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Brain Advance Access originally published online on October 25, 2006
Brain 2006 129(12):3224-3237; doi:10.1093/brain/awl297
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© 2006 The Author(s)
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations

Jens P. Dreier1,*, Johannes Woitzik5,*, Martin Fabricius7,*, Robin Bhatia9, Sebastian Major1, Chistoph Drenckhahn1, Thomas-Nicolas Lehmann2, Asita Sarrafzadeh2, Lisette Willumsen8, Jed A. Hartings10, Oliver W. Sakowitz6, Jörg H. Seemann3, Anja Thieme4, Martin Lauritzen7 and Anthony J. Strong9

1 Department of Experimental Neurology and Neurology, Charité University Medicine Berlin Berlin 2 Department of Neurosurgery, Charité University Medicine Berlin Berlin 3 Department of Neuroradiology, Charité University Medicine Berlin Berlin 4 Department of Anaesthesiology, Charité University Medicine Berlin Berlin 5 Department of Neurosurgery, University Hospital Mannheim Faculty for Clinical Medicine of the University of Heidelberg, Mannheim 6 Department of Neurosurgery, University of Heidelberg Heidelberg, Germany 7 Department of Clinical Neurophysiology Glostrup Hospital, Copenhagen, Denmark 8 Department of Neurosurgery, University of Copenhagen Glostrup Hospital, Copenhagen, Denmark 9 Department of Neurosurgery, King's College London, UK 10 The Division of Psychiatry and Neuroscience, Walter Reed Army Institute of Research Silver Spring, MD, USA

Correspondence to: Jens P. Dreier, Department of Neurology, Campus Charité Mitte, Charité University Medicine Berlin, Schumannstrasse 20-21, 10117 Berlin, Germany E-mail: jens.dreier{at}charite.de

Progressive ischaemic damage in animals is associated with spreading mass depolarizations of neurons and astrocytes, detected as spreading negative slow voltage variations. Speculation on whether spreading depolarizations occur in human ischaemic stroke has continued for the past 60 years. Therefore, we performed a prospective multicentre study assessing incidence and timing of spreading depolarizations and delayed ischaemic neurological deficit (DIND) in patients with major subarachnoid haemorrhage (SAH) requiring aneurysm surgery. Spreading depolarizations were recorded by electrocorticography with a subdural electrode strip placed on cerebral cortex for up to 10 days. A total of 2110 h recording time was analysed. The clinical state was monitored every 6 h. Delayed infarcts after SAH were verified by serial CT scans and/or MRI. Electrocorticography revealed 298 spreading depolarizations in 13 of the 18 patients (72%). A clinical DIND was observed in seven patients 7.8 days (7.3, 8.2) after SAH. DIND was time-locked to a sequence of recurrent spreading depolarizations in every single case (positive and negative predictive values: 86 and 100%, respectively). In four patients delayed infarcts developed in the recording area. As in the ischaemic penumbra of animals, delayed infarction was preceded by progressive prolongation of the electrocorticographic depression periods associated with spreading depolarizations to >60 min in each case. This study demonstrates that spreading depolarizations have a high incidence in major SAH and occur in ischaemic stroke. Repeated spreading depolarizations with prolonged depression periods are an early indicator of delayed ischaemic brain damage after SAH. In view of experimental evidence and the present clinical results, we suggest that spreading depolarizations with prolonged depressions are a promising target for treatment development in SAH and ischaemic stroke.

Key Words: cortical spreading depression; electrocorticography; ischaemic stroke; spreading ischaemia; subarachnoid haemorrhage

Abbreviations: AD, anoxic depolarization; DIND, delayed ischaemic neurological deficit; DSA, digital subtraction angiography; ICP, intracranial pressure; MCA, middle cerebral artery; SAH, subarachnoid haemorrhage; SD, spreading depression; TCD, transcranial Doppler sonography

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Received April 8, 2006. Revised September 14, 2006. Accepted September 15, 2006.

*These authors contributed equally to this work.


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