EEG Correlates of Language Function in Traumatic Disorders of Consciousness

[en] Background/Objective: Behavioral examinations may fail to detect language function in patients with severe traumatic brain injury (TBI) due to confounds such as having an endotracheal tube. We investigated whether resting and stimulus-evoked electroencephalography (EEG) methods detect the presence of language function in patients with severe TBI. Methods: Four EEG measures were assessed: (1) resting background (applying Forgacs’ criteria), (2) reactivity to speech, (3) background and reactivity (applying Synek’s criteria); and (4) an automated support vector machine (classifier for speech versus rest). Cohen’s kappa measured agreement between the four EEG measures and evidence of language function on a behavioral coma recovery scale-revised (CRS-R) and composite (CRS-R or functional MRI) reference standard. Sensitivity and specificity of each EEG measure were calculated against the reference standards. Results: We enrolled 17 adult patients with severe TBI (mean ± SD age 27.0 ± 7.0 years; median [range] 11.5 [2–1173] days post-injury) and 16 healthy subjects (age 28.5 ± 7.8 years). The classifier, followed by Forgacs’ criteria for resting background, demonstrated the highest agreement with the behavioral reference standard. Only Synek’s criteria for background and reactivity showed significant agreement with the composite reference standard. The classifier and resting background showed balanced sensitivity and specificity for behavioral (sensitivity = 84.6% and 80.8%; specificity = 57.1% for both) and composite reference standards (sensitivity = 79.3% and 75.9%, specificity = 50% for both). Conclusions: Methods applying an automated classifier, resting background, or resting background with reactivity may identify severe TBI patients with preserved language function. Automated classifier methods may enable unbiased and efficient assessment of larger populations or serial timepoints, while qualitative visual methods may be practical in community settings. © 2020, Springer Science+Business Media, LLC, part of Springer Nature and Neurocritical Care Society.

Disciplines :

Neurosciences & behavior

Author, co-author :

Chatelle, Camille ; Université de Liège - ULiège

Rosenthal, E. S.; Center for Neurotechnology and Neurorecovery, Massachusetts General Hospital, Boston, MA, United States, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, United States, Clinical Data Animation Center, Massachusetts General Hospital, Boston, MA, United States

Bodien, Y. G.; Center for Neurotechnology and Neurorecovery, Massachusetts General Hospital, Boston, MA, United States, Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Boston, MA, United States

Spencer-Salmon, C. A.; Center for Neurotechnology and Neurorecovery, Massachusetts General Hospital, Boston, MA, United States

Giacino, J. T.; Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Boston, MA, United States

Edlow, B. L.; Center for Neurotechnology and Neurorecovery, Massachusetts General Hospital, Boston, MA, United States, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Boston, MA, United States

Language :

English

Title :

EEG Correlates of Language Function in Traumatic Disorders of Consciousness

Publication date :

2020

Journal title :

Neurocritical Care

ISSN :

1541-6933

eISSN :

1556-0961

Publisher :

Springer

Peer reviewed :

Peer Reviewed verified by ORBi

Name of the research project :

Wallonie Bruxelles International Excellence Scholarship Program

Funders :

NINDS - National Institute of Neurological Disorders and Stroke
AAN - American Academy of Neurology
ABF - American Brain Foundation
JSMF - James S McDonnell Foundation
Rappaport Foundation
Tiny Blue Dot Foundation
BAEF - Belgian American Educational Foundation
EC - European Commission

Funding text :

The authors thank the nursing staffs of the Massachusetts General Hospital Neurosciences ICU, Multidisciplinary ICU, and the Surgical ICU. We also thank Joseph Cohen and the EEG technologists, as well as Kellie Cahill and the MRI technologists for their assistance with data acquisition. We are grateful to the patients and families in this study for their participation and support. The study was funded by the NIH National Institute of Neurological Disorders and Stroke (K23NS094538, K23NS105950, R21NS109627, RF1NS115268), NIH Director’s Office (DP2HD101400), American Academy of Neurology/American Brain Foundation, James S. McDonnell Foundation, Rappaport Foundation, Tiny Blue Dot Foundation, The Belgian American Educational Foundation, Wallonie Bruxelles International Excellence Scholarship Program and the European Commission (H2020-MSCA-IF-2016-ADOC-752686). The authors report no disclosures.

Available on ORBi :

since 30 August 2020

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Bibliography

Luaute J, Maucort-Boulch D, Tell L, et al. Long-term outcomes of chronic minimally conscious and vegetative states. Neurology. 2010;75(3):246–52.
Erler KS, Whiteneck GG, Juengst SB, et al. Predicting the trajectory of participation after traumatic brain injury: a longitudinal analysis. J Head Trauma Rehabil. 2018;33(4):257–65.
Whyte J, Gosseries O, Chervoneva I, et al. Predictors of short-term outcome in brain-injured patients with disorders of consciousness. Prog Brain Res. 2009;177(4):257–65.
Giacino JT, Kalmar K. The vegetative and minimally conscious states: a comparison of clinical features and functional outcome. J Head Trauma Rehabil 1997;12(4). https://journals.lww.com/headtraumarehab/Fulltext/1997/08000/The-Vegetative-and-Minimally-Conscious-States-A.5.aspx.
Bodien YG, Carlowicz CA, Chatelle C, Giacino JT. Sensitivity and specificity of the coma recovery scale-revised total score in detection of conscious awareness. Arch Phys Med Rehabil. 2016;97(3):490–2.
Gill-Thwaites H. Lotteries, loopholes and luck: misdiagnosis in the vegetative state patient. Brain Inj. 2006;20(13–14):1321–8.
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.
Stender J, Gosseries O, Bruno M-A, et al. Diagnostic precision of PET imaging and functional MRI in disorders of consciousness: a clinical validation study. Lancet. 2014;384(9942):514–22.
Andrews K, Murphy L, Munday R, Littlewood C. Misdiagnosis of the vegetative state: retrospective study in a rehabilitation unit. BMJ. 1996;313(7048):13–6.
Teasdale G, Jennett B. Assessment of coma and impaired consciousness. Lancet Neurol. 1974;304:81–4.
Wijdicks EFM, Bamlet WR, Maramattom BV, Manno EM, McClelland RL. Validation of a new coma scale: the FOUR score. Ann Neurol. 2005;58(4):585–93.
Wannez S, Heine L, Thonnard M, Gosseries O, Laureys S. The repetition of behavioral assessments in diagnosis of disorders of consciousness. Ann Neurol. 2017;81(6):883–9.
Cruse D, Chennu S, Chatelle C, et al. Bedside detection of awareness in the vegetative state: a cohort study. Lancet. 2011;378(9809):2088–94.
Monti MM, Vanhaudenhuyse A, Coleman MR, et al. Willful modulation of brain activity in disorders of consciousness. N Engl J Med. 2010;362(7):579–89.
Owen AM, Coleman MR, Boly M, Davis MH, Laureys S, Pickard JD. Detecting awareness in the vegetative state. Science. 2006;313(5792):1402.
Giacino JT, Katz DI, Schiff ND, et al. Comprehensive systematic review update 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. Neurology. 2018;91(10):450–60.
Rohaut B, Eliseyev A, Claassen J. Uncovering consciousness in unresponsive ICU patients: technical, medical and ethical considerations. Crit Care. 2019;23:78.
Schiff ND. Cognitive motor dissociation following severe brain injuries. JAMA Neurol. 2015;72(12):1413–5.
Cruse D, Chennu S, Chatelle C, et al. Relationship between etiology and covert cognition in the minimally conscious state. Neurology. 2012;78(11):816–22.
Edlow BL, Chatelle C, Spencer CA, et al. Early detection of consciousness in patients with acute severe traumatic brain injury. Brain. 2017;140(9):2399–414.
Bodien YG, Giacino JT, Edlow BL. Functional MRI motor imagery tasks to detect command following in traumatic disorders of consciousness. Front Neurol. 2017;8:688.
Claassen J, Doyle K, Matory A, et al. Detection of brain activation in unresponsive patients with acute brain injury. N Engl J Med. 2019;26:2497–505.
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):3833–9.
Coleman MR, Davis MH, Rodd JM, et al. Towards the routine use of brain imaging to aid the clinical diagnosis of disorders of consciousness. Brain. 2009;132(Pt 9):2541–52.
Gosseries O, Zasler ND, Laureys S. Recent advances in disorders of consciousness: focus on the diagnosis. Brain Inj. 2014;28(9):1141–50.
Stender J, Kupers R, Rodell A, et al. Quantitative rates of brain glucose metabolism distinguish minimally conscious from vegetative state patients. J Cereb Blood Flow Metab. 2015;35(1):58–65.
Forgacs PB, Conte MM, Fridman EA, Voss HU, Victor JD, Schiff ND. Preservation of electroencephalographic organization in patients with impaired consciousness and imaging-based evidence of command-following. Ann Neurol. 2014;76(6):869–79.
Engemann DA, Raimondo F, King J-R, et al. Robust EEG-based cross-site and cross-protocol classification of states of consciousness. Brain. 2018;141(11):3179–92.
Stender J, Mortensen KN, Thibaut A, et al. The minimal energetic requirement of sustained awareness after brain injury. Curr Biol. 2016;26(11):1494–9.
Curley WH, Forgacs PB, Voss HU, Conte MM, Schiff ND. Characterization of EEG signals revealing covert cognition in the injured brain. Brain. 2018;141(5):1404–21.
Edlow BL, Chatelle C, Spencer CA, et al. Early detection of consciousness in patients with acute severe traumatic brain injury. Brain. 2017;140(1):23–31.
American Clinical Neurophysiology Society. Guideline 7: guidelines for writing EEG reports. J Clin Neurophysiol. 2006;23(2):118–21.
Synek VM. Prognostically important EEG coma patterns in diffuse anoxic and traumatic encephalopathies in adults. J Clin Neurophysiol. 1988;5(2):161–74.
Bagnato S, Boccagni C, Prestandrea C, Sant’Angelo A, Castiglione A, Galardi G. Prognostic value of standard. Clin Neurophysiol. 2010;121(3):274–80.
Noirhomme Q, Brecheisen R, Lesenfants D, Antonopoulos G, Laureys S. “Look at my classifier’s result”: disentangling unresponsive from (minimally) conscious patients. Neuroimage. 2017;145:288–303.
Schnakers C, Edlow BL, Chatelle C, Giacino JT. Minimally conscious state. In: The Neurology of Conciousness. 2016.
Stuss DT, Binns MA, Carruth FG, et al. The acute period of recovery from traumatic brain injury: posttraumatic amnesia or posttraumatic confusional state? J Neurosurg. 1999;90(4):635–43.
Alberg AJ, Park JW, Hager BW, Brock MV, Diener-West M. The use of “overall accuracy” to evaluate the validity of screening or diagnostic tests. J Gen Intern Med. 2004;19:460–5.
Schnakers C, Perrin F, Schabus M, et al. Voluntary brain processing in disorders of consciousness. Neurology. 2008;71(20):1614–20.
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(9):1746–60.
Kirsch M, Guldenmund P, Ali Bahri M, et al. Sedation of patients with disorders of consciousness during neuroimaging: Effects on resting state functional brain connectivity. In: Anesthesia and Analgesia. 2017.
Threlkeld ZD, Bodien YG, Rosenthal ES, et al. Functional networks reemerge during recovery of consciousness after acute severe traumatic brain injury. Cortex. 2018;106:299–308.
Bodien YG, Threlkeld ZD, Edlow BL. Default mode network dynamics in covert consciousness. Cortex. 2019.
Steppacher I, Eickhoff S, Jordanov T, Kaps M, Witzke W, Kissler J. N400 predicts recovery from disorders of consciousness. Ann Neurol. 2013;73(5):594–602.
Balconi M, Arangio R, Guarnerio C. Disorders of consciousness and N400 ERP measures in response to a semantic task. J Neuropsychiatry Clin Neurosci. 2013;25:237–43.
Cruse D, Beukema S, Chennu S, Malins JG, Owen AM, McRae K. The reliability of the N400 in single subjects: implications for patients with disorders of consciousness. NeuroImage Clin. 2014;4:788–99.
Erlbeck H, Kübler A, Kotchoubey B, Veser S. Task instructions modulate the attentional mode affecting the auditory MMN and the semantic N400. Front Hum Neurosci. 2014;8:654.
Rohaut B, Faugeras F, Chausson N, et al. Probing ERP correlates of verbal semantic processing in patients with impaired consciousness. Neuropsychologia. 2015;66:279–92.
Beukema S, Gonzalez-Lara LE, Finoia P, et al. A hierarchy of event-related potential markers of auditory processing in disorders of consciousness. NeuroImage Clin. 2016;12:359.