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. Dengler & 70 others Nils 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

57 Citations (Scopus)

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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Wounds and Injuries
Research
Ischemia
Biomarkers
Ions
Gray Matter

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

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

In: Journal of Cerebral Blood Flow and Metabolism, Vol. 37, No. 5, 01.05.2017, p. 1595-1625.

Research output: Contribution to journalReview article

Dreier, JP, Fabricius, M, Ayata, C, Sakowitz, OW, William Shuttleworth, C, Dohmen, C, Graf, R, Vajkoczy, P, Helbok, R, Suzuki, M, Schiefecker, AJ, Major, S, Winkler, MKL, Kang, EJ, Milakara, D, Oliveira-Ferreira, AI, Reiffurth, C, Revankar, GS, Sugimoto, K, Dengler, NF, Hecht, N, Foreman, B, Feyen, B, Kondziella, D, Friberg, CK, Piilgaard, H, Rosenthal, ES, Westover, MB, Maslarova, A, Santos, E, Hertle, D, Sánchez-Porras, R, Jewell, SL, Balança, B, Platz, J, Hinzman, JM, Lückl, J, Schoknecht, K, Schöll, M, Drenckhahn, C, Feuerstein, D, Eriksen, N, Horst, V, Bretz, JS, Jahnke, P, Scheel, M, Bohner, G, Rostrup, E, Pakkenberg, B, Heinemann, U, Claassen, J, Carlson, AP, Kowoll, CM, Lublinsky, S, Chassidim, Y, Shelef, I, Friedman, A, Brinker, G, Reiner, M, Kirov, SA, Andrew, RD, Farkas, E, Güresir, E, Vatter, H, Chung, LS, Brennan, K, Lieutaud, T, Marinesco, S, Maas, AI, Sahuquillo, J, Dahlem, MA, Richter, F, Herreras, O, Boutelle, MG, Okonkwo, DO, Bullock, MR, Witte, OW, Martus, P, Van Den Maagdenberg, AMJM, Ferrari, MD, Dijkhuizen, RM, Shutter, LA, Andaluz, N, Schulte, AP, Macvicar, B, Watanabe, T, Woitzik, J, Lauritzen, M, Strong, AJ & Hartings, JA 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, vol. 37, no. 5, pp. 1595-1625. https://doi.org/10.1177/0271678X16654496
Dreier, Jens P. ; Fabricius, Martin ; Ayata, Cenk ; Sakowitz, Oliver W. ; William Shuttleworth, C. ; Dohmen, Christian ; Graf, Rudolf ; Vajkoczy, Peter ; Helbok, Raimund ; Suzuki, Michiyasu ; Schiefecker, Alois J. ; Major, Sebastian ; Winkler, Maren K.L. ; Kang, Eun Jeung ; Milakara, Denny ; Oliveira-Ferreira, Ana I. ; Reiffurth, Clemens ; Revankar, Gajanan S. ; Sugimoto, Kazutaka ; Dengler, Nora F. ; Hecht, Nils ; Foreman, Brandon ; Feyen, Bart ; Kondziella, Daniel ; Friberg, Christian K. ; Piilgaard, Henning ; Rosenthal, Eric S. ; Westover, M. Brandon ; Maslarova, Anna ; Santos, Edgar ; Hertle, Daniel ; Sánchez-Porras, Renán ; Jewell, Sharon L. ; Balança, Baptiste ; Platz, Johannes ; Hinzman, Jason M. ; Lückl, Janos ; Schoknecht, Karl ; Schöll, Michael ; Drenckhahn, Christoph ; Feuerstein, Delphine ; Eriksen, Nina ; Horst, Viktor ; Bretz, Julia S. ; Jahnke, Paul ; Scheel, Michael ; Bohner, Georg ; Rostrup, Egill ; Pakkenberg, Bente ; Heinemann, Uwe ; Claassen, Jan ; Carlson, Andrew P. ; Kowoll, Christina M. ; Lublinsky, Svetlana ; Chassidim, Yoash ; Shelef, Ilan ; Friedman, Alon ; Brinker, Gerrit ; Reiner, Michael ; Kirov, Sergei A. ; Andrew, R. David ; Farkas, Eszter ; Güresir, Erdem ; Vatter, Hartmut ; Chung, Lee S. ; Brennan, Kc ; Lieutaud, Thomas ; Marinesco, Stephane ; Maas, Andrew Ir ; Sahuquillo, Juan ; Dahlem, Markus A. ; Richter, Frank ; Herreras, Oscar ; Boutelle, Martyn G. ; Okonkwo, David O. ; Bullock, M. Ross ; Witte, Otto W. ; Martus, Peter ; Van Den Maagdenberg, Arn M.J.M. ; Ferrari, Michel D. ; Dijkhuizen, Rick M. ; Shutter, Lori A. ; Andaluz, Norberto ; Schulte, André P. ; Macvicar, Brian ; Watanabe, Tomas ; Woitzik, Johannes ; Lauritzen, Martin ; Strong, Anthony J. ; Hartings, Jed A. / Recording, analysis, and interpretation of spreading depolarizations in neurointensive care : Review and recommendations of the COSBID research group. In: Journal of Cerebral Blood Flow and Metabolism. 2017 ; Vol. 37, No. 5. pp. 1595-1625.
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TY - JOUR

T1 - Recording, analysis, and interpretation of spreading depolarizations in neurointensive care

T2 - Review and recommendations of the COSBID research group

AU - Dreier, Jens P.

AU - Fabricius, Martin

AU - Ayata, Cenk

AU - Sakowitz, Oliver W.

AU - William Shuttleworth, C.

AU - Dohmen, Christian

AU - Graf, Rudolf

AU - Vajkoczy, Peter

AU - Helbok, Raimund

AU - Suzuki, Michiyasu

AU - Schiefecker, Alois J.

AU - Major, Sebastian

AU - Winkler, Maren K.L.

AU - Kang, Eun Jeung

AU - Milakara, Denny

AU - Oliveira-Ferreira, Ana I.

AU - Reiffurth, Clemens

AU - Revankar, Gajanan S.

AU - Sugimoto, Kazutaka

AU - Dengler, Nora F.

AU - Hecht, Nils

AU - Foreman, Brandon

AU - Feyen, Bart

AU - Kondziella, Daniel

AU - Friberg, Christian K.

AU - Piilgaard, Henning

AU - Rosenthal, Eric S.

AU - Westover, M. Brandon

AU - Maslarova, Anna

AU - Santos, Edgar

AU - Hertle, Daniel

AU - Sánchez-Porras, Renán

AU - Jewell, Sharon L.

AU - Balança, Baptiste

AU - Platz, Johannes

AU - Hinzman, Jason M.

AU - Lückl, Janos

AU - Schoknecht, Karl

AU - Schöll, Michael

AU - Drenckhahn, Christoph

AU - Feuerstein, Delphine

AU - Eriksen, Nina

AU - Horst, Viktor

AU - Bretz, Julia S.

AU - Jahnke, Paul

AU - Scheel, Michael

AU - Bohner, Georg

AU - Rostrup, Egill

AU - Pakkenberg, Bente

AU - Heinemann, Uwe

AU - Claassen, Jan

AU - Carlson, Andrew P.

AU - Kowoll, Christina M.

AU - Lublinsky, Svetlana

AU - Chassidim, Yoash

AU - Shelef, Ilan

AU - Friedman, Alon

AU - Brinker, Gerrit

AU - Reiner, Michael

AU - Kirov, Sergei A.

AU - Andrew, R. David

AU - Farkas, Eszter

AU - Güresir, Erdem

AU - Vatter, Hartmut

AU - Chung, Lee S.

AU - Brennan, Kc

AU - Lieutaud, Thomas

AU - Marinesco, Stephane

AU - Maas, Andrew Ir

AU - Sahuquillo, Juan

AU - Dahlem, Markus A.

AU - Richter, Frank

AU - Herreras, Oscar

AU - Boutelle, Martyn G.

AU - Okonkwo, David O.

AU - Bullock, M. Ross

AU - Witte, Otto W.

AU - Martus, Peter

AU - Van Den Maagdenberg, Arn M.J.M.

AU - Ferrari, Michel D.

AU - Dijkhuizen, Rick M.

AU - Shutter, Lori A.

AU - Andaluz, Norberto

AU - Schulte, André P.

AU - Macvicar, Brian

AU - Watanabe, Tomas

AU - Woitzik, Johannes

AU - Lauritzen, Martin

AU - Strong, Anthony J.

AU - Hartings, Jed A.

PY - 2017/5/1

Y1 - 2017/5/1

N2 - 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.

AB - 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.

KW - Spreading depolarization

KW - anoxic depolarization

KW - asphyxial depolarization

KW - brain edema

KW - brain trauma

KW - cerebral blood flow

KW - epilepsy

KW - epileptogenesis

KW - focal ischemia

KW - global ischemia

KW - global ischemia

KW - intracerebral hemorrhage

KW - neurocritical care

KW - neuroprotection

KW - neurovascular coupling

KW - peri-infarct depolarization

KW - spreading depression

KW - spreading ischemia

KW - subarachnoid hemorrhage

KW - vasospasm

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DO - 10.1177/0271678X16654496

M3 - Review article

VL - 37

SP - 1595

EP - 1625

JO - Journal of Cerebral Blood Flow and Metabolism

JF - Journal of Cerebral Blood Flow and Metabolism

SN - 0271-678X

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