Clinical and Biological Correlates of Neurotoxicity Associated with CAR T-cell Therapy in Patients with B-cell Acute Lymphoblastic Leukemia
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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
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Clinical-pathologic correlation in these individuals resulted in valuable observations that may be instructive in understanding mechanisms of immune-induced pathologies, including those of checkpoint inhibitors, CAR-T cells, and infections such as COVID-19.
“Clinical–pathologic correlation in these individuals resulted in valuable observations that may be instructive in understanding mechanisms of immune-induced pathologies, including those of checkpoint inhibitors, CAR-T cells, and infections such as COVID-19, known to target mucosal tissues and cause severe CRS [1, 5, 8, 18, 19].”
From Immune reconstitution and clinical recovery following anti-CD28 antibody (TGN1412)-induced cytokine storm (2021) · cites this paper as [8]
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Experimental — accuracy not yet measuredCytokine release syndrome and neurotoxicity are the most serious immune-related adverse events, and they are most prominently reported in patients given CAR-T cells.
“The most severe of these immune-related adverse events (irAEs) are cytokine release syndrome (CRS) and neurotoxicity, most prominently described in patients treated with CAR-T-cells [6–11].”
From Immune reconstitution and clinical recovery following anti-CD28 antibody (TGN1412)-induced cytokine storm (2021) · cites this paper as [8]
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- Authors
- Santomasso, B. D., Park, J. H., Salloum, D., Riviere, I., Flynn, J., Mead, E., Halton, E., Wang, X., Senechal, B., Purdon, T., Cross, J. R., Liu, H., Vachha, B., Chen, X., DeAngelis, L. M., Li, D., Bernal, Y., Gonen, M., Wendel, H.-G., Sadelain, M., & Brentjens, R. J.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- 6Center for Cell Engineering, Memorial Sloan Kettering Cancer Center, New York, New York.
- Juno Therapeutics (United States) (US)
- 9Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, New York.
- Corresponding author
- Park, Jae H.
- Brentjens, Renier J.
- ORCID
- Venue
- Cancer Discovery
- Published
- 2018-08-01
- Volume
- 8
- Issue
- 8
- Pages
- 958-971
- ISSN
- 2159-8274 (ISSN-L)
- 2159-8290
- PMC
- PMC6385599
- OpenAlex
- W2805523469
- Cited by
- 942
- References
- 47
- Citations by year
- 2026: 92 · 2025: 110 · 2024: 116 · 2023: 122 · 2022: 123 · 2021: 153 · 2020: 140 · 2019: 69 · 2018: 16
- FWCI
- 35.54
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cancer Discovery (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (5P01 CA0237669-38, 5P01 CA190174-02, 1P50 CA192937-01A1)
- Carson Family Charitable Trust
- Emerald Foundation
- Mr. and Mrs. Goodwyn Commonwealth Fund
- Canada Club of New York
- William Laurence and Blanche Hughes Foundation
- Experimental Therapeutics Center of Memorial Sloan Kettering Cancer Center
- Juno Therapeutics
- Lake Road Foundation
- Memorial Sloan Kettering Cancer Center (P30 CA008748)
- Parker Institute for Cancer Immunotherapy
- American Society of Clinical Oncology
- American Society of Hematology
- Leukemia and Lymphoma Society
- National Comprehensive Cancer Center
- Topics
- Health Sciences › Medicine › Oncology › CAR-T cell therapy research
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Acute Lymphoblastic Leukemia research
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Keywords
- CAR T-cell therapy, neurotoxicity, CD19, B-cell acute lymphoblastic leukemia, inflammatory cytokines, cerebrospinal fluid, interleukin-6, interleukin-8, MCP-1, CXCL10, seizures, myoclonus, systemic inflammation, CAR-T cell expansion, disease burden
- MeSH terms
- Adrenal Cortex Hormones, Adult, Female, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Receptors, Antigen, T-Cell, T-Lymphocytes, Precursor B-Cell Lymphoblastic Leukemia-Lymphoma, Cytokines, Antigens, CD19, Adoptive Transfer, Neurotoxicity Syndromes, Tumor Burden, Young Adult, Neuroimaging, Antibodies, Monoclonal, Humanized
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