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Detection of Spreading Depolarization with Intraparenchymal Electrodes in the Injured Human Brain

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Abstract

Background

Spreading depolarization events following ischemic and traumatic brain injury are associated with poor patient outcome. Currently, monitoring these events is limited to patients in whom subdural electrodes can be placed at open craniotomy. This study examined whether these events can be detected using intra-cortical electrodes, opening the way for electrode insertion via burr hole.

Methods

Animal work was carried out on adult Sprague–Dawley rats in a laboratory setting to investigate the feasibility of recording depolarization events. Subsequently, 8 human patients requiring craniotomy for traumatic brain injury or aneurysmal subarachnoid hemorrhage were monitored for depolarization events in an intensive care setting with concurrent strip (subdural) and depth (intra-parenchymal) electrode recordings.

Results

(1) Depolarization events can be reliably detected from intra-cortically placed electrodes. (2) A reproducible slow potential change (SPC) waveform morphology was identified from intra-cortical electrodes on the depth array. (3) The depression of cortical activity known to follow depolarization events was identified consistently from both intra-cortical and sub-cortical electrodes on the depth array.

Conclusions

Intra-parenchymally sited electrodes can be used to consistently identify depolarization events in humans. This technique greatly extends the capability of monitoring for spreading depolarization events in injured patients, as electrodes can be sited without the need for craniotomy. The method provides a new investigative tool for the evaluation of the contribution of these events to secondary brain injury in human patients.

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Notes

  1. For the purposes of this study no distinction was made between events of short and long duration [10] and all are referred to as “SD.”

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Acknowledgments

This work was funded in part by a Wellcome Trust/Department of Health Healthcare Innovation Challenge Fund (Grant HICF—1010-080) and in part by the U.S. Army CDMRP PH/TBI Research Program (contract number W81XWH-08-2-0016) and the Mayfield Education and Research Foundation. We thank Chi Leng Leong for help with the figures. All animal work was carried out at the University of Cincinnati. All human clinical investigations were carried out at Kings College Hospital, London, UK.

Conflict of interest

Toby Jeffcote, Jason M Hinzman, Sharon L Jewell, Robert M Learney, Clemens Pahl, Christos Tolias, Daniel C Walsh, Agnieszka Zakrzewska, Martin E Fabricius, Anthony J Strong, Jed A Hartings, and Martyn G Boutelle declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Neurosurgery, King’s College Hospital, London, UK

    Toby Jeffcote, Christos Tolias, Daniel C. Walsh & Agnieszka Zakrzewska

  2. Department of Bioengineering, Imperial College, London, UK

    Toby Jeffcote, Robert M. Learney & Martyn G. Boutelle

  3. Department of Neurosurgery, University of Cincinnati (UC) Neuroscience Institute, UC College of Medicine, Cincinnati, OH, USA

    Jason M. Hinzman & Jed A. Hartings

  4. Department of Neurophysiology, King’s College Hospital, London, UK

    Sharon L. Jewell

  5. Department of Intensive Care Medicine, King’s College Hospital, London, UK

    Clemens Pahl

  6. Division of Critical Care Neurology, Mayo Clinic, Minnesota, US, USA

    Sara Hocker

  7. Department of Clinical Neurophysiology, Rigshospitalet, Copenhagen, Denmark

    Martin E. Fabricius

  8. Department of Academic Neurosurgery, Institute of Psychiatry, King’s College London, London, UK

    Anthony J. Strong

Authors
  1. Toby Jeffcote
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  2. Jason M. Hinzman
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  8. Sara Hocker
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  9. Agnieszka Zakrzewska
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  10. Martin E. Fabricius
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  11. Anthony J. Strong
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  12. Jed A. Hartings
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  13. Martyn G. Boutelle
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Corresponding authors

Correspondence to Jed A. Hartings or Martyn G. Boutelle.

Additional information

Jed A. Hartings and Martyn G. Boutelle contributed equally to this work.

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Jeffcote, T., Hinzman, J.M., Jewell, S.L. et al. Detection of Spreading Depolarization with Intraparenchymal Electrodes in the Injured Human Brain. Neurocrit Care 20, 21–31 (2014). https://doi.org/10.1007/s12028-013-9938-7

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  • DOI: https://doi.org/10.1007/s12028-013-9938-7

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