Brain histopathology in patients with systemic lupus erythematosus: identification of lesions associated with clinical neuropsychiatric lupus syndromes and the role of complement

Rheumatology (Oxford). 2017 Jan;56(1):77-86. doi: 10.1093/rheumatology/kew341. Epub 2016 Oct 25.

Abstract

Objectives: Neuropsychiatric (NP) involvement is a poorly understood manifestation of SLE. We studied post-mortem histopathology in relation to clinical NPSLE syndromes and complement deposition in brains of NPSLE and SLE patients and controls. Furthermore, we investigated the correlation between cerebral post-mortem histopathology and ex vivo 7 T MRI findings in SLE and NPSLE.

Methods: A nationwide search for autopsy material yielded brain tissue from 16 NPSLE and 18 SLE patients. Brains obtained from 24 patients who died of acute cardiac events served as controls. Apart from a histopathological evaluation, paraffin-embedded cortical tissue was stained for components of the classical, lectin and terminal complement pathways.

Results: Diffuse vasculopathy, microinfarction, macroinfarction, vasculitis and microthrombi occurred significantly more often in NPSLE than SLE patients and were absent in controls. Focal vasculopathy was found in both SLE patients and controls. Complement deposition was strongly associated with both SLE and NPSLE, but not with controls (P < 0.001). Microthrombi were found uniquely in NPSLE and were associated with C4d and C5b-9 deposits (P < 0.05). A 7 T MRI was unable to detect most small vessel injury that was visible histopathologically.

Conclusion: Our study demonstrates that histopathological lesions in NPSLE represent a continuum, ranging from non-specific lesions such as focal vasculopathy, to more specific lesions including C4d- and C5b-9-associated microthrombi and diffuse vasculopathy related to clinical syndromes defining NPSLE. Complement deposition may be a key factor in the interaction between circulating autoantibodies and thromboischaemic lesions observed in NPSLE. Therefore, complement inhibition may have novel therapeutic potential in NPSLE.

Keywords: complement; histology; neuropsychiatric lupus; systemic lupus erythematosus.

MeSH terms

  • Adult
  • Aged
  • Autoantibodies / immunology
  • Autopsy
  • Brain / diagnostic imaging
  • Brain / metabolism
  • Brain / pathology*
  • Brain Infarction / diagnostic imaging
  • Brain Infarction / etiology
  • Brain Infarction / metabolism
  • Brain Infarction / pathology*
  • Case-Control Studies
  • Complement C4b / immunology
  • Complement C4b / metabolism
  • Complement C5b / immunology
  • Complement C5b / metabolism
  • Complement Membrane Attack Complex / immunology
  • Complement Membrane Attack Complex / metabolism
  • Complement Pathway, Classical
  • Complement Pathway, Mannose-Binding Lectin
  • Complement System Proteins / immunology
  • Complement System Proteins / metabolism
  • Female
  • Humans
  • Immunohistochemistry
  • Intracranial Thrombosis / diagnostic imaging
  • Intracranial Thrombosis / etiology
  • Intracranial Thrombosis / metabolism
  • Intracranial Thrombosis / pathology*
  • Lupus Erythematosus, Systemic / metabolism
  • Lupus Erythematosus, Systemic / pathology
  • Lupus Vasculitis, Central Nervous System / complications
  • Lupus Vasculitis, Central Nervous System / diagnostic imaging
  • Lupus Vasculitis, Central Nervous System / metabolism
  • Lupus Vasculitis, Central Nervous System / pathology*
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Peptide Fragments / immunology
  • Peptide Fragments / metabolism
  • Vasculitis, Central Nervous System / diagnostic imaging
  • Vasculitis, Central Nervous System / etiology
  • Vasculitis, Central Nervous System / metabolism
  • Vasculitis, Central Nervous System / pathology*

Substances

  • Autoantibodies
  • Complement Membrane Attack Complex
  • Peptide Fragments
  • Complement C4b
  • complement C4d
  • Complement C5b
  • Complement System Proteins