Semin Neurol 2022; 42(03): 249-258
DOI: 10.1055/s-0042-1756298
Review Article

Behavioral Assessment of Patients with Disorders of Consciousness

1   Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
2   Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Charlestown, Massachusetts
,
Douglas I. Katz
3   Department of Neurology, Boston University School of Medicine, Boston, Massachusetts
4   Brain Injury Program, Encompass Health Braintree Rehabilitation Hospital, Braintree, Massachusetts
,
Nicholas D. Schiff
5   Feil Family Brain and Mind Institute, Weill Cornell Medicine, New York, New York
6   Department of Neurology, Weill Cornell Brain and Spine Institute, Weill Cornell Medicine, New York, NY, United States
,
Joseph T. Giacino
2   Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Charlestown, Massachusetts
› Author Affiliations
Funding Epstein Foundation, James S. McDonnell Foundation, U.S. Department of Health and Human Services, National Institutes of Health, National Institute of Neurological Disorders and Stroke, U01 NS1365885, National Institute of Neurological Disorders and Stroke, U01-NS086090, National Institute of Neurological Disorders and Stroke, 1U01NS093334-01, National Institute of Neurological Disorders and Stroke, U54N, National Institute on Disability, Independent Living, and Rehabilitation Research, 90DPTB0011, National Institute on Disability, Independent Living, and Rehabilitation Research, 90DP0039, Tiny Blue Dot Foundation, U.S. Department of Defense, W81XWH-14-2-0176.

Abstract

Severe brain injury is associated with a period of impaired level of consciousness that can last from days to months and results in chronic impairment. Systematic assessment of level of function in patients with disorders of consciousness (DoC) is critical for diagnosis, prognostication, and evaluation of treatment efficacy. Approximately 40% of patients who are thought to be unconscious based on clinical bedside behavioral assessment demonstrate some signs of consciousness on standardized behavioral assessment. This finding, in addition to a growing body of literature demonstrating the advantages of standardized behavioral assessment of DoC, has led multiple professional societies and clinical guidelines to recommend standardized assessment over routine clinical evaluation of consciousness. Nevertheless, even standardized assessment is susceptible to biases and misdiagnosis, and examiners should consider factors, such as fluctuating arousal and aphasia, that may confound evaluation. We review approaches to behavioral assessment of consciousness, recent clinical guideline recommendations for use of specific measures to evaluate patients with DoC, and strategies for mitigating common biases that may confound the examination.



Publication History

Article published online:
13 September 2022

© 2022. Thieme. All rights reserved.

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  • References

  • 1 Katz DI, Polyak M, Coughlan D, Nichols M, Roche A. Natural history of recovery from brain injury after prolonged disorders of consciousness: outcome of patients admitted to inpatient rehabilitation with 1-4 year follow-up. Prog Brain Res 2009; 177: 73-88
  • 2 Giacino JT. Disorders of consciousness: differential diagnosis and neuropathologic features. Semin Neurol 1997; 17 (02) 105-111
  • 3 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
  • 4 Giacino JT, Ashwal S, Childs N. et al. The minimally conscious state: definition and diagnostic criteria. Neurology 2002; 58 (03) 349-353
  • 5 Thibaut A, Bodien YG, Laureys S, Giacino JT. Minimally conscious state “plus”: diagnostic criteria and relation to functional recovery. J Neurol 2020; 267 (05) 1245-1254
  • 6 Bodien YG, Martens G, Ostrow J, Sheau K, Giacino JT. Cognitive impairment, clinical symptoms and functional disability in patients emerging from the minimally conscious state. NeuroRehabilitation 2020; 46 (01) 65-74
  • 7 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
  • 8 Nakase-Richardson R, Yablon SA, Sherer M, Evans CC, Nick TG. Serial yes/no reliability after traumatic brain injury: implications regarding the operational criteria for emergence from the minimally conscious state. J Neurol Neurosurg Psychiatry 2008; 79 (02) 216-218
  • 9 Nakase-Richardson R, Yablon SA, Sherer M, Nick TG, Evans CC. Emergence from minimally conscious state: insights from evaluation of posttraumatic confusion. Neurology 2009; 73 (14) 1120-1126
  • 10 Golden K, Erler KS, Wong J, Giacino JT, Bodien YG. Should consistent command-following be added to the criteria for emergence from the minimally conscious state?. Arch Phys Med Rehabil 2022; Apr 6:S0003-9993(22)00294-5 DOI: 10.1016/j.apmr.2022.03.010.
  • 11 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
  • 12 Andrews K, Murphy L, Munday R, Littlewood C. Misdiagnosis of the vegetative state: retrospective study in a rehabilitation unit. BMJ 1996; 313 (7048): 13-16
  • 13 Childs NL, Mercer WN, Childs HW. Accuracy of diagnosis of persistent vegetative state. Neurology 1993; 43 (08) 1465-1467
  • 14 Wang J, Hu X, Hu Z, Sun Z, Laureys S, Di H. The misdiagnosis of prolonged disorders of consciousness by a clinical consensus compared with repeated coma-recovery scale-revised assessment. BMC Neurol 2020; 20 (01) 343
  • 15 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): 514-522
  • 16 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
  • 17 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
  • 18 Royal College of Physicians. Prolonged disorders of consciousness following sudden onset brain injury: national clinical guidelines. 2020. London: RCP; Accessed July 19, 2022 at: https://www.rcplondon.ac.uk/guidelines-policy/prolonged-disorders-consciousness-following-sudden-onset-brain-injury-national-clinical-guidelines
  • 19 Giacino JT, Whyte J, Nakase-Richardson R. et al. Minimum competency recommendations for programs that provide rehabilitation services for persons with disorders of consciousness: a position statement of the American Congress of Rehabilitation Medicine and the National Institute on Disability, Independent Living and Rehabilitation Research Traumatic Brain Injury Model Systems. Arch Phys Med Rehabil 2020; 101 (06) 1072-1089
  • 20 Giacino JT, Kalmar K, Whyte J. The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 2004; 85 (12) 2020-2029
  • 21 Seel RT, Sherer M, Whyte J. et al; American Congress of Rehabilitation Medicine, Brain Injury-Interdisciplinary Special Interest Group, Disorders of Consciousness Task Force. Assessment scales for disorders of consciousness: evidence-based recommendations for clinical practice and research. Arch Phys Med Rehabil 2010; 91 (12) 1795-1813
  • 22 Hicks R, Giacino J, Harrison-Felix C, Manley G, Valadka A, Wilde EA. Progress in developing common data elements for traumatic brain injury research: version two–the end of the beginning. J Neurotrauma 2013; 30 (22) 1852-1861
  • 23 La Porta F, Caselli S, Ianes AB. et al. Can we scientifically and reliably measure the level of consciousness in vegetative and minimally conscious States? Rasch analysis of the coma recovery scale-revised. Arch Phys Med Rehabil 2013; 94 (03) 527-535.e1
  • 24 Gerrard P, Zafonte R, Giacino JT. Coma Recovery Scale-Revised: evidentiary support for hierarchical grading of level of consciousness. Arch Phys Med Rehabil 2014; 95 (12) 2335-2341
  • 25 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 (03) 490-492.e1
  • 26 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
  • 27 Lucca LF, Lofaro D, Pignolo L. et al. Outcome prediction in disorders of consciousness: the role of coma recovery scale revised. BMC Neurol 2019; 19 (01) 68-68
  • 28 Portaccio E, Morrocchesi A, Romoli AM. et al. Score on Coma Recovery Scale-Revised at admission predicts outcome at discharge in intensive rehabilitation after severe brain injury. Brain Inj 2018; 32 (06) 730-734
  • 29 Portaccio E, Morrocchesi A, Romoli AM. et al; Intensive Rehabilitation Unit Study Group of the IRCCS Don Gnocchi Foundation, Italy. Improvement on the Coma Recovery Scale-Revised during the first four weeks of hospital stay predicts outcome at discharge in intensive rehabilitation after severe brain injury. Arch Phys Med Rehabil 2018; 99 (05) 914-919
  • 30 Tamashiro M, Rivas ME, Ron M, Salierno F, Dalera M, Olmos L. A Spanish validation of the Coma Recovery Scale-Revised (CRS-R). Brain Inj 2014; 28 (13–14): 1744-1747
  • 31 Estraneo A, Moretta P, De Tanti A, Gatta G, Giacino JT, Trojano L. Italian Crs-R Multicentre Validation Group. An Italian multicentre validation study of the coma recovery scale-revised. Eur J Phys Rehabil Med 2015; 51 (05) 627-634
  • 32 Lombardi F, Gatta G, Sacco S, Muratori A, Carolei A. The Italian version of the Coma Recovery Scale-Revised (CRS-R). Funct Neurol 2007; 22 (01) 47-61
  • 33 Sacco S, Altobelli E, Pistarini C, Cerone D, Cazzulani B, Carolei A. Validation of the Italian version of the Coma Recovery Scale-Revised (CRS-R). Brain Inj 2011; 25 (05) 488-495
  • 34 Schnakers C, Majerus S, Giacino J. et al. A French validation study of the Coma Recovery Scale-Revised (CRS-R). Brain Inj 2008; 22 (10) 786-792
  • 35 Simões JF, Jesus LM, Voegeli D, Sá-Couto P, Fernandes J, Morgado M. Assessment of comatose patients: a Portuguese instrument based on the Coma Recovery Scale - revised and using nursing standard terminology. J Adv Nurs 2011; 67 (05) 1129-1141
  • 36 Løvstad M, Frøslie KF, Giacino JT, Skandsen T, Anke A, Schanke AK. Reliability and diagnostic characteristics of the JFK coma recovery scale-revised: exploring the influence of rater's level of experience. J Head Trauma Rehabil 2010; 25 (05) 349-356
  • 37 Iazeva EG, Legostaeva LA, Zimin AA. et al. A Russian validation study of the Coma Recovery Scale-Revised (CRS-R). Brain Inj 2018; (e-pub ahead of print). DOI: 10.1080/02699052.2018.1539248.
  • 38 Maurer-Karattup P, Giacino J, Luther M, Eifert B. Diagnosis of disorders of consciousness with the German version of Coma Recovery Scale-Revised (CRS-R). Neurol Rehabil 2010; 16: 232-246
  • 39 Binder M, Górska U, Wójcik-Krzemień A, Gociewicz K. A validation of the Polish version of the Coma Recovery Scale-Revised (CRSR). Brain Inj 2018; 32 (02) 242-246
  • 40 Han HJ, Kim EJ, Lee HJ, Pyun SB, Joa KL, Jung HY. Validation of Korean Version of Coma Recovery Scale-Revised (K-CRSR). Ann Rehabil Med 2018; 42 (04) 536-541
  • 41 Di H, He M, Zhang Y. et al. Chinese translation of the Coma Recovery Scale-Revised. Brain Inj 2017; 31 (03) 363-365
  • 42 Zhang Y, Wang J, Schnakers C. et al. Validation of the Chinese version of the Coma Recovery Scale-Revised (CRS-R). Brain Inj 2019; 33 (04) 529-533
  • 43 Bodien YG, Chatelle C, Taubert A, Uchani S, Giacino JT, Ehrlich-Jones L. Updated measurement characteristics and clinical utility of the Coma Recovery Scale-Revised among individuals with acquired brain injury. Arch Phys Med Rehabil 2021; 102 (01) 169-171
  • 44 Slomine BSSS, Suskauer SJ, Nicholson R, Giacino JT. Preliminary validation of the coma recovery scale for pediatrics in typically developing young children. Brain Inj 2019; 33 (13–14): 1640-1645
  • 45 Pincherle A, Jöhr J, Chatelle C. et al. Motor behavior unmasks residual cognition in disorders of consciousness. Ann Neurol 2019; 85 (03) 443-447
  • 46 Schnakers C, Chatelle C, Vanhaudenhuyse A. et al. The Nociception Coma Scale: a new tool to assess nociception in disorders of consciousness. Pain 2010; 148 (02) 215-219
  • 47 Aubinet C, Chatelle C, Gillet S. et al. The brief evaluation of receptive aphasia test for the detection of language impairment in patients with severe brain injury. Brain Inj 2021; 35 (06) 705-717
  • 48 Mélotte E, Belorgeot M, Herr R. et al. The development and validation of the SWADOC: a study protocol for a multicenter prospective cohort study. Front Neurol 2021; 12: 662634
  • 49 Annen J, Filippini MM, Bonin E. et al. Diagnostic accuracy of the CRS-R index in patients with disorders of consciousness. Brain Inj 2019; 33 (11) 1409-1412
  • 50 Sattin D, Minati L, Rossi D. et al. The Coma Recovery Scale Modified Score: a new scoring system for the Coma Recovery Scale-revised for assessment of patients with disorders of consciousness. Int J Rehabil Res 2015; 38 (04) 350-356
  • 51 Whyte J, Giacino JT, Heinemann AW. et al. Brain Injury Functional Outcome Measure (BI-FOM): a single instrument capturing the range of recovery in moderate-severe traumatic brain injury. Arch Phys Med Rehabil 2021; 102 (01) 87-96
  • 52 Ottenbacher KJ, Hsu Y, Granger CV, Fiedler RC. The reliability of the Functional Independence Measure: a quantitative review. Arch Phys Med Rehabil 1996; 77 (12) 1226-1232
  • 53 Sherer M, Nakase-Thompson R, Yablon SA, Gontkovsky ST. Multidimensional assessment of acute confusion after traumatic brain injury. Arch Phys Med Rehabil 2005; 86 (05) 896-904
  • 54 Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet 1974; 2 (7872): 81-84
  • 55 Marmarou A, Lu J, Butcher I. et al. Prognostic value of the Glasgow Coma Scale and pupil reactivity in traumatic brain injury assessed pre-hospital and on enrollment: an IMPACT analysis. J Neurotrauma 2007; 24 (02) 270-280
  • 56 Wilde EA, Whiteneck GG, Bogner J. et al. Recommendations for the use of common outcome measures in traumatic brain injury research. Arch Phys Med Rehabil 2010; 91 (11) 1650-1660.e17
  • 57 Maas AI, Roozenbeek B, Manley GT. Clinical trials in traumatic brain injury: past experience and current developments. Neurotherapeutics 2010; 7 (01) 115-126
  • 58 Reith FC, Brennan PM, Maas AI, Teasdale GM. Lack of standardization in the use of the Glasgow Coma Scale: results of international surveys. J Neurotrauma 2016; 33 (01) 89-94
  • 59 Fischer M, Rüegg S, Czaplinski A. et al. Inter-rater reliability of the Full Outline of UnResponsiveness score and the Glasgow Coma Scale in critically ill patients: a prospective observational study. Crit Care 2010; 14 (02) R64
  • 60 Martens G, Bodien Y, Sheau K, Christoforou A, Giacino JT. Which behaviours are first to emerge during recovery of consciousness after severe brain injury?. Ann Phys Rehabil Med 2020; 63 (04) 263-269
  • 61 Bodien YG, Barra A, Temkin NR. et al; TRACK-TBI Investigators. Diagnosing Level of Consciousness: the limits of the Glasgow Coma Scale total score. J Neurotrauma 2021; 38 (23) 3295-3305
  • 62 Wijdicks EF, Bamlet WR, Maramattom BV, Manno EM, McClelland RL. Validation of a new coma scale: the FOUR score. Ann Neurol 2005; 58 (04) 585-593
  • 63 Iyer VN, Mandrekar JN, Danielson RD, Zubkov AY, Elmer JL, Wijdicks EF. Validity of the FOUR score coma scale in the medical intensive care unit. Mayo Clin Proc 2009; 84 (08) 694-701
  • 64 Foo CC, Loan JJM, Brennan PM. The relationship of the FOUR score to patient outcome: a systematic review. J Neurotrauma 2019; 36 (17) 2469-2483
  • 65 Schnakers C, Giacino J, Kalmar K. et al. Does the FOUR score correctly diagnose the vegetative and minimally conscious states?. Ann Neurol 2006; 60 (06) 744-745 , author reply 745
  • 66 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
  • 67 Fins JJ. Rights Come to Mind: Brain Injury, Ethics, and the Struggle for Consciousness. New York, NY: Cambridge University Press; 2015
  • 68 Aubinet C, Cassol H, Bodart O. et al. Simplified evaluation of CONsciousness disorders (SECONDs) in individuals with severe brain injury: a validation study. Ann Phys Rehabil Med 2021; 64 (05) 101432
  • 69 Whyte J, DiPasquale MC, Vaccaro M. Assessment of command-following in minimally conscious brain injured patients. Arch Phys Med Rehabil 1999; 80 (06) 653-660
  • 70 DiPasquale MC, Whyte J. The use of quantitative data in treatment planning for minimally conscious patients. J Head Trauma Rehabil 1996; 11 (06) 9-17
  • 71 Schnakers C, Bessou H, Rubi-Fessen I. et al. Impact of aphasia on consciousness assessment: a cross-sectional study. Neurorehabil Neural Repair 2015; 29 (01) 41-47
  • 72 Aubinet C, Chatelle C, Gosseries O, Carrière M, Laureys S, Majerus S. Residual implicit and explicit language abilities in patients with disorders of consciousness: a systematic review. Neurosci Biobehav Rev 2022; 132: 391-409
  • 73 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
  • 74 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
  • 75 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
  • 76 Monti MM, Vanhaudenhuyse A, Coleman MR. et al. Willful modulation of brain activity in disorders of consciousness. N Engl J Med 2010; 362 (07) 579-589
  • 77 Schiff ND. Cognitive motor dissociation following severe brain injuries. JAMA Neurol 2015; 72 (12) 1413-1415
  • 78 Wang F, Di H, Hu X. et al. Cerebral response to subject's own name showed high prognostic value in traumatic vegetative state. BMC Med 2015; 13: 83
  • 79 Sokoliuk R, Degano G, Banellis L. et al. Covert speech comprehension predicts recovery from acute unresponsive states. Ann Neurol 2021; 89 (04) 646-656
  • 80 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
  • 81 Bodien YG, Chatelle C, Edlow BL. Functional networks in disorders of consciousness. Semin Neurol 2017; 37 (05) 485-502
  • 82 Monti MM, Schnakers C. Flowchart for implementing advanced imaging and electrophysiology in patients with disorders of consciousness: to fMRI or not to fMRI?. Neurology 2022; 98 (11) 452-459
  • 83 Curley WH, Bodien YG, Zhou DW. et al. Electrophysiological correlates of thalamocortical function in acute severe traumatic brain injury. Cortex 2022; 152: 136-152
  • 84 Gill-Thwaites H, Munday R. The Sensory Modality Assessment and Rehabilitation Technique (SMART): a valid and reliable assessment for vegetative state and minimally conscious state patients. Brain Inj 2004; 18 (12) 1255-1269
  • 85 Shiel A, Horn SA, Wilson BA, Watson MJ, Campbell MJ, McLellan DL. The Wessex Head Injury Matrix (WHIM) main scale: a preliminary report on a scale to assess and monitor patient recovery after severe head injury. Clin Rehabil 2000; 14 (04) 408-416
  • 86 Rader MA, Ellis DW. The Sensory Stimulation Assessment Measure (SSAM): a tool for early evaluation of severely brain-injured patients. Brain Inj 1994; 8 (04) 309-321
  • 87 Ansell BJ, Keenan JE. The Western Neuro Sensory Stimulation Profile: a tool for assessing slow-to-recover head-injured patients. Arch Phys Med Rehabil 1989; 70 (02) 104-108
  • 88 Pape TL, Mallinson T, Guernon A. Psychometric properties of the disorders of consciousness scale. Arch Phys Med Rehabil 2014; 95 (09) 1672-1684
  • 89 Rappaport M, Dougherty AM, Kelting DL. Evaluation of coma and vegetative states. Arch Phys Med Rehabil 1992; 73 (07) 628-634
  • 90 Weaver JA, Cogan AM, O'Brien KA, Hansen P, Giacino JT, Whyte J, Bender Pape T, van der Wees P, Mallinson T. Determining the Hierarchy of Coma Recovery Scale-Revised Rating Scale Categories and Alignment with Aspen Consensus Criteria for Patients with Brain Injury: A Rasch Analysis. J Neurotrauma. 2022 Jun 16. Doi: 10.1089/neu.2022.0095. Epub ahead of print. PMID: 35570725