Clinical and Biological Correlates of Neurotoxicity Associated with CAR T-cell Therapy in Patients with B-cell Acute Lymphoblastic Leukemia

Cancer Discov. 2018 Aug;8(8):958-971. doi: 10.1158/2159-8290.CD-17-1319. Epub 2018 Jun 7.

Abstract

CD19-specific chimeric antigen receptor (CAR) T-cell therapy is highly effective against relapsed or refractory acute lymphoblastic leukemia (ALL), but is hindered by neurotoxicity. In 53 adult patients with ALL, we found a significant association of severe neurotoxicity with high pretreatment disease burden, higher peak CAR T-cell expansion, and early and higher elevations of proinflammatory cytokines in blood. Patients with severe neurotoxicity had evidence of blood-cerebrospinal fluid (CSF) barrier disruption correlating with neurotoxicity grade without association with CSF white blood cell count or CAR T-cell quantity in CSF. Proinflammatory cytokines were enriched in CSF during severe neurotoxicity with disproportionately high levels of IL6, IL8, MCP1, and IP10, suggesting central nervous system-specific production. Seizures, seizure-like activity, myoclonus, and neuroimaging characteristics suggested excitatory neurotoxicity, and we found elevated levels of endogenous excitatory agonists in CSF during neurotoxicity.Significance: We detail the neurologic symptoms and blood, CSF, and neuroimaging correlates of neurotoxicity associated with CD19 CAR T cells and identify neurotoxicity risk factors. Our findings implicate cellular components other than T cells and suggest novel links between systemic inflammation and characteristic neurotoxicity symptoms. Cancer Discov; 8(8); 958-71. ©2018 AACR.This article is highlighted in the In This Issue feature, p. 899.

Publication types

  • Clinical Trial, Phase I
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer / adverse effects*
  • Adrenal Cortex Hormones / therapeutic use
  • Adult
  • Antibodies, Monoclonal, Humanized / therapeutic use
  • Antigens, CD19 / immunology*
  • Cytokines / blood
  • Cytokines / cerebrospinal fluid*
  • Female
  • Humans
  • Magnetic Resonance Imaging / methods
  • Male
  • Middle Aged
  • Neuroimaging / methods
  • Neurotoxicity Syndromes / cerebrospinal fluid
  • Neurotoxicity Syndromes / diagnostic imaging*
  • Neurotoxicity Syndromes / drug therapy
  • Neurotoxicity Syndromes / etiology
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma / immunology
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma / pathology
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma / therapy*
  • Receptors, Antigen, T-Cell / metabolism
  • T-Lymphocytes / immunology
  • T-Lymphocytes / transplantation*
  • Tumor Burden
  • Young Adult

Substances

  • Adrenal Cortex Hormones
  • Antibodies, Monoclonal, Humanized
  • Antigens, CD19
  • CD19 molecule, human
  • Cytokines
  • Receptors, Antigen, T-Cell
  • tocilizumab