Management of cytokine release syndrome and neurotoxicity in chimeric antigen receptor (CAR) T cell therapy

References

• Maude SL, Teachey DT, Porter DL, et al. CD19-targeted chimeric antigen receptor T-cell therapy for acute lymphoblastic leukemia. Blood. 2015;125(26):4017–4023.
   PubMed Web of Science ®Google Scholar
• Ruella M, Kalos M. Adoptive immunotherapy for cancer. Immunol Rev. 2014;257(1):14–38.
   PubMed Web of Science ®Google Scholar
• June CH, Sadelain M. Chimeric antigen receptor therapy. N Engl J Med. 2018;379(1):64–73.
   PubMed Web of Science ®Google Scholar
• Lee DW, Kochenderfer JN, Stetler-Stevenson M, et al. T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: A phase 1 dose-escalation trial. Lancet. 2015;385(9967):517–528.
   PubMed Web of Science ®Google Scholar
• Grupp SA, Kalos M, Barrett D, et al. Chimeric antigen receptor–modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368(16):1509–1518.
   PubMed Web of Science ®Google Scholar
• Brentjens RJ, Davila ML, Riviere I, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med. 2013;5(177):138–177.
   Web of Science ®Google Scholar
• Porter DL, Levine BL, Kalos M, et al. Chimeric antigen receptor–modified T cells in Chronic Lymphoid leukemia. N Engl J Med. 2011;365(8):725–733.
   PubMed Web of Science ®Google Scholar
• Kochenderfer JN, Dudley ME, Feldman SA, et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor–transduced T cells. Blood. 2012;119(12):2709–2720.
   PubMed Web of Science ®Google Scholar
• Davila ML, Riviere I, Wang X, et al. Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med. 2014;6(224):224ra25.
   PubMed Web of Science ®Google Scholar
• Turtle CJ, Hay KA, Hanafi L-A, et al. Durable molecular remissions in chronic lymphocytic leukemia treated with CD19-specific chimeric antigen receptor–modified T cells after failure of ibrutinib. J Clin Oncol. 2017;35(26):3010–3020.
   PubMed Web of Science ®Google Scholar
• Turtle CJ, Hanafi L-A, Berger C, et al. CD19 CAR–T cells of defined CD4+: CD8+composition in adult B cell ALL patients. J Clin Invest. 2016;126(6):2123–2138.
   PubMed Web of Science ®Google Scholar
• Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371(16):1507–1517.
   PubMed Web of Science ®Google Scholar
• Neelapu SS, Locke FL, Bartlett NL, et al. Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma. N Engl J Med. 2017;377(26):2531–2544.
   PubMed Web of Science ®Google Scholar
• Schuster SJ, Svoboda J, Chong EA, et al. Chimeric antigen receptor T cells in refractory B-cell lymphomas. N Engl J Med. 2017;377(26):2545–2554.
   PubMed Web of Science ®Google Scholar
• Brudno JN, Kochenderfer JN. Toxicities of chimeric antigen receptor T cells: Recognition and management. Blood. 2016;127(26):3321–3330.
   PubMed Web of Science ®Google Scholar
• Xu X-J, Tang Y-M. Cytokine release syndrome in cancer immunotherapy with chimeric antigen receptor engineered T cells. Cancer Lett. 2014;343(2):172–178.
   PubMed Web of Science ®Google Scholar
• Namuduri M, Brentjens RJ. Medical management of side effects related to CAR T cell therapy in hematologic malignancies. Expert Rev Hematol. 2016;9(6):511–513.
   PubMed Web of Science ®Google Scholar
• Hay KA, Hanafi L-A, Li D, et al. Kinetics and biomarkers of severe cytokine release syndrome after CD19 chimeric antigen receptor-modified T cell therapy. Blood. 2017;130(21):2295–2306.
   PubMed Web of Science ®Google Scholar
• CAR T cells infiltrate brain, safely target tumors. Cancer Discov. 2017. Available from: http://cancerdiscovery.aacrjournals.org/content/early/2017/07/28/2159-8290.CD-NB2017-109
   Google Scholar
• Raje NS, Berdeja JG, Lin Y, et al. bb2121 anti-BCMA CAR T-cell therapy in patients with relapsed/refractory multiple myeloma: Updated results from a multicenter phase I study. J clin oncol. 2018;36(15_suppl):8007.
   Google Scholar
• Foster JB, Maude SL. New developments in immunotherapy for pediatric leukemia. Curr Opin Pediatr. 2018;30(1):25–29.
   PubMed Web of Science ®Google Scholar
• Ruella M, Gill S. How to train your T cell: Genetically engineered chimeric antigen receptor T cells versus bispecific T-cell engagers to target CD19 in B acute lymphoblastic leukemia. Expert Opin Biol Ther. 2015;15(6):761–766.
   PubMed Web of Science ®Google Scholar
• Giavridis T, Sjc VDS, Eyquem J, et al. CAR T cell–induced cytokine release syndrome is mediated by macrophages and abated by IL-1 blockade. Nat Med. 2018;24(6):731–738.
   PubMed Web of Science ®Google Scholar
• Norelli M, Camisa B, Barbiera G, et al. Monocyte-derived IL-1 and IL-6 are differentially required for cytokine-release syndrome and neurotoxicity due to CAR T cells. Nat Med. 2018;24(6):739–748.
   PubMed Web of Science ®Google Scholar
• Neelapu SS, Tummala S, Kebriaei P, et al. Chimeric antigen receptor T-cell therapy — assessment and management of toxicities. Nat Rev Clin Oncol. 2018;15(1):47–62.
   Web of Science ®Google Scholar
• Taraseviciute A, Tkachev V, Ponce R, et al. Chimeric antigen receptor T cell–mediated neurotoxicity in nonhuman primates. Cancer Discov. 2018;8(6):750–763.
   PubMed Web of Science ®Google Scholar
• Singh N, Hofmann TJ, Gershenson Z, et al. Monocyte lineage-derived IL-6 does not affect chimeric antigen receptor T-cell function. Cytotherapy. 2017;19(7):867–880.
   PubMed Web of Science ®Google Scholar
• Kalos M, Levine BL, Porter DL, et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med. 2011;3(95):95ra73.
   PubMed Web of Science ®Google Scholar
• Lee DW, Gardner R, Porter DL, et al. Current concepts in the diagnosis and management of cytokine release syndrome. Blood. 2014;124(2):188–195.
   PubMed Web of Science ®Google Scholar
• Obstfeld AE, Frey NV, Mansfield K, et al. Cytokine release syndrome associated with chimeric-antigen receptor T-cell therapy: Clinicopathological insights. Blood. 2017;130(23):2569–2572.
   PubMed Web of Science ®Google Scholar
• Gust J, Hay KA, Hanafi L-A, et al. Endothelial activation and blood–brain barrier disruption in neurotoxicity after adoptive immunotherapy with CD19 CAR-T cells. Cancer Discov. 2017;7(12):1404–1419.
   PubMed Web of Science ®Google Scholar
• Porter DL, Hwang W-T, Frey NV, et al. Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci Transl Med. 2015;7(303):303ra139.
   PubMed Web of Science ®Google Scholar
• Abramson JS, Palomba L, Gordon LI, et al. Transcend NHL 001: Immunotherapy with the CD19-directed CAR T-cell product JCAR017 results in high complete response rates in relapsed or refractory B-cell non-Hodgkin lymphoma. Blood. 2016;128(22):4192.
   Web of Science ®Google Scholar
• Fitzgerald JC, Weiss SL, Maude SL, et al. Cytokine release syndrome after chimeric antigen receptor T cell therapy for acute lymphoblastic leukemia. Crit Care Med. 2017;45(2):e124–31.
   PubMed Web of Science ®Google Scholar
• Lee DW, Santomasso BD, Locke FL, et al. ASBMT consensus grading for cytokine release syndrome and neurologic toxicity associated with immune effector cells. Biol Blood Marrow Transplant. 2018 Dec 25. pii: S1083-8791(18)31691-4. doi: 10.1016/j.bbmt.2018.12.758. [Epub ahead of print]
   Google Scholar
• Morgan RA, Yang JC, Kitano M, et al. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther. 2010;18(4):843–851.
   PubMed Web of Science ®Google Scholar
• Kochenderfer JN, Wilson WH, Janik JE, et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood. 2010;116(20):4099–4102.
   PubMed Web of Science ®Google Scholar
• Brentjens R, Yeh R, Bernal Y, et al. Treatment of chronic lymphocytic leukemia with genetically targeted autologous T cells: Case report of an unforeseen adverse event in a Phase I clinical trial. Mol Ther. 2010;18(4):666–668.
   PubMed Web of Science ®Google Scholar
• Teachey DT, Lacey SF, Shaw PA, et al. Identification of predictive biomarkers for cytokine release syndrome after chimeric antigen receptor T-cell therapy for acute lymphoblastic leukemia. Cancer Discov. 2016;6(6):664–679.
   PubMed Web of Science ®Google Scholar
• Schultz DR, Arnold PI. Properties of four acute phase proteins: C-reactive protein, serum amyloid A protein, alpha 1-acid glycoprotein, and fibrinogen. Semin Arthritis Rheum. 1990;20(3):129–147.
   PubMed Web of Science ®Google Scholar
• Pepys MB, Hirschfield GM. C-reactive protein: A critical update. J Clin Invest. 2003;111(12):1805–1812.
   PubMed Web of Science ®Google Scholar
• Locke FL, Neelapu SS, Bartlett NL, et al. Phase 1 results of ZUMA-1: A multicenter study of KTE-C19 Anti-CD19 CAR T cell therapy in refractory aggressive lymphoma. Mol Ther. 2017;25(1):285–295.
   PubMed Web of Science ®Google Scholar
• Hu Y, Sun J, Wu Z, et al. Predominant cerebral cytokine release syndrome in CD19-directed chimeric antigen receptor-modified T cell therapy. J Hematol Oncol. 2016;9(1):70.
   PubMedGoogle Scholar
• Fry TJ, Shah NN, Orentas RJ, et al. CD22-targeted CAR T cells induce remission in B-ALL that is naive or resistant to CD19-targeted CAR immunotherapy. Nat Med. 2018;24(1):20–28.
   PubMed Web of Science ®Google Scholar
• Locke FL, Neelapu SS, Bartlett NL, et al. Clinical and biologic covariates of outcomes in ZUMA-1: A pivotal trial of axicabtagene ciloleucel (axi-cel; KTE-C19) in patients with refractory aggressive non-Hodgkin lymphoma (r-NHL). J clin oncol. 2017;35(15_suppl):7512.
   Google Scholar
• Maude SL, Laetsch TW, Buechner J, et al. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med. 2018;378(5):439–448.
   PubMed Web of Science ®Google Scholar
• Gofshteyn JS, Shaw PA, Teachey DT, et al. Neurotoxicity after CTL019 in a pediatric and young adult cohort. Ann Neurol. 2018;84(4):537–546.
   PubMed Web of Science ®Google Scholar
• Jones G, Tocilizumab: DC. A review of its safety and efficacy in rheumatoid arthritis. Clin Med Insights Arthritis Musculoskelet Disord. 2010;3:81–89.
   PubMedGoogle Scholar
• Oldfield V, Dhillon S, Plosker GL. Tocilizumab. Drugs. 2009;69(5):609–632.
   PubMed Web of Science ®Google Scholar
• Teachey DT, Rheingold SR, Maude SL, et al. Cytokine release syndrome after blinatumomab treatment related to abnormal macrophage activation and ameliorated with cytokine-directed therapy. Blood. 2013;121(26):5154–5157.
   PubMed Web of Science ®Google Scholar
• Lang VR, Englbrecht M, Rech J, et al. Risk of infections in rheumatoid arthritis patients treated with tocilizumab. Rheumatology. 2012;51(5):852–857.
   PubMed Web of Science ®Google Scholar
• Actemra [package insert]. San Francisco, CA: Genentech, Inc.; 2018.
   Google Scholar
• Yescarta [package insert]. Santa Monica, CA: Kite Pharma, Inc.; 2017.
   Google Scholar
• Liu Y-C, Stone K, van Rhee F. Siltuximab for multicentric Castleman disease. Expert Rev Hematol. 2014;7(5):545–557.
   PubMed Web of Science ®Google Scholar
• Williams SCP. First IL-6-blocking drug nears approval for rare blood disorder. Nat Med. 2013;19(10):1193.
   PubMed Web of Science ®Google Scholar