Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma

Jed A. Hartings, Tomas Watanabe, Ross Bullock, David O. Okonkwo, Martin Fabricius, Johannes Woitzik, Jens P. Dreier, Ava Puccio, Lori A. Shutter, Clemens Pahl, Anthony J. Strong

Research output: Contribution to journalArticle

116 Citations (Scopus)

Abstract

Cortical spreading depolarizations occur spontaneously after ischaemic, haemorrhagic and traumatic brain injury. Their effects vary spatially and temporally as graded phenomena, from infarction to complete recovery, and are reflected in the duration of depolarization measured by the negative direct current shift of electrocorticographic recordings. In the focal ischaemic penumbra, peri-infarct depolarizations have prolonged direct current shifts and cause progressive recruitment of the penumbra into the core infarct. In traumatic brain injury, the effects of spreading depolarizations are unknown, although prolonged events have not been observed in animal models. To determine whether detrimental penumbral-type depolarizations occur in human brain trauma, we analysed electrocorticographic recordings obtained by subdural electrode-strip monitoring during intensive care. Of 53 patients studied, 10 exhibited spreading depolarizations in an electrophysiologic penumbra (i.e. isoelectric cortex with no spontaneous activity). All 10 patients (100) with isoelectric spreading depolarizations had poor outcomes, defined as death, vegetative state, or severe disability at 6 months. In contrast, poor outcomes were observed in 60 of patients (12/20) who had spreading depolarizations with depression of spontaneous activity and only 26 of patients (6/23) who had no depolarizations (χ2, P<0.001). Spontaneous electrocorticographic activity and direct current shifts of depolarizations were further examined in nine patients. Direct current shift durations (n=295) were distributed with a significant positive skew (range 0:51-16:19min:s), evidencing a normally distributed group of short events and a sub-group of prolonged events. Prolonged direct current shifts were more commonly associated with isoelectric depolarizations (median 2min 36s), whereas shorter depolarizations occurred with depression of spontaneous activity (median 2min 10s; P<0.001). In the latter group, direct current shift durations correlated with electrocorticographic depression periods, and were longer when preceded by periodic epileptiform discharges than by continuous delta (0.5-4.0Hz) or higher frequency activity. Prolonged direct current shifts (>3min) also occurred mainly within temporal clusters of events. Our results show for the first time that spreading depolarizations are associated with worse clinical outcome after traumatic brain injury. Furthermore, based on animal models of brain injury, the prolonged durations of depolarizations raise the possibility that these events may contribute to maturation of cortical lesions. Prolonged depolarizations, measured by negative direct current shifts, were associated with (i) isoelectricity or periodic epileptiform discharges; (ii) prolonged depression of spontaneous activity and (iii) occurrence in temporal clusters. Depolarizations with these characteristics are likely to reflect a worse prognosis.

Original languageEnglish
Pages (from-to)1529-1540
Number of pages12
JournalBrain
Volume134
Issue number5
DOIs
StatePublished - May 1 2011
Externally publishedYes

Fingerprint

Animal Models
Persistent Vegetative State
Critical Care
Brain Injuries
Infarction
Electrodes
Traumatic Brain Injury

Keywords

  • acute brain injury
  • cortical spreading depression
  • craniotomy
  • electroencephalography
  • signal processing

ASJC Scopus subject areas

  • Clinical Neurology

Cite this

Hartings, J. A., Watanabe, T., Bullock, R., Okonkwo, D. O., Fabricius, M., Woitzik, J., ... Strong, A. J. (2011). Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma. Brain, 134(5), 1529-1540. https://doi.org/10.1093/brain/awr048

Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma. / Hartings, Jed A.; Watanabe, Tomas; Bullock, Ross; Okonkwo, David O.; Fabricius, Martin; Woitzik, Johannes; Dreier, Jens P.; Puccio, Ava; Shutter, Lori A.; Pahl, Clemens; Strong, Anthony J.

In: Brain, Vol. 134, No. 5, 01.05.2011, p. 1529-1540.

Research output: Contribution to journalArticle

Hartings, JA, Watanabe, T, Bullock, R, Okonkwo, DO, Fabricius, M, Woitzik, J, Dreier, JP, Puccio, A, Shutter, LA, Pahl, C & Strong, AJ 2011, 'Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma', Brain, vol. 134, no. 5, pp. 1529-1540. https://doi.org/10.1093/brain/awr048
Hartings JA, Watanabe T, Bullock R, Okonkwo DO, Fabricius M, Woitzik J et al. Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma. Brain. 2011 May 1;134(5):1529-1540. https://doi.org/10.1093/brain/awr048
Hartings, Jed A. ; Watanabe, Tomas ; Bullock, Ross ; Okonkwo, David O. ; Fabricius, Martin ; Woitzik, Johannes ; Dreier, Jens P. ; Puccio, Ava ; Shutter, Lori A. ; Pahl, Clemens ; Strong, Anthony J. / Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma. In: Brain. 2011 ; Vol. 134, No. 5. pp. 1529-1540.
@article{d3783bfa69bf4eac8a30c056b6f88bc4,
title = "Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma",
abstract = "Cortical spreading depolarizations occur spontaneously after ischaemic, haemorrhagic and traumatic brain injury. Their effects vary spatially and temporally as graded phenomena, from infarction to complete recovery, and are reflected in the duration of depolarization measured by the negative direct current shift of electrocorticographic recordings. In the focal ischaemic penumbra, peri-infarct depolarizations have prolonged direct current shifts and cause progressive recruitment of the penumbra into the core infarct. In traumatic brain injury, the effects of spreading depolarizations are unknown, although prolonged events have not been observed in animal models. To determine whether detrimental penumbral-type depolarizations occur in human brain trauma, we analysed electrocorticographic recordings obtained by subdural electrode-strip monitoring during intensive care. Of 53 patients studied, 10 exhibited spreading depolarizations in an electrophysiologic penumbra (i.e. isoelectric cortex with no spontaneous activity). All 10 patients (100) with isoelectric spreading depolarizations had poor outcomes, defined as death, vegetative state, or severe disability at 6 months. In contrast, poor outcomes were observed in 60 of patients (12/20) who had spreading depolarizations with depression of spontaneous activity and only 26 of patients (6/23) who had no depolarizations (χ2, P<0.001). Spontaneous electrocorticographic activity and direct current shifts of depolarizations were further examined in nine patients. Direct current shift durations (n=295) were distributed with a significant positive skew (range 0:51-16:19min:s), evidencing a normally distributed group of short events and a sub-group of prolonged events. Prolonged direct current shifts were more commonly associated with isoelectric depolarizations (median 2min 36s), whereas shorter depolarizations occurred with depression of spontaneous activity (median 2min 10s; P<0.001). In the latter group, direct current shift durations correlated with electrocorticographic depression periods, and were longer when preceded by periodic epileptiform discharges than by continuous delta (0.5-4.0Hz) or higher frequency activity. Prolonged direct current shifts (>3min) also occurred mainly within temporal clusters of events. Our results show for the first time that spreading depolarizations are associated with worse clinical outcome after traumatic brain injury. Furthermore, based on animal models of brain injury, the prolonged durations of depolarizations raise the possibility that these events may contribute to maturation of cortical lesions. Prolonged depolarizations, measured by negative direct current shifts, were associated with (i) isoelectricity or periodic epileptiform discharges; (ii) prolonged depression of spontaneous activity and (iii) occurrence in temporal clusters. Depolarizations with these characteristics are likely to reflect a worse prognosis.",
keywords = "acute brain injury, cortical spreading depression, craniotomy, electroencephalography, signal processing",
author = "Hartings, {Jed A.} and Tomas Watanabe and Ross Bullock and Okonkwo, {David O.} and Martin Fabricius and Johannes Woitzik and Dreier, {Jens P.} and Ava Puccio and Shutter, {Lori A.} and Clemens Pahl and Strong, {Anthony J.}",
year = "2011",
month = "5",
day = "1",
doi = "10.1093/brain/awr048",
language = "English",
volume = "134",
pages = "1529--1540",
journal = "Brain",
issn = "0006-8950",
publisher = "Oxford University Press",
number = "5",

}

TY - JOUR

T1 - Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma

AU - Hartings, Jed A.

AU - Watanabe, Tomas

AU - Bullock, Ross

AU - Okonkwo, David O.

AU - Fabricius, Martin

AU - Woitzik, Johannes

AU - Dreier, Jens P.

AU - Puccio, Ava

AU - Shutter, Lori A.

AU - Pahl, Clemens

AU - Strong, Anthony J.

PY - 2011/5/1

Y1 - 2011/5/1

N2 - Cortical spreading depolarizations occur spontaneously after ischaemic, haemorrhagic and traumatic brain injury. Their effects vary spatially and temporally as graded phenomena, from infarction to complete recovery, and are reflected in the duration of depolarization measured by the negative direct current shift of electrocorticographic recordings. In the focal ischaemic penumbra, peri-infarct depolarizations have prolonged direct current shifts and cause progressive recruitment of the penumbra into the core infarct. In traumatic brain injury, the effects of spreading depolarizations are unknown, although prolonged events have not been observed in animal models. To determine whether detrimental penumbral-type depolarizations occur in human brain trauma, we analysed electrocorticographic recordings obtained by subdural electrode-strip monitoring during intensive care. Of 53 patients studied, 10 exhibited spreading depolarizations in an electrophysiologic penumbra (i.e. isoelectric cortex with no spontaneous activity). All 10 patients (100) with isoelectric spreading depolarizations had poor outcomes, defined as death, vegetative state, or severe disability at 6 months. In contrast, poor outcomes were observed in 60 of patients (12/20) who had spreading depolarizations with depression of spontaneous activity and only 26 of patients (6/23) who had no depolarizations (χ2, P<0.001). Spontaneous electrocorticographic activity and direct current shifts of depolarizations were further examined in nine patients. Direct current shift durations (n=295) were distributed with a significant positive skew (range 0:51-16:19min:s), evidencing a normally distributed group of short events and a sub-group of prolonged events. Prolonged direct current shifts were more commonly associated with isoelectric depolarizations (median 2min 36s), whereas shorter depolarizations occurred with depression of spontaneous activity (median 2min 10s; P<0.001). In the latter group, direct current shift durations correlated with electrocorticographic depression periods, and were longer when preceded by periodic epileptiform discharges than by continuous delta (0.5-4.0Hz) or higher frequency activity. Prolonged direct current shifts (>3min) also occurred mainly within temporal clusters of events. Our results show for the first time that spreading depolarizations are associated with worse clinical outcome after traumatic brain injury. Furthermore, based on animal models of brain injury, the prolonged durations of depolarizations raise the possibility that these events may contribute to maturation of cortical lesions. Prolonged depolarizations, measured by negative direct current shifts, were associated with (i) isoelectricity or periodic epileptiform discharges; (ii) prolonged depression of spontaneous activity and (iii) occurrence in temporal clusters. Depolarizations with these characteristics are likely to reflect a worse prognosis.

AB - Cortical spreading depolarizations occur spontaneously after ischaemic, haemorrhagic and traumatic brain injury. Their effects vary spatially and temporally as graded phenomena, from infarction to complete recovery, and are reflected in the duration of depolarization measured by the negative direct current shift of electrocorticographic recordings. In the focal ischaemic penumbra, peri-infarct depolarizations have prolonged direct current shifts and cause progressive recruitment of the penumbra into the core infarct. In traumatic brain injury, the effects of spreading depolarizations are unknown, although prolonged events have not been observed in animal models. To determine whether detrimental penumbral-type depolarizations occur in human brain trauma, we analysed electrocorticographic recordings obtained by subdural electrode-strip monitoring during intensive care. Of 53 patients studied, 10 exhibited spreading depolarizations in an electrophysiologic penumbra (i.e. isoelectric cortex with no spontaneous activity). All 10 patients (100) with isoelectric spreading depolarizations had poor outcomes, defined as death, vegetative state, or severe disability at 6 months. In contrast, poor outcomes were observed in 60 of patients (12/20) who had spreading depolarizations with depression of spontaneous activity and only 26 of patients (6/23) who had no depolarizations (χ2, P<0.001). Spontaneous electrocorticographic activity and direct current shifts of depolarizations were further examined in nine patients. Direct current shift durations (n=295) were distributed with a significant positive skew (range 0:51-16:19min:s), evidencing a normally distributed group of short events and a sub-group of prolonged events. Prolonged direct current shifts were more commonly associated with isoelectric depolarizations (median 2min 36s), whereas shorter depolarizations occurred with depression of spontaneous activity (median 2min 10s; P<0.001). In the latter group, direct current shift durations correlated with electrocorticographic depression periods, and were longer when preceded by periodic epileptiform discharges than by continuous delta (0.5-4.0Hz) or higher frequency activity. Prolonged direct current shifts (>3min) also occurred mainly within temporal clusters of events. Our results show for the first time that spreading depolarizations are associated with worse clinical outcome after traumatic brain injury. Furthermore, based on animal models of brain injury, the prolonged durations of depolarizations raise the possibility that these events may contribute to maturation of cortical lesions. Prolonged depolarizations, measured by negative direct current shifts, were associated with (i) isoelectricity or periodic epileptiform discharges; (ii) prolonged depression of spontaneous activity and (iii) occurrence in temporal clusters. Depolarizations with these characteristics are likely to reflect a worse prognosis.

KW - acute brain injury

KW - cortical spreading depression

KW - craniotomy

KW - electroencephalography

KW - signal processing

UR - http://www.scopus.com/inward/record.url?scp=79957469956&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79957469956&partnerID=8YFLogxK

U2 - 10.1093/brain/awr048

DO - 10.1093/brain/awr048

M3 - Article

VL - 134

SP - 1529

EP - 1540

JO - Brain

JF - Brain

SN - 0006-8950

IS - 5

ER -