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Incidence and Risk Factors for Intraoperative Seizures During Elective Craniotomy

Kutteruf, Rachel, MD*; Yang, Jen-Ting, MD, MS*; Hecker, James G., PhD, MD*; Kinney, Gregory A., PhD; Furman, Michele A., REEG/EP T, CNIM; Sharma, Deepak, MBBS, MD, DM‡,§

Journal of Neurosurgical Anesthesiology: April 2019 - Volume 31 - Issue 2 - p 234–240
doi: 10.1097/ANA.0000000000000506
Clinical Investigations
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SDC

Background: Perioperative seizures may affect 1% to 50% of patients undergoing craniotomy and adversely impact outcomes. However, data on intraoperative seizures are limited. This retrospective case-control study investigated the incidence and risk factors for intraoperative seizures during elective supratentorial craniotomy involving evoked potential monitoring.

Materials and Methods: Patients aged 18 years or above undergoing elective supratentorial craniotomy with evoked potential monitoring who experienced intraoperative seizures at our institution between December 2008 and March 2014 were compared with a control group generated using a random number generator. Six controls were used for each case from among the patients who underwent elective supratentorial craniotomy during the same calendar year. Multivariate analysis was conducted using logistic regression to identify the risk factors for intraoperative seizures.

Results: Among the 1916 patients who met the inclusion criteria, 45 (2.3%) had intraoperative seizures. The majority of seizures occurred during burr-hole placement or craniotomy, before lesion manipulation. Timing of seizures relative to motor evoked potential runs and stimulus intensity was variable. Significant risk factors for intraoperative seizures were seizure history (odds ratio [OR], 2.18; 95% confidence interval [CI], 1.07-4.46; P=0.03), diagnosis of brain tumor (OR, 2.41; 95% CI, 1.16-4.19; P=0.02), and temporal craniotomy (OR, 5.18; 95% CI, 2.03-13.25; P=0.001). Intraoperative prophylactic use of phenytoin/fosphenytoin and levetiracetam was protective against seizure (phenytoin/fosphenytoin: OR, 0.12; 95% CI, 0.04-0.35; P<0.001 and levetiracetam: OR, 0.40; 95% CI, 0.17-0.94; P=0.04). Phenytoin/fosphenytoin was more protective than levetiracetam (OR, 0.31; 95% CI, 0.10-0.99; P=0.048).

Conclusions: The overall incidence of intraoperative seizures was 2.3%. Independent risk factors for intraoperative seizures were seizure history, diagnosis of intracranial tumor, and temporal craniotomy. Intraoperative prophylactic anticonvulsant use was protective.

Departments of *Anesthesiology & Pain Medicine

Rehabilitation Medicine

Anesthesiology & Pain Medicine

§Neurological Surgery, University of Washington, Seattle, WA

The authors have no conflicts of interest to disclose.

Address correspondence to: Deepak Sharma, MBBS, MD, DM, Department of Anesthesiology and Pain Medicine, and Neurological Surgery, University of Washington, P.O. Box 359724, 325, 9th Ave, Seattle, WA (e-mail: dsharma@uw.edu).

Received January 9, 2018

Accepted April 5, 2018

Intraoperative seizure during craniotomy is a potential complication with serious ramifications, including increased cerebral metabolic rate of oxygen (CMRO2), increased intracranial pressure, delayed emergence from anesthesia, and disturbance of the surgical field.1 The reported incidence of perioperative seizures in patients undergoing craniotomy varies widely, ranging from 0.5% to 50%.2–5 The use of perioperative prophylactic anticonvulsants in patients without a history of seizures is controversial.1 Several guidelines recommend against the use of prophylactic anticonvulsants in aneurysmal subarachnoid hemorrhage,6 newly diagnosed brain tumors,7 and brain metastases.8 Despite these guidelines, a survey of American Association of Neurological Surgeons found that 70% prescribe prophylactic anticonvulsants after craniotomy.9

Data on intraoperative seizures are limited and risk factors for intraoperative seizures during elective craniotomy are unknown. The primary aim of this study was to determine the incidence and risk factors for intraoperative seizures during elective supratentorial craniotomy with evoked potential monitoring. In addition, we sought to describe the clinical characteristics of patients with intraoperative seizures and to evaluate the effectiveness of prophylactic anticonvulsants in this setting.

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MATERIALS AND METHODS

The Institutional Review Board at the University of Washington (Human Subjects Application #49415) approved this retrospective chart review and granted waiver of consent. Inclusion criteria were adult patients (aged 18 y and above) undergoing elective supratentorial craniotomy with intraoperative evoked potential monitoring at Harborview Medical Center (Seattle, WA) between December 2008 and March 2014. Exclusion criteria were emergent surgery, patients younger than 18 years, no intraoperative evoked potential monitoring, and craniotomy for posterior fossa lesions.

Data sources included institutional electronic medical records, including information in Online Record of Clinical Activity (ORCA), Anesthesia Information Management System (AIMS), the anesthesiology Continuous Quality Improvement (CQI) database, and the intraoperative neuromonitoring database (Cadwell Laboratories, Kennewick, WA). Data collected included clinical, pathologic, radiologic, surgical, and anesthetic characteristics, as well as evoked potential measurements. The primary outcome was intraoperative seizure identified from the CQI database, verified by notations in anesthetic record and neurosurgical procedure notes. The seizures were reported to the CQI database based on real-time clinical observation made in by the anesthesiology and neurosurgery teams as well as electroencephalogram (EEG) findings noted by the neuromonitoring team (when available). For each recorded seizure, there was a corresponding note in the anesthesiology as well as neurosurgery operative record documenting the clonic/jerking movement involving the extremities with or without involvement of the face. Twenty patients had EEG running at the time of seizure. In all of those patients, all channels showed seizure activity. Seventeen patients had 4 channels running; there were 1 each of 2, 3, and 10 channels. In order to ensure potential artefacts were differentiated from seizure activity on the EEG, the Neuromonitoring team ensured that all patients had a stable EEG without EMG immediately before the seizure event. Technical factors that can present artifacts on EEG, such as high impedance, 60 Hz noise as well as other sourced of high frequency electrical noise were managed and minimized by the software (common mode rejection), and by careful attention to setup and low impedance electrodes. The observation of relatively quiet, noise-free EEG channels showing regular EEG rhythms ensured that the technical noise was well managed to start with. Electrical noise generated by electrocautery can present in a manner that might be misinterpreted as seizure activity; but this is relatively easily discernible as the EEG seizure activity will have a lower amplitude, a more regular rhythm, and most significantly, electrocautery noise will cease shortly following the discontinuation of its use. The appearance of EEG seizure activity on quiet, noise-free channels which coincided with the surgeon and anesthesiologist’s observation of patient movement provided confirmation of the association of EEG activity with seizure.

A case-control study design was used to identify the risk factors for intraoperative seizure. A control group was obtained by using a random number generator to randomly select 6 controls for each case of intraoperative seizure from the patients who underwent elective supratentorial craniotomy during the same year as each seizure patient. The controls were included from the same year as the cases to avoid potential confounding factors, such as changes in surgical or anesthetic providers, care standard, and practice patterns, which may have varied over the 6-year study period. This matching procedure could also increase precision of the estimates.10

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Institutional Anesthetic Management for Elective Supratentorial Craniotomy

At our institution, it is standard practice to perform general anesthesia with total IV anesthetics for all patients undergoing elective supratentorial craniotomy with evoked potential monitoring. All patients receive infusions of propofol and remifentanil with/without adjuvants at the discretion of the attending anesthesiologist. Muscle relaxants are not used, beyond those required for intubation. All patients receive standard American Society of Anesthesiologists (ASA) monitoring and invasive arterial blood pressure monitoring. Some patients, at the discretion of the anesthesia provider, also have central venous access and may have jugular bulb catheters placed for cerebral oximetry monitoring. The use of prophylactic intraoperative anticonvulsants is a joint decision between the neurosurgeon and anesthesiologist. Our institutional practice involves checking plasma in the patients on phenytoin immediately preoperatively. In patients with subtherapeutic phenytoin levels, additional dose of phenytoin is administered. However, checking levetiracetam plasma levels is not a routine practice. If a decision was made to administer anticonvulsants intraoperatively, phenytoin was administered at a dose of 15 to 20 mg/kg at the discretion of the attending anesthesiologist and levetiracetam at a fixed dose of 1000 mg. However, subsequent plasma levels of anticonvulsants were not checked again. The use of evoked potential monitoring for each case is based on the discretion of neurosurgery attending.

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Institutional Intraoperative Evoked Potential Monitoring

Somatosensory evoked potentials (SSEPs) and transcranial motor evoked potentials (tcMEPs) are setup following anesthesia induction by a dedicated intraoperative neurophysiology team. Standard ½′′ subcutaneous needles are used at all stimulation and recording sites. Tibial and median nerve SSEPs are stimulated at the ankle and wrist, respectively, and recorded at Cz′-Fz, C3′-Fz, C4′-Fz, and Fz-mastoid. In addition, peripheral pickups are placed at Erb’s point (median) and abductor hallucis (tibial). tcMEPs are stimulated with electrodes placed at C3 and C4, with polarity switching accomplished via software control. tcMEP responses are recorded at contralateral thenar and abductor hallucis muscles. In addition, 4 channels of EEG activity are typically recorded using C3′/C4′-Fz, Cz′-Fz, and Fz′-mastoid. For SSEPs and tcMEPs, the usual filter settings are 30 to 1000 Hz. Analysis time is set at 50 msec for median nerve stimulation and 100 msec for tibial and tcMEP stimulation. Tibial and median nerves are stimulated at 3.1 Hz using a 0.2 msec duration pulse at an intensity of 50 and 25 mA, respectively. tcMEPs are stimulated using a train of 4 to 9 pulses with an interstimulus interval of 2 msec and a maximum intensity of 560 V. EEG filter settings are set from 0.5 to 50 Hz; processed EEG is analyzed with 10 second epochs of raw EEG. SSEPs are monitored at 10 minute timed intervals throughout the procedure. tcMEPs are manually monitored at 5 to 15 minute intervals and may be delayed occasionally to eliminate patient movement during critical portions of the surgical procedure. In many instances the use of tcMEPs was discontinued at the advent of seizure activity. EEG monitoring is continuous throughout the procedure. A Cadwell Cascade Pro or Elite neurophysiological monitoring system (Cadwell Laboratories) is used for stimulation and recording.

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Statistical Analysis

Descriptive statistics were used to present the characteristics of patients with intraoperative seizures. Data are presented as number (percent), mean±SD, or median (range), as appropriate. For the case-control study, univariate analyses were conducted using logistic regression with intraoperative seizure as the outcome variable and the year of surgery as a covariate. The explanatory variables were age, sex, comorbidities, preoperative diagnosis, surgical procedure, craniotomy side and approach, presence of intraoperative brain swelling, intraoperative prophylactic anticonvulsant medication, and preoperative radiologic finding, respectively. To address potential collinearity among identified risk factors, a secondary multivariate analysis was conducted using logistic regression with intraoperative seizure as the outcome variable, and year of surgery and those significant risk factors identified in the univariate analyses as the covariates. By using this model, the significance of each significant risk factor was examined, respectively by controlling for all other identified risk factors. For all analyses, a 2-sided P<0.05 was considered statistically significant. All statistical analyses were performed using STATA version 13.1 (StataCorp LP, College Station, TX).

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RESULTS

Intraoperative Seizures

During the study period, 1916 patients underwent elective supratentorial craniotomy with evoked potential monitoring at our institution and met the inclusion criteria. Among these, 45 patients (2.3%) had intraoperative seizures. There was an increase in the incidence of intraoperative seizures between 2010 and 2011 (Fig. 1), which was temporally associated with an institutional change in the agents used for intraoperative seizure prophylaxis. In 2010, phenytoin was replaced by levetiracetam for seizure prophylaxis. In late 2011, due to concerns about increasing rates of intraoperative seizures, levetiracetam was replaced with fosphenytoin. This change appeared to coincide with a decrease in the incidence of intraoperative seizures during elective craniotomies.

FIGURE 1

FIGURE 1

The patients who suffered intraoperative seizures were 47±13 years old, and 51% of them were male individuals. Only 31% had a history of seizures and 47% were on anticonvulsant medications preoperatively (29% levetiracetam, 16% phenytoin, and 2% both levetiracetam and phenytoin). The majority (62%) of these patients did not receive prophylactic anticonvulsant medication intraoperatively, although 22% received prophylactic levetiracetam and 13% received prophylactic phenytoin or fosphenytoin (Fig. 2). Phenytoin was administered at a dose of 15 to 20 mg/kg at the discretion of the attending anesthesiologist and levetiracetam at a fixed dose of 1000 mg. The most common intracranial pathology among patients with intraoperative seizures was tumor (53%), followed by aneurysm (27%) (Fig. 3). The most common craniotomy approach in patients with intraoperative seizures was frontotemporal (56%), followed by temporal (22%), and frontal (18%). The vast majority of seizures (87%) occurred during burr-hole placement and craniotomy, with a few occurring during lesion manipulation (4%) or closure (7%). All patients with intraoperative seizures were started on anticonvulsant medications postoperatively by the Neurosurgery team.

FIGURE 2

FIGURE 2

FIGURE 3

FIGURE 3

All patients (both seizure and control groups) received total IV anesthesia. The dose of propofol and remifentanil at the time of seizure was 159±54.5 and 0.19±0.09 mcg/kg/min, respectively. The majority of patients (82%) were normocapnic (ETCO2=30 to 40 mm Hg) at the time of seizure, whereas 16% were hypocapnic (ETCO2<30 mm Hg) and 3% were hypercapnic (ETCO2>40 mm Hg). Fifty-six percent of the patients who seized were electively kept intubated at the conclusion of surgery at the discretion of the operative team.

All patients underwent intraoperative evoked potential monitoring consisting of SSEPs, MEPs, and EEG. The timing of seizures in relation to MEP runs was variable, (median 57.5 [0 to 142] min), as was the median number of MEP runs before seizure (6 [0 to 72]). Highest MEP stimulation intensity before seizure was also variable, with a median train of 6 (range, 3 to 8), median electrical potential of 365 (range, 160 to 560) V, and median current of 771.5 (range, 332 to 1312) mA. Of note, no seizures were noted in patients undergoing spine surgery with similar intraoperative evoked potential monitoring and TIVA anesthetics during the same period. Figure 4 demonstrates the EEG from a representative case of intraoperative seizure.

FIGURE 4

FIGURE 4

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Case-Control Study

To match the 45 patients with intraoperative seizures, 270 control patients without intraoperative seizure were selected using a random number generator. The mean age of the control group was 49.5±14.4 years old (P=0.34, compared with the case group.) The univariate analyses were composed of 4 potential contributing factors, including patient characteristics, preoperative radiologic findings, surgical diagnosis, and approach, and prophylactic anticonvulsant use. The estimates are summarized in Tables 1–3. A history of preoperative seizure was significantly associated with intraoperative seizure (odds ratio [OR], 2.18; confidence interval [CI], 1.07-4.46; P=0.03), whereas age, sex, other investigated medical conditions, and preoperative radiologic findings (lesion size, mass effect, midline shift, hydrocephalus, and cerebral edema) were not associated with intraoperative seizures. Brain tumor diagnosis was associated with higher likelihood of intraoperative seizure compared with arteriovenous malformation, aneurysm, and vascular occlusion. The difference was significant between brain tumor and other diagnoses altogether (surgical diagnosis analysis 2 in Table 2: OR, 2.41; 95% CI, 1.16-4.19; P=0.02). Likewise, temporal craniotomy were associated with the highest likelihood of intraoperative seizure and the difference was significant between temporal and other approaches altogether (surgical approach analysis 2 in Table 2: OR, 5.18; 95% CI, 2.03-13.25; P=0.001). There was no significant difference in intraoperative seizures either in patients taking anticonvulsants preoperatively compared with those who did not (P=0.45), or in patients receiving local anesthetics before incision compared with those who did not (P=0.55). However, prophylactic intraoperative use of phenytoin or fosphenytoin was associated with a significant reduction in intraoperative seizures compared with levetiracetam (OR, 0.31; 95% CI, 0.10-0.99; P=0.048) or no use of intraoperative prophylaxis (OR, 0.12; 95% CI, 0.04-0.35; P<0.001). Among the patients with tumors (24 cases and 93 controls), there was no statistically significant difference in the histopathologic diagnosis of the tumor.

TABLE 1

TABLE 1

TABLE 2

TABLE 2

TABLE 3

TABLE 3

Multivariate logistic regression (Table 4) demonstrated that after controlling for the other significant risk factors identified in the univarite analyses, seizure history (OR, 2.76; 95% CI, 1.22-6.23; P=0.02), diagnosis of brain tumor (OR, 2.15; 95% CI, 1.04-4.46; P=0.04), and temporal craniotomy approach (OR, 6.57; 95% CI, 2.17-19.85; P=0.001) remained significant. In addition, prophylactic intraoperative use of phenytoin/fosphenytoin and levetiracetam were found to be protective against intraoperative seizure compared with no use of prophylactic anticonvulsants (phenytoin/fosphenytoin: OR, 0.09; 95% CI, 0.03-0.29; P<0.001 and levetiracetam: OR, 0.34; 95% CI, 0.14-0.87; P=0.03). When compared with each other, phenytoin/fosphenytoin was significantly more protective than levetiracetam (OR, 0.28; 95% CI, 0.08-0.98; P=0.046). The result is robust to the sensitivity test using P-value of 0.1 as the criterion of forward selection.

TABLE 4

TABLE 4

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DISCUSSION

In summary, the overall incidence of intraoperative seizures during elective supratentorial craniotomy with evoked potential monitoring during the study period was 2.3%. A history of seizures, diagnosis of intracranial tumor, and temporal craniotomy approach were associated with higher risk of intraoperative seizure, whereas intraoperative prophylactic anticonvulsant use was protective; although phenytoin/fosphenytoin provided better protection than levetiracetam or no prophylaxis. To the best of our knowledge, this study provides the first estimates of this intraoperative complication and identifies the risk factors for the same.

Intraoperative seizures during cranial surgery may be detrimental. In a previous report, Howe et al,5 noted a 0.5% incidence of intraoperative seizures in a cohort of 400 patients with EEG monitoring. Although specific anesthetic and monitoring details were not provided, the seizures in their series were identified on EEG and the patients were not reported to receive evoked potential monitoring. Electrical stimulation of the brain has been reported to result in a clinical seizure.11,12 However, the seizure-inducing current amplitude thresholds are typically 2 to 3 orders of magnitude above the maximum tcMEPs and evoked potential monitoring is generally considered safe.11,12 In fact, tcMEPs during spinal deformity surgery do not appear to trigger intraoperative seizures in patients suffering seizures preoperatively.13 It has been demonstrated that a craniotomy affects current spread from a MEP while this is not seen in spinal surgery.14 However, in a recent study, Ulkatan et al,15 investigated the incidence of seizures during the intraoperative monitoring of MEPs in a wide spectrum of surgeries including orthopedic spine, spinal cord, and peripheral nerves, interventional radiology procedures, and craniotomies. In this mixed surgical population cohort of 4179 patients, 32 (0.8%) had intraoperative seizures and the incidence of seizures in cranial procedures was 1.8%.15 None of the patients who underwent surgery for conditions of the spinal cord, neck, or peripheral nerves or who underwent cranial or noncranial interventional radiology procedures had intraoperative seizures. Although the incidence of intraoperative seizures was low, the study did indicate a relatively higher risk during craniotomy.15 Our findings add to the existing literature by specifically providing estimates of seizure during supratentorial craniotomy with evoked potential monitoring and identifying risk factors for the same.

It is not surprising that a history of seizure put patients at increased risk for intraoperative seizures, especially during intracranial procedures. It has been previously demonstrated that patients with seizure disorders are at increased risk of perioperative seizures even when intracranial procedures are excluded from analysis.16 Factors that may play a role in this increased risk of intraoperative and perioperative seizures include missed doses of antiepileptic medications, medication interactions, administration of medications that lower the seizure threshold, altered gastrointestinal absorption, and sleep deprivation.16 Although a history of seizure was an independent risk factor for intraoperative seizures, the majority of patients in our study group did not have a history of seizures. Anesthesiologists should remain vigilant about the possibility of intraoperative seizure during craniotomy with MEP monitoring even in patients without a seizure history.

Wong et al2,3 reported the incidence of perioperative seizures following craniotomy for a variety of pathologies, based on literature review. They found that early postoperative seizures occurred in 1% to 12% of patients with intracranial tumors,2 while 4% to 42% of patients undergoing craniotomy for aneurysm experienced a perioperative seizure.3 Others have observed perioperative seizures in 15% to 50% of patients undergoing brain tumor suergery.4 It is hypothesized that tumor-related seizures are due to structural and metabolic derangements related to the mass itself, as well as the subsequent craniotomy that is often necessary for diagnosis and treatment.4 We found that patients with intracranial tumors had a higher risk of seizures during surgery (OR, 3.04; 95% CI, 1.44-6.44; P=0.004). This may have implications for administration of prophylactic intraoperative anticonvulsants. Practice guidelines published in 2000 by the American Academy of Neurology advised that antiepileptic medications are not effective in preventing first seizures in patients with newly diagnosed brain tumors and those patients who are started on antiepileptics in the perioperative period should be quickly tapered off of these medications.7 These recommendations were based on a meta-analysis that found limited or no benefit to the use of prophylactic anticonvulsants in the postcraniotomy setting, particularly in those patients without preexisting seizures.4,7 However, our finding may warrant consideration for prophylactic anticonvulsants to prevent intraoperative seizures during temporal craniotomy with evoked potential monitoring in patients with supratentorial tumors who have a history of seizures.

We also found temporal craniotomy to be an independent risk factor for intraoperative seizure. The surgical approach may, in fact, be a surrogate for the location of the intracranial pathology. The association of frontal or temporal lobe tumors with increased risk of perioperative seizures appears to corroborate our observation.17–19 The majority of intraoperative seizures identified in the current study occurred before brain or lesion manipulation, suggesting direct cortical stimulation was not the cause of the seizure. Rather, the seizure threshold may have been lowered due to factors related to the lesion itself, such as the production of inflammatory biomarkers, changes in neurotransmitter activity, or regional metabolic changes resulting from intracranial pathology.17

Levetiracetam has been shown to have a more favorable side effect profile than phenytoin,20,21 which has led to a reduction in the use of phenytoin for seizure prophylaxis in the perioperative period. Specifically, phenytoin is capable of cytochrome P450 hepatic enzyme induction and can thus interfere with the efficacy and metabolism of many other medications, including corticosteroids and chemotherapeutic agents often used in the treatment of brain tumors.4,21,22 Levetiracetam undergoes primarily renal metabolism and thus, has limited impact on other coadministered medications.4 Studies evaluating the efficacy of levetiracetam versus phenytoin in the prevention of postoperative seizures following craniotomy have had mixed results, with some studies finding no significant difference in efficacy20,22 and others showing levetiracetam to be more effective.21 However, we found prophylactic phenytoin or fosphenytoin to be more effective than levetiracetam in preventing intraoperative seizures. Although levetiracetam may be less effective in this setting due to possible underdosing (fixed dose administration as opposed to weight based) or renal clearance, the reason for this is unclear and warrants further investigation. Of note, levetiracetam has been reported to be associated with a paradoxical increase (>25%) in seizure frequency in patients with refractory epilepsy.23

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Limitations

There are several limitations of this study. First, it is a single institution, retrospective study and patients were not randomized into treatment groups. Data collection is subject to potential documentation bias. Perioperative and intraoperative environments were not standardized. The administration of prophylactic anticonvulsants was dependent on the providers involved in the case and plasma levels of anticonvulsant agents were not checked intraoperatively. Therefore, underdosing of anticonvulsant agents cannot be ruled out. Confounding factors that were not measured may have affected the results of this study. In addition, the incidence of the outcome of interest (intraoperative seizures) is small and the limited EEG montage does not allow definitely excluding movement artefact. A larger study population would provide better statistical power for a more robust analysis of potential risk factors.

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CONCLUSIONS

The incidence of intraoperative seizures during elective craniotomy with evoked potential monitoring is low. Patients are at increased risk of intraoperative seizure if they have a history of seizure, a tumor diagnosis, or are undergoing a temporal craniotomy. The risk of intraoperative seizure may be reduced with the administration of prophylactic intraoperative phenytoin or fosphenytoin compared with no prophylaxis or levetiracetam.

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Keywords:

intraoperative; seizure; craniotomy; anesthesia; phenytoin; fosphenytoin; levetiracetam

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