Abstract
The aim of this review was to provide up-to-date information about the usefulness of clinical neurophysiology testing in the management of critically ill patients. Evoked potentials (EPs) and electroencephalogram (EEG) are non-invasive clinical neurophysiology tools that allow an objective assessment of the central nervous system’s function at the bedside in intensive care unit (ICU). These tests are quite useful in diagnosing cerebral complications, and establishing the vital and functional prognosis in ICU. EEG keeps a particularly privileged importance in detecting seizures phenomena such as subclinical seizures and non-convulsive status epilepticus. Quantitative EEG (QEEG) analysis techniques commonly called EEG Brain mapping can provide obvious topographic displays of digital EEG signals characteristics, showing the potential distribution over the entire scalp including filtering, frequency, and amplitude analysis and color mapping. Evidences of usefulness of QEEG for seizures detection in ICU are provided by several recent studies. Furthermore, beyond detection of epileptic phenomena, changes of some QEEG panels are early warning indicators of sedation level as well as brain damage or dysfunction in ICU. EPs offer the opportunity for assessing brainstem’s functional integrity, as well as subcortical and cortical brain areas. A multimodal use, combining EEG and various modalities of EPs is recommended since this allows a more accurate functional exploration of the brain and helps caregivers to tailor therapeutic measures according to neurological worsening trends and to anticipate the prognosis in ICU.
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References
American Electroencephalographic Society Guidelines in Electroencephalography (1994) Evoked potentials, and polysomnography. J Clin Neurophysiol 11:1–147
Guerit JM, Amantini A, Amodio P, Andersen KV, Butler S et al (2009) Consensus on the use of neurophysiological tests in the intensive care unit (ICU): electroencephalogram (EEG), evoked potentials (EP), and electroneuromyography (ENMG). Neurophysiol Clin 39:71–83
Kull LL, Emerson RG (2005) Continuous EEG monitoring in the intensive care unit: technical and staffing considerations. J Clin Neurophysiol 22:107–118
Hirsch LJ, Kull LL (2004) Continuous EEG monitoring in the intensive care unit. Am J Electroneurodiagnostic Technol 44:137–158
Fischer C (1997) The use of EEG in the diagnosis of brain death in France. Neurophysiol Clin 27:373–382
Guerit JM (1992) Evoked potentials: a safe brain-death confirmatory tool? Eur J Med 1:233–243
Guerit JM (2004) The concept of brain death. Adv Exp Med Biol 550:15–21
Guerit JM (2007) Electroencephalography: the worst traditionally recommended tool for brain death confirmation. Intensive Care Med 33:9–10
Hantson P, de Tourtchaninoff M, Guerit JM, Vanormelingen P, Mahieu P (1997) Multimodality evoked potentials as a valuable technique for brain death diagnosis in poisoned patients. Transplant Proc 29:3345–3346
Claassen J, Taccone FS, Horn P, Holtkamp M, Stocchetti N et al (2013) Recommendations on the use of EEG monitoring in critically ill patients: consensus statement from the neurointensive care section of the ESICM. Intensive Care Med 39:1337–1351
Freye E (2005) Cerebral Monitoring in the Operating Room and the Intensive Care Unit: an introductory for the clinician and a guide for the novice wanting to open a window to the brain. Part III: Spinal cord evoked potentials. J Clin Monit Comput 19:169–178
Rossetti AO, Reichhart MD, Schaller MD, Despland PA, Bogousslavsky J (2004) Propofol treatment of refractory status epilepticus: a study of 31 episodes. Epilepsia 45:757–763
Stocchetti N, Le Roux P, Vespa P, Oddo M, Citerio G et al (2013) Clinical review: neuromonitoring—an update. Crit Care 17:201
Swisher CB, Sinha SR (2016) Utilization of quantitative EEG trends for critical care continuous EEG monitoring: a survey of neurophysiologists. J Clin Neurophysiol 33:538–544
Swisher CB, White CR, Mace BE, Dombrowski KE, Husain AM et al (2015) Diagnostic accuracy of electrographic seizure detection by neurophysiologists and non-neurophysiologists in the adult ICU using a panel of quantitative EEG trends. J Clin Neurophysiol 32:324–330
Dericioglu N, Yetim E, Bas DF, Bilgen N, Caglar G et al (2015) Non-expert use of quantitative EEG displays for seizure identification in the adult neuro-intensive care unit. Epilepsy Res 109:48–56
Sackellares JC, Shiau DS, Halford JJ, LaRoche SM, Kelly KM (2011) Quantitative EEG analysis for automated detection of nonconvulsive seizures in intensive care units. Epilepsy Behav 22(Suppl 1):S69–S73
Freye E (2005) Cerebral monitoring in the operating room and the intensive care unit—an introductory for the clinician and a guide for the novice wanting to open a window to the brain. Part II: sensory-evoked potentials (SSEP, AEP, VEP). J Clin Monit Comput 19:77–168
Bein B (2006) Entropy. Best Pract Res Clin Anaesthesiol 20:101–109
Bischoff P, Schmidt G (2006) Monitoring methods: SNAP. Best Pract Res Clin Anaesthesiol 20:141–146
Drover D, Ortega HR (2006) Patient state index. Best Pract Res Clin Anaesthesiol 20:121–128
Hirsch LJ, LaRoche SM, Gaspard N, Gerard E, Svoronos A et al (2013) American Clinical Neurophysiology Society’s Standardized Critical Care EEG Terminology: 2012 version. J Clin Neurophysiol 30:1–27
Le Roux P, Menon DK, Citerio G, Vespa P, Bader MK et al (2014) The international multidisciplinary consensus conference on multimodality monitoring in neurocritical care: a list of recommendations and additional conclusions: a statement for healthcare professionals from the neurocritical care society and the European society of intensive care medicine. Neurocrit Care 21(Suppl 2):282–296
Synek VM (1988) Prognostically important EEG coma patterns in diffuse anoxic and traumatic encephalopathies in adults. J Clin Neurophysiol 5:161–174
Young GB, Bolton CF, Archibald YM, Austin TW, Wells GA (1992) The electroencephalogram in sepsis-associated encephalopathy. J Clin Neurophysiol 9:145–152
LeBlanc JM, Dasta JF, Kane-Gill SL (2006) Role of the bispectral index in sedation monitoring in the ICU. Ann Pharmacother 40:490–500
Theilen HJ, Ragaller M, Tscho U, May SA, Schackert G et al (2000) Electroencephalogram silence ratio for early outcome prognosis in severe head trauma. Crit Care Med 28:3522–3529
Oddo M, Carrera E, Claassen J, Mayer SA, Hirsch LJ (2009) Continuous electroencephalography in the medical intensive care unit. Crit Care Med 37:2051–2056
Kurtz P, Gaspard N, Wahl AS, Bauer RM, Hirsch LJ et al (2014) Continuous electroencephalography in a surgical intensive care unit. Intensive Care Med 40:228–234
Azabou E, Magalhaes E, Braconnier A, Yahiaoui L, Moneger G et al (2015) Early standard electroencephalogram abnormalities predict mortality in septic Intensive Care Unit patients. PLoS One 10:e0139969
Gilmore EJ, Gaspard N, Choi HA, Cohen E, Burkart KM et al (2015) Acute brain failure in severe sepsis: a prospective study in the medical intensive care unit utilizing continuous EEG monitoring. Intensive Care Med 41:686–694
Nuwer M (1997) Assessment of digital EEG, quantitative EEG, and EEG brain mapping: report of the American Academy of Neurology and the American Clinical Neurophysiology Society. Neurology 49:277–292
Thakor NV, Tong S (2004) Advances in quantitative electroencephalogram analysis methods. Annu Rev Biomed Eng 6:453–495
Haider HA, Esteller R, Hahn CD, Westover MB, Halford JJ et al (2016) Sensitivity of quantitative EEG for seizure identification in the intensive care unit. Neurology 87:935–944
Shepherd J, Jones J, Frampton G, Bryant J, Baxter L et al (2013) Clinical effectiveness and cost-effectiveness of depth of anaesthesia monitoring (E-Entropy, Bispectral Index and Narcotrend): a systematic review and economic evaluation. Health Technol Assess 17:1–264
Rathakrishnan R, Gotman J, Dubeau F, Angle M (2011) Using continuous electroencephalography in the management of delayed cerebral ischemia following subarachnoid hemorrhage. Neurocrit Care 14:152–161
Vespa PM, Nuwer MR, Juhasz C, Alexander M, Nenov V et al (1997) Early detection of vasospasm after acute subarachnoid hemorrhage using continuous EEG ICU monitoring. Electroencephalogr Clin Neurophysiol 103:607–615
Hebb MO, McArthur DL, Alger J, Etchepare M, Glenn TC et al (2007) Impaired percent alpha variability on continuous electroencephalography is associated with thalamic injury and predicts poor long-term outcome after human traumatic brain injury. J Neurotrauma 24:579–590
Vespa PM, Boscardin WJ, Hovda DA, McArthur DL, Nuwer MR et al (2002) Early and persistent impaired percent alpha variability on continuous electroencephalography monitoring as predictive of poor outcome after traumatic brain injury. J Neurosurg 97:84–92
Ma Y, Ouyang B, Guan X (2016) Use of quantitative electroencephalogram in patients with septic shock. Zhonghua Yi Xue Za Zhi 96:195–198
Azabou E, Fischer C, Mauguiere F, Vaugier I, Annane D, et al. (2015) Prospective Cohort Study Evaluating the Prognostic Value of Simple EEG Parameters in Postanoxic Coma. Clin EEG Neurosci
Gilmore EJ, Gaspard N, Choi HA, Cohen E, Burkart KM et al (2015) Acute brain failure in severe sepsis: a prospective study in the medical intensive care unit utilizing continuous EEG monitoring. Intensive Care Med 41:686–694
Hermans MC, Westover MB, van Putten MJ, Hirsch LJ, Gaspard N (2016) Quantification of EEG reactivity in comatose patients. Clin Neurophysiol 127:571–580
Yamada T (1988) The anatomic and physiologic bases of median nerve somatosensory evoked potentials. Neurol Clin 6:705–733
Kimura J, Ishida T, Suzuki S, Kudo Y, Matsuoka H et al (1986) Far-field recording of the junctional potential generated by median nerve volleys at the wrist. Neurology 36:1451–1457
Yamada T, Ishida T, Kudo Y, Rodnitzky RL, Kimura J (1986) Clinical correlates of abnormal P14 in median SEPs. Neurology 36:765–771
Yamada T, Kimura J, Nitz DM (1980) Short latency somatosensory evoked potentials following median nerve stimulation in man. Electroencephalogr Clin Neurophysiol 48:367–376
Mauguiere F, Grand C, Fischer C, Courjon J (1982) Aspects of early somatosensory and auditory evoked potentials in neurologic comas and brain death. Rev Electroencephalogr Neurophysiol Clin 12:280–285
Hashimoto I (1982) Auditory evoked potentials from the human midbrain: slow brain stem responses. Electroencephalogr Clin Neurophysiol 53:652–657
Kaseda Y, Tobimatsu S, Morioka T, Kato M (1991) Auditory middle-latency responses in patients with localized and non-localized lesions of the central nervous system. J Neurol 238:427–432
Luaute J, Fischer C, Adeleine P, Morlet D, Tell L et al (2005) Late auditory and event-related potentials can be useful to predict good functional outcome after coma. Arch Phys Med Rehabil 86:917–923
Fischer C, Morlet D, Bouchet P, Luaute J, Jourdan C et al (1999) Mismatch negativity and late auditory evoked potentials in comatose patients. Clin Neurophysiol 110:1601–1610
Yingling CD, Hosobuchi Y, Harrington M (1990) P300 as a predictor of recovery from coma. Lancet 336:873
Fischer C, Luaute J, Nemoz C, Morlet D, Kirkorian G et al (2006) Improved prediction of awakening or nonawakening from severe anoxic coma using tree-based classification analysis. Crit Care Med 34:1520–1524
Narayan RK, Greenberg RP, Miller JD, Enas GG, Choi SC et al (1981) Improved confidence of outcome prediction in severe head injury. A comparative analysis of the clinical examination, multimodality evoked potentials, CT scanning, and intracranial pressure. J Neurosurg 54:751–762
Fischer C, Morlet D, Luaute J (2004) Sensory and cognitive evoked potentials in the prognosis of coma. Suppl Clin Neurophysiol 57:656–661
Rappaport M, Hall K, Hopkins HK, Belleza T (1981) Evoked potentials and head injury. 1. Rating of evoked potential abnormality. Clin Electroencephalogr 12:154–166
Rappaport M, Hopkins HK, Hall K, Belleza T (1981) Evoked potentials and head injury. 2. Clinical applications. Clin Electroencephalogr 12:167–176
Caramia MD, Bernardi G, Zarola F, Rossini PM (1988) Neurophysiological evaluation of the central nervous impulse propagation in patients with sensorimotor disturbances. Electroencephalogr Clin Neurophysiol 70:16–25
Desmedt JE, Manil J, Borenstein S, Debecker J, Lambert C et al (1966) Evaluation of sensory nerve conduction from averaged cerebral evoked potentials in neuropathies. Electromyography 6:263–269
Parry GJ, Aminoff MJ (1987) Somatosensory evoked potentials in chronic acquired demyelinating peripheral neuropathy. Neurology 37:313–316
Rattay F, Potrusil T, Wenger C, Wise AK, Glueckert R et al (2013) Impact of morphometry, myelinization and synaptic current strength on spike conduction in human and cat spiral ganglion neurons. PLoS One 8:e79256
Klistorner A, Garrick R, Barnett MH, Graham SL, Arvind H et al (2013) Axonal loss in non-optic neuritis eyes of patients with multiple sclerosis linked to delayed visual evoked potential. Neurology 80:242–245
Walsh JC, Yiannikas C, McLeod JG (1984) Abnormalities of proximal conduction in acute idiopathic polyneuritis: comparison of short latency evoked potentials and F-waves. J Neurol Neurosurg Psychiatry 47:197–200
Amantini A, Grippo A, Fossi S, Cesaretti C, Piccioli A et al (2005) Prediction of ‘awakening’ and outcome in prolonged acute coma from severe traumatic brain injury: evidence for validity of short latency SEPs. Clin Neurophysiol 116:229–235
Zammit C, Knight WA (2013) Severe traumatic brain injury in adults. Emerg Med Pract 15:1–28
Sharshar T, Carlier R, Bernard F, Guidoux C, Brouland JP et al (2007) Brain lesions in septic shock: a magnetic resonance imaging study. Intensive Care Med 33:798–806
Sharshar T, Gray F, Poron F, Raphael JC, Gajdos P et al (2002) Multifocal necrotizing leukoencephalopathy in septic shock. Crit Care Med 30:2371–2375
Zauner C, Gendo A, Kramer L, Kranz A, Grimm G et al (2000) Metabolic encephalopathy in critically ill patients suffering from septic or nonseptic multiple organ failure. Crit Care Med 28:1310–1315
Meythaler JM, Peduzzi JD, Eleftheriou E, Novack TA (2001) Current concepts: diffuse axonal injury-associated traumatic brain injury. Arch Phys Med Rehabil 82:1461–1471
Mikacenic C, Hahn WO, Price BL, Harju-Baker S, Katz R et al (2015) Biomarkers of endothelial activation are associated with poor outcome in critical illness. PLoS One 10:e0141251
Latronico N, Bolton CF (2011) Critical illness polyneuropathy and myopathy: a major cause of muscle weakness and paralysis. Lancet Neurol 10:931–941
Latronico N, Fenzi F, Recupero D, Guarneri B, Tomelleri G et al (1996) Critical illness myopathy and neuropathy. Lancet 347:1579–1582
Zochodne DW, Bolton CF, Wells GA, Gilbert JJ, Hahn AF et al (1987) Critical illness polyneuropathy. A complication of sepsis and multiple organ failure. Brain 110(Pt 4):819–841
Presneill JJ, Waring PM, Layton JE, Maher DW, Cebon J et al (2000) Plasma granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor levels in critical illness including sepsis and septic shock: relation to disease severity, multiple organ dysfunction, and mortality. Crit Care Med 28:2344–2354
Walser H, Emre M, Janzer R (1986) Somatosensory evoked potentials in comatose patients: correlation with outcome and neuropathological findings. J Neurol 233:34–40
Bozza FA, D’Avila JC, Ritter C, Sonneville R, Sharshar T et al (2013) Bioenergetics, mitochondrial dysfunction, and oxidative stress in the pathophysiology of septic encephalopathy. Shock 39(Suppl 1):10–16
Le Gall JR, Lemeshow S, Saulnier F (1993) A new Simplified Acute Physiology Score (SAPS II) based on a European/North American multicenter study. JAMA 270:2957–2963
Polito A, Eischwald F, Maho AL, Azabou E, Annane D et al (2013) Pattern of brain injury in the acute setting of human septic shock. Crit Care 17:R204
Sharshar T, Bozza F, Chretien F (2014) Neuropathological processes in sepsis. Lancet Neurol 13:534–536
Sharshar T, Gray F, Lorin de la Grandmaison G, Hopkinson NS, Ross E et al (2003) Apoptosis of neurons in cardiovascular autonomic centres triggered by inducible nitric oxide synthase after death from septic shock. Lancet 362:1799–1805
Sonneville R, Vanhorebeek I, den Hertog HM, Chretien F, Annane D et al (2015) Critical illness-induced dysglycemia and the brain. Intensive Care Med 41:192–202
Sonneville R, Verdonk F, Rauturier C, Klein IF, Wolff M et al (2013) Understanding brain dysfunction in sepsis. Ann Intensive Care 3:15
Sutter R, Chalela JA, Leigh R, Kaplan PW, Yenokyan G et al (2015) Significance of parenchymal brain damage in patients with critical illness. Neurocrit Care 23:243–252
Kane NM, Curry SH, Butler SR, Cummins BH (1993) Electrophysiological indicator of awakening from coma. Lancet 341:688
Naccache L, Puybasset L, Gaillard R, Serve E, Willer JC (2005) Auditory mismatch negativity is a good predictor of awakening in comatose patients: a fast and reliable procedure. Clin Neurophysiol 116:988–989
Fossi S, Amantini A, Grippo A, Innocenti P, Amadori A et al (2006) Continuous EEG-SEP monitoring of severely brain injured patients in NICU: methods and feasibility. Neurophysiol Clin 36:195–205
Moulton R, Kresta P, Ramirez M, Tucker W (1991) Continuous automated monitoring of somatosensory evoked potentials in posttraumatic coma. J Trauma 31:676–683 (discussion 683–675)
Facco E, Munari M, Baratto F, Behr AU, Giron GP (1993) Multimodality evoked potentials (auditory, somatosensory and motor) in coma. Neurophysiol Clin 23:237–258
Guerit JM (1994) The interest of multimodality evoked potentials in the evaluation of chronic coma. Acta Neurol Belg 94:174–182
Guerit JM, de Tourtchaninoff M, Soveges L, Mahieu P (1993) The prognostic value of three-modality evoked potentials (TMEPs) in anoxic and traumatic comas. Neurophysiol Clin 23:209–226
Logi F, Fischer C, Murri L, Mauguiere F (2003) The prognostic value of evoked responses from primary somatosensory and auditory cortex in comatose patients. Clin Neurophysiol 114:1615–1627
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Azabou, E., Fischer, C., Guerit, J.M. et al. Neurophysiological assessment of brain dysfunction in critically ill patients: an update. Neurol Sci 38, 715–726 (2017). https://doi.org/10.1007/s10072-017-2824-x
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DOI: https://doi.org/10.1007/s10072-017-2824-x