Invasive monitoring: stereoelectroencephalography (sEEG) versus subdural electrode (SDE) versus hybrid evaluation





Introduction


Invasive monitoring can play a crucial role in the localization of seizure foci in children with drug-resistant epilepsy . Invasive monitoring is indicated in cases of focal epilepsy in which the noninvasive phase 1 evaluation does not definitively localize the seizure focus, but leads to testable hypotheses about the localization of the seizure focus based on semiology, anatomy, and electroclinical findings . Various methods exist for invasive monitoring including subdural electrode (SDE) recordings , stereoelectroencephalography (sEEG) , and also hybrid variations of SDE that include placement of depth electrodes . These approaches are associated with different risks and benefits, which has led to some debate about which of these invasive monitoring approaches is ideal in different contexts.


In this chapter, we will review these three different approaches and discuss the advantages and disadvantages of each approach. The technique for each approach is described briefly along with indications and contra-indications. Since most of the evidence for outcomes for these different methods is from comparative systematic reviews and metaanalyses of observational data , we review the outcomes reported by these studies in a single section and then discuss the implications of these findings. Finally, recommendations are provided based on this available evidence.


Subdural electrode recordings


Implantation of subdural grid and strip electrodes was the mainstay of pediatric invasive monitoring in North America for many years . The purpose of any invasive monitoring investigation is to delineate the epileptogenic zone (EZ) when noninvasive evaluation fails to do so. SDE achieves this via the higher spatial resolution of direct epicortical recordings . There are different variations on the SDE technique, which include the “hybrid” methods that will be discussed separately.


Subdural electrode recording technique


In general, SDE involves a unilateral, or in some cases bilateral , craniotomy for implantation of the subdural grid and or strip electrodes. Surgery is performed under general anesthesia. Typically, a broad exposure of the brain is performed via a hemicraniotomy to facilitate the placement of the grid and strip electrodes. The dura is opened in a standard fashion and electrodes are placed based on the preoperative hypothesis about the localization of the seizure focus and the need for functional mapping (see Fig. 4.1A and D ). The dura is then closed with a dural graft to minimize the mass effect from electrodes. Grid electrodes are embedded in silastic and often spaced at standard intervals. The silastic grid is secured to the surrounding dura prior to closure to secure the electrode in position. Dura is typically closed in a watertight fashion. After dural closure, the bone flap is replaced. There is considerable variation in the technique for bone fixation, though some groups utilize bent cranial plates to generate a hinge that expands the intracranial volume to minimize the mass effect from the electrodes . Electrodes are typically tunneled toward the vertex to minimize CSF leak with a margin of at least 1 cm from the incision edge to minimize CSF leak and risk of infection.




Figure 4.1


Summary of X-ray ( top panel ) and photo depiction ( bottom panel ) of the different invasive monitoring methods described in this chapter. This includes SDE ( left , A/D), sEEG ( middle , B/E), and hybrid ( right , C/F).


It is important to note that there can be considerable variation in the types of electrodes used and the position of electrodes implanted. For example, variation in electrode spacing ranges from relatively sparse recordings to high-density arrays (see Fig. 4.1D and F for contrast in interelectrode spacing). Also, arrays can be customized for particular brain regions, such as the temporal pole, which is typically difficult to cover with high-density grid electrodes . Additionally, coverage of brain regions beyond the convexity such as the parahippocampal gyrus or interhemispheric fissure can be recorded by using specific exposure and implantation methods .


Indications and contra-indications


The indication for invasive monitoring with SDE is to delineate the EZ when noninvasive tests cannot do this with sufficient accuracy . An alternative indication, particularly in pediatrics, is for functional mapping in a child that would not tolerate an awake craniotomy .


Contra-indications in pediatrics are relative and include (1) a child who may not safely tolerate prolonged invasive monitoring in the epilepsy monitoring unit, (2) inadequate preimplantation hypothesis, and (3) medical comorbidities that would preclude safe invasive monitoring. It is crucial that invasive monitoring of any type is only performed in the setting of well-defined preimplantation hypotheses that would lead to potential surgical resection.


Relative advantages and disadvantages


The advantages and disadvantages of SDE are summarized in Table 4.1 . A major advantage of the SDE technique is that no electrodes are implanted into the brain parenchyma, which may have certain safety advantages (e.g., the risk of intraparenchymal hemorrhage is low). Additionally, the interpretation of SDE can be intuitive given that the spatial conformation of grid electrodes directly maps to the cortical surface, unlike intracerebral recordings whereby electrodes cross sulci are recorded from spatially distinct regions from a single electrode trajectory. Further, though several studies and practices by several groups demonstrate the feasibility of functional stimulation mapping with sEEG , this mapping may be more intuitive with SDE given that adjacent electrode contacts are adjacent to each other on the brain surface .



Table 4.1

Comparison of the subdural electrode, stereoelectroencephalography, and hybrid invasive monitoring methods.
























Modality Surgical technique Advantages Disadvantages
Subdural electrodes Large craniotomy with implantation of grid and strip surface electrodes.


  • Coverage of the cortical surface is easily achieved.



  • Interpretation of recordings is intuitive as spatial location of electrodes corresponds to position on brain surface.



  • Motor and language mapping can be performed with dense cortical surface coverage.




  • Large craniotomy is required.



  • If hypothesis is nonlateralized, bilateral craniotomies are required.



  • Complication rate is higher than sEEG.



  • Mesial brain regions may require special exposure for coverage.



  • Sulcal and certain deep brain regions cannot be covered.

Stereo-EEG Stereotactic or robot-assisted stereotactic percutaneous implantation of intracerebral electrodes.


  • Does not require a craniotomy. Electrodes with percutaneous stereotactic technique.



  • Records from both superficial and deep brain regions, including sulcal banks.



  • Bilateral recordings does not require bilateral craniotomies



  • Lower risk of morbidity and mortality relative to SDE.



  • Advantageous when laterality is not established.




  • Does not provide dense cortical surface coverage, which may make motor and language mapping more difficult.



  • Requires specialized equipment and stereotactic expertise.



  • Interpretation of recordings is less intuitive because a single electrode records from multiple distant brain regions.

Hybrid Large craniotomy with implantation of both grid, strip, and depth electrodes.


  • Allows the dense cortical surface recordings of SDE with simultaneous depth recordings.



  • Has advantages of SDE with simultaneous depth recordings.



  • Motor and language mapping can be performed with dense cortical surface coverage.




  • Large craniotomy is required.



  • If hypothesis is nonlateralized, bilateral craniotomies are required.



  • Complication rate is higher than sEEG and potentially SDE.



  • Depth electrode placement is probably not as accurate as sEEG since electrodes are placed via open craniotomy.



Disadvantages include the need for a craniotomy and in the case of a bilateral preimplantation hypothesis, bilateral craniotomies. Additionally, special approaches are necessary for recording from mesial regions including the basal temporal, temporal polar, parahippocampal, and interhemispheric regions. Most important, sulcal regions, which make up two-thirds of the cerebral cortex, cannot be recorded using this method.


Stereoelectroencephalography


sEEG was developed in Paris decades ago and has been the mainstay of invasive monitoring in France since that time . In recent years, possibly due to advances in surgical robotics and stereotactic neurosurgery, sEEG has become popularized throughout North America . It is important to recognize that sEEG is a comprehensive methodology for localization of the EZ, rather than a simple electrode implantation method . The “stereo” in sEEG means 3D not stereotactic as is often depicted in the literature. sEEG starts with careful analysis of seizure semiology, electroclinical correlation, and anatomical considerations to arrive at testable anatomo-electro-clinical hypotheses about seizure localization . Electrode implantation is then tailored to test these hypotheses for each individual patient.


Stereoelectroencephalography technique


The technique for sEEG implantation in children is described in detail elsewhere . The preoperative phase of the procedure is crucial for planning electrode trajectories that maximize coverage of gray matter that test the predetermined anatomo-electro-clinical hypotheses while avoiding vascular structures. To this end, preoperative imaging is obtained typically in the form of a thin-cut postcontrast MPRAGE T1 MRI and some form of vascular imaging. Contrast enhancement can diminish gray matter definition on the MPRAGE T1, but this can be improved through custom optimization of the imaging parameters. The French sEEG guidelines recommend CT angiogram, digital subtraction angiography, or postcontrast Mr imaging for vascular imaging. The structural (MPRAGE Mr) and vascular imaging are merged and electrode trajectories are then planned. It is our view that if more than 20 electrodes are necessary, then further preoperative testing is necessary to reach a more finite preimplantation hypothesis. Electrode implantations should not be “fishing expeditions.”


In the operating room, the patient is placed under general anesthesia with head fixation in a stereotactic frame. A stereotactic technique that is either frame-based or frameless can be performed. Our center utilizes a ROSA robot with bone fiducials for electrode implantation. The skin and bone can be opened with an awl and the bone and dura opened with the drill . Guidance anchors are placed, a stylet pass is made to the target, and the electrode is then inserted and secured to the anchor bolt. Once all of the electrodes are placed, a secure dressing is applied and the patient is taken to the epilepsy monitoring unit after recovering in the perioperative unit.


Indications and contra-indications


The indication for sEEG is to test anatomo-electro-clinical hypotheses generated from the preimplantation phase 1 evaluation. This hypothesis must not be able to be tested without invasive recordings. Unlike SDE, sEEG is not used extensively in pediatrics for language or motor mapping when seizure localization is not needed, though we have used it for this purpose at our center with good results.


Contra-indications are relative and include (1) lack of a well-established hypothesis that can be tested with a reasonable number of electrodes, (2) bone thickness <2 mm (the exact number is debated), and (3) medical or behavioral comorbidities that would prevent safe chronic recordings in the EMU.


Relative advantages and disadvantages


A main advantage of sEEG is the ability to test anatomo-electro-clinical hypotheses in three dimensions with electrodes placed to record from both deep and superficial brain structures. Additionally, sEEG electrodes are implanted without a craniotomy. It is important to note that often a craniotomy is still required for subsequent treatment once the EZ is identified. There’s evidence that sEEG is associated with decreased pain compared to craniotomy methods and decreased utilization of pain medicine .


A disadvantage of sEEG relative to SDE or hybrid methods is that there is relatively sparse spacing between electrode contacts that are aligned across an electrode shaft. Due to this configuration of recording and stimulation electrodes, language and motor mapping may be more difficult or at least less intuitive. For teams new to sEEG, this electrode configuration can also make the interpretation of sEEG recordings a challenge as electrodes that are close to each other on an electrode shaft can record from distinct brain regions. Additionally, sEEG implantation is best performed with specialized equipment, including a stereotactic frame, stereotactic robot, and specialized imaging protocols. The upfront cost of this equipment may be prohibitive for some hospitals depending on resource availability.


Hybrid approach: subdural and depth electrodes (hybrid)


Hybrid approach technique


The hybrid approach combines craniotomy-based SDE with depth electrode implantation to target deep brain structures not typically covered by SDE . The rationale is to have the benefits of dense cortical surface coverage while achieving some coverage from deep structures important in epilepsy evaluation such as the amygdala, hippocampus, entorhinal cortex, cingulate, and/or insula . The technique is like SDE in which a large craniotomy is performed under general anesthesia for placement of grid and strip electrodes. After the craniotomy, depth electrodes are implanted using either an image guidance system or a stereotactic frame through an open craniotomy. Robotic assistance can also be utilized for electrode placement. Electrode tunneling and closure are similar to the SDE technique.


Indications and contra-indications


The indications and contra-indications for this procedure are similar to SDE. Again, the indication for this procedure is a testable hypothesis about the localization of the EZ based on noninvasive phase 1 studies. When a mesial EZ is suspected, but an SDE approach is preferred, then a hybrid approach could be indicated to record from mesial structures. In other words, if the hippocampus, amygdala, or insula, for example, are implicated in the EZ, then a hybrid approach could be indicated to record from those deep structures in the setting of an SDE craniotomy.


Relative advantages and disadvantages


The primary advantage of the hybrid approach is the simultaneous advantage of dense surface SDE recordings and selected depth recordings to record from deeper structures. The complication rate of this approach is probably higher, though, in existing comparative metaanalyses, the hybrid approach is often grouped together with SDE . Though theoretically an unlimited number of depth electrodes could be placed, these should be selected carefully to maximize the benefit of each electrode. Further, placement of depth electrodes is probably less accurate than sEEG given that the electrodes are implanted through an open craniotomy that allows for brain shift. Similar to SDE, an additional disadvantage is the necessity of bilateral craniotomies if the focus is not lateralized.


Reported outcomes of each technique


Both before and after the popularization of sEEG throughout North America, retrospective observational studies have reported the outcomes of both sEEG, SDE, and hybrid approaches . These data have been reviewed extensively in systematic reviews and metaanalyses . A comparison of SDE and sEEG suggests that SDE is associated with a higher rate of invasive investigations leading to craniotomy and intervention. However, of patients who did undergo invasive monitoring informed resection, sEEG was associated with a higher rate of ultimate seizure freedom. Available systematic reviews show that sEEG is associated with lower rates of both morbidity and mortality . While the mortality associated with invasive monitoring is low, systematic reviews suggest it is about twice as high for SDE . The complication rate is higher for SDE and hybrid approaches compared to sEEG, but as pointed out by Lee et al. and others, the nature of complications for SDE and sEEG are different and comparing rates alone may not be sufficient. For example, since sEEG is associated with more intraparenchymal hemorrhage than SDE, it may be that sEEG is more likely to be associated with permanent neurologic deficits compared to SDE. Ultimately, all of these invasive monitoring procedures overall have acceptable and comparable safety and effectiveness profiles based on available evidence.


Discussion


We have just examined evidence comparing the safety and effectiveness of available invasive monitoring techniques. The conclusion is that the safety and effectiveness profile of each of these procedures is quite similar. Indeed, our recent decision analysis comparing SDE and sEEG shows that the effectiveness probability for each of these procedures leading to seizure freedom without a complication is virtually the same . We used this model also to compare the cost-effectiveness (CE) of SDE and sEEG strategies showing that the CE of each of these strategies (with assumptions based on available cost data) are similar . As we have discussed above, the start-up costs of developing an sEEG program are considerable compared to SDE. Given the available evidence, a reasonable approach is for programs to focus most on whatever modality they have the most experience with. For most invasive monitoring indications, this is probably a reasonable approach.


Epilepsy surgery is a rapidly changing field with novel interventions, such as responsive neurostimulation and deep brain stimulation for children with drug-resistant epilepsy . These techniques are effective at controlling different forms of drug-resistant epilepsy and have shown incredible promise, but to be clear, far more evidence is needed. However, there has begun to be a trend toward planning invasive monitoring investigations to facilitate neuromodulation in addition to potential resection strategies . For this reason, it is possible that the indications for sEEG relative to SDE will change in the coming years. For example, if recordings of the centromedian nucleus or the pulvinar are needed to determine the best target for a chronically implanted depth electrode, then sEEG has clear advantages over a craniotomy with SDE or a hybrid approach.


Evidence-based recommendations


Currently, there is insufficient evidence to recommend one invasive monitoring modality over another. However, it is unclear that the superiority of one method over another should drive decision-making as each of these methods is considerably different. Additionally, the safety and effectiveness of the invasive monitoring approach are highly dependent on the expertise and experience of each team. Therefore, there is room for SDE, sEEG, and hybrid approaches in pediatric epilepsy surgery and the decision to use each modality should be tailored to each patient’s indication and needs, along with the expertise of the center.



References

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Feb 15, 2025 | Posted by in NEUROSURGERY | Comments Off on Invasive monitoring: stereoelectroencephalography (sEEG) versus subdural electrode (SDE) versus hybrid evaluation

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