A 360° electronic device for recording high-resolution intraoperative electrocorticography of the brain during awake craniotomy

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  • 1 Departments of Neurosurgery and
  • 2 Neurology, Mayo Clinic, Jacksonville, Florida;
  • 3 Departments of Neurology and
  • 4 Physiology and Biomedical Engineering, Mayo Clinic, Rochester, Minnesota;
  • 5 Department of Radiology, Mayo Clinic, Jacksonville, Florida;
  • 6 Department of Mathematics, University of Texas at Austin, Austin, Texas; and
  • 7 Department of Anesthesiology, Mayo Clinic, Jacksonville, Florida
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OBJECTIVE

Epilepsy is common among patients with supratentorial brain tumors; approximately 40%–70% of patients with glioma develop brain tumor–related epilepsy (BTRE). Intraoperative localization of the epileptogenic zone during surgical tumor resection (real-time data) may improve intervention techniques in patients with lesional epilepsy, including BTRE. Accurate localization of the epileptogenic signals requires electrodes with high-density spatial organization that must be placed on the cortical surface during surgery. The authors investigated a 360° high-density ring-shaped cortical electrode assembly device, called the “circular grid,” that allows for simultaneous tumor resection and real-time electrophysiology data recording from the brain surface.

METHODS

The authors collected data from 99 patients who underwent awake craniotomy from January 2008 to December 2018 (29 patients with the circular grid and 70 patients with strip electrodes), of whom 50 patients were matched-pair analyzed (25 patients with the circular grid and 25 patients with strip electrodes). Multiple variables were then retrospectively assessed to determine if utilization of this device provides more accurate real-time data and improves patient outcomes.

RESULTS

Matched-pair analysis showed higher extent of resection (p = 0.03) and a shorter transient motor recovery period during the hospitalization course (by approximately 6.6 days, p ≤ 0.05) in the circular grid patients. Postoperative versus preoperative Karnofsky Performance Scale (KPS) score difference/drop was greater for the strip electrode patients (p = 0.007). No significant difference in postoperative seizures between the 2 groups was present (p = 0.80).

CONCLUSIONS

The circular grid is a safe, feasible tool that grants direct access to the cortical surgical surface for tissue resection while simultaneously monitoring electrical activity. Application of the circular grid to different brain pathologies may improve intraoperative epileptogenic detection accuracy and functional outcomes, while decreasing postoperative complications.

ABBREVIATIONS AD = afterdischarge; ECoG = electrocorticography; EOR = extent of resection; HD = high-density; KPS = Karnofsky Performance Scale; LOS = length of hospital stay.

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Contributor Notes

Correspondence Alfredo Quiñones-Hinojosa: Mayo Clinic, Jacksonville, FL. quinones@mayo.edu.

INCLUDE WHEN CITING Published online July 5, 2019; DOI: 10.3171/2019.4.JNS19261.

Disclosures Drs. Tatum, Quiñones-Hinojosa, and ReFaey filed a patent disclosing this device and technology (patent application no. PCT/US2018/039956).

  • 1

    Almeida AN, Martinez V, Feindel W: The first case of invasive EEG monitoring for the surgical treatment of epilepsy: historical significance and context. Epilepsia 46:10821085, 2005

    • Search Google Scholar
    • Export Citation
  • 2

    Arechiga N, ReFaey K, Rincon-Torroella J, Chaichana K, Quiñones-Hinojosa A: Cortical/subcortical motor mapping for gliomas, in Quiñones-Hinojosa A (ed): Video Atlas of Neurosurgery: Contemporary Tumor and Skull Base Surgery. Philadelphia: Elsevier, 2016, Vol 1

    • Search Google Scholar
    • Export Citation
  • 3

    Berger MS: Functional mapping-guided resection of low-grade gliomas. Clin Neurosurg 42:437452, 1995

  • 4

    Berger MS, Kincaid J, Ojemann GA, Lettich E: Brain mapping techniques to maximize resection, safety, and seizure control in children with brain tumors. Neurosurgery 25:786792, 1989

    • Search Google Scholar
    • Export Citation
  • 5

    Berger MS, Ojemann GA: Intraoperative brain mapping techniques in neuro-oncology. Stereotact Funct Neurosurg 58:153161, 1992

  • 6

    Berger MS, Ojemann GA, Lettich E: Neurophysiological monitoring during astrocytoma surgery. Neurosurg Clin N Am 1:6580, 1990

  • 7

    Blumcke I, Spreafico R, Haaker G, Coras R, Kobow K, Bien CG, : Histopathological findings in brain tissue obtained during epilepsy surgery. N Engl J Med 377:16481656, 2017

    • Search Google Scholar
    • Export Citation
  • 8

    Brunner P, Ritaccio AL, Lynch TM, Emrich JF, Wilson JA, Williams JC, : A practical procedure for real-time functional mapping of eloquent cortex using electrocorticographic signals in humans. Epilepsy Behav 15:278286, 2009

    • Search Google Scholar
    • Export Citation
  • 9

    Chaichana KL, Cabrera-Aldana EE, Jusue-Torres I, Wijesekera O, Olivi A, Rahman M, : When gross total resection of a glioblastoma is possible, how much resection should be achieved? World Neurosurg 82:e257e265, 2014

    • Search Google Scholar
    • Export Citation
  • 10

    Chaichana KL, Jusue-Torres I, Lemos AM, Gokaslan A, Cabrera-Aldana EE, Ashary A, : The butterfly effect on glioblastoma: is volumetric extent of resection more effective than biopsy for these tumors? J Neurooncol 120:625634, 2014

    • Search Google Scholar
    • Export Citation
  • 11

    Chaichana KL, Jusue-Torres I, Navarro-Ramirez R, Raza SM, Pascual-Gallego M, Ibrahim A, : Establishing percent resection and residual volume thresholds affecting survival and recurrence for patients with newly diagnosed intracranial glioblastoma. Neuro Oncol 16:113122, 2014

    • Search Google Scholar
    • Export Citation
  • 12

    Cho JR, Koo DL, Joo EY, Seo DW, Hong SC, Jiruska P, : Resection of individually identified high-rate high-frequency oscillations region is associated with favorable outcome in neocortical epilepsy. Epilepsia 55:18721883, 2014

    • Search Google Scholar
    • Export Citation
  • 13

    de Bittencourt PR, Sandmann MC, Moro MS, de Araújo JC: Simple, cost-effective technique for portable digital eletrocorticography. Arq Neuropsiquiatr 58 (2B):424427, 2000

    • Search Google Scholar
    • Export Citation
  • 14

    Engel J Jr: The etiologic classification of epilepsy. Epilepsia 52:11951197, 1205–1209, 2011

  • 15

    Eseonu CI, Eguia F, ReFaey K, Garcia O, Rodriguez FJ, Chaichana K, : Comparative volumetric analysis of the extent of resection of molecularly and histologically distinct low grade gliomas and its role on survival. J Neurooncol 134:6574, 2017

    • Search Google Scholar
    • Export Citation
  • 16

    Eseonu CI, ReFaey K, Garcia O, Raghuraman G, Quinones-Hinojosa A: Volumetric analysis of extent of resection, survival, and surgical outcomes for insular gliomas. World Neurosurg 103:265274, 2017

    • Search Google Scholar
    • Export Citation
  • 17

    Eseonu CI, Rincon-Torroella J, Lee YM: ReFaey K, Tripathi P, Quinones-Hinojosa A: Intraoperative seizures in awake craniotomy for perirolandic glioma resections that undergo cortical mapping. J Neurol Surg A Cent Eur Neurosurg 79:239246, 2018

    • Search Google Scholar
    • Export Citation
  • 18

    Eseonu CI, Rincon-Torroella J, ReFaey K, Lee YM, Nangiana J, Vivas-Buitrago T, : Awake craniotomy vs craniotomy under general anesthesia for perirolandic gliomas: evaluating perioperative complications and extent of resection. Neurosurgery 81:481489, 2017

    • Search Google Scholar
    • Export Citation
  • 19

    Feyissa AM, Worrell GA, Tatum WO, Mahato D, Brinkmann BH, Rosenfeld SS, : High-frequency oscillations in awake patients undergoing brain tumor-related epilepsy surgery. Neurology 90:e1119e1125, 2018

    • Search Google Scholar
    • Export Citation
  • 20

    Formaggio E, Storti SF, Tramontano V, Casarin A, Bertoldo A, Fiaschi A, : Frequency and time-frequency analysis of intraoperative ECoG during awake brain stimulation. Front Neuroeng 6:1, 2013

    • Search Google Scholar
    • Export Citation
  • 21

    Haglund MM, Berger MS, Shamseldin M, Lettich E, Ojemann GA: Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 34:567576, 1994

    • Search Google Scholar
    • Export Citation
  • 22

    Hervey-Jumper SL, Li J, Lau D, Molinaro AM, Perry DW, Meng L, : Awake craniotomy to maximize glioma resection: methods and technical nuances over a 27-year period. J Neurosurg 123:325339, 2015

    • Search Google Scholar
    • Export Citation
  • 23

    Kwan P, Arzimanoglou A, Berg AT, Brodie MJ, Allen Hauser W, Mathern G, : Definition of drug resistant epilepsy: consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies. Epilepsia 51:10691077, 2010

    • Search Google Scholar
    • Export Citation
  • 24

    Kwan P, Brodie MJ: Early identification of refractory epilepsy. N Engl J Med 342:314319, 2000

  • 25

    Lara-Velazquez M, Al-Kharboosh R, Jeanneret S, Vazquez-Ramos C, Mahato D, Tavanaiepour D, : Advances in brain tumor surgery for glioblastoma in adults. Brain Sci 7:E166, 2017

    • Search Google Scholar
    • Export Citation
  • 26

    Lima GLO, Dezamis E, Corns R, Rigaux-Viode O, Moritz-Gasser S, Roux A, : Surgical resection of incidental diffuse gliomas involving eloquent brain areas. Rationale, functional, epileptological and oncological outcomes. Neurochirurgie 63:250258, 2017

    • Search Google Scholar
    • Export Citation
  • 27

    Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, : The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97109, 2007

    • Search Google Scholar
    • Export Citation
  • 28

    Marks WJ: Invasive clinical neurophysiology in epilepsy and movement disorders, in Aminoff MJ (ed): Aminoff’s Electrodiagnosis in Clinical Neurology, ed 6. Philadelphia: Saunders, 2012

    • Search Google Scholar
    • Export Citation
  • 29

    Merrill DR, Bikson M, Jefferys JG: Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J Neurosci Methods 141:171198, 2005

    • Search Google Scholar
    • Export Citation
  • 30

    Mostofa AG, Punganuru SR, Madala HR, Al-Obaide M, Srivenugopal KS: The process and regulatory components of inflammation in brain oncogenesis. Biomolecules 7:E34, 2017

    • Search Google Scholar
    • Export Citation
  • 31

    Nossek E, Matot I, Shahar T, Barzilai O, Rapoport Y, Gonen T, : Intraoperative seizures during awake craniotomy: incidence and consequences: analysis of 477 patients. Neurosurgery 73:135140, 2013

    • Search Google Scholar
    • Export Citation
  • 32

    Ojemann GA: Neurosurgical management of epilepsy: a personal perspective in 1983. Appl Neurophysiol 46:1118, 1983

  • 33

    Quiñones-Hinojosa A, Ojemann SG, Sanai N, Dillon WP, Berger MS: Preoperative correlation of intraoperative cortical mapping with magnetic resonance imaging landmarks to predict localization of the Broca area. J Neurosurg 99:311318, 2003

    • Search Google Scholar
    • Export Citation
  • 34

    Sanai N, Berger MS: Glioma extent of resection and its impact on patient outcome. Neurosurgery 62:753766, 2008

  • 35

    Sanai N, Berger MS: Mapping the horizon: techniques to optimize tumor resection before and during surgery. Clin Neurosurg 55:1419, 2008

    • Search Google Scholar
    • Export Citation
  • 36

    Sanai N, Berger MS: Operative techniques for gliomas and the value of extent of resection. Neurotherapeutics 6:478486, 2009

  • 37

    Sanai N, Mirzadeh Z, Berger MS: Functional outcome after language mapping for glioma resection. N Engl J Med 358:1827, 2008

  • 38

    Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS: An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 115:38, 2011

    • Search Google Scholar
    • Export Citation
  • 39

    Shorvon SD: The etiologic classification of epilepsy. Epilepsia 52:10521057, 2011

  • 40

    Skirboll SS, Ojemann GA, Berger MS, Lettich E, Winn HR: Functional cortex and subcortical white matter located within gliomas. Neurosurgery 38:678685, 1996

    • Search Google Scholar
    • Export Citation
  • 41

    Tamura Y, Ogawa H, Kapeller C, Prueckl R, Takeuchi F, Anei R, : Passive language mapping combining real-time oscillation analysis with cortico-cortical evoked potentials for awake craniotomy. J Neurosurg 125:15801588, 2016

    • Search Google Scholar
    • Export Citation
  • 42

    Taplin AM, de Pesters A, Brunner P, Hermes D, Dalfino JC, Adamo MA, : Intraoperative mapping of expressive language cortex using passive real-time electrocorticography. Epilepsy Behav Case Rep 5:4651, 2016

    • Search Google Scholar
    • Export Citation
  • 43

    Tatum WO IV, Quinones-Hinojosa A: Onco-epilepsy: more than tumor and seizures. Mayo Clin Proc 93:11811184, 2018

  • 44

    van ’t Klooster MA, van Klink NE, Leijten FS, Zelmann R, Gebbink TA, Gosselaar PH, : Residual fast ripples in the intraoperative corticogram predict epilepsy surgery outcome. Neurology 85:120128, 2015

    • Search Google Scholar
    • Export Citation
  • 45

    Vogel RW: Understanding anodal and cathodal stimulation. The ASNM Monitor. December 1, 2017 (https://www.asnm.org/blogpost/1635804/290597/Understanding-Anodal-and-Cathodal-Stimulation) [Accessed May 8, 2019]

    • Export Citation
  • 46

    von Koch CS, Quinones-Hinojosa A, Gulati M, Lyon R, Peacock WJ, Yingling CD: Clinical outcome in children undergoing tethered cord release utilizing intraoperative neurophysiological monitoring. Pediatr Neurosurg 37:8186, 2002

    • Search Google Scholar
    • Export Citation
  • 47

    Voorhies JM, Cohen-Gadol A: Techniques for placement of grid and strip electrodes for intracranial epilepsy surgery monitoring: pearls and pitfalls. Surg Neurol Int 4:98, 2013

    • Search Google Scholar
    • Export Citation
  • 48

    Walker JA, Quiñones-Hinojosa A, Berger MS: Intraoperative speech mapping in 17 bilingual patients undergoing resection of a mass lesion. Neurosurgery 54:113118, 2004

    • Search Google Scholar
    • Export Citation
  • 49

    Wesseling P, Capper D: WHO 2016 Classification of gliomas. Neuropathol Appl Neurobiol 44:139150, 2018

  • 50

    World Health Organization GWH: Epilepsy Fact Sheet. Geneva: WHO, 2019 (https://www.who.int/news-room/fact-sheets/detail/epilepsy) [Accessed May 9, 2019]

    • Search Google Scholar
    • Export Citation
  • 51

    Wyler AR, Ojemann GA, Lettich E, Ward AA Jr: Subdural strip electrodes for localizing epileptogenic foci. J Neurosurg 60:11951200, 1984

    • Search Google Scholar
    • Export Citation
  • 52

    Yuan Y, Peizhi Z, Xiang W, Yanhui L, Ruofei L, Shu J, : Intraoperative seizures and seizures outcome in patients underwent awake craniotomy. J Neurosurg Sci [epub ahead of print], 2016

    • Search Google Scholar
    • Export Citation

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