Treatment completion, asparaginase completion, and oncologic outcomes among children, adolescents and young adults with acute lymphoblastic leukemia treated with DFCI Consortium Protocols.


Journal

Leukemia
ISSN: 1476-5551
Titre abrégé: Leukemia
Pays: England
ID NLM: 8704895

Informations de publication

Date de publication:
05 Jan 2024
Historique:
received: 05 06 2023
accepted: 07 12 2023
revised: 04 12 2023
medline: 5 1 2024
pubmed: 5 1 2024
entrez: 4 1 2024
Statut: aheadofprint

Résumé

Adolescents and young adult (AYA) patients with acute lymphoblastic leukemia (ALL) face worse outcomes than children. While pediatric-inspired protocols have improved outcomes, the ability of patients to complete these intensive regimens and the reasons for discontinuation are unknown. We analyzed a cohort of 332 AYA patients (aged 15-49 years) and 1159 children (aged 1-14 years) with Ph-negative ALL treated on DFCI consortium protocols. We found that AYA patients completed treatment at lower rates than children (60.8% vs. 89.7%, p < 0.001), primarily due to higher rates of early treatment failure (14.5% vs. 2.4%, p < 0.001). Withdrawal from treatment for toxicity, social/personal, or unknown reasons was uncommon, but higher among AYA patients (9.3% vs 4.7%, p = 0.001). Patients who remained on assigned therapy for one year had favorable overall survival (AYA 5-year OS 88.9%; children 5-year OS 96.4%; p < 0.001). Among patients who continued treatment for 1 year, AYA patients completed asparaginase (defined as receiving 26+ weeks) at lower rates than children (79.1% vs. 89.6%, p < 0.001). Patients who received more weeks of consolidation asparaginase had higher overall and event-free survival. Efforts should focus on identifying patients at risk for early treatment failure and optimizing asparaginase delivery.

Identifiants

pubmed: 38177437
doi: 10.1038/s41375-023-02115-4
pii: 10.1038/s41375-023-02115-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature Limited.

Références

U.S. Cancer Statistics Working Group. U.S. Cancer Statistics Data Visualizations Tool, based on November 2018 submission data (1999–2016): U.S. Department of Health and Human Services, Centers for Disease Control and Prevention and National Cancer Institute; www.cdc.gov/cancer/dataviz , June (2019).
Vrooman LM, Blonquist TM, Stevenson KE, Supko JG, Hunt SK, Cronholm SM, et al. Efficacy and Toxicity of Pegaspargase and Calaspargase Pegol in Childhood Acute Lymphoblastic Leukemia: Results of DFCI 11-001. J Clin Oncol. 2021;39:3496–505. https://doi.org/10.1200/JCO.20.03692 . Epub 2021 Jul 6. PMID: 34228505.
doi: 10.1200/JCO.20.03692 pubmed: 34228505
Hunger SP, Lu X, Devidas M, Camitta BM, Gaynon PS, Winick NJ, et al. Improved survival for children and adolescents from 1990-2005: a report from the Children’s Oncology Group. J Clin Oncol. 2012;30:1663–9.
doi: 10.1200/JCO.2011.37.8018 pubmed: 22412151 pmcid: 3383113
Pui CH, Campana D, Pei D, Bowman WP, Sandlund JT, Kaste SC, et al. Treating childhood acute lymphoblastic leukemia without cranial irradiation. N. Engl J Med. 2009;360:2730–41.
doi: 10.1056/NEJMoa0900386 pubmed: 19553647 pmcid: 2754320
Patel B, Rai L, Buck G, Richards SM, Mortuza Y, Mitchell W, et al. Minimal residual disease is a significant predictor of treatment failure in non T-lineage adult acute lymphoblastic leukaemia: final results of the international trial UKALL XII/ECOG2993. Br J Haematol. 2010;148:80–9. https://doi.org/10.1111/j.1365-2141.2009.07941.x . Epub 2009 Oct 26. PMID: 19863538.
doi: 10.1111/j.1365-2141.2009.07941.x pubmed: 19863538
Larson RA, Dodge RK, Burns CP, Lee EJ, Stone RM, Schulman P, et al. A five-drug remission induction regimen with intensive consolidation for adults with acute lymphoblastic leukemia: cancer and leukemia group B study 8811. Blood 1995;85:2025–37. PMID: 7718875
doi: 10.1182/blood.V85.8.2025.bloodjournal8582025 pubmed: 7718875
Roberts KG. Genetics and prognosis of ALL in children vs adults. Hematol Am Soc Hematol Educ Program. 2018;2018:137–45. https://doi.org/10.1182/asheducation-2018.1.137 .
doi: 10.1182/asheducation-2018.1.137
Roberts KG, Li Y, Payne-Turner D, Harvey RC, Yang YL, Pei D, et al. Targetable kinase-activating lesions in Ph-like acute lymphoblastic leukemia. N. Engl J Med. 2014;371:1005–15. https://doi.org/10.1056/NEJMoa1403088 .
doi: 10.1056/NEJMoa1403088 pubmed: 25207766 pmcid: 4191900
Stock W, La M, Sanford B, Bloomfield CD, Vardiman JW, Gaynon P, et al. Children’s Cancer Group; Cancer and Leukemia Group B studies What determines the outcomes for adolescents and young adults with acute lymphoblastic leukemia treated on cooperative group protocols? A comparison of Children’s Cancer Group and Cancer and Leukemia Group B studies. Blood. 2008;112:1646–54. https://doi.org/10.1182/blood-2008-01-130237 .
doi: 10.1182/blood-2008-01-130237 pubmed: 18502832 pmcid: 2518876
Stock W, Luger SM, Advani AS, Geyer S, Harvey R, Mullighan C, et al. Favorable outcomes for older adolescents and young adults with acute lymphoblastic leukemia: early results of U.S. Intergroup trial C10403. Blood. 2014;124:796. Abstract 796.
doi: 10.1182/blood.V124.21.796.796
DeAngelo DJ, Stevenson KE, Dahlberg SE, Silverman LB, Couban S, Supko JG, et al. Long-term outcome of a pediatric-inspired regimen used for adults aged 18-50 years with newly diagnosed acute lymphoblastic leukemia. Leukemia 2015;29:526–34.
doi: 10.1038/leu.2014.229 pubmed: 25079173
Huguet F, Leguay T, Raffoux E, Thomas X, Beldjord K, Delabesse E, et al. Pediatric-inspired therapy in adults with Philadelphia chromosome-negative acute lymphoblastic leukemia: the GRAALL-2003 study. J Clin Oncol. 2009;27:911–8.
doi: 10.1200/JCO.2008.18.6916 pubmed: 19124805
Stock W, Luger SM, Advani AS, Yin J, Harvey RC, Mullighan CG, et al. A pediatric regimen for older adolescents and young adults with acute lymphoblastic leukemia: results of CALGB 10403. Blood 2019;133:1548–59.
doi: 10.1182/blood-2018-10-881961 pubmed: 30658992 pmcid: 6450431
Advani AS, Larsen E, Laumann K, Luger SM, Liedtke M, Devidas M, et al. Comparison of CALGB 10403 (Alliance) and COG AALL0232 toxicity results in young adults with acute lymphoblastic leukemia. Blood Adv. 2021;5:504–12. https://doi.org/10.1182/bloodadvances.2020002439 . PMID: 33496745; PMCID: PMC7839367.
doi: 10.1182/bloodadvances.2020002439 pubmed: 33496745 pmcid: 7839367
Gupta S, Wang C, Raetz EA, Schore R, Salzer WL, Larsen EC, et al. Impact of Asparaginase Discontinuation on Outcome in Childhood Acute Lymphoblastic Leukemia: A Report From the Children’s Oncology Group. J Clin Oncol. 2020;38:1897–905. https://doi.org/10.1200/JCO.19.03024 . Epub 2020 Apr 10. PMID: 32275469; PMCID: PMC7280050.
doi: 10.1200/JCO.19.03024 pubmed: 32275469 pmcid: 7280050
Gottschalk Højfeldt S, Grell K, Abrahamsson J, Lund B, Vettenranta K, Jónsson ÓG, et al. Relapse risk following truncation of pegylated asparaginase in childhood acute lymphoblastic leukemia. Blood 2021;137:2373–82. https://doi.org/10.1182/blood.2020006583 . PMID: 33150360.
doi: 10.1182/blood.2020006583 pubmed: 33150360
Silverman LB, Gelber RD, Dalton VK, Asselin BL, Barr RD, Clavell LA, et al. Improved outcome for children with acute lymphoblastic leukemia: Results of Dana-Farber Consortium Protocol 91- 01. Blood. 2001;97:1211–8.
doi: 10.1182/blood.V97.5.1211 pubmed: 11222362
Barry E, DeAngelo DJ, Neuberg D, Stevenson K, Loh ML, Asselin BL, et al. Favorable outcome for adolescents with acute lymphoblastic leukemia treated on Dana-Farber Cancer Institute Acute Lymphoblastic Leukemia Consortium Protocols. J Clin Oncol. 2007;25:813–9. https://doi.org/10.1200/JCO.2006.08.6397 . PMID: 17327603.
doi: 10.1200/JCO.2006.08.6397 pubmed: 17327603
Vrooman LM, Blonquist TM, Harris MH, Stevenson KE, Place AE, Hunt SK, et al. Refining risk classification in childhood B acute lymphoblastic leukemia: results of DFCI ALL Consortium Protocol 05-001. Blood Adv 2018;2:1449–58. https://doi.org/10.1182/bloodadvances.2018016584 . PMID: 29941458; PMCID: PMC6020806.
doi: 10.1182/bloodadvances.2018016584 pubmed: 29941458 pmcid: 6020806
Vrooman LM, Stevenson KE, Supko JG, O’Brien J, Dahlberg SE, Asselin BL, et al. Postinduction dexamethasone and individualized dosing of Escherichia Coli L-asparaginase each improve outcome of children and adolescents with newly diagnosed acute lymphoblastic leukemia: results from a randomized study-Dana-Farber Cancer Institute ALL Consortium Protocol 00-01. J Clin Oncol. 2013;31:1202–10.
doi: 10.1200/JCO.2012.43.2070 pubmed: 23358966 pmcid: 3595424
DeAngelo D, Dahlberg S, Silverman L, Couban S, Amrein P, Seftel M, et al. A Multicenter Phase II Study Using a Dose Intensified Pediatric Regimen in Adults with Untreated Acute Lymphoblastic Leukemia. Blood 2015;110:587.
doi: 10.1182/blood.V110.11.587.587
Aldoss I, Yin J, Wall A, Mrózek K, Liedtke M, Claxton DF, et al. The impact of early PEG-asparaginase discontinuation in young adults with ALL: a post hoc analysis of the CALGB 10403 study. Blood Adv. 2023;7:196–204.
doi: 10.1182/bloodadvances.2022007791 pubmed: 36269846
Litzow MR, Sun Z, Paletta E, Mattison R, Lazarus H, Rowe J, et al. Consolidation therapy with blinatumomab improves overall survival in newly diagnosed adult patients with B-lineage acute lymphoblastic leukemia in measurable residual disease negative remission: Results from the ECOG-ACRIN E1910 randomized phase III National Cooperative Clinical Trials Network trial. Blood 2022;140:LBA–1.
doi: 10.1182/blood-2022-171751

Auteurs

Yannis K Valtis (YK)

Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Yael Flamand (Y)

Department of Data Science, Dana Farber Cancer Institute, Boston, MA, USA.

Shai Shimony (S)

Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA.

Andrew E Place (AE)

Department of Pediatric Oncology, Dana-Farber Cancer Institute and Division of Pediatric Hematology Oncology, Boston Children's Hospital, Boston, MA, USA.

Lewis B Silverman (LB)

Department of Pediatric Oncology, Dana-Farber Cancer Institute and Division of Pediatric Hematology Oncology, Boston Children's Hospital, Boston, MA, USA.

Lynda M Vrooman (LM)

Department of Pediatric Oncology, Dana-Farber Cancer Institute and Division of Pediatric Hematology Oncology, Boston Children's Hospital, Boston, MA, USA.

Andrew M Brunner (AM)

Department of Hematology/Oncology, Massachusetts General Hospital, Boston, MA, USA.

Stephen E Sallan (SE)

Department of Pediatric Oncology, Dana-Farber Cancer Institute and Division of Pediatric Hematology Oncology, Boston Children's Hospital, Boston, MA, USA.

Martha Wadleigh (M)

Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA.

Richard M Stone (RM)

Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA.

Daniel J DeAngelo (DJ)

Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA.

Marlise R Luskin (MR)

Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA. marlise_luskin@dfci.harvard.edu.

Classifications MeSH