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Cortical Spreading Depolarizations and Clinically Measured Scalp EEG Activity After Aneurysmal Subarachnoid Hemorrhage and Traumatic Brain Injury

Neurocritical Care volume 37, pages 49–59 (2022)Cite this article

Abstract

Background

Spreading depolarizations (SDs) are associated with worse outcome following subarachnoid hemorrhage (SAH) and traumatic brain injury (TBI), but gold standard detection requires electrocorticography with a subdural strip electrode. Electroencephalography (EEG) ictal–interictal continuum abnormalities are associated with poor outcomes after TBI and with both delayed cerebral ischemia (DCI) and poor outcomes after SAH. We examined rates of SD detection in patients with SAH and TBI with intraparenchymal and subdural strip electrodes and assessed which continuous EEG (cEEG) measures were associated with intracranially quantified SDs.

Methods

In this single-center cohort, we included patients with SAH and TBI undergoing ≥ 24 h of interpretable intracranial monitoring via eight-contact intraparenchymal or six-contact subdural strip platinum electrodes or both. SDs were rated according to established consensus criteria and compared with cEEG findings rated according to the American Clinical Neurophysiology Society critical care EEG monitoring consensus criteria: lateralized rhythmic delta activity, generalized rhythmic delta activity, lateralized periodic discharges, generalized periodic discharges, any ictal–interictal continuum, or a composite scalp EEG tool for seizure risk estimation: the 2HELPS2B score. Among patients with SAH, cEEG was assessed for validated DCI biomarkers: new or worsening epileptiform abnormalities and new background deterioration.

Results

Over 6 years, SDs were recorded in 5 (18%) of 28 patients recorded with intraparenchymal electrodes and 4 (40%) of 10 patients recorded with subdural strip electrodes. There was no significant association between occurrence of SDs and day 1 cEEG findings (American Clinical Neurophysiology Society main terms lateralized periodic discharges, generalized periodic discharges, lateralized rhythmic delta activity, or seizures, individually or in combination). After SAH, established cEEG DCI predictors were not associated with SDs.

Conclusions

Intraparenchymal recordings yielded low rates of SD, and documented SDs were not associated with ictal–interictal continuum abnormalities or other cEEG DCI predictors. Identifying scalp EEG correlates of SD may require training computational EEG analytics and use of gold standard subdural strip electrocorticography recordings.

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Funding

This work was supported by National Institutes of Health National Institute of Neurological Disorders and Stroke Grants 1K23NS105950 (ESR), KL2TR002542 (DYC), and K08NS112601 (DYC); United States Army Grant W81XWH-BAA-15-1 (ESR); the American Heart Association (18POST34030369; DYC); the Andrew David Heitman Foundation (ESR, ABP, DYC); the Aneurysm and AVM Foundation (DYC); and the Brain Aneurysm Foundation’s Timothy P. Susco and Andrew David Heitman Foundation Chairs of Research (DYC).

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Author notes

  1. David Y. Chung, Eric S. Rosenthal have equally contributed.

Authors and Affiliations

  1. Department of Neurology, Massachusetts General Hospital, Boston, MA, USA

    Shravan Sivakumar, Spyridoula Tsetsou, David Y. Chung & Eric S. Rosenthal

  2. Department of Neurosurgery, Massachusetts General Hospital, Boston, MA, USA

    Aman B. Patel, Christopher J. Stapleton, Benjamin L. Grannan & Jeffrey S. Schweitzer

Authors
  1. Shravan Sivakumar
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  2. Spyridoula Tsetsou
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  3. Aman B. Patel
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  4. Christopher J. Stapleton
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  5. Benjamin L. Grannan
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  6. Jeffrey S. Schweitzer
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  7. David Y. Chung
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  8. Eric S. Rosenthal
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Contributions

SS conceptualized the study design; conducted the data acquisition, analysis, and interpretation; and drafted and revised the manuscript. ABP, CJS, BLG, and JSS conceptualized the study design, performed intracranial monitoring, and contributed to drafting the manuscript. DYC contributed to the study design and Fig. modeling and conducted the data review, analysis, and interpretation, as well as manuscript revisions. ST contributed to data review and manuscript revisions. ESR conceptualized the study design and performed data analysis and interpretation, as well as manuscript drafting and revisions. DYC and ESR contributed equally to this work.

Corresponding author

Correspondence to Eric S. Rosenthal.

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Conflicts of interest

SS has nothing to disclose. ST has nothing to disclose. DYC has nothing to disclose. BLG has nothing to disclose. ABP has nothing to disclose. CJS has nothing to disclose. JSS has nothing to disclose. ESR reports consulting fees from UCB Pharma, Inc. and Ceribell, Inc.; medicolegal consultation; funding from National Institutes of Health National Institute of Neurological Disorders and Stroke grant 1K23NS105950 and United States Army grant W81XWH-BAA-15–1. ESR’s institution is a subcontract to Moberg ICU Solutions, whose clinical monitoring equipment was used in clinical practice in this patient population.

Ethical approval

The authors adhered to ethical guidelines, and this study was approved by the institutional review board.

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Sivakumar, S., Tsetsou, S., Patel, A.B. et al. Cortical Spreading Depolarizations and Clinically Measured Scalp EEG Activity After Aneurysmal Subarachnoid Hemorrhage and Traumatic Brain Injury. Neurocrit Care 37 (Suppl 1), 49–59 (2022). https://doi.org/10.1007/s12028-021-01418-7

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