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Predictive Value of EEG-Awakening for Behavioral Awakening from Coma

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Predictive Value of EEG-Awakening for Behavioral Awakening from Coma Kang et al. Ann. Intensive Care (2015) 5:52 DOI 10.1186/s13613-015-0094-4 RESEARCH Open Access Predictive value of EEG‑awakening for behavioral awakening from coma Xiao‑gang Kang, Feng Yang, Wen Li, Chen Ma, Li Li* and Wen Jiang* Abstract Background: A reliable predictor for early recovery of consciousness in comatose patients is of great clinical signifi‑ cance. Here we aimed to investigate the potentially prognostic value of electroencephalogram-reactivity (EEG-R) in combination with sleep spindles, termed EEG-awakening, for behavioral awakening in etiologically diverse comatose patients. Methods: We performed a prospectively observational study on a sample of patients, all of whom were in coma last‑ ing longer than 3 days. Continuous EEG monitoring was performed for at least 24 h to detect the presence of EEG-R and sleep spindles. We then followed patients for 1 month to determine their subsequent level of consciousness, classifying them as either awakened or non-awakened. Finally, Univariate and multivariate analyses were employed to assess the association of predictors with consciousness recovery. Results: One hundred and six patients with different etiologies leading to coma were included in the study. Of these, 48 patients (45.3 %) awoke and 58 patients (54.7 %) did not awake in the month after the onset of the study. Of note, 26 patients (24.5 %) had a good neurological outcome, and 31 patients (29.3 %) died. Univariate analysis revealed that the Glasgow Coma Scale (GCS) score, EEG-R, sleep spindles, and EEG-awakening were all associated with one-month awakening. Comparisons of the area under the receiving operator characteristic curve (AUC) showed that EEG- awakening (0.839; 0.757–0.921) was superior to all of the following: EEG-R (0.798; 0.710–0.886), sleep spindles (0.772; 0.680–0.864), and GCS scores (0.720; 0.623–0.818). However, age, gender, etiology, and pupillary light reflex did not correlate significantly with one-month awakening. Further logistic regression analysis showed that only EEG-awak‑ ening and GCS scores at study entry were significant independent predictors of awakening and that the prognostic model containing these two variables yielded an outstanding predictive performance with an AUC of 0.903. Conclusions: EEG-awakening incorporates both EEG-R and sleep spindles and is an excellent predictor for early behavioral awakening in comatose patients. The prognostic model combining EEG-awakening and GCS scores shows an outstanding discriminative power for awakening. Keywords: Coma, Prognosis, Electroencephalogram reactivity, Sleep spindles Background common causes of coma include traumatic brain injury, Coma is a severe disorder of consciousness that is char- anoxic encephalopathy, vascular, metabolic, or infectious acterized by a deficiency of behavioral responsiveness diseases. Acute coma is a major reason of Neurological as well as disturbances in sleep-wake cycles that include Intensive Care Unit (N-ICU) admissions and carries high extended periods of eye closure and muscle inactivity mortality, and neuro-cognitive morbidity, with patients [1]. It is a leading cause of death and disability, and can often suffering from subsequent disability [3, 4]. For result from diffuse bihemispheric cortical or white-mat- therapeutic, ethical, and economic reasons, family mem- ter damage, or from focal brainstem lesions [2]. The most bers consistently ask when, or if, a patient will wake up, i.e., regain consciousness [5]. Despite improvements in *Correspondence: [email protected]; [email protected] neurocritical care, electrophysiology, and neuroimaging, Department of Neurology, Xijing Hospital, Fourth Military Medical University, Xi’an 710032, China © 2015 Kang et al. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Kang et al. Ann. Intensive Care (2015) 5:52 Page 2 of 8 accurate prediction for consciousness recovery in coma- functional disabilities up to time of the injury; (2) spinal tose patients remains challenging [6–8]. cord impairment; (3) severe, coexisting systemic disease Consciousness is a multifaceted concept, but has tra- with a limited life expectancy; (4) EEG showing non-con- ditionally been divided into two main components:: vulsive status epilepticus. All patients received standard arousal (i.e., wakefulness, or vigilance) and awareness intensive care and were followed for 1 month after entry (e.g., awareness of the environment and of the self) [2]. into the study, for which the last-observed-carried-for- Arousal reflects a function of the ascending reticular ward principle was designed to deal with missing data at activating system (ARAS) [9], while awareness is more the follow-up as it was needed. complicated and has been attributed to the functional integrity of the cerebral cortex and its subcortical con- EEG recording nections [10, 11]. Given this stratification, arousal is Bedside video-EEG (Solar 2000 N, Solar Electronic Tech- taken as a prerequisite for awareness [9]. Thus, to achieve nologies Co., Ltd, Beijing, China) was performed within a more accurate prediction of consciousness recovery, we 3 days of N-ICU admission. Briefly, an array of 20 scalp need to develop an objective test based on the functional electrodes were arranged according to the international assessment of both ARAS and cortical network integrity. 10–20 system and was then continuously recorded for Electroencephalogram (EEG) is the neurological main- at least 24 h. Sedatives and/or anesthetic agents (dexme- stay of electrophysiological testing and has been regarded detomidine or midazolam) were discontinued for at least as a useful and promising tool in determining the prog- 12 h and no patient was under hypothermic therapy at nosis of comatose patients. Continuous EEG is increas- the time of EEG recordings. EEG findings were catego- ingly used in N-ICU to directly and dynamically monitor rized according to the presence or absence of the follow- brain functioning. Given that EEG reactivity (EEG-R) to ing: (1) EEG-R, defined as a clear, reproducible change in external stimuli can be interpreted as a sign of function- either the background frequency or amplitude following ing of some cortical areas [12] and that sleep spindles in repetitive auditory and nociceptive stimulations. This EEG may reflect the preserved functional integrity of the excluded “stimulus-induced-evolving lateralized rhyth- ARAS [13], we sought to predict awakening in a cohort mic delta activity” or induction of muscle artifacts alone of etiologically diverse comatose patients by integrating [15]. (2) Sleep spindles, defined as waxing–waning wave- these two parameters. forms with a frequency ranging from 12 to 16 Hz, dura- Corresponding to traditional awakening, which is tion between 0.5 and 2 s, and occurring in the context of characterized by the presence of behavioral respon- EEG activity [1]. (3) EEG-awakening, defined as the pres- siveness and sleep-wake cycles, we propose a new EEG ence of both EEG-R and sleep spindles. All EEG record- term: EEG-awakening, as defined by the presence of ings were interpreted by two EEG-certified neurologists both EEG-R and sleep spindles. In the following study, (J.B. and X.X.) who were blind to all clinical data. Agree- we examined the predictive value of EEG-awakening for ment was determined with the unweighted Cohen kappa behavioral awakening in comatose patients. statistic. Methods Predictor variable and outcome definitions Patients We based our clinical and EEG variables on available We conducted a prospective study that enrolled consecu- observation in all selected patients. As a result, the fol- tive comatose patients admitted from March 2009 to lowing variables were systematically assessed for each March 2013 to the N-ICU at one of the largest hospitals patient: age, gender, etiology, pupillary light reflex, in Northwestern China, Xijing Hospital, Fourth Mili- Glasgow Coma Scale (GCS) score on admission to the tary Medical University. The ethics committee of Xijing N-ICU, EEG-R, and sleep spindles. Pupillary light reflex Hospital approved all parameters for the study, includ- was observed in response to 1-second stimuli of blue ing a waiver for informed consent since the study design light at 5 cm distance under natural light during daytime did not modify usual medical practices. We adhered to a in the ward of N-ICU. Patients were evaluated daily for strict definition of “coma” as originally defined by Plum 1 month after entry into the study to determine recov- and Posner [14] as: a complete lack of awareness of the ery of consciousness, at which point they either stayed environment, no eye opening in response to external in the N-ICU or were transferred to the neurorehabilita- stimuli, and no purposeful movement to noxious stimu- tion ward. Recovery of consciousness was defined as the lation. The patients with acute coma for more than 3 days patient’s ability to show a clearly discernible evidence were included in this study. Exclusion criteria were as of self or environmental awareness and was assessed follows: (1) premorbid history of developmental, psy- according to clinical criteria for minimally conscious state chiatric, or neurological illness resulting in documented (MCS) and for emergence from MCS [16], confirmed by Kang et al. Ann. Intensive Care (2015) 5:52 Page 3 of 8 Coma Recovery Scale–Revised (CRS-R) [17]. In order to Table 1 Patient characteristics of the 106 patients improve diagnostic accuracy, each patient was evaluated Characteristic Value at least five times by CRS-R. For the purpose of statistical analysis, we classified patients into those who recovered Age, year, mean (SD) 50.9 (20.9) consciousness (awakened group) and those who did not Gender, male, no.
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