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EEG Correlates of Language Function in Traumatic Disorders of Consciousness

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Abstract

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.

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References

  1. 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.

    Article  CAS  PubMed  Google Scholar 

  2. 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.

    Article  PubMed  Google Scholar 

  3. 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.

    Google Scholar 

  4. 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.

  5. 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.

    Article  PubMed  Google Scholar 

  6. Gill-Thwaites H. Lotteries, loopholes and luck: misdiagnosis in the vegetative state patient. Brain Inj. 2006;20(13–14):1321–8.

    Article  PubMed  Google Scholar 

  7. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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.

    Article  PubMed  Google Scholar 

  9. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Teasdale G, Jennett B. Assessment of coma and impaired consciousness. Lancet Neurol. 1974;304:81–4.

    Article  Google Scholar 

  11. 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.

    Article  PubMed  Google Scholar 

  12. 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.

    Article  PubMed  Google Scholar 

  13. 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.

    Article  PubMed  Google Scholar 

  14. 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.

    Article  CAS  PubMed  Google Scholar 

  15. Owen AM, Coleman MR, Boly M, Davis MH, Laureys S, Pickard JD. Detecting awareness in the vegetative state. Science. 2006;313(5792):1402.

    Article  CAS  PubMed  Google Scholar 

  16. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Rohaut B, Eliseyev A, Claassen J. Uncovering consciousness in unresponsive ICU patients: technical, medical and ethical considerations. Crit Care. 2019;23:78.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Schiff ND. Cognitive motor dissociation following severe brain injuries. JAMA Neurol. 2015;72(12):1413–5.

    Article  PubMed  Google Scholar 

  19. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  21. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  22. 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.

    Article  Google Scholar 

  23. 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.

    Article  CAS  PubMed  Google Scholar 

  24. 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.

    Article  CAS  PubMed  Google Scholar 

  25. Gosseries O, Zasler ND, Laureys S. Recent advances in disorders of consciousness: focus on the diagnosis. Brain Inj. 2014;28(9):1141–50.

    Article  PubMed  Google Scholar 

  26. 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.

    Article  CAS  PubMed  Google Scholar 

  27. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  28. 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.

    Article  PubMed  Google Scholar 

  29. 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.

    Article  CAS  PubMed  Google Scholar 

  30. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  31. 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.

    Google Scholar 

  32. American Clinical Neurophysiology Society. Guideline 7: guidelines for writing EEG reports. J Clin Neurophysiol. 2006;23(2):118–21.

    Article  Google Scholar 

  33. Synek VM. Prognostically important EEG coma patterns in diffuse anoxic and traumatic encephalopathies in adults. J Clin Neurophysiol. 1988;5(2):161–74.

    Article  CAS  PubMed  Google Scholar 

  34. Bagnato S, Boccagni C, Prestandrea C, Sant’Angelo A, Castiglione A, Galardi G. Prognostic value of standard. Clin Neurophysiol. 2010;121(3):274–80.

    Article  CAS  PubMed  Google Scholar 

  35. 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.

    Article  PubMed  Google Scholar 

  36. Schnakers C, Edlow BL, Chatelle C, Giacino JT. Minimally conscious state. In: The Neurology of Conciousness. 2016.

  37. 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.

    Article  CAS  PubMed  Google Scholar 

  38. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Schnakers C, Perrin F, Schabus M, et al. Voluntary brain processing in disorders of consciousness. Neurology. 2008;71(20):1614–20.

    Article  CAS  PubMed  Google Scholar 

  40. 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.

    Article  PubMed  Google Scholar 

  41. 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.

  42. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Bodien YG, Threlkeld ZD, Edlow BL. Default mode network dynamics in covert consciousness. Cortex. 2019.

  44. 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.

    Article  PubMed  Google Scholar 

  45. 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.

    Article  PubMed  Google Scholar 

  46. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  47. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  48. 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.

    Article  PubMed  Google Scholar 

  49. 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.

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

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.

Author information

Author notes

  1. Camille Chatelle, Eric S. Rosenthal: Co-first authors.

  2. Joseph T. Giacino, Brian L. Edlow: Co-senior authors.

Authors and Affiliations

  1. GIGA Consciousness, Coma Science Group, University of Liège, Avenue de l’Hôpital, 11, 4000, Liège, Belgium

    Camille Chatelle

  2. Center for Neurotechnology and Neurorecovery, Massachusetts General Hospital, Boston, MA, USA

    Camille Chatelle, Eric S. Rosenthal, Yelena G. Bodien, Camille A. Spencer-Salmon & Brian L. Edlow

  3. Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA

    Eric S. Rosenthal

  4. Clinical Data Animation Center, Massachusetts General Hospital, Boston, MA, USA

    Eric S. Rosenthal

  5. Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Boston, MA, USA

    Yelena G. Bodien & Joseph T. Giacino

  6. Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA

    Brian L. Edlow

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  1. Camille Chatelle
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Contributions

CC substantially contributed to conception and design; acquisition of data; analysis and interpretation of data; drafting the article. ESR substantially contributed to conception and design; analysis and interpretation of data; drafting the article. YGB contributed to acquisition of data; critical review of manuscript. CASS contributed to acquisition and analysis of data; critical review of manuscript. JTG substantially contributed to conception and design; critical review of manuscript. BLE substantially contributed to conception and design; acquisition of data; analysis and interpretation of data; drafting the article; Final approval of the version to be published.

Corresponding author

Correspondence to Camille Chatelle.

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Chatelle, C., Rosenthal, E.S., Bodien, Y.G. et al. EEG Correlates of Language Function in Traumatic Disorders of Consciousness. Neurocrit Care 33, 449–457 (2020). https://doi.org/10.1007/s12028-019-00904-3

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