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Frame-based versus robot-assisted stereo-electro-encephalography for drug-resistant epilepsy

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Abstract

Background

Stereoelectroencephalography (SEEG) is an effective presurgical invasive evaluation for drug-resistant epilepsies. The introduction of robotic devices provides a simplified, accurate, and safe alternative to the conventional SEEG technique. We report our institutional experience with robot-assisted SEEG and compare its in vivo accuracy, operation efficiency, and safety with the more traditional SEEG workflow.

Methods

All patients with medically refractory focal epilepsy who underwent SEEG depth electrode implantation between 2014 and 2022 were included in this study. Technical advancements of the robot-assisted technique are described. Analyses of patient demographics, electrode implantation accuracy, operation time, and procedure-related complications were performed.

Results

One hundred and sixty-six patients underwent 167 SEEG procedures. The first 141 procedures were performed using a conventional approach involving a Leksell stereotactic system, and the last 26 procedures were robot-assisted. Among the 1726 depth electrodes that were inserted, the median entry point localization error was as follows: conventional (1.0 mm; range, 0.1–33.5 mm) and robot-assisted (1.1 mm; range, 0–4.8 mm) (P = 0.17). The median target point localization error was as follows: conventional (2.8 mm; range, 0.1–49 mm) and robot-assisted (1.8 mm; range, 0–30.3 mm) (P < 0.001). The median operation time was significantly reduced with the robot-assisted workflow (90 min vs. 77.5 min; P < 0.01). Total complication rates were as follows: conventional (17.7%) and robot-assisted (11.5%) (P = 0.57). Major complication rates were 3.5% and 7.7% (P = 0.77), respectively.

Conclusions

SEEG is a safe and highly accurate method that provides essential guidance for epilepsy surgery. Implementing SEEG in conjunction with multimodal planning systems and robotic devices can further increase safety margin, surgical efficiency, and accuracy.

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Data availability

The data that support the findings of this study are available on request from the corresponding author, CCL. The data are not publicly available due to the containing information that could compromise the privacy of research participants.

Abbreviations

EZ:

Epileptogenic zone

SEEG:

Stereoelectroencephalography

MRI:

Magnetic resonance imaging

CT:

Computed tomography

CTA:

Computed tomography angiography

EP:

Entry point

TP:

Target point

LE:

Localization error

References

  1. Mullin JP, Shriver M, Alomar S, Najm I, Bulacio J, Chauvel P, Gonzalez-Martinez J (2016) Is SEEG safe? A systematic review and meta-analysis of stereo-electroencephalography-related complications. Epilepsia 57:386–401. https://doi.org/10.1111/epi.13298

    Article  PubMed  Google Scholar 

  2. Cossu M, Cardinale F, Castana L, Citterio A, Francione S, Tassi L, Benabid AL, Lo Russo G (2005) Stereoelectroencephalography in the presurgical evaluation of focal epilepsy: a retrospective analysis of 215 procedures. Neurosurgery 57:706–718

    Article  PubMed  Google Scholar 

  3. Sindou M, Guenot M, Isnard J, Ryvlin P, Fischer C, Mauguiere F (2006) Temporo-mesial epilepsy surgery: outcome and complications in 100 consecutive adult patients. Acta Neurochir (Wien) 148:39–45. https://doi.org/10.1007/s00701-005-0644-x

    Article  CAS  PubMed  Google Scholar 

  4. Gonzalez-Martinez J, Bulacio J, Alexopoulos A, Jehi L, Bingaman W, Najm I (2013) Stereoelectroencephalography in the “difficult to localize” refractory focal epilepsy: early experience from a North American epilepsy center. Epilepsia 54:323–330. https://doi.org/10.1111/j.1528-1167.2012.03672.x

    Article  PubMed  Google Scholar 

  5. Serletis D, Bulacio J, Bingaman W, Najm I, González-Martínez J (2014) The stereotactic approach for mapping epileptic networks: a prospective study of 200 patients. J Neurosurg 121:1239–1246. https://doi.org/10.3171/2014.7.Jns132306

    Article  PubMed  Google Scholar 

  6. Cardinale F, Casaceli G, Raneri F, Miller J, Russo GL (2016) Implantation of stereoelectroencephalography electrodes: a systematic review. J Clin Neurophysiol 33:490–502

    Article  PubMed  Google Scholar 

  7. Cardinale F, Cossu M, Castana L, Casaceli G, Schiariti MP, Miserocchi A, Fuschillo D, Moscato A, Caborni C, Arnulfo G, Lo Russo G (2013) Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures. Neurosurgery 72:353–366. https://doi.org/10.1227/NEU.0b013e31827d1161

    Article  PubMed  Google Scholar 

  8. Cossu M, Cardinale F, Colombo N, Mai R, Nobili L, Sartori I, Lo Russo G (2005) Stereoelectroencephalography in the presurgical evaluation of children with drug-resistant focal epilepsy. J Neurosurg 103:333–343. https://doi.org/10.3171/ped.2005.103.4.0333

    Article  PubMed  Google Scholar 

  9. Gonzalez-Martinez J, Mullin J, Vadera S, Bulacio J, Hughes G, Jones S, Enatsu R, Najm I (2014) Stereotactic placement of depth electrodes in medically intractable epilepsy. J Neurosurg 120:639–644. https://doi.org/10.3171/2013.11.Jns13635

    Article  PubMed  Google Scholar 

  10. McGonigal A, Bartolomei F, Regis J, Guye M, Gavaret M, Trebuchon-Da Fonseca A, Dufour H, Figarella-Branger D, Girard N, Peragut JC, Chauvel P (2007) Stereoelectroencephalography in presurgical assessment of MRI-negative epilepsy. Brain 130:3169–3183. https://doi.org/10.1093/brain/awm218

    Article  PubMed  Google Scholar 

  11. Taussig D, Chipaux M, Lebas A, Fohlen M, Bulteau C, Ternier J, Ferrand-Sorbets S, Delalande O, Dorfmüller G (2014) Stereo-electroencephalography (SEEG) in 65 children: an effective and safe diagnostic method for pre-surgical diagnosis, independent of age. Epileptic Disord 16:280–295. https://doi.org/10.1684/epd.2014.0679

    Article  PubMed  Google Scholar 

  12. Yan H, Katz JS, Anderson M, Mansouri A, Remick M, Ibrahim GM, Abel TJ (2019) Method of invasive monitoring in epilepsy surgery and seizure freedom and morbidity: a systematic review. Epilepsia 60:1960–1972

    Article  PubMed  Google Scholar 

  13. Chassoux F, Devaux B, Landré E, Turak B, Nataf F, Varlet P, Chodkiewicz J-P, Daumas-Duport C (2000) Stereoelectroencephalography in focal cortical dysplasia: a 3D approach to delineating the dysplastic cortex. Brain 123:1733–1751. https://doi.org/10.1093/brain/123.8.1733

    Article  PubMed  Google Scholar 

  14. Guenot M, Isnard J, Ryvlin P, Fischer C, Ostrowsky K, Mauguiere F, Sindou M (2001) 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 77:29–32. https://doi.org/10.1159/000064595

    Article  CAS  PubMed  Google Scholar 

  15. Munari C, Hoffmann D, Francione S, Kahane P, Tassi L, Lo Russo G, Benabid AL (1994) Stereo-electroencephalography methodology: advantages and limits. Acta Neurol Scand Suppl 152:56–67. https://doi.org/10.1111/j.1600-0404.1994.tb05188.x

    Article  CAS  PubMed  Google Scholar 

  16. Talairach J, Bancaud J (1973) Stereotaxic approach to epilepsy. In: Progress in neurological surgery, vol 5. Karger Publishers pp 297–354

  17. De Almeida AN, Olivier A, Quesney F, Dubeau F, Savard G, Andermann F (2006) Efficacy of and morbidity associated with stereoelectroencephalography using computerized tomography–or magnetic resonance imaging-guided electrode implantation. J Neurosurg 104:483–487. https://doi.org/10.3171/jns.2006.104.4.483

    Article  PubMed  Google Scholar 

  18. Tanriverdi T, Ajlan A, Poulin N, Olivier A (2009) Morbidity in epilepsy surgery: an experience based on 2449 epilepsy surgery procedures from a single institution: Clinical article. J Neurosurg JNS 110:1111–1123. https://doi.org/10.3171/2009.8.Jns08338

    Article  Google Scholar 

  19. van der Loo LE, Schijns O, Hoogland G, Colon AJ, Wagner GL, Dings JTA, Kubben PL (2017) Methodology, outcome, safety and in vivo accuracy in traditional frame-based stereoelectroencephalography. Acta Neurochir (Wien) 159:1733–1746. https://doi.org/10.1007/s00701-017-3242-9

    Article  PubMed  Google Scholar 

  20. Dorfer C, Stefanits H, Pataraia E, Wolfsberger S, Feucht M, Baumgartner C, Czech T (2014) Frameless stereotactic drilling for placement of depth electrodes in refractory epilepsy: operative technique and initial experience. Neurosurgery 10(Suppl 4):582–590. https://doi.org/10.1227/neu.0000000000000509

    Article  PubMed  Google Scholar 

  21. Nowell M, Rodionov R, Diehl B, Wehner T, Zombori G, Kinghorn J, Ourselin S, Duncan J, Miserocchi A, McEvoy A (2014) A novel method for implementation of frameless StereoEEG in epilepsy surgery. Neurosurgery 10(Suppl 4):525–533. https://doi.org/10.1227/neu.0000000000000544

    Article  PubMed  Google Scholar 

  22. Abel TJ, Varela Osorio R, Amorim-Leite R, Mathieu F, Kahane P, Minotti L, Hoffmann D, Chabardes S (2018) Frameless robot-assisted stereoelectroencephalography in children: technical aspects and comparison with Talairach frame technique. J Neurosurg: Pediatr 22:37–46. https://doi.org/10.3171/2018.1.PEDS17435

    Article  PubMed  Google Scholar 

  23. Bourdillon P, Châtillon C-E, Moles A, Rheims S, Catenoix H, Montavont A, Ostrowsky-Coste K, Boulogne S, Isnard J, Guénot M (2019) Effective accuracy of stereoelectroencephalography: robotic 3D versus Talairach orthogonal approaches. J Neurosurg JNS 131:1938–1946. https://doi.org/10.3171/2018.7.JNS181164

    Article  Google Scholar 

  24. C-E Châtillon K Mok J Hall A Olivier 2011 Comparative study of manual versus robot-assisted frameless stereotaxy for intracranial electrode implantationhttps://doi.org/10.13140/2.1.4217.7925

  25. De Benedictis A, Trezza A, Carai A, Genovese E, Procaccini E, Messina R, Randi F, Cossu S, Esposito G, Palma P, Amante P, Rizzi M, Marras CE (2017) Robot-assisted procedures in pediatric neurosurgery. Neurosurg Focus 42:E7. https://doi.org/10.3171/2017.2.Focus16579

    Article  PubMed  Google Scholar 

  26. Dorfer C, Minchev G, Czech T, Stefanits H, Feucht M, Pataraia E, Baumgartner C, Kronreif G, Wolfsberger S (2017) A novel miniature robotic device for frameless implantation of depth electrodes in refractory epilepsy. J Neurosurg 126:1622–1628. https://doi.org/10.3171/2016.5.Jns16388

    Article  PubMed  Google Scholar 

  27. González-Martínez J, Bulacio J, Thompson S, Gale J, Smithason S, Najm I, Bingaman W (2016) Technique, results, and complications related to robot-assisted stereoelectroencephalography. Neurosurgery 78:169–180. https://doi.org/10.1227/neu.0000000000001034

    Article  PubMed  Google Scholar 

  28. Kim LH, Feng AY, Ho AL, Parker JJ, Kumar KK, Chen KS, Grant GA, Henderson JM, Halpern CH (2020) Robot-assisted versus manual navigated stereoelectroencephalography in adult medically-refractory epilepsy patients. Epilepsy Res 159:106253

    Article  CAS  PubMed  Google Scholar 

  29. Mavridis IN, Lo WB, Wimalachandra WSB, Philip S, Agrawal S, Scott C, Martin-Lamb D, Carr B, Bill P, Lawley A, Seri S, Walsh AR (2021) Pediatric stereo-electroencephalography: effects of robot assistance and other variables on seizure outcome and complications. J Neurosurg Pediatr 28:404–415. https://doi.org/10.3171/2021.2.PEDS20810

    Article  PubMed  Google Scholar 

  30. Ollivier I, Behr C, Cebula H, Timofeev A, Benmekhbi M, Valenti MP, Staack AM, Scholly J, Kehrli P, Hirsch E, Proust F (2017) Efficacy and safety in frameless robot-assisted stereo-electroencephalography (SEEG) for drug-resistant epilepsy. Neurochirurgie 63:286–290. https://doi.org/10.1016/j.neuchi.2017.03.002

    Article  CAS  PubMed  Google Scholar 

  31. Sharma JD, Seunarine KK, Tahir MZ, Tisdall MM (2019) Accuracy of robot-assisted versus optical frameless navigated stereoelectroencephalography electrode placement in children. J Neurosurg Pediatr 23:297–302

    Article  PubMed  Google Scholar 

  32. Vakharia VN, Sparks R, O’Keeffe AG, Rodionov R, Miserocchi A, McEvoy A, Ourselin S, Duncan J (2017) Accuracy of intracranial electrode placement for stereoencephalography: a systematic review and meta-analysis. Epilepsia 58:921–932. https://doi.org/10.1111/epi.13713

    Article  PubMed  PubMed Central  Google Scholar 

  33. Vakharia VN, Rodionov R, Miserocchi A, McEvoy AW, O’Keeffe A, Granados A, Shapoori S, Sparks R, Ourselin S, Duncan JS (2021) Comparison of robotic and manual implantation of intracerebral electrodes: a single-centre, single-blinded, randomised controlled trial. Sci Rep 11:17127. https://doi.org/10.1038/s41598-021-96662-4

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  34. Cardinale F, Rizzi M, Vignati E, Cossu M, Castana L, d’Orio P, Revay M, Costanza MD, Tassi L, Mai R (2019) Stereoelectroencephalography: retrospective analysis of 742 procedures in a single centre. Brain 142:2688–2704

    Article  PubMed  Google Scholar 

  35. van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn CJ (2010) Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol 9:167–176. https://doi.org/10.1016/s1474-4422(09)70340-0

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank individuals who contributed to the study or manuscript preparation but who do not fulfill all the criteria of authorship.

Funding

The study was supported in part by the National Health Research Institutes, under project NHRI-EX112- 11006NC. This support was in the form of personnel, access to clinical databases, and supplies related to SEEG.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan

    Chang-Lin Han, Hsin-Hung Chen, Yi-Hsiu Chen, Chun-Fu Lin, Yu-Wei Chen & Cheng-Chia Lee

  2. Department of Neurology, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan

    Chien-Chen Chou, Chien Chen & Hsiang-Yu Yu

  3. School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan

    Chien-Chen Chou, Hsin-Hung Chen, Chun-Fu Lin, Chien Chen, Hsiang-Yu Yu & Cheng-Chia Lee

  4. Brain Research Center, National Yang Ming Chiao Tung University, Taipei, Taiwan

    Chien-Chen Chou, Chien Chen, Hsiang-Yu Yu & Cheng-Chia Lee

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  1. Chang-Lin Han
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Correspondence to Cheng-Chia Lee.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the Taipei Veterans General Hospital and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Han, CL., Chou, CC., Chen, HH. et al. Frame-based versus robot-assisted stereo-electro-encephalography for drug-resistant epilepsy. Acta Neurochir 166, 85 (2024). https://doi.org/10.1007/s00701-024-05983-6

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