The Value of SINO Robot and Angio Render Technology for Stereoelectroencephalography Electrode Implantation in Drug-Resistant Epilepsy

Abstract

Background Stereoelectroencephalography (SEEG) electrodes are implanted using a variety of stereotactic technologies to treat refractory epilepsy. The value of the SINO robot for SEEG electrode implantation is not yet defined. The aim of the current study was to assess the value of the SINO robot in conjunction with Angio Render technology for SEEG electrode implantation and to assess its efficacy.

Methods Between June 2018 and October 2020, 58 patients underwent SEEG electrode implantation to resect or ablate their epileptogenic zone (EZ). The SINO robot and the Angio Render technology was used to guide the electrodes and visualize the individual vasculature in a three-dimensional (3D) fashion. The 3D view functionality was used to increase the safety and accuracy of the electrode implantation, and for reducing the risk of hemorrhage by avoiding blood vessels.

Results In this study, 634 SEEG electrodes were implanted in 58 patients, with a mean of 10.92 (range: 5–18) leads per patient. The mean entry point localization error (EPLE) was 0.94 ± 0.23 mm (range: 0.39–1.63 mm), and the mean target point localization error (TPLE) was 1.49 ± 0.37 mm (range: 0.80–2.78 mm). The mean operating time per lead (MOTPL) was 6. 18 ± 1.80 minutes (range: 3.02–14.61 minutes). The mean depth of electrodes was 56.96 ± 3.62 mm (range: 27.23–124.85 mm). At a follow-up of at least 1 year, in total, 81.57% (47/58) patients achieved an Engel class I seizure freedom. There were two patients with asymptomatic intracerebral hematomas following SEEG electrode placement, with no late complications or mortality in this cohort.

Conclusions The SINO robot in conjunction with Angio Render technology-in SEEG electrode implantation is safe and accurate in mitigating the risk of intracranial hemorrhage in patients suffering from drug-resistant epilepsy.

Keywords

SINO robot - Angio Render technology - vessel visualization - stereoelectroencephalography - drug-resistant epilepsy

Introduction

Epilepsy is a medically significant condition that is considerable prevalent across various age groups. Despite notable advancements in the field of antiepileptic drugs, more than 30% of the patients continue to experience seizures, thus having drug-resistant epilepsy.[1] Epilepsy surgery is highly successful for treating drug-resistant epilepsy. Patients who have had surgery for drug-resistant epilepsy have increased dramatically during the past 20 years.[2] Accurate preoperative localization of the epileptogenic zone (EZ) and understanding of the epileptic network are essential for a successful epilepsy surgery. Stereoelectroencephalography (SEEG) is an accurate, safe, and effective procedure for localizing EZ in drug-resistant epilepsy patients.[3] SEEG can be helpful for the three-dimensional (3D) definition of the EZ.[4]·Precise surgical planning and reliable stereotactic techniques ensure safe implantation of SEEG electrodes.[3] Many neurosurgical centers have applied multimodal image fusion technology in epilepsy surgery, especially the cerebrovascular reconstruction technology. Several stereotactic technologies,[5] such as classic frame-based,[6] frameless navigation,[7] and robotic guidance,[8] are now used to implant SEEG electrodes. Accuracy of electrode placement is affected by many factors and has been the subject of several studies.[8] [9] [10] It was shown that that the frameless ROSA (Medtech, Montpellier, France) robot-assisted SEEG electrode implantation for drug-resistant epilepsy patients was safe and effective.[11] [12] [13] [14]

The SINO robot (Sinovation Medical, Beijing, China) is specifically designed as a stereotactic device. It consists of a robot arm with a high-precision six-axis force sensor and a mobile case as a base unit. The device is equipped with a high-precision pressure sensor and guided by a custom algorithm. It can monitor its force feedback in real time, stopping its movement when encountering obstacles, such as a doctor or a patient.

The SinoPlan system is tailor-made for neurosurgical operation planning. It relies on the Angio Render technology, developed for cortical vessel imaging and visualization, to minimize intracranial hemorrhage risk during depth electrode insertion.[15] The Angio Render Technology is based on computed tomography angiography (CTA) data, digital subtraction angiography (DSA) data, or magnetic resonance angiography (MRA) data/magnetic resonance venography (MRV) data. The SinoPlan system realizes optimal co-registered 3D views of the sulcal anatomy and vasculature of the brain, helping to plan SEEG electrode trajectories. SEEG electrode trajectories and intracranial vessels can be displayed 3-dimensionally directly in the SinoPlan system. The imaging system of the SINO robot is established on the SinoPlan system.

The objective of the current study was to assess the value of the SINO robot in conjunction with Angio Render technology in SEEG electrode implantation. We also assess its efficacy by examining factors such as localization error, operation time, and complications.

Subjects

Between June 2018 and October 2020, 58 consecutive patients who met the International League Against Epilepsy's criterion of drug-resistant epilepsy.[16] underwent a SINO robot–guided SEEG electrode implantation. The patient population was divided into those who underwent epileptic lesion removal surgery or radiofrequency thermocoagulation (RFTC). This study was conducted under the ethical standards of the Declaration of Helsinki. It was approved by the Ethics Committee Board of Fujian Medical University Union Hospital, and informed consent was obtained from all participants.

Magnetic Resonance Imaging Acquisition

All the images were acquired using a 3-T MR scanner (MAGNETOM Prisma, Siemens Healthcare, Erlangen, Germany). The high-resolution structural magnetic resonance imaging (MRI) protocol included sagittal T1-weighted magnetization-prepared rapid acquisition with gradient echo image (T1-MPRAGE), axial T2-weighted (T2W) fast spin echo (FSE) images, and axial fluid-attenuated inversion recovery (FLAIR) T2W images.

Contrast-enhanced magnetic resonance angiography and venography (CE-MRAV) was performed in the axial plane immediately after 3D time-of-flight (TOF) MRA. Contrast material (gadobutrol: 0.1 mmol/kg) was injected via the antecubital vein at a rate of 2.5 mL/s followed by a saline (0.9%) bolus of 20 mL at 2.5 mL/s. The 3D volume was acquired with the following imaging parameters: repetition time (TR) = 3.70 milliseconds; echo time (TE) = 1.32 milliseconds; slice thickness = 1.2 mm; pixel bandwidth = 390 Hz/pixel; flip angle = 22 degrees; field of view = 240 × 195 mm²; voxel size = 0.6 × 0.6 × 1.2 mm³. Parallel image acquisition using the GRAPPA (Generalized Autocalibrating Partially Parallel Acquisition) algorithm was applied with an acceleration factor of 3.

Trajectory Planning

Within the SINO platform, medical professionals engage in the process of reconstructing various components of the patient's brain, including the tissue structure, skull, blood vessels, fiber tracts, and other relevant anatomical aspects. These components are subsequently integrated and fused together. The cerebral cortex was reconstructed using a thin-layer T2 FLAIR sequence, while the cerebral vasculature was reconstructed using a CE-MRAV sequence. The skull layer was imaged using a thin-scan CT sequence, and the scalp was visualized using a T1-weighted 3 dimensional sequence. Initially, the SINO platform was employed to perform co-registration of thin-slice head CT scans with a thickness of 1 mm to head MRI scans also with a thickness of 1 mm. Subsequently, the reconstructed blood vessels were generated using CE-MRAV data. To assure surgical safety, it is imperative to visualize all vessels with a diameter greater than 1 mm. It is worth mentioning that the unique Angio Render vascular 3D visualization technology of the SINO platform can fully display the intracranial vascular structure.[15] Therefore, it allows surgeons to directly plan electrode trajectories from a 3D view, effectively avoiding the main blood vessels ([Fig. 1]). The minimum distance of trajectory planning from vessels is 2 mm. Neurosurgeons can develop an SEEG electrode implantation strategy through the utilization of 3D image reconstruction techniques.

Fig. 1 Planned electrode trajectories in a three-dimensional view.

The number and position of electrodes implanted were determined by prior working hypotheses regarding the probable localization of the EZs based on semiology, scalp EEG data, and the results of other noninvasive investigations (MRI, positron emission tomography [PET]). The aims of SEEG electrode placement are (1) to identify the EZ, (2) to investigate its association with functional regions, and (3) to assess the possibility of surgical excision.[17] The precision of electrode implantation is enhanced by orthogonal trajectories, while oblique trajectories can help sample the cortical convexity.[17] The SINO robotic guiding platform may realize oblique electrode trajectories is necessary and does not require totally orthogonal electrode trajectories. The process of SEEG implantation typically entails the placement of electrodes in a single hemisphere, although there are infrequent instances where both hemispheres are involved. Bilateral monitoring was also convenient if there was any question about onset laterality in some patients due to negative lateralizing information after ictal scalp EEG and functional imaging, especially the bitemporal lobe epilepsy.[18] Trajectories of the electrodes avoiding vessels were determined by 3D T1-weighted MRI, and MRA was computed with stereotactic software (Sinovation Medical) during preoperative planning. The software was used to direct the robotic arm connected to a Mayfield or Dora three-pin frame during the implantation of the electrodes (0.8 mm diameter, 8–16 contacts, 2 mm length, 1.5 mm spacing). To calculate the electrode length accurately and conveniently, the entry point (EP) was set on the scalp ([Fig. 2]).

Fig. 2 Three-dimensionally reconstructed images of four typical cases after electrode implantation. Epileptic lesion in the (a) right parietal occipital lobe, (b) left frontal lobe, (c) a hypothalamic hamartoma, and (d) left temporal lobe.

Surgical Procedure

Preoperatively, five or six bone fiducials (Sinovation Medical) were placed around the surgical field under local anesthesia to improve the accuracy of localization.[19] Then a thin-slice (1-mm) head CT scan was performed and co-registered with the planning MR images.

The patients were then positioned either supine, lateral, or prone under general anesthesia. The patients were then placed in the Mayfield clamp with their heads firmly secured to the operating table (patients younger than 3 years had their skulls fixed with pediatric head pins, and those older than 10 years had adult head pins). The SINO platform base was attached to the headframe. The patient underwent registration with the planning CT scans by utilizing the robotic arm for bone fiducial recognition ([Fig. 3a]). After strict sterile preparation of the surgical area, the operation begins. The robotic arm moves alternately to each planned trajectory.

Fig. 3 Operation and stereoelectroencephalography (SEEG) electrode implantation. (a) Patient registration for recognition based on bone fiducials. (b) Twist drill holes in the skull through the scalp under robotic arm guidance. (c) Firmly screwed guidance anchor bolted into the burr hole. (d) Puncturing the brain to open the electrode trajectory using a sterilized stylet. (e) Mark SEEG electrodes as target length. (f) Rubber rings for SEEG electrodes were secured by polyurethane bolt caps.

The high-precision pressure sensor on the robotic arm plays an important role.

When the surgeon steps on a foot-operated safety switch, they could simultaneously drag the end of the robotic arm. The high-precision pressure sensor could sense the force on the robotic arm and control it to move with the operator's hand. Then, the end of the robotic arm could only move in the previously determined direction of the electrode trajectories. With this technology, the distance between the end of the robotic arm and the patient's head could be adjusted, greatly facilitating the subsequent operation.

Once the EP was identified, a 2-mm drill bit under the control of a robotic arm was utilized to generate twist drill holes for direct access to the skull ([Fig. 3b]). The bone debris in the burr hole was removed, followed by the insertion of a sharp coagulation electrode with a diameter of 2 mm to penetrate the dura mater. Subsequently, the guide anchor bolts were securely fastened into the designated aperture (see [Fig. 3c]). The length of the trajectory was measured by using a stylet, which punctured the brain to provide an opening for the electrode route (see [Fig. 3d]). The desired length of the SEEG electrodes were marked with rubber rings, as depicted in [Fig. 3e]. The SEEG electrodes were placed into the designated burr hole with the guidance of an anchor bolt to achieve the desired length. Subsequently, the electrodes were fixed using polyurethane bolt caps, as depicted in [Fig. 3f]. The robotic arm then proceeded to the subsequent target. Following the insertion of all electrodes, Vaseline gauze was applied around each bolt and covered with a sterile gauze. A postoperative CT scan was performed and co-registered with the preoperative MRI to assess the accuracy of the electrode position, to pinpoint the location of each electrode contact in the software workstation (Sinovation) and to ensure the absence of postoperative bleeding.

SEEG Recording

SEEG recordings were performed 1 week to 1 month after surgery with reduced medication to capture spontaneous habitual seizures using a video-EEG system (Neuvo Amplifier, Neuroscan Compumedics, Australia) that allowed simultaneous recording of up to 256 contacts at a sampling rate of 10,000 Hz (bandpass filter of 0–2,500 Hz). Deep EEG activity was observed between contiguous contacts at various levels along the axis of each electrode, and visual analysis was performed on SEEG traces to determine interictal and ictal patterns. Prior to the clinical onset of the seizure, the area displaying the initial distinct SEEG change was visually designated as the seizure-onset zone (SOZ). When SEEG ictal onsets exhibited low-voltage fast activity in the beta and gamma bands, or recruiting and periodic rapid discharge of spikes, they were deemed significant. When interictal epileptiform discharges (IEDs) comprised spikes, poly spikes, spike and wave complexes, or poly spike and wave complexes, they were deemed significant. Electrical stimulations were performed after the patients experienced two to three habitual seizures or auras. Electrically elicited seizures (EES) were deemed significant when they demonstrated clinical similarity to spontaneously recorded seizures.

RFTC and Resection

In all patients, the strategy of surgical resection and SEEG-guided RFTC was discussed during a patient management conference based on multimodal data, including MRI, PET, video EEG, and SEEG, after the EZ was determined.[20] [21]

The SINO platform plays a very important role in determining RFTC contacts, which can support the 3D measurement of the distance between contacts and intracranial vasculature. It was believed that the range of RFTC could be largest at the appropriate parameter, and the resulting lesions were reported to be 5 to 7 mm in diameter.[22] Therefore, we advocate that the distance between contacts and intracranial vessels of more than 4 mm is a safe distance for RFTC.

SEEG-guided RFTC was performed without anesthesia using a radiofrequency generator system (model no. R2000B-M1, BNS, Beijing, China) after the recording period and prior to removing the electrodes. In 40 seconds, a maximal output of 7.5 W produced lesions between two adjacent contacts of the selected electrodes. In patients with a history of frequent seizures prior to RFTC, SEEG surveillance was sometimes extended for a few days following thermocoagulation. A second RFTC procedure would be performed if seizures persisted following the initial RFTC procedure. The electrodes were removed under anesthesia 1 to 2 days after completion of the final RFTC procedure, and the patients were subsequently discharged.

Following a precise delineation of resection area, a neuronavigationally guided craniotomy could be performed, using the SINO platform. Prior to the surgical procedure, it is imperative to establish a comprehensive understanding of the vascular architecture near the anatomical boundary, employing a 3D approach. Furthermore, in cases of neuronavigational inaccuracydue to brain shift, the 3D visualization of the vascular structure might be employed to identify the precise location of the resection area.

Data Analysis and Outcome

The study retrospectively examined and reported on many factors, including demographic data, number of electrodes, surgery duration, and accuracy. Additionally, information on seizure outcomes and complications associated with the procedure was also gathered. The time from locating the first trajectory to securing the last electrode was defined as operating time (OPT). The patients' outcome was quantified at least 1 year after the procedure by an epileptologist based on the Engel outcome scale. The preoperative MRI was co-registered with the postoperative CT scans to visualize the actual electrode position and evaluate the positioning accuracy. The EP localization error (EPLE) and the target point (TP) localization error (TPLE) were defined as the Euclidean distance between the planned EP or target point coordinates and the coordinates of the postimplantation electrode EP or TP. The actual location coordinates (Xa, Ya, Za) and planned location coordinates (Xb, Yb, Zb) were recorded by the SINO platform workstation. The localization errors between entry and target points were calculated for each electrode ([Fig. 4]), applying the following equation[23] ( [Eq. 1]):

Fig. 4 The target point localization errors were calculated for each electrode. The figure shows the case of hypothalamic hamartoma.

The localization errors between the entry and target points.

The depth of electrodes was defined as the Euclidean distance between postimplantation EP and TP, and it has the same formula as [Eq. 1].

In the Results section, the overall placement error is shown as the mean ± standard deviation (SD).

Results

Within 2 years, there were 58 patients with a mean age of 18. 10 ± 12.97 years (range: 4–45 years; 32 males and 26 females). In total, 634 SEEG electrodes were implanted and the number was 10.92 (range: 5–18) electrodes per patient. Six patients had bilateral electrode implantation. The mean operating time per lead (MOTPL) was 6.18 ± 1.80 minutes (range: 3.02–14.61 minutes). The mean EPLE was 0.94 ± 0.23 mm (range: 0.39–1.63 mm), and the mean TPLE was 1.49 ± 0.37 mm (range: 0.80–2.78 mm). The mean depth of electrodes was 56.96 ± 3.62 mm (range: 27.23–124.85 mm). More details are summarized in [Table 1].

Table 1 Statistical analysis related to electrode implantation

No. of patients	58
Bilateral implantation	6
No. of implanted electrodes	634
Mean no. of electrodes/patient	10.92 (range: 5–18)
Mean operating time per electrode (min)	6. 18 ± 1.80 (range: 3.02–14.61)
Mean errors
Entry point error (mm)	0.94 ± 0.23 (range: 0.39–1.63)
Target point error (mm)	1.49 ± 0.37 (range: 0.80–2.78)
Target point location
Frontal	30.44% (193/634)
Temporal	35.48% (225/634)
Parietal	12.30% (78/634)
Occipital	9.78% (62/634)
Insula	5.85% (37/634)
Hypothalamic hamartoma	6.15% (39/634)
Mean depth (mm)
Mean depth of all electrodes	56.96 ± 3.62 (range: 27.23–124.85)
Mean depth of electrodes with frontal target	47.49 ± 0.65 (range: 41.6–54.91)
Mean depth of electrodes with temporal target	66.70 ± 1.92 (range: 46.13–124.85)
Mean depth of electrodes with parietal target	41.27 ± 2.47 (range: 32.48–61.26)
Mean depth of electrodes with occipital target	50.41 ± 2.96 (range: 27.23–63.28)
Mean depth of electrodes with target in the insula	54.37 ± 3.33 (range: 47.79–72.13)
Mean depth of electrodes targeting the hypothalamic hamartoma	91.91 ± 0.93 (range: 84.06–108.61)

Note: Values expressed as the mean ± standard deviation (SD).

Seventeen patients underwent surgical resection (9 anterior temporal lobectomies, 5 frontal epileptic focal resections, and 3 parietal epileptic focal resections). The remaining 41 patients underwent SEEG-guided RFTC (including 6 hypothalamic hamartomas).

Complications

No notable complications were observed in this study. However, asymptomatic intracranial hemorrhage was detected on postoperative CT in two cases following implantation (three implanted electrodes), in eight cases following SEEG-guided RFTC, and in two cases following surgical resection. No instances of infection were seen in this study.

Epilepsy Outcomes

In the present investigation, all the participants underwent follow-up assessments for a minimum duration of 1 year. In the RFTC group, a total of 41 patients were included in the analysis. Among these patients, 33 of 41 (80.48%) achieved seizure freedom and were classified as Engel class I. Additionally, 6 of 41 patients (14.63%) were classified as Engel class II, indicating a partial reduction in seizures. Finally, 2 of 41 patients (4.89%) were classified as Engel class III, indicating a lack of improvement in seizure control. In the resection group, a total of 82.35% (14 of 17) of patients achieved seizure freedom according to the Engel class I classification. The remaining 17.65% (3 of 17) of patients fell into the Engel class II category ([Table 2]).

Table 2 Epilepsy outcomes after follow up in 58 patients who underwent SEEG

SEEG and epilepsy outcomes	Value
Seizure capture	100%
Duration of monitoring (d)	14.58 ± 4.27
Length of stay (d)	15.91 ± 2.83
Epileptogenic zone localization	100%
Follow-up (mo)	14.37 ± 1.57
Resection	17
Engel class
I	82.35% (14/17)
II	17.65% (3/17)
III	0
IV	0
Histology
Hippocampus sclerosis	5
FCD	6
TSC	3
Gliosis	3
RFTC	41
Engel class
I	80.48% (33/41)
II	14.63% (6/41)
III	4.89% (2/41)
IV	0

Abbreviations: FCD, focal cortical dysplasia; RFTC, radiofrequency thermocoagulation; SEEG, stereoelectroencephalography; TSC, tuberous sclerosis complex.

Note: Values expressed as the mean ± standard deviation (SD).

Discussion

The aim of the current study was to assess the value of the SINO robot in conjunction with Angio Render technology in SEEG electrode implantation. The primary focus was on assessing the safety and accuracy of this approach in mitigating the risk of intracranial hemorrhage in patients suffering from drug-resistant epilepsy. We also assessed the efficacy of SINO robot–assisted SEEG electrode implantation by examining factors such as localization error, operation time, and complications.

Vakharia et al published a meta-analysis and systematic review about the accuracy of SEEG electrode placement.[5] Their study showed that ROSA robot-assisted SEEG electrode implantation had a mean EPLE of 1. 17 mm (95% confidence interval [CI]: 0.80–1.53 mm) and a TPLE of 1.71 mm (95% CI: 1.66–1.75 mm). In our study, the SINO robotic trajectory guidance system was at least as accurate as other systems. The SINO robotic trajectory guidance systems clearly indicated the EP position and electrode length. Previous studies on stereotactic robots of this property are summarized in [Table 3].

Table 3 Previously reported studies about stereotactic robots of electrode implantation

Study	Method	Patients	Electrodes (total)	Electrodes/case	Mean time per electrode (min)	Entry point accuracy (mm)	Target point accuracy (mm)	Complications
Vakharia et al[5]	Robotic trajectory guidance system	–		–	–	1.17 (95% confidence interval [CI]: 0.80–1.53)	1.71 mm (interquartile range (IQR): 1.20–2.30 mm)	Not specified
González-Martínez et al[26]	ROSA robot	101	1245	12.5	10.4	1.2 mm (IQR: 0.78–1.83 mm)	1.7 mm (IQR: 1.20–2.30 mm)	4 patients (4%): 2 subdural hematomas and 2 intraparenchymal hematomas
Ollivier et al[40]	ROSA robot	66	857	12.98	9.01	1. 1 (0.15–2.48)	2.09 (1.06–3.72)	1 patient with symptomatic intraparenchhymal hematoma, 8 patients with asymptomatic postoperative bleeding
Ho et al[41]	ROSA robot	7	222	11.1	10.98	1.75 ± 0.94 (range: 0.91–3.62)	3.39 ± 1.078 (range: 0.9–4.02)	Nil
Spyrantis et al[12]	ROSA robot	5	40	8	9.38	2.96 ± 0.24	2.53 ± 0.24	Nil
Iordanou et al[42]	ROSA robot	25	Oblique: 109	–	–	1.76; SD: 1.62	–	Not specified
			Orthogonal: 210	–	–	1.32; SD: 1.19	–
Candela-Cantó et al[8]	Robotic arm Neuromate (Renishaw)	14	164	–	–	1.57 (range: 1–2.25)	1.77 (range: 1.2–2.6)	1 patient with meningitis without demonstrated germ; 1 patient with right frontal hematoma
Machetanz et al[43]	frame (Radionics Brown-Roberts-Wells, Boston, Massachusetts, USA)	12	91	7.58	15.1 ± 1.9	1.5 ± 0.6	1.5 ± 0.8	Intracranial hemorrhage: 3 (5.0%)
	ROSA robot	15	129	8.6	9.1 ± 1.7	0.7 ± 0.5	1.6 ± 0.8	1 patient with subdural hematoma
Zhang et al[9]	SINO robot	16	162	10. 13 ± 2.70	10. 13 ± 2.70	1.56 (IQR: 0.00–2.24)	1.56 (IQR: 0.00–2.24)	Not specified
Yao et al[44]	SINO Robotic	87	777	8.9 ± 2.2	7.9 ± 1.3	1.48 ± 1.46	1.61 ± 1.3	Intracranial hemorrhage: 6 (6.7%)
	CRW stereotactic frame	60	464	7.9 ± 2.5	13.5 ± 3.1	1.59 ± 0.9	1.64 ± 1.3	Intracranial hemorrhage: 6 (6.7%)
Dedrickson et al[45]	Globus ExcelsiusGPS robot	5	59	11.8 ± 3.7	–	1.6 ± 1.2 mm	–	No complications
Vasconcellos et al[25]	Overall	811	8,184	10.06	15.1	1.48 (range: 0–8.37)	2.13 (range: 0–7.3)	–
	ROSA	411	4,848	11.8	11.45	1.49 (range: 0.3–6.38)	2.5 (range: 0–9.02)
	Neuromate	202	1,585	7.8	36.6	1.66 (range: 0–8.37)	2.09 (range: 0–7.33)
	Sinovation	140	1,330	9.5	9.9	1.39	1.64 (range: 0.33–3.61)
	ISys1	58	421	7.25	15.7	1.23 (range: 0.1–3.4)	1.61 (range: 0.3–6.7)
Li et al[46]	SINO Robotic	28	161	5.75	–	0.87 mm (IQR: 0.50–1.41 mm)	2.74 mm (IQR: 2.01–3.63 mm)	4/152 electrodes bleeding
Gomes et al[24]	Robotic assisted	232	–	8.5–15.6	MD –3.35 min; 95% CI –3.68,–3.03; p < 0.00001	MD 0.04 mm; 95% CI –0.21, –0.29; p = 0.76	MD: 0.57 mm; 95% CI: –1.08; –0.06; p = 0.03	Intracranial hemorrhage in 9/145 (6.2%)
	Traditional hand guided	196	–	4.5–12.56				Intracranial hemorrhage 8/139 (5.7%)
Gorbachuk et al[47]	SINO Robotic	20	185	9.25	7.9 ± 2.3	–	–	2/20 (10%) patients were bleeding; 2/185 (1%) electrodes were bleeding
Present study	SINO robotic	58	634	10.92 (range: 5–18)	6.18 ± 1.80 min (range: 3.02–14.6 1 min)	0.94 ± 0.23 mm (range: 0.39–1.63 mm)	1.49 ± 0.37 mm (range: 0.80–2.78 mm)	2 patients had asymptomatic brain hematomas

Sources: Vakharia et al,[5] Martínez et al,[26] Ollivier et al,[40] Ho et al,[41] Spyrantis et al,[12] Iordanou et al,[42] Candela-Cantó et al,[8] Machetanz et al,[43] Machetanz et al,[43] Zhang et al,[9] Yao et al,[44] Dedrickson et al,[45] Vasconcellos et al,[25] Zhao et al,[46] Gomes et al,[24] and Gorbachuk et al.[47]

A systematic review and meta-analysis indicate that the mean OPT per electrode in the robot-assisted group is significantly less than that in the traditional hand-guided group.[24] On the other hand, in another systematic review and meta-analysis on robot-assisted SEEG electrode placementthe mean OPT per electrode of Sinovation (9.9 minutes) was shorter than that of ROSA (11.45 minutes).[25] González-Martínez et al reported the results of 101 robot-assisted SEEG procedures.[26] In total, with the help of the ROSA robotic trajectory guidance system, 1,245 depth electrodes were implanted, with the mean OPT per electrode of 10.4 minutes.[26] Spyrantis et al[12] performed five robot-assisted SEEG procedures with the ROSA robotic trajectory guidance system; 40 SEEG electrodes were implanted in total; the MOTPL was 9.38 minutes. In our series of cases, the MOTPL was 6.18 ± 1.80 minutes, a markedly reduced time compared with previous reports; we attribute this result to the SINO robot's excellent performance and the proficiency and tacit cooperation of the operators.

Liu et al[15] compared PC-MRA images with intraoperative photographs for the first time to evaluate the effectiveness of cortical vascular imaging. The results showed good agreement. However, 17 of 93 vessels, (18.3%), which were located deep in the sulci were not visualized. A clearer sulci visualization could greatly aid surgical planning since the sulci could be displayed darker in the cortex volume rendering according to their depth information. This finding strongly implies that the cortex vision accuracy is crucial for preserving the cortical arteries' structural integrity and preventing intracerebral hemorrhage to the greatest extent. The sulcal anatomy and vasculature may be seen in the best co-registered 3D views by the SINO Angio robot's Render technology, enhancing the safety of SEEG electrode implantation.

Cardinale et al published a meta-analysis and systematic review about the morbidity and mortality in SEEG electrode placement.[14] [27] They reported 35 major complications (including four fatalities) in approximately 4,000 patients implanted with approximately 33,000 electrodes. In three of the four fatal cases, a large intracerebral hemorrhage occured[30] Other major immediate complications after electrode implantation included 14 cases of nonfatal intracerebral hemorrhage. Mullin et al published another systematic review of the morbidity and mortality of intracranial SEEG electrode placement.[31] The most common complications were hemorrhage (pooled prevalence: 1.0%; 95% CI: 0.6–1.4%) and infection (pooled prevalence: 0.8%; 95% CI: 0.3–1.2%). Therefore, reducing the incidence of intracerebral hemorrhage would positively affect the outcome of SEEG electrode implantation.

Intracerebral hemorrhage during stereotactic procedures can cause severe morbidity and mortality. Planning stereotactic procedures to avoid conflicts with the cerebral vasculature requires vascular imaging. The gold standard for cerebral vascular imaging is DSA.[32] Li et al studied the size of vessels, which is clinically significant for SEEG implantation planning. They found that electrode conflicts with vessels 1 to 1.5 mm in size did not result in radiologically detectable or clinically significant hemorrhages and suggested that vessels under 1 to 1.5 mm in diameter should be excluded from consideration while designing the SEEG electrode trajectory.[33]

Nowadays, DSA, CTA, and MRA all allow for high-resolution (diameter: 1.5 mm) vascular imaging.[34] [35] The most widely utilized angiographic techniques are CTA and DSA, although MRA enables high-resolution vascular visualization without additional radiation dangers. In this study, based on CE-MRAV all vessels that are greater than 1 mm in diameter will be imaged and visualized. Therefore, all clinically relevant blood vessels can be visualized before SEEG implantation. Accurate co-registered 3D views of the vasculature and sulcal anatomy are critical for planning SEEG trajectories while avoiding the blood vessels.[36] The SINO plan system effectively applies the Angio Render technology, reconstructing individual 3D views of the sulcal and vasculature anatomy. These anatomical and vascular maps are possibly the main reason for the absence of intracerebral hemorrhages after implantation of 634 SEEG electrodes in our series. Stereotactic RFTC was developed as a surgical treatment for focal epilepsy, primarily as an alternative to traditional surgery, between the 1970s and the 1990s. SEEG-guided RFTC may be a significant therapeutic option when a large epileptic network (multifocal ictal onsets) is involved, which is inaccessible for resection. This contrasts with the situation of a limited-volume epileptic zone accessible to a total or subtotal RFTC in a location where surgery is risky (such as periventricular heterotopia or insular ictal onset zone). In fact, the functional disruption of such a network could be caused by lesioning different areas of the network.[37] Even if a complete cure for epilepsy cannot be achieved, a significant improvement may result, and patients occasionally develop drug sensitivity. These outcomes are typically not long-lasting, probably because of the reconfiguration of the epileptic network. Repeating SEEG-guided RFTC seems being a good option in these cases, and the new intrusive information regarding potential modifications to the epileptic network may assist in designating new, ideal targets to cause additional network disruption. Additionally, several procedural factors affect the efficiency and security of stereotactic RFTC, including radiofrequency delivery duration, number of coagulation sites, rate of power rise, distance between the dipole contacts, and variations in the substrates that are coagulated.

Staudt et al researched the best way to spread out RF lesions over various SEEG electrodes.[38] The biggest lesions may be created when the radiofrequency power is administered over a prolonged period at less than 3 W, according to both in vitro and in vivo studies. The size of the lesion is also influenced by the linear separation of the electrodes, with the greatest lesions occurring when the linear gap is between 5 and 12 mm. According to the RFTC characteristics of the electrode channel, the electrode position was designed to ensure the maximum thermal coagulation volume when choosing electrodes contacts which exhibited notable patterns of ictal onset, interictal discharges (IEDs), and/or electrically elicited seizures (EES) during SEEG recordings. The greatest lesion, measuring 100.74 mm² (mean of 74. 1 ± 11.3 mm²), was produced with a power of 3 W at 8 mm of electrode spacing. To ensure the safety of RFTC, it is crucial to know the distance between the electrode and the blood vessel prior to performing RFTC: The electrode distance from the blood vessel should not be less than 6 mm. The SINO plan method efficiently employs Angio Render technology, reconstructing individual 3D representations of the sulcal and vascular anatomy.[39] This substantially simplifies determining the electrode's distance from the blood vessel prior to RFTC.

This study demonstrated the utility of the SINO robotic trajectory guidance system in SEEG electrode implantation, with minimal error in entry and target points, no intervention complications, and a positive postoperative outcome after EZ ablation in many patients.

Limitations of the Study

The data in this study were limited as it was a single-center study with no controls. This study showed the value of Angio Render technology in clinical application, but it did not evaluate the incidence of hemorrhage before electrode implantation and RFTC.

Conclusion

Our preliminary study on the use of the SINO robot for guidance of SEEG electrode placement allows obtaining MOTPL, accuracy, and safety, which are comparable with previously published series of robot-assistance for SEEG electrode placement. The SINO plan system applies Angio Render technology, effectively achieving 3D visualization of intracranial vessels, thereby improving the safety of surgery.

Conflict of Interest

None declared.

Authors' Contributions

R.J. conceived and coordinated the study. S.SW. and R.J. signed, performed, and analyzed the experiments, and wrote the manuscript. Y.D. and J.Z., Z.Q. performed data collection and data analysis. S.SS. revised the manuscript. Z.C. statistical analysis. All the authors reviewed the results and approved the final version of the manuscript.

Data Availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

• References

• 1 Rugg-Gunn F, Miserocchi A, McEvoy A. Epilepsy surgery. Pract Neurol 2020; 20 (01) 4-14
• 2 Engel Jr J. Evolution of concepts in epilepsy surgery. Epileptic Disord 2019; 21 (05) 391-409
• 3 Cardinale F, Cossu M, Castana L. et al. Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures. Neurosurgery 2013; 72 (03) 353-366 , discussion 366
• 4 Gholipour T, Koubeissi MZ, Shields DC. Stereotactic electroencephalography. Clin Neurol Neurosurg 2020; 189: 105640
• 5 Vakharia VN, Sparks R, O'Keeffe AG. et al. Accuracy of intracranial electrode placement for stereoencephalography: a systematic review and meta-analysis. Epilepsia 2017; 58 (06) 921-932
• 6 van der Loo LE, Schijns OEMG, Hoogland G. et al. Methodology, outcome, safety and in vivo accuracy in traditional frame-based stereoelectroencephalography. Acta Neurochir (Wien) 2017; 159 (09) 1733-1746
• 7 Song S, Dai Y, Chen Z, Shi S. Accuracy and feasibility analysis of SEEG electrode implantation using the VarioGuide Frameless Navigation System in patients with drug-resistant epilepsy. J Neurol Surg A Cent Eur Neurosurg 2021; 82 (05) 430-436
• 8 Candela-Cantó S, Aparicio J, López JM. et al. Frameless robot-assisted stereoelectroencephalography for refractory epilepsy in pediatric patients: accuracy, usefulness, and technical issues. Acta Neurochir (Wien) 2018; 160 (12) 2489-2500
• 9 Zhang D, Cui X, Zheng J. et al. Neurosurgical robot-assistant stereoelectroencephalography system: operability and accuracy. Brain Behav 2021; 11 (10) e2347
• 10 Cardinale F, Rizzi M, d'Orio P. et al. A new tool for touch-free patient registration for robot-assisted intracranial surgery: application accuracy from a phantom study and a retrospective surgical series. Neurosurg Focus 2017; 42 (05) E8
• 11 Brandmeir NJ, Savaliya S, Rohatgi P, Sather M. The comparative accuracy of the ROSA stereotactic robot across a wide range of clinical applications and registration techniques. J Robot Surg 2018; 12 (01) 157-163
• 12 Spyrantis A, Cattani A, Strzelczyk A, Rosenow F, Seifert V, Freiman TM. Robot-guided stereoelectroencephalography without a computed tomography scan for referencing: Analysis of accuracy. Int J Med Robot 2018; 14 (02) 14
• 13 Lu C, Chen S, An Y. et al. How can the accuracy of SEEG be increased?: an analysis of the accuracy of multilobe-spanning SEEG electrodes based on a frameless stereotactic robot-assisted system. Ann Palliat Med 2021; 10 (04) 3699-3705
• 14 Abel TJ, Varela Osorio R, Amorim-Leite R. et al. Frameless robot-assisted stereoelectroencephalography in children: technical aspects and comparison with Talairach frame technique. J Neurosurg Pediatr 2018; 22 (01) 37-46
• 15 Liu W, Guo H, Du X. et al. Cortical vessel imaging and visualization for image guided depth electrode insertion. Comput Med Imaging Graph 2013; 37 (02) 123-130
• 16 Kwan P, Arzimanoglou A, Berg AT. et al. Definition of drug resistant epilepsy: consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies. Epilepsia 2010; 51 (06) 1069-1077
• 17 Isnard J, Taussig D, Bartolomei F. et al. French guidelines on stereoelectroencephalography (SEEG). Neurophysiol Clin 2018; 48 (01) 5-13
• 18 Mascia A, Casciato S, De Risi M. et al. Bilateral epileptogenesis in temporal lobe epilepsy due to unilateral hippocampal sclerosis: a case series. Clin Neurol Neurosurg 2021; 208: 106868
• 19 Liu Q, Mao Z, Wang J. et al. The accuracy of a novel self-tapping bone fiducial marker for frameless robot-assisted stereo-electro-encephalography implantation and registration techniques. Int J Med Robot 2023; 19 (02) e2479
• 20 Moles A, Guénot M, Rheims S. et al. SEEG-guided radiofrequency coagulation (SEEG-guided RF-TC) versus anterior temporal lobectomy (ATL) in temporal lobe epilepsy. J Neurol 2018; 265 (09) 1998-2004
• 21 Lee CY, Li HT, Wu T, Cheng MY, Lim SN, Lee ST. Efficacy of limited hippocampal radiofrequency thermocoagulation for mesial temporal lobe epilepsy. J Neurosurg 2018; 131 (03) 781-789
• 22 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) 1368-1374
• 23 Tabak J. Geometry: The Language of Space and Form. New York, NY:: Infobase Publishing;; 2014
• 24 Gomes FC, Larcipretti ALL, Nager G. et al. Robot-assisted vs. manually guided stereoelectroencephalography for refractory epilepsy: a systematic review and meta-analysis. Neurosurg Rev 2023; 46 (01) 102
• 25 Vasconcellos FN, Almeida T, Müller Fiedler A. et al. Robotic-assisted stereoelectroencephalography: a systematic review and meta-analysis of safety, outcomes, and precision in refractory epilepsy patients. Cureus 2023; 15 (10) e47675
• 26 González-Martínez J, Bulacio J, Thompson S. et al. Technique, results, and complications related to robot-assisted stereoelectroencephalography. Neurosurgery 2016; 78 (02) 169-180
• 27 Cardinale F, Casaceli G, Raneri F, Miller J, Lo Russo G. Implantation of stereoelectroencephalography electrodes: a systematic review. J Clin Neurophysiol 2016; 33 (06) 490-502
• 28 Guenot M, Isnard J, Ryvlin P. et al. Neurophysiological monitoring for epilepsy surgery: the Talairach SEEG method. StereoElectroEncephaloGraphy. Indications, results, complications and therapeutic applications in a series of 100 consecutive cases. Stereotact Funct Neurosurg 2001; 77 (1–4): 29-32
• 29 Derrey S, Lebas A, Parain D. et al. Delayed intracranial hematoma following stereoelectroencephalography for intractable epilepsy: case report. J Neurosurg Pediatr 2012; 10 (06) 525-528
• 30 Serletis D, Bulacio J, Bingaman W, Najm I, González-Martínez J. The stereotactic approach for mapping epileptic networks: a prospective study of 200 patients. J Neurosurg 2014; 121 (05) 1239-1246
• 31 Mullin JP, Shriver M, Alomar S. et al. Is SEEG safe? A systematic review and meta-analysis of stereo-electroencephalography-related complications. Epilepsia 2016; 57 (03) 386-401
• 32 Jung SC, Kang DW, Turan TN. Vessel and vessel wall imaging. Front Neurol Neurosci 2016; 40: 109-123
• 33 Li K, Vakharia VN, Sparks R. et al. Stereoelectroencephalography electrode placement: detection of blood vessel conflicts. Epilepsia 2019; 60 (09) 1942-1948
• 34 Feng AY, Ho AL, Kim LH. et al. Utilization of novel high-resolution, MRI-based vascular imaging modality for preoperative stereoelectroencephalography planning in children: a technical note. Stereotact Funct Neurosurg 2020; 98 (01) 1-7
• 35 Vakharia VN, Sparks R, Vos SB. et al. The effect of vascular segmentation methods on stereotactic trajectory planning for drug-resistant focal epilepsy: a retrospective cohort study. World Neurosurg X 2019; 4: 100057
• 36 Cardinale F, Pero G, Quilici L. et al. Cerebral angiography for multimodal surgical planning in epilepsy surgery: description of a new three-dimensional technique and literature review. World Neurosurg 2015; 84 (02) 358-367
• 37 Bourdillon P, Devaux B, Job-Chapron AS, Isnard J. SEEG-guided radiofrequency thermocoagulation. Neurophysiol Clin 2018; 48 (01) 59-64
• 38 Staudt MD, Maturu S, Miller JP. Radiofrequency energy and electrode proximity influences stereoelectroencephalography-guided radiofrequency thermocoagulation lesion size: an in vitro study with clinical correlation. Oper Neurosurg (Hagerstown) 2018; 15 (04) 461-469
• 39 Du X, Ding H, Zhou W, Zhang G, Wang G. Cerebrovascular segmentation and planning of depth electrode insertion for epilepsy surgery. Int J CARS 2013; 8 (06) 905-916
• 40 Ollivier I, Behr C, Cebula H. et al. Efficacy and safety in frameless robot-assisted stereo-electroencephalography (SEEG) for drug-resistant epilepsy. Neurochirurgie 2017; 63 (04) 286-290
• 41 Ho AL, Muftuoglu Y, Pendharkar AV. et al. Robot-guided pediatric stereoelectroencephalography: single-institution experience. J Neurosurg Pediatr 2018; 22 (05) 1-8
• 42 Iordanou JC, Camara D, Ghatan S, Panov F. Approach angle affects accuracy in robotic stereoelectroencephalography lead placement. World Neurosurg 2019; 128: e322-e328
• 43 Machetanz K, Grimm F, Wuttke TV. et al. Frame-based and robot-assisted insular stereo-electroencephalography via an anterior or posterior oblique approach. J Neurosurg 2021; 135 (05) 1477-1486
• 44 Yao Y, Hu W, Zhang C. et al. A comparison between robot-guided and stereotactic frame-based stereoelectroencephalography (SEEG) electrode implantation for drug-resistant epilepsy. J Robot Surg 2023; 17 (03) 1013-1020
• 45 Dedrickson T, Davidar AD, Azad TD, Theodore N, Anderson WS. Use of the Globus ExcelsiusGPS system for robotic stereoelectroencephalography: an initial experience. World Neurosurg 2023; 175: e686-e692
• 46 Li P, Zhou Y, Zhang Q. et al. Frameless robot-assisted stereoelectroencephalography-guided radiofrequency: methodology, results, complications and stereotactic application accuracy in pediatric hypothalamic hamartomas. Front Neurol 2023; 14: 1259171
• 47 Gorbachuk M, Machetanz K, Weinbrenner E. et al. Robot-assisted stereoencephalography vs subdural electrodes in the evaluation of temporal lobe epilepsy. Epilepsia Open 2023; 8 (03) 888-897

Publication History

Received: 25 July 2023

Accepted: 17 January 2024

Accepted Manuscript online:
04 April 2024

Article published online:
03 July 2024