Conventional and Investigational Approaches Leveraging Clinical EEG for Prognosis in Acute Disorders of Consciousness

William H. Curley; Angela Comanducci; Matteo Fecchio

doi:10.1055/s-0042-1755220

Seminars in Neurology, Table of Contents

Semin Neurol 2022; 42(03): 309-324
DOI: 10.1055/s-0042-1755220

Review Article

Conventional and Investigational Approaches Leveraging Clinical EEG for Prognosis in Acute Disorders of Consciousness

Authors

William H. Curley

¹Harvard Medical School, Boston, Massachusetts

²Department of Neurology, Center for Neurotechnology and Neurorecovery, Massachusetts General Hospital, Boston, Massachusetts
Angela Comanducci

³IRCSS Fondazione Don Carlo Gnocchi ONLUS, Milan, Italy

⁴Università Campus Bio-Medico di Roma, Rome, Italy
Matteo Fecchio

²Department of Neurology, Center for Neurotechnology and Neurorecovery, Massachusetts General Hospital, Boston, Massachusetts

Abstract

Prediction of recovery of consciousness after severe brain injury is difficult and limited by a lack of reliable, standardized biomarkers. Multiple approaches for analysis of clinical electroencephalography (EEG) that shed light on prognosis in acute severe brain injury have emerged in recent years. These approaches fall into two major categories: conventional characterization of EEG background and quantitative measurement of resting state or stimulus-induced EEG activity. Additionally, a small number of studies have associated the presence of electrophysiologic sleep features with prognosis in the acute phase of severe brain injury. In this review, we focus on approaches for the analysis of clinical EEG that have prognostic significance and that could be readily implemented with minimal additional equipment in clinical settings, such as intensive care and intensive rehabilitation units, for patients with acute disorders of consciousness.

Keywords

EEG - acute brain injury - disorders of consciousness - prognosis - coma

Full Text

References

References
1 Maas AIR, Menon DK, Adelson PD. et al; InTBIR Participants and Investigators. Traumatic brain injury: integrated approaches to improve prevention, clinical care, and research. Lancet Neurol 2017; 16 (12) 987-1048
2 NIH Consensus Development Panel on Rehabilitation of Persons With Traumatic Brain Injury. Consensus conference. Rehabilitation of persons with traumatic brain injury. JAMA 1999; 282 (10) 974-983
3 Fins JJ. Being conscious of their burden: severe brain injury and the two cultures challenge. Ann N Y Acad Sci 2009; 1157: 131-147
4 Nguyen KPL, Pai V, Rashid S, Treece J, Moulton M, Baumrucker SJ. Prognostication in anoxic brain injury. Am J Hosp Palliat Care 2018; 35 (11) 1446-1455
5 Thomassen A, Wernberg M. Prevalence and prognostic significance of coma after cardiac arrest outside intensive care and coronary units. Acta Anaesthesiol Scand 1979; 23 (02) 143-148
6 Laver S, Farrow C, Turner D, Nolan J. Mode of death after admission to an intensive care unit following cardiac arrest. Intensive Care Med 2004; 30 (11) 2126-2128
7 Dragancea I, Rundgren M, Englund E, Friberg H, Cronberg T. The influence of induced hypothermia and delayed prognostication on the mode of death after cardiac arrest. Resuscitation 2013; 84 (03) 337-342
8 Turgeon AF, Lauzier F, Simard JF. et al; Canadian Critical Care Trials Group. Mortality associated with withdrawal of life-sustaining therapy for patients with severe traumatic brain injury: a Canadian multicentre cohort study. CMAJ 2011; 183 (14) 1581-1588
9 Fins JJ, Schiff ND, Foley KM. Late recovery from the minimally conscious state: ethical and policy implications. Neurology 2007; 68 (04) 304-307
10 Fins JJ. Rights Come to Mind: Brain Injury, Ethics, and the Struggle for Consciousness. New York, NY: Cambridge University Press; 2015
11 Giacino JT, Fins JJ, Laureys S, Schiff ND. Disorders of consciousness after acquired brain injury: the state of the science. Nat Rev Neurol 2014; 10 (02) 99-114
12 Edlow BL, Fins JJ. Assessment of covert consciousness in the intensive care unit: clinical and ethical considerations. J Head Trauma Rehabil 2018; 33 (06) 424-434
13 Pisa FE, Biasutti E, Drigo D, Barbone F. The prevalence of vegetative and minimally conscious states: a systematic review and methodological appraisal. J Head Trauma Rehabil 2014; 29 (04) E23-E30
14 van Erp WS, Lavrijsen JC, van de Laar FA, Vos PE, Laureys S, Koopmans RT. The vegetative state/unresponsive wakefulness syndrome: a systematic review of prevalence studies. Eur J Neurol 2014; 21 (11) 1361-1368
15 Chakraborty R, El-Jawahri AR, Litzow MR, Syrjala KL, Parnes AD, Hashmi SK. A systematic review of religious beliefs about major end-of-life issues in the five major world religions. Palliat Support Care 2017; 15 (05) 609-622
16 Laureys S, Celesia GG, Cohadon F. et al; European Task Force on Disorders of Consciousness. Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med 2010; 8: 68
17 Kobylarz EJ, Schiff ND. Neurophysiological correlates of persistent vegetative and minimally conscious states. Neuropsychol Rehabil 2005; 15 (3-4): 323-332
18 Giacino JT, Ashwal S, Childs N. et al. The minimally conscious state: definition and diagnostic criteria. Neurology 2002; 58 (03) 349-353
19 Bruno MA, Vanhaudenhuyse A, Thibaut A, Moonen G, Laureys S. From unresponsive wakefulness to minimally conscious PLUS and functional locked-in syndromes: recent advances in our understanding of disorders of consciousness. J Neurol 2011; 258 (07) 1373-1384
20 Naccache L. Minimally conscious state or cortically mediated state?. Brain 2018; 141 (04) 949-960
21 Giacino J, Whyte J. The vegetative and minimally conscious states: current knowledge and remaining questions. J Head Trauma Rehabil 2005; 20 (01) 30-50
22 Sherer M, Katz DI, Bodien YG. et al. Post-traumatic confusional state: a case definition and diagnostic criteria. Arch Phys Med Rehabil 2020; 101 (11) 2041-2050
23 Schiff ND. Cognitive motor dissociation following severe brain injuries. JAMA Neurol 2015; 72 (12) 1413-1415
24 Edlow BL, Chatelle C, Spencer CA. et al. Early detection of consciousness in patients with acute severe traumatic brain injury. Brain 2017; 140 (09) 2399-2414
25 Edlow BL, Claassen J, Schiff ND, Greer DM. Recovery from disorders of consciousness: mechanisms, prognosis and emerging therapies. Nat Rev Neurol 2021; 17 (03) 135-156
26 Gosseries O, Zasler ND, Laureys S. Recent advances in disorders of consciousness: focus on the diagnosis. Brain Inj 2014; 28 (09) 1141-1150
27 Thibaut A, Panda R, Annen J. et al. Preservation of brain activity in unresponsive patients identifies MCS star. Ann Neurol 2021; 90 (01) 89-100
28 Schiff ND. Recovery of consciousness after brain injury: a mesocircuit hypothesis. Trends Neurosci 2010; 33 (01) 1-9
29 Schnakers C, Vanhaudenhuyse A, Giacino J. et al. Diagnostic accuracy of the vegetative and minimally conscious state: clinical consensus versus standardized neurobehavioral assessment. BMC Neurol 2009; 9: 35
30 Wutzl B, Golaszewski SM, Leibnitz K. et al. Narrative review: quantitative EEG in disorders of consciousness. Brain Sci 2021; 11 (06) 11
31 Pauli R, O'Donnell A, Cruse D. Resting-state electroencephalography for prognosis in disorders of consciousness following traumatic brain injury. Front Neurol 2020; 11: 586945
32 Fidali BC, Stevens RD, Claassen J. Novel approaches to prediction in severe brain injury. Curr Opin Neurol 2020; 33 (06) 669-675
33 Van der Lande GJM, Blume C, Annen J. Sleep and circadian disturbance in disorders of consciousness: current methods and the way towards clinical implementation. Semin Neurol 2022; [online ahead of print]
34 Giacino JT, Katz DI, Schiff ND. et al. 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 2018; 91 (10) 450-460
35 Kondziella D, Bender A, Diserens K. et al; EAN Panel on Coma, Disorders of Consciousness. European Academy of Neurology guideline on the diagnosis of coma and other disorders of consciousness. Eur J Neurol 2020; 27 (05) 741-756
36 Comanducci A, Boly M, Claassen J. et al. Clinical and advanced neurophysiology in the prognostic and diagnostic evaluation of disorders of consciousness: review of an IFCN-endorsed expert group. Clin Neurophysiol 2020; 131 (11) 2736-2765
37 Rossetti AO. Clinical neurophysiology for neurological prognostication of comatose patients after cardiac arrest. Clin Neurophysiol Pract 2017; 2: 76-80
38 Hockaday JM, Potts F, Epstein E, Bonazzi A, Schwab RS. Electroencephalographic changes in acute cerebral anoxia from cardiac or respiratory arrest. Electroencephalogr Clin Neurophysiol 1965; 18: 575-586
39 Synek VM. Prognostically important EEG coma patterns in diffuse anoxic and traumatic encephalopathies in adults. J Clin Neurophysiol 1988; 5 (02) 161-174
40 Synek VM. Revised EEG coma scale in diffuse acute head injuries in adults. Clin Exp Neurol 1990; 27: 99-111
41 Bagnato S, Boccagni C, Prestandrea C, Sant'Angelo A, Castiglione A, Galardi G. Prognostic value of standard EEG in traumatic and non-traumatic disorders of consciousness following coma. Clin Neurophysiol 2010; 121 (03) 274-280
42 Boccagni C, Bagnato S, Sant Angelo A, Prestandrea C, Galardi G. Usefulness of standard EEG in predicting the outcome of patients with disorders of consciousness after anoxic coma. J Clin Neurophysiol 2011; 28 (05) 489-492
43 Estraneo A, Moretta P, Loreto V. et al. Predictors of recovery of responsiveness in prolonged anoxic vegetative state. Neurology 2013; 80 (05) 464-470
44 Rae-Grant AD, Barbour PJ, Reed J. Development of a novel EEG rating scale for head injury using dichotomous variables. Electroencephalogr Clin Neurophysiol 1991; 79 (05) 349-357
45 Bagnato S, Boccagni C, Sant'Angelo A, Prestandrea C, Mazzilli R, Galardi G. EEG predictors of outcome in patients with disorders of consciousness admitted for intensive rehabilitation. Clin Neurophysiol 2015; 126 (05) 959-966
46 Young GB, McLachlan RS, Kreeft JH, Demelo JD. An electroencephalographic classification for coma. Can J Neurol Sci 1997; 24 (04) 320-325
47 Müller M, Rossetti AO, Zimmermann R. et al. Standardized visual EEG features predict outcome in patients with acute consciousness impairment of various etiologies. Crit Care 2020; 24 (01) 680
48 Logi F, Pasqualetti P, Tomaiuolo F. Predict recovery of consciousness in post-acute severe brain injury: the role of EEG reactivity. Brain Inj 2011; 25 (10) 972-979
49 Cavinato M, Freo U, Ori C. et al. Post-acute P300 predicts recovery of consciousness from traumatic vegetative state. Brain Inj 2009; 23 (12) 973-980
50 Gütling E, Gonser A, Imhof HG, Landis T. EEG reactivity in the prognosis of severe head injury. Neurology 1995; 45 (05) 915-918
51 Estraneo A, Fiorenza S, Magliacano A. et al; IBIA DoC-SIG. Multicenter prospective study on predictors of short-term outcome in disorders of consciousness. Neurology 2020; 95 (11) e1488-e1499
52 Alvarez V, Sierra-Marcos A, Oddo M, Rossetti AO. Yield of intermittent versus continuous EEG in comatose survivors of cardiac arrest treated with hypothermia. Crit Care 2013; 17 (05) R190
53 Admiraal MM, van Rootselaar AF, Hofmeijer J. et al. Electroencephalographic reactivity as predictor of neurological outcome in postanoxic coma: a multicenter prospective cohort study. Ann Neurol 2019; 86 (01) 17-27
54 Cloostermans MC, van Meulen FB, Eertman CJ, Hom HW, van Putten MJ. Continuous electroencephalography monitoring for early prediction of neurological outcome in postanoxic patients after cardiac arrest: a prospective cohort study. Crit Care Med 2012; 40 (10) 2867-2875
55 Rossetti AO, Carrera E, Oddo M. Early EEG correlates of neuronal injury after brain anoxia. Neurology 2012; 78 (11) 796-802
56 Hofmeijer J, Tjepkema-Cloostermans MC, van Putten MJ. Burst-suppression with identical bursts: a distinct EEG pattern with poor outcome in postanoxic coma. Clin Neurophysiol 2014; 125 (05) 947-954
57 Becker DA, Schiff ND, Becker LB. et al. A major miss in prognostication after cardiac arrest: burst suppression and brain healing. Epilepsy Behav Case Rep 2016; 7: 1-5
58 Hofmeijer J, Beernink TM, Bosch FH, Beishuizen A, Tjepkema-Cloostermans MC, van Putten MJ. Early EEG contributes to multimodal outcome prediction of postanoxic coma. Neurology 2015; 85 (02) 137-143
59 Bagnato S, Boccagni C, Sant'Angelo A, Prestandrea C, Virgilio V, Galardi G. EEG epileptiform abnormalities at admission to a rehabilitation department predict the risk of seizures in disorders of consciousness following a coma. Epilepsy Behav 2016; 56: 83-87
60 Pascarella A, Trojano L, Loreto V, Bilo L, Moretta P, Estraneo A. Long-term outcome of patients with disorders of consciousness with and without epileptiform activity and seizures: a prospective single centre cohort study. J Neurol 2016; 263 (10) 2048-2056
61 Fierain A, Gaspard N, Lejeune N. et al. Beware of nonconvulsive seizures in prolonged disorders of consciousness: long-term EEG monitoring is the key. Clin Neurophysiol 2022; 136: 228-234
62 Hesdorffer DC, Benn EK, Cascino GD, Hauser WA. Is a first acute symptomatic seizure epilepsy? Mortality and risk for recurrent seizure. Epilepsia 2009; 50 (05) 1102-1108
63 Vespa PM, Miller C, McArthur D. et al. Nonconvulsive electrographic seizures after traumatic brain injury result in a delayed, prolonged increase in intracranial pressure and metabolic crisis. Crit Care Med 2007; 35 (12) 2830-2836
64 Dennis LJ, Claassen J, Hirsch LJ, Emerson RG, Connolly ES, Mayer SA. Nonconvulsive status epilepticus after subarachnoid hemorrhage. Neurosurgery 2002; 51 (05) 1136-1143 , discussion 1144
65 Passero S, Rocchi R, Rossi S, Ulivelli M, Vatti G. Seizures after spontaneous supratentorial intracerebral hemorrhage. Epilepsia 2002; 43 (10) 1175-1180
66 Westhall E, Rosén I, Rundgren M. et al. Time to epileptiform activity and EEG background recovery are independent predictors after cardiac arrest. Clin Neurophysiol 2018; 129 (08) 1660-1668
67 Ruijter BJ, Tjepkema-Cloostermans MC, Tromp SC. et al. Early electroencephalography for outcome prediction of postanoxic coma: a prospective cohort study. Ann Neurol 2019; 86 (02) 203-214
68 Rossetti AO, Oddo M, Liaudet L, Kaplan PW. Predictors of awakening from postanoxic status epilepticus after therapeutic hypothermia. Neurology 2009; 72 (08) 744-749
69 Barbella G, Lee JW, Alvarez V. et al. Prediction of regaining consciousness despite an early epileptiform EEG after cardiac arrest. Neurology 2020; 94 (16) e1675-e1683
70 Curley WH, Forgacs PB, Voss HU, Conte MM, Schiff ND. Characterization of EEG signals revealing covert cognition in the injured brain. Brain 2018; 141 (05) 1404-1421
71 Schiff ND, Giacino JT, Kalmar K. et al. Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 2007; 448 (7153): 600-603
72 Williams ST, Conte MM, Goldfine AM. et al. Common resting brain dynamics indicate a possible mechanism underlying zolpidem response in severe brain injury. eLife 2013; 2: e01157
73 Gibson RM, Fernández-Espejo D, Gonzalez-Lara LE. et al. Multiple tasks and neuroimaging modalities increase the likelihood of detecting covert awareness in patients with disorders of consciousness. Front Hum Neurosci 2014; 8: 950
74 Wannez S, Heine L, Thonnard M, Gosseries O, Laureys S. Coma Science Group collaborators. The repetition of behavioral assessments in diagnosis of disorders of consciousness. Ann Neurol 2017; 81 (06) 883-889
75 Piarulli A, Bergamasco M, Thibaut A, Cologan V, Gosseries O, Laureys S. EEG ultradian rhythmicity differences in disorders of consciousness during wakefulness. J Neurol 2016; 263 (09) 1746-1760
76 Vespa PM, Boscardin WJ, Hovda DA. et al. Early and persistent impaired percent alpha variability on continuous electroencephalography monitoring as predictive of poor outcome after traumatic brain injury. J Neurosurg 2002; 97 (01) 84-92
77 Hebb MO, McArthur DL, Alger J. et al. 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 2007; 24 (04) 579-590
78 Tolonen A, Särkelä MOK, Takala RSK. et al. Quantitative EEG parameters for prediction of outcome in severe traumatic brain injury: development study. Clin EEG Neurosci 2018; 49 (04) 248-257
79 O'Donnell A, Pauli R, Banellis L. et al. The prognostic value of resting-state EEG in acute post-traumatic unresponsive states. Brain Commun 2021; 3 (02) b017
80 Kustermann T, Ata Nguepnjo Nguissi N, Pfeiffer C. et al. Brain functional connectivity during the first day of coma reflects long-term outcome. Neuroimage Clin 2020; 27: 102295
81 Schiff ND. Mesocircuit mechanisms underlying recovery of consciousness following severe brain injuries: model and predictions. In: Monti M, Sannita W. eds. Brain Function and Responsiveness in Disorders of Consciousness. Switzerland: Springer International Publishing; 2016
82 Fridman EA, Beattie BJ, Broft A, Laureys S, Schiff ND. Regional cerebral metabolic patterns demonstrate the role of anterior forebrain mesocircuit dysfunction in the severely injured brain. Proc Natl Acad Sci U S A 2014; 111 (17) 6473-6478
83 Lutkenhoff ES, Chiang J, Tshibanda L. et al. Thalamic and extrathalamic mechanisms of consciousness after severe brain injury. Ann Neurol 2015; 78 (01) 68-76
84 Coulborn S, Taylor C, Naci L, Owen AM, Fernández-Espejo D. Disruptions in effective connectivity within and between default mode network and anterior forebrain mesocircuit in prolonged disorders of consciousness. Brain Sci 2021; 11 (06) 11
85 Fischer DB, Boes AD, Demertzi A. et al. A human brain network derived from coma-causing brainstem lesions. Neurology 2016; 87 (23) 2427-2434
86 Forgacs PB, Frey H-P, Velazquez A. et al. Dynamic regimes of neocortical activity linked to corticothalamic integrity correlate with outcomes in acute anoxic brain injury after cardiac arrest. Ann Clin Transl Neurol 2017; 4 (02) 119-129
87 Forgacs PB, Allen BB, Wu X. et al. Corticothalamic connectivity in aneurysmal subarachnoid hemorrhage: relationship with disordered consciousness and clinical outcomes. Neurocrit Care 2022; 36 (03) 760-771
88 Frohlich J, Crone JS, Johnson MA. et al. Neural oscillations track recovery of consciousness in acute traumatic brain injury patients. Hum Brain Mapp 2022; 43 (06) 1804-1820
89 Alkhachroum A, Eliseyev A, Der-Nigoghossian CA. et al. EEG to detect early recovery of consciousness in amantadine-treated acute brain injury patients. J Neurol Neurosurg Psychiatry 2020; 91 (06) 675-676
90 Curley WH, Bodien YG, Zhou DW. et al. Electrophysiological correlates of thalamocortical function in acute severe traumatic brain injury. Cortex 2022; 152: 136-152
91 Owen AM, Coleman MR, Boly M, Davis MH, Laureys S, Pickard JD. Detecting awareness in the vegetative state. Science 2006; 313 (5792): 1402
92 Cruse D, Chennu S, Chatelle C. et al. Bedside detection of awareness in the vegetative state: a cohort study. Lancet 2011; 378 (9809): 2088-2094
93 Goldfine AM, Victor JD, Conte MM, Bardin JC, Schiff ND. Determination of awareness in patients with severe brain injury using EEG power spectral analysis. Clin Neurophysiol 2011; 122 (11) 2157-2168
94 Goldfine AM, Bardin JC, Noirhomme Q, Fins JJ, Schiff ND, Victor JD. Reanalysis of “Bedside detection of awareness in the vegetative state: a cohort study”. Lancet 2013; 381 (9863): 289-291
95 Schiff ND. Uncovering hidden integrative cerebral function in the intensive care unit. Brain 2017; 140 (09) 2259-2262
96 Claassen J, Doyle K, Matory A. et al. Detection of brain activation in unresponsive patients with acute brain injury. N Engl J Med 2019; 380 (26) 2497-2505
97 Iotzov I, Fidali BC, Petroni A, Conte MM, Schiff ND, Parra LC. Divergent neural responses to narrative speech in disorders of consciousness. Ann Clin Transl Neurol 2017; 4 (11) 784-792
98 Braiman C, Fridman EA, Conte MM. et al. Cortical response to the natural speech envelope correlates with neuroimaging evidence of cognition in severe brain injury. Curr Biol 2018; 28 (23) 3833-3839.e3
99 Chatelle C, Rosenthal ES, Bodien YG, Spencer-Salmon CA, Giacino JT, Edlow BL. EEG correlates of language function in traumatic disorders of consciousness. Neurocrit Care 2020; 33 (02) 449-457
100 Sokoliuk R, Degano G, Banellis L. et al. Covert speech comprehension predicts recovery from acute unresponsive states. Ann Neurol 2021; 89 (04) 646-656
101 Edlow BL, Naccache L. Unmasking covert language processing in the intensive care unit with electroencephalography. Ann Neurol 2021; 89 (04) 643-645
102 Chatelle C, Spencer CA, Cash SS, Hochberg LR, Edlow BL. Feasibility of an EEG-based brain-computer interface in the intensive care unit. Clin Neurophysiol 2018; 129 (08) 1519-1525
103 Royal College of Physicians. Prolonged Disorders of Consciousness following Sudden Onset Brain Injury. National Clinical Guidelines. London: Royal College of Physicians; 2020
104 Scolding N, Owen AM, Keown J. Prolonged disorders of consciousness: a critical evaluation of the new UK guidelines. Brain 2021; 144 (06) 1655-1660
105 Menon DK, Chennu S. Inverting the Turing test - machine learning to detect cognition in the ICU. N Engl J Med 2019; 380 (26) 2575-2576
106 Evans BM, Bartlett JR. Prediction of outcome in severe head injury based on recognition of sleep related activity in the polygraphic electroencephalogram. J Neurol Neurosurg Psychiatry 1995; 59 (01) 17-25
107 Valente M, Placidi F, Oliveira AJ. et al. Sleep organization pattern as a prognostic marker at the subacute stage of post-traumatic coma. Clin Neurophysiol 2002; 113 (11) 1798-1805
108 Yang XA, Song CG, Yuan F. et al. Prognostic roles of sleep electroencephalography pattern and circadian rhythm biomarkers in the recovery of consciousness in patients with coma: a prospective cohort study. Sleep Med 2020; 69: 204-212
109 Cologan V, Schabus M, Ledoux D, Moonen G, Maquet P, Laureys S. Sleep in disorders of consciousness. Sleep Med Rev 2010; 14 (02) 97-105
110 Cologan V, Drouot X, Parapatics S. et al. Sleep in the unresponsive wakefulness syndrome and minimally conscious state. J Neurotrauma 2013; 30 (05) 339-346
111 Rossi Sebastiano D, Visani E, Panzica F. et al. Sleep patterns associated with the severity of impairment in a large cohort of patients with chronic disorders of consciousness. Clin Neurophysiol 2018; 129 (03) 687-693
112 Gottshall JL, Rossi Sebastiano D. Sleep in disorders of consciousness: diagnostic, prognostic, and therapeutic considerations. Curr Opin Neurol 2020; 33 (06) 684-690
113 Bai Y, Lin Y, Ziemann U. Managing disorders of consciousness: the role of electroencephalography. J Neurol 2021; 268 (11) 4033-4065
114 Pan J, Wu J, Liu J, Wu J, Wang F. A systematic review of sleep in patients with disorders of consciousness: from diagnosis to prognosis. Brain Sci 2021; 11 (08) 11
115 Rossi Sebastiano D, Varotto G, Sattin D, Franceschetti S. EEG assessment in patients with disorders of consciousness: aims, advantages, limits, and pitfalls. Front Neurol 2021; 12: 649849
116 Snider SB, Kowalski RG, Hammond F. et al. Comparison of common outcome measures for assessing independence in patients diagnosed with disorders of consciousness: a traumatic brain injury model systems study. medRxiv. 2022
117 Young GB, Blume WT, Campbell VM. et al. Alpha, theta and alpha-theta coma: a clinical outcome study utilizing serial recordings. Electroencephalogr Clin Neurophysiol 1994; 91 (02) 93-99