A Multivariate Approach to Quantifying Risk Factors Impacting Stereotactic Robotic-Guided Stereoelectroencephalography.


Journal

Operative neurosurgery (Hagerstown, Md.)
ISSN: 2332-4260
Titre abrégé: Oper Neurosurg (Hagerstown)
Pays: United States
ID NLM: 101635417

Informations de publication

Date de publication:
27 Sep 2024
Historique:
received: 10 05 2024
accepted: 13 08 2024
medline: 27 9 2024
pubmed: 27 9 2024
entrez: 27 9 2024
Statut: aheadofprint

Résumé

Stereoelectroencephalography (SEEG) is an important method for invasive monitoring to establish surgical candidacy in approximately half of refractory epilepsy patients. Identifying factors affecting lead placement can mitigate potential surgical risks. This study applies multivariate analyses to identify perioperative factors affecting stereotactic electrode placement. We collected registration and accuracy data for consecutive patients undergoing SEEG implantation between May 2022 and November 2023. Stereotactic robotic guidance, using intraoperative imaging and a novel frame-based fiducial, was used for planning and SEEG implantation. Entry-point (EE), target-point (TE), and angular errors were measured, and statistical univariate and multivariate linear regression analyses were performed. Twenty-seven refractory epilepsy patients (aged 15-57 years) undergoing SEEG were reviewed. Sixteen patients had unilateral implantation (10 left-sided, 6 right-sided); 11 patients underwent bilateral implantation. The mean number of electrodes per patient was 18 (SD = 3) with an average registration mean error of 0.768 mm (SD = 0.108). Overall, 486 electrodes were reviewed. Univariate analysis showed significant correlations of lead error with skull thickness (EE: P = .003; TE: P = .012); entry angle (EE: P < .001; TE: P < .001; angular error: P = .030); lead length (TE: P = .020); and order of electrode implantation (EE: P = .003; TE: P = .001). Three multiple linear regression models were used. All models featured predictors of implantation region (157 temporal, 241 frontal, 79 parietal, 9 occipital); skull thickness (mean = 5.80 mm, SD = 2.97 mm); order (range: 1-23); and entry angle in degrees (mean = 75.47, SD = 11.66). EE and TE error models additionally incorporated lead length (mean = 44.08 mm, SD = 13.90 mm) as a predictor. Implantation region and entry angle were significant predictors of error (P ≤ .05). Our study identified 2 primary predictors of SEEG lead error, region of implantation and entry angle, with nonsignificant contributions from lead length or order of electrode placement. Future considerations for SEEG may consider varying regional approaches and angles for more optimal accuracy in lead placement.

Sections du résumé

BACKGROUND AND OBJECTIVES OBJECTIVE
Stereoelectroencephalography (SEEG) is an important method for invasive monitoring to establish surgical candidacy in approximately half of refractory epilepsy patients. Identifying factors affecting lead placement can mitigate potential surgical risks. This study applies multivariate analyses to identify perioperative factors affecting stereotactic electrode placement.
METHODS METHODS
We collected registration and accuracy data for consecutive patients undergoing SEEG implantation between May 2022 and November 2023. Stereotactic robotic guidance, using intraoperative imaging and a novel frame-based fiducial, was used for planning and SEEG implantation. Entry-point (EE), target-point (TE), and angular errors were measured, and statistical univariate and multivariate linear regression analyses were performed.
RESULTS RESULTS
Twenty-seven refractory epilepsy patients (aged 15-57 years) undergoing SEEG were reviewed. Sixteen patients had unilateral implantation (10 left-sided, 6 right-sided); 11 patients underwent bilateral implantation. The mean number of electrodes per patient was 18 (SD = 3) with an average registration mean error of 0.768 mm (SD = 0.108). Overall, 486 electrodes were reviewed. Univariate analysis showed significant correlations of lead error with skull thickness (EE: P = .003; TE: P = .012); entry angle (EE: P < .001; TE: P < .001; angular error: P = .030); lead length (TE: P = .020); and order of electrode implantation (EE: P = .003; TE: P = .001). Three multiple linear regression models were used. All models featured predictors of implantation region (157 temporal, 241 frontal, 79 parietal, 9 occipital); skull thickness (mean = 5.80 mm, SD = 2.97 mm); order (range: 1-23); and entry angle in degrees (mean = 75.47, SD = 11.66). EE and TE error models additionally incorporated lead length (mean = 44.08 mm, SD = 13.90 mm) as a predictor. Implantation region and entry angle were significant predictors of error (P ≤ .05).
CONCLUSION CONCLUSIONS
Our study identified 2 primary predictors of SEEG lead error, region of implantation and entry angle, with nonsignificant contributions from lead length or order of electrode placement. Future considerations for SEEG may consider varying regional approaches and angles for more optimal accuracy in lead placement.

Identifiants

pubmed: 39329517
doi: 10.1227/ons.0000000000001383
pii: 01787389-990000000-01342
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © Congress of Neurological Surgeons 2024. All rights reserved.

Références

Löscher W, Potschka H, Sisodiya SM, Vezzani A. Drug resistance in epilepsy: clinical impact, potential mechanisms, and new innovative treatment options. Pharmacol Rev. 2020;72(3):606-638.
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.
Bancaud J. La Stéréo-Électroencéphalographie Dans l’épilepsie: Informations Neurophysiopathologiques Apportées par l’investigation Fonctionnelle Stéreotaxique. Rapport Présenté a La Société d’électroencéphalographie de Langue Franc̦aise (Marseille, Octobre 1962). Masson; 1965. Accessed July 8, 2024. https://cir.nii.ac.jp/crid/1130000796521239552.bib?lang=en
Abel TJ, Muthiah N, Hect JL, et al. Cost-effectiveness of invasive monitoring strategies in epilepsy surgery. J Neurosurg. 2023;139(1):222-228.
Kovac S, Vakharia VN, Scott C, Diehl B. Invasive epilepsy surgery evaluation. Seizure. 2017;44:125-136.
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(5):1239-1246.
Yang C, Luan G, Wang Q, Liu Z, Zhai F, Wang Q. Localization of epileptogenic zone with the correction of pathological networks. Front Neurol. 2018;9:143.
Khoo HM, Hall JA, Dubeau F, et al. Technical aspects of SEEG and its interpretation in the delineation of the epileptogenic zone. Neurol Med Chir (Tokyo). 2020;60(12):565-580.
Bernabei JM, Arnold TC, Shah P, et al. Electrocorticography and stereo EEG provide distinct measures of brain connectivity: implications for network models. Brain Commun. 2021;3(3):fcab156.
Dasgupta D, Miserocchi A, McEvoy AW, Duncan JS. Previous, current, and future stereotactic EEG techniques for localising epileptic foci. Expert Rev Med Devices. 2022;19(7):571-580.
Kaur M, Szaflarski JP, Ver Hoef L, Pati S, Riley KO, Jaisani Z. Long-term seizure freedom following intracranial sEEG monitoring: therapeutic benefit of a diagnostic technique. Epilepsy Behav Rep. 2019;12:100345.
Fomenko A, Serletis D. Robotic stereotaxy in cranial neurosurgery: a qualitative systematic review. Neurosurgery. 2018;83(4):642-650.
Fomenko A, El Idrissi FE, Aji N, et al. Introduction and history of robotics in neurosurgery. In: Al-Salihi, M.M., Tubbs, R.S., Ayyad, A., Goto, T., Maarouf, M, eds. Introduction to Robotics in Minimally Invasive Neurosurgery. Springer, Cham. 2022.
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(5):e8.
Bourdillon P, Châtillon CE, Moles A, et al. Effective accuracy of stereoelectroencephalography: robotic 3D versus Talairach orthogonal approaches. J Neurosurg. 2019;131(6):1938-1946.
Cardinale F, Rizzi M, Vignati E, et al. Stereoelectroencephalography: retrospective analysis of 742 procedures in a single centre. Brain. 2019;142(9):2688-2704.
Cardinale F, Casaceli G, Raneri F, Miller J, Lo Russo G. Implantation of stereoelectroencephalography electrodes: a systematic review. J Clin Neurophysiol. 2016;33(6):490-502.
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(3):386-401.
Mathon B, Clemenceau S, Hasboun D, et al. Safety profile of intracranial electrode implantation for video-EEG recordings in drug-resistant focal epilepsy. J Neurol. 2015;262(12):2699-2712.
Bourdillon P, Ryvlin P, Isnard J, et al. Stereotactic electroencephalography is a safe procedure, including for insular implantations. World Neurosurg. 2017;99:353-361.
Miller C, Schatmeyer B, Landazuri P, et al. sEEG for expansion of a surgical epilepsy program: safety and efficacy in 152 consecutive cases. Epilepsia Open. 2021;6(4):694-702.
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(9):1733-1746.
Spyrantis A, Cattani A, Woebbecke T, et al. Electrode placement accuracy in robot-assisted epilepsy surgery: a comparison of different referencing techniques including frame-based CT versus facial laser scan based on CT or MRI. Epilepsy Behav. 2019;91:38-47.
Sharma A, Song R, Sarmey N, et al. Validation and safety profile of a novel, noninvasive fiducial attachment for stereotactic robotic-guided stereoelectroencephalography: a case series. Oper Neurosurg. 2024;27(4):440-448.
Jansen T, Gathen M, Touet A, et al. Spine examination during COVID-19 pandemic via video consultation. Z Orthop Unfall. 2021;159(2):193-201.
Corrales Zúniga IA, Sauceda Malespín NL, Vega Vílchez AL, Duarte Frenky OJ, Hong G, Vanegas Sáenz JR. Evaluation of the ergonomic sitting position adopted by dental students while using dental simulators. J Dent Sci. 2023;18(2):526-533.
Cakar A, Kose O, Dogruoz F, Selcuk H, Kirtis T, Egerci OF. Validity and reliability of hallux valgus angle measurement on smartphone digital photographs. J Foot Ankle Res. 2023;16(1):70.
Girgis F, Ovruchesky E, Kennedy J, Seyal M, Shahlaie K, Saez I. Superior accuracy and precision of SEEG electrode insertion with frame-based vs. frameless stereotaxy methods. Acta Neurochir (Wien). 2020;162(10):2527-2532.
Kullmann A, Akberali F, Van Gompel JJ, et al. Implantation accuracy of novel polyimide stereotactic electroencephalographic depth electrodes—a human cadaveric study. Front Med Technol. 2024;6:1320762.
Marill KA, Lewis RJ. Advanced statistics: linear regression, Part II: multiple linear regression. Acad Emerg Med. 2004;11(1):94-102.
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(4):3699-3705.
Kandregula S, Matias CM, Malla BR, Sperling MR, Wu C, Sharan AD. Accuracy of electrode insertion using frame-based with robot guidance technique in stereotactic electroencephalography: supine versus lateral position. World Neurosurg. 2021;154:e325-e332.
Rollo PS, Rollo MJ, Zhu P, Woolnough O, Tandon N. Oblique trajectory angles in robotic stereo-electroencephalography. J Neurosurg. 2021;135(1):245-254.
Granados A, Rodionov R, Vakharia V, et al. Automated computation and analysis of accuracy metrics in stereoencephalography. J Neurosci Methods. 2020;340:108710.
Hou Z, Chen X, Shi XJ, et al. Comparison of neuronavigation and frame-based stereotactic systems in implanting epileptic depth electrodes. Turk Neurosurg. 2016;26(4):574-581.
González-Martínez J, Bulacio J, Thompson S, et al. Technique, results, and complications related to robot-assisted stereoelectroencephalography. Neurosurgery. 2016;78(2):169-180.
De Barros A, Zaldivar-Jolissaint JF, Hoffmann D, et al. Indications, techniques, and outcomes of robot-assisted insular stereo-electro-encephalography: a review. Front Neurol. 2020;11:1033.
Vakharia VN, Rodionov R, Miserocchi A, et al. Comparison of robotic and manual implantation of intracerebral electrodes: a single-centre, single-blinded, randomised controlled trial. Sci Rep. 2021;11(1):17127.
Sharma JD, Seunarine KK, Tahir MZ, Tisdall MM. Accuracy of robot-assisted versus optical frameless navigated stereoelectroencephalography electrode placement in children. J Neurosurg Pediatr. 2019;23(3):297-302.
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(5):430-436.
Jones JC, Alomar S, McGovern RA, et al. Techniques for placement of stereotactic electroencephalographic depth electrodes: comparison of implantation and tracking accuracies in a cadaveric human study. Epilepsia. 2018;59(9):1667-1675.
Iordanou JC, Camara D, Ghatan S, Panov F. Approach angle affects accuracy in robotic stereoelectroencephalography lead placement. World Neurosurg. 2019;128:e322-e328.
Bonda DJ, Pruitt R, Theroux L, et al. Robot-assisted stereoelectroencephalography electrode placement in twenty-three pediatric patients: a high-resolution analysis of individual lead placement time and accuracy at a single institution. Childs Nerv Syst. 2021;37(7):2251-2259.
Katz J, Armstrong C, Kvint S, Kennedy BC. Stereoelectroencephalography in the very young: case report. Epilepsy Behav Rep. 2022;19:100552.
Ho AL, Muftuoglu Y, Pendharkar AV, et al. Robot-guided pediatric stereoelectroencephalography: single-institution experience. J Neurosurg Pediatr. 2018;22(5):1-8.
McGovern RA, Knight EP, Gupta A, et al. Robot-assisted stereoelectroencephalography in children. J Neurosurg Pediatr. 2019;23(3):288-296.
Ho AL, Feng AY, Kim LH, et al. Stereoelectroencephalography in children: a review. Neurosurg Focus. 2018;45(3):e7.
Angus-Leppan H, Clay TA. Adult occipital lobe epilepsy: 12-years on. J Neurol. 2021;268(10):3926-3934.
Kim LH, Feng AY, Ho AL, et al. Robot-assisted versus manual navigated stereoelectroencephalography in adult medically-refractory epilepsy patients. Epilepsy Res. 2020;159:106253.

Auteurs

Ryan R Song (RR)

Cleveland Clinic Lerner College of Medicine of Case Western Reserve University, Cleveland, Ohio, USA.

Akshay Sharma (A)

Cleveland Clinic Epilepsy Center, Cleveland Clinic Foundation, Cleveland, Ohio, USA.
Department of Neurosurgery, Cleveland Clinic Foundation, Cleveland, Ohio, USA.

Nehaw Sarmey (N)

Cleveland Clinic Epilepsy Center, Cleveland Clinic Foundation, Cleveland, Ohio, USA.
Department of Neurosurgery, Cleveland Clinic Foundation, Cleveland, Ohio, USA.

Stephen Harasimchuk (S)

Cleveland Clinic Epilepsy Center, Cleveland Clinic Foundation, Cleveland, Ohio, USA.

Juan Bulacio (J)

Cleveland Clinic Epilepsy Center, Cleveland Clinic Foundation, Cleveland, Ohio, USA.

Richard Rammo (R)

Cleveland Clinic Epilepsy Center, Cleveland Clinic Foundation, Cleveland, Ohio, USA.
Department of Neurosurgery, Cleveland Clinic Foundation, Cleveland, Ohio, USA.

William Bingaman (W)

Cleveland Clinic Lerner College of Medicine of Case Western Reserve University, Cleveland, Ohio, USA.
Cleveland Clinic Epilepsy Center, Cleveland Clinic Foundation, Cleveland, Ohio, USA.
Department of Neurosurgery, Cleveland Clinic Foundation, Cleveland, Ohio, USA.

Demitre Serletis (D)

Cleveland Clinic Lerner College of Medicine of Case Western Reserve University, Cleveland, Ohio, USA.
Cleveland Clinic Epilepsy Center, Cleveland Clinic Foundation, Cleveland, Ohio, USA.
Department of Neurosurgery, Cleveland Clinic Foundation, Cleveland, Ohio, USA.

Classifications MeSH