Electrocorticography in patients with severe traumatic brain injury

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Abstract

Introduction. The frequency of adverse outcomes in patients with severe traumatic brain injury (TBI) exceeds 25%. Epileptic seizures and vasospasm, in the absence of pathogenetic treatment, cause irreversible brain damage and thus complicate the course of severe TBI. Bedside electroencephalography (EEG) is traditionally used to diagnose these conditions. However, its low spatial resolution when recording from the scalp and a large number of artefacts that make it challenging to analyse the data.

Materials and methods. Electrocorticography (ECoG) monitoring was performed using subdural electrodes implanted in the traumatic brain lesion during TBI surgery in 11 patients during the acute period of severe TBI. All patients were concurrently monitored using scalp EEG with subdermal needle electrodes.

Results. Analysis of scalp recordings showed frequency disturbances and oscillation asymmetry in all patients, while sporadic epileptiform activity and rhythmic and periodic patterns were detected in 18% and 64% of subjects, respectively. Analysis of invasive EEG showed sporadic epileptiform activity in 27% of patients, while rhythmic and periodic patterns were present in 91%. Moreover, epileptiform activity was registered only by the subdural leads in 3 patients. The total percentage of subjects in whom we registered clinical and electrographic signs of convulsive and non-convulsive status epilepticus using EEG and ECoG was 55%. We found indirect EEG signs of slow-spreading cortical depolarization in one patient whose level of consciousness was coma, followed by an electrographic pattern of status epilepticus on ECoG.

Conclusion. ECoG recording, while patients with severe TBI are in the intensive care unit, increases the diagnostic capabilities of this method, allowing electrographic seizures to be recorded more often and more accurately, but also to detect indirect signs of slow-spreading cortical depolarization using standard EEG amplifiers. Electrode implantation during TBI surgery is safe and does not significantly change the surgical approach.

About the authors

Mikhail V. Sinkin

Sklifosofsky Research Institute of Emergency Care, Moscow

Author for correspondence.
Email: platonova@neurology.ru
Russian Federation

Alexander E. Talypov

Sklifosofsky Research Institute of Emergency Care, Moscow

Email: platonova@neurology.ru
Russian Federation

Olga O. Kordonskaya

Sklifosofsky Research Institute of Emergency Care, Moscow

Email: platonova@neurology.ru
Russian Federation

Ilya G. Komoltsev

Institute of Higher Nervous Activity and Neurophysiology, Moscow

Email: platonova@neurology.ru
Russian Federation

Alexander A. Solodov

Sklifosofsky Research Institute of Emergency Care, Moscow

Email: platonova@neurology.ru
Russian Federation

Andrey A. Grin

Sklifosofsky Research Institute of Emergency Care, Moscow

Email: platonova@neurology.ru
Russian Federation

Vladimir V. Krylov

Sklifosofsky Research Institute of Emergency Care, Moscow

Email: platonova@neurology.ru
Russian Federation

References

  1. Traumatic brain injury: time to end the silence. Lancet Neurol 2010; 9: 331. doi: 10.1016/S1474-4422(10)70069-7. PMID: 20298955.
  2. Puras Yu.V., Talypov A.E., Krylov V.V. [Mortality in victims with severe concomitant traumatic brain injury]. Neyrokhirurgiya 2010; 1: 31–39. (In Russ.)
  3. Talypov A.E. [Surgical treatment of severe traumatic brain injury: med. sci. diss.]. Moscow, 2015. 413 p. (In Russ.)
  4. Nepomnyashchiy V.P., Likhterman L.B., Yartsev V.V., Akshulakov S.K. [Epi- demiology of traumatic brain injury and its consequences]. Konovalov A.N., Likhterman L.B., Potapov A.A. (eds.) Klinicheskoye rukovodstvo po cherep- no-mozgovoy travme: in 3 V. Moscow, 1998. V. 1: 129–151. (In Russ.)
  5. Krylov V.V., Konovalov A.N., Dashyan V.G. et al. [State of the neurosurgical service of the Russian Federation]. Voprosy neyrokhirurgii im. N.N. Burdenko 2017; 81(1): 5–12. doi: 10.17116/neiro20178075-12. PMID: 28291209. (In Russ.)
  6. Vespa P.M., McArthur D.L., Xu Y. et al. Nonconvulsive seizures after traumatic brain injury are associated with hippocampal atrophy. Neurology 2010; 75: 792–798. doi: 10.1212/WNL.0b013e3181f07334. PMID: 20805525.
  7. Neligan A., Shorvon S.D. Frequency and prognosis of convulsive status epi- lepticus of different causes: a systematic review. Arch Neurol 2010; 67: 931–940. doi: 10.1001/archneurol.2010.169. PMID: 20697043.
  8. Alroughani R., Javidan M., Qasem A., Alotaibi N. Non-convulsive status epilepticus; the rate of occurrence in a general hospital. Seizure 2009; 18: 38–42. doi: 10.1016/j.seizure.2008.06.013. PMID: 18755608.
  9. Vespa P.M., Nuwer M.R., Nenov V. et al. Increased incidence and impact of nonconvulsive and convulsive seizures after traumatic brain injury as detected by continuous electroencephalographic monitoring. J Neurosurg 1999; 91: 750– 760. doi: 10.3171/jns.1999.91.5.0750. PMID: 10541231.
  10. Sokolova E.Yu., Savin I.A., Lubnin A.Yu. et al. [Non-convulsive status ep- ilepticus as a cause of unconsciousness]. Vestnik intensivnoy terapii 2014; (2): 18–25. (In Russ.)
  11. Kaimovskii I.L., Lebedeva A.V., Mutaeva R.S. et al. [Risk factors for post-traumatic epilepsy in adults]. Zh Nevrol Psikhiatr im S S Korsakova. 2013; 113(4 Pt 2): 25–28. PMID: 23739451.
  12. Ramantani G., Maillard L., Koessler L. Correlation of invasive EEG and scalp EEG. Seizure 2016; 41: 196–200. doi: 10.1016/j.seizure.2016.05.018. PMID: 27324839.
  13. Dreier J.P., Fabricius M., Ayata C. et al. Recording, analysis, and interpretation of spreading depolarizations in neurointensive care: review and recommendations of the COSBID research group. J Cereb Blood Flow Metab 2017; 37: 1595–1625. doi: 10.1177/0271678X16654496. PMID: 27317657.
  14. Munari C., Hoffmann D., Francione S. et al. Stereo-electroencephalography methodology: advantages and limits. Acta Neurol Scand Suppl 1994; 152: 56–67. doi: 10.1111/j.1600-0404.1994.tb05188.x. PMID: 8209659.
  15. Waziri A., Claassen J., Stuart R.M. et al. Intracortical electroencephalography in acute brain injury. Ann Neurol 2009; 66: 366–377. DOI: 10.1002/ ana.21721. PMID: 19798724.
  16. Luders H.O., Noachtar S. Atlas and classification of electroencephalography. Philadelphia, 2000.
  17. Hirsch L., LaRoche S.M., Gaspard N. et al. American Clinical Neurophysiology Society’s standardized critical care EEG terminology: 2012 version. J Clin Neurophysiology 2013; 30: 1–27. doi: 10.1097/WNP.0b013e3182784729. PMID: 23377439.
  18. Sinkin M.V., Krylov V.V. [Rhytmic and periodic EEG patterns. Classification and clinical significance]. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova 2018; 118(10): 9–20. doi: 10.17116/jnevro20181181029. PMID: 30698539. (In Russ.)
  19. Beniczky S., Hirsch L.J., Kaplan P.W. et al. Unified EEG terminology and criteria for nonconvulsive status epilepticus. Epilepsia 2013; 54: 28–29. doi: 10.1111/epi.12270. PMID: 24001066.
  20. Struck A.F., Ustun B., Ruiz A.R. et al. Association of an electroencephalography-based risk score with seizure probability in hospitalized patients. JAMA Neurol 2017; 74: 1419–1424. doi: 10.1001/jamaneurol.2017.2459. PMID: 29052706.
  21. Hill C.E., Blank L.J., Thibault D. et al. Continuous EEG is associated with favorable hospitalization outcomes for critically ill patients. Neurology 2019; 92: e9–e18. doi: 10.1212/WNL.0000000000006689. PMID: 30504428.
  22. Kramer D.R., Fujii T., Ohiorhenuan I., Liu C.Y. Cortical spreading depolarization: pathophysiology, implications, and future directions. J Clin Neurosci 2016; 24: 22–27. doi: 10.1016/j.jocn.2015.08.004. PMID: 26461911.
  23. Gavvala J., Abend N., LaRoche S. et al. Continuous EEG monitoring: a survey of neurophysiologists and neurointensivists. Epilepsia 2014; 55: 1864–1871. doi: 10.1111/epi.12809. PMID: 25266728.
  24. Sharova E.V., Chelyapina M.V., Korobkova E.V. et al. [EEG correlates of consciousness recovery after severe traumatic brain injury]. Voprosy neyrokhirur- gii im. N.N. Burdenko 2014; 78(1): 14–25. (In Russ.)
  25. Tao J.X., Ray A., Hawes-Ebersole S., Ebersole J.S. Intracranial EEG sub- strates of scalp EEG interictal spikes. Epilepsia 2005; 46: 669–676. doi: 10.1111/j.1528-1167.2005.11404.x. PMID: 15857432.
  26. Olejniczak P. Neurophysiologic basis of EEG. J Clin Neurophysiol 2006; 23:186–189. doi: 10.1097/01.wnp.0000220079.61973.6c. PMID: 16751718.
  27. Krylov V.V., Gekht A.B., Trifonov I.S. et al. [Surgical treatment of patients with magnetic resonance-negative drug-resistant forms of epilepsy]. Nevrologicheskiy zhurnal 2016; 21(4): 213–218. doi: 10.18821/1560-9545-2016-21-4- 213-218. (In Russ.)
  28. Krylov V.V., Talypov A.E., Levchenko O.V. et al. [Surgery for severe traumatic brain injury]. Moscow, 2019. (In Russ.)
  29. Vespa P.M., McArthur D.L., Xu Y. et al. Nonconvulsive seizures after traumatic brain injury are associated with hippocampal atrophy. Neurology 2010; 75: 792–798. doi: 10.1212/WNL.0b013e3181f07334. PMID: 20805525.
  30. Vespa P.M., Miller C., McArthur D. et al. Nonconvulsive electrographic seizures after traumatic brain injury result in a delayed, prolonged increase in intra- cranial pressure and metabolic crisis. Crit Care Medicine 2007; 35: 2830–2836. doi: 10.1097/01.CCM.0000295667.66853.BC. PMID: 18074483.
  31. Friedman D., Claassen J., Hirsch L.J. Continuous electroencephalogram monitoring in the intensive care unit. Anesth Analogy 2009; 109: 506–523. doi: 10.1213/ane.0b013e3181a9d8b5. PMID: 19608827.
  32. Alroughani R., Javidan M., Qasem A., Alotaibi N. Non-convulsive status epilepticus; the rate of occurrence in a general hospital. Seizure 2009; 18: 38–42. doi: 10.1016/j.seizure.2008.06.013. PMID: 18755608.
  33. Westhall E., Rosén I., Rossetti A.O. et al. Interrater variability of EEG interpretation in comatose cardiac arrest patients. Clin Neurophysiol 2015; 126: 2397–2404. doi: 10.1016/j.clinph.2015.03.017. PMID: 25934481.
  34. Rossetti A.O., Hirsch L.J., Drislane F.W. Nonconvulsive seizures and nonconvulsive status epilepticus in the Neuro ICU should or should not be treated aggressively: a debate. Clin Neurophysiol Pract 2019; 4: 170–177. DOI: 10.1016/j. cnp.2019.07.001. PMID: 31886441.
  35. Dreier J.P., Fabricius M., Ayata C. et al. Recording, analysis, and interpretation of spreading depolarizations in neurointensive care: review and recommendations of the COSBID research group. J Cereb Blood Flow Metab 2017; 37: 1595–1625. doi: 10.1177/0271678X16654496. PMID: 27317657.
  36. Dreier J.P. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 2011; 17: 439–447. doi: 10.1038/nm.2333. PMID: 21475241.
  37. Kramer D.R., Fujii T., Ohiorhenuan I., Liu C.Y. Interplay between cortical spreading depolarization and seizures. Stereotact Funct Neurosurg 2017; 95: 1–5. doi: 10.1159/000452841. PMID: 28088802.
  38. Fabricius M., Fuhr S., Willumsen L. et al. Association of seizures with cortical spreading depression and peri-infarct depolarisations in the acutely injured human brain. Clin Neurophysiol 2008; 119: 1973–1984. DOI: 10.1016/j. clinph.2008.05.025. PMID: 18621582.

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Copyright (c) 2020 Sinkin M.V., Talypov A.E., Kordonskaya O.O., Komoltsev I.G., Solodov A.A., Grin A.A., Krylov V.V.

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