Increased intracranial pressure after diffuse traumatic brain injury exacerbates neuronal somatic membrane poration but not axonal injury: evidence for primary intracranial pressure-induced neuronal perturbation

J Cereb Blood Flow Metab. 2012 Oct;32(10):1919-32. doi: 10.1038/jcbfm.2012.95. Epub 2012 Jul 11.

Abstract

Increased intracranial pressure (ICP) associated with traumatic brain injury (TBI) is linked to increased morbidity. Although our understanding of the pathobiology of TBI has expanded, questions remain regarding the specific neuronal somatic and axonal damaging consequences of elevated ICP, independent of its impact on cerebral perfusion pressure (CPP). To investigate this, Fischer rats were subjected to moderate TBI. Measurements of ICP revealed two distinct responses to injury. One population exhibited transient increases in ICP that returned to baseline levels acutely, while the other displayed persistent ICP elevation (>20 mm Hg). Utilizing these populations, the effect of elevated ICP on neuronal pathology associated with diffuse TBI was analyzed at 6 hours after TBI. No difference in axonal injury was observed, however, rats exhibiting persistently elevated ICP postinjury revealed a doubling of neurons with chronic membrane poration compared with rats exhibiting only transient increases in ICP. Elevated postinjury ICP was not associated with a concurrent increase in DNA damage; however, traditional histological assessments did reveal increased neuronal damage, potentially associated with redistribution of cathepsin-B from the lysosomal compartment into the cytosol. These findings indicate that persistently increased ICP, without deleterious alteration of CPP, exacerbates neuronal plasmalemmal perturbation that could precipitate persistent neuronal impairment and ultimate neuronal death.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Axons / pathology*
  • Brain / blood supply
  • Brain / pathology*
  • Brain Injuries / complications*
  • Brain Injuries / pathology*
  • Cathepsin B / analysis
  • Cell Membrane / pathology
  • Intracranial Hypertension / complications*
  • Intracranial Hypertension / pathology*
  • Male
  • Neurons / pathology*
  • Rats
  • Rats, Inbred F344

Substances

  • Cathepsin B