Recording, analysis, and interpretation of spreading depolarizations in neurointensive care: Review and recommendations of the COSBID research group

Jens P. Dreier, Martin Fabricius, Cenk Ayata, Oliver W. Sakowitz, C. William Shuttleworth, Christian Dohmen, Rudolf Graf, Peter Vajkoczy, Raimund Helbok, Michiyasu Suzuki, Alois J. Schiefecker, Sebastian Major, Maren K.L. Winkler, Eun Jeung Kang, Denny Milakara, Ana I. Oliveira-Ferreira, Clemens Reiffurth, Gajanan S. Revankar, Kazutaka Sugimoto, Nora F. DenglerNils Hecht, Brandon Foreman, Bart Feyen, Daniel Kondziella, Christian K. Friberg, Henning Piilgaard, Eric S. Rosenthal, M. Brandon Westover, Anna Maslarova, Edgar Santos, Daniel Hertle, Renán Sánchez-Porras, Sharon L. Jewell, Baptiste Balança, Johannes Platz, Jason M. Hinzman, Janos Lückl, Karl Schoknecht, Michael Schöll, Christoph Drenckhahn, Delphine Feuerstein, Nina Eriksen, Viktor Horst, Julia S. Bretz, Paul Jahnke, Michael Scheel, Georg Bohner, Egill Rostrup, Bente Pakkenberg, Uwe Heinemann, Jan Claassen, Andrew P. Carlson, Christina M. Kowoll, Svetlana Lublinsky, Yoash Chassidim, Ilan Shelef, Alon Friedman, Gerrit Brinker, Michael Reiner, Sergei A. Kirov, R. David Andrew, Eszter Farkas, Erdem Güresir, Hartmut Vatter, Lee S. Chung, Kc Brennan, Thomas Lieutaud, Stephane Marinesco, Andrew Ir Maas, Juan Sahuquillo, Markus A. Dahlem, Frank Richter, Oscar Herreras, Martyn G. Boutelle, David O. Okonkwo, M. Ross Bullock, Otto W. Witte, Peter Martus, Arn M.J.M. Van Den Maagdenberg, Michel D. Ferrari, Rick M. Dijkhuizen, Lori A. Shutter, Norberto Andaluz, André P. Schulte, Brian Macvicar, Tomas Watanabe, Johannes Woitzik, Martin Lauritzen, Anthony J. Strong, Jed A. Hartings

Research output: Contribution to journalReview article

78 Scopus citations

Abstract

Spreading depolarizations (SD) are waves of abrupt, near-complete breakdown of neuronal transmembrane ion gradients, are the largest possible pathophysiologic disruption of viable cerebral gray matter, and are a crucial mechanism of lesion development. Spreading depolarizations are increasingly recorded during multimodal neuromonitoring in neurocritical care as a causal biomarker providing a diagnostic summary measure of metabolic failure and excitotoxic injury. Focal ischemia causes spreading depolarization within minutes. Further spreading depolarizations arise for hours to days due to energy supply-demand mismatch in viable tissue. Spreading depolarizations exacerbate neuronal injury through prolonged ionic breakdown and spreading depolarization-related hypoperfusion (spreading ischemia). Local duration of the depolarization indicates local tissue energy status and risk of injury. Regional electrocorticographic monitoring affords even remote detection of injury because spreading depolarizations propagate widely from ischemic or metabolically stressed zones; characteristic patterns, including temporal clusters of spreading depolarizations and persistent depression of spontaneous cortical activity, can be recognized and quantified. Here, we describe the experimental basis for interpreting these patterns and illustrate their translation to human disease. We further provide consensus recommendations for electrocorticographic methods to record, classify, and score spreading depolarizations and associated spreading depressions. These methods offer distinct advantages over other neuromonitoring modalities and allow for future refinement through less invasive and more automated approaches.

Original languageEnglish (US)
Pages (from-to)1595-1625
Number of pages31
JournalJournal of Cerebral Blood Flow and Metabolism
Volume37
Issue number5
DOIs
StatePublished - May 1 2017

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Keywords

  • Spreading depolarization
  • anoxic depolarization
  • asphyxial depolarization
  • brain edema
  • brain trauma
  • cerebral blood flow
  • epilepsy
  • epileptogenesis
  • focal ischemia
  • global ischemia
  • global ischemia
  • intracerebral hemorrhage
  • neurocritical care
  • neuroprotection
  • neurovascular coupling
  • peri-infarct depolarization
  • spreading depression
  • spreading ischemia
  • subarachnoid hemorrhage
  • vasospasm

ASJC Scopus subject areas

  • Neurology
  • Clinical Neurology
  • Cardiology and Cardiovascular Medicine

Cite this

Dreier, J. P., Fabricius, M., Ayata, C., Sakowitz, O. W., William Shuttleworth, C., Dohmen, C., Graf, R., Vajkoczy, P., Helbok, R., Suzuki, M., Schiefecker, A. J., Major, S., Winkler, M. K. L., Kang, E. J., Milakara, D., Oliveira-Ferreira, A. I., Reiffurth, C., Revankar, G. S., Sugimoto, K., ... Hartings, J. A. (2017). Recording, analysis, and interpretation of spreading depolarizations in neurointensive care: Review and recommendations of the COSBID research group. Journal of Cerebral Blood Flow and Metabolism, 37(5), 1595-1625. https://doi.org/10.1177/0271678X16654496