Neutrophil-associated central nervous system inflammation in tuberculous meningitis immune reconstitution inflammatory syndrome

Clin Infect Dis. 2014 Dec 1;59(11):1638-47. doi: 10.1093/cid/ciu641. Epub 2014 Aug 8.

Abstract

Background: The immunopathogenesis of tuberculosis-associated immune reconstitution inflammatory syndrome (IRIS) remains incompletely understood, and we know of only 1 disease site-specific study of the underlying immunology; we recently showed that Mycobacterium tuberculosis culture positivity and increased neutrophils in the cerebrospinal fluid (CSF) of patients with tuberculous meningitis (TBM) are associated with TBM-IRIS. In this study we investigated inflammatory mediators at the disease site in patients with TBM-IRIS.

Methods: We performed lumbar puncture at 3-5 time points in human immunodeficiency virus (HIV)-infected patients with TBM (n = 34), including at TBM diagnosis, at initiation of antiretroviral therapy (ART) (day 14), 14 days after ART initiation, at presentation of TBM-IRIS, and 14 days thereafter. We determined the concentrations of 40 mediators in CSF (33 paired with blood) with Luminex or enzyme-linked immunosorbent assays. Findings were compared between patients who developed TBM-IRIS (n = 16) and those who did not (TBM-non-IRIS; n = 18).

Results: At TBM diagnosis and 2 weeks after ART initiation, TBM-IRIS was associated with severe, compartmentalized inflammation in the CSF, with elevated concentrations of cytokines, chemokines, neutrophil-associated mediators, and matrix metalloproteinases, compared with TBM-non-IRIS. Patients with TBM-non-IRIS whose CSF cultures were positive for M. tuberculosis at TBM diagnosis (n = 6) showed inflammatory responses similar to those seen in patients with TBM-IRIS at both time points. However, at 2 weeks after ART initiation, S100A8/A9 was significantly increased in patients with TBM-IRIS, compared with patients with TBM-non-IRIS whose cultures were positive at baseline.

Conclusions: A high baseline M. tuberculosis antigen load drives an inflammatory response that manifests clinically as TBM-IRIS in most, but not all, patients with TBM. Neutrophils and their mediators, especially S100A8/A9, are closely associated with the central nervous system inflammation that characterizes TBM-IRIS.

Keywords: HIV; antiretroviral therapy; therapy-complications; tuberculosis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adult
  • Anti-Retroviral Agents / therapeutic use
  • Cytokines / blood
  • Female
  • HIV Infections / blood*
  • HIV Infections / cerebrospinal fluid
  • HIV Infections / drug therapy
  • Humans
  • Immune Reconstitution Inflammatory Syndrome / blood*
  • Immune Reconstitution Inflammatory Syndrome / cerebrospinal fluid
  • Immune Reconstitution Inflammatory Syndrome / immunology*
  • Inflammation / blood
  • Inflammation / cerebrospinal fluid
  • Inflammation / immunology
  • Leukocyte Count
  • Male
  • Mycobacterium tuberculosis / immunology
  • Neutrophils / immunology*
  • Neutrophils / pathology
  • Prospective Studies
  • Tuberculosis, Meningeal / blood*
  • Tuberculosis, Meningeal / cerebrospinal fluid
  • Tuberculosis, Meningeal / immunology*

Substances

  • Anti-Retroviral Agents
  • Cytokines