Advances in intracranial monitoring

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Intracranial monitoring using electroencephalography (IC-EEG) continues to play a critical role in the assessment of patients with medically intractable localization-related epilepsy. There has been minimal change in grid or electrode design in the last 15–20 years, and the surgical approaches for implantation are unchanged. Intracranial monitoring using EEG allows detailed definition of the region of ictal onset and defines the epileptogenic zone, particularly with regard to adjacent potentially eloquent tissue. Recent developments of IC-EEG include the coregistration of functional imaging data such as magnetoencephalography to the frameless navigation systems. Despite significant inherent limitations that are often overlooked, IC-EEG remains the gold standard for localization of the epileptogenic cortex. Intracranial electrodes take a variety of different forms and may be placed either in the subdural (subdural strips and grids, depth electrodes) or extradural spaces (sphenoidal, peg, and epidural electrodes). Each form has its own advantages and shortcomings but extensive subdural implantation of electrodes is most common and is most comprehensively discussed. The indications for intracranial electrodes are reviewed.

Abbreviations used in this paper: EEG = electroencephalography; FDG = fluorine-18-labeled fluorodeoxyglucose; IC-EEG = intracranial EEG; MEG = magnetoencephalography; TLE = temporal lobe epilepsy.

Abstract

Intracranial monitoring using electroencephalography (IC-EEG) continues to play a critical role in the assessment of patients with medically intractable localization-related epilepsy. There has been minimal change in grid or electrode design in the last 15–20 years, and the surgical approaches for implantation are unchanged. Intracranial monitoring using EEG allows detailed definition of the region of ictal onset and defines the epileptogenic zone, particularly with regard to adjacent potentially eloquent tissue. Recent developments of IC-EEG include the coregistration of functional imaging data such as magnetoencephalography to the frameless navigation systems. Despite significant inherent limitations that are often overlooked, IC-EEG remains the gold standard for localization of the epileptogenic cortex. Intracranial electrodes take a variety of different forms and may be placed either in the subdural (subdural strips and grids, depth electrodes) or extradural spaces (sphenoidal, peg, and epidural electrodes). Each form has its own advantages and shortcomings but extensive subdural implantation of electrodes is most common and is most comprehensively discussed. The indications for intracranial electrodes are reviewed.

Essentials of Intracranial Monitoring for Epilepsy

Intracranial EEG monitoring plays a critical role in the assessment of patients with medically refractory partial epilepsy (or localization-related epilepsy).11,12,19,23,43 Controversies exist about the limits of IC-EEG, and the utilization of invasive monitoring differs significantly between centers, countries, and even geographic regions within a country.6,18 However, from a practical perspective, most large experienced tertiary centers apply similar principles in determining a patient's candidacy for intracranial electrode placement, monitoring, and use. Due to advances in noninvasive imaging, intracranial electrodes are used in ~25–40% of surgical cases in most large epilepsy centers.12 Their use is higher in pediatric surgical patient series due to the propensity of children to harbor neocortical epilepsy and the inherent difficulties of localizing neocortical epilepsy noninvasively.15,17,18,22,26 Intracranial electrodes remain, at present, the gold standard for delineating the epileptogenic tissue that can be considered the region of the brain from which arises the abnormal electrical discharges that when propagated yield the clinically important seizure pattern.22,30,57

From a surgical perspective this may be considered the region of tissue that must be removed to ameliorate seizure activity. The decision whether or not to place electrodes in a patient, as well as the location and configuration of electrodes placed, arises from an organized review of all noninvasive studies in a patient at a multidisciplinary surgical planning conference. Seizure symptomatology, scalp EEG findings, and MR imaging results are uniform components of an evaluation, and noninvasive functional localization studies such as ictal-SPECT, subtraction ictal-SPECT coregistered to MR imaging, MEG, and FDG-PET may be added all or in part. The relative contribution and role for these studies has recently been reviewed.27,55 Intracranial grid monitoring is also critically important in defining eloquent function in the adjacent brain. Intracranial electrodes are typically placed during large cran-iotomies.15,40 Extensive exposure of the brain via craniotomy allows subdural grids to be placed directly over the convexity of the brain (Fig. 1). Under a continuous wash of lactated Ringer irrigation, smaller strip electrodes may be gently slid into regions not directly exposed by craniotomy that require sampling. As a result, extensive coverage of the neocortex can be achieved (Fig. 2). The decision of exactly which grids, strips, and depths to use arises from a working relationship between the epileptologist and the epilepsy neurosurgeon. The epileptologist determines the optimum extent of coverage based on noninvasive localization studies and makes recommendations and requests about the grid and depth electrodes that are used. The neurosurgeon refines and adapts these recommendations with regard to safety and feasibility based upon training, prior surgical experience, or anatomical findings at surgery such as large draining veins or areas of focal arachnoiditis and adhesion. The wires from the grids typically exit separately from the craniotomy incision, and multiple precautions are usually incorporated to prevent or minimize cerebrospinal fluid leaks. A period of inpatient extraoperative monitoring ensues in which the clinically important seizure pattern is observed and captured on video EEG. Direct brain mapping through grid stimulation is often performed, particularly if the area implicated in epileptogenesis is proximal to areas believed or known to be eloquent.

Fig. 1.
Fig. 1.

Large craniotomies ensure adequate room to position grids to enable detailed mapping of epileptogenic cortex and adjacent eloquent regions. This photograph depicting a large craniotomy taken after bone removal and before dural opening in a child in whom extensive subdural grid investigation was to be undertaken.

Fig. 2.
Fig. 2.

Extensive coverage of the neocortex is often necessary for neocortical epilepsy (which overwhelmingly predominates in children), particularly when MR imaging is normal or discordant with EEG findings. In this photograph a child has undergone placement of extensive subdural electrodes including interhemispheric and subfrontal strips, subtemporal strips, temporal depth electrodes, and a large frontotemporal convexity grid. Gridbased mapping and resection enabled the patient to become seizure free.

Less commonly, extradural electrodes may be placed using bur holes. Sphenoidal electrodes may be placed percutaneously while the patient is under sedation and using a local anesthetic.11,42 Sphenoidal electrodes are less invasive and as such have lower risks of causing hemorrhage or infection.25,49 Depth electrodes are placed into the parenchyma of the brain and may be used alone or in conjunction with extensive subdural grid coverage.43,48 They may be placed using conventional frame-based stereotactic techniques (most commonly from an occipitotemporal approach to longitudinally sample the medial temporal lobe) or using frameless stereotactic techniques.10,35,48

After using monitoring and stimulation to determine eloquence in the adjacent brain, a grid map is developed that becomes the road map for the secondary operation (Fig. 3).29,39,51 At the time of the secondary operation the grid is exposed through the same surgical corridor and the epileptogenic region is defined, exposed, isolated, and resected while adjacent tissue is protected.23,45 Occasionally alternative techniques such as multiple subpial transections or subpial aspiration are undertaken if the epileptogenic region is also eloquent.5,9

Fig. 3.
Fig. 3.

Advances in coregistration software have allowed the creation of images that incorporate MR imaging and reflect the topography of the underlying cortex. Photographs courtesy of Hyunmi Kim, M.D.

Intracranial Electrode Placement Indications

Temporal Lobe Epilepsy

Temporal lobe epilepsy is the most common form of epilepsy that is treated surgically. The utilization of intracranial electrodes will vary between centers according to the experience of the surgeons with both noninvasive techniques for localization and their experience and confidence with intracranial recordings.7,8,10 For cases in which there is a clear MR imaging abnormality such as hippocampal sclerosis or atrophy, and there is concordant symptomatology for partial complex seizures and good lateralization on scalp EEG, intracranial recording is not necessary.10,12,50 If, however, there is discordance in data such that EEG suggests unilateral onset but MR imaging reveals structural changes bilaterally, then monitoring both temporal lobes invasively appears to be warranted. Similarly if EEG localizes poorly and non-specifically50,44 but MR imaging shows unilateral structural changes (atrophy or sclerosis), then monitoring with invasive electrodes is likely to be warranted.12,44 If only the symptomatology suggests mesial temporal onset but MR imaging and EEG are not supportive of this finding, then it is very unlikely that intracranial recordings will significantly contribute to surgical decision-making.12

The results of detailed neuropsychological studies may also affect the decision whether to use intracranial electrodes in TLE. There are two critical roles for neuropsychological tests in TLE. The first role is to aid in the determination as to whether ictal onset is bilateral or unilateral. This is particularly important when imaging results are normal. The second important role is to aid in the determination of whether temporal lobe involvement is primarily lateral (neocortical) or medial (limbic). A large verbal memory deficit in dominant-lobe TLE or a substantial disparity in verbal and nonverbal memory may suggest medial temporal lobe involvement and affect the extent of electrode placement, or may suggest a greater role for depth electrodes, which are better suited to monitor medial structures. In contrast, less verbal memory impairment may suggest a greater involvement of neocortical structures. This finding may warrant greater exploration using extensive grid and strip electrodes but may spare the patient the need for a large medial temporal resection and its attendant risk for verbal memory insult.

Additional contributions of neuropsychological assessment may include evaluation of coping (with the stresses of surgery and recovery) and evaluation of changes in abilities after surgery, yet these issues do not play as direct a role in the decision-making process surrounding the use of intracranial electrodes. Intracranial monitoring can facilitate identification of good candidates for a temporal lobe resection that spares potentially eloquent structures such as the hippocampus and parahippocampal gyrus. This issue is particularly important for dominant-hemisphere nonlesional TLE in patients with relatively preserved memory function preoperatively, because such patients are at greatest risk for postoperative verbal memory decline.

An important consideration in the surgical approach to temporal lobe seizures is whether the seizures are characteristic mesial temporal lobe seizures or whether they arise from the temporal neocortex.31 A propensity to lateral or midtemporal spikes on EEG or symptoms consisting of a complex visual or auditory aura in the symptomatology may be indicators of temporal neocortical disease.32,44 Magnetic resonance imaging findings supporting a temporal neocortical origin may include disordered gray-white architecture or focal areas of visible dysplasia.27 In such cases, invasive temporal lobe monitoring using small sub-dural grids and strips is important in confirming neocortical disease as well as for defining a rational extent of resection.44

Extratemporal Epilepsy

If localization-related seizures arise outside of the temporal region, then subdural grid monitoring is almost always needed in the absence of a clearly demonstrable lesion on MR imaging with concordant EEG.1,12,26,45 Even some lesional cases will be evaluated with intracranial electrodes because it has been clearly demonstrated that the region of epileptogenesis may extend well beyond the focal area of abnormality noted on MR imaging. Focal dysplasias and hamartomatous tumors such as dysembryoplastic neuroepithelial tumors and gangliogliomas are particularly inviting for more comprehensive evaluation, whereas tubers, hamartomas, and gliomas may be reasonably treated using a lesionectomy followed by a wait-and-see approach.34,38 A more extended discussion of specific indications in intracranial electrodes is available in several recent reviews.4,12,52–54

Limitations and Risks of Intracranial Electrodes

Although intracranial grids have provided an unparalleled opportunity to study the anatomy of the epileptic human brain, there are significant limitations and risks associated with their use.13,16,24,37,47 These limitations and risks include cost, patient discomfort, patient immobility, risks for infection and bleeding, aseptic meningitis, limited time in which to monitor the patient, need for staged neurosurgical interventions, and some inherent limitations as to the localization of the epileptogenic cortex.16,24,33 Twenty percent of the estimated 2 million Americans with epilepsy have medically intractable disease, and these patients account for more than 75% of the overall costs of epilepsy diagnosis and treatment.27 Patient discomfort can be considerable due to the size of the cranial incisions and the need for extensive muscle dissection during electrode implantation. Exiting wires can become caught if the patient moves and place painful traction directly on the dura.

Proper cortical sampling requires extensive placement of electrodes across the cortex, but large or confluent veins or dural venous lakes may present a surgical obstruction to proper and desired placement. The tearing of surface draining veins and consequent risk of severe hemorrhage or venous infarction is perhaps the most serious acute complication arising from use of subdural electrodes. Hemorrhages, however, can also arise in a more delayed and insidious fashion and are highly variable in their degree of clinical relevance. Table 1 outlines the reported incidences of infectious and hemorrhagic complications from 8 large case series reported within the last 15 years.

TABLE 1

Summary of complications arising from the use of intracranial electrodes in 8 large recently reported patient series*

Author & YearCenter LocationNo. of Patients% w/ EDH% w/ SDH% w/ TND% w/ CSF Leak% Rate of Infection% w/ Permanent Death /Disability
Johnston et al., 2006St. Louis, Missouri, US1120.83.31.62.40
Fountas and Smith, 2007Augusta, Georgia (MCG), US1851.61.1NDND1.11.1
Burneo et al., 2006London, Ontario, Canada11612NDND10
Hamer et al., 2002Cleveland Clinic, Ohio, US1872.5011ND12.5
Lee et al., 2000Asan, Seoul, South Korea5027.8NDND3.9ND
Onal et al., 2003HSC, Toronto, Canada35ND14ND209ND
Simon et al., 2003CHOP, Philadelphia, Pennsylvania, US6700ND320ND
Wiggins et al., 1999Henry Ford Hospital, Detroit, Michigan, US3830NDND5.7ND

*Asan = Asan Medical Center; CHOP = Children's Hospital of Philadelphia; CSF = cerebrospinal fluid; EDH = epidural hematoma; HSC = Hospital for Sick Children; MCG = Medical College of Georgia; ND = not discussed; SDH = subdural hematoma; TND = transient neurological deficit.

It is immediately evident that the incidence of complications varies considerably across these reports. There are a number of potential reasons for this variability. First, almost all of the series are retrospectively reported, which is a methodology notoriously inaccurate for its sensitivity. For example, some centers may perform postoperative CT scans at a greater frequency than others. Such a center would likely demonstrate greater sensitivity in the detection of asymptomatic hemorrhages. Other centers might routinely obtain cultures at the time intracranial electrodes are inserted. These centers might detect a higher rate of infection than those who utilize signs and symptoms of clinical infection to make the diagnosis. Furthermore, the number of patients at even the largest centers is small, which means that a small number of events can significantly impact the overall incidence rate. Several broad conclusions are evident, however. The incidence of hemorrhage in recent case series ranges from 0 to 14% and the incidence of infection ranges from 0 to 12%. As such, it appears reasonable to conclude that serious, potentially life-threatening hemorrhagic complications can and do occur, albeit at a low rate. Investigators at multiple centers allude to a learning curve and the importance of meticulous surgical technique and patient observation postoperatively to minimize the impact of these complications. Results are mixed as to whether prolonged monitoring and/or more electrodes are associated with higher risks of infection.16,24,40,56.

Perhaps the primary limitation to IC-EEG is that surface-based grid and strip electrodes best sample the surface cortex immediately on the convexity.29 Due to extensive sulci, approximately 60% of the cortex is below the surface. Deep regions of epileptogenic tissue may be difficult to localize because of the rapid spread of abnormal discharges. Due to the abundance of collateral projections found in neocortical tissue there is nearly immediate wide distribution of electrical activity from a deep epileptogenic region. The proper localization of such a focus may prove very challenging or impossible when only surface electrodes (subdural grids) are utilized, because the grid may detect a spread pattern rather than the primary region of ictal onset. Grid limitation in localizing epilepsy is further considered in later segments of this paper.

Recent Advances, Issues, and Controversies in the Use of Intracranial Electrodes

There have been essentially no substantive technical advances in intracranial electrode design in the last 10–15 years that have achieved widespread utilization in the epilepsy surgery community. Subdural grids are made of thin sheets of Silastic (medical grade silicone sheets) that have imbedded platinum electrodes at 1 cm intervals. Platinum is the preferred agent because it is the best-known conductor of electricity. These grids are available commercially from several manufacturers in North America (Ad-Tech Medical, PMT, and Integra) and a number of epilepsy centers use grids made in their own labs.2 Commercially available subdural grids come in a variety of shapes and configurations (Fig. 4). The largest widely available grid is an 8 × 8 configuration with the electrodes 1 cm apart. Other commonly used grid sizes are 4 × 8, 4 × 5, and 2 × 6. Strip electrodes typically employ a single row of electrodes with a variable number of contacts; examples include 1 × 4, 1 × 6, and 1 × 8 layouts. Other configurations include T-shaped grids and tapered grids (which are advocated by some groups for lateral temporal coverage). Most centers use commercially available grids because they have excellent performance profiles, are approved by the US Food and Drug Administration, and spare the infrastructure and resources necessary for grid manufacture on site. However, Backensto2 demonstrated a 62% cost savings when using grids created in-house compared with a commercially available product. They also cited the capability to individually customize grid design and configuration for an individual patient as a strong rationale supporting in-house manufacturing of subdural grids. Our group has utilized both in-house and commercially available products and have found both quite satisfactory. The ultimate choice of grid materials used at our center depends on surgeon preference.

Fig. 4.
Fig. 4.

Photograph demonstrating a partial range of the shapes and sizes of commercially available subdural grid, strip, and depth electrodes. Featured products are from PMT Corporation; however, very similar products are available from other manufacturers as well (see text).

Extradural electrode designs incorporate ball electrodes, bolts, pegs, and strips.46 Ross and colleagues46 described a percutaneous epidural screw electrode and Barnett et. al3 described a new peg-shaped electrode in a publication from 1990. There has otherwise been little technical change in the past 15 years. The primary reason why little effort has gone into electrode refinement appears to be that current electrodes provide good results and great strides have been made in amplifiers and EEG data acquisition systems, such that the overall process of IC-EEG is quite effective. Depth electrodes, sphenoidal electrodes, and foramen ovale electrodes are similarly available and have varied little recently in technical design from those used 20 years ago. Ives21 from the University of Western Ontario recently described a new silver/silver/chloride sphenoidal electrode that can be placed percutaneously in the subdermal space.

Evolution of Surgical Approaches: Technical and Conceptual Advances

The overwhelming majority of recent publications addressing surgical approaches for intracranial electrodes address the burgeoning field of deep brain stimulation rather than epilepsy. However, two major changes in surgical technique can be observed in the last 10–15 years. One change reflects technological advancement and the other represents an evolution in the surgical conceptual approach to a unique clinical problem. The major recent technological advance in the surgical approach to electrode placement involves the incorporation of frameless navigation systems into the surgical protocol. The second advance involves the role of multistaged epilepsy surgery.

Frameless navigation systems represent a real and significant advance in neurosurgery because they provide the surgeon real-time feedback and anatomical confirmation. Utilizing image fusion techniques, several different investigative groups have coregistered noninvasive functional imaging data such as MEG data or ictal-SPECT data onto the frameless platform. The practical result of this coregistration is that the surgeon receives real-time intraoperative feedback not only on anatomical information but also on the regions of the cortex that are implicated in epileptogenesis. This feedback can ensure that grids are optimally placed over the regions of brain most strongly implicated by noninvasive imaging and localization techniques (Fig. 5).

Fig. 5.
Fig. 5.

Intraoperative photograph demonstrating use of intraoperative MEG-guided frameless stereotactic grid insertion. Note that the surgeon at left is holding a pointer for the frameless navigation system and confirming localization using images on the center monitor. This monitor shows MR images projected onto the BrainLab platform onto which MEG dipole clusters have been coregistered. As a result there is real-time feedback between both anatomical and functional data and the exposed brain.

Otsubo and colleagues41 from the Hospital for Sick Children in Toronto, Canada first reported the utility of frameless stereotaxy with scalp EEG electrodes on 3D CT scans in 1995. Eight patients who underwent epilepsy surgery were evaluated. Standardized scalp electrode placements using the 10–20 standardized system were utilized and several patients also had sphenoidal electrodes placed. Three-dimensional CT scans were obtained and coregistered successfully with the scalp and sphenoidal electrodes. This process enabled colocalization of EEG anomalies with underlying brain anatomy and formed the conceptual framework for later studies from this group.

In 2004, Holowka and associates20 reported the utility of 3D reconstructed magnetic source images superimposed on the MR imaging-based ISG Wand Neuronavigation System in a series of 16 children undergoing epilepsy surgery. Interictal MEG data was superimposed on the ISG protocol MR imaging, resulting in real-time intraoperative capability to display dipole clusters on the exposed brain. Magnetoencephalography spike clusters were correlated with IC-EEG findings from subdural grids, and these results guided resection. Follow-up studies by Grondin et al.14 and Ochi and Otsubo39 extended the preliminary observations of the initial report and provided further experience and evidence to support the utility of these techniques.

Murphy and associates in 200436 reported the superiority of frameless navigation systems compared with conventional frame-based navigation systems for the placement of depth electrodes in a series of 13 patients undergoing depth electrode implantation (5 also had subdural grids placed concomitantly). These authors found that frameless navigation systems provided a useful projection of the planned trajectory that enabled them to avoid high-risk areas for hemorrhage such as the sylvian fissure. They also found that the frameless system eliminated the obstruction frequently present in conventional frame-based stereotactic systems. They found this system particularly useful when simultaneously placing a subdural grid.

The Comprehensive Epilepsy Surgery Service at the University of Alabama at Birmingham has utilized MEG-guided grid placement since 2003 in both adults and children. We have used both StealthStation image guidance (Sofamor Danek/Medtronic) and Brain Lab VectorVision (BrainLAB Corp.) systems and found them to be equally effective (Fig. 6). We concur with the conclusions of the Toronto group that these techniques are useful in the placement of the grids (to avoid edge-of-grid phenomena) as well as in the interpretation of the IC-EEG and planning of the resection. We favor using the EEG findings and MEG findings cooperatively to optimize the region of resection to include areas of tightly clustered dipoles and regions of abnormal ictal EEG activity (Fig. 7).

Fig. 6.
Fig. 6.

IScreen shot from the BrainLab-based neuronavigation platform onto which MEG dipoles have been coregistered. Dipoles can be clearly visualized and aid the surgeon both in placement of subdural electrodes as well as in planning the resection. In this particular case the dipoles arise in the occipital cortex.

Fig. 7.
Fig. 7.

Photograph of an intraoperative MEG-guided frameless navigation placement of a subdural grid. Note the use of the pointer to confirm the epicenter of the dipole clusters. Using this approach we have found grids to be well-centered and have encountered almost no “edge-of-grid” phenomena.

Effect of Advances in Noninvasive Imaging: Limitations to Using IC-EEG as the Gold Standard

As detailed above, the use of intracranial electrodes still represents the gold standard in localization of epileptogenic tissue. Yet there are substantial limitations to utilizing IC-EEG as the gold standard. Knowlton and colleagues29 have elucidated these shortcomings in a pair of reports emanating from a large prospective 5-year trial that sought to collect observational data to assess the role of MEG, FDG-PET, and ictal-SPECT in epilepsy surgery candidates. In this prospective trial, 265 patients were evaluated and 169 patients met the criteria of medically intractable epilepsy with nonlocalizing MR imaging findings or ambiguous EEG-MR imaging correlation. Patients were studied using conventional 1.5T (or 3T) MR imaging and scalp video EEG as well as a variable combination of MEG, ictal-SPECT, and FDG-PET. The patient series was large and broadly selected, which potentially increases the applicability of the results. Sensitivity, specificity, and positive predictive value were predicted for each imaging test in terms of its capacity for sublobar localization using IC-EEG. Several important findings emerged from this study. Magnetic source imaging consistently showed sensitivity, specificity, and positive predictive values higher than FDG-PET or ictal-SPECT. The greatest sensitivity was demonstrated when FDG-PET findings were combined with MEG values. Yet the most important conclusion emphasized by the authors pertained to the limitation of utilizing IC-EEG as the gold standard for localization. In a significant number of cases, the imaging test ultimately proved correct in localization but was considered a false negative result because of lack of concordance with IC-EEG. Seventy-two patients had seizures recorded with IC-EEG, yet the seizures in 17% of the patients could not be localized using implanted electrodes. This percentage is high for a gold standard, and most seizures were believed to arise as a result of an ictal focus deep within a sulcus. Electroencephalography clues to this disparity included nonfocal desynchronization and apparent attenuation. When assessed against surgical outcomes, imaging specificity was noted to rise for all modalities. An accompanying paper that assesses the same patient group from the perspective of surgical outcome draws similar conclusions.28 The aim of the study was to determine whether at this time and development any of the commonly applied functional imaging tests for localization could replace or augment IC-EEG. The authors concluded that modest concordance rates between noninvasive imaging studies preclude the replacement of IC-EEG, and that noninvasive studies have a very important function in augmenting IC-EEG. The authors cited cases of nonlocalizing IC-EEG in patients who became seizure-free following resection based upon imaging with attenuated or desynchronized EEG. Finally, each of the studies was found to make an independent contribution to localization and surgical decision making if conclusively positive (unequivocally localized).28

Collectively this information emphasizes the limitations of IC-EEG as the gold standard for localization. Perhaps more importantly it represents an initial and important step in the development of the capability to recognize where noninvasive studies may augment and ultimately reduce the need for IC-EEG. As technological progress allows reduction in signal-to-noise ratios, a better understanding of MEG spike characteristics, and better estimates of the putative onset of ictal activity, it is likely that these less invasive, less costly, and less risk-inherent alternatives will gradually eclipse the preeminence currently held by intracranial electrodes in the localization of elusive epilepsy.

Conclusions

The potential role for meaningful surgical intervention for the treatment of medically refractory, localization-related epilepsy has never been as great as it is now. Yet the future holds greater promise. It appears likely that there will be continued refinement in intracranial electrode design and implementation. With Bluetooth and lay person satellite navigation as common as they currently are, it does not seem unbelievable to imagine wireless grids in the foreseeable future. Perhaps these intracranial electrodes could be implanted for a prolonged duration of monitoring that may even span into the outpatient realm. Advances in nanotechnology are likely to substantially refine the precision of intracranial monitoring and may ultimately allow prolonged and highly focal monitoring. At present there is minimal reported application of nanotechnology to the field of invasive monitoring. It appears virtually certain that noninvasive localization imaging will become more refined and the roles of noninvasive tests and intracranial electrodes will continue to evolve. It appears most likely that their relationship will remain an augmentative and cooperative one for the immediate future.

Acknowledgment

The authors thank Derek M. Bonner for his help in photographing the surgical procedures.

Disclaimer

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

References

  • 1

    Alarcón GValentín AWatt CSelway RPLacruz MEElwes RD: Is it worth pursuing surgery for epilepsy in patients with normal neuroimaging?. J Neurol Neurosurg Psychiatry 77:4744802006

  • 2

    Backensto EM: Patient-specific platinum intracranial electrodes as a diagnostic tool in the surgical treatment of the epilepsies. J Clin Eng 19:57621994

  • 3

    Barnett GHBurgess RCAwad IASkipper GJEdwards CRLuders H: Epidural peg electrodes for the presurgical evaluation of intractable epilepsy. Neurosurgery 27:1131151990

  • 4

    Bauman JAFeoli ERomanelli PDoyle WKDevinsky OWeiner HL: Multistage epilepsy surgery: safety, efficacy, and utility of a novel approach in pediatric extratemporal epilepsy. Neurosurgery 56:3183342005

  • 5

    Blount JPLangburt WOtsubo HChitoku SOchi AWeiss S: Multiple subpial transections in the treatment of pediatric epilepsy. J Neurosurg 100:2 Suppl1181242004

  • 6

    Burneo JGSteven DAMcLachlan RSParrent AG: Morbidity associated with the use of intracranial electrodes for epilepsy surgery. Can J Neurol Sci 33:2232272006

  • 7

    Cohen-Gadol AABradley CCWilliamson AKim JHWesterveld MDuckrow RB: Normal magnetic resonance imaging and medial temporal lobe epilepsy: the clinical syndrome of paradoxical temporal lobe epilepsy. J Neurosurg 102:9029092005

  • 8

    Cohen-Gadol AASpencer DD: Use of an anteromedial subdural strip electrode in the evaluation of medial temporal lobe epilepsy. Technical note. J Neurosurg 99:9219232003

  • 9

    Devinsky ORomanelli POrbach DPacia SDoyle W: Surgical treatment of multifocal epilepsy involving eloquent cortex. Epilepsia 44:7187232003

  • 10

    Dubeau FMcLachlan RS: Invasive electrographic recording techniques in temporal lobe epilepsy. Can J Neurol Sci 27:1 SupplS29S34S50S222000

  • 11

    Engel J JrHenry TRRisinger MWMazziotta JCSutherling WWLevesque MF: Presurgical evaluation for partial epilepsy: relative contributions of chronic depth-electrode recordings versus FDG-PET and scalp-sphenoidal ictal EEG. Neurology 40:167016771990

  • 12

    Faught EBlount JClinical neurophysiology III: intracranial electrodes. Wheless JWillmore LJBrumback RA: Advanced Epilepsy Hamilton, OntarioBC Decker[In press]2008

  • 13

    Fountas KNSmith JR: Subdural electrode-associated complications: a 20-year experience. Stereotact Funct Neurosurg 85:2642722007

  • 14

    Grondin RChuang SOtsubo HHolowka SSnead OC IIIRaybaud C: The role of magnetoencephalography in pediatric epilepsy surgery. Childs Nerv Syst 22:7797852006

  • 15

    Hader WJMackay MOtsubo HChitoku SWeiss SBecker L: Cortical dysplastic lesions in children with intractable epilepsy: role of complete resection. J Neurosurg 100:2 Suppl1101172004

  • 16

    Hamer HMMorris HHMascha EJKarafa MTBingaman WEBej MD: Complications of invasive video-EEG monitoring with subdural grid electrodes. Neurology 58:971032002

  • 17

    Handler MLaoprasert P: Outcome after aggressive surgery for pediatric neocortical epilepsy. J Neurosurg Pediatrics 1:A3512008. (Abstract)

  • 18

    Harvey ASCross JHShinnar SMathern BW: ILAE Pediatric Epilepsy Surgery Survey Taskforce: Defining the spectrum of international practice in pediatric epilepsy surgery patients. Epilepsia 49:1461552008

  • 19

    Henry TRRoss DASchuh LADrury I: Indications and outcome of ictal recording with intracerebral and subdural electrodes in refractory complex partial seizures. J Clin Neurophysiol 16:4264381999

  • 20

    Holowka SAOtsubo HIida KPang ESharma RHunjan A: Three-dimensionally reconstructed magnetic source imaging and neuronavigation in pediatric epilepsy: technical note. Neurosurgery 55:12262004

  • 21

    Ives JR: New chronic EEG electrode for critical/intensive care unit monitoring. J Clin Neurophysiol 22:1191232005

  • 22

    Jayakar P: Invasive EEG monitoring in children: when, where, and what?. J Clin Neurophysiol 16:4084181999

  • 23

    Jayakar PDuchowny MResnick TJ: Subdural monitoring in the evaluation of children for epilepsy surgery. J Child Neurol 9:2 Suppl61661994

  • 24

    Johnston JM JrMangano FTOjemann JGPark TSTrevathan ESmyth MD: Complications of invasive subdural electrode monitoring at St. Louis Children's Hospital, 1994–2005. J Neurosurg 105:5 Suppl3433472006

  • 25

    Kissani NAlarcon GDad MBinnie CDPolkey CE: Sensitivity of recordings at sphenoidal electrode site for detecting seizure onset: evidence from scalp, superficial and deep foramen ovale recordings. Clin Neurophysiol 112:2322402001

  • 26

    Kloss SPieper TPannek HHolthausen HTuxhorn I: Epilepsy surgery in children with focal cortical dysplasia (FCD): results of long-term seizure outcome. Neuropediatrics 33:21262002

  • 27

    Knowlton RC: Multimodality imaging in partial epilepsies. Curr Opin Neurol 17:1651722004

  • 28

    Knowlton RCElgavish RABartolucci AOjha BLimdi NBlount J: Functional imaging II: prediction of epilepsy surgery outcome. Ann Neurol [epub ahead of print]2008

  • 29

    Knowlton RCElgavish RHowell JBlount JBurneo JGFaught E: Magnetic source imaging versus intracranial electroencephalogram in epilepsy surgery: a prospective study. Ann Neurol 59:8358422006

  • 30

    Knowlton RCElgavish RALimdi NBartolucci AOjha BBlount J: Functional imaging: I. Relative predictive value of intracranial electroencephalography. Ann Neurol [epub ahead of print]2008

  • 31

    Kutsy RLFarrell DFOjemann GA: Ictal patterns of neocortical seizures monitored with intracranial electrodes: correlation with surgical outcome. Epilepsia 40:2572661999

  • 32

    Lee SASpencer DDSpencer SS: Intracranial EEG seizure-onset patterns in neocortical epilepsy. Epilepsia 41:2973072000

  • 33

    Lee WSLee JKLee SAKang JKKo TS: Complications and results of subdural grid electrode implantation in epilepsy surgery. Surg Neurol 54:3463512000

  • 34

    Minkin KKlein OMancini JLena G: Surgical strategies and seizure control in pediatric patients with dysembryoplastic neuroepithelial tumors: a single-institution experience. J Neurosurg Pediatrics 1:2062102008

  • 35

    Murphy MAO'Brien TJCook MJ: Insertion of depth electrodes with or without subdural grids using frameless stereotactic guidance systems—technique and outcome. Br J Neurosurg 16:1191252002

  • 36

    Murphy MAO'Brien TJMorris KCook MJ: Multimodality image-guided surgery for the treatment of medically refractory epilepsy. J Neurosurg 100:4524622004

  • 37

    Musleh WYassari RHecox KKohrman MChico MFrim D: Low incidence of subdural grid-related complications in prolonged pediatric EEG monitoring. Pediatr Neurosurg 42:2842872006

  • 38

    Nolan MASakuta RChuang NOtsubo HRutka JTSnead OC III: Dysembryoplastic neuroepithelial tumors in childhood: long-term outcome and prognostic features. Neurology 62:227022762004

  • 39

    Ochi AOtsubo H: Magnetoencephalography-guided epilepsy surgery for children with intractable focal epilepsy: SickKids experience. Int J Psychophysiol 68:1041102008

  • 40

    Onal COtsubo HAraki TChitoku SOchi AWeiss S: Complications of invasive subdural grid monitoring in children with epilepsy. J Neurosurg 98:101710262003

  • 41

    Otsubo HHwang PAHunjan AArmstrong DHolowka SDrake JM: Use of frameless stereotaxy with location of electroencephalographic electrodes on three-dimensional computed tomographic images in epilepsy surgery. J Clin Neurophysiol 12:3633711995

  • 42

    Pacia SVJung WJDevinsky O: Localization of mesial temporal lobe seizures with sphenoidal electrodes. J Clin Neurophysiol 15:2562611998

  • 43

    Pondal-Sordo MDiosy DTéllez-Zenteno JFSahjpaul RWiebe S: Usefulness of intracranial EEG in the decision process for epilepsy surgery. Epilepsy Res 74:1761822007

  • 44

    Prasad APacia SVVazquez BDoyle WKDevinsky O: Extent of ictal origin in mesial temporal sclerosis patients monitored with subdural intracranial electrodes predicts outcome. J Clin Neurophysiol 20:2432482003

  • 45

    Roberts DWJobst BCSiegel AMLewis PJDarcey TMThadani VM: Investigation of extra-temporal epilepsy. Stereotact Funct Neurosurg 77:2162182001

  • 46

    Ross DAHenry TRDickinson LD: A percutaneous epidural screw electrode for intracranial electroencephalogram recordings. Neurosurgery 33:3323341993

  • 47

    Simon SLTelfeian ADuhaime AC: Complications of invasive monitoring used in intractable pediatric epilepsy. Pediatr Neurosurg 38:47522003

  • 48

    Spencer SSSpencer DDWilliamson PDMattson RH: The localizing value of depth electroencephalography in 32 patients with refractory epilepsy. Ann Neurol 12:2482531982

  • 49

    Sperling MRGuina L: The necessity for sphenoidal electrodes in the presurgical evaluation of temporal lobe epilepsy: pro position. J Clin Neurophysiol 20:2993042003

  • 50

    Vossler DGKraemer DLHaltiner AMRostad SWKjos BODavis BJ: Intracranial EEG in temporal lobe epilepsy: location of seizure onset relates to degree of hippocampal pathology. Epilepsia 45:4975032004

  • 51

    Wang YAgarwal RNguyen DDomocos VGotman J: Intracranial electrode visualization in invasive pre-surgical Evaluation for Epilepsy. Conf Proc IEEE Eng Med Biol Soc 1:9529552005

  • 52

    Weiner HL: Tuberous sclerosis and multiple tubers: localizing the epileptogenic zone. Epilepsia 45:4 Suppl41422004

  • 53

    Weiner HLCarlson CRidgway EBZaroff CMMiles DLaJoie J: Epilepsy surgery in young children with tuberous sclerosis: results of a novel approach. Pediatrics 117:149415022006

  • 54

    Weiner HLFerraris NLaJoie JMiles DDevinsky O: Epilepsy surgery for children with tuberous sclerosis complex. J Child Neurol 19:6876892004

  • 55

    Wheless JWWillmore LJBreier JIKataki MSmith JrKing DW: A comparison of magnetoencephalography, MRI, and V-EEG in patients evaluated for epilepsy surgery. Epilepsia 40:9319411999

  • 56

    Wiggins GCElisevich KSmith BJ: Morbidity and infection in combined subdural grid and strip electrode investigation for intractable epilepsy. Epilepsy Res 37:73801999

  • 57

    Zumsteg DWieser HG: Presurgical evaluation: current role of invasive EEG. Epilepsia 41:3 SupplS55S602000

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Article Information

Address correspondence to: Jeffrey P. Blount, M.D., ACC 400, 1600 7th Avenue South, Birmingham, Alabama 35233. email:

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Large craniotomies ensure adequate room to position grids to enable detailed mapping of epileptogenic cortex and adjacent eloquent regions. This photograph depicting a large craniotomy taken after bone removal and before dural opening in a child in whom extensive subdural grid investigation was to be undertaken.

  • View in gallery

    Extensive coverage of the neocortex is often necessary for neocortical epilepsy (which overwhelmingly predominates in children), particularly when MR imaging is normal or discordant with EEG findings. In this photograph a child has undergone placement of extensive subdural electrodes including interhemispheric and subfrontal strips, subtemporal strips, temporal depth electrodes, and a large frontotemporal convexity grid. Gridbased mapping and resection enabled the patient to become seizure free.

  • View in gallery

    Advances in coregistration software have allowed the creation of images that incorporate MR imaging and reflect the topography of the underlying cortex. Photographs courtesy of Hyunmi Kim, M.D.

  • View in gallery

    Photograph demonstrating a partial range of the shapes and sizes of commercially available subdural grid, strip, and depth electrodes. Featured products are from PMT Corporation; however, very similar products are available from other manufacturers as well (see text).

  • View in gallery

    Intraoperative photograph demonstrating use of intraoperative MEG-guided frameless stereotactic grid insertion. Note that the surgeon at left is holding a pointer for the frameless navigation system and confirming localization using images on the center monitor. This monitor shows MR images projected onto the BrainLab platform onto which MEG dipole clusters have been coregistered. As a result there is real-time feedback between both anatomical and functional data and the exposed brain.

  • View in gallery

    IScreen shot from the BrainLab-based neuronavigation platform onto which MEG dipoles have been coregistered. Dipoles can be clearly visualized and aid the surgeon both in placement of subdural electrodes as well as in planning the resection. In this particular case the dipoles arise in the occipital cortex.

  • View in gallery

    Photograph of an intraoperative MEG-guided frameless navigation placement of a subdural grid. Note the use of the pointer to confirm the epicenter of the dipole clusters. Using this approach we have found grids to be well-centered and have encountered almost no “edge-of-grid” phenomena.

References

1

Alarcón GValentín AWatt CSelway RPLacruz MEElwes RD: Is it worth pursuing surgery for epilepsy in patients with normal neuroimaging?. J Neurol Neurosurg Psychiatry 77:4744802006

2

Backensto EM: Patient-specific platinum intracranial electrodes as a diagnostic tool in the surgical treatment of the epilepsies. J Clin Eng 19:57621994

3

Barnett GHBurgess RCAwad IASkipper GJEdwards CRLuders H: Epidural peg electrodes for the presurgical evaluation of intractable epilepsy. Neurosurgery 27:1131151990

4

Bauman JAFeoli ERomanelli PDoyle WKDevinsky OWeiner HL: Multistage epilepsy surgery: safety, efficacy, and utility of a novel approach in pediatric extratemporal epilepsy. Neurosurgery 56:3183342005

5

Blount JPLangburt WOtsubo HChitoku SOchi AWeiss S: Multiple subpial transections in the treatment of pediatric epilepsy. J Neurosurg 100:2 Suppl1181242004

6

Burneo JGSteven DAMcLachlan RSParrent AG: Morbidity associated with the use of intracranial electrodes for epilepsy surgery. Can J Neurol Sci 33:2232272006

7

Cohen-Gadol AABradley CCWilliamson AKim JHWesterveld MDuckrow RB: Normal magnetic resonance imaging and medial temporal lobe epilepsy: the clinical syndrome of paradoxical temporal lobe epilepsy. J Neurosurg 102:9029092005

8

Cohen-Gadol AASpencer DD: Use of an anteromedial subdural strip electrode in the evaluation of medial temporal lobe epilepsy. Technical note. J Neurosurg 99:9219232003

9

Devinsky ORomanelli POrbach DPacia SDoyle W: Surgical treatment of multifocal epilepsy involving eloquent cortex. Epilepsia 44:7187232003

10

Dubeau FMcLachlan RS: Invasive electrographic recording techniques in temporal lobe epilepsy. Can J Neurol Sci 27:1 SupplS29S34S50S222000

11

Engel J JrHenry TRRisinger MWMazziotta JCSutherling WWLevesque MF: Presurgical evaluation for partial epilepsy: relative contributions of chronic depth-electrode recordings versus FDG-PET and scalp-sphenoidal ictal EEG. Neurology 40:167016771990

12

Faught EBlount JClinical neurophysiology III: intracranial electrodes. Wheless JWillmore LJBrumback RA: Advanced Epilepsy Hamilton, OntarioBC Decker[In press]2008

13

Fountas KNSmith JR: Subdural electrode-associated complications: a 20-year experience. Stereotact Funct Neurosurg 85:2642722007

14

Grondin RChuang SOtsubo HHolowka SSnead OC IIIRaybaud C: The role of magnetoencephalography in pediatric epilepsy surgery. Childs Nerv Syst 22:7797852006

15

Hader WJMackay MOtsubo HChitoku SWeiss SBecker L: Cortical dysplastic lesions in children with intractable epilepsy: role of complete resection. J Neurosurg 100:2 Suppl1101172004

16

Hamer HMMorris HHMascha EJKarafa MTBingaman WEBej MD: Complications of invasive video-EEG monitoring with subdural grid electrodes. Neurology 58:971032002

17

Handler MLaoprasert P: Outcome after aggressive surgery for pediatric neocortical epilepsy. J Neurosurg Pediatrics 1:A3512008. (Abstract)

18

Harvey ASCross JHShinnar SMathern BW: ILAE Pediatric Epilepsy Surgery Survey Taskforce: Defining the spectrum of international practice in pediatric epilepsy surgery patients. Epilepsia 49:1461552008

19

Henry TRRoss DASchuh LADrury I: Indications and outcome of ictal recording with intracerebral and subdural electrodes in refractory complex partial seizures. J Clin Neurophysiol 16:4264381999

20

Holowka SAOtsubo HIida KPang ESharma RHunjan A: Three-dimensionally reconstructed magnetic source imaging and neuronavigation in pediatric epilepsy: technical note. Neurosurgery 55:12262004

21

Ives JR: New chronic EEG electrode for critical/intensive care unit monitoring. J Clin Neurophysiol 22:1191232005

22

Jayakar P: Invasive EEG monitoring in children: when, where, and what?. J Clin Neurophysiol 16:4084181999

23

Jayakar PDuchowny MResnick TJ: Subdural monitoring in the evaluation of children for epilepsy surgery. J Child Neurol 9:2 Suppl61661994

24

Johnston JM JrMangano FTOjemann JGPark TSTrevathan ESmyth MD: Complications of invasive subdural electrode monitoring at St. Louis Children's Hospital, 1994–2005. J Neurosurg 105:5 Suppl3433472006

25

Kissani NAlarcon GDad MBinnie CDPolkey CE: Sensitivity of recordings at sphenoidal electrode site for detecting seizure onset: evidence from scalp, superficial and deep foramen ovale recordings. Clin Neurophysiol 112:2322402001

26

Kloss SPieper TPannek HHolthausen HTuxhorn I: Epilepsy surgery in children with focal cortical dysplasia (FCD): results of long-term seizure outcome. Neuropediatrics 33:21262002

27

Knowlton RC: Multimodality imaging in partial epilepsies. Curr Opin Neurol 17:1651722004

28

Knowlton RCElgavish RABartolucci AOjha BLimdi NBlount J: Functional imaging II: prediction of epilepsy surgery outcome. Ann Neurol [epub ahead of print]2008

29

Knowlton RCElgavish RHowell JBlount JBurneo JGFaught E: Magnetic source imaging versus intracranial electroencephalogram in epilepsy surgery: a prospective study. Ann Neurol 59:8358422006

30

Knowlton RCElgavish RALimdi NBartolucci AOjha BBlount J: Functional imaging: I. Relative predictive value of intracranial electroencephalography. Ann Neurol [epub ahead of print]2008

31

Kutsy RLFarrell DFOjemann GA: Ictal patterns of neocortical seizures monitored with intracranial electrodes: correlation with surgical outcome. Epilepsia 40:2572661999

32

Lee SASpencer DDSpencer SS: Intracranial EEG seizure-onset patterns in neocortical epilepsy. Epilepsia 41:2973072000

33

Lee WSLee JKLee SAKang JKKo TS: Complications and results of subdural grid electrode implantation in epilepsy surgery. Surg Neurol 54:3463512000

34

Minkin KKlein OMancini JLena G: Surgical strategies and seizure control in pediatric patients with dysembryoplastic neuroepithelial tumors: a single-institution experience. J Neurosurg Pediatrics 1:2062102008

35

Murphy MAO'Brien TJCook MJ: Insertion of depth electrodes with or without subdural grids using frameless stereotactic guidance systems—technique and outcome. Br J Neurosurg 16:1191252002

36

Murphy MAO'Brien TJMorris KCook MJ: Multimodality image-guided surgery for the treatment of medically refractory epilepsy. J Neurosurg 100:4524622004

37

Musleh WYassari RHecox KKohrman MChico MFrim D: Low incidence of subdural grid-related complications in prolonged pediatric EEG monitoring. Pediatr Neurosurg 42:2842872006

38

Nolan MASakuta RChuang NOtsubo HRutka JTSnead OC III: Dysembryoplastic neuroepithelial tumors in childhood: long-term outcome and prognostic features. Neurology 62:227022762004

39

Ochi AOtsubo H: Magnetoencephalography-guided epilepsy surgery for children with intractable focal epilepsy: SickKids experience. Int J Psychophysiol 68:1041102008

40

Onal COtsubo HAraki TChitoku SOchi AWeiss S: Complications of invasive subdural grid monitoring in children with epilepsy. J Neurosurg 98:101710262003

41

Otsubo HHwang PAHunjan AArmstrong DHolowka SDrake JM: Use of frameless stereotaxy with location of electroencephalographic electrodes on three-dimensional computed tomographic images in epilepsy surgery. J Clin Neurophysiol 12:3633711995

42

Pacia SVJung WJDevinsky O: Localization of mesial temporal lobe seizures with sphenoidal electrodes. J Clin Neurophysiol 15:2562611998

43

Pondal-Sordo MDiosy DTéllez-Zenteno JFSahjpaul RWiebe S: Usefulness of intracranial EEG in the decision process for epilepsy surgery. Epilepsy Res 74:1761822007

44

Prasad APacia SVVazquez BDoyle WKDevinsky O: Extent of ictal origin in mesial temporal sclerosis patients monitored with subdural intracranial electrodes predicts outcome. J Clin Neurophysiol 20:2432482003

45

Roberts DWJobst BCSiegel AMLewis PJDarcey TMThadani VM: Investigation of extra-temporal epilepsy. Stereotact Funct Neurosurg 77:2162182001

46

Ross DAHenry TRDickinson LD: A percutaneous epidural screw electrode for intracranial electroencephalogram recordings. Neurosurgery 33:3323341993

47

Simon SLTelfeian ADuhaime AC: Complications of invasive monitoring used in intractable pediatric epilepsy. Pediatr Neurosurg 38:47522003

48

Spencer SSSpencer DDWilliamson PDMattson RH: The localizing value of depth electroencephalography in 32 patients with refractory epilepsy. Ann Neurol 12:2482531982

49

Sperling MRGuina L: The necessity for sphenoidal electrodes in the presurgical evaluation of temporal lobe epilepsy: pro position. J Clin Neurophysiol 20:2993042003

50

Vossler DGKraemer DLHaltiner AMRostad SWKjos BODavis BJ: Intracranial EEG in temporal lobe epilepsy: location of seizure onset relates to degree of hippocampal pathology. Epilepsia 45:4975032004

51

Wang YAgarwal RNguyen DDomocos VGotman J: Intracranial electrode visualization in invasive pre-surgical Evaluation for Epilepsy. Conf Proc IEEE Eng Med Biol Soc 1:9529552005

52

Weiner HL: Tuberous sclerosis and multiple tubers: localizing the epileptogenic zone. Epilepsia 45:4 Suppl41422004

53

Weiner HLCarlson CRidgway EBZaroff CMMiles DLaJoie J: Epilepsy surgery in young children with tuberous sclerosis: results of a novel approach. Pediatrics 117:149415022006

54

Weiner HLFerraris NLaJoie JMiles DDevinsky O: Epilepsy surgery for children with tuberous sclerosis complex. J Child Neurol 19:6876892004

55

Wheless JWWillmore LJBreier JIKataki MSmith JrKing DW: A comparison of magnetoencephalography, MRI, and V-EEG in patients evaluated for epilepsy surgery. Epilepsia 40:9319411999

56

Wiggins GCElisevich KSmith BJ: Morbidity and infection in combined subdural grid and strip electrode investigation for intractable epilepsy. Epilepsy Res 37:73801999

57

Zumsteg DWieser HG: Presurgical evaluation: current role of invasive EEG. Epilepsia 41:3 SupplS55S602000

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