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Outcome after individualized stereoelectroencephalography (sEEG) implantation and navigated resection in patients with lesional and non-lesional focal epilepsy

  • Jun Thorsteinsdottir
  • Christian Vollmar
  • Jörg-Christian Tonn
  • Friedrich-Wilhelm Kreth
  • Soheyl Noachtar
  • Aurelia PeraudEmail author
Original Communication
  • 46 Downloads

Abstract

Background

Refined localization of the epileptogenic zone (EZ) in patients with pharmacoresistant focal epilepsy proceeding to resective surgery might improve postoperative outcome. We here report seizure outcome after stereo EEG (sEEG) evaluation with individually planned stereotactically implanted depth electrodes and subsequent tailored resection.

Methods

A cohort of consecutive patients with pharmacoresistant focal epilepsy, evaluated with a non-invasive evaluation protocol and invasive monitoring with personalized, stereotactically implanted depth electrodes for sEEG was analyzed. Co-registration of post-implantation CT scan to presurgical MRI data was used for 3D reconstructions of the patients’ brain surface and mapping of neurophysiology data. Individual multimodal 3D maps of the EZ were used to guide subsequent tailored resections. The outcome was rated according to the Engel classification.

Results

Out of 914 patients who underwent non-invasive presurgical evaluation, 85 underwent sEEG, and 70 were included in the outcome analysis. Median follow-up was 31.5 months. Seizure-free outcome (Engel class I A-C, ILAE class 1–2) was achieved in 83% of the study cohort. Patients exhibiting lesional and non-lesional (n = 42, 86% vs. n = 28, 79%), temporal and extratemporal (n = 45, 80% vs. n = 25, 84%), and right- and left-hemispheric epilepsy (n = 44, 82% vs. n = 26, 85%) did similarly well. This remains also true for those with an EZ adjacent to or distant from eloquent cortex (n = 21, 86% vs. n = 49, 82%). Surgical outcome was independent of resected tissue volume.

Conclusion

Favourable post-surgical outcome can be achieved in patients with resistant focal epilepsy, using individualized sEEG evaluation and tailored navigated resection, even in patients with non-lesional or extratemporal focal epilepsy.

Keywords

Epilepsy Depth electrodes sEEG Navigation Lesional 

Notes

Compliance with ethical standards

Conflicts of interest

JCT discloses support for counselling and travel grants by Brainlab.

Ethical standard

The study has been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Informed consent was obtained from all patients.

References

  1. 1.
    Kwan P, Schachter SC, Brodie MJ (2011) Drug-resistant epilepsy. N Engl J Med 365(10):919–926.  https://doi.org/10.1056/NEJMra1004418 Google Scholar
  2. 2.
    Rosenow F, Luders H (2001) Presurgical evaluation of epilepsy. Brain 124(Pt 9):1683–700Google Scholar
  3. 3.
    Noachtar S, Borggraefe I (2009) Epilepsy surgery: a critical review. Epilepsy Behav 15(1):66–72.  https://doi.org/10.1016/j.yebeh.2009.02.028 Google Scholar
  4. 4.
    Bartolomei F, Trebuchon A, Bonini F, Lambert I, Gavaret M, Woodman M et al (2016) What is the concordance between the seizure onset zone and the irritative zone? A SEEG quantified study. Clin Neurophysiol 127(2):1157–1162.  https://doi.org/10.1016/j.clinph.2015.10.029 Google Scholar
  5. 5.
    Ryvlin P, Cross JH, Rheims S (2014) Epilepsy surgery in children and adults. Lancet Neurol 13(11):1114–1126.  https://doi.org/10.1016/S1474-4422(14)70156-5 Google Scholar
  6. 6.
    David O, Blauwblomme T, Job AS, Chabardes S, Hoffmann D, Minotti L et al (2011) Imaging the seizure onset zone with stereo-electroencephalography. Brain 134(Pt 10):2898–2911.  https://doi.org/10.1093/brain/awr238 Google Scholar
  7. 7.
    Wellmer J, von der Groeben F, Klarmann U, Weber C, Elger CE, Urbach H et al (2012) Risks and benefits of invasive epilepsy surgery workup with implanted subdural and depth electrodes. Epilepsia 53(8):1322-32.  https://doi.org/10.1111/j.1528-1167.2012.03545.x Google Scholar
  8. 8.
    de Tisi J, Bell GS, Peacock JL, McEvoy AW, Harkness WF, Sander JW et al (2011) The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study. Lancet 378(9800):1388–1395.  https://doi.org/10.1016/S0140-6736(11)60890-8 Google Scholar
  9. 9.
    West S, Nolan SJ, Cotton J, Gandhi S, Weston J, Sudan A et al (2015) Surgery for epilepsy. Cochrane Database Syst Rev.  https://doi.org/10.1002/14651858.CD010541.pub2 Google Scholar
  10. 10.
    Winkler PA, Vollmar C, Krishnan KG, Pfluger T, Bruckmann H, Noachtar S (2000) Usefulness of 3-D reconstructed images of the human cerebral cortex for localization of subdural electrodes in epilepsy surgery. Epilepsy Res 41(2):169–78Google Scholar
  11. 11.
    Vollmar CNS, Winkler PA (2008) Multimodal image processing in pre-surgical planning. In: HO L (ed) Textbook of epilepsy surgery. Informa UK Ltd, London, pp 771–777Google Scholar
  12. 12.
    Engel J (2001) Classification of epileptic disorders. Epilepsia 42(3):316Google Scholar
  13. 13.
    Wieser HG, Blume WT, Fish D, Goldensohn E, Hufnagel A, King D et al (2001) ILAE Commission Report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia 42(2):282–6Google Scholar
  14. 14.
    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(2):323–30.  https://doi.org/10.1111/j.1528-1167.2012.03672.x Google Scholar
  15. 15.
    Gonzalez-Martinez J, Mullin J, Bulacio J, Gupta A, Enatsu R, Najm I et al (2014) Stereoelectroencephalography in children and adolescents with difficult-to-localize refractory focal epilepsy. Neurosurgery 75(3):258–68.  https://doi.org/10.1227/NEU.0000000000000453 (discussion 67–8) Google Scholar
  16. 16.
    Tellez-Zenteno JF, Hernandez Ronquillo L, Moien-Afshari F, Wiebe S (2010) Surgical outcomes in lesional and non-lesional epilepsy: a systematic review and meta-analysis. Epilepsy Res 89(2–3):310–318  https://doi.org/10.1016/j.eplepsyres.2010.02.007 Google Scholar
  17. 17.
    Garcia-Lorenzo B, Del Pino-Sedeno T, Rocamora R, Lopez JE, Serrano-Aguilar P, Trujillo-Martin MM (2018) Stereoelectroencephalography for refractory epileptic patients considered for surgery: systematic review, meta-analysis, and economic evaluation. Neurosurgery.  https://doi.org/10.1093/neuros/nyy261 Google Scholar
  18. 18.
    Bulacio JC, Jehi L, Wong C, Gonzalez-Martinez J, Kotagal P, Nair D et al (2012) Long-term seizure outcome after resective surgery in patients evaluated with intracranial electrodes. Epilepsia 53(10):1722–30.  https://doi.org/10.1111/j.1528-1167.2012.03633.x Google Scholar
  19. 19.
    Carrette E, Vonck K, De Herdt V, Van Dycke A, El Tahry R, Meurs A et al (2010) Predictive factors for outcome of invasive video-EEG monitoring and subsequent resective surgery in patients with refractory epilepsy. Clin Neurol Neurosurg 112(2):118–126.  https://doi.org/10.1016/j.clineuro.2009.10.017 Google Scholar
  20. 20.
    Immonen A, Jutila L, Muraja-Murro A, Mervaala E, Aikia M, Lamusuo S et al (2010) Long-term epilepsy surgery outcomes in patients with MRI-negative temporal lobe epilepsy. Epilepsia 51(11):2260–9.  https://doi.org/10.1111/j.1528-1167.2010.02720.x Google Scholar
  21. 21.
    Gonzalez-Martinez J, Mullin J, Vadera S, Bulacio J, Hughes G, Jones S et al (2014) Stereotactic placement of depth electrodes in medically intractable epilepsy. J Neurosurg 120(3):639–644  https://doi.org/10.3171/2013.11.JNS13635 Google Scholar
  22. 22.
    Bien CG, Szinay M, Wagner J, Clusmann H, Becker AJ, Urbach H (2009) Characteristics and surgical outcomes of patients with refractory magnetic resonance imaging-negative epilepsies. Arch Neurol 66(12):1491–1499.  https://doi.org/10.1001/archneurol.2009.283 Google Scholar
  23. 23.
    Remi J, Vollmar C, de Marinis A, Heinlin J, Peraud A, Noachtar S (2011) Congruence and discrepancy of interictal and ictal EEG with MRI lesions in focal epilepsies. Neurology 77(14):1383–1390.  https://doi.org/10.1212/WNL.0b013e31823152c3 Google Scholar
  24. 24.
    Chang EF, Wang DD, Barkovich AJ, Tihan T, Auguste KI, Sullivan JE et al (2011) Predictors of seizure freedom after surgery for malformations of cortical development. Ann Neurol 70(1):151–162Google Scholar
  25. 25.
    DiLorenzo DJ, Mangubat EZ, Rossi MA, Byrne RW (2014) Chronic unlimited recording electrocorticography-guided resective epilepsy surgery: technology-enabled enhanced fidelity in seizure focus localization with improved surgical efficacy. J Neurosurg 120(6):1402–1414.  https://doi.org/10.3171/2014.1.JNS131592 Google Scholar
  26. 26.
    Hamiwka L, Jayakar P, Resnick T, Morrison G, Ragheb J, Dean P et al (2005) Surgery for epilepsy due to cortical malformations: ten-year follow-up. Epilepsia 46(4):556–60.  https://doi.org/10.1111/j.0013-9580.2005.52504.x Google Scholar
  27. 27.
    O’Brien TJ, So EL, Mullan BP, Cascino GD, Hauser MF, Brinkmann BH et al (2000) Subtraction peri-ictal SPECT is predictive of extratemporal epilepsy surgery outcome. Neurology 55(11):1668–1677Google Scholar
  28. 28.
    Sakamoto S, Takami T, Tsuyuguchi N, Morino M, Ohata K, Inoue Y et al (2009) Prediction of seizure outcome following epilepsy surgery: asymmetry of thalamic glucose metabolism and cerebral neural activity in temporal lobe epilepsy. Seizure 18(1):1–6.  https://doi.org/10.1016/j.seizure.2008.05.004 Google Scholar
  29. 29.
    Zentner J, Hufnagel A, Wolf HK, Ostertun B, Behrens E, Campos MG et al (1995) Surgical treatment of temporal lobe epilepsy: clinical, radiological, and histopathological findings in 178 patients. J Neurol Neurosurg Psychiatry 58(6):666–73Google Scholar
  30. 30.
    McIntosh AM, Averill CA, Kalnins RM, Mitchell LA, Fabinyi GC, Jackson GD et al (2012) Long-term seizure outcome and risk factors for recurrence after extratemporal epilepsy surgery. Epilepsia 53(6):970–8.  https://doi.org/10.1111/j.1528-1167.2012.03430.x Google Scholar
  31. 31.
    Delev D, Oehl B, Steinhoff BJ, Nakagawa J, Scheiwe C, Schulze-Bonhage A et al (2018) Surgical treatment of extratemporal epilepsy: results and prognostic factors. Neurosurgery.  https://doi.org/10.1093/neuros/nyy099 Google Scholar
  32. 32.
    Liang S, Li A, Zhao M, Jiang H, Meng X, Sun Y (2010) Anterior temporal lobectomy combined with anterior corpus callosotomy in patients with temporal lobe epilepsy and mental retardation. Seizure 19(6):330–334.  https://doi.org/10.1016/j.seizure.2010.05.001 Google Scholar
  33. 33.
    Schramm J, Lehmann TN, Zentner J, Mueller CA, Scorzin J, Fimmers R et al (2011) Randomized controlled trial of 2.5-cm versus 3.5-cm mesial temporal resection in temporal lobe epilepsy–Part 1: intent-to-treat analysis. Acta Neurochir (Wien) 153(2):209–219.  https://doi.org/10.1007/s00701-010-0900-6 Google Scholar
  34. 34.
    Wyler AR, Hermann BP, Somes G (1995) Extent of medial temporal resection on outcome from anterior temporal lobectomy: a randomized prospective study. Neurosurgery 37(5):982–990 (discussion 90–1) Google Scholar
  35. 35.
    Althausen A, Gleissner U, Hoppe C, Sassen R, Buddewig S, von Lehe M et al (2013) Long-term outcome of hemispheric surgery at different ages in 61 epilepsy patients. J Neurol Neurosurg Psychiatry 84(5):529–536.  https://doi.org/10.1136/jnnp-2012-303811 Google Scholar
  36. 36.
    Dorward IG, Titus JB, Limbrick DD, Johnston JM, Bertrand ME, Smyth MD (2011) Extratemporal, nonlesional epilepsy in children: postsurgical clinical and neurocognitive outcomes. J Neurosurg Pediatr 7(2):179–188.  https://doi.org/10.3171/2010.11.PEDS10265 Google Scholar
  37. 37.
    Elsharkawy AE, Behne F, Oppel F, Pannek H, Schulz R, Hoppe M et al (2008) Long-term outcome of extratemporal epilepsy surgery among 154 adult patients. J Neurosurg 108(4):676–686.  https://doi.org/10.3171/JNS/2008/108/4/0676 Google Scholar
  38. 38.
    Lee JJ, Lee SK, Lee SY, Park KI, Kim DW, Lee DS et al (2008) Frontal lobe epilepsy: clinical characteristics, surgical outcomes and diagnostic modalities. Seizure 17(6):514–523.  https://doi.org/10.1016/j.seizure.2008.01.007 Google Scholar
  39. 39.
    Liava A, Francione S, Tassi L, Lo Russo G, Cossu M, Mai R et al (2012) Individually tailored extratemporal epilepsy surgery in children: anatomo-electro-clinical features and outcome predictors in a population of 53 cases. Epilepsy Behav 25(1):68–80  https://doi.org/10.1016/j.yebeh.2012.05.008 Google Scholar
  40. 40.
    Pinheiro-Martins AP, Bianchin MM, Velasco TR, Terra VC, Araujo D, Wichert-Ana L et al (2012) Independent predictors and a prognostic model for surgical outcome in refractory frontal lobe epilepsy. Epilepsy Res 99(1–2):55–63.  https://doi.org/10.1016/j.eplepsyres.2011.10.008 Google Scholar
  41. 41.
    Tigaran S, Cascino GD, McClelland RL, So EL, Richard Marsh W (2003) Acute postoperative seizures after frontal lobe cortical resection for intractable partial epilepsy. Epilepsia 44(6):831–5Google Scholar
  42. 42.
    Urbach H, Binder D, von Lehe M, Podlogar M, Bien CG, Becker A et al (2007) Correlation of MRI and histopathology in epileptogenic parietal and occipital lobe lesions. Seizure 16(7):608–614.  https://doi.org/10.1016/j.seizure.2007.04.009 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Jun Thorsteinsdottir
    • 1
  • Christian Vollmar
    • 2
  • Jörg-Christian Tonn
    • 1
  • Friedrich-Wilhelm Kreth
    • 1
  • Soheyl Noachtar
    • 2
  • Aurelia Peraud
    • 1
    • 3
    Email author
  1. 1.Department of NeurosurgeryUniversity Hospital of Munich, Ludwig-Maximilians-UniversityMunichGermany
  2. 2.Department of NeurologyUniversity Hospital of Munich, Ludwig-Maximilians-UniversityMunichGermany
  3. 3.Department of NeurosurgeryUniversity Hospital of UlmUlmGermany

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