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 Kl Winkler; Eun-Jeung Kang; Denny Milakara; Ana I Oliveira-Ferreira; Clemens Reiffurth; Gajanan S Revankar; Kazutaka Sugimoto; Nora F Dengler; 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; K C 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 Mjm 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

doi:10.1177/0271678x16654496

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 Kl 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, K C 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 Mjm 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

122 Citationer (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.

Originalsprog	Engelsk
Tidsskrift	Journal of Cerebral Blood Flow and Metabolism
Vol/bind	37
Udgave nummer	5
Sider (fra-til)	1595-1625
Antal sider	31
ISSN	0271-678X
DOI	https://doi.org/10.1177/0271678x16654496
Status	Udgivet - 1 maj 2017

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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., 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

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, MK, Kang, E-J, 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, KC, 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, AM, 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, bind 37, nr. 5, s. 1595-1625. https://doi.org/10.1177/0271678x16654496

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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.",

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doi = "10.1177/0271678x16654496",

language = "English",

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journal = "Journal of Cerebral Blood Flow and Metabolism",

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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 Kl

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, K C

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 Mjm

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.

U2 - 10.1177/0271678x16654496

DO - 10.1177/0271678x16654496

M3 - Review

C2 - 27317657

SN - 0271-678X

VL - 37

SP - 1595

EP - 1625

JO - Journal of Cerebral Blood Flow and Metabolism

JF - Journal of Cerebral Blood Flow and Metabolism

IS - 5

ER -

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

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