The clinical efficacy of first-generation carcinoembryonic antigen (CEACAM5)-specific CAR T cells is limited by poor persistence and transient pre-conditioning-dependent respiratory toxicity

Cancer Immunol Immunother. 2017 Nov;66(11):1425-1436. doi: 10.1007/s00262-017-2034-7. Epub 2017 Jun 28.

Abstract

The primary aim of this clinical trial was to determine the feasibility of delivering first-generation CAR T cell therapy to patients with advanced, CEACAM5+ malignancy. Secondary aims were to assess clinical efficacy, immune effector function and optimal dose of CAR T cells. Three cohorts of patients received increasing doses of CEACAM5+-specific CAR T cells after fludarabine pre-conditioning plus systemic IL2 support post T cell infusion. Patients in cohort 4 received increased intensity pre-conditioning (cyclophosphamide and fludarabine), systemic IL2 support and CAR T cells. No objective clinical responses were observed. CAR T cell engraftment in patients within cohort 4 was significantly higher. However, engraftment was short-lived with a rapid decline of systemic CAR T cells within 14 days. Patients in cohort 4 had transient, acute respiratory toxicity which, in combination with lack of prolonged CAR T cell persistence, resulted in the premature closure of the trial. Elevated levels of systemic IFNγ and IL-6 implied that the CEACAM5-specific T cells had undergone immune activation in vivo but only in patients receiving high-intensity pre-conditioning. Expression of CEACAM5 on lung epithelium may have resulted in this transient toxicity. Raised levels of serum cytokines including IL-6 in these patients implicate cytokine release as one of several potential factors exacerbating the observed respiratory toxicity. Whilst improved CAR designs and T cell production methods could improve the systemic persistence and activity, methods to control CAR T 'on-target, off-tissue' toxicity are required to enable a clinical impact of this approach in solid malignancies.

Keywords: CEA; Chimeric antigen receptor; Persistence; T cells; Toxicity.

Publication types

  • Clinical Trial, Phase I

MeSH terms

  • Abdominal Pain / etiology
  • Adult
  • Aged
  • Anemia / etiology
  • Carcinoembryonic Antigen / genetics
  • Carcinoembryonic Antigen / immunology*
  • Carcinoembryonic Antigen / metabolism
  • Cohort Studies
  • Cyclophosphamide / administration & dosage
  • Cyclophosphamide / adverse effects
  • Drug Resistance, Neoplasm
  • Female
  • GPI-Linked Proteins / genetics
  • GPI-Linked Proteins / immunology
  • GPI-Linked Proteins / metabolism
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Immunotherapy, Adoptive / adverse effects
  • Immunotherapy, Adoptive / methods*
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism
  • Interleukin-6 / immunology
  • Interleukin-6 / metabolism
  • Lung / metabolism
  • Male
  • Middle Aged
  • Myeloablative Agonists / adverse effects
  • Myeloablative Agonists / agonists
  • Neoplasms / genetics
  • Neoplasms / immunology
  • Neoplasms / therapy*
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology*
  • Receptors, Antigen, T-Cell / metabolism
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / transplantation
  • Treatment Outcome
  • Vidarabine / administration & dosage
  • Vidarabine / adverse effects
  • Vidarabine / analogs & derivatives
  • Vomiting / etiology

Substances

  • CEACAM5 protein, human
  • Carcinoembryonic Antigen
  • GPI-Linked Proteins
  • Interleukin-6
  • Myeloablative Agonists
  • Receptors, Antigen, T-Cell
  • Interferon-gamma
  • Cyclophosphamide
  • Vidarabine
  • fludarabine