no. 23 (2014): 3664–3671.
- 31M. Hunault, J.-L. Harousseau, M. Delain, et al., “Better Outcome of Adult Acute Lymphoblastic Leukemia After Early Genoidentical Allogeneic Bone Marrow Transplantation (BMT) Than After Late High-Dose Therapy and Autologous BMT: A GOELAMS Trial,” Blood 104, no. 10 (2004): 3028–3037.
- 32N. Vey, X. Thomas, C. Picard, et al., “Allogeneic Stem Cell Transplantation Improves the Outcome of Adults With t(1;19)/E2A-PBX1 and t(4;11)/MLL-AF4 Positive B-Cell Acute Lymphoblastic Leukemia: Results of the Prospective Multicenter LALA-94 Study,” Leukemia 20, no. 12 (2006): 2155–2161.
- 33J. J. Cornelissen, B. van der Holt, G. E. G. Verhoef, et al., “Myeloablative Allogeneic Versus Autologous Stem Cell Transplantation in Adult Patients With Acute Lymphoblastic Leukemia in First Remission: A Prospective Sibling Donor Versus No-Donor Comparison,” Blood 113, no. 6 (2009): 1375–1382.
- 34N. Gökbuget, M. Kneba, T. Raff, 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 120, no. 9 (2012): 1868–1876.
- 35N. Dhédin, A. Huynh, S. Maury, et al., “Role of Allogeneic Stem Cell Transplantation in Adult Patients With Ph-Negative Acute Lymphoblastic Leukemia,” Blood 125, no. 16 (2015): 2486–2496.
- 36D. W. Beelen, R. Arnold, M. Stelljes, et al., “Long-Term Results of Allogeneic Stem Cell Transplantation in Adult Ph- Negative High-Risk Acute Lymphoblastic Leukemia,” Transplantation and Cellular Therapy 28, no. 12 (2022): 834–842.
- 37V. Bachanova, D. I. Marks, M.-J. Zhang, et al., “Ph+ ALL Patients in First Complete Remission Have Similar Survival After Reduced Intensity and Myeloablative Allogeneic Transplantation: Impact of Tyrosine Kinase Inhibitor and Minimal Residual Disease,” Leukemia 28, no. 3 (2014): 658–665.
- 38D. Modi, S. Alkassis, S. Kim, et al., “Allogeneic Stem Cell Transplant Outcomes Between TBI-Containing Reduced Intensity and Myeloablative Conditioning Regimens for ALL in Complete Remission,” Leukemia & Lymphoma 64, no. 7 (2023): 1285–1294.
- 39I. de Oliveira Fernans Junior and L. J. Arcuri, “Myeloablative or Reduced-Intensity/Non-Myeloablative Hematopoietic Cell Transplantation for Philadelphia-Positive Acute Lymphoblastic Leukemia in Adults Older Than 40 Years Old—A Secondary Analysis of a CIBMTR Database,” Annals of Hematology 103, no. 2 (2024): 603–607, https://doi.org/10.1007/s00277-023-05532-8.
- 40E. Mora, J. Montoro, A. Balaguer, et al., “Total Body Irradiation Versus Thiotepa/Busulfan-Based Conditioning Regimens for Myeloablative Allogeneic Stem Cell Transplantation in Adults With Acute Lymphoblastic Leukemia,” Bone Marrow Transplantation 59, no. 8 (2024): 1137–1145.
- 41F. Khimani, M. Dutta, R. Faramand, et al., “Impact of Total Body Irradiation-Based Myeloablative Conditioning Regimens in Patients With Acute Lymphoblastic Leukemia Undergoing Allogeneic Hematopoietic Stem Cell Transplantation: Systematic Review and Meta-Analysis,” Transplantation and Cellular Therapy 27, no. 7 (2021): 620.e1–620.e9.
- 42C. Peters, J.-H. Dalle, F. Locatelli, et al., “Total Body Irradiation or Chemotherapy Conditioning in Childhood ALL: A Multinational, Randomized, Noninferiority Phase III Study,” Journal of Clinical Oncology 39, no. 4 (2021): 295–307.
- 43H. Pfeifer, B. Wassmann, W. Bethge, et al., “Randomized Comparison of Prophylactic and Minimal Residual Disease-Triggered Imatinib After Allogeneic Stem Cell Transplantation for BCR-ABL1-Positive Acute Lymphoblastic Leukemia,” Leukemia 27, no. 6 (2013): 1254–1262.
- 44S. Giebel, A. Czyz, O. Ottmann, et al., “Use of Tyrosine Kinase Inhibitors to Prevent Relapse After Allogeneic Hematopoietic Stem Cell Transplantation for Patients With Philadelphia Chromosome-Positive Acute Lymphoblastic Leukemia: A Position Statement of the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation,” Cancer 122, no. 19 (2016): 2941–2951.
- 45Z. Warraich, P. Tenneti, T. Thai, et al., “Relapse Prevention With Tyrosine Kinase Inhibitors After Allogeneic Transplantation for Philadelphia Chromosome-Positive Acute Lymphoblast Leukemia: A Systematic Review,” Biology of Blood and Marrow Transplantation 26, no. 3 (2020): e55–e64.
- 46N. Saini, D. Marin, C. Ledesma, et al., “Impact of TKIs Post-Allogeneic Hematopoietic Cell Transplantation in Philadelphia Chromosome-Positive ALL,” Blood 136, no. 15 (2020): 1786–1789.
- 47H. Kantarjian, A. Stein, N. Gökbuget, et al., “Blinatumomab Versus Chemotherapy for Advanced Acute Lymphoblastic Leukemia,” New England Journal of Medicine 376, no. 9 (2017): 836–847.
- 48H. M. Kantarjian, D. J. DeAngelo, M. Stelljes, et al., “Inotuzumab Ozogamicin Versus Standard Therapy for Acute Lymphoblastic Leukemia,” New England Journal of Medicine 375, no. 8 (2016): 740–753, https://doi.org/10.1056/NEJMoa1509277.
- 49S. L. Maude, T. W. Laetsch, J. Buechner, et al., “Tisagenlecleucel in Children and Young Adults With B-Cell Lymphoblastic Leukemia,” New England Journal of Medicine 378, no. 5 (2018): 439–448.
- 50A. Spyridonidis, “How I Treat Measurable (Minimal) Residual Disease in Acute Leukemia After Allogeneic Hematopoietic Cell Transplantation,” Blood 135, no. 19 (2020): 1639–1649.
- 51M. L. Green, W. M. Leisenring, H. Xie, et al., “CMV Reactivation After Allogeneic HCT and Relapse Risk: Evidence for Early Protection in Acute Myeloid Leukemia,” Blood 122, no. 7 (2013): 1316–1324.
- 52K. Takenaka, T. Nishida, Y. Asano-Mori, et al., “Cytomegalovirus Reactivation After Allogeneic Hematopoietic Stem Cell Transplantation Is Associated With a Reduced Risk of Relapse in Patients With Acute Myeloid Leukemia Who Survived to Day 100 After Transplantation: The Japan Society for Hematopoietic Cell Transplantation Transplantation-Related Complication Working Group,” Biology of Blood and Marrow Transplantation 21, no. 11 (2015): 2008–2016.
- 53Y. Akahoshi, H. Nakasone, K. Takenaka, et al., “CMV Reactivation After Allogeneic HCT Is Associated With a Reduced Risk of Relapse in Acute Lymphoblastic Leukemia,” Blood Advances 7, no. 12 (2023): 2699–2708.
- 54Z. Peric, J. Wilson, N. Durakovic, et al., “Early Human Cytomegalovirus Reactivation Is Associated With Lower Incidence of Relapse of Myeloproliferative Disorders After Allogeneic Hematopoietic Stem Cell Transplantation,” Bone Marrow Transplantation 53, no. 11 (2018): 1450–1456.
- 55S. Giebel, M. Labopin, M. Houhou, et al., “Autologous Versus Allogeneic Hematopoietic Cell Transplantation for Older Patients With Acute Lymphoblastic Leukemia. An Analysis From the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation,” Bone Marrow Transplantation 58, no. 4 (2023): 393–400.
- 56G. Battipaglia, M. Labopin, S. Mielke, et al., “Thiotepa-Based Regimens Are Valid Alternatives to Total Body Irradiation-Based Reduced-Intensity Conditioning Regimens in Patients With Acute Lymphoblastic Leukemia: A Retrospective Study on Behalf of the Acute Leukemia Working Party of the European Society for Blood and Marrow Transplantation,” Transplantation and Cellular Therapy 30, no. 1 (2024): 95.e1–95.e10.
- 57R. Foà, R. Bassan, A. Vitale, et al., “Dasatinib–Blinatumomab for Ph-Positive Acute Lymphoblastic Leukemia in Adults,” New England Journal of Medicine 383, no. 17 (2020): 1613–1623.
- 58R. Foà, R. Bassan, L. Elia, et al., “Long-Term Results of the Dasatinib-Blinatumomab Protocol for Adult Philadelphia-Positive ALL,” Journal of Clinical Oncology 42 (2023): JCO2301075.
- 59E. Jabbour, N. J. Short, N. Jain, et al., “Ponatinib and Blinatumomab for Philadelphia Chromosome-Positive Acute Lymphoblastic Leukaemia: A US, Single-Centre, Single-Arm, Phase 2 Trial,” Lancet Haematology 10, no. 1 (2023): e24–e34.
- 60M. R. Litzow, Z. Sun, R. J. Mattison, et al., “Blinatumomab for MRD-Negative Acute Lymphoblastic Leukemia in Adults,” New England Journal of Medicine 391, no. 4 (2024): 320–333.
- 61P. Chevallier, T. Leguay, M. Delord, et al., “Inotuzumab Ozogamicin and Low-Intensity Chemotherapy in Older Patients With Newly Diagnosed CD22+ Philadelphia Chromosome-Negative B-Cell Precursor Acute Lymphoblastic Leukemia,” Journal of Clinical Oncology 42, no. 36 (2024): 4327–4341.