Altered Mental Status at the Extreme: Behavioral Evaluation of Disorders of Consciousness

Abstract

Disorders of consciousness represent altered mental status at its most severe, comprising a continuum between coma, the vegetative state/unresponsive wakefulness syndrome, the minimally conscious state, and emergence from the minimally conscious state. Patients often transition between these levels throughout their recovery, and determining a patient's current level can be challenging, particularly in the acute care setting. Although healthcare providers have classically relied on a bedside neurological exam or the Glasgow Coma Scale to aid with assessment of consciousness, studies have identified multiple limitations of doing so. Neurobehavioral assessment measures, such as the Coma Recovery Scale-Revised, have been developed to address these shortcomings. Each behavioral metric has strengths as well as weaknesses when applied in the acute care setting. In this review, we appraise common assessment approaches, outline alternative measures for fine-tuning these assessments in the acute care setting, and highlight strategies for implementing these practices in an interdisciplinary manner.

Keywords

disorders of consciousness - coma - vegetative state - unresponsive wakefulness syndrome - minimally conscious state - behavioral evaluation

^* Co-last authors.

Publication History

Article published online:
05 August 2024

• References

• 1 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
• 2 Laureys S. The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn Sci 2005; 9 (12) 556-559
• 3 Tindall SC. Level of consciousness. In: H Kenneth Walker, W Dallas Hall, J Willis Hurst, eds. Clinical Methods: The History, Physical, and Laboratory Examinations. 3rd ed.. Butterworths; 1990: 296-299
• 4 Edlow BL, Takahashi E, Wu O. et al. Neuroanatomic connectivity of the human ascending arousal system critical to consciousness and its disorders. J Neuropathol Exp Neurol 2012; 71 (06) 531-546
• 5 Boes AD, Fischer D, Geerling JC, Bruss J, Saper CB, Fox MD. Connectivity of sleep- and wake-promoting regions of the human hypothalamus observed during resting wakefulness. Sleep 2018; 41 (09) zsy108
• 6 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
• 7 Giacino JT, Katz DI, Schiff ND, Bodien YG. Assessment and rehabilitative management of individuals with disorders of consciousness. In: Brain Injury Medicine: Principles and Practice. 3rd ed. New York, NY: Demos Medical Publishing; 2021. . Accessed July 29, 2024. https://www.springerpub.com/brain-injury-medicine-third-edition-9780826143044.html
• 8 Jennett B, Plum F. Persistent vegetative state after brain damage. A syndrome in search of a name. Lancet 1972; 1 (7753) 734-737
• 9 Seel RT, Sherer M, Whyte J. et al. Assessment scales for disorders of consciousness: evidence-based recommendations for clinical practice and research. Arch Phys Med Rehabil 2010; 91 (12) 1795-1813
• 10 van Erp WS, Lavrijsen JCM, Vos PE, Bor H, Laureys S, Koopmans RTCM. The vegetative state: prevalence, misdiagnosis, and treatment limitations. J Am Med Dir Assoc 2015; 16 (01) 85.e9-85.e14
• 11 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
• 12 Giacino JT, Kalmar K. The vegetative and minimally conscious states: a comparison of clinical features and functional outcome. J Head Trauma Rehabil 1997; 12 (04) 36-51
• 13 Hirschberg R, Giacino JT. The vegetative and minimally conscious states: diagnosis, prognosis and treatment. Neurol Clin 2011; 29 (04) 773-786
• 14 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
• 15 Jain R, Ramakrishnan AG. Electrophysiological and neuroimaging studies - during resting state and sensory stimulation in disorders of consciousness: a review. Front Neurosci 2020; 14: 555093
• 16 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
• 17 Sun Y, Wang J, Heine L. et al. Personalized objects can optimize the diagnosis of EMCS in the assessment of functional object use in the CRS-R: a double blind, randomized clinical trial. BMC Neurol 2018; 18 (01) 38
• 18 Roquet D, Foucher JR, Froehlig P. et al. Resting-state networks distinguish locked-in from vegetative state patients. Neuroimage Clin 2016; 12: 16-22
• 19 Arnts H, van Erp WS, Lavrijsen JCM, van Gaal S, Groenewegen HJ, van den Munckhof P. On the pathophysiology and treatment of akinetic mutism. Neurosci Biobehav Rev 2020; 112: 270-278
• 20 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
• 21 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
• 22 Bodien YG, Katz DI, Schiff ND, Giacino JT. Behavioral assessment of patients with disorders of consciousness. Semin Neurol 2022; 42 (03) 249-258
• 23 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
• 24 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
• 25 Giacino JT, Bodien Y, Chatlle C. Coma Recovery Scale-Revised ©2004 Administration and Scoring Guidelines. Accessed July 22, 2024 at: https://www.tbims.org/combi/crs/CRS%20Syllabus.pdf
• 26 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
• 27 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
• 28 Coma Recovery Scale-Revised (CRS-R) Frequently Asked Questions. . Accessed February 29, 2024 at: http://www.tbims.org/crs/CRSR_FAQs.pdf
• 29 Weaver JA, Cogan AM, O'Brien KA. et al. 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; 39 (19-20): 1417-1428
• 30 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 (C): 73-88
• 31 Faugeras F, Rohaut B, Valente M. et al. Survival and consciousness recovery are better in the minimally conscious state than in the vegetative state. Brain Inj 2018; 32 (01) 72-77
• 32 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
• 33 Boltzmann M, Schmidt SB, Gutenbrunner C. et al. The influence of the CRS-R score on functional outcome in patients with severe brain injury receiving early rehabilitation. BMC Neurol 2021; 21 (01) 44
• 34 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
• 35 Bodien YG, Vora I, Barra A. et al. Feasibility and validity of the Coma Recovery Scale-Revised for accelerated standardized testing: a practical assessment tool for detecting consciousness in the intensive care unit. Ann Neurol 2023; 94 (05) 919-924
• 36 Wijdicks EFM, Bamlet WR, Maramattom BV, Manno EM, McClelland RL. Validation of a new coma scale: the FOUR score. Ann Neurol 2005; 58 (04) 585-593
• 37 Schnakers C, Giacino J, Kalmar K. et al. Does the FOUR score correctly diagnose the vegetative and minimally conscious states?. [1] Ann Neurol 2006; 60 (06) 744-745 , author reply 745
• 38 Iyer VN, Mandrekar JN, Danielson RD, Zubkov AY, Elmer JL, Wijdicks EFM. Validity of the FOUR score coma scale in the medical intensive care unit. Mayo Clin Proc 2009; 84 (08) 694-701
• 39 Wijdicks EFM, Kramer AA, Rohs Jr T. et al. Comparison of the full outline of UnResponsiveness score and the Glasgow Coma Scale in predicting mortality in critically ill patients. Crit Care Med 2015; 43 (02) 439-444
• 40 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
• 41 Day KV, DiNapoli MV, Whyte J. Detecting early recovery of consciousness: a comparison of methods. Neuropsychol Rehabil 2018; 28 (08) 1233-1241
• 42 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
• 43 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
• 44 Pignat JM, Mauron E, Jöhr J. et al. Outcome prediction of consciousness disorders in the acute stage based on a complementary motor behavioural tool. PLoS One 2016; 11 (06) e0156882
• 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 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
• 47 Sensory Modality Assessment and Rehabilitation Technique | RehabMeasures Database. Accessed February 29, 2024 at: https://www.sralab.org/rehabilitation-measures/sensory-modality-assessment-and-rehabilitation-technique
• 48 Miranda F, Arevalo-Rodriguez I, Díaz G. et al. Confusion Assessment Method for the intensive care unit (CAM-ICU) for the diagnosis of delirium in adults in critical care settings. Cochrane Database Syst Rev 2023; 11 (11) CD013126
• 49 Papadimitriou C, Weaver JA, Guernon A, Walsh E, Mallinson T, Pape TLB. “Fluctuation is the norm”: rehabilitation practitioner perspectives on ambiguity and uncertainty in their work with persons in disordered states of consciousness after traumatic brain injury. PLoS One 2022; 17 (04) e0267194
• 50 Egbebike J, Shen Q, Doyle K. et al. Cognitive-motor dissociation and time to functional recovery in patients with acute brain injury in the USA: a prospective observational cohort study. Lancet Neurol 2022; 21 (08) 704-713
• 51 Schiff ND. Cognitive motor dissociation following severe brain injuries. JAMA Neurol 2015; 72 (12) 1413-1415
• 52 Norton L, Kazazian K, Gofton T. et al. Functional neuroimaging as an assessment tool in critically ill patients. Ann Neurol 2023; 93 (01) 131-141
• 53 Bender A, Jox RJ, Grill E, Straube A, Lulé D. Persistent vegetative state and minimally conscious state: a systematic review and meta-analysis of diagnostic procedures. Dtsch Arztebl Int 2015; 112 (14) 235-242
• 54 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
• 55 Di H, Boly M, Weng X, Ledoux D, Laureys S. Neuroimaging activation studies in the vegetative state: predictors of recovery?. Clin Med (Lond) 2008; 8 (05) 502-507
• 56 Young MJ, Kazazian K, Fischer D, Lissak IA, Bodien YG, Edlow BL. Disclosing results of tests for covert consciousness: a framework for ethical translation. Neurocrit Care 2024; 40 (03) 865-878
• 57 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
• 58 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
• 59 Hall KM, Hamilton BB, Gordon WA, Zasler ND. Characteristics and comparisons of functional assessment indices: disability rating scale, functional independence measure, and functional assessment measure. J Head Trauma Rehabil 1993; 8 (02) 60-74
• 60 Whyte J, Kunz R. Rancho Los Amigos Scale. In: Encyclopedia of Clinical Neuropsychology. 2018.
• 61 Rossato E, Verzini E, Scandola M, Ferrari F, Bonadiman S. Role of LCF scale as an outcome prognostic index in patients with traumatic brain injury. Neurol Sci 2021; 42 (07) 2747-2752
• 62 Lin K, Wroten M. Ranchos Los Amigos. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2024. . Accessed July 28, 2024 at: https://www.ncbi.nlm.nih.gov/books/NBK448151/
• 63 Hammond FM, Zafonte RD, Sherer M. et al. Assessing the benefits and risks of amantadine for irritability and aggression after traumatic brain injury. PM R. 2024; 16 (07) 661-668
• 64 Bruno MA, Majerus S, Boly M. et al. Functional neuroanatomy underlying the clinical subcategorization of minimally conscious state patients. J Neurol 2012; 259 (06) 1087-1098
• 65 Chatelle C, Bodien YG, Carlowicz C. et al. Detection and interpretation of impossible and improbable Coma Recovery Scale-Revised scores. Arch Phys Med Rehabil 2016; 97 (08) 1295-1300.e4
• 66 Katz DI, Zasler ND, Zafonte RD. Systems of care and natural history of traumatic brain injury. In: Brain Injury Medicine, Third Edition: Principles and Practice. 2021.
• 67 Hagen C. Rancho Los Amigos — Revised. Centre for Neuro skills. Accessed July 25, 2024 at: www.neuroskills.com/education-and-resources/rancho-los-amigos-revised/
• 68 Giacino JT, Whyte J, Bagiella E. et al. Placebo-controlled trial of amantadine for severe traumatic brain injury. N Engl J Med 2012; 366 (09) 819-826
• 69 Katz DI, Whyte J, Chang H. et al. Effect of lesion burden on recovery and response to amantadine in patients with traumatic disorders of consciousness. Arch Phys Med Rehabil 2014; 95 (10) e4
• 70 Passler MA, Riggs RV. Positive outcomes in traumatic brain injury-vegetative state: patients treated with bromocriptine. Arch Phys Med Rehabil 2001; 82 (03) 311-315
• 71 Kim YW, Shin JC, An YS. Effects of methylphenidate on cerebral glucose metabolism in patients with impaired consciousness after acquired brain injury. Clin Neuropharmacol 2009; 32 (06) 335-339
• 72 Moattari M, Alizadeh Shirazi F, Sharifi N, Zareh N. Effects of a sensory stimulation by nurses and families on level of cognitive function, and basic cognitive sensory recovery of comatose patients with severe traumatic brain injury: a randomized control trial. Trauma Mon 2016; 21 (04) e23531
• 73 Oh H, Seo W. Sensory stimulation programme to improve recovery in comatose patients. J Clin Nurs 2003; 12 (03) 394-404
• 74 Fleminger S, Greenwood R, Oliver D. Pharmacological management for agitation and aggression in people with acquired brain injury. Cochrane Database Syst Rev 2006; (04) CD003299
• 75 Whyte J, Rajan R, Rosenbaum A. et al. Zolpidem and restoration of consciousness. Am J Phys Med Rehabil 2014; 93 (02) 101-113
• 76 Du B, Shan A, Zhang Y, Zhong X, Chen D, Cai K. Zolpidem arouses patients in vegetative state after brain injury: quantitative evaluation and indications. Am J Med Sci 2014; 347 (03) 178-182
• 77 Schnakers C, Magee WL, Harris B. Sensory stimulation and music therapy programs for treating disorders of consciousness. Front Psychol 2016; 7 (MAR): 297
• 78 Feeney DM, Gonzalez A, Law WA. Amphetamine, haloperidol, and experience interact to affect rate of recovery after motor cortex injury. Science 1982; 217 (4562) 855-857
• 79 Wilson MS, Gibson CJ, Hamm RJ. Haloperidol, but not olanzapine, impairs cognitive performance after traumatic brain injury in rats. Am J Phys Med Rehabil 2003; 82 (11) 871-879
• 80 Hoffman AN, Cheng JP, Zafonte RD, Kline AE. Administration of haloperidol and risperidone after neurobehavioral testing hinders the recovery of traumatic brain injury-induced deficits. Life Sci 2008; 83 (17-18): 602-607
• 81 Baguley IJ, Nott MT, Slewa-Younan S, Heriseanu RE, Perkes IE. Diagnosing dysautonomia after acute traumatic brain injury: evidence for overresponsiveness to afferent stimuli. Arch Phys Med Rehabil 2009; 90 (04) 580-586
• 82 Perkes I, Baguley IJ, Nott MT, Menon DK. A review of paroxysmal sympathetic hyperactivity after acquired brain injury. Ann Neurol 2010; 68 (02) 126-135
• 83 Agitated Behavior Scale | RehabMeasures Database. Accessed February 29, 2024 at: https://www.sralab.org/rehabilitation-measures/agitated-behavior-scale
• 84 Orientation Log | RehabMeasures Database. Accessed February 29, 2024 at: https://www.sralab.org/rehabilitation-measures/orientation-log
• 85 Berg Balance Scale | RehabMeasures Database. Accessed February 29, 2024 at: https://www.sralab.org/rehabilitation-measures/berg-balance-scale
• 86 Disability Rating Scale (for TBI) | RehabMeasures Database. Accessed February 29, 2024 at: https://www.sralab.org/rehabilitation-measures/disability-rating-scale-tbi
• 87 Functional Independence Measure | RehabMeasures Database. Accessed February 29, 2024 at: https://www.sralab.org/rehabilitation-measures/functional-independence-measure
• 88 Functional Assessment Measure | RehabMeasures Database. Accessed February 29, 2024 at: https://www.sralab.org/rehabilitation-measures/functional-assessment-measure