Subdural electrodes versus stereoelectroencephalography for pediatric epileptogenic zone localization: a retrospective cohort study

Madison RemickDepartments of Neurological Surgery,

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Emefa AkwayenaDepartments of Neurological Surgery,

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Emily HarfordDepartments of Neurological Surgery,

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Akanksha ChilukuriDepartments of Neurological Surgery,

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Gretchen E. WhiteGeneral Internal Medicine, and

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Taylor J. AbelDepartments of Neurological Surgery,
Bioengineering, University of Pittsburgh, Pennsylvania

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OBJECTIVE

The objective of this study was to compare the relative safety and effectiveness of invasive monitoring with subdural electrodes (SDEs) and stereoelectroencephalography (sEEG) in pediatric patients with drug-resistant epilepsy.

METHODS

A retrospective cohort study was performed in 176 patients who underwent invasive monitoring evaluations at UPMC Children’s Hospital of Pittsburgh between January 2000 and September 2021. To examine differences between SDE and sEEG groups, independent-samples t-tests for continuous variables and Pearson chi-square tests for categorical variables were performed. A p value < 0.1 was considered statistically significant.

RESULTS

There were 134 patients (76%) in the SDE group and 42 (24%) in the sEEG group. There was a difference in the proportion with complications (17.9% in the SDE group vs 7.1% in the sEEG group, p = 0.09) and resection (75.4% SDE vs 21.4% sEEG, p < 0.01) between SDE and sEEG patients. However, there was no observable difference in the rates of postresection seizure freedom at 1-year clinical follow-up (60.2% SDE vs 75.0% sEEG, p = 0.55).

CONCLUSIONS

These findings reveal a difference in rates of surgical complications and resection between SDEs and sEEG. Larger prospective, multi-institutional pediatric comparative effectiveness studies may further explore these associations.

ABBREVIATIONS

DRE = drug-resistant epilepsy; EZ = epileptogenic zone; RCT = randomized controlled trial; RNS = responsive neural stimulation; SDE = subdural electrode; sEEG = stereoelectroencephalography; SLA = stereotactic laser ablation.

OBJECTIVE

The objective of this study was to compare the relative safety and effectiveness of invasive monitoring with subdural electrodes (SDEs) and stereoelectroencephalography (sEEG) in pediatric patients with drug-resistant epilepsy.

METHODS

A retrospective cohort study was performed in 176 patients who underwent invasive monitoring evaluations at UPMC Children’s Hospital of Pittsburgh between January 2000 and September 2021. To examine differences between SDE and sEEG groups, independent-samples t-tests for continuous variables and Pearson chi-square tests for categorical variables were performed. A p value < 0.1 was considered statistically significant.

RESULTS

There were 134 patients (76%) in the SDE group and 42 (24%) in the sEEG group. There was a difference in the proportion with complications (17.9% in the SDE group vs 7.1% in the sEEG group, p = 0.09) and resection (75.4% SDE vs 21.4% sEEG, p < 0.01) between SDE and sEEG patients. However, there was no observable difference in the rates of postresection seizure freedom at 1-year clinical follow-up (60.2% SDE vs 75.0% sEEG, p = 0.55).

CONCLUSIONS

These findings reveal a difference in rates of surgical complications and resection between SDEs and sEEG. Larger prospective, multi-institutional pediatric comparative effectiveness studies may further explore these associations.

Invasive monitoring with direct brain recordings is often necessary to localize the epileptogenic zone (EZ) prior to resective neurosurgery.1,2 Over approximately the last 50 years, a variety of different electrode implantation techniques have been used, including subdural grids and strips (subdural electrodes [SDEs]), subdural strips without grids, and stereoelectroencephalography (sEEG).3,4 Until recently, these techniques have had a geographic distribution based on tradition, with SDEs more popular in North America and sEEG more prevalent in France and Italy.57 The recent advances in neuroimaging, stereotactic targeting, and neurosurgical robotics have led to the increasing use of sEEG throughout North America and the world.812 sEEG is an attractive alternative because it obviates the need to perform a craniotomy prior to localizing the EZ.13 However, because there are no randomized controlled trials (RCTs) to compare SDE and sEEG invasive monitoring strategies, which of these techniques is 1) associated with fewer complications and 2) associated with the highest success of seizure freedom remains unknown.14 Descriptive retrospective cohort studies with observational data have emerged in recent years to help answer this question and allow for the meta-analysis of large data sets.1517

Thus, this study describes a large retrospective cohort of pediatric patients who underwent invasive monitoring via either SDEs or sEEG at the Children’s Hospital of Pittsburgh. We hypothesize that sEEG is associated with a lower rate of complications due to lack of a craniotomy. We also hypothesize that SDEs are associated with a higher rate of postmonitoring resection given that placement of SDEs requires a craniotomy.

Methods

Patient Cohort and Study Criteria

A retrospective chart review was conducted to identify all patients who underwent invasive monitoring using either SDEs or sEEG for phase II evaluation of drug-resistant epilepsy (DRE) between January 2000 and September 2021 at UPMC Children’s Hospital of Pittsburgh. This study was prospectively reviewed and approved by the IRB of the University of Pittsburgh.

In total, 203 patients were identified through the Pediatric Neurosurgery Database of the University of Pittsburgh Medical Center. Patients were included in the final cohort if they underwent either SDE or sEEG implantation for phase II evaluation of DRE and were 21 years of age or younger at the time of surgery. Additionally, SDE patients implanted with depth electrodes were included in the SDE cohort, which was defined on the basis of undergoing a craniotomy. Patients who underwent SDE with the use of burr holes or strip electrodes were excluded. Following application of the inclusion and exclusion criteria, 176 patient records were included in the final cohort (Fig. 1).

FIG. 1.
FIG. 1.

Patient identification and selection process.

Data Collection

Patient data were extracted from the electronic medical record, including sex, age at surgery, invasive monitoring technique, associated pathology, invasive monitoring–related complications, postmonitoring intervention, length of clinical follow-up, and seizure outcome over the course of clinical follow-up.

The clinical decision for patients to undergo invasive monitoring was made at the discretion of the multidisciplinary epilepsy conference, in which all patients with DRE who are candidates for epilepsy surgery are discussed. All invasive monitoring instances prior to 2019 were with SDEs and all instances following January 2019 were with sEEG. There have been no SDE procedures since sEEG was started. Additionally, stereotactic laser ablation (SLA) or responsive neural stimulation (RNS) were only used after 2019. The decision to proceed with invasive monitoring was only made if noninvasive methods could not adequately identify the patient’s EZ.

The primary outcome of interest was the proportion of complications among patients monitored with SDE versus sEEG. We were specifically interested in invasive monitoring complications, rather than complications related to the ultimate intervention (e.g., resection, SLA, or RNS). Data on all complications related to electrode implantation and removal were collected and complications were assessed by a neurosurgeon (T.J.A.) to be related to invasive monitoring or resection. Neurological deficits were classified as transient if lasting 6 months or less, and permanent if lasting more than 6 months following electrode explantation. Incidences of hemorrhage and hematoma were only classified as a complication if they were symptomatic, resulted in subsequent neurological deficit, or required a return to the operating room.

As a secondary outcome, we assessed the proportion of patients who achieved seizure freedom at 1-year follow-up after resection with informed invasive monitoring. It is noteworthy that these comparisons are limited by the small number of sEEG patients as this procedure was not introduced at our institution until 2019. We did not compare patients who underwent ablation to those who had resection because ablation and resection have different outcome characteristics and ablation was only performed in patients in the sEEG group. SLA was performed in patients when either: 1) the EZ was confined to a small onset region, such that undergoing SLA was believed to provide the opportunity for an optimal seizure outcome; or 2) as a palliative option, when SLA was believed to provide beneficial seizure control, but resection of the region was not expected to be associated with seizure freedom, making a large, more invasive procedure less desirable. When the goal of surgery was seizure freedom, traditional craniotomy with resection was discussed as a mode of treatment that could be considered if SLA did not provide the desired outcome. Both the Engel class and the International League Against Epilepsy frameworks were used to classify seizure freedom.18,19

Statistical Analysis

Comparisons of continuous variables were performed using independent-samples t-tests. Comparisons of categorical variables were performed using the Pearson chi-square test with corresponding p values. All statistical analyses were conducted using IBM SPSS Statistics software (version 27.0.1.0, IBM Corp.). Given the exploratory nature of this study, a p value < 0.1 was considered significant.

Results

Patient Cohort

One hundred seventy-six pediatric patients underwent invasive monitoring using either SDE or sEEG over the course of 2 decades, with 76% of patients monitored with SDEs and 24% with sEEG. Additionally, 32% of the SDE patients also received depth electrode implantation. SDE and sEEG patients had similar characteristics, except sEEG patients were significantly older than SDE patients (14 vs 11 years, p < 0.01; Table 1).

TABLE 1.

Patient demographic and intervention data

VariableSDE, n = 134sEEG, n = 42
Female, n (%)60 (44.8)18 (42.9)
Age, yrs*
 Mean ± SD10.9 ± 4.913.9 ± 4.2
 Median (IQR)12.0 (7–15)14.5 (12–18)
MRI positive, n (%)85 (63.4)27 (64.3)
Laterality, n (%)
 Bilat12 (9.0)7 (16.7)
 Unilat122 (91.0)35 (83.3)
Surgical intervention, n (%)*
 Resection101 (75.4)9 (21.4)
 SLA0 (0)14 (33.3)

IQR = interquartile range.

Chi-square tests were conducted for categorical variables and unpaired t-tests for continuous variables.

p < 0.1.

Similar proportions of SDE and sEEG patients demonstrated lesions on MRI. When examining pathologies among groups, malformations of cortical development, gliosis, and tumor represented more than two-thirds of patients undergoing SDE (Fig. 2 upper), and a similar proportion of sEEG patients was represented by malformations of cortical development, postischemic/traumatic changes, gliosis, and tumor (Fig. 2 lower). Subsequent electrode implantation was bilateral in 12 SDE patients (9.0%) compared to 7 sEEG patients (16.7%; Table 1).

FIG. 2.
FIG. 2.

Upper: Pathologies associated with patients undergoing SDE implantation. Lower: Pathologies associated with patients undergoing sEEG.

Complications

A higher proportion of patients undergoing SDE experienced complications (17.9% with SDEs vs 7.1% with sEEG, p = 0.09; Table 2). In the SDE group, there were 8 SDE-related complications, consisting of 3 infections and 5 hemorrhages. All reported SDE-related hemorrhages were symptomatic, but only 2 required subsequent return to the operating room. One SDE patient experienced an electrode tract hemorrhage that was directly related to a depth electrode. In comparison, there were 2 monitoring-related complications reported among sEEG patients. One patient had a lead fracture and the other a symptomatic intraparenchymal hemorrhage not requiring a return to the operating room. The lead fracture occurred in a 3-year-old who had turned her head while waking up during anesthesia, which fractured an anchor bolt and severed the sEEG electrode. There was a statistically significant difference in transient neurological deficits, i.e., 16 reported incidences among SDE patients versus 1 sEEG-related deficit (p = 0.07). Additionally, a significantly greater proportion of SDE patients experienced transient weakness compared with sEEG patients (6.7% vs 0%, p = 0.08). There were no SDE- or sEEG-associated permanent neurological deficits or deaths.

TABLE 2.

Summary of postoperative complications

ComplicationSDE, n = 134sEEG, n = 42
Overall morbidity, n (%)*24 (17.9)3 (7.1)
Invasive monitoring–related complications, n (%)8 (6.0)2 (4.8)
 Infection3 (2.2)0 (0)
 Lead fracture*0 (0)1 (2.4)
 Hemorrhage5 (3.7)1 (2.4)
  Epidural hematoma2 (1.5)0 (0)
  Subdural hematoma2 (1.5)0 (0)
  Intraparenchymal hemorrhage1 (0.7)1 (2.4)
Transient neurological deficits, n (%)*16 (11.9)1 (2.4)
 Altered mental status2 (1.5)1 (2.4)
 Hemiparesis2 (1.5)0 (0)
 Mutism1 (0.7)0 (0)
 Paresthesia2 (1.5)0 (0)
 Weakness*9 (6.7)0 (0)

Chi-square tests were conducted for each categorical variable.

p < 0.01.

Resection Status

Three-fourths (75.4%) of the SDE patients underwent subsequent resection following invasive monitoring compared with 9 sEEG patients (21.4%, p < 0.01; Table 1). No patients in the SDE group underwent SLA per the practice pattern at our institution.

Follow-Up and Seizure Freedom

In the cohort, 123 SDE and 25 sEEG patients maintained at least 1 year of clinical follow-up, with 93 SDE and 17 sEEG patients reporting seizure outcomes at this time point. Independent of surgical intervention, there was no observable difference in the incidence of seizure freedom among SDE versus sEEG patients (60.2% vs 41.2%, p = 0.14; Table 3). Among patients who underwent resection, 93 SDE- and 4 sEEG-monitored patients reported seizure outcomes at 1 year. There was no significant difference in the proportion of patients achieving seizure freedom at this time point (60.2% with SDEs vs 75.0% with sEEG, p = 0.55; Table 3). Thirteen sEEG-monitored patients underwent an SLA, 4 (30.8%) of whom achieved seizure freedom at 1 year.

TABLE 3.

Summary of postoperative seizure freedom

VariableSDE, n = 93sEEG, n = 17
Postop seizure freedom, n (%)56 (60.2)7/17 (41.2)
 Post-resection seizure freedom56 (60.2)3/4 (75.0)
 Post-ablative seizure freedom4/13 (30.8)

Chi-square tests were conducted for each categorical variable and no p value was < 0.10.

Discussion

These data add to a growing number of observational studies comparing the safety and effectiveness of SDEs and sEEG. The primary benefit of sEEG is its ability to record from deep structures such as the hippocampus, hypothalamus, insula, and deep frontal lobes that would be insufficiently covered by SDEs without the need for craniotomy. Systematic reviews have shown that sEEG is likely the safer technique when compared to SDEs, in addition to being better tolerated by patients and more time-efficient for surgeons.1,14 In contrast, SDEs allow for continuous coverage over larger areas of superficial cortex, which can be extensively mapped to guide resection around areas of executive functioning. Ultimately, however, unless pre-invasive monitoring data regarding the EZ are suggestive of surface localization, especially near or within eloquent cortex, then sEEG provides the most adaptable monitoring approach.20 For example, some centers preferentially use sEEG for language mapping prior to resection.21

A recent systematic review of invasive monitoring outcomes demonstrated that SDE implantation is associated with higher morbidity and mortality compared to sEEG.15 This finding of differences in complication rates following SDE implantation or sEEG is consistent with the findings of previous meta-analyses of invasive monitoring complications that did not compare the two modalities.2224 That same review revealed that SDEs are associated with higher rates of resective intervention, but among patients who did undergo resection, sEEG was associated with higher rates of seizure freedom. One potential explanation for this finding is that because SDEs require craniotomy, there is a bias toward resection even when invasive monitoring findings may lead just as clearly to resection. It is also possible that because sEEG obviates a craniotomy, more complex patients, potentially with bilateral involvement, are explored, which might be inherently more complex and lead to fewer resections. However, a follow-up individual patient data meta-analysis using these same data did not show any differences in seizure freedom rates after either SDE- or sEEG-informed resection with long-term follow-up.16

Until recently, a limitation of the existing literature was that comparisons of SDE and sEEG complication rates have been made across rather than within epilepsy surgery programs.15,16,23,25,26 This is due to the fact that historically, sEEG and SDEs have been used in geographically distinct locations, with most sEEG centers focused in Europe and SDEs in North America. However, recent retrospective observational studies show findings similar to the systematic reviews described above. For example, one US study showed that sEEG was associated with higher rates of seizure freedom and lower rates of complications.27 A recent single-center pediatric series demonstrated that while sEEG was associated with lower rates of complications, seizure freedom rates were similar to those seen with SDEs.28 In contrast, a large multi-institutional case series recently showed that sEEG is a safe and effective means of EZ localization for pediatric patients, and complication profiles and seizure freedom outcomes were likely associated with the experience of each center.29 Furthermore, a comparative effectiveness study shows that while SDE-monitored patients are more likely to undergo resection, they are also more likely to experience perioperative complications, in addition to a lower likelihood of achieving subsequent seizure freedom.30 The authors emphasized that SDEs and sEEG are inherently unique procedures that result in unique complication profiles, and their findings were consistent with those in previous studies regarding the differences in complication rates between these techniques.15

In light of existing work, our paper provides further support for the association of sEEG with a lower complication rate compared to SDEs. In the current era, patients now have the option of laser ablation or neuromodulation after invasive monitoring, highlighting the importance of future studies that will need to evaluate real-world effectiveness of invasive monitoring given these more recent treatment options. While this study was unable to make comparisons between SDE and sEEG patients undergoing resection versus neuromodulation due to limitations in sample size, other recent studies have highlighted the importance of considering these other treatment modalities.28,31

Limitations of the Study

This is one of the largest available retrospective cohort studies examining pediatric invasive monitoring outcomes, which is a major strength of our data. There are numerous inherent limitations, which include selection bias, evolution of treatment selection over time, and relatively small sample size in our sEEG group. This study involves the work of four different surgeons who utilized different techniques at different times across a 20-year time span that allowed for potential confounders. The techniques, surgeons, and surgical technologies available to them are all variables that are simultaneously evolving and improving over time and are unable to be controlled for in this analysis. For example, different surgical technologies with varying levels of complexity and means of intraoperative registration have been shown to impact surgeon learning curves.32 Additionally, the learning curves for procedures such as sEEG have been shown to be shorter for those experienced in stereotactic neurosurgery. Nevertheless, these data are important and can be incorporated into future systematic reviews, propensity score matching analyses, and meta-analyses as it is unlikely there will ever be an RCT comparing sEEG and SDE.

Conclusions

This retrospective cohort study shows that sEEG is associated with a lower complication rate compared to SDEs. Future meta-analyses should include a subset analysis of studies that investigated differences in complication and seizure-freedom rates between sEEG and SDE patients treated at the same center.

Acknowledgments

Dr. Abel is funded by NIH grant no. R21DC019217 and no. R01DC013315.

Disclosures

Dr. Abel is a consultant for and receives funding from the Monteris Medical Corporation, which is not related to the content of this study.

Author Contributions

Conception and design: Abel, Remick. Acquisition of data: Abel, Remick, Akwayena, Harford, Chilukuri. Analysis and interpretation of data: Abel, Remick, White. Drafting the article: Abel, Remick, Akwayena, Chilukuri, White. Critically revising the article: Abel, Remick, White. Reviewed submitted version of manuscript: Abel, Remick, Akwayena, White. Statistical analysis: Abel, Remick, White. Administrative/technical/material support: Akwayena, Harford.

Supplemental Information

Videos

Video Abstract. https://vimeo.com/748747596.

Previous Presentations

Portions of this work were presented in poster form at the American Epilepsy Society Annual Conference in Chicago, Illinois, on December 5, 2021.

References

  • 1

    Katz JS, Abel TJ. Stereoelectroencephalography versus subdural electrodes for localization of the epileptogenic zone: what is the evidence? Neurotherapeutics. 2019;16(1):5966.

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

    Jobst BC, Bartolomei F, Diehl B, et al. Intracranial EEG in the 21st century. Epilepsy Curr. 2020;20(4):180188.

  • 3

    Taussig D, Montavont A, Isnard J. Invasive EEG explorations. Neurophysiol Clin. 2015;45(1):113119.

  • 4

    Taussig D, Chipaux M, Fohlen M, et al. Invasive evaluation in children (SEEG vs subdural grids). Seizure. 2020;77:4351.

  • 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.

    • Search Google Scholar
    • Export Citation
  • 6

    Engel J Jr. Evolution of concepts in epilepsy surgery. Epileptic Disord. 2019;21(5):391409.

  • 7

    Abou-Al-Shaar H, Brock AA, Kundu B, Englot DJ, Rolston JD. Increased nationwide use of stereoencephalography for intracranial epilepsy electroencephalography recordings. J Clin Neurosci. 2018;53:132134.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Faraji AH, Remick M, Abel TJ. Contributions of robotics to the safety and efficacy of invasive monitoring with stereoelectroencephalography. Front Neurol. 2020;11:570010.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Candela S, Vanegas MI, Darling A, et al. Frameless robot-assisted pallidal deep brain stimulation surgery in pediatric patients with movement disorders: precision and short-term clinical results. J Neurosurg Pediatr. 2018;22(4):416425.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Neudorfer C, Hunsche S, Hellmich M, El Majdoub F, Maarouf M. Comparative study of robot-assisted versus conventional frame-based deep brain stimulation stereotactic neurosurgery. Stereotact Funct Neurosurg. 2018;96(5):327334.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

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

  • 12

    Mavridis IN, Lo WB, Wimalachandra WSB, et al. Pediatric stereo-electroencephalography: effects of robot assistance and other variables on seizure outcome and complications. J Neurosurg Pediatr. 2021;28(4):404415.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Englot DJ. A modern epilepsy surgery treatment algorithm: incorporating traditional and emerging technologies. Epilepsy Behav. 2018;80:6874.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Jayakar P, Gotman J, Harvey AS, et al. Diagnostic utility of invasive EEG for epilepsy surgery: indications, modalities, and techniques. Epilepsia. 2016;57(11):17351747.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Yan H, Katz JS, Anderson M, et al. Method of invasive monitoring in epilepsy surgery and seizure freedom and morbidity: a systematic review. Epilepsia. 2019;60(9):19601972.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Remick M, Ibrahim GM, Mansouri A, Abel TJ. Patient phenotypes and clinical outcomes in invasive monitoring for epilepsy: an individual patient data meta-analysis. Epilepsy Behav. 2020;102:106652.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Hernán MA. Causal analyses of existing databases: no power calculations required. J Clin Epidemiol. 2022;144:203205.

  • 18

    Steriade C, Sperling MR, DiVentura B, et al. Proposal for an updated seizure classification framework in clinical trials. Epilepsia. 2022;63(3):565572.

  • 19

    Engel J Jr. Surgery for seizures. N Engl J Med. 1996;334(10):647652.

  • 20

    Richardson RM. Decision making in epilepsy surgery. Neurosurg Clin N Am. 2020;31(3):471479.

  • 21

    Aron O, Jonas J, Colnat-Coulbois S, Maillard L. Language mapping using stereo electroencephalography: a review and expert opinion. Front Hum Neurosci. 2021;15:619521.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Arya R, Mangano FT, Horn PS, Holland KD, Rose DF, Glauser TA. Adverse events related to extraoperative invasive EEG monitoring with subdural grid electrodes: a systematic review and meta-analysis. Epilepsia. 2013;54(5):828839.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    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.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Mullin JP, Sexton D, Al-Omar S, Bingaman W, Gonzalez-Martinez J. Outcomes of subdural grid electrode monitoring in the stereoelectroencephalography era. World Neurosurg. 2016;89:255258.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Toth M, Papp KS, Gede N, et al. Surgical outcomes related to invasive EEG monitoring with subdural grids or depth electrodes in adults: a systematic review and meta-analysis. Seizure. 2019;70:1219.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Sacino MF, Huang SS, Schreiber J, Gaillard WD, Oluigbo CO. 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
    • Search Google Scholar
    • Export Citation
  • 27

    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
    • Search Google Scholar
    • Export Citation
  • 28

    Talai A, Eschbach K, Stence NV, et al. Comparison of subdural grid and stereoelectroencephalography in a cohort of pediatric patients. Epilepsy Res. 2021;177:106758.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Lepard JR, Kim I, Arynchyna A, et al. Early implementation of stereoelectroencephalography in children: a multiinstitutional case series. J Neurosurg Pediatr. 2021;28(6):669676.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Jehi L, Morita-Sherman M, Love TE, et al. Comparative effectiveness of stereotactic electroencephalography versus subdural grids in epilepsy surgery. Ann Neurol. 2021;90(6):927939.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31

    McGrath H, Mandel M, Sandhu MRS, et al. Optimizing the surgical management of MRI-negative epilepsy in the neuromodulation era. Epilepsia Open. 2022;7(1):151159.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32

    Machetanz K, Grimm F, Schuhmann M, Tatagiba M, Gharabaghi A, Naros G. Time efficiency in stereotactic robot-assisted surgery: an appraisal of the surgical procedure and surgeon’s learning curve. Stereotact Funct Neurosurg. 2021;99(1):2533.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand
  • View in gallery
    FIG. 1.

    Patient identification and selection process.

  • View in gallery
    FIG. 2.

    Upper: Pathologies associated with patients undergoing SDE implantation. Lower: Pathologies associated with patients undergoing sEEG.

  • 1

    Katz JS, Abel TJ. Stereoelectroencephalography versus subdural electrodes for localization of the epileptogenic zone: what is the evidence? Neurotherapeutics. 2019;16(1):5966.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Jobst BC, Bartolomei F, Diehl B, et al. Intracranial EEG in the 21st century. Epilepsy Curr. 2020;20(4):180188.

  • 3

    Taussig D, Montavont A, Isnard J. Invasive EEG explorations. Neurophysiol Clin. 2015;45(1):113119.

  • 4

    Taussig D, Chipaux M, Fohlen M, et al. Invasive evaluation in children (SEEG vs subdural grids). Seizure. 2020;77:4351.

  • 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.

    • Search Google Scholar
    • Export Citation
  • 6

    Engel J Jr. Evolution of concepts in epilepsy surgery. Epileptic Disord. 2019;21(5):391409.

  • 7

    Abou-Al-Shaar H, Brock AA, Kundu B, Englot DJ, Rolston JD. Increased nationwide use of stereoencephalography for intracranial epilepsy electroencephalography recordings. J Clin Neurosci. 2018;53:132134.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Faraji AH, Remick M, Abel TJ. Contributions of robotics to the safety and efficacy of invasive monitoring with stereoelectroencephalography. Front Neurol. 2020;11:570010.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Candela S, Vanegas MI, Darling A, et al. Frameless robot-assisted pallidal deep brain stimulation surgery in pediatric patients with movement disorders: precision and short-term clinical results. J Neurosurg Pediatr. 2018;22(4):416425.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Neudorfer C, Hunsche S, Hellmich M, El Majdoub F, Maarouf M. Comparative study of robot-assisted versus conventional frame-based deep brain stimulation stereotactic neurosurgery. Stereotact Funct Neurosurg. 2018;96(5):327334.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

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

  • 12

    Mavridis IN, Lo WB, Wimalachandra WSB, et al. Pediatric stereo-electroencephalography: effects of robot assistance and other variables on seizure outcome and complications. J Neurosurg Pediatr. 2021;28(4):404415.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Englot DJ. A modern epilepsy surgery treatment algorithm: incorporating traditional and emerging technologies. Epilepsy Behav. 2018;80:6874.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Jayakar P, Gotman J, Harvey AS, et al. Diagnostic utility of invasive EEG for epilepsy surgery: indications, modalities, and techniques. Epilepsia. 2016;57(11):17351747.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Yan H, Katz JS, Anderson M, et al. Method of invasive monitoring in epilepsy surgery and seizure freedom and morbidity: a systematic review. Epilepsia. 2019;60(9):19601972.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Remick M, Ibrahim GM, Mansouri A, Abel TJ. Patient phenotypes and clinical outcomes in invasive monitoring for epilepsy: an individual patient data meta-analysis. Epilepsy Behav. 2020;102:106652.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Hernán MA. Causal analyses of existing databases: no power calculations required. J Clin Epidemiol. 2022;144:203205.

  • 18

    Steriade C, Sperling MR, DiVentura B, et al. Proposal for an updated seizure classification framework in clinical trials. Epilepsia. 2022;63(3):565572.

  • 19

    Engel J Jr. Surgery for seizures. N Engl J Med. 1996;334(10):647652.

  • 20

    Richardson RM. Decision making in epilepsy surgery. Neurosurg Clin N Am. 2020;31(3):471479.

  • 21

    Aron O, Jonas J, Colnat-Coulbois S, Maillard L. Language mapping using stereo electroencephalography: a review and expert opinion. Front Hum Neurosci. 2021;15:619521.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Arya R, Mangano FT, Horn PS, Holland KD, Rose DF, Glauser TA. Adverse events related to extraoperative invasive EEG monitoring with subdural grid electrodes: a systematic review and meta-analysis. Epilepsia. 2013;54(5):828839.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    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.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Mullin JP, Sexton D, Al-Omar S, Bingaman W, Gonzalez-Martinez J. Outcomes of subdural grid electrode monitoring in the stereoelectroencephalography era. World Neurosurg. 2016;89:255258.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Toth M, Papp KS, Gede N, et al. Surgical outcomes related to invasive EEG monitoring with subdural grids or depth electrodes in adults: a systematic review and meta-analysis. Seizure. 2019;70:1219.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Sacino MF, Huang SS, Schreiber J, Gaillard WD, Oluigbo CO. 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
    • Search Google Scholar
    • Export Citation
  • 27

    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
    • Search Google Scholar
    • Export Citation
  • 28

    Talai A, Eschbach K, Stence NV, et al. Comparison of subdural grid and stereoelectroencephalography in a cohort of pediatric patients. Epilepsy Res. 2021;177:106758.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Lepard JR, Kim I, Arynchyna A, et al. Early implementation of stereoelectroencephalography in children: a multiinstitutional case series. J Neurosurg Pediatr. 2021;28(6):669676.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Jehi L, Morita-Sherman M, Love TE, et al. Comparative effectiveness of stereotactic electroencephalography versus subdural grids in epilepsy surgery. Ann Neurol. 2021;90(6):927939.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31

    McGrath H, Mandel M, Sandhu MRS, et al. Optimizing the surgical management of MRI-negative epilepsy in the neuromodulation era. Epilepsia Open. 2022;7(1):151159.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32

    Machetanz K, Grimm F, Schuhmann M, Tatagiba M, Gharabaghi A, Naros G. Time efficiency in stereotactic robot-assisted surgery: an appraisal of the surgical procedure and surgeon’s learning curve. Stereotact Funct Neurosurg. 2021;99(1):2533.

    • Crossref
    • Search Google Scholar
    • Export Citation

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