Impact of intraoperative direct cortical stimulation dynamics on perioperative seizures and afterdischarge frequency in patients undergoing awake craniotomy

Collin J. LarkinDepartment of Neurological Surgery, Northwestern University, Feinberg School of Medicine and McGaw Medical Center, Chicago;

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Ketan YerneniDepartment of Neurological Surgery, Northwestern University, Feinberg School of Medicine and McGaw Medical Center, Chicago;

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Constantine L. KarrasDepartment of Neurological Surgery, Northwestern University, Feinberg School of Medicine and McGaw Medical Center, Chicago;

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Zachary A. AbecassisDepartment of Neurological Surgery, Northwestern University, Feinberg School of Medicine and McGaw Medical Center, Chicago;

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Guangyu ZhouDepartment of Neuroscience, Northwestern University, Feinberg School of Medicine, Chicago; and

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Christina ZelanoDepartment of Neuroscience, Northwestern University, Feinberg School of Medicine, Chicago; and

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Ashley N. SelnerDepartment of Neurological Surgery, Northwestern University, Feinberg School of Medicine and McGaw Medical Center, Chicago;

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Jessica W. TemplerDepartment of Neurology, Northwestern University, Feinberg School of Medicine and McGaw Medical Center, Chicago, Illinois

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Matthew C. TateDepartment of Neurological Surgery, Northwestern University, Feinberg School of Medicine and McGaw Medical Center, Chicago;
Department of Neurology, Northwestern University, Feinberg School of Medicine and McGaw Medical Center, Chicago, Illinois

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OBJECTIVE

Intraoperative stimulation is used as a crucial adjunct in neurosurgical oncology, allowing for greater extent of resection while minimizing morbidity. However, limited data exist regarding the impact of cortical stimulation on the frequency of perioperative seizures in these patients.

METHODS

A retrospective chart review of patients undergoing awake craniotomy with electrocorticography data by a single surgeon at the authors’ institution between 2013 and 2020 was conducted. Eighty-three patients were identified, and electrocorticography, stimulation, and afterdischarge (AD)/seizure data were collected and analyzed. Stimulation characteristics (number, amplitude, density [stimulations per minute], composite score [amplitude × density], total and average stimulation duration, and number of positive stimulation sites) were analyzed for association with intraoperative seizures (ISs), ADs, and postoperative clinical seizures.

RESULTS

Total stimulation duration (p = 0.005), average stimulation duration (p = 0.010), and number of stimulations (p = 0.020) were found to significantly impact AD incidence. A total stimulation duration of more than 145 seconds (p = 0.04) and more than 60 total stimulations (p = 0.03) resulted in significantly higher rates of ADs. The total number of positive stimulation sites was associated with increased IS (p = 0.048). Lesions located within the insula (p = 0.027) were associated with increased incidence of ADs. Patients undergoing repeat awake craniotomy were more likely to experience IS (p = 0.013). Preoperative antiepileptic drug use, seizure history, and number of prior resections of any type showed no impact on the outcomes considered.

The charge transferred to the cortex per second during mapping was significantly higher in the 10 seconds leading to AD than at any other time point examined in patients experiencing ADs, and was significantly higher than any time point in patients not experiencing ADs or ISs. Although the rate of transfer for patients experiencing ISs was highest in the 10 seconds prior to the seizure, it was not significantly different from those who did not experience an AD or IS.

CONCLUSIONS

The data suggest that intraoperative cortical stimulation is a safe and effective technique in maximizing extent of resection while minimizing neurological morbidity in patients undergoing awake craniotomies, and that surgeons may avoid ADs and ISs by minimizing duration and total number of stimulations and by decreasing the overall charge transferred to the cortex during mapping procedures.

ABBREVIATIONS

AD = afterdischarge; AED = antiepileptic drug; ECoG = electrocorticography; EOR = extent of resection; IDH = isocitrate dehydrogenase; IS = intraoperative seizure; LOS = length of stay.
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