ELSEVIER Brain Research 725 (1996) 184-191
BRAIN
RESEARCH
Research report
The effects in vivo of hypoxia on brain injury
Paul Pearigen, Ryder Gwinn, Roger P. Simon *
Department of Neurology, Unit'ersity c)[ Cali~brnia, San Francisco, USA
Accepted 7 February 1996
Abstract
To separately analyze the hypoxic component of hypoxic-ischemic encephalopathy, rats were prepared such that their paO2 was
maintained at 20 mmHg while maintaining systemic arterial pressures. During the 20-rain experiment, brain oxygen concentration and
extracellular amino acid concentrations were monitored. At sacrifice, the brains were studied for morphologic evidence of injury by
immunocytochemical staining for the non-constituitive stress protein HSP-72 or neuronal death by acid fuchsin staining. Oxygenated rats
subjected to global ischemia were prepared for comparison. In these experiments, hypoxia resulted in no increase in extracellular
glutamate concentration, and no morphologic injury was detected. Thus, hypoxia without ischemia is well tolerated by brain.
Keywords: Hypoxia; Heat shock protein; Hypoxia-ischemia; Glutamate
1. Introduction
It is a clinical axiom that removal of oxygen from the
brain will result in the death of that organ. However, the
mechanism by which such brain injury occurs is not quite
as clear in the experimental literature. In vivo, hypoxic
injury to the brain almost always occurs in the setting of
ischemia; what portion of the injury results from oxygen
deprivation as opposed to loss of blood flow may be
difficult to establish in the intact organism. Clinically, this
distinction is usually ignored and the terms hypoxic en-
cephalopathy and ischemic encephalopathy are generally
used interchangeably. To best order interventions during
critical care situations, the relative roles of hypoxia and
ischemia in 'hypoxic-ischemic encephalopathy' should be
defined.
The pathogenesis of hypoxic-ischemic injury to the
brain has been clarified over the last decade [6]. Injury
begins with elevation of glutamate concentrations in the
extracellular compartment, which opens voltage-gated and
receptor-operated calcium channels. The resultant intra-
cellular calcium toxicity induces catabolic processes within
the cell, ultimately resulting in cell death. Early and subtle
injury can be detected immunocytochemically by the use
of antibodies to nonconstitutive heatshock proteins (HSP)
* Corresponding author. Present address: Department of Neurology,
University of Pittsburgh Medical School 325 Scaife Hall, Pittsburgh, PA
15213, USA. Fax: (1) (412) 648-1239.
induced in nervous system cells by a wide range of stress,
including seizures and ischemia [12,16,17]. HSP induction
represents a response to the presence of denatured protein
in the cell [1]. The presence of denatured proteins activate
heatshock factors [18] which bind to heat shock elements,
resulting in the transcription of HSP RNA [19,20]. Neu-
rons which imunocytochemically stain with HSP antibody
therefore contain denatured protein as evidence of injury.
We used the techniques of in vivo microdialysis [10] and
heat shock protein immunocytochemistry to examine the
role of pure hypoxia, in the absence of ischemia, in brain
injury. Acid fuchsin staining was used to identify dead
cells.
2. Materials and methods
2.1. Animal preparation
2.1.1. Ventilation and physiologic monitoring
Adult male Sprague-Dawley rats (325-375 g) were
intubated, placed on a homeothermic blanket to maintain
rectal temperature at 36.5-37.5°C, and mechanically venti-
lated using a Harvard small animal ventilator with 2%
halothane in 24% oxygen with a balance of nitrogen gas. A
femoral artery catheter was placed for continuous blood
pressure recording and for arterial blood gas sampling. A
femoral vein was canalized for administration of neuro-
muscular paralyzing agents and normal saline. Cutaneous
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