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Electroencephalographic Patterns in Neurocritical Care: Pathologic Contributors or Epiphenomena?

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References

  1. Trinka E, Cock H, Hesdorffer D, Rossetti A, Scheffer IE, Shinnar S, et al. A definition and classification of status epilepticus—report of the ILAE task force on classification of status epilepticus. Epilepsia. 2015;56:1515–23.

    Article  PubMed  Google Scholar 

  2. Young GB, Jordan KG, Doig GS. An assessment of nonconvulsive seizures in the intensive care unit using continuous EEG monitoring: an investigation of variables associated with mortality. Neurology. 1996;47(1):83–9.

    Article  PubMed  CAS  Google Scholar 

  3. Leitinger M, Beniczky S, Rohracher A, Gardella E, Kalss G, Qerama E, et al. Salzburg consensus criteria for non-convulsive status epilepticus—approach to clinical application. Epilepsy Behav. 2015;49:158–63.

    Article  PubMed  CAS  Google Scholar 

  4. Harvey AS, Bowe JM, Hopkins IJ, Shield LK, Cook DJ, Berkovic SF. Ictal 99mTc-HMPAO single photon emission computed tomography in children with temporal lobe epilepsy. Epilepsia. 1993;34:869–77.

    Article  PubMed  CAS  Google Scholar 

  5. Kapur J, Macdonald RJ. Rapid seizure-induced benzodiazepine and Zn2+ sensitivity of hippocampal dentate granule cell GABAA receptors. J Neurosci. 1997;17:7532–40.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Naylor DE, Liu H, Niguet J, Wasterlain CG. Rapid surface accumulation of NMDA receptors increases glutamatergic excitation during status epilepticus. Neurobiol Dis. 2013;54:225–38.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Lothman E. The biochemical basis and pathophysiology of status epilepticus. Neurology. 1990;40:13–23.

    PubMed  CAS  Google Scholar 

  8. Bruel C, Hagemann G, Witte OW. Uncoupling of blood flow and metabolism in focal epilepsy. Epilepsia. 1998;39:1235–42.

    Article  Google Scholar 

  9. Huang YC, Weng HH, Tsai YT, Huang YC, Hsiao MC, Wu CY, et al. Periictal magnetic resonance imaging in status epilepticus. Epilepsy Res. 2009;86(1):72–81.

    Article  PubMed  Google Scholar 

  10. Chatzikonstantinou A, Gass A, Forster A, Hennerici MG, Szabo K. Features of acute DWI abnormalities related to status epilepticus. Epilepsy Res. 2011;97(1–2):45–51.

    Article  PubMed  Google Scholar 

  11. Szabo K, Poepel A, Pohlmann-Eden B, Hirsch J, Back T, Sedlaczek O, et al. Diffusion-weighted and perfusion MRI demonstrates parenchymal changes in complex partial status epilepticus. Brain. 2005;128(Pt 6):1369–76.

    Article  PubMed  Google Scholar 

  12. Waziri A, Claassen J, Stuart RM, Arif H, Schmidt JM, Mayer SA, et al. Intracortical electroencephalography in acute brain injury. Ann Neurol. 2009;66(3):366–77.

    Article  PubMed  Google Scholar 

  13. Vespa P, Tubi M, Claassen J, Buitrago-Blanco M, McArthur D, Velazquez AG, et al. Metabolic crisis occurs with seizures and periodic discharges after brain trauma. Ann Neurol. 2016;79(4):579–90.

    Article  PubMed  Google Scholar 

  14. Claassen J, Perotte A, Albers D, Kleinberg S, Schmidt JM, Tu B, et al. Nonconvulsive seizures after subarachnoid hemorrhage: multimodal detections and outcomes. Ann Neurol. 2013;74(1):53–64.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Wijdicks EF, Hijdra A, Young GB, Basseti CL, Wiebe S. Practice parameter: prediction of outcome in comatose survivors after cardiopulmonary resuscitation (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology. 2006;67(2):203–10.

    Article  PubMed  CAS  Google Scholar 

  16. Rossetti AO, Oddo M, Liaudet L, Kaplan PW. Predictors of awakening from postanoxic status epilepticus after therapeutic hypothermia. Neurology. 2009;72:744–9.

    Article  PubMed  Google Scholar 

  17. Westhall E, Rundgren M, Lilja G, Friberg H, Cronberg T. Postanoxic status epilepticus can be identified and treatment guided successfully by continuous electroencephalography. Hypothermia Temp Manag. 2013;3:84–7.

    Article  Google Scholar 

  18. Seder DB, Sunde K, Rubertsson S, Mooney M, Stammet P, Riker RR, et al. Neurologic outcomes and postresuscitation care of patients with myoclonus following cardiac arrest. Crit Care Med. 2015;43(5):965–72.

    Article  PubMed  Google Scholar 

  19. Oddo M, Rossetti AO. Early multimodal outcome prediction after cardiac arrest in patients treated with hypothermia. Crit Care Med. 2014;42:1340–7.

    Article  PubMed  Google Scholar 

  20. Elmer J, Rittenberger JC, Faro J, Molyneaux BJ, Popescu A, Callaway CW, et al. Clinically distinct electroencephalographic phenotypes of early myoclonus after cardiac arrest. Ann Neurol. 2016;80:175–84.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Glauser T, Shinnar S, Gloss D, Alldredge B, Arya R, Bainbridge J, et al. Evidence-based guideline: treatment of convulsive status epilepticus in children and adults: report of the guideline committee of the American Epilepsy Society. Epilepsy Curr. 2016;16(1):48–61.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Reynolds AS, Holmes MG, Agarwal S, Claassen J. Phenotypes of early myoclonus do not predict outcome. Ann Neurol. 2017;81(3):475–6.

    Article  PubMed  Google Scholar 

  23. Chong DJ, Hirsch LJ. Which EEG patterns warrant treatment in the critically Ill? Reviewing the evidence for treatment of periodic epileptiform discharges and related patterns. J Clin Neurophysiol. 2005;22:79–91.

    Article  PubMed  Google Scholar 

  24. Struck AF, Westover MB, Hall LT, Deck GM, Cole AJ, Rosenthal ES. Metabolic correlates of the ictal-interictal continuum: FDG-PET during continuous EEG. Neurocrit Care. 2016;24(3):324–31.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Pohlmann-Eden B, Hoch DB, Cochius JL, Chiappa KH. Periodic lateralized epileptiform discharges—a critical review. J Clin Neurophysiol. 1996;13(6):519–30.

    Article  PubMed  CAS  Google Scholar 

  26. Hirsch LJ, LaRoche SM, Gaspard N, Gerard E, Svoronos A, Herman ST, et al. American clinical neurophysiology society’s standardized critical care terminology: 2012. J Clin Neurophysiol. 2013;30(1):1–27.

    Article  PubMed  CAS  Google Scholar 

  27. Hirsch LJ, Claassen J, Myer SA, Emerson RG. Stimulus-induced rhythmic, periodic, or ictal discharges (SIRPIDS): a common EEG phenomenon in the critically Ill. Epilepsia. 2004;45(2):109–23.

    Article  PubMed  Google Scholar 

  28. Brenner RP, Schaul N. Periodic EEG patterns: classification, clinical correlation, and pathophysiology. J Clin Neurophysiol. 1990;7:249–67.

    Article  PubMed  CAS  Google Scholar 

  29. Rodriguez Ruiz A, Vlachy J, Lee JW, Gilmore EJ, Haider HA, Gaspard N, et al. Association of periodic and rhythmic electroencephalographic patterns with seizures in critically Ill patients. JAMA Neurol. 2017;74(2):181–8.

    Article  PubMed  Google Scholar 

  30. Akman CI, Abou Khaled KJ, Segal E, Micic V, Riviello JJ. Generalized periodic epileptiform discharges in critically ill children: clinical features and outcome. Epilepsy Res. 2013;106:378–85.

    Article  PubMed  Google Scholar 

  31. Bhatt AB, Popescu A, Waterhouse EJ, Abou-Khalil BW. De novo generalized periodic discharges related to anesthetic withdrawal resolve spontaneously. J Clin Neurophysiol. 2014;31(3):194–8.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Garcı´a-Morales I, Garcı´a MT, Gala´n-Da´vila L, Gomez-Escalonilla C, Saiz-Diaz R, Martinez-Salio A, et al. Periodic lateralized epileptiform discharges: Etiology, clinical aspects, seizures, and evolution in 130 patients. J Clin Neurophysiol. 2002;19(2):172–7.

    Article  Google Scholar 

  33. San Juan Orta D, Chiappa KH, Quiroz AZ, Costello DJ, Cole AJ. Prognosis implications of periodic epileptiform discharges. Arch Neurol. 2009;66(8):985–91.

    Article  Google Scholar 

  34. Reiher J, Rivest J, Grand’Maison F, Leduc CP. Periodic lateralized epileptiform discharges with transitional rhythmic discharges: association with seizures. Electroencephalogr Clin Neurophysiol. 1991;78:12–7.

    Article  PubMed  CAS  Google Scholar 

  35. Braksick SA, Burkholder DB, Tsetsou S, Martineau L, Mandrekar J, Rossetti AO, et al. Associated factors and prognostic implications of stimulus-induced rhythmic, periodic, or ictal discharges. JAMA Neurol. 2016;73(5):585–90.

    Article  PubMed  Google Scholar 

  36. Ergun EL, Salanci BV, Erbas B, Saygi S. SPECT in periodic lateralized epileptiform discharges (PLEDs): a case report on PLEDs. Ann Nucl Med. 2006;20(3):227–31.

    Article  PubMed  Google Scholar 

  37. Bozkurt MF, Saygi S, Erbas B. SPECT in a patient with postictal PLEDs: is hyperperfusion evidence of electrical seizure? Clin Electroencephalogr. 2002;33(4):171–3.

    Article  PubMed  Google Scholar 

  38. Assal F, Papazyan JP, Slosman DO, Jallon P, Goerres GW. SPECT in periodic lateralized epileptiform discharges (PLED): a form of partial status epilepticus? Seizure. 2001;10(4):260–6.

    Article  PubMed  CAS  Google Scholar 

  39. Venkatraman A, Khawaja A, Bag AK, Mirza M, Szaflarski JP, Pati S. Perfusion MRI can impact treatment decision in ictal-interictal continuum. J Clin Neurophysiol. 2017;34(4):e15–8.

    Article  PubMed  Google Scholar 

  40. Smith CC, Tatum WO, Gupta V, Pooley RA, Freeman WD. SPECT-negative SIRPIDs: less aggressive neurointensive care? J Clin Neurophysiol. 2014;31(3):e6–10.

    Article  PubMed  Google Scholar 

  41. Witsch J, Frey HP, Schmidt JM, Velazquez A, Falo CM, Reznick M, et al. Electroencephalographic periodic discharges and frequency-dependent brain tissue hypoxia in acute brain injury. JAMA Neurol. 2017;74(3):301–9.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Speckmann EJ, Elger CE, Gorji A. Neurophysiologic basis of EEG and DC potentials. In: Schomer DL, Lopes da Silva FH. Niedermeyer’s Electroencephalography. 6th ed. Philadelphia: Lippincott Williams & Wilkins; 2011:1453–1454.

  43. Gaspard N, Manganas L, Rampal N, Petroff OA, Hirsch LJ. Similarity of lateralized rhythmic delta activity to periodic lateralized epileptiform discharges in critically ill patients. JAMA Neurol. 2013;70(10):1288–95.

    PubMed  Google Scholar 

  44. Kaplan PW, Bauer G. Clinical definitions of impaired responsiveness: from locked in states to coma. In: Schomer DL, Lopes da Silva FH, 6th eds. Current Practice of Clinical Electroencephalography. Philadelphia: Lippincott Williams & Wilkins; 2011.

  45. Hartings JA, Wilson JA, Hinzman JM, Pollandt S, Dreier JP, DiNapoli V, et al. Spreading depression in continuous electroencephalography of brain trauma. Ann Neurol. 2014;76(5):681–94.

    Article  PubMed  Google Scholar 

  46. Charles AC, Baca SM. Cortical spreading depression and migraine. Nat Rev Neurol. 2013;9(11):637–44.

    Article  PubMed  Google Scholar 

  47. Astrup J, Siesjo BK, Symon L. Thresholds in cerebral ischemia—the ischemic penumbra. Stroke. 1981;12(6):723–5.

    Article  PubMed  CAS  Google Scholar 

  48. Woitzik J, Hecht N, Pinczolits A, Sandow N, Major S, Winkler MK, et al. Propagation of cortical spreading depolarization in the human cortex after malignant stroke. Neurology. 2013;80(12):1095–102.

    Article  PubMed  Google Scholar 

  49. Yuzawa I, Sakadzic S, Srinivsan VJ, Shin SK, Eikermann-Haerter K, Boas DA, et al. Cortical spreading depression impairs oxygen delivery and metabolism in mice. J Cereb Blood Flow Metab. 2012;32(2):376–86.

    Article  PubMed  CAS  Google Scholar 

  50. Dreier JP. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med. 2011;17(4):439–47.

    Article  PubMed  CAS  Google Scholar 

  51. Dreier JP, Major S, Manning A, Woitzik J, Drenckhahn C, Steinbrink J, et al. Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid hemorrhage. Brain. 2009;132(Pt 7):1866–81.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Unekawa M, Tomita M, Tomita Y, Toriumi H, Suzuki N. Sustained decrease and remarkable increase in red blood cell velocity in intraparenchymal capillaries associated with potassium-induced cortical spreading depression. Microcirculation. 2012;19(2):166–74.

    Article  PubMed  CAS  Google Scholar 

  53. Jespersen SN, Ostergaard L. The roles of cerebral blood flow, capillary transit time heterogeneity, and oxygen tension in brain oxygenation and metabolism. J Cereb Blood Flow Metab. 2012;32(2):264–77.

    Article  PubMed  CAS  Google Scholar 

  54. Hartings JA, Bullock MR, Okonkwo DO, Murray LS, Murray GD, Fabricius M, et al. Spreading depolarisations and outcome after traumatic brain injury: a prospective observational study. Lancet Neurol. 2011;10(12):1058–64.

    Article  PubMed  Google Scholar 

  55. Leao AAP. Spreading depression of activity in the cerebral cortex. J Neurophysiol. 1944;7:359–90.

    Article  Google Scholar 

  56. Leao, AAP. Spreading Depression. In: Purpura, D.P., Penry K., Tower, D.B., Woodry, D.M., & Walter, R.D. (Eds.), Experimental models of epilepsy 1972 (pp. 173–195). New York: Raven Press.

  57. Van Harreveld A, Stamm JS. Spreading cortical convulsions and depressions. J Neurophysiol. 1953;16(4):352–66.

    Article  Google Scholar 

  58. Dreier JP, Major S, Pannek HW, Woitzik J, Scheel M, Wiesenthal D, et al. Spreading convulsions, spreading depolarizations and epileptogenesis in human cerebral cortex. Brain. 2012;13(Pt 1):259–75.

    Article  Google Scholar 

  59. Fabricius M, Fuhr S, Willumsen L, Dreier JP, Bhatia R, Boutelle MG, et al. Association of seizures with cortical spreading depression and peri-infarct depolarisations in the acutely injured human brain. Clin Neurophysiol. 2008;119(9):1973–84.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Sharbough FW, Messick JM Jr, Sundt TM Jr. Correlation of continuous electroencephalograms with cerebral blood flow measurements during carotid endarterectomy. Stroke. 1973;4:674–83.

    Article  Google Scholar 

  61. Foreman B, Claassen J. Quantitative EEG for the detection of brain ischemia. Crit Care. 2012;16:216.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Schneider AL, Jordan KG. Regional attenuation without delta (RAWOD): a distinctive EEG pattern that can aid in the diagnosis and management of severe acute ischemic stroke. Am J Electroneurodiagnostic Technol. 2005;45:102–17.

    Article  PubMed  Google Scholar 

  63. Kohno K, Hoehn-Berlage M, Mies G, Back T, Hossmann KA. Relationship between diffusion-weighted MR images, cerebral blood flow, and energy state in experimental brain infarction. Magn Reson Imaging. 1995;13:73–80.

    Article  PubMed  CAS  Google Scholar 

  64. de Vos CC, van Maarseveen SM, Brouwers PJ, van Putten MJ. Continuous EEG monitoring during thrombolysis in acute hemispheric stroke patients using the brain symmetry index. J Clin Neurophysiol. 2008;25:77–82.

    Article  PubMed  Google Scholar 

  65. Sheorajpanday RV, Nagels G, Weeren AJ, De Deyn PP. Quantitative EEG in ischemic stroke: correlation with infarct volume and functional status in posterior circulation and lacunar syndromes. Clin Neurophysiol. 2011;122:884–90.

    Article  PubMed  Google Scholar 

  66. Finnigan SP, Rose SE, Chalk JB. Rapid EEG changes indicate reperfusion after tissue plasminogen activator injection in acute ischaemic stroke. Clin Neurophysiol. 2006;117:2338–9.

    Article  PubMed  Google Scholar 

  67. Frontera JA, Fernandez A, Schmidt JM, Claassen J, Wartenberg KE, Badjatia N, et al. Defining vasospasm after subarachnoid hemorrhage: what is the most clinically relevant definition? Stroke. 2009;40:1963–8.

    Article  PubMed  Google Scholar 

  68. LaRovere KL, O’Brien NF. Transcranial doppler sonography in pediatric neurocritical care: a review of clinical applications and case illustrations in the pediatric intensive care unit. J Ultrasound Med. 2015;34(12):2121–32.

    Article  PubMed  Google Scholar 

  69. O’Brien NF, Reuter-Rice KE, Khanna S, Peterson BM, Quinto KB. Vasospasm in children with traumatic brain injury. Intensive Care Med. 2010;36(4):680–7.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Rao VK, Haridas A, Nguyen TT, Lulla R, Wainwright MS, Goldstein JL. Symptomatic cerebral vasospasm following resection of a medulloblastoma in a child. Neurocrit Care. 2013;18(1):84–8.

    Article  PubMed  Google Scholar 

  71. Claassen J, Hirsch LJ, Frontera JA, Fernandez A, Schmidt M, Kapinos G, et al. Prognostic significance of continuous EEG monitoring in patients with subarachnoid hemorrhage. Neurocrit Care. 2006;4(2):103–12.

    Article  PubMed  Google Scholar 

  72. Rivierez M, Landau-Ferey J, Grob R, Grosskopf D, Philippon J. Value of electroencephalogram in prediction and diagnosis of vasospasm after intracranial aneurysmal rupture. Acta Neurochir (Wien). 1991;110:17–23.

    Article  CAS  Google Scholar 

  73. Kim JA, Rosenthal ES, Biswal S, Zafar S, Shenoy AV, O’Connor KL. Epileptiform abnormalities predict delayed cerebral ischemia in subarachnoid hemorrhage. Clin Neurophysiol. 2017;128(6):1091–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Claassen J, Hirsch LJ, Kreiter KT, Du EY, Connolly ES, Emerson RG, et al. Quantitative continuous EEG for detecting delayed cerebral ischemia in patients with poor-grade subarachnoid hemorrhage. Clin Neurophysiol. 2004;115:2699–710.

    Article  PubMed  Google Scholar 

  75. Rathakrishnan R, Gotman J, Dubeau F, Angle M. Using continuous electroencephalography in the management of delayed cerebral ischemia following subarachnoid hemorrhage. Neurocrit Care. 2011;14(2):152–61.

    Article  PubMed  Google Scholar 

  76. Shmidt JM. Bioinformatics for multimodal monitoring. In: Miller CM, Torbey MT, editors. Neurocritical care monitoring. New York: Demos Medical Publishing; 2015. p. 135–7.

    Google Scholar 

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Acknowledgements

We would like to thank Jed Hartings, Ph.D., for graciously providing us with a figure of cortical spreading depolarizations (Fig. 3). We would also like to thank Michelle Wotowiec, MA, for critical review of this manuscript.

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Appavu, B., Riviello, J.J. Electroencephalographic Patterns in Neurocritical Care: Pathologic Contributors or Epiphenomena?. Neurocrit Care 29, 9–19 (2018). https://doi.org/10.1007/s12028-017-0424-5

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