Pediatric stereo-electroencephalography: effects of robot assistance and other variables on seizure outcome and complications

Ioannis N. Mavridis Departments of Neurosurgery,

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William B. Lo Departments of Neurosurgery,

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Welege Samantha Buddhika Wimalachandra Departments of Neurosurgery,

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Sunny Philip Neurology, and

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Shakti Agrawal Neurology, and

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Caroline Scott Neurophysiology, Birmingham Children’s Hospital, Birmingham, United Kingdom

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Darren Martin-Lamb Neurophysiology, Birmingham Children’s Hospital, Birmingham, United Kingdom

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Bryony Carr Neurophysiology, Birmingham Children’s Hospital, Birmingham, United Kingdom

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Peter Bill Neurophysiology, Birmingham Children’s Hospital, Birmingham, United Kingdom

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Andrew Lawley Neurophysiology, Birmingham Children’s Hospital, Birmingham, United Kingdom

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Stefano Seri Neurophysiology, Birmingham Children’s Hospital, Birmingham, United Kingdom

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A. Richard Walsh Departments of Neurosurgery,

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OBJECTIVE

The safety of stereo-electroencephalography (SEEG) has been investigated; however, most studies have not differentiated pediatric and adult populations, which have different anatomy and physiology. The purpose of this study was to assess SEEG safety in the pediatric setting, focusing on surgical complications and the identification of patient and surgical risk factors, if any. The authors also aimed to determine whether robot assistance in SEEG was associated with a change in practice, surgical parameters, and clinical outcomes.

METHODS

The authors retrospectively studied all SEEG cases performed in their department from December 2014 to March 2020. They analyzed both demographic and surgical variables and noted the types of surgery-related complications and their management. They also studied the clinical outcomes of a subset of the patients in relation to robot-assisted and non–robot-assisted SEEG.

RESULTS

Sixty-three children had undergone 64 SEEG procedures. Girls were on average 3 years younger than the boys (mean age 11.1 vs 14.1 years, p < 0.01). The overall complication rate was 6.3%, and the complication rate for patients with left-sided electrodes was higher than that for patients with right-sided electrodes (11.1% vs 3.3%), although the difference between the two groups was not statistically significant. The duration of recording was positively correlated to the number of implanted electrodes (r = 0.296, p < 0.05). Robot assistance was associated with a higher number of implanted electrodes (mean 12.6 vs 7.6 electrodes, p < 0.0001). Robot-assisted implantations were more accurate, with a mean error of 1.51 mm at the target compared to 2.98 mm in nonrobot implantations (p < 0.001). Clinical outcomes were assessed in the first 32 patients treated (16 in the nonrobot group and 16 in the robot group), 23 of whom proceeded to further resective surgery. The children who had undergone robot-assisted SEEG had better eventual seizure control following subsequent epilepsy surgery. Of the children who had undergone resective epilepsy surgery, 42% (5/12) in the nonrobot group and 82% (9/11) in the robot group obtained an Engel class IA outcome at 1 year (χ2 = 3.885, p = 0.049). Based on Kaplan-Meier survival analysis, the robot group had a higher seizure-free rate than the nonrobot group at 30 months postoperation (7/11 vs 2/12, p = 0.063). Two complications, whose causes were attributed to the implantation and head-bandaging steps, required surgical intervention. All complications were either transient or reversible.

CONCLUSIONS

This is the largest single-center, exclusively pediatric SEEG series that includes robot assistance so far. SEEG complications are uncommon and usually transient or treatable. Robot assistance enabled implantation of more electrodes and improved epilepsy surgery outcomes, as compared to those in the non–robot-assisted cases.

ABBREVIATIONS

CT = computed tomography; MRI = magnetic resonance imaging; SEEG = stereo-electroencephalography.

OBJECTIVE

The safety of stereo-electroencephalography (SEEG) has been investigated; however, most studies have not differentiated pediatric and adult populations, which have different anatomy and physiology. The purpose of this study was to assess SEEG safety in the pediatric setting, focusing on surgical complications and the identification of patient and surgical risk factors, if any. The authors also aimed to determine whether robot assistance in SEEG was associated with a change in practice, surgical parameters, and clinical outcomes.

METHODS

The authors retrospectively studied all SEEG cases performed in their department from December 2014 to March 2020. They analyzed both demographic and surgical variables and noted the types of surgery-related complications and their management. They also studied the clinical outcomes of a subset of the patients in relation to robot-assisted and non–robot-assisted SEEG.

RESULTS

Sixty-three children had undergone 64 SEEG procedures. Girls were on average 3 years younger than the boys (mean age 11.1 vs 14.1 years, p < 0.01). The overall complication rate was 6.3%, and the complication rate for patients with left-sided electrodes was higher than that for patients with right-sided electrodes (11.1% vs 3.3%), although the difference between the two groups was not statistically significant. The duration of recording was positively correlated to the number of implanted electrodes (r = 0.296, p < 0.05). Robot assistance was associated with a higher number of implanted electrodes (mean 12.6 vs 7.6 electrodes, p < 0.0001). Robot-assisted implantations were more accurate, with a mean error of 1.51 mm at the target compared to 2.98 mm in nonrobot implantations (p < 0.001). Clinical outcomes were assessed in the first 32 patients treated (16 in the nonrobot group and 16 in the robot group), 23 of whom proceeded to further resective surgery. The children who had undergone robot-assisted SEEG had better eventual seizure control following subsequent epilepsy surgery. Of the children who had undergone resective epilepsy surgery, 42% (5/12) in the nonrobot group and 82% (9/11) in the robot group obtained an Engel class IA outcome at 1 year (χ2 = 3.885, p = 0.049). Based on Kaplan-Meier survival analysis, the robot group had a higher seizure-free rate than the nonrobot group at 30 months postoperation (7/11 vs 2/12, p = 0.063). Two complications, whose causes were attributed to the implantation and head-bandaging steps, required surgical intervention. All complications were either transient or reversible.

CONCLUSIONS

This is the largest single-center, exclusively pediatric SEEG series that includes robot assistance so far. SEEG complications are uncommon and usually transient or treatable. Robot assistance enabled implantation of more electrodes and improved epilepsy surgery outcomes, as compared to those in the non–robot-assisted cases.

In Brief

Authors of this study assessed stereo-electroencephalography (SEEG) safety in the pediatric setting, focusing on surgical complications, and explored whether robot assistance was associated with a change in practice, surgical parameters, and clinical outcomes. SEEG complications are uncommon and usually transient or treatable. Robot assistance enabled implantation of more electrodes and improved epilepsy surgery outcome compared to those in non—robot-assisted cases. This is the largest single-center, exclusively pediatric SEEG series that includes robot assistance so far.

Although stereo-electroencephalography (SEEG) was developed in the second half of the 20th century (by Jean Talairach and Jean Bancaud1,2), it is the 21st century that brought its value in epilepsy surgery to the foreground and revolutionized its use. This minimally invasive technique requires accurate implantation of depth electrodes using stereotactic methodology and has been increasingly used to identify epileptogenic foci (zones) as part of the epilepsy surgery workup in patients with medically refractory epilepsy.3–12

SEEG has a well-established safety, accuracy, and efficacy profile in both adult and pediatric populations and permits bilateral, deep, and multilobar investigations while avoiding large craniotomies.2,7,12,13 Therefore, it offers an attractive less invasive alternative to subdural grid and strip electrode implantation for epilepsy focus localization for subsequent resective surgical planning.2

In the last 2 decades, the use of SEEG has become more widespread mainly because of advancements in intraoperative image guidance, surgical robotics, and computer-based surgical planning. Nowadays, SEEG can be performed on a frame-based or frameless basis, using stereotactic instruments or a neurosurgical robot.1 Robot-assistance technology has greatly enhanced the efficiency and feasibility of SEEG without sacrificing safety or precision7,14 and is therefore gaining popularity.3

Despite advances in epilepsy surgery over the last few decades, SEEG complications do still occur and little is known regarding their risk factors, especially in children. In our department, we started using SEEG in 2014, and since December 2016 we have routinely performed SEEG procedures using the neuromate robotic system (Renishaw plc). The purpose of this study was to explore the potential effects of patient-specific and surgery-related variables on the safety of pediatric SEEG, focusing on the surgical complications of the procedure in order to suggest ways to minimize them. We also aimed to determine whether the use of robotic assistance was associated with a change in practice, surgical parameters, and clinical outcomes, in particular as related to seizure outcome and complications.

Methods

We retrospectively analyzed all SEEG cases performed in our department between December 5, 2014, and March 6, 2020. The Leksell Stereotactic System (Elekta AB) was used in all implantations. All patients had preoperative magnetic resonance imaging (MRI) studies, intraoperative stereotactic computed tomography (CT) scans, and postoperative CT scans.

Surgical Technique

Electrode implantations were planned using volumetric T1-weighted MRI with contrast. The first 2 cases were planned on the StealthStation S7 (Medtronic); thereafter, all cases were planned using the neuroinspire software (Renishaw plc). During planning, no blood vessel was within a safety zone 5 mm in diameter placed around each planned electrode tract.

For every case, after inducing anesthesia, a Leksell Coordinate Frame G (Elekta AB) was applied. The child was then transferred to the CT scanner, and a volumetric CT scan was obtained with the Leksell fiducial box attached. The CT scan was then fused onto the planning MRI scan on neuroinspire or StealthStation S7 (first 2 cases only) and an output was obtained, either Leksell coordinates (i.e., X, Y, Z, arc angle, and ring angle) or output to drive the Renishaw robot. When using the Leksell Stereotactic Arc (Elekta AB) to implant electrodes, the arc was used in the conventional coronal plane. A reference marker was placed on the forehead of the child (usually an electrocardiogram marker) prior to the CT scanning and used to confirm the accuracy of the system before electrode implantation.

A volumetric CT scan was obtained in the first 24 hours after implantation, usually within 3 hours, to assess for any complications. This scan was then fused onto the preoperative scans on neuroinspire, and the accuracy of each electrode implantation was assessed by measuring the distance between the actual and planned electrode at the entry and target points in millimeters. Electrode contacts in gray matter were selected for recording.

Spencer Probe depth electrodes (Ad-Tech Medical Instrument Corp.) were used in the first 11 electrode implantations; thereafter, the MICRODEEP depth electrodes (DIXI Medical) were used in the remaining 53 implantations. The dura mater was bluntly perforated when using the Spencer electrodes; when using the DIXI electrodes, the dura was penetrated with the monopolar diathermy probe supplied by the company by setting its depth to 3 mm beyond the inner table of the skull.

All electrodes were secured in place with the guiding bolts supplied: a minimum skull thickness of 2 mm was required for adequate fixation. All post-SEEG surgeries were open resective surgeries based on SEEG and imaging findings.

Methodology

For each case, we studied the demographic and surgical variables. Demographic variables were age and gender. Surgical variables were the following: laterality of implants (unilateral or bilateral), side of implantation (left or right), number of implanted electrodes (side based and total), and duration of recording (from the time of insertion until explantation of electrodes). In patients with surgery-related complications, the nature of these events was noted, as well as their cause (where identifiable), severity, and management. We also studied clinical outcomes of the first 32 patients (16 non–robot-assisted, 16 robot-assisted), of whom 23 proceeded to further resective surgery. Seizure outcome was classified according to the Engel Seizure Outcome Classification.51

Statistical Analysis

Studied variables were assessed for statistically significant differences between groups with respect to gender (boys vs girls), age (< 10 years vs ≥ 10 years), laterality of implants (unilateral vs bilateral), side of implantation (right vs left), total number of implanted electrodes (< 10 electrodes vs ≥ 10 electrodes), duration of recording (≤ 5 days vs > 5 days), use of the neuromate robot (yes/no), and surgical complications (yes/no). Normally distributed variables were expressed as mean ± standard deviation. The Student t-test was used for the comparison of means between two groups. The chi-square test was used for categorical variables. Pearson’s correlation coefficient (r) was used to explore the association between two continuous variables. The Mann-Whitney U-test was used for nonparametric data. Cox’s F-test was used to compare two survival distributions. A p value < 0.05 was considered statistically significant.

Results

Sixty-three children had undergone 64 implantations, recordings, and explantations of SEEG electrodes during the study period. The cohort included 24 boys and 39 girls, 4–18 years of age. The first 16 cases were performed without robot assistance. From the 17th case onward, the neuromate robot was used (48 cases). Table 1 shows the characteristics of our cohort based on the studied variables.

TABLE 1.

Summary of characteristics in 64 cases in which SEEG surgery was performed

CharacteristicNo. of Cases
Age
 <10 yrs16
 ≥10 yrs48
Gender
 Boys25
 Girls39
Laterality of implants
 Unilat48
 Bilat16
Side of implantation*
 Rt30
 Lt18
No. of electrodes
 <1020
 ≥1044
Duration of recording
 ≤5 days29
 >5 days35
Robot assistance
 Yes48
 No16
Complications
 Yes4
 No60

Cases with unilateral implantation.

Demographic Variables

Age

The mean patient age was 12.2 years. Three-quarters of the patients were older than 10 years. Between the groups of children aged < 10 and ≥ 10 years, there was no difference in gender, laterality of implants, side of implantation, number of electrodes, and duration of recording. The complication rate was not affected by age: 5% for ages < 10 years and 6.3% for ages ≥ 10 years.

Gender

There was a slight female preponderance in our series (60.9%). Interestingly, boys in the series were significantly older than the girls (14.1 vs 11.1 years, t = 3.46, p < 0.01). Moreover, the complication rate was higher for boys than for girls (8.0% vs 5.1%, p > 0.1).

Surgical Variables

Laterality of Implants

One-quarter of the patients received bilateral implants (Fig. 1). There was no difference in the studied variables (i.e., age, gender, side of implantation, number of electrodes, and duration of recording) between uni- and bilateral implantation groups. The complication rate was the same (6.3%) for children with unilateral implants and those with bilateral implants.

FIG. 1.
FIG. 1.

Postoperative CT scanogram obtained in an 11-year-old girl who had undergone robot-assisted SEEG electrode implantation (10 in the right cerebral hemisphere and 4 in the left). Scalp EEG electrodes are also visible.

Side of Implantation

Among patients with unilateral SEEG electrodes, there was no side-dependent difference in the studied variables (i.e., age, gender, number of electrodes, and duration of recording). The majority (62.5%) of them had right-hemisphere implantations, and the complication rate was higher for the patients with left-sided electrodes (11.1% vs 3.3%, χ2 = 1.162, p = 0.281), although the difference between the two was not statistically significant.

Number of Electrodes

A total of 726 SEEG electrodes were implanted. The mean number of electrodes per implantation was 11.3, ranging between 3 and 16. We found a positive correlation (r = 0.296, p < 0.05) between the number of electrodes and the duration of recording. There was no difference in the studied variables (i.e., age, gender, laterality of implantation, and side of implantation) as relates to the number of electrodes. The complication rate was not significantly affected by the number of electrodes (5% for < 10 implants and 6.8% for ≥ 10 implants).

Duration of Recording

The mean duration of recording was 5.8 days, ranging between 1 and 12 days. We found no difference in the studied variables (i.e., age, gender, laterality of implantation, and side of implantation) as relates to the duration of recording. The complication rate was not affected by the duration of recording (6.9% for < 5 days and 5.7% for ≥ 5 days of recording).

Robot Assistance

The neuromate robot was used in the majority of our cases (75%). The mean number of electrodes was significantly higher in the robot group than the nonrobot group (12.6 vs 7.6 electrodes, t = 6.76, p < 0.0001). The complication rate was the same (6.3%) in the two groups. Moreover, there was no difference between the two groups in terms of laterality of implants, duration of recording, and proportion of patients proceeding to further epilepsy surgery.

Electrode Implantation Accuracy

As expected, the entry and target point errors had a positively skewed distribution that could not be normalized with the traditional transformations (log, cube root). We performed inferential statistics using a nonparametric test (Mann-Whitney U-test) with an alpha value of 0.05. The mean target error for the robot-assisted group was significantly lower than the Leksell arc for the non–robot-assisted group (mean 1.51 vs 2.98 mm, z = 2.88, p < 0.001). The mean entry errors were 0.56 and 1.56 mm, respectively (i.e., no significant difference).

Epilepsy Surgery Outcome

The first 16 children underwent non–robot-assisted SEEG surgery. Their seizure outcomes were compared to those of the first 16 children who had undergone robot-assisted surgery (Table 2). Twelve (75%) of the 16 children in the nonrobot group and 11 (69%) of the 16 in the robot-assisted group went on to have resective epilepsy surgery. The mean follow-up duration for these two groups was 26 months.

TABLE 2.

Characteristics and seizure outcome in the first 32 patients undergoing SEEG investigations

Case No.Age (yrs)*BilatRobot AssistanceNo. of ElectrodesResective SurgeryHistologyEngel Class at 12 MosComplication
114NoNo3Rt frontalFCDIbIVB
215NoNo5Rt frontalFCDIbIVB
317YesNo6Rt temporalNondiagnosticIA
417NoNo8Rt posteromedial frontal resectionGliosisIVB
515NoNo7Lt frontal lobectomyHyaline astrocytic inclusionsIA
65NoNo5Rt frontal lobectomyTuberous sclerosisIVB
716NoNo6Lt occipital & partial parietal resectionGliosisIIIC
89YesNo9Rt temporal lobectomyFCDIIaIA
912NoNo7Rt pst frontal resectionNormalIA
1012NoNo7
1112NoNo5Extradural hematoma
1215YesNo9Lt pst medial frontal resectionFCDIIbIA
1314NoNo11Rt pst frontal resectionFCD (unclassifiable)IVB
147NoNo7
1518NoNo7
166NoNo8Rt temporal lobectomy & hippocampectomyHippocampal sclerosisII
1712YesYes14
184NoYes11Rt frontal lobectomyFCDIbIA
1915NoYes11Rt temporal lobectomy & hippocampectomyNondiagnosticIA
2017NoYes15
2114NoYes15Rt pst frontal resectionNormalIA
2211YesYes14Resection of rt medial frontal focusFCDIIaIA
2314YesYes16
2414NoYes14Lt temporal lobectomy & hippocampectomyHippocampal sclerosisIVB
2510NoYes9Lt pst frontal & anterior insular resectionHyaline astrocytic inclusionsIA
2618YesYes13Lt temporal lobectomy & hippocampectomyHippocampal sclerosisIIICDisplaced guiding bolt, fractured & retained electrode
2718NoYes7Lt occipital lobectomyGlioneuronal heterotopiaIA
287NoYes10
2910NoYes11
309YesYes7Lt occipital lobectomyHypoglycemic scarringIA
3110NoYes10Lt temporal lobectomy & hippocampectomyHippocampal sclerosisIA
3218NoYes10Rt pst frontal resectionNormalIA

FCD = focal cortical dysplasia; pst = posterior.

At SEEG implantation.

The mean age of the nonrobot group was 12.9 years and that of the robot group was 12.8 years. In terms of surgical location, the nonrobot group had 8 (67%) frontal, 3 (25%) temporal, and 1 (8%) occipital resection; the robot group had 5 (45%) frontal, 4 (36%) temporal, and 2 (18%) occipital resections. The left-to-right hemispheric surgery was 3:9 in the nonrobot group and 6:5 in the robot group.

The robot group obtained an Engel class IA seizure outcome at 12 months postoperation more frequently than the nonrobot group (56% [9/16] vs 31% [5/16], χ2 = 2.032, p = 0.154). Of those patients who underwent further epilepsy surgery, the proportion obtaining seizure freedom (i.e., Engel class IA) at 12 months was significantly higher in the robot group than in the nonrobot group (82% [9/11] vs 42% [5/12], χ2 = 3.885, p = 0.049). Similarly, the proportion of children obtaining better seizure control (i.e., Engel class I–III) at 12 months was also higher in the robot group (91% [10/11] vs 58% [7/12], χ2 = 3.159, p = 0.076). Comparing the survival distributions of the two cohorts using Kaplan-Meier analysis, we found the robot group had a higher seizure-freedom rate at 30 months’ follow-up (7/11 [64%] vs 2/12 [17%], Cox’s F-test: p = 0.063; Fig. 2). The mean age was similar in the seizure-free and non–seizure-free children (12.7 vs 12.1 years).

FIG. 2.
FIG. 2.

Kaplan-Meier curve demonstrating the seizure-free rates (survival) of the 12 nonrobot and 11 robot-assisted cases that underwent resective surgery following SEEG investigation.

Complications

The overall complication rate in our series was 6.3% (4/64). Robot assistance had been used in 3 of the 4 cases. Three of the cases were left implantations, and 1 case was a right implantation. The mean age of the patients with complications was 13.8 years. Half of these patients (2/4) required surgery to treat the complication (cases 11 and 26; Table 2). The patient in case 11 demonstrated an asymptomatic left frontal extradural hematoma on postoperative CT and required a craniotomy for evacuation (Fig. 3). For this patient, and the first 10 patients treated in our department, dural perforation was performed using a blunt stylet. After case 11, the technique and instrument for dural perforation was changed to a sharp stylet with concurrent monopolar diathermy. Also, the patient in this case was taking sodium valproate at the time of implantation, which may have been a contributing factor; however, 4 other children in our series were also on this antiepileptic medication and had no hemorrhagic events. In case 26, a right temporal guiding bolt displacement and an associated fractured and retained electrode were apparent on the postoperative day 1 CT—and therefore were likely to have occurred immediately after the implantation procedure—and were exacerbated by head bandaging (Fig. 4). This necessitated an additional burr hole for retrieval after explantation of the other electrodes. The retained electrode was the only right-sided “check” implantation in a predominantly left-hemisphere implantation of 12 electrodes. Two other patients developed transient neurological deficits including one right-handed patient with dysphasia.

FIG. 3.
FIG. 3.

Case 11. Postoperative day 1 axial CT scan obtained in a patient who had undergone implantation of left SEEG electrodes, showing a left frontal extradural hematoma associated with an overlying burr hole for electrode insertion.

FIG. 4.
FIG. 4.

Axial CT scan (A) and inferior view of the 3D reconstruction (B) demonstrating a fractured right anterior hippocampus electrode (asterisks) and detached guiding bolt (white arrowheads). Note the discontinuation of the electrode lead between the loose bolt and skull. Figure is available in color online only.

Finally, although it was not considered a surgical complication, it should be noted that, 2 days after complete withdrawal of his antiepileptic medications (postoperative day 5), a 16-year-old boy with 15 right-sided electrodes had status epilepticus with respiratory arrest on our neurosurgery ward. After resuscitation, his breathing returned spontaneously, without intubation or intensive care, and he was discharged home 5 days later. He went on to have resective surgery.

All SEEG complications in this study were either transient or treatable, and no patient experienced permanent sequelae due to a surgical complication. We identified no patient-related or other surgical risk factors relating to the complications.

Discussion

In the last decade, SEEG has been increasingly used as the invasive EEG modality of choice for presurgical evaluation of epilepsy patients. This trend was mirrored by better insight into seizure semiology and network,14–19 technological advancement for accurate and efficient electrode placement, further appreciation of the electrophysiological data (e.g., stimulation mapping), improved surgical technique for resection of deep epileptogenic lesions, and the possibility of radiofrequency thermocoagulation.20 The increased application of SEEG is based on its safety profile and efficacy in identifying and locating an epileptogenic focus to guide resective surgery.

Table 3 summarizes all reports of epilepsy surgery outcomes in children investigated via SEEG with at least 1 year of follow-up. Robot assistance was used in most of them. Only 10 of 24 reports focused exclusively on children (age ≤ 18 years), whereas the rest included both adults and children. The largest pediatric SEEG cohort so far was included in Cardinale et al.’s report on patients of all ages (185 children, robot-assisted surgery).4 The largest exclusively pediatric SEEG report came from Taussig et al. (65 children, non–robot-assisted surgery).21 Children have cranial and cerebral anatomy and physiology that are different from those in adults. Their perioperative care is different as well and can be challenging because of their limited understanding and compliance.22 Therefore, it is important to ascertain the pediatric-specific SEEG safety and efficacy profile. In this study, the largest single-center, exclusively pediatric SEEG series to include robot assistance so far, we aimed to assess the safety of SEEG in children and compare the seizure outcomes of pediatric patients undergoing robot-assisted and non–robot-assisted SEEG evaluation.

TABLE 3.

Epilepsy surgery outcome in children investigated via SEEG with ≥ 1 year of follow-up

Authors & YearCountryNo. of SEEG PatientsPediatric-Only StudyEngel Class IA*SEEG & ES PatientsEngel Class I–IIIRobot Assistance
Cossu et al., 200535Italy211No44.1%17478.2%Yes§
Cossu et al., 20055 Italy35Yes42.9%3574.3%Yes§
Cossu et al., 201234 Italy15Yes40%1361.5%Yes
Gonzalez-Martinez et al., 201332 US100No33%75No
Dorfmüller et al., 201431 France19Yes84.2%19100%Yes
Dylgjeri et al., 201417 France10Yes70%10100%Yes
Gonzalez-Martinez & Lachhwani, 20142 US30No33.3%1883.3%No
Gonzalez-Martinez et al., 201436 US122No45.9%90No
Liava et al., 201437 Italy24Yes75%24No
Serletis et al., 201438 US200No30.5%134Yes§
Taussig et al., 201421 France65Yes52.3%5182.4%No
González-Martínez et al., 20166 US100No45%6892.6%Yes
Yang et al., 201739 China48No52.1%4283.3%No
Abel et al., 20183 France18Yes27.8%1283.3%No
Abel et al., 20183 France17Yes23.5%1266.7%Yes
Alomar et al., 201815 US135No3.7%1794.1%Yes
Cobourn et al., 201827 US4No75%4100%**Yes
Goldstein et al., 201813 US25Yes32%18††77.8%Yes§
Ho et al., 20187 US20No30%12‡‡75%Yes
Cardinale et al., 20194 Italy713No25.8%470Yes§
McGovern et al., 201822 US57Yes17.5%4271%Yes
Toledano et al., 201940 Spain71No45.1%61No
Kappen et al., 202018 UK53No30.2%2680.8%Yes
Méreaux et al., 202020 France46No50%4190.2%Yes§

ES = epilepsy surgery; UK = United Kingdom; US = United States.

Of those who underwent SEEG.

Of those who underwent SEEG and epilepsy surgery.

Engel class I.

In a proportion of patients.

Insular SEEG.

At 9.3 months’ mean follow-up.

Six or more months’ follow-up: 15 patients.

Those who had epilepsy surgery and at least 3 months’ follow-up.

Preponderance of, and Younger Age in, Females Undergoing SEEG Evaluation

The ratio of girls to boys who had undergone SEEG investigation was 1.5:1. Furthermore, the observation that girls were on average 3 years younger than boys (age 11.1 vs 14.1 years, p < 0.01) could be explained by Taylor’s theory.23 He suggested that cerebral maturation is slower in boys; therefore, the time frame for a potential epileptogenic insult, which is more likely to affect a brain still undergoing maturation, is longer in boys.23

The mean age in our series was 12.2 years. In the literature, the mean age of patients in pediatric SEEG series ranges between 8.2 and 12 years.5,21,22 Taussig et al.21 compared epilepsy surgery outcome between two pediatric SEEG groups based on age and found that younger children (age < 5 years) had better outcomes than the children older than 5 years of age (Engel class I 79% vs 59%, respectively) at a mean 2-year follow-up.21

Hemispheres Investigated With SEEG

Οur experience of 25% bilateral SEEG investigations is comparable to findings in previous pediatric SEEG series (7%–56%).3,13,24,25 The 62.5% frequency of right-sided SEEG implantations is also within the range described in the literature (18.8%–64.3%, among unilaterally implanted patients).3,24,25

Postoperative Care and Recording Duration

Kim et al.26 reported an average 1.4 days of intensive care unit (ICU) stay. At our institution, all children were transferred back to a dedicated telemetry bed space on the neurosurgery ward. The children were nursed by neurosurgically trained staff. All children had “rescue” antiepileptic medication prescribed in case of prolonged seizure following medication reduction. None of the children were admitted to the ICU during hospitalization.

The mean number of implants per patient in our series was 11.3, which is in line with the 6–14 electrodes described in published series.3,5,7,13,21,22,24,25,27,28 The mean duration and range of recording in our patients were 5.8 and 1–12 days, respectively, values again comparable with those in the pediatric SEEG literature (mean duration 5.4–8 days,13,21,26,27 range 1–21 days5).

The fact that a greater duration of recording was not associated with more complications in our series underlines the safety of the recording period. It also suggests that such adverse events are mostly related to the implantation, not the recording period. The positive statistically significant correlation between the number of electrodes and the duration of recording could be explained by the observation that more electrodes are used in difficult cases in which a longer recording time and longer stimulation mapping were required.

Higher Complication Rate in Left-Sided Implantation

Children with left-sided electrodes had a higher complication rate than those with right-sided electrodes (11.1% vs 3.3%). During the recording period, regular neurological assessment included the Glasgow Coma Scale (which includes verbal response and therefore speech), limb power, pupillary light response, and any concerns raised by the children or their families. Therefore, it is interesting that one of the three left-sided complications was dysphasia. In this particular case, the child’s left hemisphere was dominant. The same cerebral disturbance to the right hemisphere homotopic to the left-hemisphere language network would not have caused speech impairment. Thus, dominant-hemisphere SEEG surgery may indeed carry a higher overall risk of postoperative neurological impairment.

Children with left-sided electrodes had a higher complication rate than those with right-sided electrodes (11.1% vs 3.3%). During the recording period, regular neurological assessment included the Glasgow Coma Scale (which includes verbal response and therefore speech), limb power, pupillary light response, and any concerns raised by the children or their families. Therefore, it is interesting that one of the three left-sided complications was dysphasia. In this particular case, the child’s left hemisphere was dominant. The same cerebral disturbance to the right hemisphere homotopic to the left-hemisphere language network would not have caused speech impairment. Thus, dominant-hemisphere SEEG surgery may indeed carry a higher overall risk of postoperative neurological impairment.

Robot Assistance

In our study, the mean number of electrodes per patient in the robot-assisted group was 12.6, significantly higher than the nonrobot mean of 7.6 (p < 0.0001). We started using more electrodes mainly because of the robot-related advantages, namely improved accuracy and safety, decreased surgical time, and greater possibilities for trajectory angles. In comparison, the mean number of implanted SEEG electrodes in the literature is 6–12 for robot-assisted cases5,7,13,21,22,24,27,28 and for non–robot-assisted cases, 7–13 electrodes.3,25 Bourdillon et al.1 reported a significantly higher number of implanted electrodes per patient in the Talairach-approach group than in the robot-assisted group (mean 12.6 vs 11.3 electrodes, p = 0.008). It should be noted that, although these authors used the same robotic system as our team, their patient population was pediatric and adult combined, with a mean age of 30 years in the robot-assisted group.

Robot-assisted techniques are considered to facilitate more electrode trajectory possibilities3 and to increase implantation’s accuracy in SEEG.1 In comparison to our experience, Candela-Cantó et al., who used the neuromate robot in 14 children, reported 7 intraoperative technical issues, mainly electrode collisions, which occurred in 4 children.29 Higher in vivo accuracy of SEEG electrode positioning is obviously crucial, as it can lead to more successful epileptogenic zone identification, more precise resective surgery, and thus better seizure outcomes and fewer complications.11 In robot-assisted SEEG patients, a median target point error of 1.7–2.7 mm has been reported,6,9,14,30 compared to a 2.9-mm median target point deviation in non–robot-assisted cases.11

An often ignored but important factor affecting accuracy is the maintenance of equipment. The neuromate robot, for example, requires calibration every 3 months, and the Leksell stereotactic frame requires annual maintenance that includes an accuracy check.

Finally, despite a higher number of electrodes in the robot-assisted group of our study, the complication rate was not higher. In other words, the robot allowed denser SEEG without increasing the risks.

Epilepsy Surgery Outcome

The use of a robot did not change the proportion of children proceeding to resective surgery. The seizure outcome, in terms of the proportion of patients attaining an Engel class IA outcome or Engel class I–III outcome, was better in the robot-assisted group. These two findings suggest that both robot-assisted and nonrobot SEEG adequately localized the epileptogenic zone, but the robot-assisted technique defined its extent and therefore the resection margin more accurately.31 One confounding factor was switching the technique from non–robot-assisted to robot-assisted surgery at our 17th case. This coincided with the learning curve of interpreting SEEG results, which may be involved in the improved outcome of the robot group.

In the literature, the proportion of SEEG-investigated children who became seizure free (Engel class IA) at 12 months after epilepsy surgery ranged widely between 17.5% and 84.2% (non–robot-assisted surgery: 27.8%–75%, robot-assisted surgery: 17.5–84.2%; Table 3). Similarly, among children who proceeded to epilepsy surgery after SEEG investigation, the proportion of patients who obtained at least worthwhile seizure improvement (Engel class I–III) ranged between 61.5% and 100% (non–robot-assisted surgery: 82.4–83.3%, robot-assisted surgery: 61.5%–100%). The respective proportion of Engel class I–III outcomes in our robot-assisted group was 90.9%, above the upper limit of the range of published data from exclusively pediatric series in which only non–robot-assisted cases were included. However, the heterogeneity of the study samples, including the difference in the primary etiology of epilepsy, must be taken into account.

Predictive Factors for Seizure Freedom

In their pediatric SEEG series, Abel et al.3 found no effect of robot assistance on the rate of resective epilepsy surgery, as was shown in our study. While they found that robot assistance had no effect on the seizure-freedom rate, the robot-assisted group in our study had a better seizure-freedom outcome. Other factors affecting seizure freedom in patients undergoing SEEG have been identified as well.4,22,32 In the pediatric series of McGovern et al.,22 resective epilepsy surgery, older age, and shorter SEEG-related hospital stay were associated with seizure freedom. In children who underwent resective surgery, older age was the only significant factor associated with seizure freedom. In our cohort, the mean age was similar in the seizure-free and non–seizure-free children.

Finally, it has been shown that the presence of pathological abnormalities and type of primary etiology are significant predictors of seizure freedom in patients who undergo SEEG plus epilepsy surgery.4,32 Gonzalez-Martinez et al. found that an abnormal pathological finding (mainly cortical dysplasia type I and hippocampal sclerosis) was strongly associated with postoperative seizure control.32 Cardinale et al. showed that focal cortical dysplasia type II, glioneuronal tumors, balloon cells, hippocampal sclerosis, older age at epilepsy onset, and periventricular nodular heterotopia were significantly associated with seizure freedom.4

Complications

The overall SEEG surgical complication rate in our series was 6.3%. Table 4 summarizes previous reports of SEEG complication rates in children. It is generally accepted that SEEG is a well-tolerated and safe procedure with a complication rate between 0% and 14.3% in pediatric patients (non–robot-assisted procedure: 0%–5.6%, robot-assisted procedure: 0%–14.3%).5 Contrary to the higher complication rate in robot-assisted cases reported in the literature,5 robot application in our study did not increase adverse events. Abel et al. also reported no difference.3

TABLE 4.

Complication rates of SEEG in children

Authors & YearCountrySample SizeComplication Rate*Robot Assistance
Munari et al., 199441France705.7%No
Guenot et al., 200142France1005%No
Cossu et al., 200535Italy2113.3%Yes
Cossu et al., 20055Italy352.9%Yes
Cossu et al., 201234Italy156.7%Yes
Cardinale et al., 201330Italy5002.6%Yes
Gonzalez-Martinez et al., 201332US1001%No
Dorfmüller et al., 201431France190%Yes
Dylgjeri et al., 201417France100%Yes
Gonzalez-Martinez & Lachhwani, 20142US300%No
Gonzalez-Martinez et al., 201436US1222.5%No
Serletis et al., 201438US2004.5%Yes
Taussig et al., 201421France650%No
Mathon et al., 201533France1573.8%No
González-Martínez et al., 20166US1001%Yes
Bourdillon et al., 201716France5253.6%Yes
De Benedictis et al., 201728Italy360%Yes
Ollivier et al., 20179France669.1%Yes
van der Loo et al., 201711The Netherlands718.5%No
Yang et al., 201739China488.3%No
Zhang et al., 201743China440%No
Abel et al., 20183France185.6%No
Abel et al., 20183France175.9%Yes
Alomar et al., 201815US1352.2%Yes
Bourdillon et al., 20181France502%No
Bourdillon et al., 20181France502%Yes
Budke et al., 201825Spain150%No
Candela-Cantó et al., 201829Spain1414.3%Yes
Cobourn et al., 201827US40%Yes
Dewan et al., 201844US150%No
Goldstein et al., 201813US2512%Yes
Ho et al., 20187US200%Yes
Salado et al., 201819France998%No
Cardinale et al., 20194Italy7131.8%Yes
McGovern et al., 201822US573.5%Yes
McGovern et al., 201924US5492.2%Yes
Tandon et al., 201945US1160%Yes
Toledano et al., 201940Spain714.2%No
Willems et al., 201912Germany1816.7%§Yes
Alexander et al., 202046US20%Yes
Bottan et al., 202014Canada410%Yes
Joswig et al., 202047Canada1452.1%Yes
Kappen et al., 202018UK533.8%Yes
Kim et al., 202026US380%Yes
Méreaux et al., 202020France468.7%Yes

Asymptomatic imaging findings that required no treatment are not included.

Sample included adults.

In a proportion of patients.

Transient headache noticed in 55.6% of those patients was not considered a complication.

Overall, 3.1% of our cases required further surgery because of a surgical complication and 1.6% underwent craniotomy. All complications were treatable, and no patient developed permanent sequelae. We attribute the transient neurological deficits to transient dysfunction of the implanted hemisphere, probably due to irritation by the implants. Neither misplaced electrodes nor hemorrhages were found on the postoperative CT scans of these patients. The displaced guiding bolt and associated fractured and retained electrode were apparent on the postoperative day 1 CT and therefore were likely to have occurred immediately after the implantation procedure. It was the only right-sided electrode as a check in a patient with otherwise left-sided implantation. While the padding and multiple electrodes reduced and spread the pressure among the left-sided bolts, the single, proud right-sided bolt was more prone to displacement, leading to the subsequent electrode fracture. Therefore, padding on the side of fewer electrodes is more, if not as important as that on the contralateral side.

While it is usually recommended to perform postoperative imaging within 24 hours after implantation, complications in asymptomatic SEEG patients are likely to be underreported because of the lack of routine imaging after explantation.12

It should be noted that having seizures itself can increase the risk of other complications, particularly during the recording period. Cardinale et al. reported a patient with status epilepticus who developed an intracerebral hematoma after explantation of electrodes.4

Table 5 summarizes the reported SEEG complications and their frequencies. Not all of them are clinically significant, and most of them are uncommon. Transient headache, if considered as a complication at all, has been reported as the commonest side effect of the procedure.12 Intracranial hemorrhage, in its various forms, constitutes a major component (25% of our complications) of the complications list.

TABLE 5.

Complications of SEEG and their frequencies1,3–8,10–13,15–22,24,25,27–30,32,33,35,36,38–42,44,45,47–50

ComplicationFrequency
Transient headache0–55.6%
Asymptomatic ICH/SAH0–28.6%
Relevant leukocytosis0–16.7%
Asymptomatic local brain edema0–11.1%
Brain infection0–8%
Aseptic meningitis0–7.1%
Asymptomatic SDH0–6.7%
Transient neurological deficit0–5.9%
Symptomatic SDH0–5.9%
Material failure (retained/broken/deflected/pulled-out electrode, broken/migrated fixation screw, broken drill)0–5.6%
Transient low-grade fever0–5.6%
Symptomatic ICH0–5.6%
Noncerebral infection (wound infection, pneumonia, UTI, Clostridioides difficile gastroenteritis*)0–5.6%
Vein thrombosis (extracranial)0–4.3%
Temporal bone fracture0–3%
Pulmonary embolism0–2.9%
Permanent neurological deficit0–2.8%
Symptomatic local brain edema0–2.8%
Death0–2.2%
Acute pneumocephalus0–2%
EDH requiring evacuation0–1.4%
Cardiac complications/cardiac arrest0–0.7%
Vasospasm0–0.6%
Shock during anesthesia0–0.6%
Hydrocephalus (posthemorrhagic)0–0.5%
CSF leak0–0.4%
Hyponatremia0–0.2%
Internal carotid artery dissection0–0.2%
Allergic reaction (to iodine contrast medium)0–0.2%
Psychotic attack0–0.2%
Atelectasis0–0.1%
Leg compartment syndrome0–0.1%

CSF = cerebrospinal fluid; EDH = extradural hematoma; ICH = intracerebral hematoma; SAH = subarachnoid hemorrhage; SDH = subdural hematoma; UTI = urinary tract infection.

Also known as Clostridium difficile gastroenteritis.

MRI is the gold-standard imaging for SEEG targeting and trajectory calculations, and contrast-enhanced scans are necessary to minimize the perioperative bleeding risk. Each electrode trajectory must be planned carefully to avoid blood vessels (and conflicts between electrodes).

Male sex, increased number of electrodes, and increasing age have been associated with a greater risk of postimplantation hemorrhage.31,48 In our study, the mean age of patients with complications was similar to the cohort average. González-Martínez et al. reported that all intracranial hematomas (4%) were topographically related to the entry point of frontal and parietal electrodes.6 Mathon et al. found that overall and hemorrhagic SEEG complications were significantly associated with MRI-negative epilepsy cases.33

Cossu et al.34 has reported the only pediatric death in their cohort of mainly unilateral implantations in 15 infants and very young children (mean age 34.1 months), with all surgeries performed using the neuromate robot. Their single death (6.7%) was attributable to massive brain edema and severe hyponatremia of undetermined cause. In view of the particular risks of intracranial surgery in this specific age group, the authors thoughtfully recommended reserving SEEG evaluations for infants with realistic chances of benefiting from surgery. Finally, we note that some complications are clinically silent (Table 5). For example, Willems et al. reported a C-reactive protein peak 2 days postoperatively (mean 1.5 mg/dl, range 0–5.3 mg/dl, reference < 0.5 mg/dl).12 In our opinion, this is the normal postoperative physiological response. Our unit does not routinely perform postoperative inflammatory marker or neutrophil count tests.

Conclusions

We present the largest single-center, exclusively pediatric SEEG series that includes robot assistance to date. SEEG is safe in children, and its complications, which are more frequent with left-sided implants, are uncommon and usually treatable. The use of robot assistance in our series enabled more SEEG electrodes to be implanted without increasing surgical complications and was associated with an improved epilepsy surgery outcome, probably because of more accurate localization of the epileptogenic foci. Robot assistance also improved the epilepsy surgery outcome compared to those in non–robot-assisted cases.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Mavridis. Acquisition of data: Mavridis, Seri. Analysis and interpretation of data: Mavridis, Lo. Drafting the article: Mavridis. Critically revising the article: Mavridis, Lo, Seri, Walsh. Approved the final version of the manuscript on behalf of all authors: Mavridis. Statistical analysis: Mavridis, Lo. Administrative/technical/material support: all authors. Study supervision: Lo, Walsh.

Supplemental Information

Abstract Presentations

Abstracts detailing some of the findings of this work have been accepted for oral presentation at the 48th Annual Meeting of the International Society for Pediatric Neurosurgery to be held in Singapore on December 6–10, 2022.

References

  • 1

    Bourdillon P, Châtillon CE, Moles A, et al. Effective accuracy of stereoelectroencephalography: robotic 3D versus Talairach orthogonal approaches. J Neurosurg. 2018;131(6):19381946.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Gonzalez-Martinez J, Lachhwani D. Stereoelectroencephalography in children with cortical dysplasia: technique and results. Childs Nerv Syst. 2014;30(11):18531857.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Abel TJ, Varela Osorio R, Amorim-Leite R, et al. Frameless robot-assisted stereoelectroencephalography in children: technical aspects and comparison with Talairach frame technique. J Neurosurg Pediatr. 2018;22(1):3746.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Cardinale F, Rizzi M, Vignati E, et al. Stereoelectroencephalography: retrospective analysis of 742 procedures in a single centre. Brain. 2019;142(9):26882704.

  • 5

    Cossu M, Cardinale F, Colombo N, et al. Stereoelectroencephalography in the presurgical evaluation of children with drug-resistant focal epilepsy. J Neurosurg. 2005;103(4)(suppl):333343.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    González-Martínez J, Bulacio J, Thompson S, et al. Technique, results, and complications related to robot-assisted stereoelectroencephalography. Neurosurgery. 2016;78(2):169180.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Ho AL, Muftuoglu Y, Pendharkar AV, et al. Robot-guided pediatric stereoelectroencephalography: single-institution experience. J Neurosurg Pediatr. 2018;22(5):489496.

  • 8

    Mullin JP, Shriver M, Alomar S, et al. Is SEEG safe? A systematic review and meta-analysis of stereo-electroencephalography-related complications. Epilepsia. 2016;57(3):386401.

  • 9

    Ollivier I, Behr C, Cebula H, et al. Efficacy and safety in frameless robot-assisted stereo-electroencephalography (SEEG) for drug-resistant epilepsy. Neurochirurgie. 2017;63(4):286290.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Scorza D, De Momi E, Plaino L, et al. Retrospective evaluation and SEEG trajectory analysis for interactive multi-trajectory planner assistant. Int J CARS. 2017;12(10):17271738.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    van der Loo LE, Schijns OEMG, Hoogland G, et al. Methodology, outcome, safety and in vivo accuracy in traditional frame-based stereoelectroencephalography. Acta Neurochir (Wien). 2017;159(9):17331746.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Willems LM, Reif PS, Spyrantis A, et al. Invasive EEG-electrodes in presurgical evaluation of epilepsies: Systematic analysis of implantation-, video-EEG-monitoring- and explantation-related complications, and review of literature. Epilepsy Behav. 2019;91:3037.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Goldstein HE, Youngerman BE, Shao B, et al. Safety and efficacy of stereoelectroencephalography in pediatric focal epilepsy: a single-center experience. J Neurosurg Pediatr. 2018;22(4):444452.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Bottan JS, Rubino PA, Lau JC, et al. Robot-assisted insular depth electrode implantation through oblique trajectories: 3-dimensional anatomical nuances, technique, accuracy, and safety. Oper Neurosurg (Hagerstown). 2020;18(3):278283.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Alomar S, Mullin JP, Smithason S, Gonzalez-Martinez J. Indications, technique, and safety profile of insular stereoelectroencephalography electrode implantation in medically intractable epilepsy. J Neurosurg. 2018;128(4):11471157.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Bourdillon P, Ryvlin P, Isnard J, et al. Stereotactic electroencephalography is a safe procedure, including for insular implantations. World Neurosurg.2017;99:353361.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Dylgjeri S, Taussig D, Chipaux M, et al. Insular and insulo-opercular epilepsy in childhood: an SEEG study. Seizure. 2014;23(4):300308.

  • 18

    Kappen P, Eltze C, Tisdall M, et al. Stereo-EEG exploration in the insula/operculum in paediatric patients with refractory epilepsy. Seizure. 2020;78:6370.

  • 19

    Salado AL, Koessler L, De Mijolla G, et al. sEEG is a safe procedure for a comprehensive anatomic exploration of the insula: a retrospective study of 108 procedures representing 254 transopercular insular electrodes. Oper Neurosurg (Hagerstown). 2018;14(1):18.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Méreaux JL, Gilard V, Le Goff F, et al. Practice of stereoelectroencephalography (sEEG) in drug-resistant epilepsy: Retrospective series with surgery and thermocoagulation outcomes. Neurochirurgie. 2020;66(3):139143.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Taussig D, Chipaux M, Lebas A, et al. Stereo-electroencephalography (SEEG) in 65 children: an effective and safe diagnostic method for pre-surgical diagnosis, independent of age. Epileptic Disord. 2014;16(3):280295.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    McGovern RA, Knight EP, Gupta A, et al. Robot-assisted stereoelectroencephalography in children. J Neurosurg Pediatr. 2018;23(3):288296.

  • 23

    Taylor DC. Differential rates of cerebral maturation between sexes and between hemispheres. Evidence from epilepsy. Lancet. 1969;2(7612):140142.

  • 24

    McGovern RA, Ruggieri P, Bulacio J, et al. Risk analysis of hemorrhage in stereo-electroencephalography procedures. Epilepsia. 2019;60(3):571580.

  • 25

    Budke M, Avecillas-Chasin JM, Villarejo F. Implantation of depth electrodes in children using VarioGuide® frameless navigation system: technical note. Oper Neurosurg (Hagerstown). 2018;15(3):302309.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Kim LH, Parker JJ, Ho AL, et al. Postoperative outcomes following pediatric intracranial electrode monitoring: a case for stereoelectroencephalography (SEEG). Epilepsy Behav. 2020;104(pt A):106905.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Cobourn K, Fayed I, Keating RF, Oluigbo CO. Early outcomes of stereoelectroencephalography followed by MR-guided laser interstitial thermal therapy: a paradigm for minimally invasive epilepsy surgery. Neurosurg Focus. 2018;45(3):E8.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    De Benedictis A, Trezza A, Carai A, et al. Robot-assisted procedures in pediatric neurosurgery. Neurosurg Focus. 2017;42(5):E7.

  • 29

    Candela-Cantó S, Aparicio J, López JM, et al. Frameless robot-assisted stereoelectroencephalography for refractory epilepsy in pediatric patients: accuracy, usefulness, and technical issues. Acta Neurochir (Wien). 2018;160(12):24892500.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Cardinale F, Cossu M, Castana L, et al. Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures. Neurosurgery. 2013;72(3):353366.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Dorfmüller G, Ferrand-Sorbets S, Fohlen M, et al. Outcome of surgery in children with focal cortical dysplasia younger than 5 years explored by stereo-electroencephalography. Childs Nerv Syst. 2014;30(11):18751883.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Gonzalez-Martinez J, Bulacio J, Alexopoulos A, et al. Stereoelectroencephalography in the “difficult to localize” refractory focal epilepsy: early experience from a North American epilepsy center. Epilepsia. 2013;54(2):323330.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Mathon B, Clemenceau S, Hasboun D, et al. Safety profile of intracranial electrode implantation for video-EEG recordings in drug-resistant focal epilepsy. J Neurol. 2015;262(12):26992712.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Cossu M, Schiariti M, Francione S, et al. Stereoelectroencephalography in the presurgical evaluation of focal epilepsy in infancy and early childhood. J Neurosurg Pediatr. 2012;9(3):290300.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Cossu M, Cardinale F, Castana L, et al. Stereoelectroencephalography in the presurgical evaluation of focal epilepsy: a retrospective analysis of 215 procedures. Neurosurgery. 2005;57(4):706718.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Gonzalez-Martinez J, Mullin J, Vadera S, et al. Stereotactic placement of depth electrodes in medically intractable epilepsy. J Neurosurg. 2014;120(3):639644.

  • 37

    Liava A, Mai R, Tassi L, et al. Paediatric epilepsy surgery in the posterior cortex: a study of 62 cases. Epileptic Disord. 2014;16(2):141164.

  • 38

    Serletis D, Bulacio J, Bingaman W, et al. The stereotactic approach for mapping epileptic networks: a prospective study of 200 patients. J Neurosurg. 2014;121(5):12391246.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Yang M, Ma Y, Li W, et al. A retrospective analysis of stereoelectroencephalography and subdural electroencephalography for preoperative evaluation of intractable epilepsy. Stereotact Funct Neurosurg. 2017;95(1):1320.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Toledano R, Martínez-Álvarez R, Jiménez-Huete A, et al. Stereoelectroencephalography in the preoperative assessment of patients with refractory focal epilepsy: experience at an epilepsy centre. Article in Spanish. Neurologia. Published online July 20, 2019. doi:10.1016/j.nrl.2019.05.002

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Munari C, Hoffmann D, Francione S, et al. Stereo-electroencephalography methodology: advantages and limits. Acta Neurol Scand Suppl. 1994;152:5669.

  • 42

    Guenot M, Isnard J, Ryvlin P, et al. Neurophysiological monitoring for epilepsy surgery: the Talairach SEEG method. StereoElectroEncephaloGraphy. Indications, results, complications and therapeutic applications in a series of 100 consecutive cases. Stereotact Funct Neurosurg. 2001;77(1-4):2932.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Zhang G, Chen G, Meng D, et al. Stereoelectroencephalography based on the Leksell stereotactic frame and Neurotech operation planning software. Medicine (Baltimore). 2017;96(23):e7106.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Dewan MC, Shults R, Hale AT, et al. Stereotactic EEG via multiple single-path omnidirectional trajectories within a single platform: institutional experience with a novel technique. J Neurosurg. 2018;129(5):11731181.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Tandon N, Tong BA, Friedman ER, et al. Analysis of morbidity and outcomes associated with use of subdural grids vs stereoelectroencephalography in patients with intractable epilepsy. JAMA Neurol. 2019;76(6):672681.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    Alexander H, Fayed I, Oluigbo CO. Rigid cranial fixation for robot-assisted stereoelectroencephalography in toddlers: technical considerations. Oper Neurosurg (Hagerstown). 2020;18(6):614620.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47

    Joswig H, Lau JC, Abdallat M, et al. Stereoelectroencephalography versus subdural strip electrode implantations: feasibility, complications, and outcomes in 500 intracranial monitoring cases for drug-resistant epilepsy. Neurosurgery. 2020;87(1):E23E30.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48

    Narváez-Martínez Y, García S, Roldán P, et al. Stereoelectroencephalography by using O-Arm® and Vertek® passive articulated arm: technical note and experience of an epilepsy referral centre. Article in Spanish. Neurocirugia (Astur). 2016;27(6):277284.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49

    Sacino MF, Huang SS, Schreiber J, et al. Is the use of stereotactic electroencephalography safe and effective in children? A meta-analysis of the use of stereotactic electroencephalography in comparison to subdural grids for invasive epilepsy monitoring in pediatric subjects. Neurosurgery. 2019;84(6):11901200.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50

    Vadera S, Mullin J, Bulacio J, et al. Stereoelectroencephalography following subdural grid placement for difficult to localize epilepsy. Neurosurgery. 2013;72(5):723729.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51

    Engel J Jr, Van Ness PC, Rasmussen TB, Ojemann LM. Outcome with respect to epileptic seizures. In: Engel J Jr, ed.Surgical Treatment of the Epilepsies.2nd ed. Raven Press;1993:609621.

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Image from Mavridis et al. (pp 404–415).

  • FIG. 1.

    Postoperative CT scanogram obtained in an 11-year-old girl who had undergone robot-assisted SEEG electrode implantation (10 in the right cerebral hemisphere and 4 in the left). Scalp EEG electrodes are also visible.

  • FIG. 2.

    Kaplan-Meier curve demonstrating the seizure-free rates (survival) of the 12 nonrobot and 11 robot-assisted cases that underwent resective surgery following SEEG investigation.

  • FIG. 3.

    Case 11. Postoperative day 1 axial CT scan obtained in a patient who had undergone implantation of left SEEG electrodes, showing a left frontal extradural hematoma associated with an overlying burr hole for electrode insertion.

  • FIG. 4.

    Axial CT scan (A) and inferior view of the 3D reconstruction (B) demonstrating a fractured right anterior hippocampus electrode (asterisks) and detached guiding bolt (white arrowheads). Note the discontinuation of the electrode lead between the loose bolt and skull. Figure is available in color online only.

  • 1

    Bourdillon P, Châtillon CE, Moles A, et al. Effective accuracy of stereoelectroencephalography: robotic 3D versus Talairach orthogonal approaches. J Neurosurg. 2018;131(6):19381946.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Gonzalez-Martinez J, Lachhwani D. Stereoelectroencephalography in children with cortical dysplasia: technique and results. Childs Nerv Syst. 2014;30(11):18531857.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Abel TJ, Varela Osorio R, Amorim-Leite R, et al. Frameless robot-assisted stereoelectroencephalography in children: technical aspects and comparison with Talairach frame technique. J Neurosurg Pediatr. 2018;22(1):3746.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Cardinale F, Rizzi M, Vignati E, et al. Stereoelectroencephalography: retrospective analysis of 742 procedures in a single centre. Brain. 2019;142(9):26882704.

  • 5

    Cossu M, Cardinale F, Colombo N, et al. Stereoelectroencephalography in the presurgical evaluation of children with drug-resistant focal epilepsy. J Neurosurg. 2005;103(4)(suppl):333343.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    González-Martínez J, Bulacio J, Thompson S, et al. Technique, results, and complications related to robot-assisted stereoelectroencephalography. Neurosurgery. 2016;78(2):169180.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Ho AL, Muftuoglu Y, Pendharkar AV, et al. Robot-guided pediatric stereoelectroencephalography: single-institution experience. J Neurosurg Pediatr. 2018;22(5):489496.

  • 8

    Mullin JP, Shriver M, Alomar S, et al. Is SEEG safe? A systematic review and meta-analysis of stereo-electroencephalography-related complications. Epilepsia. 2016;57(3):386401.

  • 9

    Ollivier I, Behr C, Cebula H, et al. Efficacy and safety in frameless robot-assisted stereo-electroencephalography (SEEG) for drug-resistant epilepsy. Neurochirurgie. 2017;63(4):286290.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Scorza D, De Momi E, Plaino L, et al. Retrospective evaluation and SEEG trajectory analysis for interactive multi-trajectory planner assistant. Int J CARS. 2017;12(10):17271738.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    van der Loo LE, Schijns OEMG, Hoogland G, et al. Methodology, outcome, safety and in vivo accuracy in traditional frame-based stereoelectroencephalography. Acta Neurochir (Wien). 2017;159(9):17331746.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Willems LM, Reif PS, Spyrantis A, et al. Invasive EEG-electrodes in presurgical evaluation of epilepsies: Systematic analysis of implantation-, video-EEG-monitoring- and explantation-related complications, and review of literature. Epilepsy Behav. 2019;91:3037.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Goldstein HE, Youngerman BE, Shao B, et al. Safety and efficacy of stereoelectroencephalography in pediatric focal epilepsy: a single-center experience. J Neurosurg Pediatr. 2018;22(4):444452.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Bottan JS, Rubino PA, Lau JC, et al. Robot-assisted insular depth electrode implantation through oblique trajectories: 3-dimensional anatomical nuances, technique, accuracy, and safety. Oper Neurosurg (Hagerstown). 2020;18(3):278283.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Alomar S, Mullin JP, Smithason S, Gonzalez-Martinez J. Indications, technique, and safety profile of insular stereoelectroencephalography electrode implantation in medically intractable epilepsy. J Neurosurg. 2018;128(4):11471157.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Bourdillon P, Ryvlin P, Isnard J, et al. Stereotactic electroencephalography is a safe procedure, including for insular implantations. World Neurosurg.2017;99:353361.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Dylgjeri S, Taussig D, Chipaux M, et al. Insular and insulo-opercular epilepsy in childhood: an SEEG study. Seizure. 2014;23(4):300308.

  • 18

    Kappen P, Eltze C, Tisdall M, et al. Stereo-EEG exploration in the insula/operculum in paediatric patients with refractory epilepsy. Seizure. 2020;78:6370.

  • 19

    Salado AL, Koessler L, De Mijolla G, et al. sEEG is a safe procedure for a comprehensive anatomic exploration of the insula: a retrospective study of 108 procedures representing 254 transopercular insular electrodes. Oper Neurosurg (Hagerstown). 2018;14(1):18.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Méreaux JL, Gilard V, Le Goff F, et al. Practice of stereoelectroencephalography (sEEG) in drug-resistant epilepsy: Retrospective series with surgery and thermocoagulation outcomes. Neurochirurgie. 2020;66(3):139143.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Taussig D, Chipaux M, Lebas A, et al. Stereo-electroencephalography (SEEG) in 65 children: an effective and safe diagnostic method for pre-surgical diagnosis, independent of age. Epileptic Disord. 2014;16(3):280295.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    McGovern RA, Knight EP, Gupta A, et al. Robot-assisted stereoelectroencephalography in children. J Neurosurg Pediatr. 2018;23(3):288296.

  • 23

    Taylor DC. Differential rates of cerebral maturation between sexes and between hemispheres. Evidence from epilepsy. Lancet. 1969;2(7612):140142.

  • 24

    McGovern RA, Ruggieri P, Bulacio J, et al. Risk analysis of hemorrhage in stereo-electroencephalography procedures. Epilepsia. 2019;60(3):571580.

  • 25

    Budke M, Avecillas-Chasin JM, Villarejo F. Implantation of depth electrodes in children using VarioGuide® frameless navigation system: technical note. Oper Neurosurg (Hagerstown). 2018;15(3):302309.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Kim LH, Parker JJ, Ho AL, et al. Postoperative outcomes following pediatric intracranial electrode monitoring: a case for stereoelectroencephalography (SEEG). Epilepsy Behav. 2020;104(pt A):106905.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Cobourn K, Fayed I, Keating RF, Oluigbo CO. Early outcomes of stereoelectroencephalography followed by MR-guided laser interstitial thermal therapy: a paradigm for minimally invasive epilepsy surgery. Neurosurg Focus. 2018;45(3):E8.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    De Benedictis A, Trezza A, Carai A, et al. Robot-assisted procedures in pediatric neurosurgery. Neurosurg Focus. 2017;42(5):E7.

  • 29

    Candela-Cantó S, Aparicio J, López JM, et al. Frameless robot-assisted stereoelectroencephalography for refractory epilepsy in pediatric patients: accuracy, usefulness, and technical issues. Acta Neurochir (Wien). 2018;160(12):24892500.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Cardinale F, Cossu M, Castana L, et al. Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures. Neurosurgery. 2013;72(3):353366.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Dorfmüller G, Ferrand-Sorbets S, Fohlen M, et al. Outcome of surgery in children with focal cortical dysplasia younger than 5 years explored by stereo-electroencephalography. Childs Nerv Syst. 2014;30(11):18751883.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Gonzalez-Martinez J, Bulacio J, Alexopoulos A, et al. Stereoelectroencephalography in the “difficult to localize” refractory focal epilepsy: early experience from a North American epilepsy center. Epilepsia. 2013;54(2):323330.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Mathon B, Clemenceau S, Hasboun D, et al. Safety profile of intracranial electrode implantation for video-EEG recordings in drug-resistant focal epilepsy. J Neurol. 2015;262(12):26992712.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Cossu M, Schiariti M, Francione S, et al. Stereoelectroencephalography in the presurgical evaluation of focal epilepsy in infancy and early childhood. J Neurosurg Pediatr. 2012;9(3):290300.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Cossu M, Cardinale F, Castana L, et al. Stereoelectroencephalography in the presurgical evaluation of focal epilepsy: a retrospective analysis of 215 procedures. Neurosurgery. 2005;57(4):706718.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Gonzalez-Martinez J, Mullin J, Vadera S, et al. Stereotactic placement of depth electrodes in medically intractable epilepsy. J Neurosurg. 2014;120(3):639644.

  • 37

    Liava A, Mai R, Tassi L, et al. Paediatric epilepsy surgery in the posterior cortex: a study of 62 cases. Epileptic Disord. 2014;16(2):141164.

  • 38

    Serletis D, Bulacio J, Bingaman W, et al. The stereotactic approach for mapping epileptic networks: a prospective study of 200 patients. J Neurosurg. 2014;121(5):12391246.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Yang M, Ma Y, Li W, et al. A retrospective analysis of stereoelectroencephalography and subdural electroencephalography for preoperative evaluation of intractable epilepsy. Stereotact Funct Neurosurg. 2017;95(1):1320.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Toledano R, Martínez-Álvarez R, Jiménez-Huete A, et al. Stereoelectroencephalography in the preoperative assessment of patients with refractory focal epilepsy: experience at an epilepsy centre. Article in Spanish. Neurologia. Published online July 20, 2019. doi:10.1016/j.nrl.2019.05.002

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Munari C, Hoffmann D, Francione S, et al. Stereo-electroencephalography methodology: advantages and limits. Acta Neurol Scand Suppl. 1994;152:5669.

  • 42

    Guenot M, Isnard J, Ryvlin P, et al. Neurophysiological monitoring for epilepsy surgery: the Talairach SEEG method. StereoElectroEncephaloGraphy. Indications, results, complications and therapeutic applications in a series of 100 consecutive cases. Stereotact Funct Neurosurg. 2001;77(1-4):2932.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Zhang G, Chen G, Meng D, et al. Stereoelectroencephalography based on the Leksell stereotactic frame and Neurotech operation planning software. Medicine (Baltimore). 2017;96(23):e7106.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Dewan MC, Shults R, Hale AT, et al. Stereotactic EEG via multiple single-path omnidirectional trajectories within a single platform: institutional experience with a novel technique. J Neurosurg. 2018;129(5):11731181.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Tandon N, Tong BA, Friedman ER, et al. Analysis of morbidity and outcomes associated with use of subdural grids vs stereoelectroencephalography in patients with intractable epilepsy. JAMA Neurol. 2019;76(6):672681.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    Alexander H, Fayed I, Oluigbo CO. Rigid cranial fixation for robot-assisted stereoelectroencephalography in toddlers: technical considerations. Oper Neurosurg (Hagerstown). 2020;18(6):614620.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47

    Joswig H, Lau JC, Abdallat M, et al. Stereoelectroencephalography versus subdural strip electrode implantations: feasibility, complications, and outcomes in 500 intracranial monitoring cases for drug-resistant epilepsy. Neurosurgery. 2020;87(1):E23E30.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48

    Narváez-Martínez Y, García S, Roldán P, et al. Stereoelectroencephalography by using O-Arm® and Vertek® passive articulated arm: technical note and experience of an epilepsy referral centre. Article in Spanish. Neurocirugia (Astur). 2016;27(6):277284.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49

    Sacino MF, Huang SS, Schreiber J, et al. Is the use of stereotactic electroencephalography safe and effective in children? A meta-analysis of the use of stereotactic electroencephalography in comparison to subdural grids for invasive epilepsy monitoring in pediatric subjects. Neurosurgery. 2019;84(6):11901200.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50

    Vadera S, Mullin J, Bulacio J, et al. Stereoelectroencephalography following subdural grid placement for difficult to localize epilepsy. Neurosurgery. 2013;72(5):723729.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51

    Engel J Jr, Van Ness PC, Rasmussen TB, Ojemann LM. Outcome with respect to epileptic seizures. In: Engel J Jr, ed.Surgical Treatment of the Epilepsies.2nd ed. Raven Press;1993:609621.

    • PubMed
    • Search Google Scholar
    • Export Citation

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