Actigraphy assessments of circadian sleep-wake cycles in the Vegetative and Minimally Conscious States

BMC Medicine

Steven Laureys¹  Adrian M Owen²  Tristan A Bekinschtein³  Audrey Vanhaudenhuyse¹  Olivia Gosseries¹  Marie-Aurélie Bruno¹  Julia C Nantes²  Athena Demertzi¹  Aurore Thibaut¹  Damian Cruse² 

[1] Coma Science Group: Department of Neurology and Cyclotron Research Centre, University Hospital and University of Liège, Allée du 6 août n° 8, Sart Tilman B30 - 4000, Belgium;Brain and Mind Institute, University of Western Ontario, 1151 Richmond Street, London, ON N6A 3K7, Canada;Cognition and Brain Sciences Unit, Medical Research Council, 15 Chaucer Road, Cambridge, CB2 7EF, UK

关键词: actigraphy;    sleep;    circadian rhythms;    Minimally Conscious State;    Vegetative State;   

Others  :  857216
DOI  :  10.1186/1741-7015-11-18

 received in 2012-08-23, accepted in 2013-01-24,  发布年份 2013

【 摘 要 】

Background

The Vegetative and Minimally Conscious States (VS; MCS) are characterized by absent or highly disordered signs of awareness alongside preserved sleep-wake cycles. According to international diagnostic guidelines, sleep-wake cycles are assessed by means of observations of variable periods of eye-opening and eye-closure. However, there is little empirical evidence for true circadian sleep-wake cycling in these patients, and there have been no large-scale investigations of the validity of this diagnostic criterion.

Methods

We measured the circadian sleep-wake rhythms of 55 VS and MCS patients by means of wrist actigraphy, an indirect method that is highly correlated with polysomnographic estimates of sleeping/waking.

Results

Contrary to the diagnostic guidelines, a significant proportion of patients did not exhibit statistically reliable sleep-wake cycles. The circadian rhythms of VS patients were significantly more impaired than those of MCS patients, as were the circadian rhythms of patients with non-traumatic injuries relative to those with traumatic injuries. The reliability of the circadian rhythms were significantly predicted by the patients' levels of visual and motor functioning, consistent with the putative biological generators of these rhythms.

Conclusions

The high variability across diagnoses and etiologies highlights the need for improved guidelines for the assessment of sleep-wake cycles in VS and MCS, and advocates the use of actigraphy as an inexpensive and non-invasive alternative.

【 授权许可】

   
2013 Cruse et al; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Laureys S, Celesia GG, Cohadon F, Lavrijsen J, Leon-Carrion J, Sannita WG, Sazbon L, Schmutzhard E, von Wild KR, Zeman A, Dolce G: Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med 2010, 8:68. BioMed Central Full Text
• [2]Laureys S: The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn Sci 2005, 9:556-559.
• [3]Jennett B, Plum F: Persistent vegetative state after brain damage. A syndrome in search of a name. Lancet 1972, 1:734-737.
• [4]Giacino JT, Kalmar K, Whyte J: The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 2004, 85:2020-2029.
• [5]The Multi-Society Task Force on PVS: Medical aspects of the persistent vegetative state (1). N Engl J Med 1994, 330:1499-1508.
• [6]Royal College of Physicians: The permanent vegetative state. Review by a working group convened by the Royal College of Physicians and endorsed by the Conference of Medical Royal Colleges and their faculties of the United Kingdom. J R Coll Physicians Lond 1996, 30:119-121. Updated 2003
• [7]Giacino JT, Ashwal S, Childs N, Cranford R, Jennett B, Katz DI, Kelly JP, Rosenberg JH, Whyte J, Zafonte RD, Zasler ND: The minimally conscious state: definition and diagnostic criteria. Neurology 2002, 58:349-353.
• [8]Owen AM, Coleman MR, Boly M, Davis MH, Laureys S, Pickard JD: Detecting awareness in the vegetative state. Science 2006, 313:1402.
• [9]Monti MM, Vanhaudenhuyse A, Coleman MR, Boly M, Pickard JD, Tshibanda L, Owen AM, Laureys S: Willful modulation of brain activity in disorders of consciousness. N Engl J Med 2010, 362:579-589.
• [10]Cruse D, Chennu S, Chatelle C, Bekinschtein TA, Fernández-Espejo D, Pickard JD, Laureys S, Owen AM: Bedside detection of awareness in the vegetative state - a cohort study. Lancet 2011, 378:2088-2094.
• [11]Refinetti R: Circadian Physiology. Boca Raton, FL: Taylor & Francis Group; 2006.
• [12]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, 26:342-392.
• [13]Landsness E, Bruno MA, Noirhomme Q, Riedner B, Gosseries O, Schnakers C, Massimini M, Laureys S, Tononi G, Boly M: Electrophysiological correlates of behavioural changes in vigilance in vegetative state and minimally conscious state. Brain 2011, 134:2222-2232.
• [14]Isono M, Wakabayashi Y, Fujiki MM, Kamida T, Kobayashi H: Sleep cycle in patients in a state of permanent unconsciousness. Brain Inj 2002, 16:705-712.
• [15]Fukudome Y, Abe I, Saku Y, Matsumura K, Sadoshima S, Utunomiya H, Fujishima M: Circadian blood pressure in patients in a persistent vegetative state. Am J Physiol 1996, 270:R1109-1114.
• [16]Pattoneri P, Tirabassi G, Pela G, Astorri E, Mazzucchi A, Borghetti A: Circadian blood pressure and heart rate changes in patients in a persistent vegetative state after traumatic brain injury. J Clin Hypertens (Greenwich) 2005, 7:734-739.
• [17]Guan J, You C, Liu Y, Zhang R, Wang Z: Characteristics of infradian and circadian rhythms in the persistent vegetative state. J Int Med Res 2011, 39:2281-2287.
• [18]Oksenberg A, Arons E, Sazbon L, Mizrahi A, Radwan H: Sleep-related erections in vegetative state patients. Sleep 2000, 23:953-957.
• [19]Candelieri A, Cortese MD, Dolce G, Riganello F, Sannita WG: Visual pursuit: within-day variability in the severe disorder of consciousness. J Neurotrauma 2011, 28:2013-2017.
• [20]Bekinschtein TA, Golombek DA, Simonetta SH, Coleman MR, Manes FF: Circadian rhythms in the vegetative state. Brain Inj 2009, 23:915-919.
• [21]de Souza L, Benedito-Silva AA, Pires ML, Poyares D, Tufik S, Calil HM: Further validation of actigraphy for sleep studies. Sleep 2003, 26:81-85.
• [22]Berger AM, Wielgus KK, Young-McCaughan S, Fischer P, Farr L, Lee KA: Methodological challenges when using actigraphy in research. J Pain Symptom Manage 2008, 36:191-199.
• [23]Spivak E, Oksenberg A, Catz A: The feasibility of sleep assessment by actigraph in patients with tetraplegia. Spinal Cord 2007, 45:765-770.
• [24]Brown A, Smolensky M, D'Alonzo G, Redmond D, Conrad E, Hsi B: Circadian rhythm in human activity objectively quantified by actigraphy. Prog Clin Biol Res 1990, 341A:77-83.
• [25]Girardin J-L, Kripke DF, Ancoli-Israel S, Klauber MR, Sepulveda RS, Mowen M-A, Assmus JD, Langer RD: Circadian sleep, illumination, and activity patterns in women: influences of aging and time reference. Physiol Behav 2000, 68:347-352.
• [26]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.
• [27]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, 18:1432-1434.
• [28]Nelson W, Tong YL, Lee JK, Halberg F: Methods for cosinor-rhythmometry. Chronobiologia 1979, 6:305-323.
• [29]Saper CB, Scammell TE, Lu J: Hypothalamic regulation of sleep and circadian rhythms. Nature 2005, 437:1257-1263.
• [30]Schiff ND: Central thalamic contributions to arousal regulation and neurological disorders of consciousness. Ann N Y Acad Sci 2008, 1129:105-118.
• [31]Fernandez-Espejo D, Junque C, Bernabeu M, Roig-Rovira T, Vendrell P, Mercader JM: Reductions of thalamic volume and regional shape changes in the vegetative and the minimally conscious states. J Neurotrauma 2010, 27:1187-1193.
• [32]Fernández-Espejo D, Bekinschtein T, Monti MM, Pickard JD, Junque C, Coleman MR, Owen AM: Diffusion weighted imaging distinguishes the vegetative state from the minimally conscious state. NeuroImage 2011, 54:103-112.
• [33]Adams JH, Graham DI, Murray LS, Scott G: Diffuse axonal injury due to nonmissile head-injury in humans - an analysis of 45 cases. Ann Neurol 1982, 12:557-563.
• [34]Kinney HC, Samuels MA: Neuropathology of the persistent vegetative state. A review. J Neuropathol Exp Neurol 1994, 53:548-558.
• [35]Adams JH, Jennett B, McLellan DR, Murray LS, Graham DI: The neuropathology of the vegetative state after head injury. J Clin Pathol 1999, 52:804-806.
• [36]Jennett B, Adams JH, Murray LS, Graham DI: Neuropathology in vegetative and severely disabled patients after head injury. Neurology 2001, 56:486-490.
• [37]Adams JH, Duchen LW: Greenfield's Neuropathology. 5th edition. New York, New York: Oxford University Press; 1992.
• [38]Adams JH, Graham DI, Jennett B: The neuropathology of the vegetative state after an acute brain insult. Brain 2000, 123:1327-1338.
• [39]Kinney HC, Korein J, Panigrahy A, Dikkes P, Goode R: Neuropathological findings in the brain of Karen Ann Quinlan. The role of the thalamus in the persistent vegetative state. N Engl J Med 1994, 330:1469-1475.
• [40]Veasey SC, Davis CW, Fenik P, Zhan G, Hsu YJ, Pratico D, Gow A: Long-term intermittent hypoxia in mice: protracted hypersomnolence with oxidative injury to sleep-wake brain regions. Sleep 2004, 27:194-201.
• [41]Shochat T, Martin J, Marler M, Ancoli-Israel S: Illumination levels in nursing home patients: effects on sleep and activity rhythms. J Sleep Res 2000, 9:373-379.
• [42]Ancoli-Israel S, Martin JL, Kripke DF, Marler M, Klauber MR: Effect of light treatment on sleep and circadian rhythms in demented nursing home patients. J Am Geriatr Soc 2002, 50:282-289.
• [43]Campbell SS, Kripke DF, Gillin JC, Hrubovcak JC: Exposure to light in healthy elderly subjects and Alzheimer's patients. Physiol Behav 1988, 42:141-144.
• [44]Giacino J, Whyte J: The vegetative and minimally conscious states: current knowledge and remaining questions. J Head Trauma Rehabil 2005, 20:30-50.