Neuropathological spectrum of anti-IgLON5 disease and stages of brainstem tau pathology: updated neuropathological research criteria of the disease-related tauopathy

Acta Neuropathol. 2024 Oct 14;148(1):53. doi: 10.1007/s00401-024-02805-y.

Abstract

Anti-IgLON5 disease is a unique condition that bridges autoimmunity and neurodegeneration. Since its initial description 10 years ago, an increasing number of autopsies has led to the observation of a broader spectrum of neuropathologies underlying a particular constellation of clinical symptoms. In this study, we describe the neuropathological findings in 22 patients with anti-IgLON5 disease from 9 different European centers. In 15 patients (68%), we observed a hypothalamic and brainstem-predominant tauopathy of varying severity in which the original research neuropathological criteria were readily applicable. This pathology was observed in younger patients (median age at onset 61 years) with a long disease duration (median 9 years). In contrast, in 7 (32%) patients, the originally described brainstem tauopathy was nearly absent or only minimal in the form of delicate threads, despite mild-to-moderate neurodegenerative features, consistent clinical symptoms and the presence of anti-IgLON5 antibodies in CSF and serum. These patients were older at onset (median 79 years) and had shorter disease duration (median < 1 year). Overall, about one-third of the patients showed concomitant TDP-43 pathology within the regions affected by tau pathology and/or neurodegeneration. Based on these observations and in view of the spectrum of the tau burden in the core regions involved in the disease, we propose a simple staging system: stage 1 mild neurodegeneration without overt or only minimal tau pathology, stage 2 moderate neurodegeneration and mild/ moderate tauopathy and stage 3 prominent neurodegeneration and tau pathology. This staging intends to reflect a potential (age- and time-dependent) progression of tau pathology, supporting the current notion that tau accumulation is a secondary phenomenon related to the presence of anti-IgLON5 antibodies in the CNS. Finally, we adapt the original research criteria of the anti-IgLON5 disease-related tauopathy to include the spectrum of pathologies observed in this larger postmortem series.

Keywords: 3R; 4R tau; ALS; Anti-IgLON5 disease; Anti-IgLON5 tauopathy; Atypical; Brainstem tauopathy; Dementia; IgLON5; Motor neuron disease; Neuropathology; PSP; Stages; TDP-43.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Autoantibodies / immunology
  • Brain Stem* / immunology
  • Brain Stem* / metabolism
  • Brain Stem* / pathology
  • Cell Adhesion Molecules, Neuronal* / immunology
  • Cell Adhesion Molecules, Neuronal* / metabolism
  • DNA-Binding Proteins / metabolism
  • Female
  • Humans
  • Male
  • Middle Aged
  • Tauopathies* / immunology
  • Tauopathies* / pathology
  • tau Proteins* / immunology
  • tau Proteins* / metabolism

Substances

  • IgLON5 protein, human
  • tau Proteins
  • Cell Adhesion Molecules, Neuronal
  • Autoantibodies
  • DNA-Binding Proteins
  • TARDBP protein, human