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Doing More with Less: A Minimally Invasive, Cost-Conscious Approach to Stereoelectroencephalography
Journal Pre-proof Doing more with less: A minimally invasive, cost-conscious approach to stereoelectroencephalography Alexander C. Whiting, MD, Joshua S. Catapano, MD, Baltazar Zavala, MD, PhD, Corey T. Walker, MD, Jakub Godzik, MD, Tsinsue Chen, MD, Kris A. Smith, MD PII:
S1878-8750(19)32485-4
DOI:
https://doi.org/10.1016/j.wneu.2019.09.055
Reference:
WNEU 13354
To appear in:
World Neurosurgery
Received Date: 9 August 2019 Revised Date:
9 September 2019
Accepted Date: 10 September 2019
Please cite this article as: Whiting AC, Catapano JS, Zavala B, Walker CT, Godzik J, Chen T, Smith KA, Doing more with less: A minimally invasive, cost-conscious approach to stereoelectroencephalography, World Neurosurgery (2019), doi: https://doi.org/10.1016/j.wneu.2019.09.055. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Elsevier Inc. All rights reserved.
Doing more with less: A minimally invasive, cost-conscious approach to stereoelectroencephalography
Alexander C. Whiting, MD Joshua S. Catapano, MD Baltazar Zavala, MD, PhD Corey T. Walker, MD Jakub Godzik, MD Tsinsue Chen, MD Kris A. Smith, MD
Department of Neurosurgery Barrow Neurological Institute St. Joseph’s Hospital and Medical Center Phoenix, Arizona
Correspondence: Kris A. Smith, MD c/o Neuroscience Publications; Barrow Neurological Institute St. Joseph’s Hospital and Medical Center 350 W. Thomas Rd.; Phoenix, AZ 85013 Tel: 602.406.3593; Fax: 602.406.4104 E-mail: [email protected]
SUBMISSION CATEGORY: Doing more with less
RUNNING TITLE: A minimally invasive approach to SEEG
KEY WORDS: Epilepsy; functional neurosurgery; SEEG; stereoelectroencephalography
Whiting AC et al. 1 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch ABSTRACT Objective: Stereoelectroencephalography (SEEG) is a technique that is often used for mapping the epileptogenic zone before epilepsy surgery. Many SEEG depth electrode implantation techniques involve the use of extensive technological equipment and shaving of the patient’s entire head before electrode implantation. Our goal was to evaluate an SEEG depth electrode implantation technique that used readily available cost-effective neurosurgical equipment, was minimally invasive in nature, and required negligible hair shaving. Methods: Data on demographic characteristics, operative time, hemorrhagic complications, implantation complications, infection, morbidity, and mortality among patients who underwent this procedure were retrospectively reviewed. Results: Between April 2016 and March 2018, 23 patients underwent implantation of 213 depth electrodes with use of this technique. Mean (SD) operative time was 123 (32) minutes (range, 66–181 minutes). A mean (SD) of 9.3 (1.4) electrodes were placed for each patient (range, 8–13 electrodes). Two of the 213 electrodes (0.9%) were associated with postimplantation asymptomatic hemorrhage. One of the 213 electrodes (0.5%) was placed extradurally or incorrectly. None of the 213 electrodes were associated with symptomatic complications. No patients experienced infectious complications at any point in the preoperative, perioperative, or postoperative stages. Conclusions: This minimally invasive, cost-effective technique for SEEG depth electrode implantation is a safe, efficient method that uses basic neurosurgical equipment that is readily available. Utilization of this technique may be useful in neurosurgery centers with more limited resources. This study suggests that leaving patient hair largely intact throughout the procedure does not present an additional infection risk.
Whiting AC et al. 2 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch
INTRODUCTION Surgery for epilepsy can be a profoundly successful neurosurgical intervention in appropriately screened patients.[1] To maximize success, appropriate presurgical evaluation is necessary to precisely identify the epileptogenic tissue for surgery. Scalp electroencephalogram (EEG) is frequently limited in its ability to target and identify the source and spread of seizures.[2] Thus, invasive intracranial monitoring is often necessary. The stereotactic placement of intracranial depth electrodes for epilepsy monitoring, or stereoelectroencephalography (SEEG), was developed by Talairach and Bencaud in the 1960s.[3-5] Because SEEG is associated with a low rate of complications, allows simultaneous placement of bilateral electrodes, permits easy removal of electrodes, and can provide three-dimensional (3-D) maps of the epileptogenic zone, use of SEEG has increased over the past decade.[6] In 2016, SEEG overtook subdural grids as the most commonly performed procedure for intracranial monitoring in the US Medicare population.[7] With the increase in use, SEEG has undergone an explosion in technological advancements, and new practices have been developed for inserting the depth electrodes. While the original Talairach method was complex and time-intensive, newer methods for placing SEEG depth electrodes are associated with low complication profiles and significantly shorter implantation times.[8] Various technologies, including frames made with 3D printing and robotic assistance devices, are currently being used worldwide.[9,10] Despite extensive advancements in SEEG, most institutions routinely shave much or all of the patient’s head before placement of the SEEG depth electrodes. At our institution, we shave almost none of the patient’s hair, and we recently implemented a relatively simple, low-cost method for implanting SEEG depth electrodes without the use of complex technology. The goal of this study
Whiting AC et al. 3 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch was to evaluate the complication rate, infection rate, and operative time among patients who had undergone this procedure and compare these findings with those among patients treated with more technologically complex techniques currently available.
METHODS Patient Selection This study was conducted with approval by the St. Joseph’s Hospital and Medical Center Institutional Review Board for Human Research in Phoenix, Arizona. All patients provided informed consent for the SEEG procedure. Informed consent from the patients for data analyses presented in this study was not required because of the retrospective nature of the research. At our institution, patients are selected for SEEG after extensive evaluation by a multidisciplinary epilepsy team that includes our staff neurosurgeon, multiple epilepsy neurologists, neuropsychologists, and neuroradiologists. Preoperative evaluation includes a tailored combination of continuous video EEG in an epilepsy monitoring unit, magnetoencephalography, magnetic resonance imaging, positron emission tomography/computed tomography, intracarotid sodium amobarbital procedure, and a battery of neuropsychological testing. Medical management has failed for all patients evaluated for surgery. The goal of SEEG depth electrode implantation is to ascertain which, if any, surgical intervention is most appropriate for curative or palliative treatment of these patients’ epilepsy. Data for all patients who were recommended for and underwent SEEG depth electrode implantation on the basis of our modified, minimally invasive technique between April 2016 and March 2018 were retrospectively analyzed. Patient data were retrospectively reviewed regarding age, sex, age of epilepsy onset, prior surgical procedures, time of surgery, number and location of electrodes placed, and need for placement of
Whiting AC et al. 4 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch additional electrodes. Patient data were reviewed regarding intraoperative and postoperative complications, including hemorrhage, extradural placement of electrodes, infection, morbidity, and mortality. Data were collected regarding seizures recorded, laterality of seizures, whether SEEG monitoring led to surgery, and seizure outcome classification if surgery was performed. All surgical procedures were performed by the senior author (K.A.S.).
Technique Before surgery, a surgical plan is discussed and devised by the multidisciplinary epilepsy team regarding the number and trajectory of electrodes needed for appropriate intracranial monitoring. On the day of surgery, thin-cut magnetic resonance imaging, magnetoencephalography, and any other necessary imaging are loaded onto the StealthStation surgical navigation system (Medtronic). The patient is brought into the operating room and placed under general endotracheal anesthesia. The patient is then placed in 3-point fixation in the Mayfield clamp, typically in a neutral, supine position (Figure 1). The pins are placed far enough posteriorly to allow placement of frontal and temporal electrodes bilaterally without difficulty. If electrodes are planned in posterior locations, such as the occipital lobe, the pin placement can be adjusted to allow comfortable placement of the electrodes in these locations. A patient-tracking reference is attached to the Mayfield clamp with a multifunctional arm. The Stealth (Medtronic) registration probe is used to trace the surface of the face and scalp, registering the patient with the image guidance system. Accuracy is verified using the probe by correlating anatomic landmarks with imaging findings. Using the probe, potential trajectories are planned bilaterally. Trajectories are tailored on the basis of the conclusions of the multidisciplinary epilepsy team, but they frequently involve
Whiting AC et al. 5 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch amygdala, hippocampus, cingulate, and orbitofrontal gyrus electrode placement. Numerous additional electrodes are specifically tailored for 3-D coverage of magnetoencephalography spike clusters if such clusters are present. Care is taken to ensure that each trajectory plan avoids all surface vasculature and avoids traversing sulci. Each trajectory plan is named and saved for later use, after the patient is prepped and draped. At each site where an electrode is to be implanted, a small 0.5 × 0.5-cm area is shaved. The remaining hair is combed and braided as necessary to allow an extensive sterile preparation of the head while still allowing easy identification of the shaved areas. The hair and scalp are extensively prepared for surgery with a povidone-iodine solution. The patient is draped sterilely, and a Vertek (Medtronic) precision-aiming, multifunctional arm is attached to the Mayfield clamp. Starting on one side, the SEEG depth electrodes are then placed systematically one at a time using the same step-wise protocol. The Stealth image guidance probe is used to recreate the previously determined trajectory over one of the shaved regions. Using the StealthStation, the distance to the targeted location is measured. The Vertek arm is aligned along the desired trajectory using the image guidance probe and locked in place (Figure 2A). A small stab incision is made at the entry site. Reducing tubes are placed into the Vertek arm. The Triton (Medtronic) high-speed drill with 2.4-mm drill bit is advanced through the reducing tubes and then through the incision to the outer cortex of the skull. The drill is used to create a guidance hole through the skull, and a drill stop is attached to the bit at the estimated skull thickness depth to avoid plunging through the dura after perforating the inner cortex of the skull (Figure 2B). The anchor bolt (PMT, Chanhassen) is guided down the reducing tube into the twist drill hole. A small piercing probe is carefully inserted through the anchor bolt to penetrate the dura and ensure the electrode will pass easily without resistance (Figure 2C). The 0.8-mm-diameter PMT electrode is
Whiting AC et al. 6 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch then carefully measured to the appropriate depth, which is measured with the Stealth probe from the top of the anchor bolt to the predetermined target point on the specific trajectory plan, and the depth is marked using the electrode locking cap (Figure 2D). The Vertek arm is then loosened and moved to the next location. The electrode is placed down the bolt into the brain to the level of the locking cap at the previously tailored measurement and is sealed in place (Figure 3). All electrodes are placed systematically using this technique. The patient’s head is then carefully wrapped in gauze and removed from the Mayfield clamp. Intraoperative CT with either the Bodytom (Samsung) or the O-Arm (Medtronic) is obtained while the patient is still under anesthesia to ensure satisfactory electrode position relative to the planned trajectories before leaving the operating room. The patient is extubated and taken to the postanesthesia care unit. The patients are monitored for several days in an epilepsy monitoring unit under the care of the neurology team. SEEG data are recorded, and after sufficient information has been collected, the decision is made to either proceed with or abstain from additional surgery. Patients then return to the operating room at the end of the monitoring period for removal of the SEEG depth electrodes and implementation of the surgical procedure designated by the epilepsy team. Patients who are not recommended for additional surgery at that time or are recommended for surgery in a delayed fashion have only their depth electrodes removed.
RESULTS Demographics Twenty-three patients underwent SEEG depth electrode implantation with the modified technique. Patient demographic characteristics are included in Table 1. The mean (standard deviation [SD]) age of included patients was 32.4 (10.4) years (range, 18–57 years). The mean
Whiting AC et al. 7 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch (SD) length of time since receiving a diagnosis of epilepsy was 14.4 (8.7) years (range, 3–34.7 years). Sixteen patients were male, and 7 patients were female. Seventeen patients had no prior cranial surgery. The 6 patients with prior surgery included 3 patients who had undergone prior resective epilepsy surgery, 1 patient who had undergone resection of a low grade tumor, 1 patient who had undergone ventriculoperitoneal shunt placement, and 1 patient who had undergone evacuation of a traumatic epidural hematoma.
SEEG Depth Electrode Implantation A total of 213 SEEG depth electrodes were implanted in the 23 patients. A total of 118 depth electrodes were placed on the left side of the brain, and 95 depth electrodes were placed on the right side of the brain (Table 1). The mean (SD) duration of the procedure from the start of the first incision to when the patient was taken out of the head clamp was 123 (32) minutes (range, 66–181 minutes). A mean (SD) of 9.3 (1.4) electrodes were placed in each patient (range, 8–13 electrodes). A mean operative duration of 13.2 minutes per electrode was calculated on the basis of these data. Two of the 23 patients (8.7%) experienced a complication related to SEEG depth electrode implantation. Three of 213 (1.4%) electrodes placed were associated with complications. One electrode was placed extradurally and was not replaced or removed until after SEEG monitoring was complete. No other electrodes were placed incorrectly. In another patient, 2 electrodes were associated with small hemorrhages. One electrode caused trace subarachnoid blood around the entry site, and 1 electrode caused a delayed, asymptomatic intraparenchymal hemorrhage. None of the 213 implanted electrodes were associated with symptomatic complications. Patients were monitored in a dedicated epilepsy monitoring unit using the implanted SEEG depth electrodes for a mean (SD) of 7.6 (2.5) days (range, 5–14 days).
Whiting AC et al. 8 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch All 23 patients had seizures recorded during the monitoring phase. Nine of 23 (39.1%) had bilateral seizures recorded.
Surgical Outcomes Fifteen of 23 patients had resective surgery performed after monitoring was complete. Eight of 23 patients (34.8%) did not undergo resective surgery: 3 patients had vagal nerve stimulators placed, 1 patient had a responsive neurostimulation system placed in a delayed fashion, and 4 patients had depth electrodes removed with no further surgery performed. Among the 15 patients who underwent resective surgery, seizure outcome follow-up was performed at a mean (SD) of 7.8 (7.2) months after surgery (range, 1–26 months). Six patients had Engel class I seizure outcomes, 5 patients had Engel class II seizure outcomes, 4 patients had Engel class III seizure outcomes, and no patients had Engel class IV seizure outcomes.[11]
Complications Complications related to depth electrode placement are mentioned above, and all complications are detailed in Table 2. No patients experienced complications throughout monitoring. Two of 23 (9%) patients experienced perioperative or postoperative complications after monitoring was complete. One patient experienced status epilepticus 13 days after a resective surgical procedure tailored to his SEEG monitoring results. Status epilepticus resolved with treatment, and the patient was asymptomatic after recovery.. Despite shaving only a small area of each patient’s head, no infections were recorded at any point in the patients’ monitoring, perioperative procedures, or postoperative recovery.
Whiting AC et al. 9 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch DISCUSSION SEEG has become a pivotal tool in the work-up for intractable, medication-resistant epilepsy. The ability to create a 3-D map of the epileptogenic zone and seizure spread through a relatively minimalistic, bilateral approach has revolutionized preoperative invasive monitoring. As our experience with SEEG has increased over the past several decades, several new techniques have been proposed and evaluated, many involving new technology. Table 3 highlights several studies that specifically analyze these various techniques, their complication profiles, and their operative times. Our goal was to evaluate an SEEG depth electrode implantation technique that used readily available, cost-effective neurosurgical equipment along these same parameters. In addition, many epilepsy surgical centers will shave the patient’s entire head, or at least a large portion of it, for ease of placement of the SEEG electrodes.[9,12,13] Our technique involves shaving only a small portion of the patient’s head, and frequently it can be difficult to tell that any hair has been shaved at all. We also attempted to evaluate the infection risk of placing SEEG electrodes with this minimal shaving technique. Our study involved 23 patients and 213 SEEG depth electrodes that were implanted with use of this technique. Two of 213 (0.9%) of the implanted electrodes were associated with hemorrhage during placement. One of 213 (0.5%) of the implanted electrodes was placed outside the dura, which did not require any additional surgery. No patients had symptomatic complications or died. These complication rates are low and compare favorably with those associated with other techniques (Table 3). A large meta-analysis of SEEG safety by Mullin et al.[8] found that 1.0% of electrodes were associated with hemorrhagic complications. They also found a 0.3% mortality rate. The number of subjects and number of electrodes placed in our study were comparable to other recently published techniques (Table 3). All of the studied
Whiting AC et al. 10 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch techniques, including ours, use a relatively similar method for the actual placement of the bolt and the advancement of the electrode into the brain, so it is not surprising to have relatively similar rates of complications such as hemorrhage and mortality. The infection rate in our study was 0%. No patients experienced any infectious complications at any point in their preoperative, perioperative, or postoperative stages. This compares favorably to the 0.8% risk of infection found in the meta-analysis by Mullin et al.[8] Numerous studies in the neurosurgical literature have demonstrated that there is no conclusive evidence that shaving a patient’s head before performing neurosurgery reduces infection risk.[14,15] Because of the multiple wires coming out of the head during SEEG monitoring, it seems counterintuitive that a large swath of hair around the wires would not present a problem, but in our experience it does not increase the difficulty of performing electrode implantation. Quick but careful combing and braiding of even the longest, thickest hair can provide easy, clear access to the areas for electrode implantation. This study suggests that leaving the hair in place does not present additional infection risk. As shaving the head can be traumatic and potentially discouraging for patients, it seems reasonable to avoid this result if at all possible. While recent studies have demonstrated the cost-effectiveness of SEEG and surgical intervention compared with nonintervention, to our knowledge no study has analyzed the direct costs of different SEEG techniques.[16] Individual hospital expenses of purchasing a robotic arm or 3-D-printed frames are not readily available, but these represent technologies that certainly cost more than using the equipment already readily available in most operating rooms. The equipment used for SEEG depth electrode implantation at our institution is normally used for standard image-guided biopsies such as those frequently performed at all major neurosurgical centers. While much of the new SEEG technology is exciting and will continue to improve and
Whiting AC et al. 11 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch evolve, many neurosurgery centers around the world may not have access to or be able to afford this novel equipment and can use this relatively cost-effective technique. The pre-operative evaluation and invasive monitoring for potential epilepsy surgery is already an expensive, laborintensive process. By utilizing standard neurosurgical equipment for SEEG, neurosurgical centers in countries with more limited resources may find this technique practical. Conversely, it should be noted that this technique, while utilizing more basic neurosurgery equipment than many current SEEG electrode placement techniques, still requires the use of neuronavigation, SEEG depth electrodes, and post-operative epilepsy monitoring in an epilepsy monitoring unit. This all requires a level of resource-commitment that may not be available in many neurosurgical centers in lower-resource areas of the world. The goal of SEEG depth electrode implantation and monitoring is to create a functional 3-D map of the epileptogenic zone. The preoperative hypothesis about the location of the epileptogenic zone created by the multidisciplinary epilepsy team is the most important aspect in determining the perioperative placement of the implanted SEEG depth electrodes.[9] In our technique, with use of the hypothesis determined by the multidisciplinary epilepsy team, the electrode trajectories are mapped out and chosen after the patient is intubated and fixated in the Mayfield clamp. This allows the planning and implantation portions of the procedure to occur quickly and seamlessly. Our operative time and time per electrode compared favorably with the other studies that analyzed operative time (Table 3). This study has several limitations. The study was limited by its retrospective nature. While the number of patients and electrodes in this study is comparable to several other SEEG technique studies, these are relatively small numbers and may not accurately detect differences in complication rates when these rates are inherently low. Because there was frequently no
Whiting AC et al. 12 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch preoperative trajectory plan created with this technique, we were unable to directly measure deviation of the depth electrode from its presumed trajectory, but only one electrode was considered to be misplaced on postoperative computed tomography. Because this was not a comparison study, it is difficult to determine differences between our technique and other techniques with respect to complication rates and operative techniques. Additionally, it should be noted that our operative technique shares similarities to other frameless, neuronavigation-based techniques (Table 3) with that exception that our technique involves negligible hair shaving.
CONCLUSION This study highlights a minimally invasive, cost-conscious technique for SEEG depth electrode implantation that results in complication profiles and operative times comparable to those associated with other techniques. Utilization of this technique may be useful in neurosurgery centers with more limited resources. Although we shaved only a small area of each patient’s head, the infection rate was 0%, which suggests that this method does not increase the likelihood of infection during implantation and monitoring.
Whiting AC et al. 13 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch ACKNOWLEDGMENTS: We thank the staff of Neuroscience Publications at Barrow Neurological Institute for assistance with manuscript preparation.
REFERENCES 1. Wiebe S, Blume WT, Girvin JP, et al. A randomized, controlled trial of surgery for temporallobe epilepsy. N Engl J Med. 2001;345:311-318. 2. Enatsu R, Mikuni N. Invasive evaluations for epilepsy surgery: a review of the literature. Neurol Med Chir (Tokyo). 2016;56:221-227. 3. Bancaud J, Angelergues R, Bernouilli C, et al. Functional stereotaxic exploration (SEEG) of epilepsy. Electroencephalogr Clin Neurophysiol. 1970;28:85-86. 4. Dorfer C, Stefanits H, Pataraia E, et al. Frameless stereotactic drilling for placement of depth electrodes in refractory epilepsy: operative technique and initial experience. Neurosurgery. 2014;10 Suppl 4:582-590; discussion 590-581. 5. Isnard J, Taussig D, Bartolomei F, et al. French guidelines on stereoelectroencephalography (SEEG). Neurophysiol Clin. 2018;48:5-13. 6. Podkorytova I, Hoes K, Lega B. Stereo-encephalography versus subdural electrodes for seizure localization. Neurosurg Clin N Am. 2016;27:97-109. 7. Abou-Al-Shaar H, Brock AA, Kundu B, et al. Increased nationwide use of stereoencephalography for intracranial epilepsy electroencephalography recordings. J Clin Neurosci. 2018;53:132-134. 8. Mullin JP, Shriver M, Alomar S, et al. Is SEEG safe? A systematic review and meta-analysis of stereo-electroencephalography-related complications. Epilepsia. 2016;57:386-401.
Whiting AC et al. 14 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch 9. Gonzalez-Martinez J, Bulacio J, Thompson S, et al. Technique, results, and complications related to robot-assisted stereoelectroencephalography. Neurosurgery. 2016;78:169-180. 10. Dewan MC, Shults R, Hale AT, et al. Stereotactic EEG via multiple single-path omnidirectional trajectories within a single platform: institutional experience with a novel technique. J Neurosurg. 2018;129:1173-1181. 11. Engel J. Surgical Treatment of Epilepsies, 2nd ed: Raven Press; 1993. 12. Dorfer C, Minchev G, Czech T, et al. A novel miniature robotic device for frameless implantation of depth electrodes in refractory epilepsy. J Neurosurg. 2017;126:16221628. 13. Nowell M, Rodionov R, Diehl B, et al. A novel method for implementation of frameless StereoEEG in epilepsy surgery. Neurosurgery. 2014;10 Suppl 4:525-533; discussion 533524. 14. Broekman ML, van Beijnum J, Peul WC, et al. Neurosurgery and shaving: what's the evidence? J Neurosurg. 2011;115:670-678. 15. Horgan MA, Kernan JC, Schwartz MS, et al. Shaveless brain surgery: safe, well tolerated, and cost effective. Skull Base Surg. 1999;9:253-258. 16. Garcia-Lorenzo B, Del Pino-Sedeno T, Rocamora R, et al. Stereoelectroencephalography for refractory epileptic patients considered for surgery: systematic review, meta-analysis, and economic evaluation. Neurosurgery. 2019;84:326-338. 17. Gonzalez-Martinez J, Mullin J, Vadera S, et al. Stereotactic placement of depth electrodes in medically intractable epilepsy. J Neurosurg. 2014;120:639-644.
Whiting AC et al. 15 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch 18. Balanescu B, Franklin R, Ciurea J, et al. A personalized stereotactic fixture for implantation of depth electrodes in stereoelectroencephalography. Stereotact Funct Neurosurg. 2014;92:117-125. 19. Narvaez-Martinez Y, Garcia S, Roldan P, et al. [Stereoelectroencephalography by using OArm((R)) and Vertek((R)) passive articulated arm: technical note and experience of an epilepsy referral centre]. Neurocirugia (Astur). 2016;27:277-284. 20. Yu H, Pistol C, Franklin R, et al. Clinical accuracy of customized stereotactic fixtures for stereoelectroencephalography. World Neurosurg. 2018;109:82-88. 21. 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;22:37-46. 22. Ho AL, Muftuoglu Y, Pendharkar AV, et al. Robot-guided pediatric stereoelectroencephalography: single-institution experience. J Neurosurg Pediatr. 2018;22:1-8.
Whiting AC et al. 16 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch FIGURE LEGENDS Figure 1. Patient positioning prior to stereoelectroencephalography depth electrode implantation. Used with permission from Barrow Neurological Institute, Phoenix, Arizona. Figure 2. Stereoelectroencephalography depth electrode implantation steps. (A) Trajectory planning using the image guidance probe through the Vertek (Medtronic) arm. (B) After a stab skin incision, the guidance hole is drilled using a high-speed drill. (C) The bolt is attached to the skull. (D) The length of the electrode to be placed intracranially is measured, and then the electrode is placed through the bolt to this preplanned measurement. Used with permission from Barrow Neurological Institute, Phoenix, Arizona. Figure 3. Final position of the stereoelectroencephalography depth electrode demonstrating minimal hair shaving. Used with permission from Barrow Neurological Institute, Phoenix, Arizona.
Whiting AC et al. 17 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch Table 1. Demographic and SEEG characteristics of patients with stereoelectroencephalography (SEEG) depth electrode implantation Characteristic No. (%)* Sex Male 16 (70) Female 7 (30) Prior surgery Yes 6 (26) No 17 (74) Resective surgery after monitoring Yes 15 (65) No 8 (35) Age, mean (SD), y 32.4 (10.4) Time since epilepsy diagnosis, mean (SD), y 14.4 (8.7) No. of depth electrodes placed, mean (SD) 9.3 (1.4) Duration of SEEG monitoring, mean (SD), d 7.6 (2.5) Electrode placement location Left Right Frontal 41 31 72 (34) Cingulum 15 15 30 (14) Amygdala 18 16 34 (16) Hippocampus 21 19 40 (19) Other temporal 10 6 16 (8) Parietal 5 4 9 (4) Insular 1 4 5 (2) Occipital 7 0 7 (3) Total electrodes placed 118 95 213 (100) *Data are no. (%) of patients unless otherwise indicated. SD, standard deviation
Whiting AC et al. 18 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch Table 2. Complications related to stereoelectroencephalography (SEEG) depth electrode placement, monitoring, and removal Complication No. (%) Electrodes (n=213) Hemorrhage from electrode placement 2 (0.9) Extradural placement 1 (0.5) Patients (n=23) Complications during monitoring 0 (0) Infection 0 (0) Symptomatic complications from SEEG implantation, monitoring, or removal 0 (0)
Whiting AC et al. 19 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch Table 3. Studies reviewing operating room time and complications after stereoelectroencephalography (SEEG) depth electrode implantation with different techniques Study Nowell et al. 2014[13] GonzalezMartinez et al. 2014[17] Dorfer et al. 2014[4] Balanescu et al. 2014[18] GonzalezMartinez et al. 2016[9] NarvaezMartinez et al. 2016[19] Yu et al. 2017[20] Dewan et al. 2017[10] Abel et al. 2018[21]
Dorfer et al. 2018[12] Ho et al. 2018[22]
Mortality 0
Operative Time (min) 137.0
Time Per Electrode (min) 16.1
No. of Electrodes 187
N/A
0
107.0
8.2
1586
0
N/A
0
70.9
19.1
26
0
0
N/A
0
182.0
14.0
52
100
4
1
N/A
0
130.0
10.4
1245
Prospective
10
0
0
N/A
0
239.0
34.6
69
Retrospective
21
1
0
N/A
0
124.0
15.1
173
Retrospective
15
N/A
N/A
N/A
N/A
207.0
22.7
137
Retrospective
17
5
1
N/A
0
304.0
19.5
265
Retrospective
18
2
1
N/A
0
352.0
24.0
264
Retrospective
16
0
0
1
0
91.3
15.7
93
Retrospective
20
0
0
0
0
117.0
10.5
222
Study Design Retrospective
No. of Subjects 22
Prospective
Neuronavigation, frameless 3-D-printed fixture, frameless Robot-assisted, frameless (ROSA) Neuronavigation, frameless 3-D-printed fixture, frameless 3-D-printed fixture, frameless Robot-assisted, frameless (ROSA) Talairach framebased Robot-assisted, frameless (iSys1) Robot-assisted, frameless
Technique Neuronavigation, frameless Frame-based
Hematoma 1
Symptomatic Hematoma 0
Infection 0
122
3
0
Retrospective
7
0
Retrospective
4
Prospective
Whiting AC et al. 20 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch (ROSA)
Abbreviations: N/A, not available; 3-D, three dimensional.
ABBREVIATIONS: EEG, electroencephalogram; SD, standard deviation; SEEG, stereoelectroencephalography; 3-D, three-dimensional
DISCLOSURES: None. FINANCIAL SUPPORT: None. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
S1878-8750(19)32485-4
DOI:
https://doi.org/10.1016/j.wneu.2019.09.055
Reference:
WNEU 13354
To appear in:
World Neurosurgery
Received Date: 9 August 2019 Revised Date:
9 September 2019
Accepted Date: 10 September 2019
Please cite this article as: Whiting AC, Catapano JS, Zavala B, Walker CT, Godzik J, Chen T, Smith KA, Doing more with less: A minimally invasive, cost-conscious approach to stereoelectroencephalography, World Neurosurgery (2019), doi: https://doi.org/10.1016/j.wneu.2019.09.055. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Elsevier Inc. All rights reserved.
Doing more with less: A minimally invasive, cost-conscious approach to stereoelectroencephalography
Alexander C. Whiting, MD Joshua S. Catapano, MD Baltazar Zavala, MD, PhD Corey T. Walker, MD Jakub Godzik, MD Tsinsue Chen, MD Kris A. Smith, MD
Department of Neurosurgery Barrow Neurological Institute St. Joseph’s Hospital and Medical Center Phoenix, Arizona
Correspondence: Kris A. Smith, MD c/o Neuroscience Publications; Barrow Neurological Institute St. Joseph’s Hospital and Medical Center 350 W. Thomas Rd.; Phoenix, AZ 85013 Tel: 602.406.3593; Fax: 602.406.4104 E-mail: [email protected]
SUBMISSION CATEGORY: Doing more with less
RUNNING TITLE: A minimally invasive approach to SEEG
KEY WORDS: Epilepsy; functional neurosurgery; SEEG; stereoelectroencephalography
Whiting AC et al. 1 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch ABSTRACT Objective: Stereoelectroencephalography (SEEG) is a technique that is often used for mapping the epileptogenic zone before epilepsy surgery. Many SEEG depth electrode implantation techniques involve the use of extensive technological equipment and shaving of the patient’s entire head before electrode implantation. Our goal was to evaluate an SEEG depth electrode implantation technique that used readily available cost-effective neurosurgical equipment, was minimally invasive in nature, and required negligible hair shaving. Methods: Data on demographic characteristics, operative time, hemorrhagic complications, implantation complications, infection, morbidity, and mortality among patients who underwent this procedure were retrospectively reviewed. Results: Between April 2016 and March 2018, 23 patients underwent implantation of 213 depth electrodes with use of this technique. Mean (SD) operative time was 123 (32) minutes (range, 66–181 minutes). A mean (SD) of 9.3 (1.4) electrodes were placed for each patient (range, 8–13 electrodes). Two of the 213 electrodes (0.9%) were associated with postimplantation asymptomatic hemorrhage. One of the 213 electrodes (0.5%) was placed extradurally or incorrectly. None of the 213 electrodes were associated with symptomatic complications. No patients experienced infectious complications at any point in the preoperative, perioperative, or postoperative stages. Conclusions: This minimally invasive, cost-effective technique for SEEG depth electrode implantation is a safe, efficient method that uses basic neurosurgical equipment that is readily available. Utilization of this technique may be useful in neurosurgery centers with more limited resources. This study suggests that leaving patient hair largely intact throughout the procedure does not present an additional infection risk.
Whiting AC et al. 2 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch
INTRODUCTION Surgery for epilepsy can be a profoundly successful neurosurgical intervention in appropriately screened patients.[1] To maximize success, appropriate presurgical evaluation is necessary to precisely identify the epileptogenic tissue for surgery. Scalp electroencephalogram (EEG) is frequently limited in its ability to target and identify the source and spread of seizures.[2] Thus, invasive intracranial monitoring is often necessary. The stereotactic placement of intracranial depth electrodes for epilepsy monitoring, or stereoelectroencephalography (SEEG), was developed by Talairach and Bencaud in the 1960s.[3-5] Because SEEG is associated with a low rate of complications, allows simultaneous placement of bilateral electrodes, permits easy removal of electrodes, and can provide three-dimensional (3-D) maps of the epileptogenic zone, use of SEEG has increased over the past decade.[6] In 2016, SEEG overtook subdural grids as the most commonly performed procedure for intracranial monitoring in the US Medicare population.[7] With the increase in use, SEEG has undergone an explosion in technological advancements, and new practices have been developed for inserting the depth electrodes. While the original Talairach method was complex and time-intensive, newer methods for placing SEEG depth electrodes are associated with low complication profiles and significantly shorter implantation times.[8] Various technologies, including frames made with 3D printing and robotic assistance devices, are currently being used worldwide.[9,10] Despite extensive advancements in SEEG, most institutions routinely shave much or all of the patient’s head before placement of the SEEG depth electrodes. At our institution, we shave almost none of the patient’s hair, and we recently implemented a relatively simple, low-cost method for implanting SEEG depth electrodes without the use of complex technology. The goal of this study
Whiting AC et al. 3 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch was to evaluate the complication rate, infection rate, and operative time among patients who had undergone this procedure and compare these findings with those among patients treated with more technologically complex techniques currently available.
METHODS Patient Selection This study was conducted with approval by the St. Joseph’s Hospital and Medical Center Institutional Review Board for Human Research in Phoenix, Arizona. All patients provided informed consent for the SEEG procedure. Informed consent from the patients for data analyses presented in this study was not required because of the retrospective nature of the research. At our institution, patients are selected for SEEG after extensive evaluation by a multidisciplinary epilepsy team that includes our staff neurosurgeon, multiple epilepsy neurologists, neuropsychologists, and neuroradiologists. Preoperative evaluation includes a tailored combination of continuous video EEG in an epilepsy monitoring unit, magnetoencephalography, magnetic resonance imaging, positron emission tomography/computed tomography, intracarotid sodium amobarbital procedure, and a battery of neuropsychological testing. Medical management has failed for all patients evaluated for surgery. The goal of SEEG depth electrode implantation is to ascertain which, if any, surgical intervention is most appropriate for curative or palliative treatment of these patients’ epilepsy. Data for all patients who were recommended for and underwent SEEG depth electrode implantation on the basis of our modified, minimally invasive technique between April 2016 and March 2018 were retrospectively analyzed. Patient data were retrospectively reviewed regarding age, sex, age of epilepsy onset, prior surgical procedures, time of surgery, number and location of electrodes placed, and need for placement of
Whiting AC et al. 4 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch additional electrodes. Patient data were reviewed regarding intraoperative and postoperative complications, including hemorrhage, extradural placement of electrodes, infection, morbidity, and mortality. Data were collected regarding seizures recorded, laterality of seizures, whether SEEG monitoring led to surgery, and seizure outcome classification if surgery was performed. All surgical procedures were performed by the senior author (K.A.S.).
Technique Before surgery, a surgical plan is discussed and devised by the multidisciplinary epilepsy team regarding the number and trajectory of electrodes needed for appropriate intracranial monitoring. On the day of surgery, thin-cut magnetic resonance imaging, magnetoencephalography, and any other necessary imaging are loaded onto the StealthStation surgical navigation system (Medtronic). The patient is brought into the operating room and placed under general endotracheal anesthesia. The patient is then placed in 3-point fixation in the Mayfield clamp, typically in a neutral, supine position (Figure 1). The pins are placed far enough posteriorly to allow placement of frontal and temporal electrodes bilaterally without difficulty. If electrodes are planned in posterior locations, such as the occipital lobe, the pin placement can be adjusted to allow comfortable placement of the electrodes in these locations. A patient-tracking reference is attached to the Mayfield clamp with a multifunctional arm. The Stealth (Medtronic) registration probe is used to trace the surface of the face and scalp, registering the patient with the image guidance system. Accuracy is verified using the probe by correlating anatomic landmarks with imaging findings. Using the probe, potential trajectories are planned bilaterally. Trajectories are tailored on the basis of the conclusions of the multidisciplinary epilepsy team, but they frequently involve
Whiting AC et al. 5 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch amygdala, hippocampus, cingulate, and orbitofrontal gyrus electrode placement. Numerous additional electrodes are specifically tailored for 3-D coverage of magnetoencephalography spike clusters if such clusters are present. Care is taken to ensure that each trajectory plan avoids all surface vasculature and avoids traversing sulci. Each trajectory plan is named and saved for later use, after the patient is prepped and draped. At each site where an electrode is to be implanted, a small 0.5 × 0.5-cm area is shaved. The remaining hair is combed and braided as necessary to allow an extensive sterile preparation of the head while still allowing easy identification of the shaved areas. The hair and scalp are extensively prepared for surgery with a povidone-iodine solution. The patient is draped sterilely, and a Vertek (Medtronic) precision-aiming, multifunctional arm is attached to the Mayfield clamp. Starting on one side, the SEEG depth electrodes are then placed systematically one at a time using the same step-wise protocol. The Stealth image guidance probe is used to recreate the previously determined trajectory over one of the shaved regions. Using the StealthStation, the distance to the targeted location is measured. The Vertek arm is aligned along the desired trajectory using the image guidance probe and locked in place (Figure 2A). A small stab incision is made at the entry site. Reducing tubes are placed into the Vertek arm. The Triton (Medtronic) high-speed drill with 2.4-mm drill bit is advanced through the reducing tubes and then through the incision to the outer cortex of the skull. The drill is used to create a guidance hole through the skull, and a drill stop is attached to the bit at the estimated skull thickness depth to avoid plunging through the dura after perforating the inner cortex of the skull (Figure 2B). The anchor bolt (PMT, Chanhassen) is guided down the reducing tube into the twist drill hole. A small piercing probe is carefully inserted through the anchor bolt to penetrate the dura and ensure the electrode will pass easily without resistance (Figure 2C). The 0.8-mm-diameter PMT electrode is
Whiting AC et al. 6 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch then carefully measured to the appropriate depth, which is measured with the Stealth probe from the top of the anchor bolt to the predetermined target point on the specific trajectory plan, and the depth is marked using the electrode locking cap (Figure 2D). The Vertek arm is then loosened and moved to the next location. The electrode is placed down the bolt into the brain to the level of the locking cap at the previously tailored measurement and is sealed in place (Figure 3). All electrodes are placed systematically using this technique. The patient’s head is then carefully wrapped in gauze and removed from the Mayfield clamp. Intraoperative CT with either the Bodytom (Samsung) or the O-Arm (Medtronic) is obtained while the patient is still under anesthesia to ensure satisfactory electrode position relative to the planned trajectories before leaving the operating room. The patient is extubated and taken to the postanesthesia care unit. The patients are monitored for several days in an epilepsy monitoring unit under the care of the neurology team. SEEG data are recorded, and after sufficient information has been collected, the decision is made to either proceed with or abstain from additional surgery. Patients then return to the operating room at the end of the monitoring period for removal of the SEEG depth electrodes and implementation of the surgical procedure designated by the epilepsy team. Patients who are not recommended for additional surgery at that time or are recommended for surgery in a delayed fashion have only their depth electrodes removed.
RESULTS Demographics Twenty-three patients underwent SEEG depth electrode implantation with the modified technique. Patient demographic characteristics are included in Table 1. The mean (standard deviation [SD]) age of included patients was 32.4 (10.4) years (range, 18–57 years). The mean
Whiting AC et al. 7 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch (SD) length of time since receiving a diagnosis of epilepsy was 14.4 (8.7) years (range, 3–34.7 years). Sixteen patients were male, and 7 patients were female. Seventeen patients had no prior cranial surgery. The 6 patients with prior surgery included 3 patients who had undergone prior resective epilepsy surgery, 1 patient who had undergone resection of a low grade tumor, 1 patient who had undergone ventriculoperitoneal shunt placement, and 1 patient who had undergone evacuation of a traumatic epidural hematoma.
SEEG Depth Electrode Implantation A total of 213 SEEG depth electrodes were implanted in the 23 patients. A total of 118 depth electrodes were placed on the left side of the brain, and 95 depth electrodes were placed on the right side of the brain (Table 1). The mean (SD) duration of the procedure from the start of the first incision to when the patient was taken out of the head clamp was 123 (32) minutes (range, 66–181 minutes). A mean (SD) of 9.3 (1.4) electrodes were placed in each patient (range, 8–13 electrodes). A mean operative duration of 13.2 minutes per electrode was calculated on the basis of these data. Two of the 23 patients (8.7%) experienced a complication related to SEEG depth electrode implantation. Three of 213 (1.4%) electrodes placed were associated with complications. One electrode was placed extradurally and was not replaced or removed until after SEEG monitoring was complete. No other electrodes were placed incorrectly. In another patient, 2 electrodes were associated with small hemorrhages. One electrode caused trace subarachnoid blood around the entry site, and 1 electrode caused a delayed, asymptomatic intraparenchymal hemorrhage. None of the 213 implanted electrodes were associated with symptomatic complications. Patients were monitored in a dedicated epilepsy monitoring unit using the implanted SEEG depth electrodes for a mean (SD) of 7.6 (2.5) days (range, 5–14 days).
Whiting AC et al. 8 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch All 23 patients had seizures recorded during the monitoring phase. Nine of 23 (39.1%) had bilateral seizures recorded.
Surgical Outcomes Fifteen of 23 patients had resective surgery performed after monitoring was complete. Eight of 23 patients (34.8%) did not undergo resective surgery: 3 patients had vagal nerve stimulators placed, 1 patient had a responsive neurostimulation system placed in a delayed fashion, and 4 patients had depth electrodes removed with no further surgery performed. Among the 15 patients who underwent resective surgery, seizure outcome follow-up was performed at a mean (SD) of 7.8 (7.2) months after surgery (range, 1–26 months). Six patients had Engel class I seizure outcomes, 5 patients had Engel class II seizure outcomes, 4 patients had Engel class III seizure outcomes, and no patients had Engel class IV seizure outcomes.[11]
Complications Complications related to depth electrode placement are mentioned above, and all complications are detailed in Table 2. No patients experienced complications throughout monitoring. Two of 23 (9%) patients experienced perioperative or postoperative complications after monitoring was complete. One patient experienced status epilepticus 13 days after a resective surgical procedure tailored to his SEEG monitoring results. Status epilepticus resolved with treatment, and the patient was asymptomatic after recovery.. Despite shaving only a small area of each patient’s head, no infections were recorded at any point in the patients’ monitoring, perioperative procedures, or postoperative recovery.
Whiting AC et al. 9 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch DISCUSSION SEEG has become a pivotal tool in the work-up for intractable, medication-resistant epilepsy. The ability to create a 3-D map of the epileptogenic zone and seizure spread through a relatively minimalistic, bilateral approach has revolutionized preoperative invasive monitoring. As our experience with SEEG has increased over the past several decades, several new techniques have been proposed and evaluated, many involving new technology. Table 3 highlights several studies that specifically analyze these various techniques, their complication profiles, and their operative times. Our goal was to evaluate an SEEG depth electrode implantation technique that used readily available, cost-effective neurosurgical equipment along these same parameters. In addition, many epilepsy surgical centers will shave the patient’s entire head, or at least a large portion of it, for ease of placement of the SEEG electrodes.[9,12,13] Our technique involves shaving only a small portion of the patient’s head, and frequently it can be difficult to tell that any hair has been shaved at all. We also attempted to evaluate the infection risk of placing SEEG electrodes with this minimal shaving technique. Our study involved 23 patients and 213 SEEG depth electrodes that were implanted with use of this technique. Two of 213 (0.9%) of the implanted electrodes were associated with hemorrhage during placement. One of 213 (0.5%) of the implanted electrodes was placed outside the dura, which did not require any additional surgery. No patients had symptomatic complications or died. These complication rates are low and compare favorably with those associated with other techniques (Table 3). A large meta-analysis of SEEG safety by Mullin et al.[8] found that 1.0% of electrodes were associated with hemorrhagic complications. They also found a 0.3% mortality rate. The number of subjects and number of electrodes placed in our study were comparable to other recently published techniques (Table 3). All of the studied
Whiting AC et al. 10 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch techniques, including ours, use a relatively similar method for the actual placement of the bolt and the advancement of the electrode into the brain, so it is not surprising to have relatively similar rates of complications such as hemorrhage and mortality. The infection rate in our study was 0%. No patients experienced any infectious complications at any point in their preoperative, perioperative, or postoperative stages. This compares favorably to the 0.8% risk of infection found in the meta-analysis by Mullin et al.[8] Numerous studies in the neurosurgical literature have demonstrated that there is no conclusive evidence that shaving a patient’s head before performing neurosurgery reduces infection risk.[14,15] Because of the multiple wires coming out of the head during SEEG monitoring, it seems counterintuitive that a large swath of hair around the wires would not present a problem, but in our experience it does not increase the difficulty of performing electrode implantation. Quick but careful combing and braiding of even the longest, thickest hair can provide easy, clear access to the areas for electrode implantation. This study suggests that leaving the hair in place does not present additional infection risk. As shaving the head can be traumatic and potentially discouraging for patients, it seems reasonable to avoid this result if at all possible. While recent studies have demonstrated the cost-effectiveness of SEEG and surgical intervention compared with nonintervention, to our knowledge no study has analyzed the direct costs of different SEEG techniques.[16] Individual hospital expenses of purchasing a robotic arm or 3-D-printed frames are not readily available, but these represent technologies that certainly cost more than using the equipment already readily available in most operating rooms. The equipment used for SEEG depth electrode implantation at our institution is normally used for standard image-guided biopsies such as those frequently performed at all major neurosurgical centers. While much of the new SEEG technology is exciting and will continue to improve and
Whiting AC et al. 11 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch evolve, many neurosurgery centers around the world may not have access to or be able to afford this novel equipment and can use this relatively cost-effective technique. The pre-operative evaluation and invasive monitoring for potential epilepsy surgery is already an expensive, laborintensive process. By utilizing standard neurosurgical equipment for SEEG, neurosurgical centers in countries with more limited resources may find this technique practical. Conversely, it should be noted that this technique, while utilizing more basic neurosurgery equipment than many current SEEG electrode placement techniques, still requires the use of neuronavigation, SEEG depth electrodes, and post-operative epilepsy monitoring in an epilepsy monitoring unit. This all requires a level of resource-commitment that may not be available in many neurosurgical centers in lower-resource areas of the world. The goal of SEEG depth electrode implantation and monitoring is to create a functional 3-D map of the epileptogenic zone. The preoperative hypothesis about the location of the epileptogenic zone created by the multidisciplinary epilepsy team is the most important aspect in determining the perioperative placement of the implanted SEEG depth electrodes.[9] In our technique, with use of the hypothesis determined by the multidisciplinary epilepsy team, the electrode trajectories are mapped out and chosen after the patient is intubated and fixated in the Mayfield clamp. This allows the planning and implantation portions of the procedure to occur quickly and seamlessly. Our operative time and time per electrode compared favorably with the other studies that analyzed operative time (Table 3). This study has several limitations. The study was limited by its retrospective nature. While the number of patients and electrodes in this study is comparable to several other SEEG technique studies, these are relatively small numbers and may not accurately detect differences in complication rates when these rates are inherently low. Because there was frequently no
Whiting AC et al. 12 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch preoperative trajectory plan created with this technique, we were unable to directly measure deviation of the depth electrode from its presumed trajectory, but only one electrode was considered to be misplaced on postoperative computed tomography. Because this was not a comparison study, it is difficult to determine differences between our technique and other techniques with respect to complication rates and operative techniques. Additionally, it should be noted that our operative technique shares similarities to other frameless, neuronavigation-based techniques (Table 3) with that exception that our technique involves negligible hair shaving.
CONCLUSION This study highlights a minimally invasive, cost-conscious technique for SEEG depth electrode implantation that results in complication profiles and operative times comparable to those associated with other techniques. Utilization of this technique may be useful in neurosurgery centers with more limited resources. Although we shaved only a small area of each patient’s head, the infection rate was 0%, which suggests that this method does not increase the likelihood of infection during implantation and monitoring.
Whiting AC et al. 13 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch ACKNOWLEDGMENTS: We thank the staff of Neuroscience Publications at Barrow Neurological Institute for assistance with manuscript preparation.
REFERENCES 1. Wiebe S, Blume WT, Girvin JP, et al. A randomized, controlled trial of surgery for temporallobe epilepsy. N Engl J Med. 2001;345:311-318. 2. Enatsu R, Mikuni N. Invasive evaluations for epilepsy surgery: a review of the literature. Neurol Med Chir (Tokyo). 2016;56:221-227. 3. Bancaud J, Angelergues R, Bernouilli C, et al. Functional stereotaxic exploration (SEEG) of epilepsy. Electroencephalogr Clin Neurophysiol. 1970;28:85-86. 4. Dorfer C, Stefanits H, Pataraia E, et al. Frameless stereotactic drilling for placement of depth electrodes in refractory epilepsy: operative technique and initial experience. Neurosurgery. 2014;10 Suppl 4:582-590; discussion 590-581. 5. Isnard J, Taussig D, Bartolomei F, et al. French guidelines on stereoelectroencephalography (SEEG). Neurophysiol Clin. 2018;48:5-13. 6. Podkorytova I, Hoes K, Lega B. Stereo-encephalography versus subdural electrodes for seizure localization. Neurosurg Clin N Am. 2016;27:97-109. 7. Abou-Al-Shaar H, Brock AA, Kundu B, et al. Increased nationwide use of stereoencephalography for intracranial epilepsy electroencephalography recordings. J Clin Neurosci. 2018;53:132-134. 8. Mullin JP, Shriver M, Alomar S, et al. Is SEEG safe? A systematic review and meta-analysis of stereo-electroencephalography-related complications. Epilepsia. 2016;57:386-401.
Whiting AC et al. 14 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch 9. Gonzalez-Martinez J, Bulacio J, Thompson S, et al. Technique, results, and complications related to robot-assisted stereoelectroencephalography. Neurosurgery. 2016;78:169-180. 10. Dewan MC, Shults R, Hale AT, et al. Stereotactic EEG via multiple single-path omnidirectional trajectories within a single platform: institutional experience with a novel technique. J Neurosurg. 2018;129:1173-1181. 11. Engel J. Surgical Treatment of Epilepsies, 2nd ed: Raven Press; 1993. 12. Dorfer C, Minchev G, Czech T, et al. A novel miniature robotic device for frameless implantation of depth electrodes in refractory epilepsy. J Neurosurg. 2017;126:16221628. 13. Nowell M, Rodionov R, Diehl B, et al. A novel method for implementation of frameless StereoEEG in epilepsy surgery. Neurosurgery. 2014;10 Suppl 4:525-533; discussion 533524. 14. Broekman ML, van Beijnum J, Peul WC, et al. Neurosurgery and shaving: what's the evidence? J Neurosurg. 2011;115:670-678. 15. Horgan MA, Kernan JC, Schwartz MS, et al. Shaveless brain surgery: safe, well tolerated, and cost effective. Skull Base Surg. 1999;9:253-258. 16. Garcia-Lorenzo B, Del Pino-Sedeno T, Rocamora R, et al. Stereoelectroencephalography for refractory epileptic patients considered for surgery: systematic review, meta-analysis, and economic evaluation. Neurosurgery. 2019;84:326-338. 17. Gonzalez-Martinez J, Mullin J, Vadera S, et al. Stereotactic placement of depth electrodes in medically intractable epilepsy. J Neurosurg. 2014;120:639-644.
Whiting AC et al. 15 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch 18. Balanescu B, Franklin R, Ciurea J, et al. A personalized stereotactic fixture for implantation of depth electrodes in stereoelectroencephalography. Stereotact Funct Neurosurg. 2014;92:117-125. 19. Narvaez-Martinez Y, Garcia S, Roldan P, et al. [Stereoelectroencephalography by using OArm((R)) and Vertek((R)) passive articulated arm: technical note and experience of an epilepsy referral centre]. Neurocirugia (Astur). 2016;27:277-284. 20. Yu H, Pistol C, Franklin R, et al. Clinical accuracy of customized stereotactic fixtures for stereoelectroencephalography. World Neurosurg. 2018;109:82-88. 21. 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;22:37-46. 22. Ho AL, Muftuoglu Y, Pendharkar AV, et al. Robot-guided pediatric stereoelectroencephalography: single-institution experience. J Neurosurg Pediatr. 2018;22:1-8.
Whiting AC et al. 16 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch FIGURE LEGENDS Figure 1. Patient positioning prior to stereoelectroencephalography depth electrode implantation. Used with permission from Barrow Neurological Institute, Phoenix, Arizona. Figure 2. Stereoelectroencephalography depth electrode implantation steps. (A) Trajectory planning using the image guidance probe through the Vertek (Medtronic) arm. (B) After a stab skin incision, the guidance hole is drilled using a high-speed drill. (C) The bolt is attached to the skull. (D) The length of the electrode to be placed intracranially is measured, and then the electrode is placed through the bolt to this preplanned measurement. Used with permission from Barrow Neurological Institute, Phoenix, Arizona. Figure 3. Final position of the stereoelectroencephalography depth electrode demonstrating minimal hair shaving. Used with permission from Barrow Neurological Institute, Phoenix, Arizona.
Whiting AC et al. 17 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch Table 1. Demographic and SEEG characteristics of patients with stereoelectroencephalography (SEEG) depth electrode implantation Characteristic No. (%)* Sex Male 16 (70) Female 7 (30) Prior surgery Yes 6 (26) No 17 (74) Resective surgery after monitoring Yes 15 (65) No 8 (35) Age, mean (SD), y 32.4 (10.4) Time since epilepsy diagnosis, mean (SD), y 14.4 (8.7) No. of depth electrodes placed, mean (SD) 9.3 (1.4) Duration of SEEG monitoring, mean (SD), d 7.6 (2.5) Electrode placement location Left Right Frontal 41 31 72 (34) Cingulum 15 15 30 (14) Amygdala 18 16 34 (16) Hippocampus 21 19 40 (19) Other temporal 10 6 16 (8) Parietal 5 4 9 (4) Insular 1 4 5 (2) Occipital 7 0 7 (3) Total electrodes placed 118 95 213 (100) *Data are no. (%) of patients unless otherwise indicated. SD, standard deviation
Whiting AC et al. 18 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch Table 2. Complications related to stereoelectroencephalography (SEEG) depth electrode placement, monitoring, and removal Complication No. (%) Electrodes (n=213) Hemorrhage from electrode placement 2 (0.9) Extradural placement 1 (0.5) Patients (n=23) Complications during monitoring 0 (0) Infection 0 (0) Symptomatic complications from SEEG implantation, monitoring, or removal 0 (0)
Whiting AC et al. 19 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch Table 3. Studies reviewing operating room time and complications after stereoelectroencephalography (SEEG) depth electrode implantation with different techniques Study Nowell et al. 2014[13] GonzalezMartinez et al. 2014[17] Dorfer et al. 2014[4] Balanescu et al. 2014[18] GonzalezMartinez et al. 2016[9] NarvaezMartinez et al. 2016[19] Yu et al. 2017[20] Dewan et al. 2017[10] Abel et al. 2018[21]
Dorfer et al. 2018[12] Ho et al. 2018[22]
Mortality 0
Operative Time (min) 137.0
Time Per Electrode (min) 16.1
No. of Electrodes 187
N/A
0
107.0
8.2
1586
0
N/A
0
70.9
19.1
26
0
0
N/A
0
182.0
14.0
52
100
4
1
N/A
0
130.0
10.4
1245
Prospective
10
0
0
N/A
0
239.0
34.6
69
Retrospective
21
1
0
N/A
0
124.0
15.1
173
Retrospective
15
N/A
N/A
N/A
N/A
207.0
22.7
137
Retrospective
17
5
1
N/A
0
304.0
19.5
265
Retrospective
18
2
1
N/A
0
352.0
24.0
264
Retrospective
16
0
0
1
0
91.3
15.7
93
Retrospective
20
0
0
0
0
117.0
10.5
222
Study Design Retrospective
No. of Subjects 22
Prospective
Neuronavigation, frameless 3-D-printed fixture, frameless Robot-assisted, frameless (ROSA) Neuronavigation, frameless 3-D-printed fixture, frameless 3-D-printed fixture, frameless Robot-assisted, frameless (ROSA) Talairach framebased Robot-assisted, frameless (iSys1) Robot-assisted, frameless
Technique Neuronavigation, frameless Frame-based
Hematoma 1
Symptomatic Hematoma 0
Infection 0
122
3
0
Retrospective
7
0
Retrospective
4
Prospective
Whiting AC et al. 20 676-18 D R A F T : SEEG WNS revision CLEAN.docx : June 26, 2019 : SS/pch (ROSA)
Abbreviations: N/A, not available; 3-D, three dimensional.
ABBREVIATIONS: EEG, electroencephalogram; SD, standard deviation; SEEG, stereoelectroencephalography; 3-D, three-dimensional
DISCLOSURES: None. FINANCIAL SUPPORT: None. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.