Beyond T cell toxicity - Intrathecal chemokine CXCL13 indicating B cell involvement in immune-related adverse events following checkpoint inhibition: A two-case series and literature review

Eur J Neurol. 2024 Jul;31(7):e16279. doi: 10.1111/ene.16279. Epub 2024 Mar 31.

Abstract

Background and purpose: This study was undertaken to raise awareness of a role of B cells in immune checkpoint inhibitor (ICI)-associated neurological immune-related adverse events (nirAE).

Methods: A systematic literature review was made, with case observations of a melanoma and a non-small cell lung cancer (NSCLC) patient who developed ICI-associated nirAE with cerebrospinal fluid (CSF) findings indicating B cell involvement.

Results: Two patients receiving ipilimumab/nivolumab for melanoma and chemotherapy/pembrolizumab for NSCLC developed nirAE in the form of myocarditis/myositis/myasthenia gravis overlap syndrome (triple M) and cerebellitis plus longitudinal transverse myelitis (c-LETM), respectively. Intrathecal inflammation with chemokine C-X-C motif ligand (CXCL13) elevation was present in both patients; the triple M case had acetylcholine receptor antibodies, antititin reactivity, altered CD4/CD8 T cell ratio in blood, and depressed programmed death-1 (PD-1) expression on CSF T cells; the c-LETM case showed intrathecal antibody production and plasma cells. Both patients insufficiently responded to first-line treatment. The NSCLC case improved upon administration of B cell-depleting therapy with rituximab, whereas the melanoma patient died before escalation therapy was initiated. Literature research revealed one additional ICI-associated LETM case with intrathecal CXCL13 elevation, three cases with ICI-associated aquaporin-4 antibody neuromyelitis spectrum disorder, and evidence of B cell-mediated toxicity based on antibody-mediated immune pathologies in ICI-associated immune-related adverse events.

Conclusions: The case observations highlight the plethora of uncertainties in diagnosis and treatment of ICI-associated nirAE, exemplify the heterogeneity of immune mechanisms involved, and suggest a role of B cells, which may be underdiagnosed. Intrathecal CXCL13 may serve as a biomarker of B cell involvement in nirAE, supported by intrathecal immunoglobulin synthesis, presence of plasma cells, and/or recruitment of cognate immune cells.

Keywords: cerebrospinal fluid; chemokine CXCL13; immune checkpoint inhibitor; immune‐related neurological adverse events.

Publication types

  • Case Reports
  • Systematic Review

MeSH terms

  • Aged
  • Antibodies, Monoclonal, Humanized / administration & dosage
  • Antibodies, Monoclonal, Humanized / adverse effects
  • B-Lymphocytes* / drug effects
  • B-Lymphocytes* / immunology
  • Chemokine CXCL13* / cerebrospinal fluid
  • Female
  • Humans
  • Immune Checkpoint Inhibitors* / adverse effects
  • Ipilimumab / administration & dosage
  • Ipilimumab / adverse effects
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / immunology
  • Melanoma / drug therapy
  • Myelitis, Transverse / chemically induced
  • Myelitis, Transverse / immunology
  • Nivolumab / administration & dosage
  • Nivolumab / adverse effects
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology

Substances

  • Antibodies, Monoclonal, Humanized
  • Chemokine CXCL13
  • CXCL13 protein, human
  • Immune Checkpoint Inhibitors
  • Ipilimumab
  • Nivolumab
  • pembrolizumab

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