Sleep and pathological wakefulness at time of liberation We conducted a prospective multicenter...

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    Sleep and pathological wakefulness at time of liberation

    from mechanical ventilation

    Martin Dres1,2, Magdy Younes3,4, Nuttapol Rittayamai1,5, Tetyana Kendzerska6, Irene Telias1,

    Domenico Luca Grieco1, Tai Pham1, Detajin Junhasavasdikul1, Edmond Chau1, Sangeeta

    Mehta8,11, M. Elizabeth Wilcox9,11, Richard Leung7, Xavier Drouot10, Laurent Brochard1,11

    1Keenan Research Centre, Li Ka Shing Knowledge Institute, St. Michael's Hospital, Toronto, Canada 2AP-HP, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Service de Pneumologie, Médecine intensive – Réanimation (Département "R3S"), F-75013, Paris, France 3YRT Ltd, Winnipeg, Manitoba, Canada 4Sleep Disorders Centre, Winnipeg, Manitoba, Canada 5Division of Respiratory Diseases and Tuberculosis, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, Thailand 6Division of Respirology, the Ottawa Hospital Research Institute, Ottawa, Canada 7Respirology and Sleep laboratory, St Michael’s Hospital, Toronto 8Intensive Care Unit, Mount Sinai Hospital, Toronto, Canada 9Department of Medicine (Critical Care), Toronto Western Hospital, Toronto 10CHU de Poitiers, Neurophysiologie clinique et Explorations fonctionnelles, Poitiers, France 11Interdepartmental Division of Critical Care Medicine, University of Toronto, Canada Address for correspondence Laurent Brochard Medical and Surgical Intensive Care Unit St Michael’s Hospital 209 Victoria Street, 4th Floor, Room 4-079, Toronto, ON M5B 1T8 Toronto, Canada E-mail: BrochardL@smh.ca Phone: +1 416 864 5686

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    mailto:BrochardL@smh.ca

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    Authors’ contributions:

    MD, NR, RL and LB designed the study. MD coordinated the study. MD, IT, DLG, TP, EC, SM,

    MEW, DJ and LB were responsible for patient screening, enrolment and follow-up. MD, MY,

    XD and LB analysed the data. XD, MY and TK scored PSG. MD, MY and LB wrote the manuscript.

    All authors had full access to all of the study data, contributed to drafting the manuscript or

    critically revised it for important intellectual content, approved the final version of the

    manuscript, and took responsibility for the integrity of the data and the accuracy of the data

    analysis.

    Funding:

    MD was supported by The French Intensive Care Society (SRLF bourse de mobilité 2015); The

    2015 Short Term Fellowship program of the European Respiratory Society; The 2015 Bernhard

    Dräger Award for advanced treatment of ARF of the European Society of Intensive Care

    Medicine; The Assistance Publique Hôpitaux de Paris; The Fondation pour la Recherche

    Médicale (FDM 20150734498) and by MitacsGlobalink Sorbonne Universités. LB holds the

    Keenan Chair in Critical Care and Acute Respiratory Failure.

    Running head: Pathological wakefulness and separation from mechanical ventilation

    Descriptor number: 4.13 Ventilation: Non-Invasive/Long-Term/Weaning.

    Word count: 4042

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    This article has an online data supplement, which is accessible from this issue's online table

    of contents.

    Conflict of interest: Martin Dres received personal fees from Pulsion Medical System and

    Lungpacer. Laurent Brochard’s laboratory has research contracts with Covidien (PAV), Air

    Liquide (CPR), Philips (equipment for sleep), Fisher Paykel (high flow therapy). Magdy Younes

    is the inventor of the ORP technology and receives royalties and consultation fees from

    Cerebra Health, the exclusive licensee of the technology. Nuttapol Rittayamai received a grant

    from his home institution in Thailand. The other authors have no conflict of interest relevant

    to this study.

    At a glance commentary

    Scientific Knowledge on the Subject:

    Critically ill patients can develop EEG abnormalities in the intensive care unit. The impact of

    these abnormalities at the time of liberation from mechanical ventilation is poorly established.

    We conducted standard polysomnography and calculated the odds ratio product (ORP), which

    is a continuous index evaluating sleep depth, 15 hours before a spontaneous breathing trial

    (SBT) in patients deemed ready to attempt liberation from mechanical ventilation.

    What this Study Adds to the Field:

    Abnormal patterns of sleep and wakefulness were highly prevalent and sleep scoring by

    conventional criteria did not differ between patients with successful and failed SBT. By

    contrast, the level of wakefulness, as assessed by the ORP, was significantly higher in

    patients with successful SBT. Poor correlation between sleep depth in right vs. left

    hemispheres predicted SBT failure.

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    Abstract

    Background

    Abnormal patterns of sleep and wakefulness exist in mechanically ventilated patients. This

    study aimed at investigating polysomnographic indexes as well as a continuous index

    evaluating sleep depth, the odds ratio product (ORP), to determine whether abnormal sleep

    or wakefulness are associated with the outcome of spontaneous breathing trials (SBT).

    Methods

    Mechanically ventilated patients at three sites were enrolled if an SBT was planned the

    subsequent day. Electroencephalogram was recorded using a portable sleep diagnostic device

    15 hours prior to SBT. ORP was calculated from the power of 4 electroencephalogram

    frequency bands relative to each other: it ranges from full wakefulness (2.5) to deep sleep (0).

    Correlation between right and left hemispheres ORP (R/L) was calculated.

    Results

    Among 44 patients enrolled, 37 had technically adequate signals: eleven (30%) passed the SBT

    and were extubated, 8 (21%) passed the SBT but were not deemed clinically ready for

    extubation, and 18 (49%) failed the SBT. Pathological wake or atypical sleep were highly

    prevalent but distribution of classical sleep stages was similar between groups. The mean ORP

    and the proportion of time that the ORP was >2.2 were higher in extubated patients compared

    to the other groups (P

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    Keywords: weaning, delirium, sedation, extubation, mechanical ventilation

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    Introduction

    Patients under mechanical ventilation in the intensive care unit (ICU) present a variety

    of electroencephalographic (EEG) abnormalities both during wakefulness and sleep (1–3).

    Excessive sleep fragmentation, reduced REM sleep and loss of normal circadian rhythm are

    consistent across studies, suggesting frequent sleep deprivation (3–5). The EEG during

    behaviorally-confirmed wakefulness is often abnormal in ICU patients, with an increase in

    slow wave activity (seen during sleep in outpatients) and decrease in activity of higher

    frequencies that characterize wakefulness (1,3,6,7). This pattern has been called “pathological

    wakefulness”. Patients with pathological wakefulness also often show atypical EEG patterns

    during sleep with marked reduction in EEG spindles and K complexes that help differentiate

    different stages of non-REM sleep; this is referred to as “atypical sleep” (6). Accordingly, in

    many ICU patients, it is difficult to distinguish wakefulness from sleep from the EEG alone

    using the standard rules (7). The high prevalence of sleep loss/disruption in these patients,

    and the fact that similar EEG changes are observed with experimental sleep deprivation (8,

    9),suggest that sleep loss is an important contributing factor to these EEG abnormalities (10).

    A recent study found that weaning time is longer in difficult-to-wean patients who

    have atypical sleep than in those who display normal sleep patterns (11). Reasons for failing a

    spontaneous breathing trial (SBT) are multifactorial (12, 13). Sleep deprivation may be a risk

    factor for weaning-failure since it can reduce ventilatory responses to hypoxemia (14) and

    decrease respiratory muscle endurance (15), impair immune responses (16, 17),

    cardiovascular responses (18), neuroendocrine and metabolic function (19, 20),

    neurocognitive function (21), and increase the incidence of delirium (22, 23).

    In this study we evaluated the EEG of mechan