Stereoelectroencephalography in the setting of a previously implanted responsive neural stimulation device: illustrative case

Dorian M Kusyk Departments of Neurosurgery,

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Nicholas Blaney College of Medicine, Drexel University, Philadelphia, Pennsylvania

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Timothy Quezada Neurology, and Neurosciences Institute, Allegheny Health Network, Pittsburgh, Pennsylvania; and

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Alexander C Whiting Departments of Neurosurgery,

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BACKGROUND

Responsive neural stimulation (RNS) is a relatively novel procedure for drug-resistant epilepsy, which involves implantation of a device into the skull and brain. As more devices are implanted, there may be an increasing need to perform intracranial electrocorticography in implant patients with persistent seizures. Given the device location, imaging difficulties with implanted devices, and other technical hurdles, stereoelectroencephalography (SEEG) could be especially challenging. The authors describe the first reported SEEG investigation in a patient with an RNS device, highlighting the technical challenges and clinical data ascertained.

OBSERVATIONS

A 41-year-old male with drug-resistant epilepsy presented several years after a local surgeon had placed an RNS device with two electrodes in the bilateral parieto-occipital lobes. Because of inadequate seizure control, the patient was offered a repeat SEEG investigation to characterize his epilepsy better. Although more technically challenging than a traditional SEEG implantation, the SEEG investigation was successfully performed, which led to a confirmation of bilateral hippocampal seizure onset. The patient underwent repositioning of his RNS leads with a significant decrease in his seizure frequency.

LESSONS

Concurrent implantation of SEEG electrodes in a functioning RNS device can be safely performed and can augment our understanding of a patient’s seizures.

ABBREVIATIONS

CT = computed tomography; DBS = deep brain stimulation; EMU = epilepsy monitoring unit; MPRAGE = magnetization-prepared rapid acquisition gradient echo; MRI = magnetic resonance imaging; RNS = responsive neural stimulation; SEEG = stereoelectroencephalography

BACKGROUND

Responsive neural stimulation (RNS) is a relatively novel procedure for drug-resistant epilepsy, which involves implantation of a device into the skull and brain. As more devices are implanted, there may be an increasing need to perform intracranial electrocorticography in implant patients with persistent seizures. Given the device location, imaging difficulties with implanted devices, and other technical hurdles, stereoelectroencephalography (SEEG) could be especially challenging. The authors describe the first reported SEEG investigation in a patient with an RNS device, highlighting the technical challenges and clinical data ascertained.

OBSERVATIONS

A 41-year-old male with drug-resistant epilepsy presented several years after a local surgeon had placed an RNS device with two electrodes in the bilateral parieto-occipital lobes. Because of inadequate seizure control, the patient was offered a repeat SEEG investigation to characterize his epilepsy better. Although more technically challenging than a traditional SEEG implantation, the SEEG investigation was successfully performed, which led to a confirmation of bilateral hippocampal seizure onset. The patient underwent repositioning of his RNS leads with a significant decrease in his seizure frequency.

LESSONS

Concurrent implantation of SEEG electrodes in a functioning RNS device can be safely performed and can augment our understanding of a patient’s seizures.

ABBREVIATIONS

CT = computed tomography; DBS = deep brain stimulation; EMU = epilepsy monitoring unit; MPRAGE = magnetization-prepared rapid acquisition gradient echo; MRI = magnetic resonance imaging; RNS = responsive neural stimulation; SEEG = stereoelectroencephalography

Responsive neural stimulation (RNS; NeuroPace Inc.) is a closed-loop neuromodulation device approved by the Food and Drug Administration in 2013 for the treatment of drug-resistant partial-onset seizures arising from up to two foci.1 RNS has been shown to be a safe and effective treatment for drug-resistant epilepsy, commonly defined as continued seizures after adequate trials of at least two antiseizure medications, with particular value in patients with bitemporal epilepsy or an epilepsy network involving eloquent cortex.2–5 However, a sizable proportion of patients are considered nonresponders and continue to have a significant seizure burden after implantation and programming.6 As the RNS implant volume continues to increase, the amount of nonresponders will also continue to grow, and many of these patients may benefit from an additional intracranial electrocorticography evaluation, in particular stereoelectroencephalography (SEEG).

SEEG is a safe, minimally invasive technique utilizing intracerebral electrodes to identify and map the epileptogenic zone.2,4 Many high-volume centers rely on robotic navigation utilizing high-quality thin-cut computed tomography (CT) angiography and contrast magnetic resonance imaging (MRI) to avoid potentially catastrophic blood vessel damage during placement of the electrodes.3 SEEG implantation in patients with a previously implanted RNS device represent a myriad of challenges and management concerns including procuring high-quality images with the implanted pulse generator, working through prior scar tissue and around the device, increasing the infection risk of the device, adequately covering the epileptogenic zone while avoiding the device, and avoiding short-circuiting the device during the procedure.

Here we discuss a patient with an RNS device implanted by a local surgeon, which resulted in bilateral electrode leads placed within the patient’s irritative zone but potentially not within the seizure-onset zone. Although the patient saw some improvement in his seizures after receiving the implant, he was interested in pursuing further surgery in the hope of a better outcome because of his continued seizure burden. To the best of our knowledge, this is the first report of SEEG implantation for phase 2 monitoring in a patient with an RNS implant. We present this case as an opportunity to discuss the technical pearls and pitfalls of performing this procedure and to demonstrate the data that can be used to guide management after implantation.

Illustrative Case

This case report was written in accordance with the Surgical Case Report guidelines.7

Presentation and Progression

A 41-year-old male presented to our clinic with poorly controlled seizures. He reported seizures that had begun in childhood and had failed several antiseizure medications including topiramate, zonisamide, and phenytoin. At the time of presentation, the patient had been prescribed levetiracetam and Tegretol. His RNS implant had been placed in 2017 by a different surgeon after a phase 2 intracranial investigation consisting of two depth electrodes in the left temporal region, one depth electrode in the right temporal region, and a subdural grid in the left temporal region. After identifying occasional right temporal interictal spikes and seizures with a left temporal onset, an RNS device was implanted with electrodes in the bilateral parieto-occipital lobes, which may have corresponded to an irritative zone (Fig. 1A and B). The electrode contacts did not significantly involve the hippocampus or amygdala on either side. Although the electrodes did not have the more common bihippocampal placement, the patient did report a slight decrease in seizure frequency and severity since the RNS operation, and device interrogation revealed bilateral activation over 1,000 times a day. The patient did believe that the RNS had been successful in reducing his seizures, but he continued to have a significant seizure burden, with multiple generalized tonic-clonic seizures per year; thus, he presented to our combined clinic to discuss further surgical options.

FIG. 1
FIG. 1

Preoperative imaging. Head CT demonstrating prior RNS leads. The left lead terminates in the interior temporo-occipital lobe (A) and the right lead terminates in the parieto-occipital lobe (B). Coronal T2-weighted MRI sequence (C) showing possible left mesial temporal sclerosis.

On discussion with the patient and a multidisciplinary epilepsy conference, the patient was evaluated for solutions to his refractory epilepsy. Repeat brain MRI demonstrated a small left-sided middle fossa arachnoid cyst and left-sided hippocampal sclerosis associated with atrophy, known from previously obtained radiological reports (Fig. 1C). A repeat phase 1 with the RNS deactivated revealed focal-onset impaired awareness seizures arising from the left temporal lobe with significant interictal activity from the right. Multiple options were considered and discussed with the patient including left anterior temporal lobectomy, left selective laser amygdalohippocampectomy, repositioning of the RNS electrodes into the hippocampi bilaterally, and SEEG. Because the patient did not appear to have undergone a comprehensive intracranial evaluation previously and it was unclear if he truly had independent bilateral seizure onset zones, the decision was made to proceed with SEEG with the RNS in place to definitively characterize his epilepsy.

Intervention

Preoperative planning was performed on brain MRI with contrast and preoperative CT angiography with thin-cut slices. NeuroPace has published MRI guidelines for the RNS system, which includes specific MRI-compatible model numbers, patient eligibility criteria, and scanner specifications.8 In particular, the patient’s RNS must not be at end of service and should be placed in the MRI mode. The patient should be afebrile because elevated body temperatures could theoretically increase the risk of tissue heating. The MRI system itself should be a 1.5-T, horizontal field, closed-bore system with a spatial field gradient ≤30 T/m and a gradient slew rate ≤200 T/m/s per axis. In our case, we performed the studies on a Siemens Aera 1.5 running the XA30 software, obtaining magnetization-prepared rapid acquisition gradient echo (MPRAGE) precontrast, T2 space, and MPRAGE postcontrast sequences with a total run time under 25 minutes with a transmit/receive head coil for additional signal quality. The preoperative CT angiography with thin-cut slices was performed in the usual fashion and merged with the brain MRI with contrast.

Electrode trajectories were planned with the proprietary ROSA software, with the primary hypothesis of left temporal epilepsy, a secondary hypothesis of right temporal onset, and an additional hypothesis of left frontal and left insular epilepsy. Although our group traditionally implants orthogonal electrodes, care was taken with windowing on the CT angiography to avoid transgressing any of the wires or the generator, which required a few oblique trajectories. Care was taken to keep the bolts a reasonable distance away from the RNS components to avoid potential infection seeding. We were able to implant electrodes in all the anatomical regions of interest while avoiding the generator. As expected, there was pronounced artifact from the generator site; however, windowing helped with the visualization.

In the preoperative area, the RNS was deactivated for the procedure. In the operating room, all wires, along with the pulse generator, were studied on the preoperative CT scan and marked out on the head. The patient was then secured in a supine position with a Leksell stereotactic head frame, with care taken to avoid the delineated RNS device and wires (Fig. 2A). The ROSA robot (Zimmer Biomet) was connected to the frame, and laser face registration was used to locate the patient in stereotactic space. In this case, the laser facial registration allowed us to avoid fusing with an intraoperative CT, which may have been difficult to merge because of the extensive metal artifact, particularly pronounced given the reduced quality of the intraoperative CT scanner as compared to the preoperative CT angiography. The prior incision, the generator, and the existing wires were once again marked out as an additional failsafe to make sure none of the electrode trajectories would injure the existing hardware (Fig. 2B). The two right electrodes were placed first as the most straightforward trajectories. The left electrodes were placed in sequence from posterior to anterior to leave the electrodes closest to the arachnoid cyst last and to prevent brain shift from any cerebrospinal fluid egress. No electrocautery was used to open the dura through the procedure due to the RNS device to avoid any errant current from damaging the implanted generator. Once the electrodes were tested for corrected impedances and confirmed with fluoroscopy (Fig. 2C), the patient was awakened and taken to the epilepsy monitoring unit (EMU) for phase 2 monitoring. Thin-cut CT scanning was performed, which showed accurate placement of the electrodes and no obvious complications. The patient was maintained on prophylactic intravenous antibiotics given the quality of his scalp and multiple prior surgeries.

FIG. 2
FIG. 2

A: Intraoperative photographs of patient positioning. Note the Leksell frame is positioned in such a way as to avoid the RNS implantable pulse generator (IPG) and its associated wires. B: Intraoperative photograph showing the RNS incision, the IPG, and wires marked out. C: Intraoperative fluoroscopy image with confirmation of bilateral SEEG implantation with prior RNS leads visible medially (white arrows). D: Intraoperative fluoroscopy image confirming repositioned RNS leads.

Outcome

The patient underwent 9 days of SEEG recordings in the EMU. During that time, he had four focal impaired awareness seizures. The first seizure emanated from the right hippocampus, and the following three emanated from the left hippocampus. The right hippocampal seizure involved the amygdala from the onset with early spread to the left anterior insula, followed by the left orbital frontal and prefrontal opercular region, before spreading to the left amygdalohippocampal apparatus. The left hippocampal onset seizures remained entirely confined to the left hemisphere, clearly starting as low-voltage fast activity in the hippocampus, followed by rapid spread throughout the left temporal lobe and anterior insula. The interictal record demonstrated frequent left hippocampal discharges and occasional discharges from the bilateral amygdala, the right hippocampus, and the left entorhinal cortex.

Based on phase 2 testing, the patient was offered a revision of his RNS system, with placement of bilateral hippocampal electrodes (Fig. 2D). The procedure was performed on a separate admission without complication. The patient had one seizure in the immediate postoperative period, and in the 5 months since initial programming the patient has had a significant reduction in seizure frequency with no noted clinical seizures. Of note, his RNS electrocorticography review has demonstrated multiple episodes of hippocampal activity aborted by stimulation. In the most recent month, the patient had an average of 1,707 detections daily, with approximately 90% of them coming from the left hippocampal leads. He had no sign of infection at the most recent follow-up.

Of note, the RNS system remained active during the phase 2 investigation, and it consistently identified seizures approximately 2 minutes after seizure onset on the SEEG and delivered stimulation. The SEEG data stream and the RNS data stream were synchronized via a time stamp to compare electrocorticography data directly. Figure 3 shows an example of this finding: the SEEG recording showed a left hippocampal seizure onset at approximately 9:00:26 am, but the long episode recording from the RNS device showed seizure activity in the left lead at approximately 9:02:32 am, over 2 minutes from seizure onset. This particular seizure had clinically resolved in the temporal SEEG electrodes prior to detection by the RNS device.

FIG. 3
FIG. 3

Example of phase 2 recordings. A: SEEG with recorded seizure onsets from the left hippocampal electrode at approximately 9:00 am. B: Long episode recording from the RNS device. Seizure onset in the left RNS lead is at approximately 09:02:10 am.

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Observations

The decision to pursue a comprehensive SEEG evaluation in this patient was not made lightly. There was considerable discussion in the multidisciplinary conference about whether the SEEG could be performed safely and what course to pursue. Options considered included immediately replacing the RNS electrodes with new electrodes in the bilateral amygdaloid-hippocampal structures, removing the RNS device while leaving a cranioplasty in place and then performing repeat SEEG testing, or leaving the RNS device in place while performing SEEG testing.

Repeat SEEG testing was desired, in both the hope that the patient may have a predominately unilateral seizure onset, which would make him a resection/ablation candidate, and the fear that the prolonged epilepsy course may have kindled additional seizure-onset zones. Prior groups have reported performing a laser ablation in the setting of an RNS device.9 Performing SEEG through a cranioplasty has been previously reported and would have been a safe option.10 However, the patient was particularly opposed to removing the system because it would prolong his seizure evaluation with another surgery, and he did receive partial benefit from the device with its existing configuration. Ultimately, our group pursued SEEG while preserving the current RNS system, as described above.

The reasons for RNS failure are not well documented and are likely multifaceted. Many patients may find unsatisfactory results because of the inherent nature of their epilepsy networks. However, looking at the sister technology of deep brain stimulation (DBS), we note that national lead revision rates can be up to 15% to 30%, and one of the many reasons for revision is lead malposition.11,12 Although there are differences between RNS and DBS in terms of the technology used and the pathophysiology treated, it is likely that as RNS becomes more common, RNS lead revision rates will follow. Furthermore, revision RNS surgery can be complicated by the fact that there are often more potential targets for stimulation than for movement disorders, depending on the patient’s network. Thus, repositioning the RNS leads may require repeat phase 2 testing, including repeat SEEG to better characterize the patient’s seizure network.

The phase 2 EMU stay with an active RNS device provides some insight into the mechanism of stimulation in seizure networks. The RNS system has been shown to be flexible with its implantation strategy. Although the initial design was conceptualized with its electrodes in the seizure-onset zone, increasingly centers are implanting the device with leads in the thalamus, downstream of the seizure-onset zone, with similar efficacy.13 In a similar vein, the patient’s initial RNS strategy was downstream of the seizure-onset zone; the device was able to identify the partial seizures with a delay, suggesting they were within the network, and the patient did report subjective improvement in seizure quality and quantity after the initial implant. However, it is unclear if the triggered stimulation limited the seizure propagation or if it resolved with a natural neurophysiological mechanism. Our patient’s leads were repositioned to be within his seizure-onset zone, and as of the last follow-up, he has seen a drastic improvement in his seizure count, potentially suggesting that electrodes closer to the seizure-onset zone perform better. Additionally, having the SEEG electrodes and RNS electrodes in place and recording simultaneously have the ability to provide unique real-time information about how well the RNS is functioning at identifying and treating seizures.

Lessons

As RNS becomes a more common procedure for patients with epilepsy, it is increasingly likely that patients with these implants will present to comprehensive epilepsy centers for further workup of treatment-resistant epilepsy. The above case report suggests that SEEG in these patients can be performed safely and provides necessary information to guide further therapy. As a single patient, this case report cannot speak with any confidence toward the mechanism of RNS in epilepsy networks. Furthermore, the patient’s follow-up was less than a year, and his long-term seizure outcome has yet to be determined. Although this report demonstrates the safety and offers some technical pearls regarding SEEG implantation with concurrent RNS, a compilation of multiple cases through a national or international registry would better elucidate the risk profile of performing SEEG around an RNS implant.

Acknowledgments

We thank Thomas Schmude for assistance obtaining optimal MRI scans with the RNS implant in place and Samantha Ryan for assistance developing the protocols mentioned.

Author Contributions

Conception and design: Whiting, Kusyk. Acquisition of data: Whiting, Kusyk, Quezada. Analysis and interpretation of data: Whiting, Kusyk, Quezada. Drafting the article: Whiting, Kusyk, Blaney. Critically revising the article: Whiting, Kusyk. Reviewed submitted version of manuscript: Whiting, Kusyk, Quezada. Approved the final version of the manuscript on behalf of all authors: Whiting. Statistical analysis: Whiting. Administrative/technical/material support: Whiting. Study supervision: Whiting.

Supplemental Information

Previous Presentations

An abstract of this work was presented at the 2023 American Epilepsy Society Meeting, December 1–5, 2023, in Orlando, Florida.

References

  • 1

    Food and Drug Administration. Premarket Approval (PMA). Premarket Approval (PMA): Neuropace RNS System. Published September 25, 2023. Accessed September 26, 2023. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpma/pma.cfm?id=P100026

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Geller EB, Skarpaas TL, Gross RE, et al. Brain-responsive neurostimulation in patients with medically intractable mesial temporal lobe epilepsy. Epilepsia. 2017;58(6):9941004.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Jobst BC, Kapur R, Barkley GL, et al. Brain-responsive neurostimulation in patients with medically intractable seizures arising from eloquent and other neocortical areas. Epilepsia. 2017;58(6):10051014.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Nair DR, Laxer KD, Weber PB, et al. Nine-year prospective efficacy and safety of brain-responsive neurostimulation for focal epilepsy. Neurology. 2020;95(9):e1244e1256.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Razavi B, Rao VR, Lin C, et al. Real-world experience with direct brain-responsive neurostimulation for focal onset seizures. Epilepsia. 2020;61(8):17491757.

  • 6

    Kusyk DM, Meinert J, Stabingas KC, Yin Y, Whiting AC. Systematic review and meta-analysis of responsive neurostimulation in epilepsy. World Neurosurg. 2022;167:e70e78.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Agha RA, Franchi T, Sohrabi C, Mathew G, Kerwan A. The SCARE 2020 Guideline: Updating Consensus Surgical CAse REport (SCARE) Guidelines. Int J Surg. 2020;84:226230.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Neuropace I. MRI Guidelines for the RNS® System. MRI Guidelines for the RNS® System. Published 2020. Accessed September 26, 2023. https://www.neuropace.com/wp-content/uploads/2021/02/neuropace-rns-system-mri-guidelines.pdf

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Luu CP, Kotloski RJ, Lake WB. The effective use of laser ablation to treat mesial temporal lobe epilepsy in the setting of implanted responsive neurostimulation. Oper Neurosurg (Hagerstown). 2023;24(1):e16e22.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Mallela AN, Abou-Al-Shaar H, Nayar GM, Luy DD, Barot N, González-Martínez JA. Stereotactic electroencephalography implantation through nonautologous cranioplasty: proof of concept. Oper Neurosurg (Hagerstown). 2021;21(4):258264.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Rolston JD, Englot DJ, Starr PA, Larson PS. An unexpectedly high rate of revisions and removals in deep brain stimulation surgery: analysis of multiple databases. Parkinsonism Relat Disord. 2016;33:7277.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Falowski SM, Bakay RAE. Revision surgery of deep brain stimulation leads. Neuromodulation. 2016;19(5):443450.

  • 13

    Roa JA, Abramova M, Fields M, et al. Responsive neurostimulation of the thalamus for the treatment of refractory epilepsy. Front Hum Neurosci. 2022;16:926337.

  • Collapse
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  • FIG. 1

    Preoperative imaging. Head CT demonstrating prior RNS leads. The left lead terminates in the interior temporo-occipital lobe (A) and the right lead terminates in the parieto-occipital lobe (B). Coronal T2-weighted MRI sequence (C) showing possible left mesial temporal sclerosis.

  • FIG. 2

    A: Intraoperative photographs of patient positioning. Note the Leksell frame is positioned in such a way as to avoid the RNS implantable pulse generator (IPG) and its associated wires. B: Intraoperative photograph showing the RNS incision, the IPG, and wires marked out. C: Intraoperative fluoroscopy image with confirmation of bilateral SEEG implantation with prior RNS leads visible medially (white arrows). D: Intraoperative fluoroscopy image confirming repositioned RNS leads.

  • FIG. 3

    Example of phase 2 recordings. A: SEEG with recorded seizure onsets from the left hippocampal electrode at approximately 9:00 am. B: Long episode recording from the RNS device. Seizure onset in the left RNS lead is at approximately 09:02:10 am.

  • 1

    Food and Drug Administration. Premarket Approval (PMA). Premarket Approval (PMA): Neuropace RNS System. Published September 25, 2023. Accessed September 26, 2023. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpma/pma.cfm?id=P100026

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Geller EB, Skarpaas TL, Gross RE, et al. Brain-responsive neurostimulation in patients with medically intractable mesial temporal lobe epilepsy. Epilepsia. 2017;58(6):9941004.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Jobst BC, Kapur R, Barkley GL, et al. Brain-responsive neurostimulation in patients with medically intractable seizures arising from eloquent and other neocortical areas. Epilepsia. 2017;58(6):10051014.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Nair DR, Laxer KD, Weber PB, et al. Nine-year prospective efficacy and safety of brain-responsive neurostimulation for focal epilepsy. Neurology. 2020;95(9):e1244e1256.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Razavi B, Rao VR, Lin C, et al. Real-world experience with direct brain-responsive neurostimulation for focal onset seizures. Epilepsia. 2020;61(8):17491757.

  • 6

    Kusyk DM, Meinert J, Stabingas KC, Yin Y, Whiting AC. Systematic review and meta-analysis of responsive neurostimulation in epilepsy. World Neurosurg. 2022;167:e70e78.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Agha RA, Franchi T, Sohrabi C, Mathew G, Kerwan A. The SCARE 2020 Guideline: Updating Consensus Surgical CAse REport (SCARE) Guidelines. Int J Surg. 2020;84:226230.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Neuropace I. MRI Guidelines for the RNS® System. MRI Guidelines for the RNS® System. Published 2020. Accessed September 26, 2023. https://www.neuropace.com/wp-content/uploads/2021/02/neuropace-rns-system-mri-guidelines.pdf

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Luu CP, Kotloski RJ, Lake WB. The effective use of laser ablation to treat mesial temporal lobe epilepsy in the setting of implanted responsive neurostimulation. Oper Neurosurg (Hagerstown). 2023;24(1):e16e22.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Mallela AN, Abou-Al-Shaar H, Nayar GM, Luy DD, Barot N, González-Martínez JA. Stereotactic electroencephalography implantation through nonautologous cranioplasty: proof of concept. Oper Neurosurg (Hagerstown). 2021;21(4):258264.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Rolston JD, Englot DJ, Starr PA, Larson PS. An unexpectedly high rate of revisions and removals in deep brain stimulation surgery: analysis of multiple databases. Parkinsonism Relat Disord. 2016;33:7277.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Falowski SM, Bakay RAE. Revision surgery of deep brain stimulation leads. Neuromodulation. 2016;19(5):443450.

  • 13

    Roa JA, Abramova M, Fields M, et al. Responsive neurostimulation of the thalamus for the treatment of refractory epilepsy. Front Hum Neurosci. 2022;16:926337.

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