Sleep and Circadian Disturbance in Disorders of Consciousness: Current Methods and the Way towards Clinical Implementation

Abstract

The investigation of sleep in disorders of consciousness (DoC) has shown promising diagnostic and prognostic results. However, the methods employed in this field of research are diverse. This leads to confusion in the way forward for both scientific and clinical purposes. We review the literature that has investigated sleep in DoC patients and specifically outline the methodologies used next to the presented results. We highlight what knowledge we currently have and where increased efforts are needed before further clinical implementation. Specifically, the review shows that successful methods may employ a two-stage approach to sleep scoring, where one is the application of loosened standard criteria and the other a more general factor describing closeness of the electroencephalography to a healthy pattern, including a score that describes the extent to which sleep scoring criteria can be applied. This should be performed as part of a multimodal approach that also includes investigations of eye-opening/closure and that of circadian (24-hour) rhythmicity. Taken together, this puts the most promising methodologies in the field together for a comprehensive investigation. Large-scale approaches, incorporating multiple modalities and looking at individual variation, are now needed to advance our understanding of sleep in DoC and its role in diagnosis, treatment, and recovery.

Keywords

disorders of consciousness - sleep - sleep scoring - slow waves - circadian rhythm

Publikationsverlauf

Accepted Manuscript online:
06. Juli 2022

Artikel online veröffentlicht:
13. September 2022

• References

• 1 Cirelli C, Tononi G. Is sleep essential?. PLoS Biol 2008; 6 (08) e216
• 2 Rasch B, Born J. About sleep's role in memory. Physiol Rev 2013; 93 (02) 681-766
• 3 Besedovsky L, Lange T, Haack M. The sleep-immune crosstalk in health and disease. Physiol Rev 2019; 99 (03) 1325-1380
• 4 Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Med Rev 2006; 10 (01) 49-62
• 5 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) 1072
• 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 Kotchoubey B, Pavlov YG. Approaches to sleep in severely brain damaged patients: opposite or complementary? Reply to “Sleep and circadian rhythms in severely brain-injured patients - a comment”. Clin Neurophysiol 2018; 129 (08) 1785-1787
• 8 Wislowska M, Blume C, Angerer M, Wielek T, Schabus M. Approaches to sleep in severely brain damaged patients - further comments and replies to Kotchoubey & Pavlov. Clin Neurophysiol 2018; 129 (12) 2680-2681
• 9 Rossi Sebastiano D, Franceschetti S. A response to: “Sleep and circadian rhythms in severely brain-injured patients - a comment”. Clin Neurophysiol 2018; 129 (08) 1788
• 10 Kotchoubey B, Pavlov YG. Sleep patterns open the window into disorders of consciousness. Clin Neurophysiol 2018; 129 (03) 668-669
• 11 Laureys S, Celesia GG, Cohadon F. et al Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med 2010; 8: 68
• 12 Monti MM, Laureys S, Owen AM. The vegetative state. BMJ 2010; 341 (7767): c3765
• 13 Bekinschtein T, Cologan V, Dahmen B, Golombek D. You are only coming through in waves: wakefulness variability and assessment in patients with impaired consciousness. Prog Brain Res 2009; 177: 171-189
• 14 Giacino JT, Ashwal S, Childs N. et al. The minimally conscious state: definition and diagnostic criteria. Neurology 2002; 58 (03) 349-353
• 15 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
• 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 American Academy Of Sleep Medicine. The AASM Manual for the Scoring of Sleep and Associated Events. 2007 . Accessed July 20, 2022 at: https://aasm.org/clinical-resources/scoring-manual/
• 18 Blume C, Del Giudice R, Wislowska M, Lechinger J, Schabus M. Across the consciousness continuum-from unresponsive wakefulness to sleep. Front Hum Neurosci 2015; 9 (MAR): 105
• 19 Gottshall JL, Rossi Sebastiano D. Sleep in disorders of consciousness: diagnostic, prognostic, and therapeutic considerations. Curr Opin Neurol 2020; 33 (06) 684-690
• 20 Rechtschaffen A, Kales A. A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. University of California, LA: Brain Information Service, NINDB Neurological Information Network; 1968
• 21 Guldenmund P, Soddu A, Baquero K. et al. Structural brain injury in patients with disorders of consciousness: a voxel-based morphometry study. Brain Inj 2016; 30 (03) 343-352
• 22 Annen J, Frasso G, Crone JS. et al; Coma Science Group Collaborators. Regional brain volumetry and brain function in severely brain-injured patients. Ann Neurol 2018; 83 (04) 842-853
• 23 Saletin JM, van der Helm E, Walker MP. Structural brain correlates of human sleep oscillations. Neuroimage 2013; 83: 658-668
• 24 Brown RE, Basheer R, McKenna JT, Strecker RE, McCarley RW. Control of sleep and wakefulness. Physiol Rev 2012; 92 (03) 1087-1187
• 25 Valatx JL. Disorders of consciousness: anatomical and physiological mechanisms. Adv Tech Stand Neurosurg 2004; 29: 3-22
• 26 Isono M, Wakabayashi Y, Fujiki M M, Kamida T, Kobayashi H. Sleep cycle in patients in a state of permanent unconsciousness. Brain Inj 2002; 16 (08) 705-712
• 27 Oksenberg A, Gordon C, Arons E, Sazbon L. Phasic activities of rapid eye movement sleep in vegetative state patients. Sleep 2001; 24 (06) 703-706
• 28 Chéliout-Heraut F, Rubinsztajn R, Ioos C, Estournet B. Prognostic value of evoked potentials and sleep recordings in the prolonged comatose state of children. Preliminary data. Neurophysiol Clin 2001; 31 (05) 283-292
• 29 Kampfl A, Schmutzhard E, Franz G. et al. Prediction of recovery from post-traumatic vegetative state with cerebral magnetic-resonance imaging. Lancet 1998; 351 (9118): 1763-1767
• 30 Schiff ND. Central thalamic contributions to arousal regulation and neurological disorders of consciousness. Ann N Y Acad Sci 2008; 1129: 105-118
• 31 Koch C, Massimini M, Boly M, Tononi G. Neural correlates of consciousness: progress and problems. Nat Rev Neurosci 2016; 17 (05) 307-321
• 32 David F, Schmiedt JT, Taylor HL. et al. Essential thalamic contribution to slow waves of natural sleep. J Neurosci 2013; 33 (50) 19599-19610
• 33 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
• 34 Maxwell WL, MacKinnon MA, Smith DH, McIntosh TK, Graham DI. Thalamic nuclei after human blunt head injury. J Neuropathol Exp Neurol 2006; 65 (05) 478-488
• 35 Pavlov YG, Gais S, Müller F. et al. Night sleep in patients with vegetative state. J Sleep Res 2017; 26 (05) 629-640
• 36 Estraneo A, Loreto V, Guarino I. et al. Standard EEG in diagnostic process of prolonged disorders of consciousness. Clin Neurophysiol 2016; 127 (06) 2379-2385
• 37 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
• 38 Bagnato S, Boccagni C, Prestandrea C, Fingelkurts AA, Fingelkurts AA, Galardi G. Changes in standard electroencephalograms parallel consciousness improvements in patients with unresponsive wakefulness syndrome. Arch Phys Med Rehabil 2017; 98 (04) 665-672
• 39 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
• 40 Azabou E, Navarro V, Kubis N. et al. Value and mechanisms of EEG reactivity in the prognosis of patients with impaired consciousness: a systematic review. Crit Care 2018; 22 (01) 184
• 41 Mertel I, Pavlov YG, Barner C, Müller F, Diekelmann S, Kotchoubey B. Sleep in severe disorders of consciousness: 24-h behavioral and polysomnographic recording. BMC Med 2020; 18 (01) 350
• 42 Landsness E, Bruno MA, Noirhomme Q. et al. Electrophysiological correlates of behavioural changes in vigilance in vegetative state and minimally conscious state. Brain 2011; 134 (Pt 8): 2222-2232
• 43 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
• 44 Aricò I, Naro A, Pisani LR. et al. Could combined sleep and pain evaluation be useful in the diagnosis of disorders of consciousness (DOC)? Preliminary findings. Brain Inj 2016; 30 (02) 159-163
• 45 Kang X-G, Li L, Wei D. et al. Development of a simple score to predict outcome for unresponsive wakefulness syndrome. Crit Care 2014; 18 (01) R37
• 46 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
• 47 de Biase S, Gigli GL, Lorenzut S. et al. The importance of polysomnography in the evaluation of prolonged disorders of consciousness: sleep recordings more adequately correlate than stimulus-related evoked potentials with patients' clinical status. Sleep Med 2014; 15 (04) 393-400
• 48 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 (06) 869-879
• 49 Schnakers C, Hirsch M, Noé E. et al. Covert cognition in disorders of consciousness: a meta-analysis. Brain Sci 2020; 10 (12) 1-11
• 50 Giubilei F, Formisano R, Fiorini M. et al. Sleep abnormalities in traumatic apallic syndrome. J Neurol Neurosurg Psychiatry 1995; 58 (04) 484-486
• 51 Gordon CR, Oksenberg A. Spontaneous nystagmus across the sleep-wake cycle in vegetative state patients. Electroencephalogr Clin Neurophysiol 1993; 86 (02) 132-137
• 52 Oksenberg A, Arons E, Sazbon L, Mizrahi A, Radwan H. Sleep-related erections in vegetative state patients. Sleep 2000; 23 (07) 953-957
• 53 D'Aleo G, Bramanti P, Silvestri R, Saltuari L, Gerstenbrand F, Di Perri R. Sleep spindles in the initial stages of the vegetative state. Ital J Neurol Sci 1994; 15 (07) 347-351
• 54 Nekrasova J, Kanarskii M, Yankevich D. et al. Retrospective analysis of sleep patterns in patients with chronic disorders of consciousness. Sleep Med X 2020; 2: 100024
• 55 Arnaldi D, Terzaghi M, Cremascoli R. et al. The prognostic value of sleep patterns in disorders of consciousness in the sub-acute phase. Clin Neurophysiol 2016; 127 (02) 1445-1451
• 56 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
• 57 Yang X-A, Song C-G, 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
• 58 Rossi Sebastiano D, Panzica F, Visani E. et al. Significance of multiple neurophysiological measures in patients with chronic disorders of consciousness. Clin Neurophysiol 2015; 126 (03) 558-564
• 59 Mouthon AL, van Hedel HJA, Meyer-Heim A. et al. High-density electroencephalographic recordings during sleep in children with disorders of consciousness. Neuroimage Clin 2016; 11: 468-475
• 60 Avantaggiato P, Molteni E, Formica F. et al. Polysomnographic sleep patterns in children and adolescents in unresponsive wakefulness syndrome. J Head Trauma Rehabil 2015; 30 (05) 334-346
• 61 Gibson RM, Ray LB, Laforge G, Owen AM, Fogel SM. 24-h polysomnographic recordings and electrophysiological spectral analyses from a cohort of patients with chronic disorders of consciousness. J Neurol 2020; 267 (12) 3650-3663
• 62 Wislowska M, Del Giudice R, Lechinger J. et al. Night and day variations of sleep in patients with disorders of consciousness. Sci Rep 2017; 7 (01) 266
• 63 Malinowska U, Chatelle C, Bruno MA, Noirhomme Q, Laureys S, Durka PJ. Electroencephalographic profiles for differentiation of disorders of consciousness. Biomed Eng Online 2013; 12 (01) 109
• 64 Zieleniewska M, Duszyk A, Różański P, Pietrzak M, Bogotko M, Durka P. Parametric description of EEG profiles for assessment of sleep architecture in disorders of consciousness. Int J Neural Syst 2019; 29 (03) 1850049
• 65 Ancoli-Israel S, Cole R, Alessi C, Chambers M, Moorcroft W, Pollak CP. The role of actigraphy in the study of sleep and circadian rhythms. Sleep 2003; 26 (03) 342-392
• 66 Cruse D, Thibaut A, Demertzi A. et al. Actigraphy assessments of circadian sleep-wake cycles in the vegetative and minimally conscious states. BMC Med 2013; 11 (01) 18
• 67 Angerer M, Schabus M, Raml M. et al. Actigraphy in brain-injured patients - a valid measurement for assessing circadian rhythms?. BMC Med 2020; 18 (01) 106
• 68 De Weer AS, Da Ros M, Berré J, Mélot C, Goldman S, Peigneux P. Environmental influences on activity patterns in altered states of consciousness. Eur J Neurol 2011; 18 (12) 1432-1434
• 69 Refinetti R. The circadian rhythm of body temperature. Front Biosci 2010; 15 (02) 564-594
• 70 Bekinschtein TA, Golombek DA, Simonetta SH, Coleman MR, Manes FF. Circadian rhythms in the vegetative state. Brain Inj 2009; 23 (11) 915-919
• 71 Alster J, Pratt H, Feinsod M. Density spectral array, evoked potentials, and temperature rhythms in the evaluation and prognosis of the comatose patient. Brain Inj 1993; 7 (03) 191-208
• 72 Blume C, Lechinger J, Santhi N. et al. Significance of circadian rhythms in severely brain-injured patients: a clue to consciousness?. Neurology 2017; 88 (20) 1933-1941
• 73 Blume C, Angerer M, Raml M. et al. Healthier rhythm, healthier brain? Integrity of circadian melatonin and temperature rhythms relates to the clinical state of brain-injured patients. Eur J Neurol 2019; 26 (08) 1051-1059
• 74 Leo A, Naro A, Cannavò A. et al. Could autonomic system assessment be helpful in disorders of consciousness diagnosis? A neurophysiological study. Exp Brain Res 2016; 234 (08) 2189-2199
• 75 Bagnato S, Minafra L, Bravatà V. et al. Brain-derived neurotrophic factor (Val66Met) polymorphism does not influence recovery from a post-traumatic vegetative state: a blinded retrospective multi-centric study. J Neurotrauma 2012; 29 (11) 2050-2059
• 76 Bagnato S, Galardi G, Ribaudo F. et al. Serum BDNF levels are reduced in patients with disorders of consciousness and are not modified by verticalization with robot-assisted lower-limb training. Neural Plast 2020; 2020: 5608145
• 77 Simon D, Nascimento RI, Filho EMR, Bencke J, Regner A. Plasma brain-derived neurotrophic factor levels after severe traumatic brain injury. Brain Inj 2016; 30 (01) 23-28
• 78 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
• 79 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
• 80 Posner JB, Plum F, Saper CB, Schiff N. Plum and Posner's Diagnosis of Stupor and Coma. Vol 71. Oxford: Oxford University Press; 2007
• 81 Kondziella D, Frontera JA. Pearls & Oy-sters: eyes-open coma. Neurology 2021; 96 (18) 864-867
• 82 Latkany RL, Lock B, Speaker M. Nocturnal lagophthalmos: an overview and classification. Ocul Surf 2006; 4 (01) 44-53
• 83 van Ommen HJ, Thibaut A, Vanhaudenhuyse A. et al. Resistance to eye opening in patients with disorders of consciousness. J Neurol 2018; 265 (06) 1376-1380
• 84 Muir KW. Stroke in the acute setting. Medicine 2017; 45 (03) 163-168
• 85 Van Someren EJW. Brain mechanisms of insomnia: new perspectives on causes and consequences. Physiol Rev 2021; 101 (03) 995-1046
• 86 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
• 87 Wielek T, Lechinger J, Wislowska M. et al. Sleep in patients with disorders of consciousness characterized by means of machine learning. PLoS One 2018; 13 (01) e0190458