Sleep patterns associated with the severity of impairment in a large cohort of patients with chronic disorders of consciousness

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Highlights

  • PSG is a reliable means of studying chronic DOC patients.

  • UWS/VS patients with even severe impairment show residual sleep patterns.

  • The presence of slow-wave sleep is correlated with high CRS-R scores.

Abstract

Objective

We assessed sleep patterns in 85 patients with chronic disorders of consciousness (DOC) in order to reveal any relationship with the degree of the impairment.

Methods

Nocturnal polysomnography (PSG) was scored in patients classified as being in an unresponsive wakefulness syndrome/vegetative state (UWS/VS; n = 49) or a minimally conscious state (MCS; n = 36) in accordance with the rules of the American Academy of Sleep Medicine. The PSG data in the two diagnostic groups were compared, and the PSG parameters associated with the degree of impairment were analysed.

Results

In 19/49 UWS/VS patients, signal attenuation was the only EEG pattern detectable in sleep. Non-REM 2 (NREM2) and slow-wave sleep (SWS) (but not REM) stages were more frequent in the MCS patients. The presence of SWS was the most appropriate factor for classifying patients as UWS/VS or MCS, and the duration of SWS was the main factor that significantly correlated with revised Coma Recovery Scale scores.

Conclusion

The presence of NREM sleep (namely SWS) reflects better preservation of the circuitry and structures needed to sustain this stage of sleep in DOC patients.

Significance

PSG is a simple and effective technique, and sleep patterns may reflect the degree of impairment in chronic DOC patients.

Introduction

Brain injury due to severe anoxic, hemorrhagic or traumatic events often lead to chronic disorders of consciousness (DOCs), which have recently received increasing attention because of growing medical and ethical concerns relating to patient management. A considerable proportion of survivors of severe brain damage enter an unresponsive wakefulness syndrome/vegetative state (UWS/VS) or minimally conscious state (MCS) (Laureys et al., 2010) and a number of studies have assessed more or less extensive series of DOC patients using imaging procedures or neurophysiological evaluations designed to provide information supporting the clinical assessment of different degrees of DOCs or to identify prognostic markers (see reviews by Bender et al., 2015, Kondziella et al., 2015).

One significant advantage of sleep evaluation arises from the fact that long polysomnographic (PSG) recordings are easy to make at a patient’s bedside as they do not need complex technical support. Each study and each technique has its advantages and limitations, but evidence collected over the last 50 years (Bergamasco et al., 1968, Evans and Bartlett, 1995, Valente et al., 2002, Landsness et al., 2011, Malinowska et al., 2013, Cologan et al., 2010, Cologan et al., 2013, De Biase et al., 2014, Arnaldi et al., 2016, Pavlov et al., 2017) indicates that electro-encephalography (EEG) and PSG recordings can contribute to predicting outcomes in patients observed shortly after the time of their brain injury and help in the differential diagnosis of MCS and UWS/VS. As a whole, studies of DOC patients have found that sleep patterns in MCS patients are better preserved than those UWS/VS patients, although significant differences can be found. One of the most important and cited studies by Landsness et al. (2011) did not find any markers of sleep in UWS/VS patients, thus supporting the idea that they only show behavioural signs of sleep, whereas a recent study by Pavlov et al. (2017) found that UWS/VS patients may retain circadian changes and show sleep patterns such as rapid eye movement (REM) and slow wave sleep (SWS) even in some patients with very severe clinical impairment or long-lasting illness.

Our previous neurophysiological study of chronic DOC patients found that a simple sleep score was one of the most effective parameters even in the case of extremely severe conditions, and that it was suitable for classifying the severity of brain damage and subsequent DOC (Rossi Sebastiano et al., 2015). However, this study had the limitations that sleep was only roughly classified using a semi-quantitative scale (Synek, 1988), in order to compare it with the other neurophysiological measures, and was not scored as suggested by the guidelines of the American Academy of Sleep Medicine (AASM).

The present study describes the specific and sometimes particular PSG patterns observed during whole-night recordings of 85 patients with chronic DOCs (classified on the basis of the AASM guidelines, Iber et al., 2007), and was carried out in order to assess their value in supporting clinical evaluations: the PSG data of the patients with UWS/VS or MCS group were compared, and the PSG parameters associated with the degree of the clinical impairment were analysed.

Section snippets

Patients

The study involved 85 patients consecutively admitted to Carlo Besta Neurological Institute, who were evaluated by the staff of the Coma Research Centre between January 2012 and February 2014. The DOC patients were scored using the Italian version of the revised Coma Recovery Scale (CRS-R) (Lombardi et al., 2007), and were as being in a UWS/VS (54 patients aged 49.4 ± 14.4 years, 17 women; time since the acute brain insult 35.9 ± 41.2 months) or MCS (31 patients aged 49.5 ± 14.1 years; 16

Results

Table 1, Table 2 summarise the PSG data of the MCS and UWS/VS groups. The agreement between raters was high, 4,8% of uncertain epochs and arousals were removed from the subsequent analyses. TST ranged from 21 to 515 minutes (mean 184.7 ± 110.6 minutes), and was significantly longer in the MCS patients. Even in the case of long-lasting sleep, its course seemed to be fragmentary and was interrupted by repeated arousals and phase transitions, with no statistically significant difference between

Discussion

The aim of this study was to assess sleep patterns in patients with chronic DOC in order to identify the parameters that are potentially capable of supporting clinical scores. The sleep of all of the studied DOC patients was quite short, fragmented by a number of phase transitions, and interrupted by repeated arousals. Nevertheless, we found that most chronic UWS/VS or MCS patients undergoing protracted PSG recordings including one night show modulated PGS changes indicating the occurrence of

Conclusion

In conclusion, our findings support the hypothesis that PSG recordings and staging can contribute to the assessment of patients with chronic DOCs and, despite the sleep fragmentation and repeated artefacts due to frequent arousals, that the visual evaluation of PSG traces is a simple and reliable method of assessment. We also believe that our findings can contribute to improving our understanding of the functional conditions underlying sleep patterns in patients with highly destructive brain

Conflicts of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest. We confirm that we have read the Journal’s position on issues involved in ethical publication and we affirm that our report is consistent with those guidelines.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The Coma Research Centre (CRC) project was funded by Grant No. IX/000407 0150 05/08/2010 from Lombardy Regional Government (Italy).

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