Radiofrequency ablation during stereoelectroencephalography: from diagnostic tool to therapeutic intervention. Illustrative case

Demitre Serletis Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, Ohio

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Juan Bulacio Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, Ohio

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Justin Bingaman Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, Ohio

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Elham Abushanab Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, Ohio

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Stephen P. Harasimchuk Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, Ohio

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Richard Rammo Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, Ohio

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Silvia Neme-Mercante Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, Ohio

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William Bingaman Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, Ohio

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BACKGROUND

Radiofrequency thermocoagulation (RFTC) during intracranial stereoelectroencephalography (sEEG) was first described as a safe technique for creating lesions of epileptic foci in 2004. Since that time, the method has been applied as a diagnostic and/or palliative intervention. Although widely practiced in European epilepsy surgical programs, the technique has not been popularized in the United States given the lack of Food and Drug Administration (FDA)–approved technologies permitting safe usage of in situ sEEG electrodes for this purpose.

OBSERVATIONS

The authors present a case report of a young female patient with refractory left neocortical temporal lobe epilepsy undergoing sEEG electrode implantation, who underwent sEEG-guided RFTC via a stereotactic temperature-sensing pallidotomy probe. Although used as a diagnostic step in her workup, the patient has remained seizure-free for nearly 18 months.

LESSONS

The use of in situ sEEG electrodes for RFTC remains limited in the United States. In this context, this case highlights a safe alternative and temporizing approach to performing diagnostic sEEG-guided RFTC, using a temperature-sensing pallidotomy probe to create small, precise stereotactic lesions. The authors caution careful consideration of this technique as a temporary work-around solution while also highlighting the rising need for new FDA-approved technologies for safe RFTC through in situ temperature-sensing sEEG electrodes.

ABBREVIATIONS

CT = computed tomography; EEG = electroencephalography; FDA = Food and Drug Administration; MRI = magnetic resonance imaging; PMC = patient management conference; RF = radiofrequency; RFTC = radiofrequency thermocoagulation; sEEG = stereoelectroencephalography

BACKGROUND

Radiofrequency thermocoagulation (RFTC) during intracranial stereoelectroencephalography (sEEG) was first described as a safe technique for creating lesions of epileptic foci in 2004. Since that time, the method has been applied as a diagnostic and/or palliative intervention. Although widely practiced in European epilepsy surgical programs, the technique has not been popularized in the United States given the lack of Food and Drug Administration (FDA)–approved technologies permitting safe usage of in situ sEEG electrodes for this purpose.

OBSERVATIONS

The authors present a case report of a young female patient with refractory left neocortical temporal lobe epilepsy undergoing sEEG electrode implantation, who underwent sEEG-guided RFTC via a stereotactic temperature-sensing pallidotomy probe. Although used as a diagnostic step in her workup, the patient has remained seizure-free for nearly 18 months.

LESSONS

The use of in situ sEEG electrodes for RFTC remains limited in the United States. In this context, this case highlights a safe alternative and temporizing approach to performing diagnostic sEEG-guided RFTC, using a temperature-sensing pallidotomy probe to create small, precise stereotactic lesions. The authors caution careful consideration of this technique as a temporary work-around solution while also highlighting the rising need for new FDA-approved technologies for safe RFTC through in situ temperature-sensing sEEG electrodes.

ABBREVIATIONS

CT = computed tomography; EEG = electroencephalography; FDA = Food and Drug Administration; MRI = magnetic resonance imaging; PMC = patient management conference; RF = radiofrequency; RFTC = radiofrequency thermocoagulation; sEEG = stereoelectroencephalography

We present a case report illustrating the technique of stereotactic radiofrequency thermocoagulation (RFTC) applied during the diagnostic workup of a patient with refractory left temporal lobe epilepsy undergoing stereoelectroencephalography (sEEG) for invasive electroencephalography (EEG) monitoring. In contrast to conventional sEEG-guided RFTC, most commonly performed in European epilepsy surgery programs, our approach offers a temporizing work-around solution to the existing lack of Food and Drug Administration (FDA)–approved sEEG electrode technologies for RFTC in the United States. Our proposed technique incorporates a temperature-sensing radiofrequency (RF) pallidotomy probe to create the lesion. In our case, although used as a diagnostic procedure, RFTC has resulted in nearly 18 months of seizure freedom for this patient. Herein, we describe the case details, along with a historical overview and discussion of the indications and limitations of sEEG-guided RFTC methodology, ultimately highlighting the rising need for further development of FDA-approved, temperature-sensing sEEG-electrode technologies for RFTC intervention.

Illustrative Case

A 22-year-old, right-handed female patient presented with a 10-year history of medically intractable left temporal focal epilepsy. Her first seizure occurred at the age of 12. She continued to experience monthly seizures and was transitioned through several antiseizure medications, including oxcarbazepine, levetiracetam, and lacosamide, with intermittent periods of seizure freedom. At the time of referral, she was experiencing breakthrough seizures at least once per month. Semiology was predominantly characterized by right arm and face tonic activity and, to a lesser extent, some right arm clonic activity, followed by secondary generalization (often occurring out of sleep).

As part of her noninvasive presurgical evaluation, the patient underwent video EEG, which showed interictal sharp waves with polyspikes in the left temporoparietal region, less frequently arising in the frontal region. Ictal EEG activity localized to the left temporoparietal region, with EEG-confirmed onset preceding the clinical onset by several seconds.

3-T and 7-T magnetic resonance imaging (MRI) studies were reported as nonlesional. Magnetoencephalography identified interictal left temporoparietal sharp waves and polyspikes. Positron emission tomography revealed asymmetrical hypometabolism in the left lateral temporal and temporo-opercular region. Functional MRI showed expressive speech dominance in the left hemisphere, with receptive speech distributed across both hemispheres (notably, more prominent on the left side). Upon review at multidisciplinary patient management conference (PMC), the group’s consensus favored invasive EEG monitoring via left-sided sEEG, for localization purposes.

The preimplantation hypothesis focused on the left posterior temporo-perisylvian cortex, with secondary consideration for the left temporobasal region and left frontal (premotor) area (Fig. 1). On this basis, the patient underwent successful implantation of 18 left-sided electrodes (Adtech Medical Instrument Corp.) under stereotactic robotic guidance (ROSA, Zimmer Biomet), without complication. By the sixth day postimplantation, multiple seizures were recorded (Fig. 2). All seizures shared the same areas of involvement, although, at times, the onset varied, with earlier changes seen either in the left superior temporal sulcus (electrodes D′2–4, C′4–7, and B′6–8) or in the middle frontal gyrus (M′6–8). Later evolution was mostly seen in the left middle frontal gyrus (M′6–8) as well as to a lesser degree in the left superior frontal gyrus, left superior frontal sulcus (N′1–6 and K′8–10), and the left intraparietal sulcus/superior parietal lobule (P′6–8). Moreover, cortical stimulation via systematic cortical bipolar stimulation was performed at each electrode site of interest, to validate the absence of any motor symptoms or language deficits at these locations.

FIG. 1.
FIG. 1.

Representative three-dimensional (3D) magnetic resonance (MR) reconstruction and electrode placement map (A). Multimodal co-registration views are shown (B), with T1-weighted coronal (upper left), sagittal (upper right), and axial (lower left) MR images featuring implanted electrodes (blue dots), the D′ electrode trajectory (red dots), magnetoencephalography dipoles (yellow dots), and brain PET findings (lower right).

FIG. 2.
FIG. 2.

Interictal and ictal stereoelectroencephalography (sEEG) recordings of epileptiform activity. Sharp waves were evident in interictal recordings from electrodes lying within the left superior temporal sulcus and the middle temporal gyrus; at times, from the left middle frontal gyrus and superior frontal sulcus (M, K′, and N′ electrodes) and, to a lesser degree, from the left intraparietal sulcus and superior parietal lobule (P′) (A, bipolar montage, LF 0.53, HF 300, Sens 70 μV). Interictal rhythmic, slow sharp waves with overriding fast activity were recorded from the left superior frontal gyrus and left premotor region (M) (B, bipolar/referential montages, LF 0.53, HF 300, Sens 70 μV). The first of 2 ictal patterns is shown (C), with fast discharge activity arising in superior temporal sulcus electrodes, followed by a slow DC shift and evolution into diffuse repetitive spikes in the superior frontal sulcus and premotor region (bipolar montage, LF 0.53, HF 300, Sens 70 μV). T1-weighted coronal, sagittal, and axial MR images (insets) show the location of the electrodes in the temporal and frontal lobes (electroencephalography [EEG] ictal onset shown by red dots; magnetoencephalography [MEG] dipoles, yellow dots; and electrode contacts, blue dots). A second ictal pattern was recorded (D), with tonic discharge activity in the superior frontal sulcus and middle frontal gyrus and evolution into repetitive spikes. Notably, the clinical manifestations were very subtle with this seizure pattern. Low-frequency filter (LF); High-frequency filter (HF); Sensitivity (Sens).

At the PMC, it was decided to offer the patient a 2-staged approach, starting with RF ablation of the lateral D′ contacts (superior temporal sulcus) as a diagnostic next step to test the seizure localization hypothesis, with continued sEEG monitoring for several more days to ascertain the network effects of this focal intervention. Depending on the ensuing results, a second step was to recommend awake craniotomy for the resection of both banks of the left superior temporal sulcus, under electrocorticography guidance. The recommendations were discussed with the patient and her family, and they agreed with the stepwise plan. She was brought to the operating room the following day for careful intraoperative monitoring while the procedure was conducted under conscious sedation. Fifteen minutes of preablation sEEG recordings were collected at baseline. Under sterile conditions, the D′ cap and electrode were carefully removed, replaced with a 2-mm Cosman RF pallidotomy probe (Boston Scientific) through the same D′ bolt, and attached to a G4 RF generator (Boston Scientific). The RF probe was delivered to a premeasured depth placing its tip at the D′2–3 contact location, and the first ablation was made (using a temperature setting of 75°C for 60 sec duration). Subsequently, the RF probe was manually withdrawn to place its tip at the D′3–4 contact location, and a second ablation was made. Finally, the RF probe was withdrawn to place its tip at the D′4–5 contact location, and a third ablative treatment was delivered. Ablation parameters were carefully ascertained from multiple reports in the literature, spanning in vitro and in vivo studies, confirming that reproducible lesions can be generated around 78°C–82°C over an average treatment duration of anywhere from 10 to 60 seconds, depending on the RF generator used.1–8 Consistent with other studies, no coagulation was performed in close proximity (< 2 mm) of any major vascular structures.9,10 Care was taken to ensure the temperature of the probe had fallen to less than 40°C prior to sliding it back for each successive treatment. For each ablation performed, the lead impedance attained a confirmatory maximum (plateau), indicative of treatment effect. At the end of the successive ablative treatments, the RF probe was removed and replaced with a new sEEG electrode at the D′ location, followed by 15 minutes of postablative sEEG recording. Immediate postoperative computed tomography (CT) imaging was stable. Following removal of the sEEG leads 5 days later, a repeat postoperative CT confirmed a focal area of low attenuation in the left temporal lobe, corresponding to the treatment site.

Postoperative MRI at 6 months confirmed a final ablative lesion along the upper bank of the left superior temporal sulcus (Fig. 3). In a subsequent follow-up, the patient continued to remain well and was seizure free nearly 18 months later.

FIG. 3.
FIG. 3.

Postoperative coronal T2-weighted MR image showing a linear hyperintense signal corresponding to the lesion created by sEEG-guided radiofrequency thermocoagulation (RFTC) at the site of the lateral D′ electrode contacts (arrow).

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Historical Overview

The history of stereotactic ablative procedures for functional disorders dates back to 1958, when pallidotomy and pallidoamygdalotomy were proposed by Spiegel et al.11 for the treatment of convulsive disorders. From the late 1950s and early 1960s, multiple case series were reported describing stereotaxic amygdalotomy, bilateral fornicotomy, and targeted bilateral ablation of the posterior hypothalamic nuclei (among other targets) for the treatment of various behavioral disorders, including psychomotor epilepsy.12–15 Talairach and Bancaud16 also created focal therapeutic lesions targeting the amygdala and hippocampus using radioactive yttrium. Subsequently, RFTC of the amygdala and hippocampus using monopolar coagulation was reported.17 With emerging interest in the pivotal role of the entorhinal cortex in temporal epileptogenesis and the emergence of comparatively better outcomes with open resective approaches for medial temporal lobe epilepsy, interest in stereotactic ablative procedures for epilepsy began to wane.18,19

Observations

In 2004, RFTC under sEEG guidance was first described as a safe technique for creating lesions of epileptic foci with the caveat that the methodology could serve as a diagnostic and/or palliative intervention.1,20 This led to a renewed resurgence of interest in the technique, now targeted toward select nodes within the epileptogenic zone (mapped via sEEG methodology) in patients with intractable epilepsy. The procedure relies on the creation of small ablative lesions using either mono- or bipolar stimulation (i.e., the latter as applied between 2 contiguous contacts) using an RF generator coupled to the electrodes.3,9,21 Traditionally, the method has been performed without anesthesia, toward the end of the recording period, and often just prior to electrode removal.1 It has been proposed that contacts specifically used for RFTC are selected on the basis of the following features: (1) localization to the onset of the ictal discharge itself, (2) intralesional spatial location, and/or (3) reproducibility of clinical ictal symptomatology by sEEG-guided stimulation.21 Various coagulation parameters have been proposed in the literature, varying from center to center, contingent on the RF generator and electrodes used.7,8,22 On the basis of a growing literature around this topic, therapeutic lesions are reportedly achieved by an incremental empirical increase in power until the measurable lead impedance abruptly rises (with a concomitant fall in current), often accompanied by a self-reported audible sound of “crackling” or “popping” experienced by the patient when performed awake.23 These settings were validated in vitro and in vivo using egg white and rabbit models, capturing lesional effects using a 50-V, 120-mA current for a 45- to 60-second duration, approximating temperatures nearing 78–82°C.5,6 Studies have proposed a degree of control over the size of the lesion generated using RFTC, with in vitro and in vivo results illustrating larger confluent lesions at lower energy (i.e., low power) settings, as applied between contiguous contacts of the same electrode or even across discrete, adjacent electrodes.23,24

In general, results and outcomes vary widely with the technique. In a recent systematic review of 20 studies (with a total of 360 patients undergoing RFTC for epilepsy), a favorable seizure outcome (defined as Engel class I/II) was achieved in 62% of patients with at least 12 months of follow-up.8 From this same study, favorable prognostic factors included lesional MRI, a higher number of RF ablations performed, and monopolar RFTC. Prior representative case series specifically highlighting sEEG-guided RFTC are perhaps less optimistic, with seizure-free rates of 15%–23% and responder rates of 41%–67% (reportedly highest in patients with gray matter nodular heterotopia), with an overarching complication rate of approximately 2.5%.4,20,21,25 Of relevance, to minimize the risk of complications, it has been suggested to avoid any ablative treatments with adjacent vessels in close proximity (i.e., < 2 mm) to selected contacts used in lesioning and also to avoid sites where stimulation-induced motor or speech/language effects have been observed.4,9

Over the past 20 years, the literature citing sEEG-guided RFTC has expanded the experience, with positive predictive (diagnostic) value from the procedure linked to improved postoperative outcomes.20 Notably, the use of sEEG-guided RFTC was expanded to include hypothalamic hamartomas, small focal cortical dysplasias, and periventricular nodules, among other pathologies.2,10,21,26–29 Importantly, French national guidelines on sEEG have included a specific provision on sEEG-guided RFTC, which, to date, remains the only published clinical guideline about this technique.20,30,31 It is now generally accepted that the advantages of the procedure include its diagnostic, predictive, and occasionally therapeutic effects, in some cases offering the patient a palliative treatment option with immediate effects.4,9 With the emergence of computational methods for sEEG analysis, quantifiable interictal biometric signals (including high-frequency oscillations, spikes, and cross-rate measures) have enhanced prognostication and network analysis following the procedure.32 Nevertheless, the main drawback of sEEG-guided RFTC remains the lack of real-time control of lesion progression during the procedure and the absence of intraoperative in vivo temperature monitoring at the treatment site.1,10,29

Lessons

To date, the experience of sEEG-guided RFTC has been limited mostly to European centers where ablation through the sEEG electrodes themselves is accepted and established. In North America, particularly in the United States, the use of in situ sEEG electrodes for RFTC remains limited by the lack of FDA approval for ablative lesioning through any of the existing sEEG electrode technologies currently available on the market. Importantly, there are emerging examples of the off-label use of these electrodes for RFTC under appropriate institutional review board oversight.3,23,24 In fact, FDA-approved sEEG electrode technology permitting safe RFTC, incorporating temperature-sensing capability, is reportedly under development, which will help popularize this methodology in North American epilepsy surgery programs.

In this context, our case report highlights a safe alternative and temporizing approach to performing diagnostic sEEG-guided RFTC, using instead a temperature-sensing pallidotomy probe to create a set of small stereotactic lesions, as guided by the sEEG findings. In our case, the patient has remained seizure-free nearly 18 months later. We attest that our method is not novel but rather modifies an existing historical technique to safely perform RFTC in select patients with intractable epilepsy undergoing sEEG implantation. In the United States, given the lack of existing FDA-approved electrode technology for these procedures, our approach allows for safe and precise stereotactic lesioning while concomitantly tracking the temperature at the lesion site. At the same time, limitations arise over the hemorrhagic risk of reinsertion of the probe into an implantation site and also over the inherent infection risk of this process. In our single case reported here, there were no complications; nevertheless, we caution careful consideration of these 2 factors, which should preclude widespread use of this technique. Moreover, based on our limited experience, we recommend anticipatory planning in the careful selection of appropriate larger-diameter bolts to allow for RFTC, if desired (as not all current sEEG hardware permits the passage of the pallidotomy probe described in this report). For now, we offer this technique as a temporary work-around solution, highlighting the need for further development and testing of FDA-approved technologies for safe RFTC through in situ temperature-sensing sEEG electrodes.

Disclosures

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

Author Contributions

Conception and design: Serletis, Bulacio, Neme-Mercante, W Bingaman. Acquisition of data: Serletis, Bulacio, J Bingaman, Abushanab, Neme-Mercante. Analysis and interpretation of data: Serletis, Bulacio, Abushanab, Neme-Mercante. Drafting of the article: Serletis, Rammo, Neme-Mercante. Critically revising the article: Serletis, Bulacio, Abushanab, Rammo, Neme-Mercante, W Bingaman. Reviewed submitted version of the manuscript: Serletis, Bulacio, J Bingaman, Rammo, Neme-Mercante, W Bingaman. Approved the final version of the manuscript on behalf of all authors: Serletis. Administrative/technical/material support: Serletis, Harasimchuk. Study supervision: Serletis.

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  • FIG. 1.

    Representative three-dimensional (3D) magnetic resonance (MR) reconstruction and electrode placement map (A). Multimodal co-registration views are shown (B), with T1-weighted coronal (upper left), sagittal (upper right), and axial (lower left) MR images featuring implanted electrodes (blue dots), the D′ electrode trajectory (red dots), magnetoencephalography dipoles (yellow dots), and brain PET findings (lower right).

  • FIG. 2.

    Interictal and ictal stereoelectroencephalography (sEEG) recordings of epileptiform activity. Sharp waves were evident in interictal recordings from electrodes lying within the left superior temporal sulcus and the middle temporal gyrus; at times, from the left middle frontal gyrus and superior frontal sulcus (M, K′, and N′ electrodes) and, to a lesser degree, from the left intraparietal sulcus and superior parietal lobule (P′) (A, bipolar montage, LF 0.53, HF 300, Sens 70 μV). Interictal rhythmic, slow sharp waves with overriding fast activity were recorded from the left superior frontal gyrus and left premotor region (M) (B, bipolar/referential montages, LF 0.53, HF 300, Sens 70 μV). The first of 2 ictal patterns is shown (C), with fast discharge activity arising in superior temporal sulcus electrodes, followed by a slow DC shift and evolution into diffuse repetitive spikes in the superior frontal sulcus and premotor region (bipolar montage, LF 0.53, HF 300, Sens 70 μV). T1-weighted coronal, sagittal, and axial MR images (insets) show the location of the electrodes in the temporal and frontal lobes (electroencephalography [EEG] ictal onset shown by red dots; magnetoencephalography [MEG] dipoles, yellow dots; and electrode contacts, blue dots). A second ictal pattern was recorded (D), with tonic discharge activity in the superior frontal sulcus and middle frontal gyrus and evolution into repetitive spikes. Notably, the clinical manifestations were very subtle with this seizure pattern. Low-frequency filter (LF); High-frequency filter (HF); Sensitivity (Sens).

  • FIG. 3.

    Postoperative coronal T2-weighted MR image showing a linear hyperintense signal corresponding to the lesion created by sEEG-guided radiofrequency thermocoagulation (RFTC) at the site of the lateral D′ electrode contacts (arrow).

  • 1

    Guénot M, Isnard J, Ryvlin P, Fischer C, Mauguière F, Sindou M. SEEG-guided RF thermocoagulation of epileptic foci: feasibility, safety, and preliminary results. Epilepsia. 2004;45(11):13681374.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Khoo HM, Gotman J, Hall JA, Dubeau F. Treatment of epilepsy associated with periventricular nodular heterotopia. Curr Neurol Neurosci Rep. 2020;20(12):59.

  • 3

    Shamim D, Cheng J, Pearson C, Landazuri P. Network radiofrequency ablation for drug resistant epilepsy. Epilepsy Behav Rep. 2021;16:100471.

  • 4

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