Skip to main content

Advertisement

SpringerLink
Log in

Electroencephalogram in the intensive care unit: a focused look at acute brain injury

  • Narrative Review
  • Published:
Intensive Care Medicine Aims and scope Submit manuscript

Abstract

Over the past decades, electroencephalography (EEG) has become a widely applied and highly sophisticated brain monitoring tool in a variety of intensive care unit (ICU) settings. The most common indication for EEG monitoring currently is the management of refractory status epilepticus. In addition, a number of studies have associated frequent seizures, including nonconvulsive status epilepticus (NCSE), with worsening secondary brain injury and with worse outcomes. With the widespread utilization of EEG (spot and continuous EEG), rhythmic and periodic patterns that do not fulfill strict seizure criteria have been identified, epidemiologically quantified, and linked to pathophysiological events across a wide spectrum of critical and acute illnesses, including acute brain injury. Increasingly, EEG is not just qualitatively described, but also quantitatively analyzed together with other modalities to generate innovative measurements with possible clinical relevance. In this review, we discuss the current knowledge and emerging applications of EEG in the ICU, including seizure detection, ischemia monitoring, detection of cortical spreading depolarizations, assessment of consciousness and prognostication. We also review some technical aspects and challenges of using EEG in the ICU including the logistics of setting up ICU EEG monitoring in resource-limited settings.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  1. Cohen MX (2017) Where does EEG come from and what does it mean? Trends Neurosci 40(4):208–218. https://doi.org/10.1016/j.tins.2017.02.004

    Article  CAS  PubMed  Google Scholar 

  2. Herman ST, Abend NS, Bleck TP, Chapman KE, Drislane FW, Emerson RG et al (2015) Consensus statement on continuous EEG in critically ill adults and children, part I: indications. J Clin Neurophysiol 32(2):87–95. https://doi.org/10.1097/wnp.0000000000000166

    Article  PubMed  PubMed Central  Google Scholar 

  3. Herman ST, Abend NS, Bleck TP, Chapman KE, Drislane FW, Emerson RG et al (2015) Consensus statement on continuous EEG in critically ill adults and children, part II: personnel, technical specifications, and clinical practice. J Clin Neurophysiol 32(2):96–108. https://doi.org/10.1097/wnp.0000000000000165

    Article  PubMed  PubMed Central  Google Scholar 

  4. De Deyne C, Struys M, Decruyenaere J, Creupelandt J, Hoste E, Colardyn F (1998) Use of continuous bispectral EEG monitoring to assess depth of sedation in ICU patients. Intensive Care Med 24(12):1294–1298. https://doi.org/10.1097/WNP.0000000000000165

    Article  PubMed  Google Scholar 

  5. Simmons LE, Riker RR, Prato BS, Fraser GL (1999) Assessing sedation during intensive care unit mechanical ventilation with the Bispectral Index and the Sedation-Agitation Scale. Crit Care Med 28(8):1499–1504. https://doi.org/10.1097/00003246-199908000-00016

    Article  Google Scholar 

  6. Hajat Z, Ahmad N, Andrzejowski J (2017) The role and limitations of EEG-based depth of anaesthesia monitoring in theatres and intensive care. Anaesthesia 72(Suppl 1):38–47. https://doi.org/10.1111/anae.13739

    Article  PubMed  Google Scholar 

  7. Riker RR, Fraser GL, Simmons LE, Wilkins ML (2001) Validating the Sedation-Agitation Scale with the Bispectral Index and Visual Analog Scale in adult ICU patients after cardiac surgery. Intensive Care Med 27(5):853–858. https://doi.org/10.1007/s001340100912

    Article  CAS  PubMed  Google Scholar 

  8. Vivien B, Di Maria S, Ouattara A, Langeron O, Coriat P, Riou B (2003) Overestimation of Bispectral Index in sedated intensive care unit patients revealed by administration of muscle relaxant. Anesthesiology 99(1):9–17. https://doi.org/10.1097/00000542-200307000-00006

    Article  PubMed  Google Scholar 

  9. Hirsch LJ, Fong MWK, Leitinger M, LaRoche SM, Beniczky S, Abend NS (2021) American Clinical Neurophysiology Society’s standardized critical care EEG terminology: 2021 version. J Clin Neurophysiol 38(1):1–29. https://doi.org/10.1097/WNP.0000000000000806

    Article  PubMed  PubMed Central  Google Scholar 

  10. Kane N, Acharya J, Benickzy S, Caboclo L, Finnigan S, Kaplan PW et al (2017) A revised glossary of terms most commonly used by clinical electroencephalographers and updated proposal for the report format of the EEG findings. Revision 2017. Clin Neurophysiol Pract 2:170–185. https://doi.org/10.1016/j.cnp.2017.07.002

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hirsch LJ, LaRoche SM, Gaspard N, Gerard E, Svoronos A, Herman ST et al (2013) American Clinical Neurophysiology Society’s standardized critical care EEG terminology: 2012 version. J Clin Neurophysiol 30(1):1–27. https://doi.org/10.1097/WNP.0b013e3182784729

    Article  CAS  PubMed  Google Scholar 

  12. Claassen J, Doyle K, Matory A, Couch C, Burger KM, Velazquez A et al (2019) Detection of brain activation in unresponsive patients with acute brain injury. N Engl J Med 380(26):2497–2505. https://doi.org/10.1056/NEJMoa1812757

    Article  PubMed  Google Scholar 

  13. Egbebike J, Shen Q, Doyle K, Der-Nigoghossian CA, Panicker L, Gonzales IJ et al (2022) Cognitive-motor dissociation and time to functional recovery in patients with acute brain injury in the USA: a prospective observational cohort study. Lancet Neurol 21(8):704–713. https://doi.org/10.1016/S1474-4422(22)00212-5

    Article  PubMed  Google Scholar 

  14. Rosenthal ES, Biswal S, Zafar SF, O’Connor KL, Bechek S, Shenoy AV et al (2018) Continuous electroencephalography predicts delayed cerebral ischemia after subarachnoid hemorrhage: a prospective study of diagnostic accuracy. Ann Neurol 83(5):958–969. https://doi.org/10.1002/ana.25232

    Article  PubMed  PubMed Central  Google Scholar 

  15. Hartings JA, Bullock MR, Okonkwo DO, Murray LS, Murray GD, Fabricius M et al (2011) Spreading depolarisations and outcome after traumatic brain injury: a prospective observational study. Lancet Neurol 10(12):1058–1064. https://doi.org/10.1016/S1474-4422(11)70243-5

    Article  PubMed  Google Scholar 

  16. Hartings JA, Andaluz N, Bullock MR, Hinzman JM, Mathern B, Pahl C et al (2020) Prognostic value of spreading depolarizations in patients with severe traumatic brain injury. JAMA Neurol 77(4):489–499. https://doi.org/10.1001/jamaneurol.2019.4476

    Article  PubMed  Google Scholar 

  17. Appavu B, Riviello JJ (2018) Electroencephalographic patterns in neurocritical care: pathologic contributors or epiphenomena? Neurocrit Care 29(1):9–19. https://doi.org/10.1007/s12028-017-0424-5

    Article  PubMed  Google Scholar 

  18. Payne ET, Zhao XY, Frndova H, McBain K, Sharma R, Hutchison JS et al (2014) Seizure burden is independently associated with short term outcome in critically ill children. Brain 137(Pt 5):1429–1438. https://doi.org/10.1093/brain/awu042

    Article  PubMed  PubMed Central  Google Scholar 

  19. Leitinger M, Beniczky S, Rohracher A, Gardella E, Kalss G, Qerama E et al (2015) Salzburg consensus criteria for non-convulsive status epilepticus–approach to clinical application. Epilepsy Behav 49:158–163. https://doi.org/10.1016/j.yebeh.2015.05.007

    Article  CAS  PubMed  Google Scholar 

  20. Lalgudi Ganesan S, Hahn CD (2022) Spectrograms for seizure detection in critically ill children. J Clin Neurophysiol 39(3):195–206. https://doi.org/10.1097/WNP.0000000000000868

    Article  PubMed  Google Scholar 

  21. Zafar SF, Amorim E, Williamsom CA, Jing J, Gilmore EJ, Haider GEJ et al (2020) A standardized nomenclature for spectrogram EEG patterns: inter-rater agreement and correspondence with common intensive care unit EEG patterns. Clin Neurophysiol 131(9):2298–2306. https://doi.org/10.1016/j.clinph.2020.05.032

    Article  PubMed  PubMed Central  Google Scholar 

  22. Hellström-Westas L (2018) Amplitude-integrated electroencephalography for seizure detection in newborn infants. Semin Fetal Neonatal Med 23(3):175–182. https://doi.org/10.1016/j.siny.2018.02.003

    Article  PubMed  Google Scholar 

  23. Alkachroum A, Lalgudi Ganesan S, Koren JP, Kromm J, Massad N, Reyes RA et al (2022) Quantitative EEG-based seizure estimation in super-refractory status epilepticus. Neurocrit Care 36(3):897–904. https://doi.org/10.1007/s12028-021-01395-x

    Article  Google Scholar 

  24. Haider HA, Esteller R, Hahn CD, Westover MB, Halford JJ, Lee JW et al (2016) Sensitivity of quantitative EEG for seizure identification in the intensive care unit. Neurology 87(9):935–944. https://doi.org/10.1212/WNL.0000000000003034

    Article  PubMed  PubMed Central  Google Scholar 

  25. Kaleem S, Kang JH, Sahgal A, Hernandez CE, Sinha SR, Swisher CB (2021) Electrographic seizure detection by neuroscience intensive care unit nurses via bedside real-time quantitative EEG. Neurol Clin Pract 11(5):420–428. https://doi.org/10.1212/CPJ.0000000000001107

    Article  PubMed  Google Scholar 

  26. Kurtz P, Gaspard N, Wahl AS, Bauer RM, Hirsch LJ, Wunsch H et al (2014) Continuous electroencephalography in a surgical intensive care unit. Intensive Care Med 40(2):228–234. https://doi.org/10.1007/s00134-013-3149-8

    Article  PubMed  Google Scholar 

  27. Oddo M, Carrera E, Claassen J, Mayer SA, Hirsch LJ (2009) Continuous electroencephalography in the medical intensive care unit. Crit Care Med 37(6):2051–2056. https://doi.org/10.1097/CCM.0b013e3181a00604

    Article  PubMed  Google Scholar 

  28. Kharoshankaya L, Stevenson NJ, Livingstone V, Murray DM, Murphy BP, Ahearne C et al (2016) Seizure burden and neurodevelopmental outcome in neonates with hypoxic-ischemic encephalopathy. Dev Med Child Neurol 58(12):1242–1248. https://doi.org/10.1111/dmcn.13215

    Article  PubMed  PubMed Central  Google Scholar 

  29. Amorim E, McGraw CM, Westover MB (2020) A theoretical paradigm for evaluating risk-benefit of status epilepticus treatment. J Clin Neurophysiol 37(5):385–392. https://doi.org/10.1097/WNP.0000000000000753

    Article  PubMed  PubMed Central  Google Scholar 

  30. Williams JA, Bede P, Doherty CP (2017) An exploration of the spectrum of peri-ictal MRI change; a comprehensive literature review. Seizure 50:19–32. https://doi.org/10.1016/j.seizure.2017.05.005

    Article  PubMed  Google Scholar 

  31. Ergün EL, Salanci BV, Erbaş B, Saygi S (2006) SPECT in periodic lateralized epileptiform discharges (PLEDs): a case report on PLEDs. Ann Nucl Med 20(3):227–231. https://doi.org/10.1007/BF03027435

    Article  PubMed  Google Scholar 

  32. Bozkurt MF, Saygi S, Erbas B (2002) SPECT in a patient with postictal PLEDs: is hyperperfusion evidence of electrical seizure? Clin Electroencephalogr 33(4):171–173. https://doi.org/10.1177/155005940203300407

    Article  PubMed  Google Scholar 

  33. Struck AF, Westover MB, Hall LT, Deck GM, Cole AJ et al (2016) Metabolic correlates of the ictal-interictal continuum: FDG-PET during continuous EEG. Neurocrit Care 24(3):324–331. https://doi.org/10.1007/s12028-016-0245-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Claassen J, Perotte A, Albers D, Kleinberg S, Schmidt JM, Tu B et al (2013) Nonconvulsive seizures after subarachnoid hemorrhage: multimodal detection and outcomes. Ann Neurol 74(1):53–64. https://doi.org/10.1002/ana.23859

    Article  PubMed  PubMed Central  Google Scholar 

  35. Vespa P, Tubi M, Claassen J, Buitrago-Blanco M, McArthur D, Velazquez AG et al (2016) Metabolic crisis occurs with seizures and periodic discharges after brain trauma. Ann Neurol. https://doi.org/10.1002/ana.24606

    Article  PubMed  Google Scholar 

  36. Witch J, Frey HP, Schmidt JM, Velazquez A, Falo CM, Reznik M et al (2017) Electroencephalographic periodic discharges and frequency-dependent brain tissue hypoxia in acute brain injury. JAMA Neurol 74(3):301–309. https://doi.org/10.1001/jamaneurol.2016.5325

    Article  Google Scholar 

  37. Schnakers C, Vanhaudenhuyse A, Giacino J, Ventura M, Boly M, Majerus S et al (2009) Diagnostic accuracy of the vegetative and minimally conscious state: clinical consensus versus standardized neurobehavioral assessment. BMC Neurol. https://doi.org/10.1186/1471-2377-9-35

    Article  PubMed  PubMed Central  Google Scholar 

  38. Wannez S, Vanhaudenhuyse A, Laureys S, Brédart S (2017) Mirror efficiency in the assessment of visual pursuit in patients in minimally conscious state. Brain Inj 31(11):1429–1435. https://doi.org/10.1080/02699052.2017.1376755

    Article  PubMed  Google Scholar 

  39. Alkhachroum A, Bustillo AJ, Asdaghi N, Marulanda-Londono E, Gutierrez CM, Samano D et al (2021) Withdrawal of life-sustaining treatment mediates mortality in patients with intracerebral hemorrhage with impaired consciousness. Stroke 52(12):3891–3898. https://doi.org/10.1161/STROKEAHA.121.035233

    Article  CAS  PubMed  Google Scholar 

  40. Alkhachroum A, Bustillo AJ, Asdaghi N, Ying H, Marulanda-Londono E, Gutierrez CM et al (2022) Association of acute alteration of consciousness in patients with acute ischemic stroke with outcomes and early withdrawal of care. Neurology 98(14):e1470–e1478. https://doi.org/10.1212/WNL.0000000000200018

    Article  CAS  PubMed  Google Scholar 

  41. Hockaday JM, Potts F, Epstein E, Bonazzi A, Schwab RS (1965) Electroencephalographic changes in acute cerebral anoxia from cardiac or respiratory arrest. Electroencephalogr Clin Neurophysiol 18:575–586. https://doi.org/10.1016/0013-4694(65)90075-1

    Article  CAS  PubMed  Google Scholar 

  42. Synek VM (1988) Prognostically important EEG coma patterns in diffuse anoxic and traumatic encephalopathies in adults. J Clin Neurophysiol 5(2):161–174. https://doi.org/10.1097/00004691-198804000-00003

    Article  CAS  PubMed  Google Scholar 

  43. Young GB, McLachlan RS, Kreeft JH, Demelo JD (1997) An electroencephalographic classification for coma. Can J Neurol Sci 24(4):320–325. https://doi.org/10.1017/s0317167100032996

    Article  CAS  PubMed  Google Scholar 

  44. Comanducci A, Boly M, Claassen J, De Lucia M, Gibson RM, Juan E et al (2020) Clinical and advanced neurophysiology in the prognostic and diagnostic evaluation of disorders of consciousness: review of an IFCN-endorsed expert group. Clin Neurophysiol 131(11):2736–2765. https://doi.org/10.1016/j.clinph.2020.07.015

    Article  CAS  PubMed  Google Scholar 

  45. Sivaraju A, Gilmore EJ, Wira CR, Stevens A, Rampal N, Moeller JJ et al (2015) Prognostication of post-cardiac arrest coma: early clinical and electroencephalographic predictors of outcome. Intensive Care Med 41(7):1264–1272. https://doi.org/10.1007/s00134-015-3834-x

    Article  PubMed  Google Scholar 

  46. Sutter R, Kaplan PW (2013) Clinical and electroencephalographic correlates of acute encephalopathy. J Clin Neurophysiol 30(5):443–453. https://doi.org/10.1097/WNP.0b013e3182a73bc2

    Article  PubMed  Google Scholar 

  47. Foreman B, Mahulikar A, Tadi P, Claassen J, Szaflarski J, Halford JJ et al (2016) Generalized periodic discharges and ‘triphasic waves’: a blinded evaluation of inter-rater agreement and clinical significance. Clin Neurophysiol 127(2):1073–1080. https://doi.org/10.1016/j.clinph.2015.07.018

    Article  PubMed  Google Scholar 

  48. Alkhachroum AM, Al-Abri H, Sachdeva A, Maturu S, Waldron J, Wang H et al (2018) Generalized periodic discharges with and without triphasic morphology. J Clin Neurophysiol 35(2):144–150. https://doi.org/10.1097/WNP.0000000000000441

    Article  PubMed  Google Scholar 

  49. O’Rourke D, Chen PM, Gaspard N, Foreman B, McClain L, Karakis I et al (2016) Response rates to anticonvulsant trials in patients with triphasic-wave EEG patterns of uncertain significance. Neurocrit Care 24(2):233–239. https://doi.org/10.1007/s12028-015-0151-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Dhakar MB, Sheikh ZB, Desai M, Dsai RA, Sternberg EJ, Popescu C et al (2022) Developing a standardized approach to grading the level of brain dysfunction on EEG. J Clin Neurophysiol. https://doi.org/10.1097/WNP.0000000000000919

    Article  PubMed  Google Scholar 

  51. Grigg-Damberger M, Hussein O, Kulik T (2022) Sleep spindles and K-complexes are favorable prognostic biomarkers in critically ill patients. J Clin Neurophysiol 39(5):372–382. https://doi.org/10.1097/WNP.0000000000000830

    Article  PubMed  Google Scholar 

  52. Estraneo A, Loreto V, Guarino I, Boemia V, Paone G, Moretta P et al (2016) Standard EEG in diagnostic process of prolonged disorders of consciousness. Clin Neurophysiol 127(6):2379–2385. https://doi.org/10.1016/j.clinph.2016.03.021

    Article  PubMed  Google Scholar 

  53. Ruijter B, Tjepkema-Cloostermans MC, Tromp SC, van den Bergh WM, Foudraine NA, Kornips FHM et al (2019) Early electroencephalography for outcome prediction of postanoxic coma: a prospective cohort study. Ann Neurol 86(2):203–214. https://doi.org/10.1002/ana.25518

    Article  PubMed  PubMed Central  Google Scholar 

  54. Ruijter BJ, Hofmeijer J, Tjepkema-Cloostermans MC, van Putten MJAM (2018) The prognostic value of discontinuous EEG patterns in postanoxic coma. Clin Neurophysiol 129(8):1534–1543. https://doi.org/10.1016/j.clinph.2018.04.745

    Article  PubMed  Google Scholar 

  55. Hofmeijer J, Beernink TM, Bosch FH, Beishuizen A, Tjepkema-Cloostermans MC, van Putten MJ (2015) Early EEG contributes to multimodal outcome prediction of postanoxic coma. Neurology 85(2):137–143. https://doi.org/10.1212/WNL.000000000000174

    Article  PubMed  PubMed Central  Google Scholar 

  56. Scollo-Lavizzari G, Bassetti C (1987) Prognostic value of EEG in post-anoxic coma after cardiac arrest. Eur Neurol 26(3):161–170. https://doi.org/10.1159/000116329

    Article  CAS  PubMed  Google Scholar 

  57. Rossetti AO, Tovar Quiroga DF, Juan E, Novy J, White RD, Ben-Hamouda N et al (2017) Electroencephalography predicts poor and good outcomes after cardiac arrest: a two-center study. Crit Care Med 45(7):e674–e682. https://doi.org/10.1097/CCM.0000000000002337

    Article  PubMed  Google Scholar 

  58. Caroyer S, Depondt C, Rikir E, Mavroudakis N, Peluso L, Taccone FS et al (2021) Assessment of a standardized EEG reactivity protocol after cardiac arrest. Clin Neurophysiol 132(7):1687–1693. https://doi.org/10.1016/j.clinph.2021.03.047

    Article  PubMed  Google Scholar 

  59. Admiraal MM, van Rootselaar AF, Horn J (2017) Electroencephalographic reactivity testing in unconscious patients: a systematic review of methods and definitions. Eur J Neurol 24(2):245–254. https://doi.org/10.1111/ene.13219

    Article  CAS  PubMed  Google Scholar 

  60. Datta S, Hart GK, Opdam H, Gutteridge G, Archer J (2009) Post-hypoxic myoclonic status: the prognosis is not always hopeless. Crit Care Resusc 11(1):39–41

    PubMed  Google Scholar 

  61. Elmer J, Rittenberger JC, Faro J, Molyneaux BJ, Popescu A, Callaway CW et al (2016) Clinically distinct electroencephalographic phenotypes of early myoclonus after cardiac arrest. Ann Neurol 80(2):175–184. https://doi.org/10.1002/ana.24697

    Article  PubMed  PubMed Central  Google Scholar 

  62. Sandroni C, D’Arrigo S, Cacciola S, Hoedemaekers CW, Westhall E, Kamps MJA et al (2022) Prediction of good neurological outcome in comatose survivors of cardiac arrest: a systematic review. Intensive Care Med 48(4):389–413. https://doi.org/10.1007/s00134-022-06618-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Nolan JP, Sandroni C, Böttiger BW, Cariou A, Cronberg T, Friberg H et al (2021) European Resuscitation Council and European Society of Intensive Care Medicine guidelines 2021: post-resuscitation care. Intensive Care Med 47(4):369–421

    Article  Google Scholar 

  64. Beretta S, Coppo A, Bianchi E, Zanchi C, Carone D, Stabile A et al (2018) Neurologic outcome of postanoxic refractory status epilepticus after aggressive treatment. Neurology 91(23):e2153–e2162. https://doi.org/10.1212/WNL.0000000000006615

    Article  PubMed  Google Scholar 

  65. Snider SB, Fischer D, McKeown ME, Cohen AL, Schaper FLWVJ, Amorim E et al (2022) Regional distribution of brain injury after cardiac arrest: clinical and electrographic correlates. Neurology 98(12):e1238–e1247. https://doi.org/10.1212/WNL.0000000000013301

    Article  PubMed  Google Scholar 

  66. Stecker MM, Cheung AT, Pochettino A, Kent GP, Patterson T, Weiss SJ et al (2001) Deep hypothermic circulatory arrest: I. Effects of cooling on electroencephalogram and evoked potentials. Ann Thorac Surg 71(1):14–21. https://doi.org/10.1016/s0003-4975(00)01592-7

    Article  CAS  PubMed  Google Scholar 

  67. Oddo M, Rossetti AO (2001) Deep hypothermic circulatory arrest: I. Effects of cooling on electroencephalogram and evoked potentials. Crit Care Med 42(6):1340–1347. https://doi.org/10.1097/CCM.0000000000000211

    Article  Google Scholar 

  68. Westhall E, Rosen I, Rundgrèn M, Bro-Jeppesen J, Kjaergaard J, Hassager C et al (2018) Time to epileptiform activity and EEG background recovery are independent predictors after cardiac arrest. Clin Neurophysiol 129(8):1660–1668. https://doi.org/10.1016/j.clinph.2018.05.016

    Article  CAS  PubMed  Google Scholar 

  69. Dhakar MB, Sivaraju A, Maciel CB, Youn TS, Gaspard N, Greer DM (2018) Electro-clinical characteristics and prognostic significance of post anoxic myoclonus. Resuscitation 131:114–120. https://doi.org/10.1016/j.resuscitation.2018.06.030

    Article  PubMed  Google Scholar 

  70. Hersdorffer DC, Benn EK, Cascino GD, Hauser WA (2009) Is a first acute symptomatic seizure epilepsy? Mortality and risk for recurrent seizure. Epilepsia 50(5):1102–1108. https://doi.org/10.1111/j.1528-1167.2008.01945.x

    Article  Google Scholar 

  71. Claassen J, Hirsch LJ, Frontera JA, Fernadez A, Schmidt M, Kapinos G et al (2006) Prognostic significance of continuous EEG monitoring in patients with poor-grade subarachnoid hemorrhage. Neurocrit Care 4(2):103–112. https://doi.org/10.1385/NCC:4:2:103

    Article  PubMed  Google Scholar 

  72. Vespa PM, Miller C, McArthur D, Eliseo M, Etchepare M, Hirt D et al (2007) Nonconvulsive electrographic seizures after traumatic brain injury result in a delayed, prolonged increase in intracranial pressure and metabolic crisis. Crit Care Med 35(12):2830–2836. https://doi.org/10.1385/NCC:4:2:103

    Article  PubMed  PubMed Central  Google Scholar 

  73. Gütling E, Gonser A, Imhof HG, Landis T (1995) EEG reactivity in the prognosis of severe head injury. Neurology 45(5):915–918. https://doi.org/10.1212/wnl.45.5.915

    Article  PubMed  Google Scholar 

  74. Kaplan PW (2004) The EEG in metabolic encephalopathy and coma. J Clin Neurophysiol 21(5):307–318

    PubMed  Google Scholar 

  75. Alkhachroum A, Eliseyev A, Der-Nigoghossian CA, Rubinos C, Kromm JA, Matthews E et al (2020) EEG to detect early recovery of consciousness in amantadine-treated acute brain injury patients. J Neurol Neurosurg Psychiatry 91(6):675–676. https://doi.org/10.1136/jnnp-2019-322645

    Article  PubMed  Google Scholar 

  76. Forgacs PB, Frey HP, Velazquez A, Thompson S, Brodie D, Moitra V et al (2017) Dynamic regimes of neocortical activity linked to corticothalamic integrity correlate with outcomes in acute anoxic brain injury after cardiac arrest. Ann Clin Transl Neurol 4(2):119–129. https://doi.org/10.1002/acn3.385

    Article  PubMed  PubMed Central  Google Scholar 

  77. Forgacs PB, Allen BB, Wu X, Gerber LM, Boddu S, Fakhar M et al (2022) Corticothalamic connectivity in aneurysmal subarachnoid hemorrhage: relationship with disordered consciousness and clinical outcomes. Neurocrit Care 36(3):760–771. https://doi.org/10.1007/s12028-021-01354-6

    Article  PubMed  Google Scholar 

  78. Sekar K, Schiff ND, Labar D, Forgacs PB (2019) Spectral content of electroencephalographic burst-suppression patterns may reflect neuronal recovery in comatose post-cardiac arrest patients. J Clin Neurophysiol 36(2):119–126. https://doi.org/10.1097/WNP.0000000000000536

    Article  PubMed  PubMed Central  Google Scholar 

  79. Bauerschmidt A, Eliseyev A, Doyle KW, Velasquez A, Egbebike J, Chiu W et al (2021) Predicting early recovery of consciousness after cardiac arrest supported by quantitative electroencephalography. Resuscitation 165:130–137. https://doi.org/10.1016/j.resuscitation.2021.06.008

    Article  PubMed  Google Scholar 

  80. Sitt JD, King JR, El Karoui I, Rohaut B, Faugeras F, Gramfort A et al (2014) Large scale screening of neural signatures of consciousness in patients in a vegetative or minimally conscious state. Brain 137(8):2258–2270. https://doi.org/10.1093/brain/awu141

    Article  PubMed  PubMed Central  Google Scholar 

  81. Claassen J (2020) Coma science: intensive care as the new frontier. Intensive Care Med 46(1):97–101. https://doi.org/10.1007/s00134-019-05820-w

    Article  PubMed  Google Scholar 

  82. Engemann DA, Raimondo F, King JR, Rohaut B, Louppe G, Faugeras F et al (2018) Robust EEG-based cross-site and cross-protocol classification of states of consciousness. Brain 141(11):3179–3192. https://doi.org/10.1093/brain/awy251

    Article  PubMed  Google Scholar 

  83. Edlow BL, Chatelle C, Spencer CA, Chu CJ, Bodien YG, O’Connor KL et al (2017) Early detection of consciousness in patients with acute severe traumatic brain injury. Brain 140(9):2399–2414. https://doi.org/10.1093/brain/awx176

    Article  PubMed  PubMed Central  Google Scholar 

  84. Schiff ND (2015) Cognitive motor dissociation following severe brain injuries. JAMA Neurol 72(12):1413–1415. https://doi.org/10.1001/jamaneurol.2015.2899

    Article  PubMed  Google Scholar 

  85. Curley WH, Forgacs PB, Voss HU, Conte MM, Schiff ND (2018) Characterization of EEG signals revealing covert cognition in the injured brain. Brain 141(5):1404–1421. https://doi.org/10.1093/brain/awy070

    Article  PubMed  PubMed Central  Google Scholar 

  86. Owen AM, Coleman MR, Boly M, Davis MH, Laureys S, Pickard JD (2006) Detecting awareness in the vegetative state. Science 313(5792):1402. https://doi.org/10.1126/science.1130197

    Article  CAS  PubMed  Google Scholar 

  87. Panchal AR, Bartos JA, Cabańas JG, Donnino MW, Drennan IR, Hirsch KG et al (2020) Part 3: adult basic and advanced life support: 2020 American Heart Association guidelines for cardiopulmonary resuscitation and emergency cardiovascular care. Circulation 142(16_Suppl_2):S366–S468. https://doi.org/10.1161/CIR.0000000000000916

    Article  PubMed  Google Scholar 

  88. Sandroni C, Cavallaro F, Callaway CW, Sanna T, D’Arrigo S, Kuiper MA et al (2013) Predictors of poor neurological outcome in adult comatose survivors of cardiac arrest: a systematic review and meta-analysis. Part 1: patients not treated with therapeutic hypothermia. Resuscitation 84(10):1310–1323. https://doi.org/10.1016/j.resuscitation.2013.05.013

    Article  PubMed  Google Scholar 

  89. Sandroni C, D’Arrigo S, Cacciola S, Hoedemaekers CWE, Kamps MJA, Oddo M et al (2020) Prediction of poor neurological outcome in comatose survivors of cardiac arrest: a systematic review. Intensive Care Med 46(10):1803–1851. https://doi.org/10.1007/s00134-020-06198-w

    Article  PubMed  PubMed Central  Google Scholar 

  90. Giacino JT, Katz DI, Schiff ND, Whyte J, Ashman EJ, Ashwal S et al (2018) Practice guideline update recommendations summary: disorders of consciousness: report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology; the American Congress of Rehabilitation Medicine; and the National Institute on Disability, Independent Living, and Rehabilitation Research. Neurology 91(10):450–460. https://doi.org/10.1212/WNL.0000000000005926

    Article  PubMed  PubMed Central  Google Scholar 

  91. Kondziella D, Bender A, Diserens K, van Erp W, Estraneo A, Formisano R et al (2020) European Academy of Neurology guideline on the diagnosis of coma and other disorders of consciousness. Eur J Neurol 27(5):741–756. https://doi.org/10.1111/ene.14151

    Article  CAS  PubMed  Google Scholar 

  92. Eliseyev A, Gonzales IJ, Le A, Doyle K, Egbebike J, Velazquez A et al (2021) Development of a brain-computer interface for patients in the critical care setting. PLoS ONE 16(1):e0245540. https://doi.org/10.1371/journal.pone.0245540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Chatelle C, Spencer CA, Cash SS, Hochberg LR, Edlow BL (2018) Feasibility of an EEG-based brain-computer interface in the intensive care unit. Clin Neurophysiol 129(8):1519–1525. https://doi.org/10.1016/j.clinph.2018.04.747

    Article  PubMed  PubMed Central  Google Scholar 

  94. Rohaut B, Eliseyev A, Claassen J (2019) Uncovering consciousness in unresponsive ICU patients: technical, medical and ethical considerations. Crit Care 23(1):78. https://doi.org/10.1186/s13054-019-2370-4

    Article  PubMed  PubMed Central  Google Scholar 

  95. Foreman B, Claassen J (2019) Quantitative EEG for the detection of brain ischemia. Crit Care 16(2):216. https://doi.org/10.1186/cc11230

    Article  Google Scholar 

  96. Kamitaki BK, Tu B, Wong S, Mendiratta A, Choi H (2020) Quantitative EEG changes correlate with post-clamp ischemia during carotid endarterectomy. J Clin Neurophysiol 38(3):213–220. https://doi.org/10.1097/WNP.0000000000000686

    Article  Google Scholar 

  97. Nagata K, Tagawa S, Hiroi S, Shishido F, Uemura K (2020) Electroencephalographic correlates of blood flow and oxygen metabolism provided by positron emission tomography in patients with cerebral infarction. Electroencephalogr Clin Neurophysiol 72(1):16–30. https://doi.org/10.1016/0013-4694(89)90027-8

    Article  Google Scholar 

  98. Laman DM, Wieneke GH, van Diujn H, Velduizen RJ, van Hueffelen AC (2005) QEEG changes during carotid clamping in carotid endarterectomy: spectral edge frequency parameters and relative band power parameters. J Clin Neurophysiol 22(4):244–252. https://doi.org/10.1097/01.wnp.0000167931.83516.cf

    Article  PubMed  Google Scholar 

  99. Finnigan SP, Walsh M, Rose SE, Chalk JB (2007) Quantitative EEG indices of sub-acute ischaemic stroke correlate with clinical outcomes. Clin Neurophysiol 118(11):2525–2532. https://doi.org/10.1016/j.clinph.2007.07.021

    Article  PubMed  Google Scholar 

  100. Devos CC, van Maarseven SM, Brouwers PJ, van Putten MJ (2008) Continuous EEG monitoring during thrombolysis in acute hemispheric stroke patients using the brain symmetry index. J Clin Neurophysiol 25(2):77–82. https://doi.org/10.1097/WNP.0b013e31816ef725

    Article  Google Scholar 

  101. Vespa PM, Nuwer MR, Juhász C, Alexander M, Nenov V, Martin N et al (1997) Early detection of vasospasm after acute subarachnoid hemorrhage using continuous EEG ICU monitoring. Electroencephalogr Clin Neurophysiol 103(6):607–615. https://doi.org/10.1016/s0013-4694(97)00071-0

    Article  CAS  PubMed  Google Scholar 

  102. Claassen J, Hirsch LJ, Kreiter KT, Du EY, Connolly ES, Emerson RG et al (2004) Quantitative continuous EEG for detecting delayed cerebral ischemia in patients with poor-grade subarachnoid hemorrhage. Clin Neurophysiol 115(12):2699–2710. https://doi.org/10.1016/j.clinph.2004.06.017

    Article  PubMed  Google Scholar 

  103. Rathakrishnan R, Gotman J, Dubeau F, Angle M (2020) Using continuous electroencephalography in the management of delayed cerebral ischemia following subarachnoid hemorrhage. Neurocrit Care 14(2):152–161. https://doi.org/10.1007/s12028-010-9495-2

    Article  Google Scholar 

  104. Gollwitzer S, Groemer T, Rampp S, Hagge M, Olmes D, Huttner HB et al (2015) Early prediction of delayed cerebral ischemia in subarachnoid hemorrhage based on quantitative EEG: a prospective study in adults. Clin Neurophysiol 126(8):1514–1523. https://doi.org/10.1016/j.clinph.2014.10.215

    Article  CAS  PubMed  Google Scholar 

  105. Rots ML, van Putten MJ, Hoedemaekers CW, Horn J (2016) Continuous EEG monitoring for early detection of delayed cerebral ischemia in subarachnoid hemorrhage: a pilot study. Neurocrit Care 24(2):207–216. https://doi.org/10.1007/s12028-015-0205-y

    Article  CAS  PubMed  Google Scholar 

  106. Chen HY, Elmer J, Zafar SF, Ghanta M, Moura Junior V, Rosenthal ES et al (2020) Combining transcranial Doppler and EEG data to predict delayed cerebral ischemia after subarachnoid hemorrhage. Neurology 98(5):e459–e469. https://doi.org/10.1212/WNL.0000000000013126

    Article  CAS  Google Scholar 

  107. Le Roux P, Menon DK, Citerio G, Vespa P, Bader MK, Brophy GM et al (2014) Consensus summary statement of the International Multidisciplinary Consensus Conference on Multimodality Monitoring in Neurocritical Care : a statement for healthcare professionals from the Neurocritical Care Society and the European Society of Intensive Care Medicine. Intensive Care Med 40(9):1189–1209. https://doi.org/10.1007/s00134-014-3369-6

    Article  PubMed  Google Scholar 

  108. Leáo AA (1944) Spreading depression of activity in the cerebral cortex. J Neurophysiol 7(6):359–390

    Article  Google Scholar 

  109. Leáo AA (1951) The slow voltage variation of cortical spreading depression of activity. Electroencephalogr Clin Neurophysiol 3(3):315–321. https://doi.org/10.1016/0013-4694(51)90079-x

    Article  PubMed  Google Scholar 

  110. Dreier JP (2011) The role of spreading depression, spreading depolarization and spreading ischemia in neurologic disease. Nat Med 17(4):439–447. https://doi.org/10.1038/nm.2333

    Article  CAS  PubMed  Google Scholar 

  111. Tozzi A, de Lure A, Di Filippo M, Costa C, Caproni S, Pisani A et al (2012) Critical role of calcitonin gene-related peptide receptors in cortical spreading depression. Proc Natl Acad Sci USA 109(46):18985–18990. https://doi.org/10.1073/pnas.1215435109

    Article  PubMed  PubMed Central  Google Scholar 

  112. Bosche B, Graf R, Ernestus RI, Dohmen C, Reithmeier T, Brinker G et al (2010) Recurrent spreading depolarizations after subarachnoid hemorrhage decreases oxygen availability in human cerebral cortex. Ann Neurol 67(5):607–617. https://doi.org/10.1002/ana.21943

    Article  PubMed  PubMed Central  Google Scholar 

  113. Dohmen C, Sakowitz OW (2012) Multimodal monitoring in neurointensive care medicine: state of the art. Nervenartz 83(12):1559–1568. https://doi.org/10.1007/s00115-012-3530-9

    Article  CAS  Google Scholar 

  114. Dohmen C, Sakowtiz OW, Fabricius M, Bosche B, Reithmeier T, Ernestus RI et al (2008) Spreading depolarizations occur in human ischemic stroke with high incidence. Ann Neurol 63(6):720–728. https://doi.org/10.1002/ana.21390

    Article  PubMed  Google Scholar 

  115. Dreier JP, Drenckhahn C, Woitzik J, Major S, Offenhauser N, Weber-Carstens S et al (2013) Spreading ischemia after aneurysmal subarachnoid hemorrhage. Acta Neurochir Suppl 115:125–129. https://doi.org/10.1007/978-3-7091-1192-5_26

    Article  PubMed  Google Scholar 

  116. Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ (2011) Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab 31(1):17–35. https://doi.org/10.1038/jcbfm.2010.191

    Article  PubMed  Google Scholar 

  117. Windmüller O, Lindauer U, Foddis M, Einhäupl KM, Dirnagl U, Heinemann U et al (2005) Ion changes in spreading ischaemia induce rat middle cerebral artery constriction in the absence of NO. Brain 128(9):2024–2051. https://doi.org/10.1093/brain/awh545

    Article  Google Scholar 

  118. Dreier JP, Major S, Manning A, Woitzik J, Drenckhahn SJ et al (2009) Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 132(7):1866–1881. https://doi.org/10.1093/brain/awp102

    Article  PubMed  PubMed Central  Google Scholar 

  119. Robinson D, Hartings J, Foreman B (2021) First report of spreading depolarization correlates on scalp EEG confirmed with a depth electrode. Neurocrit Care 35(Suppl 2):100–104. https://doi.org/10.1007/s12028-021-01360-8

    Article  PubMed  Google Scholar 

  120. Hartings JA, Ngwenya LB, Watanabe T, Foreman B (2018) Commentary: detecting cortical spreading depolarization with full band scalp electroencephalography: an illusion? Front Syst Neurosci 12:19. https://doi.org/10.3389/fnsys.2018.00019

    Article  PubMed  PubMed Central  Google Scholar 

  121. Drenckhahn C, Winkler MKL, Major S, Scheel M, Kang EJ, Pinczolitis A et al (2012) Correlates of spreading depolarization in human scalp electroencephalography. Brain 135(Pt 3):853–868. https://doi.org/10.1093/brain/aws010

    Article  PubMed  PubMed Central  Google Scholar 

  122. Hartings JA, Wilson JA, Hinzman JM, Pollandt S, Dreier JP, DiNapoli V et al (2014) Spreading depression in continuous electroencephalography of brain trauma. Ann Neurol 75(5):681–694. https://doi.org/10.1002/ana.24256

    Article  Google Scholar 

  123. Hukkelhoven CW, Steyerberg EW, Habbema JDF, Farace E, Marmarou A, Murray GD et al (2005) Predicting outcome after traumatic brain injury: development and validation of a prognostic score based on admission characteristics. J Neurotrauma 22(10):1025–1039. https://doi.org/10.1089/neu.2005.22.1025

    Article  PubMed  Google Scholar 

  124. Takano K, Latour LL, Formato JE, Carano RA, Helmer KG, Hasegawa Y et al (1996) The role of spreading depression in focal ischemia evaluated by diffusion mapping. Ann Neurol 39(3):308–318. https://doi.org/10.1002/ana.410390307

    Article  CAS  PubMed  Google Scholar 

  125. Mies G, Iijima T, Hossman KA (1993) Correlation between peri-infarct DC shifts and ischaemic neuronal damage in rat. NeuroReport 4(6):709–711. https://doi.org/10.1097/00001756-199306000-00027

    Article  CAS  PubMed  Google Scholar 

  126. Back T, Ginsberg MD, Dietrich WD, Watson BD (1996) Induction of spreading depression in the ischemic hemisphere following experimental middle cerebral artery occlusion: effect on infarct morphology. J Cereb Blood Flow Metab 16(2):202–213. https://doi.org/10.1097/00004647-199603000-00004

    Article  CAS  PubMed  Google Scholar 

  127. Busch E, Gyngell ML, Eis M, Hoehn-Berlage M, Hossmann KA (1996) Potassium-induced cortical spreading depressions during focal cerebral ischemia in rats: contribution to lesion growth assessed by diffusion-weighted NMR and biochemical imaging. J Cereb Blood Flow Metab 16(6):1090–1099. https://doi.org/10.1097/00004647-199611000-00002

    Article  CAS  PubMed  Google Scholar 

  128. Woitzik J, Dreier JP, Hecht N, Fiss I, Sandow N, Major S et al (2012) Delayed cerebral ischemia and spreading depolarization in absence of angiographic vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab 32(2):203–212. https://doi.org/10.1038/jcbfm.2011.169

    Article  PubMed  Google Scholar 

  129. Dreier JP, Winkler MKL, Major S, Horst V, Lublinksi S, Kola V et al (2022) Spreading depolarizations in ischaemia after subarachnoid haemorrhage, a diagnostic phase III study. Brain 145(4):1264–1284. https://doi.org/10.1093/brain/awab457

    Article  PubMed  Google Scholar 

  130. Helbok R, Hartings JA, Schiefecker A, Balanca B, Jewel S, Foreman B et al (2020) What should a clinician do when spreading depolarizations are observed in a patient? Neurocrit Care 32(1):306–310. https://doi.org/10.1007/s12028-019-00777-6

    Article  PubMed  Google Scholar 

  131. Telles JPM, Welling LC, Coelho ACSD, Rabelo NN, Teixeira MJ, Figueiredo EG (2021) Cortical spreading depolarization and ketamine: a short systematic review. Neurophysiol Clin 51(2):145–151. https://doi.org/10.1016/j.neucli.2021.01.004

    Article  PubMed  Google Scholar 

  132. Hartings JA (2017) Spreading depolarization monitoring in neurocritical care of acute brain injury. Curr Opin Crit Care 23(2):94–102. https://doi.org/10.1097/MCC.0000000000000395

    Article  PubMed  Google Scholar 

  133. Sinha SR, Sullivan L, Sabau D, San-Juan D, Dombrowski KE, Halford JJ et al (2016) American Clinical Neurophysiology Society Guideline 1: minimum technical requirements for performing clinical electroencephalography. J Clin Neurophysiol 33(4):303–307. https://doi.org/10.1097/WNP.0000000000000308

    Article  PubMed  Google Scholar 

  134. Abend NS, Dlugos DJ, Zhu X, Schwartz ES (2015) Utility of CT-compatible EEG electrodes in critically ill children. Pediatr Radiol 45(5):714–718. https://doi.org/10.1007/s00247-014-3208-5

    Article  PubMed  Google Scholar 

  135. Mirsattari SM, Lee DH, Jones D, Bihari F, Ives JR (2004) MRI compatible EEG electrode system for routine use in the epilepsy monitoring unit and intensive care unit. Clin Neurophysiol 115(9):2175–2180. https://doi.org/10.1016/j.clinph.2004.04.011

    Article  PubMed  Google Scholar 

  136. Berlin F, Carlile JA, de Burgo MI, Rochon A, Wager EE, Sellers MC et al (2011) Technical tips: electrode application and preventing skin breakdown techniques. Am J Electroneurodiagnostic Technol 51(3):206–219

    Article  Google Scholar 

  137. Waziri A, Claassen J, Stuart RM, Arif H, Schmidt JM, Mayer SA et al (2009) Intracortical electroencephalography in acute brain injury. Ann Neurol 66(3):366–377. https://doi.org/10.1002/ana.21721

    Article  PubMed  Google Scholar 

  138. Stuart RM, Waziri A, Weintraub D, Schmidt MJ, Fernandez L, Helbok R et al (2010) Intracortical EEG for the detection of vasospasm in patients with poor-grade subarachnoid hemorrhage. Neurocrit Care 13(3):355–358. https://doi.org/10.1007/s12028-010-9414-6

    Article  PubMed  Google Scholar 

  139. Dreier JP, Fabricius M, Ayata C, Sakowitz OW, Shuttleworth CW, Dohmen C et al (2017) Recording, analysis, and interpretation of spreading depolarizations in neurointensive care: Review and recommendations of the COSBID research group. J Cereb Blood Flow Metab 37(5):1595–1625. https://doi.org/10.1177/0271678x16654496

    Article  PubMed  Google Scholar 

  140. Appavu B, Foldes S, Temkit M, Jacobson A, Burrows BT, Brown D et al (2020) Intracranial electroencephalography in pediatric severe traumatic brain injury. Pediatr Crit Care Med 21(3):240–247. https://doi.org/10.1097/PCC.0000000000002136

    Article  PubMed  Google Scholar 

  141. Shellhaas RA, Chang T, Tsuchida T, Scher MS, Riviello JJ, Abend NS et al (2011) The American Clinical Neurophysiology Society’s guideline on continuous electroencephalography monitoring in neonates. J Clin Neurophysiol 28(6):611–617. https://doi.org/10.1097/WNP.0b013e31823e96d7

    Article  PubMed  Google Scholar 

  142. Rossetti AO, Schindler K, Sutter R, Rüegg S, Zubler F, Novy J (2020) Continuous vs routine electroencephalogram in critically ill adults with altered consciousness and no recent seizure: a multicenter randomized clinical trial. JAMA Neurol 77(10):1225–1232. https://doi.org/10.1001/jamaneurol.2020.2264

    Article  PubMed  Google Scholar 

  143. Gaspard N, Westover MB, Hirsch LJ (2021) Assessment of a study of continuous vs repeat-spot electroencephalography in patients with critical illness. JAMA Neurol 78(3):369. https://doi.org/10.1001/jamaneurol.2020.5348

    Article  PubMed  PubMed Central  Google Scholar 

  144. Struck AF, Ustun B, Rodriguez-Ruiz A, Lee JW, LaRoche SM, Hirsch LJ et al (2017) Association of an electroencephalography-based risk score with seizure probability in hospitalized patients. JAMA Neurol 74(12):1419–1424. https://doi.org/10.1001/jamaneurol.2017.2459

    Article  PubMed  PubMed Central  Google Scholar 

  145. Struck AF, Osman G, Rampal N, Biswal S, Legros B, Hirsch LJ et al (2017) Time-dependent risk of seizures in critically ill patients on continuous electroencephalogram. Ann Neurol 82(2):177–185. https://doi.org/10.1002/ana.24985

    Article  PubMed  PubMed Central  Google Scholar 

  146. Chiu WT, Schiefecker A, Rivero Rodriguez D, Ferreira D, Headlee A, Zeidan S et al (2022) Management of refractory status epilepticus: an international cohort study. Neurology. https://doi.org/10.1212/WNL.0000000000200818

    Article  PubMed  Google Scholar 

  147. Vespa PM, Olson DW, John S, Hobbs KS, Gururangan K, Nie K et al (2020) Evaluating the clinical impact of rapid response electroencephalography: the DECIDE multicenter prospective observational clinical study. Crit Care Med 48(9):1249–1257. https://doi.org/10.1097/CCM.0000000000004428

    Article  PubMed  PubMed Central  Google Scholar 

  148. Kromm J, Fiest KM, Alkhachroum A, Josephson C, Kramer A, Jette N (2021) Structure and outcomes of educational programs for training non-electroencephalographers in performing and screening adult EEG: a systematic review. Neurocrit Care 35(3):894–912. https://doi.org/10.1007/s12028-020-01172-2

    Article  PubMed  Google Scholar 

Download references

Funding

AA is supported by an institutional KL2 Career Development Award from the Miami CTSI NCATS UL1TR002736 and by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under Award Number K23NS126577. BA is supported by grant funding from the American Heart Association (19CDA34760291), Congressionally Directed Medical Research Program (W81XWH-19-1-0514) and Innovators in Neuroscience for Kids Foundation. JC is supported by grant funding from the NIH R01 NS106014 and R03 NS112760, and the McDonnell Foundation.

Author information

Author notes

  1. Ayham Alkhachroum and Brian Appavu: Co-first authors.

  2. Benjamin Rohaut and Jan Claassen: Co-senior authors.

Authors and Affiliations

  1. Department of Neurology, University of Miami, Miami, FL, USA

    Ayham Alkhachroum

  2. Department of Neurology, Jackson Memorial Hospital, Miami, FL, USA

    Ayham Alkhachroum

  3. Department of Child Health and Neurology, University of Arizona College of Medicine-Phoenix, Phoenix, AZ, USA

    Brian Appavu

  4. Department of Neurosciences, Phoenix Children’s Hospital, Phoenix, AZ, USA

    Brian Appavu

  5. Neurointensive Care Unit, Department of Neurosurgery, and Stroke and Epilepsy Center, TMG Asaka Medical Center, Saitama, Japan

    Satoshi Egawa

  6. Department of Neurology and Rehabilitation Medicine, University of Cincinnati, 231 Albert Sabin Way, Cincinnati, OH, USA

    Brandon Foreman

  7. Department of Neurology, Erasme Hospital, Free University of Brussels, Brussels, Belgium

    Nicolas Gaspard

  8. Comprehensive Epilepsy Center, Department of Neurology, Yale University School of Medicine, New Haven, CT, USA

    Emily J. Gilmore & Lawrence J. Hirsch

  9. Neurocritical Care and Emergency Neurology, Department of Neurology, Ale University School of Medicine, New Haven, CT, USA

    Emily J. Gilmore

  10. Department of Intensive Care Medicine, D’or Institute for Research and Education, Rio de Janeiro, Brazil

    Pedro Kurtz

  11. Neurointensive Care, Paulo Niemeyer State Brain Institute, Rio de Janeiro, Brazil

    Pedro Kurtz

  12. Department of Clinical Neurophysiology and Epilepsy Unit, AP-HP, Pitié Salpêtrière Hospital, Reference Center for Rare Epilepsies, 75013, Paris, France

    Virginie Lambrecq

  13. Departments of Critical Care Medicine and Clinical Neurosciences, Cumming School of Medicine, Calgary, AB, Canada

    Julie Kromm

  14. Hotchkiss Brain Institute, Cumming School of Medicine, Calgary, AB, Canada

    Julie Kromm

  15. Brain Injury Research Center, Department of Neurosurgery, University of California, Los Angeles, USA

    Paul Vespa

  16. Department of Neurology, Massachusetts General Hospital, Boston, MA, USA

    Sahar F. Zafar

  17. Department of Neurology, Sorbonne Université, Pitié-Salpêtrière-AP-HP and Paris Brain Institute, ICM, Inserm, CNRS, Paris, France

    Benjamin Rohaut

  18. Department of Neurology, Neurological Institute, Columbia University, New York Presbyterian Hospital, 177 Fort Washington Avenue, MHB 8 Center, Room 300, New York, NY, 10032, USA

    Jan Claassen

Authors
  1. Ayham Alkhachroum
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brian Appavu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Satoshi Egawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Brandon Foreman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nicolas Gaspard
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Emily J. Gilmore
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lawrence J. Hirsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Pedro Kurtz
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Virginie Lambrecq
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Julie Kromm
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Paul Vespa
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Sahar F. Zafar
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Benjamin Rohaut
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jan Claassen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization and drafting of the manuscript: AA, BA, BR and JC. Critical Revision of the manuscript for important intellectual content: SE, BF, NG, EG, LJH, PK, VL, JK, PV and SZ.

Corresponding author

Correspondence to Jan Claassen.

Ethics declarations

Conflict of interest

AA, BA, and SE report no disclosures. BF is supported by grant funding from the DOD (JW200215 and W81XWH1920013). He received additional support for research through the NIH/NINDS, NIH/NIBIB, and NSF. He receives speaking fees and consulting fees from UCB Pharma, and serves on the scientific advisory boards of Marinus, Inc and Sage Therapeutics. NG reports no disclosures. EJG is supported by grant funding from the NIH R01NS117904-01, is a consultant for UCB and co-founder (no financial relationship) of Intracranial Bioanalytics (IBA). LJH has received consultation fees for advising from Accure, Aquestive, Ceribell, Eisai, Marinus, Medtronic, Neurelis, Neuropace and UCB; royalties from Wolters-Kluwer for authoring chapters for UpToDate-Neurology, and from Wiley for co-authoring the book “Atlas of EEG in Critical Care”; and honoraria for speaking or running webinars from Neuropace, Natus, and UCB. PK reports no disclosures. VL reports no disclosures. JK is supported by grant funding through the University of Calgary, Office of Health and Medical Education Scholarship. PV is supported by grants from NIH and the State of California PV has received compensation for consultancy and speaker fees and expenses from Ceribell and consultancy and speaker fees from UCB Pharma. SFZ is supported by grant funding from the NIH K23NS114201 and the American Epilepsy Society (Infrastructure grant). She is a clinical neurophysiologist for Corticare. BR reports no disclosures. JC is a minority shareholder at iCE Neurosystems.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

134_2022_6854_MOESM1_ESM.tif

Supplementary file1 Supplemental Figure 1: Example of the double banana configuration for electroencephalographic monitoring. (TIF 82 kb)

134_2022_6854_MOESM2_ESM.tif

Supplementary file2 Supplemental Figure 2: Example of the flame sign on color dense spectral array, consistent with electrographic seizure activity. (TIF 11999 kb)

Supplementary file3 Supplemental Figure 3: Example of generalized sharp waves with triphasic morphology. (TIF 39867 kb)

Supplementary file4 Supplemental Figure 4: Example of bilateral sleep spindles. (TIF 50229 kb)

Supplementary file5 Supplemental Figure 5: Example of burst suppression on electroencephalography. (TIF 41771 kb)

134_2022_6854_MOESM6_ESM.tif

Supplementary file6 Supplemental Figure 6: In the traumatic brain injury patient shown in Figure 11, the SDs eventually stop spontaneously. Subsequently, cyclic focal seizures begin to occur up to 5 per hour. In this 2-hour window, seizures can be observed in the high-frequency activity represented by the black band as ‘sideways tornados’ of evolving ictal discharges and each seizure is denoted by a white arrowhead. F) This ictal rhythm is seen on high-frequency EEG as an evolving 2.5 Hz spike-wave pattern best defined in channel 3-4. (TIF 20584 kb)

134_2022_6854_MOESM7_ESM.tif

Supplementary file7 Supplemental Figure 7: Example of bilateral independent lateralized periodic discharges (BiLPDs). (TIF 32346 kb)

134_2022_6854_MOESM8_ESM.docx

Supplementary file8 Supplemental Table 1: Prevalence of acute symptomatic seizures after acute brain injuries, and their association with outcomes. (DOCX 82 kb)

134_2022_6854_MOESM9_ESM.docx

Supplementary file9 Supplemental Table 2: Recommended indications and duration for continuous electroencephalographic monitoring across different conditions. (DOCX 15 kb)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alkhachroum, A., Appavu, B., Egawa, S. et al. Electroencephalogram in the intensive care unit: a focused look at acute brain injury. Intensive Care Med 48, 1443–1462 (2022). https://doi.org/10.1007/s00134-022-06854-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00134-022-06854-3

Keywords

Search

Navigation