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Affiliation
1 From the Departments of Pediatrics (S.L.M., S.A.G.) and Pathology and Laboratory Medicine (C.H.J., B.L.L.), Perelman School of Medicine, and Abramson Cancer Center (C.H.J., B.L.L.), University of Pennsylvania, and the Division of Oncology, Center for Childhood Cancer Research and Cancer Immunotherapy Program, Children's Hospital of Philadelphia (S.L.M., S.A.G.) - all in Philadelphia; the Department of Pediatrics and Harold C. Simmons Comprehensive Cancer Center, University of Texas Southwestern Medical Center, and the Pauline Allen Gill Center for Cancer and Blood Disorders, Children's Health, Dallas (T.W.L.); the Department of Pediatric Hematology and Oncology, Oslo University Hospital, Oslo (J.B.); the Department of Pediatric Hematology and Oncology, Hospital Sant Joan de Deu Barcelona, Barcelona (S.R.); the Department of Pediatrics and Internal Medicine, University of Utah, Salt Lake City (M.B.); the Department of Pediatrics, Faculty of Medicine, University of Montreal, and the Hematology Oncology Division and Charles-Bruneau Cancer Center, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montreal (H.B.), and the Division of Haematology/Oncology/Bone Marrow Transplantation, Hospital for Sick Children, Toronto (J.K.) - all in Canada; the Division of Stem Cell Transplantation and Immunology, Hospital for Children and Adolescents, University Hospital Frankfurt, Frankfurt, Germany (P.B.); the Division of Pediatric Blood and Marrow Transplant, University of Minnesota, Minneapolis (M.R.V., H.E.S.); Children's Mercy Hospital and Clinics, Kansas City, MO (G.D.M.); Aflac Cancer and Blood Disorders Center, Emory University, Atlanta (M.Q.); the Department of Pediatric Hematology-Oncology and Stem Cell Transplantation, Ghent University Hospital, and the Cancer Research Institute Ghent (CRIG), Ghent, Belgium (B.D.M.); the Department of Pediatrics, Graduate School of Medicine Kyoto University, Kyoto, Japan (H.H.); the Department of Pediatrics, Stanford University School of Medicine, Stanford (K. Schlis, K.L.D.), and the Division of Hematology, Oncology, Blood and Marrow Transplant, Children's Hospital Los Angeles, USC Keck School of Medicine, Los Angeles (M.A.P.) - all in California; the Division of Pediatric Blood and Marrow Transplant, Duke University Medical Center, Durham, NC (P.L.M.); Oregon Health and Science University, Portland (E.R.N.); C.S. Mott Children's Hospital, Ann Arbor, MI (G.A.Y.); the Stem Cell Transplantation Unit, St. Anna Children's Hospital, Vienna (C.P.); University Hospital Robert Debré and University Paris Diderot (A. Baruchel), and Saint-Louis Hospital and University Paris Diderot (N.B.), Paris; the Royal Children's Hospital, Melbourne, VIC, Australia (F.M.); Clinica Pediatrica Universita degli Studi di Milano Bicocca, Monza, Italy (A. Balduzzi); and Novartis Pharmaceuticals (P.W., T.T., M.L., Y.Z., K. Sen, D.L.) and Novartis Institutes for Biomedical Research (K.T.M.) - both in East Hanover, NJ.
Shannon L Maude et al. N Engl J Med. 2018.
Affiliation
1 From the Departments of Pediatrics (S.L.M., S.A.G.) and Pathology and Laboratory Medicine (C.H.J., B.L.L.), Perelman School of Medicine, and Abramson Cancer Center (C.H.J., B.L.L.), University of Pennsylvania, and the Division of Oncology, Center for Childhood Cancer Research and Cancer Immunotherapy Program, Children's Hospital of Philadelphia (S.L.M., S.A.G.) - all in Philadelphia; the Department of Pediatrics and Harold C. Simmons Comprehensive Cancer Center, University of Texas Southwestern Medical Center, and the Pauline Allen Gill Center for Cancer and Blood Disorders, Children's Health, Dallas (T.W.L.); the Department of Pediatric Hematology and Oncology, Oslo University Hospital, Oslo (J.B.); the Department of Pediatric Hematology and Oncology, Hospital Sant Joan de Deu Barcelona, Barcelona (S.R.); the Department of Pediatrics and Internal Medicine, University of Utah, Salt Lake City (M.B.); the Department of Pediatrics, Faculty of Medicine, University of Montreal, and the Hematology Oncology Division and Charles-Bruneau Cancer Center, Centre Hospitalier Universitaire Sainte-Justine Research Center, Montreal (H.B.), and the Division of Haematology/Oncology/Bone Marrow Transplantation, Hospital for Sick Children, Toronto (J.K.) - all in Canada; the Division of Stem Cell Transplantation and Immunology, Hospital for Children and Adolescents, University Hospital Frankfurt, Frankfurt, Germany (P.B.); the Division of Pediatric Blood and Marrow Transplant, University of Minnesota, Minneapolis (M.R.V., H.E.S.); Children's Mercy Hospital and Clinics, Kansas City, MO (G.D.M.); Aflac Cancer and Blood Disorders Center, Emory University, Atlanta (M.Q.); the Department of Pediatric Hematology-Oncology and Stem Cell Transplantation, Ghent University Hospital, and the Cancer Research Institute Ghent (CRIG), Ghent, Belgium (B.D.M.); the Department of Pediatrics, Graduate School of Medicine Kyoto University, Kyoto, Japan (H.H.); the Department of Pediatrics, Stanford University School of Medicine, Stanford (K. Schlis, K.L.D.), and the Division of Hematology, Oncology, Blood and Marrow Transplant, Children's Hospital Los Angeles, USC Keck School of Medicine, Los Angeles (M.A.P.) - all in California; the Division of Pediatric Blood and Marrow Transplant, Duke University Medical Center, Durham, NC (P.L.M.); Oregon Health and Science University, Portland (E.R.N.); C.S. Mott Children's Hospital, Ann Arbor, MI (G.A.Y.); the Stem Cell Transplantation Unit, St. Anna Children's Hospital, Vienna (C.P.); University Hospital Robert Debré and University Paris Diderot (A. Baruchel), and Saint-Louis Hospital and University Paris Diderot (N.B.), Paris; the Royal Children's Hospital, Melbourne, VIC, Australia (F.M.); Clinica Pediatrica Universita degli Studi di Milano Bicocca, Monza, Italy (A. Balduzzi); and Novartis Pharmaceuticals (P.W., T.T., M.L., Y.Z., K. Sen, D.L.) and Novartis Institutes for Biomedical Research (K.T.M.) - both in East Hanover, NJ.
Background: In a single-center phase 1-2a study, the anti-CD19 chimeric antigen receptor (CAR) T-cell therapy tisagenlecleucel produced high rates of complete remission and was associated with serious but mainly reversible toxic effects in children and young adults with relapsed or refractory B-cell acute lymphoblastic leukemia (ALL).
Methods: We conducted a phase 2, single-cohort, 25-center, global study of tisagenlecleucel in pediatric and young adult patients with CD19+ relapsed or refractory B-cell ALL. The primary end point was the overall remission rate (the rate of complete remission or complete remission with incomplete hematologic recovery) within 3 months.
Results: For this planned analysis, 75 patients received an infusion of tisagenlecleucel and could be evaluated for efficacy. The overall remission rate within 3 months was 81%, with all patients who had a response to treatment found to be negative for minimal residual disease, as assessed by means of flow cytometry. The rates of event-free survival and overall survival were 73% (95% confidence interval [CI], 60 to 82) and 90% (95% CI, 81 to 95), respectively, at 6 months and 50% (95% CI, 35 to 64) and 76% (95% CI, 63 to 86) at 12 months. The median duration of remission was not reached. Persistence of tisagenlecleucel in the blood was observed for as long as 20 months. Grade 3 or 4 adverse events that were suspected to be related to tisagenlecleucel occurred in 73% of patients. The cytokine release syndrome occurred in 77% of patients, 48% of whom received tocilizumab. Neurologic events occurred in 40% of patients and were managed with supportive care, and no cerebral edema was reported.
Conclusions: In this global study of CAR T-cell therapy, a single infusion of tisagenlecleucel provided durable remission with long-term persistence in pediatric and young adult patients with relapsed or refractory B-cell ALL, with transient high-grade toxic effects. (Funded by Novartis Pharmaceuticals; ClinicalTrials.gov number, NCT02435849 .).
Figure 1. Screening, Enrollment, Treatment, and Follow-up
Figure 1. Screening, Enrollment, Treatment, and Follow-up
The first patient’s first visit occurred on April…
The first patient’s first visit occurred on April 8, 2015. The median time from tisagenlecleucel infusion to data cutoff was 13.1 months. The reasons for patients not enrolling in the study after screening included not meeting the inclusion criteria or meeting the exclusion criteria (11 patients, including <5% blasts in the bone marrow in 8 patients), death before acceptance of the apheresis sample at the manufacturing facility (2 patients; 1 who died from pulmonary hemorrhage and 1 who died from multiorgan failure), physician decision (1), and apheresis-related issue (1). All patients who completed screening and whose apheresis product was received and accepted by the manufacturing facility were enrolled in the study. Of the 75 patients who received an infusion, 65 (87%) received bridging chemotherapy between enrollment and infusion, and 72 (96%) received lymphodepleting chemotherapy (fludarabine–cyclophosphamide [71 patients] or cytarabine– etoposide [1]). Seventeen enrolled patients did not receive a tisagenlecleucel infusion because of product-related issues (7 patients), death (7 patients; 4 from disease progression and 1 each from sepsis, respiratory failure, and fungemia), and adverse events (3 patients; 1 each from graft-versus-host disease, systemic mycosis, and fungal pneumonia). Tisagenlecleucel product-related issues included an inability to manufacture as a result of poor cell growth for 6 patients and a technical issue unrelated to cell growth for 1 patient. Patients who received the infusion but discontinued follow-up were followed for survival. At the time of data cutoff, 27 patients had discontinued follow-up owing to death (11 patients; 7 from disease progression and 1 each from encephalitis, cerebral hemorrhage, systemic mycosis, and hepatobiliary disorders related to allogeneic hematopoietic stem-cell transplantation), lack of efficacy (9 patients; nonresponse or relapse), new therapy while in complete remission (5), and patient or guardian decision (2); 48 patients remained in follow-up. ALL denotes acute lymphoblastic leukemia.
Figure 2. Duration of Remission, Event-free Survival,…
Figure 2. Duration of Remission, Event-free Survival, and Overall Survival
Panel A shows the duration of remission, defined as the time to relapse after the onset of remission, in the 61 patients who had a best overall response of either complete remission or complete remission with incomplete hematologic recovery. Panel B shows event-free survival among the 75 patients who received an infusion, defined as the time from tisagenlecleucel infusion to the earliest of the following events: no response (8 patients), relapse before response was maintained for at least 28 days (2), or relapse after having complete remission or complete remission with incomplete hematologic recovery (17). A total of 32 patients had still not had an event at the time of data cutoff. Data for 16 more patients were censored for event-free survival — 8 patients for allogeneic stem-cell transplantation during remission, 7 patients for new cancer therapy other than stem-cell transplantation during remission (4 received humanized anti-CD19 CAR T cells, 1 received ponatinib, 1 received vincristine sulfate and blinatumomab, and 1 received antithymocyte globulin), and 1 patient for lack of adequate assessment. Ten patients were followed for relapse after new therapy, 4 of whom had a relapse or died. Panel B also shows overall survival among the 75 patients who received an infusion from the date of tisagenlecleucel infusion to the date of death from any cause. Nineteen patients died after tisagenlecleucel infusion, and 56 patients had their data censored at the time of the last follow-up. Tick marks indicate the time of censoring.
Sidaway P. Sidaway P. Nat Rev Clin Oncol. 2018 Apr;15(4):199. doi: 10.1038/nrclinonc.2018.32. Epub 2018 Feb 20. Nat Rev Clin Oncol. 2018. PMID: 29459644 No abstract available.
Hiramatsu H, Adachi S, Umeda K, Kato I, Eldjerou L, Agostinho AC, Natsume K, Tokushige K, Watanabe Y, Grupp SA. Hiramatsu H, et al. Int J Hematol. 2020 Feb;111(2):303-310. doi: 10.1007/s12185-019-02771-2. Epub 2019 Nov 11. Int J Hematol. 2020. PMID: 31709501 Clinical Trial.
Maude SL, Frey N, Shaw PA, Aplenc R, Barrett DM, Bunin NJ, Chew A, Gonzalez VE, Zheng Z, Lacey SF, Mahnke YD, Melenhorst JJ, Rheingold SR, Shen A, Teachey DT, Levine BL, June CH, Porter DL, Grupp SA. Maude SL, et al. N Engl J Med. 2014 Oct 16;371(16):1507-17. doi: 10.1056/NEJMoa1407222. N Engl J Med. 2014. PMID: 25317870 Free PMC article. Clinical Trial.
Laetsch TW, Myers GD, Baruchel A, Dietz AC, Pulsipher MA, Bittencourt H, Buechner J, De Moerloose B, Davis KL, Nemecek E, Driscoll T, Mechinaud F, Boissel N, Rives S, Bader P, Peters C, Sabnis HS, Grupp SA, Yanik GA, Hiramatsu H, Stefanski HE, Rasouliyan L, Yi L, Shah S, Zhang J, Harris AC. Laetsch TW, et al. Lancet Oncol. 2019 Dec;20(12):1710-1718. doi: 10.1016/S1470-2045(19)30493-0. Epub 2019 Oct 9. Lancet Oncol. 2019. PMID: 31606419 Free PMC article. Clinical Trial.
Liu Y, Chen X, Han W, Zhang Y. Liu Y, et al. Drugs Today (Barc). 2017 Nov;53(11):597-608. doi: 10.1358/dot.2017.53.11.2725754. Drugs Today (Barc). 2017. PMID: 29451276 Review.
Halford Z, Anderson MK, Bennett LL, Moody J. Halford Z, et al. Ann Pharmacother. 2021 Apr;55(4):466-479. doi: 10.1177/1060028020948165. Epub 2020 Aug 7. Ann Pharmacother. 2021. PMID: 32762363 Review.
Tragiannidis A, Groll AH. Tragiannidis A, et al. Paediatr Drugs. 2021 Jul 22. doi: 10.1007/s40272-021-00461-3. Online ahead of print. Paediatr Drugs. 2021. PMID: 34292515 Review.
Meyer JE, Loff S, Dietrich J, Spehr J, Jurado Jiménez G, von Bonin M, Ehninger G, Cartellieri M, Ehninger A. Meyer JE, et al. Oncoimmunology. 2021 Jul 8;10(1):1945804. doi: 10.1080/2162402X.2021.1945804. eCollection 2021. Oncoimmunology. 2021. PMID: 34290907 Free PMC article.
Mohty R, Gauthier J. Mohty R, et al. Bone Marrow Transplant. 2021 Jul 21. doi: 10.1038/s41409-021-01420-9. Online ahead of print. Bone Marrow Transplant. 2021. PMID: 34290380 Review.
Wang L, Hong R, Zhou L, Ni F, Zhang M, Zhao H, Wu W, Wang Y, Ding S, Chang AH, Hu Y, Huang H. Wang L, et al. Front Oncol. 2021 Jun 30;11:702644. doi: 10.3389/fonc.2021.702644. eCollection 2021. Front Oncol. 2021. PMID: 34277448 Free PMC article.
Meng Y, Deng B, Rong L, Li C, Song W, Ling Z, Xu J, Duan J, Wang Z, Chang AH, Feng X, Xiong X, Chen X, Pan J. Meng Y, et al. Front Oncol. 2021 Jun 30;11:640166. doi: 10.3389/fonc.2021.640166. eCollection 2021. Front Oncol. 2021. PMID: 34277400 Free PMC article.

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