Spreading depression in continuous electroencephalography of brain trauma

Authors

  • Jed A. Hartings PhD,

    1. Department of Neurosurgery, University of Cincinnati College of Medicine, Cincinnati, OH
    2. Neurotrauma Center at University of Cincinnati Neuroscience Institute, Cincinnati, OH
    3. Mayfield Clinic, Cincinnati, OH
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  • J. Adam Wilson PhD,

    1. Department of Neurosurgery, University of Cincinnati College of Medicine, Cincinnati, OH
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  • Jason M. Hinzman PhD,

    1. Department of Neurosurgery, University of Cincinnati College of Medicine, Cincinnati, OH
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  • Sebastian Pollandt MD,

    1. Department of Neurology, University of Cincinnati College of Medicine, Cincinnati, OH
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  • Jens P. Dreier MD, PhD,

    1. Center for Stroke Research, Departments of Experimental Neurology and Neurology, Charité University Medicine Berlin, Berlin, Germany
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  • Vince DiNapoli MD, PhD,

    1. Department of Neurosurgery, University of Cincinnati College of Medicine, Cincinnati, OH
    2. Mayfield Clinic, Cincinnati, OH
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  • David M. Ficker MD,

    1. Department of Neurology, University of Cincinnati College of Medicine, Cincinnati, OH
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  • Lori A. Shutter MD,

    1. Department of Neurosurgery, University of Cincinnati College of Medicine, Cincinnati, OH
    2. Neurotrauma Center at University of Cincinnati Neuroscience Institute, Cincinnati, OH
    3. Mayfield Clinic, Cincinnati, OH
    4. Department of Neurology, University of Cincinnati College of Medicine, Cincinnati, OH
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  • Norberto Andaluz MD

    Corresponding author
    1. Department of Neurosurgery, University of Cincinnati College of Medicine, Cincinnati, OH
    2. Neurotrauma Center at University of Cincinnati Neuroscience Institute, Cincinnati, OH
    3. Mayfield Clinic, Cincinnati, OH
    • Address correspondence to Dr Hartings, 231 Albert Sabin Way, ML0517, Department of Neurosurgery, University of Cincinnati, Cincinnati, OH 45267. E-mail: jed.hartings@uc.edu

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Abstract

Objective

Cortical spreading depolarizations are a pathophysiological mechanism and candidate target for advanced monitoring in acute brain injury. Here we investigated manifestations of spreading depolarization in continuous electroencephalography (EEG) as a broadly applicable, noninvasive method for neuromonitoring.

Methods

Eighteen patients requiring surgical treatment of traumatic brain injury were monitored by invasive electrocorticography (ECoG; subdural electrodes) and noninvasive scalp EEG during intensive care. Spreading depolarizations were first identified in subdural recordings, and EEG was then examined visually and quantitatively to identify correlates.

Results

A total of 455 spreading depolarizations occurred during 65.9 days of simultaneous ECoG/EEG monitoring. For 179 of 455 events (39%), depolarizations caused temporally isolated, transient depressions of spontaneous EEG amplitudes to 57% (median) of baseline power. Depressions lasted 21 minutes (median) and occurred as suppressions of high-amplitude delta activity present as a baseline pattern in the injured hemisphere. For 62 of 179 (35%) events, isolated depressions showed a clear spread of depression between EEG channels with delays of 17 minutes (median), sometimes spanning the entire hemisphere. A further 188 of 455 (41%) depolarizations were associated with continuous EEG depression that lasted hours to days due to ongoing depolarizations. Depolarizations were also evidenced in EEG as shifts in direct current potentials.

Interpretation

Leão's spreading depression can be observed in clinically standard, continuous scalp EEG, and underlying depolarizations can spread widely across the injured cerebral hemisphere. These results open the possibility of monitoring noninvasively a neuronal pathophysiological mechanism in a wide range of disorders including ischemic stroke, subarachnoid hemorrhage, and brain trauma, and suggest a novel application for continuous EEG. Ann Neurol 2014;76:681–694

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