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Minimally Invasive Electrocorticography, Continuous EEG Do Not Reliably Detect Spreading Depolarizations

Key findings

  • This single-center prospective study evaluated the frequency of spreading depolarizations (SDs) during clinical multimodal monitoring of 35 comatose adults with aneurysmal subarachnoid hemorrhage or traumatic brain injury
  • All patients underwent electrocorticography (using conventional subdural strip electrodes, minimally invasive intraparenchymal electrodes, or both types of electrodes) and were also monitored with continuous scalp EEG (cEEG)
  • SDs were detected in five of 29 patients (18%) with intraparenchymal electrodes and four of 10 patients (40%) with subdural strip electrodes
  • There were no significant associations between cEEG measures and the occurrence of SD
  • Two cEEG abnormalities, shown in previous research at Massachusetts General Hospital to predict delayed cerebral ischemia (DCI) in patients with subarachnoid hemorrhage, predicted DCI in the current study but were not specific for SDs

In patients with subarachnoid hemorrhage (SAH) or traumatic brain injury (TBI), spreading depolarizations (SDs), suppression of neural activity that propagates in waves through the cortex, are a secondary form of brain injury. SDs are associated with poorer outcomes, so monitoring for them can help in risk stratification.

However, the detection of SDs conventionally relies on invasive neuromonitoring, such as electrocorticography (ECoG) after the subdural placement of electrodes.

Massachusetts General Hospital researchers previously reported in Clinical Neurophysiology that certain abnormalities on continuous electroencephalography (cEEG) predicted delayed cerebral ischemia (DCI) after SAH. The risk of DCI may be partly due to hypermetabolism, which could trigger, or be triggered by, the initiation of SDs.

Shravan Sivakumar, MBBS, a research fellow in the Department of Neurology at Mass General, David Y. Chung, MD, PhD, an attending in the Neurocritical Care Units, Eric S. Rosenthal, MD, director of the Neuroscience Intensive Care Unit, and colleagues recently built on that research. They examined the ability of cEEG and a less invasive method of ECoG to detect SDs, but in Neurocritical Care, they present negative results.

Methods

The prospective study included 35 comatose adults who underwent ECoG monitoring at Mass General between May 2014 and May 2020 after aneurysmal SAH (n=20 with Hunt and Hess grade 4 or 5) or TBI (n=15 with Glasgow Coma Scale score ≤8).

Depending on the neurosurgical management required, ECoG was conducted with an intraparenchymal electrode inserted via a cranial bolt, a subdural strip electrode implanted during craniotomy, or both types of electrodes. All patients were also monitored with scalp cEEG.

The median duration of monitoring per patient was 120 hours (range, 72–164).

Influence of Electrode Type on SD Detection

SD detection rates with ECoG were low:

  • 5 of 29 patients (18%) who had intraparenchymal electrodes
  • 4 of 10 patients (40%) who had subdural strip electrodes

Further exploration is necessary to determine whether few SDs were detected with the less invasive form of ECoG because of the monitoring methodology itself or because patients were less severely ill than those who needed craniotomy.

SD Detection With cEEG

cEEG recordings were analyzed for the main terms of the American Clinical Neurophysiology Society (ACNS) critical care EEG monitoring consensus criteria, individually and in combination:

  • Lateralized rhythmic delta activity
  • Lateralized rhythmic delta activity
  • Lateralized periodic discharges
  • Generalized periodic discharges
  • The 2HELPS2B score, a tool for estimating seizure risk

In patients with SAH, there were no significant associations between the occurrence of SDs and any of these measures, either on the first day of monitoring or over the entire monitoring period. The same was true when patients with SAH or TBI were considered together.

The relationships were not examined for the TBI group because SDs were identified in only one patient in that cohort.

cEEG and DCI

cEEGs for patients with SAH were analyzed for the findings previously validated at Mass General as predicting DCI after SAH: new or worsening epileptiform abnormalities and new background activity deterioration.

As in the previous study, those biomarkers predicted DCI. However, they were not specific for SDs—DCI always occurred when SDs were present and when SDs were absent. It's unclear whether the biomarkers represent a contributor to DCI independent of SDs or whether scalp cEEG is insufficient to detect SDs.

Continued Scrutiny Needed

SDs have been proposed as targets for novel therapeutic approaches, so it's important to find noninvasive ways to identify them. There's sufficient evidence to recommend further study of intraparenchymal depth electrode placement for SD identification. Scalp cEEG is currently ineffective when used alone to detect SDs, and any future studies should pair it with subdural strip electrodes or the equivalent.

40%
rate of detection of spreading depolarizations with conventional subdural strip electrodes

18%
rate of detection of spreading depolarizations with minimally invasive intraparenchymal electrodes

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