Cited by 2,898CAR-T cell therapy researchAcute Lymphoblastic Leukemia researchImmunotherapy and Immune Responses

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T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial

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Lee, Daniel W, Kochenderfer, James N, Stetler-Stevenson, Maryalice, Cui, Yongzhi K, Delbrook, Cindy, Feldman, Steven A, Fry, Terry J, Orentas, Rimas, Sabatino, Marianna, Shah, Nirali N, Steinberg, Seth M, Stroncek, Dave, Tschernia, Nick, Yuan, Constance, Zhang, Hua, Zhang, Ling, Rosenberg, Steven A, Wayne, Alan S, Mackall, Crystal L·2015·The Lancet

DOI 10.1016/s0140-6736(14)61403-3PMC PMC7065359

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Abstract

Background Chimeric antigen receptor (CAR) modified T cells targeting CD19 have shown activity in case series of patients with acute and chronic lymphocytic leukaemia and B-cell lymphomas, but feasibility, toxicity, and response rates of consecutively enrolled patients treated with a consistent regimen and assessed on an intention-to-treat basis have not been reported. We aimed to define feasibility, toxicity, maximum tolerated dose, response rate, and biological correlates of response in children and young adults with refractory B-cell malignancies treated with CD19-CAR T cells. Methods This phase 1, dose-escalation trial consecutively enrolled children and young adults (aged 1-30 years) with relapsed or refractory acute lymphoblastic leukaemia or non-Hodgkin lymphoma. Autologous T cells were engineered via an 11-day manufacturing process to express a CD19-CAR incorporating an anti-CD19 single-chain variable fragment plus TCR zeta and CD28 signalling domains. All patients received fludarabine and cyclophosphamide before a single infusion of CD19-CAR T cells. Using a standard 3 + 3 design to establish the maximum tolerated dose, patients received either 1 × 10(6) CAR-transduced T cells per kg (dose 1), 3 × 10(6) CAR-transduced T cells per kg (dose 2), or the entire CAR T-cell product if sufficient numbers of cells to meet the assigned dose were not generated. After the dose-escalation phase, an expansion cohort was treated at the maximum tolerated dose. The trial is registered with ClinicalTrials.gov, number NCT01593696. Findings Between July 2, 2012, and June 20, 2014, 21 patients (including eight who had previously undergone allogeneic haematopoietic stem-cell transplantation) were enrolled and infused with CD19-CAR T cells. 19 received the prescribed dose of CD19-CAR T cells, whereas the assigned dose concentration could not be generated for two patients (90% feasible). All patients enrolled were assessed for response. The maximum tolerated dose was defined as 1 × 10(6) CD19-CAR T cells per kg. All toxicities were fully reversible, with the most severe being grade 4 cytokine release syndrome that occurred in three (14%) of 21 patients (95% CI 3·0-36·3). The most common non-haematological grade 3 adverse events were fever (nine [43%] of 21 patients), hypokalaemia (nine [43%] of 21 patients), fever and neutropenia (eight [38%] of 21 patients), and cytokine release syndrome (three [14%) of 21 patients). Interpretation CD19-CAR T cell therapy is feasible, safe, and mediates potent anti-leukaemic activity in children and young adults with chemotherapy-resistant B-precursor acute lymphoblastic leukaemia. All toxicities were reversible and prolonged B-cell aplasia did not occur. Funding National Institutes of Health Intramural funds and St Baldrick's Foundation.

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Authors: Lee, D. W., Kochenderfer, J. N., Stetler-Stevenson, M., Cui, Y. K., Delbrook, C., Feldman, S. A., Fry, T. J., Orentas, R., Sabatino, M., Shah, N. N., Steinberg, S. M., Stroncek, D., Tschernia, N., Yuan, C., Zhang, H., Zhang, L., Rosenberg, S. A., Wayne, A. S., & Mackall, C. L.
Affiliations: National Institutes of Health (US)
National Cancer Institute (US)
University of Nevada, Reno (US)
University of Southern California (US)
Corresponding author: Mackall, Crystal L
ORCID: Lee, Daniel W
Kochenderfer, James N
Cui, Yongzhi K
Delbrook, Cindy
Feldman, Steven A
Fry, Terry J
Orentas, Rimas
Shah, Nirali N
Steinberg, Seth M
Yuan, Constance
Zhang, Hua
Zhang, Ling
Rosenberg, Steven A
Wayne, Alan S
Mackall, Crystal L
Venue: The Lancet
Publisher: Elsevier BV
Published: 2015-02
Volume: 385
Issue: 9967
Pages: 517-528
ISSN: 0099-5355 (ISSN-L)
0140-6736
DOI: 10.1016/s0140-6736(14)61403-3
PMC: PMC7065359
OpenAlex: W2129702476
Cited by: 2,898
References: 37
Citations by year: 2026: 86 · 2025: 154 · 2024: 175 · 2023: 217 · 2022: 275 · 2021: 311 · 2020: 350 · 2019: 317 · 2018: 315 · 2017: 314 · 2016: 232 · 2015: 134
FWCI: 103.68
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: The Lancet (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: St. Baldrick's Foundation
Entertainment Industry Foundation
National Institutes of Health
National Cancer Institute (Z01BC011072, Z01BC010566, Z01BC011024)
National Institute of Allergy and Infectious Diseases
Topics: Health Sciences › Medicine › Oncology › CAR-T cell therapy research
Health Sciences › Medicine › Hematology › Acute Lymphoblastic Leukemia research
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords: CD19 chimeric antigen receptor, CAR T-cell therapy, acute lymphoblastic leukemia, non-Hodgkin lymphoma, relapsed or refractory B-cell malignancies, maximum tolerated dose, cytokine release syndrome, neurotoxicity, non-relapse mortality, fludarabine and cyclophosphamide conditioning
MeSH terms: Adolescent, Adult, Child, Child, Preschool, Chimera, Feasibility Studies, Female, Humans, Infant, Lymphoma, Non-Hodgkin, Male, Receptors, Antigen, T-Cell, T-Lymphocytes, Cohort Studies, Treatment Outcome, Antigens, CD19, Precursor Cell Lymphoblastic Leukemia-Lymphoma, Young Adult, Cell- and Tissue-Based Therapy

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T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial

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