Skip to main content
Top
Published in: Neurocritical Care 2/2016

01-04-2016 | Original Article

Continuous EEG Monitoring for Early Detection of Delayed Cerebral Ischemia in Subarachnoid Hemorrhage: A Pilot Study

Authors: M. L. Rots, M. J. A. M. van Putten, C. W. E. Hoedemaekers, J. Horn

Published in: Neurocritical Care | Issue 2/2016

Login to get access

Abstract

Introduction

Early identification of delayed cerebral ischemia (DCI) in patients with aneurysmal subarachnoid hemorrhage (aSAH) is a major challenge. The aim of this study was to investigate whether quantitative EEG (qEEG) features can detect DCI prior to clinical or radiographic findings.

Methods

A prospective cohort study was performed in aSAH patients in whom continuous EEG (cEEG) was recorded. We studied 12 qEEG features. We compared the time point at which qEEG changed with the time point that clinical deterioration occurred or new ischemia was noted on CT scan.

Results

Twenty aSAH patients were included of whom 11 developed DCI. The alpha/delta ratio (ADR) was the most promising feature that showed a significant difference in change over time in the DCI group (median −62 % with IQR −87 to −39 %) compared to the control group (median +27 % with IQR −32 to +104 %, p = 0.013). Based on the ROC curve, a threshold was chosen for a combined measure of ADR and alpha variability (AUC: 91.7, 95 % CI 74.2–100). The median time that elapsed between change of qEEG and clinical DCI diagnosis was seven hours (IQR −11–25). Delay between qEEG and CT scan changes was 44 h (median, IQR 14–117).

Conclusion

In this study, ADR and alpha variability could detect DCI development before ischemic changes on CT scan was apparent and before clinical deterioration was noted. Implementation of cEEG in aSAH patients can probably improve early detection of DCI.
Appendix
Available only for authorised users
Literature
1.
2.
go back to reference Koenig M. Management of delayed cerebral ischemia after subarachnoid hemorrhage. Continuum (Minneap Minn). 2012;18:579–97. Koenig M. Management of delayed cerebral ischemia after subarachnoid hemorrhage. Continuum (Minneap Minn). 2012;18:579–97.
3.
go back to reference Dorsch N, King M. A review of cerebral vasospasm in aneurysmal subarachnoid haemorrhage. J Clin Neurosci. 1994;1:19–26.CrossRefPubMed Dorsch N, King M. A review of cerebral vasospasm in aneurysmal subarachnoid haemorrhage. J Clin Neurosci. 1994;1:19–26.CrossRefPubMed
4.
go back to reference Neil-Dwyer G, Lang D, Doshi B, Gerber C, Smith P. Delayed cerebral ischaemia: the pathological substrate. Acta Neurochir. 1994;131:137–45.CrossRefPubMed Neil-Dwyer G, Lang D, Doshi B, Gerber C, Smith P. Delayed cerebral ischaemia: the pathological substrate. Acta Neurochir. 1994;131:137–45.CrossRefPubMed
5.
go back to reference Rabinstein A, Weigand S, Atkinson J, Wijdicks E. Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2005;36:992–7.CrossRefPubMed Rabinstein A, Weigand S, Atkinson J, Wijdicks E. Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2005;36:992–7.CrossRefPubMed
6.
go back to reference Claassen J, Bernardini G, Kreiter K, et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke. 2001;32:2012–20.CrossRefPubMed Claassen J, Bernardini G, Kreiter K, et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke. 2001;32:2012–20.CrossRefPubMed
7.
go back to reference Murayama Y, Malisch T, Guglielmi G, et al. Incidence of cerebral vasospasm after endovascular treatment of acutely ruptured aneurysms: report on 69 cases. J Neurosurg. 1997;87:830–5.CrossRefPubMed Murayama Y, Malisch T, Guglielmi G, et al. Incidence of cerebral vasospasm after endovascular treatment of acutely ruptured aneurysms: report on 69 cases. J Neurosurg. 1997;87:830–5.CrossRefPubMed
8.
go back to reference Bederson J, Connolly E, Batjer H, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke. 2009;40:994–1025.CrossRefPubMed Bederson J, Connolly E, Batjer H, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke. 2009;40:994–1025.CrossRefPubMed
9.
go back to reference Finnigan S, Walsh M, Rose S, Chalk J. Quantitative EEG indices of sub-acute ischaemic stroke correlate with clinical outcomes. Clin Neurophysiol. 2007;118:2525–32.CrossRefPubMed Finnigan S, Walsh M, Rose S, Chalk J. Quantitative EEG indices of sub-acute ischaemic stroke correlate with clinical outcomes. Clin Neurophysiol. 2007;118:2525–32.CrossRefPubMed
10.
go back to reference Sharbrough F, Messick J, Sundt T. Correlation of continuous electroencephalograms with cerebral blood flow measurements during carotid endarterectomy. Stroke. 1973;4:674–83.CrossRefPubMed Sharbrough F, Messick J, Sundt T. Correlation of continuous electroencephalograms with cerebral blood flow measurements during carotid endarterectomy. Stroke. 1973;4:674–83.CrossRefPubMed
11.
go back to reference Sundt T, Sharbrough F, Anderson R, Michenfelder J. Cerebral blood flow measurements and electroencephalograms during carotid endarterectomy. J Neurosurg. 1974;107:887–97.CrossRef Sundt T, Sharbrough F, Anderson R, Michenfelder J. Cerebral blood flow measurements and electroencephalograms during carotid endarterectomy. J Neurosurg. 1974;107:887–97.CrossRef
12.
go back to reference Baron J-C. Perfusion thresholds in human cerebral ischemia : historical perspective and therapeutic implications. Cerebrovasc Dis. 2001;11:2–8.CrossRefPubMed Baron J-C. Perfusion thresholds in human cerebral ischemia : historical perspective and therapeutic implications. Cerebrovasc Dis. 2001;11:2–8.CrossRefPubMed
13.
go back to reference Labar D, Fisch B, Pedley T, Fink M, Solomon R. Quantitative EEG monitoring for patients with subarachnoid hemorrhage. Electroencephalogr Clin Neurophysiol. 1991;78:325–32.CrossRefPubMed Labar D, Fisch B, Pedley T, Fink M, Solomon R. Quantitative EEG monitoring for patients with subarachnoid hemorrhage. Electroencephalogr Clin Neurophysiol. 1991;78:325–32.CrossRefPubMed
14.
go back to reference Vespa P, Nuwer M, Juhász C, et al. Early detection of vasospasm after acute subarachnoid hemorrhage using continuous EEG ICU monitoring. Electroencephalogr Clin Neurophysiol. 1997;103:607–15.CrossRefPubMed Vespa P, Nuwer M, Juhász C, et al. Early detection of vasospasm after acute subarachnoid hemorrhage using continuous EEG ICU monitoring. Electroencephalogr Clin Neurophysiol. 1997;103:607–15.CrossRefPubMed
15.
go back to reference Claassen J, Hirsch L, Kreiter K, et al. Quantitative continuous EEG for detecting delayed cerebral ischemia in patients with poor-grade subarachnoid hemorrhage. Clin Neurophysiol. 2004;115:2699–710.CrossRefPubMed Claassen J, Hirsch L, Kreiter K, et al. Quantitative continuous EEG for detecting delayed cerebral ischemia in patients with poor-grade subarachnoid hemorrhage. Clin Neurophysiol. 2004;115:2699–710.CrossRefPubMed
16.
go back to reference Rathakrishnan R, Gotman J, Dubeau F, Angle M. Using continuous electroencephalography in the management of delayed cerebral ischemia following subarachnoid hemorrhage. Neurocrit Care. 2011;14:152–61.CrossRefPubMed Rathakrishnan R, Gotman J, Dubeau F, Angle M. Using continuous electroencephalography in the management of delayed cerebral ischemia following subarachnoid hemorrhage. Neurocrit Care. 2011;14:152–61.CrossRefPubMed
17.
go back to reference Gollwitzer S, Groemer T, Rampp S, et al. Early prediction of delayed cerebral ischemia in subarachnoid hemorrhage based on quantitative EEG : a prospective study in adults. Clin Neurophysiol. 2015;126:1514–23.CrossRefPubMed Gollwitzer S, Groemer T, Rampp S, et al. Early prediction of delayed cerebral ischemia in subarachnoid hemorrhage based on quantitative EEG : a prospective study in adults. Clin Neurophysiol. 2015;126:1514–23.CrossRefPubMed
18.
go back to reference Drake C, Hunt W, Kassell N, Sano K, Pertuiset B, De Villiers J. A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neurosurg Psychiatry. 1988;51:1457.PubMedPubMedCentral Drake C, Hunt W, Kassell N, Sano K, Pertuiset B, De Villiers J. A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neurosurg Psychiatry. 1988;51:1457.PubMedPubMedCentral
19.
go back to reference Fisher C, Kistler J, Davis J. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980;6:1–9.CrossRefPubMed Fisher C, Kistler J, Davis J. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980;6:1–9.CrossRefPubMed
20.
go back to reference Van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988;19:604–7.CrossRefPubMed Van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988;19:604–7.CrossRefPubMed
21.
go back to reference Cloostermans M, de Vos C, van Putten M. A novel approach for computer assisted EEG monitoring in the adult ICU. Clin Neurophysiol. 2011;122:2100–9.CrossRefPubMed Cloostermans M, de Vos C, van Putten M. A novel approach for computer assisted EEG monitoring in the adult ICU. Clin Neurophysiol. 2011;122:2100–9.CrossRefPubMed
22.
go back to reference Van Putten M, Tavy D. Continuous quantitative EEG monitoring in hemispheric stroke patients using the brain symmetry index. Stroke. 2004;35:2489–92.CrossRefPubMed Van Putten M, Tavy D. Continuous quantitative EEG monitoring in hemispheric stroke patients using the brain symmetry index. Stroke. 2004;35:2489–92.CrossRefPubMed
23.
go back to reference Claassen J, Hirsch L, Frontera J, et al. Prognostic significance of continuous EEG monitoring in patients with poor-grade subarachnoid hemorrhage. Neurocrit Care. 2006;4:103–12.CrossRefPubMed Claassen J, Hirsch L, Frontera J, et al. Prognostic significance of continuous EEG monitoring in patients with poor-grade subarachnoid hemorrhage. Neurocrit Care. 2006;4:103–12.CrossRefPubMed
24.
go back to reference Claassen J, Taccone F, Horn P, Holtkamp M, Stocchetti N, Oddo M. Recommendations on the use of EEG monitoring in critically ill patients: consensus statement from the neurointensive care section of the ESICM. Intensiv Care Med. 2013;39:1337–51.CrossRef Claassen J, Taccone F, Horn P, Holtkamp M, Stocchetti N, Oddo M. Recommendations on the use of EEG monitoring in critically ill patients: consensus statement from the neurointensive care section of the ESICM. Intensiv Care Med. 2013;39:1337–51.CrossRef
25.
go back to reference Dankbaar J, Slooter A, Rinkel G, van der Schaaf I. Effect of different components of triple-H therapy on cerebral perfusion in patients with aneurysmal subarachnoid haemorrhage: a systematic review. Crit Care. 2010;14:R23.CrossRefPubMedPubMedCentral Dankbaar J, Slooter A, Rinkel G, van der Schaaf I. Effect of different components of triple-H therapy on cerebral perfusion in patients with aneurysmal subarachnoid haemorrhage: a systematic review. Crit Care. 2010;14:R23.CrossRefPubMedPubMedCentral
26.
go back to reference Gathier CS, van den Bergh WM, Slooter AJC, et al. HIMALAIA (Hypertension Induction in the Management of AneurysmaL subArachnoid haemorrhage with secondary IschaemiA): a randomized single-blind controlled trial of induced hypertension vs. no induced hypertension in the treatment of delayed cerebral ischem. Int J Stroke. 2014;9:375–80.CrossRefPubMed Gathier CS, van den Bergh WM, Slooter AJC, et al. HIMALAIA (Hypertension Induction in the Management of AneurysmaL subArachnoid haemorrhage with secondary IschaemiA): a randomized single-blind controlled trial of induced hypertension vs. no induced hypertension in the treatment of delayed cerebral ischem. Int J Stroke. 2014;9:375–80.CrossRefPubMed
27.
go back to reference Hofmeijer J, van Putten M. Ischemic cerebral damage: an appraisal of synaptic failure. Stroke. 2012;43:607–15.CrossRefPubMed Hofmeijer J, van Putten M. Ischemic cerebral damage: an appraisal of synaptic failure. Stroke. 2012;43:607–15.CrossRefPubMed
28.
go back to reference Leon-Carrion J, Martin-Rodriguez J, Damas-Lopez J, y Martin JB, Dominguez-Morales M. Delta-alpha ratio correlates with level of recovery after neurorehabilitation in patients with acquired brain injury. Clin Neurophysiol. 2009;120:1039–45.CrossRefPubMed Leon-Carrion J, Martin-Rodriguez J, Damas-Lopez J, y Martin JB, Dominguez-Morales M. Delta-alpha ratio correlates with level of recovery after neurorehabilitation in patients with acquired brain injury. Clin Neurophysiol. 2009;120:1039–45.CrossRefPubMed
29.
go back to reference Nuwer MR, Jordan SE, Ahn SS. Evaluation of stroke using EEG frequency analysis and topographic mapping. Neurology. 1987;37:11–53.CrossRef Nuwer MR, Jordan SE, Ahn SS. Evaluation of stroke using EEG frequency analysis and topographic mapping. Neurology. 1987;37:11–53.CrossRef
30.
go back to reference Vespa P, Boscardin J, Hovda D, et al. Early and persistent impaired percent alpha variability on continuous electroencephalography monitoring as predictive of poor outcome after traumatic brain injury. J Neurosurg. 2002;97:84–92.CrossRefPubMed Vespa P, Boscardin J, Hovda D, et al. Early and persistent impaired percent alpha variability on continuous electroencephalography monitoring as predictive of poor outcome after traumatic brain injury. J Neurosurg. 2002;97:84–92.CrossRefPubMed
Metadata
Title
Continuous EEG Monitoring for Early Detection of Delayed Cerebral Ischemia in Subarachnoid Hemorrhage: A Pilot Study
Authors
M. L. Rots
M. J. A. M. van Putten
C. W. E. Hoedemaekers
J. Horn
Publication date
01-04-2016
Publisher
Springer US
Published in
Neurocritical Care / Issue 2/2016
Print ISSN: 1541-6933
Electronic ISSN: 1556-0961
DOI
https://doi.org/10.1007/s12028-015-0205-y

Other articles of this Issue 2/2016

Neurocritical Care 2/2016 Go to the issue