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Review

Stereoelectroencephalography in epilepsy, cognitive neurophysiology, and psychiatric disease: safety, efficacy, and place in therapy

, &
Pages 1701-1716 | Published online: 28 Jun 2019

References

  • Brodie MJ, Barry SJ, Bamagous GA, Norrie JD, Kwan P. Patterns of treatment response in newly diagnosed epilepsy. Neurology. 2012;78(20):1548–1554. doi:10.1212/WNL.0b013e3182563b1922573629
  • Kwan P, Brodie MJ. Early identification of refractory epilepsy. N Engl J Med. 2000;342(5):314–319. doi:10.1056/NEJM20000203342050310660394
  • Kwan P, Arzimanoglou A, Berg AT, et al. Definition of drug resistant epilepsy: consensus proposal by the ad hoc task force of the ILAE commission on therapeutic strategies. Epilepsia. 2010;51(6):1069–1077. doi:10.1111/j.1528-1167.2009.02397.x19889013
  • Englot DJ, Wang DD, Rolston JD, Shih TT, Chang EF. Rates and predictors of long-term seizure freedom after frontal lobe epilepsy surgery: a systematic review and meta-analysis. J Neurosurg. 2012;116(5):1042–1048. doi:10.3171/2012.1.JNS11162022304450
  • Piotrowska N, Winkler PA. Otfrid Foerster, the great neurologist and neurosurgeon from Breslau (Wroclaw): his influence on early neurosurgeons and legacy to present-day neurosurgery. J Neurosurg. 2007;107(2):451–456. doi:10.3171/JNS-07/08/045117695406
  • Penfield W, Jasper HH. Epilepsy and the Functional Anatomy of the Human Brain. 1st ed. Boston: Little; 1954.
  • Voorhies JM, Cohen-Gadol A. Techniques for placement of grid and strip electrodes for intracranial epilepsy surgery monitoring: pearls and pitfalls. Surg Neurol Int. 2013;4:98. doi:10.4103/2152-7806.11570723956941
  • Gonzalez-Martinez JA. The stereo-electroencephalography: the epileptogenic zone. J Clin Neurophysiol. 2016;33(6):522–529. doi:10.1097/WNP.000000000000028727918347
  • Iida K, Otsubo H. Stereoelectroencephalography: indication and efficacy. Neurol Med Chir (Tokyo). 2017;57(8):375–385. doi:10.2176/nmc.ra.2017-000828637943
  • Talairach J, Tournoux P. Co-Planar Stereotaxic Atlas of the Human Brain: An Approach to Medical Cerebral Imaging. Stuttgart, New York: G. Thieme; Thieme Medical Publishers; 1988.
  • 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. doi:10.1097/WNP.000000000000028727918344
  • Podkorytova I, Hoes K, Lega B. Stereo-encephalography versus subdural electrodes for seizure localization. Neurosurg Clin N Am. 2016;27(1):97–109. doi:10.1016/j.nec.2015.11.00526615112
  • Scorza D, Amoroso G, Cortes C, et al. Experience-based SEEG planning: from retrospective data to automated electrode trajectories suggestions. Healthc Technol Lett. 2018;5(5):167–171. doi:10.1049/htl.2018.507530464848
  • Musolino A, Tournoux P, Missir O, Talairach J. Methodology of “in vivo” anatomical study and stereo-electroencephalographic exploration in brain surgery for epilepsy. J Neuroradiol. 1990;17(2):67–102.2123498
  • Goto T, Hongo K, Kakizawa Y, et al. Clinical application of robotic telemanipulation system in neurosurgery. Case report. J Neurosurg. 2003;99(6):1082–1084. doi:10.3171/jns.2003.99.6.108214705738
  • Sutherland GR, Maddahi Y, Gan LS, Lama S, Zareinia K. Robotics in the neurosurgical treatment of glioma. Surg Neurol Int. 2015;6(Suppl 1):S1–8. doi:10.4103/2152-7806.17002425722932
  • Gonzalez-Martinez J, Bulacio J, Thompson S, et al. Technique, results, and complications related to robot-assisted stereoelectroencephalography. Neurosurgery. 2016;78(2):169–180. doi:10.1227/NEU.000000000000103426418870
  • 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. doi:10.1111/epi.1329826899389
  • McGovern RA, Knight EP, Gupta A, et al. Robot-assisted stereoelectroencephalography in children. J Neurosurg Pediatr. 2018;23(3):288–296. doi:10.3171/2018.7.PEDS1830530544342
  • Sacino MF, Huang SS, Schreiber J, Gaillard WD, Oluigbo CO. Is the use of stereotactic electroencephalography safe and effective in children? A meta-analysis of the use of stereotactic electroencephalography in comparison to subdural grids for invasive epilepsy monitoring in pediatric subjects. Neurosurgery 2019;84(6):1190–1200. doi:10.1093/neuros/nyy466
  • Goldstein HE, Youngerman BE, Shao B, et al. Safety and efficacy of stereoelectroencephalography in pediatric focal epilepsy: a single-center experience. J Neurosurg Pediatr. 2018;22(4):444–452. doi:10.3171/2018.5.PEDS185630028270
  • 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(5):1173–1181. doi:10.3171/2017.6.JNS1788129243976
  • Yu H, Pistol C, Franklin R, Barborica A. Clinical accuracy of customized stereotactic fixtures for stereoelectroencephalography. World Neurosurg. 2018;109:82–88. doi:10.1016/j.wneu.2017.09.08928951181
  • Vakharia VN, Sparks R, O’Keeffe AG, et al. Accuracy of intracranial electrode placement for stereoencephalography: a systematic review and meta-analysis. Epilepsia. 2017;58(6):921–932. doi:10.1111/epi.1371328261785
  • Abhinav K, Prakash S, Sandeman DR. Use of robot-guided stereotactic placement of intracerebral electrodes for investigation of focal epilepsy: initial experience in the UK. Br J Neurosurg. 2013;27(5):704–705. doi:10.3109/02688697.2013.79885923808680
  • Sparks R, Vakharia V, Rodionov R, et al. Assessment of a micro-guided robotic system for seeg electrode placement in a skull phantom. American Epilepsy Society Annual Meeting; December 1–5; 2017; Washington, DC.
  • Duncan J. A randomised control trial of SEEG electrode placement methods. ISRCTN Registry. 2018 Available from: http://www.isrctn.com/ISRCTN17209025. Accessed June 18, 2019.
  • Lefranc M, Capel C, Pruvot AS, et al. The impact of the reference imaging modality, registration method and intraoperative flat-panel computed tomography on the accuracy of the ROSA(R) stereotactic robot. Stereotact Funct Neurosurg. 2014;92(4):242–250. doi:10.1159/00036293625170634
  • Cardinale F, Cossu M, Castana L, et al. Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures. Neurosurgery. 2013;72(3):353–366.
  • Sparks R, Zombori G, Rodionov R, et al. Automated multiple trajectory planning algorithm for the placement of stereo-electroencephalography (SEEG) electrodes in epilepsy treatment. Int J Comput Assist Radiol Surg. 2017;12(1):123–136. doi:10.1007/s11548-016-1452-x27368184
  • Taussig D, Montavont A, Isnard J. Invasive EEG explorations. Neurophysiol Clin. 2015;45(1):113–119. doi:10.1016/j.neucli.2014.11.00625703438
  • McGovern RA, Ruggieri P, Bulacio J, Najm I, Bingaman WE, Gonzalez-Martinez JA. Risk analysis of hemorrhage in stereo-electroencephalography procedures. Epilepsia. 2019;60(3):571–580. doi:10.1111/epi.2019.60.issue-330746685
  • Arya R, Mangano FT, Horn PS, Holland KD, Rose DF, Glauser TA. Adverse events related to extraoperative invasive EEG monitoring with subdural grid electrodes: a systematic review and meta-analysis. Epilepsia. 2013;54(5):828–839. doi:10.1111/epi.2013.54.issue-523294329
  • Tandon N, Tong BA, Friedman ER, et al. Analysis of morbidity and outcomes associated with use of subdural grids vs stereoelectroencephalography in patients with intractable epilepsy. JAMA Neurol. 2019. doi:10.1001/jamaneurol.2019.0098
  • Gooneratne IK, Mannan S, de Tisi J, et al. Somatic complications of epilepsy surgery over 25 years at a single center. Epilepsy Res. 2017;132:70–77. doi:10.1016/j.eplepsyres.2017.02.01628324680
  • Garcia-Lorenzo B, Del Pino-Sedeno T, Rocamora R, Lopez JE, Serrano-Aguilar P, Trujillo-Martin MM. Stereoelectroencephalography for refractory epileptic patients considered for surgery: systematic review, meta-analysis, and economic evaluation. Neurosurgery. 2019;84(2):326–338. doi:10.1093/neuros/nyy13729982799
  • Vadera S, Mullin J, Bulacio J, Najm I, Bingaman W, Gonzalez-Martinez J. Stereoelectroencephalography following subdural grid placement for difficult to localize epilepsy. Neurosurgery. 2013;72(5):723–729.
  • Steriade C, Martins W, Bulacio J, et al. Localization yield and seizure outcome in patients undergoing bilateral SEEG exploration. Epilepsia. 2019;60(1):107–120. doi:10.1111/epi.1462430588603
  • Cossu M, Cardinale F, Castana L, et al. Stereoelectroencephalography in the presurgical evaluation of focal epilepsy: a retrospective analysis of 215 procedures. Neurosurgery. 2005;57(4):706–718.
  • Thorsteinsdottir J, Vollmar C, Tonn JC, Kreth FW, Noachtar S, Peraud A. Outcome after individualized stereoelectroencephalography (sEEG) implantation and navigated resection in patients with lesional and non-lesional focal epilepsy. J Neurol. 2019. doi:10.1007/s00415-019-09213-3
  • Youngerman BE, Oh JY, Anbarasan D, et al. Laser ablation is effective for temporal lobe epilepsy with and without mesial temporal sclerosis if hippocampal seizure onsets are localized by stereoelectroencephalography. Epilepsia. 2018;59(3):595–606. doi:10.1111/epi.1400429392715
  • Tao JX, Wu S, Lacy M, et al. Stereotactic EEG-guided laser interstitial thermal therapy for mesial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry. 2018;89(5):542–548. doi:10.1136/jnnp-2017-31683329183959
  • Suresh S, Sweet J, Fastenau PS, Luders H, Landazuri P, Miller J. Temporal lobe epilepsy in patients with nonlesional MRI and normal memory: an SEEG study. J Neurosurg. 2015;123(6):1368–1374. doi:10.3171/2015.1.JNS14181126207602
  • Kubota Y, Ochiai T, Hori T, Kawamata T. Usefulness of StereoEEG-based tailored surgery for medial temporal lobe epilepsy. Preliminary results in 11 patients. Clin Neurol Neurosurg. 2017;158:67–71. doi:10.1016/j.clineuro.2017.04.02628482271
  • Ross L, Naduvil AM, Bulacio JC, Najm IM, Gonzalez-Martinez JA. Stereoelectroencephalography-guided laser ablations in patients with neocortical pharmacoresistant focal epilepsy: concept and operative technique. Oper Neurosurg. 2018;15(6):656–663. doi:10.1093/ons/opy106
  • Cobourn K, Fayed I, Keating RF, Oluigbo CO. Early outcomes of stereoelectroencephalography followed by MR-guided laser interstitial thermal therapy: a paradigm for minimally invasive epilepsy surgery. Neurosurg Focus. 2018;45(3):E8. doi:10.3171/2018.6.FOCUS18209
  • Ellis JA, Mejia Munne JC, Wang SH, et al. Staged laser interstitial thermal therapy and topectomy for complete obliteration of complex focal cortical dysplasias. J Clin Neurosci. 2016;31:224–228. doi:10.1016/j.jocn.2016.02.01627234607
  • Alomar S, Mullin JP, Smithason S, Gonzalez-Martinez J. Indications, technique, and safety profile of insular stereoelectroencephalography electrode implantation in medically intractable epilepsy. J Neurosurg. 2018;128(4):1147–1157. doi:10.3171/2017.1.JNS16107028621621
  • Kahane P, Ryvlin P, Hoffmann D, Minotti L, Benabid AL. From hypothalamic hamartoma to cortex: what can be learnt from depth recordings and stimulation? Epileptic Disord. 2003;5(4):205–217.14975789
  • Scholly J, Staack AM, Kahane P, et al. Hypothalamic hamartoma: epileptogenesis beyond the lesion? Epilepsia. 2017;58(Suppl 2):32–40. doi:10.1111/epi.1375528591482
  • Wei PH, An Y, Fan XT, et al. Stereoelectroencephalography-guided radiofrequency thermocoagulation for hypothalamic hamartomas: preliminary evidence. World Neurosurg. 2018;114:e1073–e1078. doi:10.1016/j.wneu.2018.03.08229605700
  • Mirandola L, Mai RF, Francione S, et al. Stereo-EEG: diagnostic and therapeutic tool for periventricular nodular heterotopia epilepsies. Epilepsia. 2017;58(11):1962–1971. doi:10.1111/epi.1389528880999
  • Thompson SA, Kalamangalam GP, Tandon N. Intracranial evaluation and laser ablation for epilepsy with periventricular nodular heterotopia. Seizure. 2016;41:211–216. doi:10.1016/j.seizure.2016.06.01927461957
  • Schmidt RF, Wu C, Lang MJ, et al. Complications of subdural and depth electrodes in 269 patients undergoing 317 procedures for invasive monitoring in epilepsy. Epilepsia. 2016;57(10):1697–1708. doi:10.1111/epi.1350327549686
  • Wellmer J, von der Groeben F, Klarmann U, et al. Risks and benefits of invasive epilepsy surgery workup with implanted subdural and depth electrodes. Epilepsia. 2012;53(8):1322–1332. doi:10.1111/j.1528-1167.2012.03545.x22708979
  • Gonzalez-Martinez J, Najm IM. Indications and selection criteria for invasive monitoring in children with cortical dysplasia. Childs Nerv Syst. 2014;30(11):1823–1829. doi:10.1007/s00381-014-2497-125296543
  • Mo JJ, Hu WH, Zhang C, et al. Value of stereo-electroencephalogram in reoperation of patients with pharmacoresistant epilepsy: a single center, retrospective study. Br J Neurosurg. 2018;32(6):663–670. doi:10.1080/02688697.2017.137434830317876
  • Bourdillon P, Cucherat M, Isnard J, et al. Stereo-electroencephalography-guided radiofrequency thermocoagulation in patients with focal epilepsy: a systematic review and meta-analysis. Epilepsia. 2018;59(12):2296–2304. doi:10.1111/epi.1458430345535
  • Bartolomei F, Lagarde S, Wendling F, et al. Defining epileptogenic networks: contribution of SEEG and signal analysis. Epilepsia. 2017;58(7):1131–1147. doi:10.1111/epi.1379128543030
  • Parvizi J, Kastner S. Promises and limitations of human intracranial electroencephalography. Nat Neurosci. 2018;21(4):474–483. doi:10.1038/s41593-018-0108-229507407
  • Ray S, Crone NE, Niebur E, Franaszczuk PJ, Hsiao SS. Neural correlates of high-gamma oscillations (60–200 Hz) in macaque local field potentials and their potential implications in electrocorticography. J Neurosci. 2008;28(45):11526–11536. doi:10.1523/JNEUROSCI.2709-08.200818987189
  • Kreiman G, Hung CP, Kraskov A, Quiroga RQ, Poggio T, DiCarlo JJ. Object selectivity of local field potentials and spikes in the macaque inferior temporal cortex. Neuron. 2006;49(3):433–445. doi:10.1016/j.neuron.2005.12.01916446146
  • Mukamel R, Gelbard H, Arieli A, Hasson U, Fried I, Malach R. Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science. 2005;309(5736):951–954. doi:10.1126/science.111616816081741
  • Manning JR, Jacobs J, Fried I, Kahana MJ. Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J Neurosci. 2009;29(43):13613–13620. doi:10.1523/JNEUROSCI.2041-09.200919864573
  • Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001;412(6843):150–157. doi:10.1038/3508400511449264
  • Niessing J, Ebisch B, Schmidt KE, Niessing M, Singer W, Galuske RA. Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science. 2005;309(5736):948–951. doi:10.1126/science.111616816081740
  • Popa I, Donos C, Barborica A, et al. Intrusive thoughts elicited by direct electrical stimulation during stereo-electroencephalography. Front Neurol. 2016;7:114. doi:10.3389/fneur.2016.0011427486431
  • Zanello M, Pallud J, Baup N, et al. History of psychosurgery at Sainte-Anne Hospital, Paris, France, through translational interactions between psychiatrists and neurosurgeons. Neurosurg Focus. 2017;43(3):E9. doi:10.3171/2017.6.FOCUS17250
  • Youngerman BE, Chan AK, Mikell CB, McKhann GM, Sheth SA. A decade of emerging indications: deep brain stimulation in the United States. J Neurosurg. 2016;125(2):461–471. doi:10.3171/2015.7.JNS14259926722851
  • Youngerman BE, Shah S, Sheth SA. DBS for Other Emerging Psychiatric Indications. New York: Thieme; 2019.
  • Widge AS, Deckersbach T, Eskandar EN, Dougherty DD. Deep brain stimulation for treatment-resistant psychiatric illnesses: what has gone wrong and what should we do next? Biol Psychiatry. 2016;79(4):e9–10. doi:10.1016/j.biopsych.2015.06.00526212895
  • Choi KS, Noecker AM, Riva-Posse P, et al. Impact of brain shift on subcallosal cingulate deep brain stimulation. Brain Stimul. 2018;11(2):445–453. doi:10.1016/j.brs.2017.12.00129246748
  • ClinicalTrials.gov. Deep Brain Stimulation (DBS) for Depression Using Directional Current Steering and Individualized Network Targeting. Available from: https://clinicaltrials.gov/ct2/show/NCT03437928.  Accessed June 4, 2019.
  • Morrell MJ, Group RNSSiES. Responsive cortical stimulation for the treatment of medically intractable partial epilepsy. Neurology. 2011;77(13):1295–1304. doi:10.1212/WNL.0b013e318230205621917777
  • Widge AS, Ellard KK, Paulk AC, et al. Treating refractory mental illness with closed-loop brain stimulation: progress towards a patient-specific transdiagnostic approach. Exp Neurol. 2017;287(Pt 4):461–472.27485972
  • ClinicalTrials.gov. Responsive Neurostimulation For Loss Of Control Eating (DBSLOC). Available from: https://clinicaltrials.gov/ct2/show/NCT03868670. Accessed June 4, 2019.
  • The Brain Initiative. Electrophysiological biomarkers to optimize DBS for depression. Available from: https://braininitiative.nih.gov/funded-awards/electrophysiological-biomarkers-optimize-dbs-depression. Accessed May 20, 2019.
  • Ciganek L, Sramka M, Nadvornik P, Fritz G. Effects of stereotactic operations in the treatment of epilepsies–neurological aspects. Acta Neurochir (Wien). 1976;(23 Suppl):201–204.793311
  • Munari C, Giallonardo AT, Brunet P, Broglin D, Bancaud J. Stereotactic investigations in frontal lobe epilepsies. Acta Neurochir Suppl (Wien). 1989;46:9–12.2505493
  • So N, Olivier A, Andermann F, Gloor P, Quesney LF. Results of surgical treatment in patients with bitemporal epileptiform abnormalities. Ann Neurol. 1989;25(5):432–439. doi:10.1002/(ISSN)1531-82492774484
  • Smith JR, Flanigin HF, King DW, et al. An 8-year experience with depth electrodes in the evaluation of ablative seizure surgery candidates. Stereotact Funct Neurosurg. 1990;54–55:60–66.
  • Hirsch LJ, Spencer SS, Williamson PD, Spencer DD, Mattson RH. Comparison of bitemporal and unitemporal epilepsy defined by depth electroencephalography. Ann Neurol. 1991;30(3):340–346. doi:10.1002/(ISSN)1531-82491952822
  • van Veelen CW, Debets RM. Functional neurosurgery in the treatment of epilepsy in The Netherlands. Aspects of presurgical evaluation and the contribution of subdural and stereotactically implanted depth electrodes in the Dutch Workgroup for functional surgery. Acta Neurochir (Wien). 1993;124(1):7–10. doi:10.1007/BF014007068279293
  • Espinosa J, Olivier A, Andermann F, Quesney F, Dubeau F, Savard G. Morbidity of chronic recording with intracranial depth electrodes in 170 patients. Stereotact Funct Neurosurg. 1994;63(1–4):63–65. doi:10.1159/0001002937624653
  • Ross DA, Brunberg JA, Drury I, Henry TR. Intracerebral depth electrode monitoring in partial epilepsy: the morbidity and efficacy of placement using magnetic resonance image-guided stereotactic surgery. Neurosurgery. 1996;39(2):327–333; discussion 333–324.
  • 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. doi:10.1159/00006459512378053
  • De Almeida AN, Olivier A, Quesney F, Dubeau F, Savard G, Andermann F. Efficacy of and morbidity associated with stereoelectroencephalography using computerized tomography–or magnetic resonance imaging-guided electrode implantation. J Neurosurg. 2006;104(4):483–487. doi:10.3171/jns.2006.104.4.48316619650
  • McGonigal A, Bartolomei F, Regis J, et al. Stereoelectroencephalography in presurgical assessment of MRI-negative epilepsy. Brain. 2007;130(Pt 12):3169–3183. doi:10.1093/brain/awm21817855377
  • Gonzalez-Martinez J, Bulacio J, Alexopoulos A, Jehi L, Bingaman W, Najm I. Stereoelectroencephalography in the “difficult to localize” refractory focal epilepsy: early experience from a North American epilepsy center. Epilepsia. 2013;54(2):323–330. doi:10.1111/epi.2013.54.issue-223016576
  • Serletis D, Bulacio J, Bingaman W, Najm I, Gonzalez-Martinez J. The stereotactic approach for mapping epileptic networks: a prospective study of 200 patients. J Neurosurg. 2014;121(5):1239–1246. doi:10.3171/2014.8.JNS13199125148007
  • Gonzalez-Martinez J, Mullin J, Vadera S, et al. Stereotactic placement of depth electrodes in medically intractable epilepsy. J Neurosurg. 2014;120(3):639–644. doi:10.3171/2013.11.JNS1363524405074
  • Taussig D, Chipaux M, Lebas A, et al. Stereo-electroencephalography (SEEG) in 65 children: an effective and safe diagnostic method for pre-surgical diagnosis, independent of age. Epileptic Disord. 2014;16(3):280–295.25256655
  • Cossu M, Fuschillo D, Casaceli G, et al. Stereoelectroencephalography-guided radiofrequency thermocoagulation in the epileptogenic zone: a retrospective study on 89 cases. J Neurosurg. 2015;123(6):1358–1367. doi:10.3171/2014.12.JNS14196826090841