Beruflich Dokumente
Kultur Dokumente
ABSTRACT
Background: The decision to extubate brain-injured patients with residual impaired consciousness holds a high degree of uncer-
tainty of success. The authors developed a pragmatic clinical score predictive of extubation failure in brain-injured patients.
Methods: One hundred and forty brain-injured patients were prospectively included after the first spontaneous breathing trial
success. Assessment of multiparametric hemodynamic, respiratory, and neurologic functions was performed just before extu-
bation. Extubation failure was defined as the need for ventilatory support during intensive care unit stay. Extubation failure
within 48h was also analyzed. Neurologic outcomes were recorded at 6 months.
Results: Extubation failure occurred in 43 (31%) patients with 31 (24%) within 48h. Predictors of extubation failure con-
sisted of upper-airway functions (cough, gag reflex, and deglutition) and neurologic status (Coma Recovery Scale-Revised
visual subscale). From the odds ratios, a four-item predictive score was developed (area under the curve, 0.85; 95% CI, 0.77
to 0.92) and internally validated by bootstrap. Cutoff was determined with sensitivity of 92%, specificity of 50%, positive
predictive value of 82%, and negative predictive value of 70% for extubation failure. Failure before and beyond 48h shared
similar risk factors. Low consciousness level patients were extubated with 85% probability of success providing the presence
of at least two operating airway functions.
Conclusions: A simplified clinical pragmatic score assessing cough, deglutition, gag reflex, and neurologic status was devel-
oped in a preliminary prospective cohort of brain-injured patients and was internally validated (bootstrapping). Extubation
appears possible, providing functioning upper airways and irrespective of neurologic status. Clinical practice generalizability
urgently needs external validation. (Anesthesiology 2017; 126:104-14)
sciousness with impaired airway protective reflexes such as What This Article Tells Us That Is New
cough and deglutition, neuromuscular weakness or paraly-
A simplified score, comprised coughing, swallowing, and gag
sis, and hypersecretion.3 In general critical care medicine, function, in combination with visual function subscale of the
it is usually assumed that restored conscious behavior is a Coma Recovery Scale Revised, was developed; the total
prerequisite to extubation.46 While separation from MV is score was correlated with successful tracheal extubation.
generally easily acquired in brain-injured patients without This clinically pragmatic score can be easily developed. External
validation of its predictive value, however, is necessary.
other comorbidity,7 extubation failure is frequent.8 Never-
theless, some patients with severe alteration of conscious-
ness could be extubated with success, and burden may be focalization on different components of the problem: ven-
associated with extubation delay.9 Few studies investigated tilatory parameters or global neurologic evaluation without
predictive factors implicated in extubation failure with clear predictors.1,8,1013 For example, Glasgow Coma Scale
This article is featured in This Month in Anesthesiology, page 1A. Supplemental Digital Content is available for this article. Direct URL
citations appear in the printed text and are available in both the HTML and PDF versions of this article. Links to the digital files are provided
in the HTML text of this article on the Journals Web site (www.anesthesiology.org). T.G. and R.C. contributed equally to this article.
Submitted for publication April 4, 2016. Accepted for publication September 6, 2016. From the Department of Perioperative Medicine
(T.G., R.C., J.M., S.K., E.F., J.-M.C.) and Biostatistics Unit, DRCI, Gabriel Montpied Hospital (B.P.), University Hospital of Clermont-Ferrand,
Clermont-Ferrand, France; and Retinoids, Reproduction and Developmental Disease (R2D2) Unit, EA 7281, University of Clermont-Ferrand
1, Clermont-Ferrand, France (T.G., E.F., J.-M.C.).
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. All Rights Reserved. Anesthesiology 2017; 126:104-14
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
<zdoi;10.1097/ALN.0000000000001379>
CRITICAL CARE MEDICINE
(GCS), in which low values often appear as limitative factors Medical, paramedical, and physiotherapist staff were
to extubation, is difficult to evaluate in intubated patients aware of the study protocol, which consisted of routine care
and patients ability to be an indicator of precise neurologic in the studied ICUs.
function is limited.14,15 As a consequence, no guideline Since all three ICUs were affiliated with the Depart-
exists in this specific population and practice variations are ment of Perioperative Medicine of the University Hospital
frequent between institutions.1 To characterize risk factors of Clermont-Ferrand, Clermont-Ferrand, France, with the
associated with extubation failure in brain-injured patients, same medical and paramedical leadership and steward-
we conducted a prospective, monocentric, observational ship, protocols related to brain-injured patients were the
study with multiparametric assessment of demographic, same. The weaning protocol followed European guidelines
neurologic, hemodynamic, and respiratory functions. The of weaning from MV for general ICU patients.4 Notably,
objective of the study was to develop and internally validate it was assumed that no tracheostomy was performed before
a simplified pragmatic score predictive of extubation failure any extubation attempt, unless the patient failed more than
in this category of patients. Some of the results of this study three spontaneous breathing trials (SBT). After resolution of
have been previously reported in the form of an abstract.16,17 acute organ dysfunctions notably increased intracranial pres-
sure and sedative drugs withdrawal, eligibility for a SBT was
Materials and Methods daily assessed. Patients were extubated when they succeeded
SBT irrespective of their neurologic status and upper-airway
Additional details are provided in the online Supplemen- function.9 At the end of a successful SBT, previous venti-
tal Digital Content (http://links.lww.com/ALN/B322). latory parameters were resumed during clinical evaluation
Clinical trial is registered with http://www.clinicaltrials.gov related to the study. Extubation and respiratory care fol-
(NCT 02235376). lowed regular guidelines and were provided by a respiratory
therapist during daytime. No prophylactic noninvasive ven-
Ethics Statement tilation (NIV) was used. If needed, standard oxygen therapy
Protocol was approved by Regional Ethics Committee was initiated after extubation without high-flow devices.
(Comit dEthique des Centres dInvestigation Clinique, Time between the end of a successful SBT and extubation
Rhne-Alpes-Auvergne, Grenoble, France, IRB 5921) on did not last more than 1h. Local standard of care prevented
June 19, 2013. Because of the observational design of this delayed extubation after a passed SBT. All SBT procedures
study, which consisted of routine care in the studied intensive were reviewed on electronic patient records by two investiga-
care units (ICUs), the need for written consent was waived. tors not in charge of patient care (J.M.C. and E.F.) in order
An information letter concerning the study was given to the to look for possible delayed extubations. Additionally, data
patient or a next of kin after recovery. from tracheostomized patients were also reviewed in order to
verify they previously failed at least three SBTs.
Patients and Setting Extubation failure was defined as the need for ventila-
The study was performed in a 13-bed neuro-ICU and 2 tory support after extubation using tracheal intubation or
general ICUs (17 and 15 beds, respectively) of a university NIV4 during ICU stay. Respiratory failure necessitating
hospital. All consecutives brain-injured adult patients with reventilation was defined as the occurrence of at least two
initial GCS less than or equal to 12 (before tracheal intu- signs among oxygen therapy greater than 9 Lmin1 to main-
bation), intubated for neurologic reason and ventilated for tain oxygen saturation measured by pulse oximetry greater
more than 48h, were screened between June 2013 and Feb- than 90%, respiratory rate greater than 35min1 with acces-
ruary 2015 (18-month period). Patients with brain struc- sory respiratory muscles involvement, respiratory or cardiac
tural lesions (isolated traumatic brain injury, subarachnoid arrest, major tracheal secretions with inadequate cough,
hemorrhage, supra- or infratentorial spontaneous intrace- Paco2 greater than 50 mmHg with pH less than 7.35, heart
rebral hematoma, supra- or infratentorial acute ischemic rate greater than 120min1, systolic blood pressure greater
stroke, or hypoxicischemic encephalopathy due to cardiac than 200 mmHg or less than 90 mmHg. Analyses of extuba-
arrest) eligible for extubation were included. Patients with tion failure before 48h as classically defined4 and at any time
spinal cord injury, status epilepticus, disorder of conscious- during ICU stay were performed. Justifications of those tim-
ness caused by alcohol or other intoxication, central nervous ings are presented in the Discussion.
system infection, tracheostomy, autoextubation, and with- Numerous clinical and paraclinical data were collected
drawal of care due to ethical reason were not included. Fol- before extubation (see Methods and Data Collection in
low-up of included patients was 6 months to assess Glasgow Supplemental Digital Content, http://links.lww.com/ALN/
Outcome Scale. B322, which extensively expose collected clinical and para-
clinical data). Of note, neurologic assessment included GCS
Weaning and Extubation Protocol with one point for verbal (total score on 10 points due to
Detailed protocols are provided in the online Supplemental inability to assess verbal component of the score with tracheal
Digital Content (http://links.lww.com/ALN/B322). intubation),18 Full Outline of UnResponsiveness (FOUR)
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Extubation Failure in Brain-injured Patients
score with three components (eyes, motor, and brainstem model were independently estimated. The bootstrap esti-
reflexes)19 (respiration item systematically rated 1 with tra- mates associated with each covariate regression coefficient,
cheal intubation and breathes above ventilator rate for every and their associated standard errors (SEs), were finally aver-
patient in our cohort since they sustain pressure support ven- aged from replicates. Log-likelihood measured the good-
tilation), and Coma Recovery Scale-Revised (CRS-R) with ness-of-fit of a model. After these multivariate analyses, a
its six components (auditory, visual, motor, oromotor/ver- receiver operating characteristic (ROC) curve was plotted for
bal, communication, and arousal),20 with specificity related the final model, and area under the curve (AUC) was esti-
to inability to vocalize due to the endotracheal tube (item mated.29 A score predicting the extubation failure was esti-
2 of the oromotor/verbal function scale [vocalization/oral mated according to OR values. The threshold value of this
movement] was validated if oral movement compatible with score was determined according to usual recommendations
vocalization attempt was observed and item 3 [intelligible by estimating several indexes as Youden, Liu, and efficiency.
verbalization] was validated if one could recognize words on Sensitivity, specificity, and negative/positive predictive val-
patient lips or if the patient was able to write words). Data ues were presented with 95% CI. A sensitivity analysis was
collection before extubation and follow-up were exclusively performed to study patterns of patients with missing data
done by four senior intensivists working in the three ICUs and considered after analyses as not missing at random. An
(R.C., T.G., S.K., and J.M.) in a specifically designed and analysis of extubation failure before 48h was also performed.
standardized case report form. Our study conforms to the recent set of reporting guidelines:
Transparent Reporting of a multivariable prediction model
Statistical Analysis for Individual Prognosis Or Diagnosis.30
It seemed difficult to propose a sample size estimation
according to literature in order to develop and validate a sim- Results
plified pragmatic score predictive of extubation failure in this See the Supplemental Digital Content (http://links.lww.
category of patients. Numerous rules of thumb have been com/ALN/B322) for more information. One hundred and
suggested for determining the minimum number of sub- forty patients eligible to extubation were included between
jects required to conduct multiple regression analyses, but June 2013 and February 2015 (fig. 1). Extubation failure
they are heterogeneous and are often with minimal empiri- occurred in 43 (31%) patients (31 patients [24%] before
cal evidence. For multiple regression models, some authors 48h). Data of extubation failure before 48h are presented in
suggested variable ratios of 15:1 or 30:1 when generaliza- online supplementary material (Tables E1 and E2, Supple-
tion was critical.2124 Considering these works and expected mental Digital Content, http://links.lww.com/ALN/B322,
extubation failure rate between 20 and 30%, we proposed to presenting data about patients with extubation failure before
include at least 120 subjects to highlight three to five predic- 48h). Further presented data correspond to extubation fail-
tive factors. All analyses were performed using Stata software ure at any time during ICU stay. Missing data were investi-
(version 13; StataCorp, USA) and done for a two-sided type gated. Among the failure group, 361 of 4,730 (7.6%) and
I error of = 5%. Patients characteristics were described among the success group, 915 of 10,670 (8.6%) data were
by numbers and percentages for categorical parameters. For missing (P = 0.45). Total percentage of missing data was
quantitative values, mean and SDs or median with inter- 8.3%. These aspects had no impact on results. No data were
quartile range were calculated and presented according to missing for the primary outcome.
statistical distribution (normal distribution of quantitative There was no difference related to demographic data,
values was checked by ShapiroWilk test). Categorical data general and neurologic initial severity scores, type of neuro-
were compared using chi-square test. Quantitative data were logic injury, pupillary status, brainstem reflexes, comorbid-
compared between independent groups (extubation suc- ity, or characteristic of tracheal intubation between success
cess/failure) using Students t test or MannWhitney U test and failure groups. More patients had alcohol abuse in the
when assumptions of t test were not met (normality studied failure group (table 1). Characteristics of patients on success-
using ShapiroWilk test and homoscedasticity using Fisher ful SBT day are presented in Table E3 (Supplemental Digital
Snedecor test). A multivariate analysis was performed using Content, http://links.lww.com/ALN/B322, presenting char-
logistic regression models by stepwise approach according to acteristics of patients on successful SBT day). No difference
univariate results (P < 0.10)25,26 and clinical relevance.27,28 between characteristics of patients was observed on success-
Results were expressed with odds ratios (OR) and 95% CI. ful SBT day. Intercurrent events (neurologic, respiratory,
The final model was validated by a two-step bootstrapping or hemodynamic) and notably intercurrent pneumonia or
process. For each step, bootstrap samples with replacements adult respiratory distress syndrome had no effect on extuba-
(n = 1,000) were generated from the training set. In the first tion outcome. Duration of MV, number of failed SBT, and
phase, the percentage of models including each initial vari- arterial blood gases had no impact.
able was determined by usual stepwise approach. Then, in Patients outcomes are presented in table 2. ICU mortal-
the second phase, parameters of generalized linear regression ity and length of stay were increased in the failure group.
(logistic for dichotomous-dependent variable) of the final There was no difference in hospital length of stay. Glasgow
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
CRITICAL CARE MEDICINE
Fig. 1. Flow chart of patients screening and recruitment. AIS = supra- or infratentorial acute ischemic stroke; GCS = Glasgow
Coma Scale; HIE = hypoxicischemic encephalopathy; ICH = supra- or infratentorial spontaneous intracerebral hematoma;
ICU = intensive care unit; SAH = subarachnoid hemorrhage; TBI = traumatic brain injury.
Data are presented as mean SD unless otherwise indicated. Percentages may not exactly total 100% because of rounding.
AIS = acute ischemic stroke; GCS = Glasgow Coma Scale; HIE = hypoxic-ischemic encephalopathy; ICH = spontaneous intracerebral hematoma; IQR
= interquartile range; NA = not appropriate; SAH = subarachnoid hemorrhage; SAPS = simplified acute physiologic score; SOFA = sequential organ
failure assessment; TBI = traumatic brain injury.
Outcome Scale was significantly higher (meaning better Causes of extubation failure are presented in Table E4
recovery) in the extubation success group at ICU discharge (Supplemental Digital Content, http://links.lww.com/
and at 6 months. ALN/B322, presenting causes of extubation failure).
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Extubation Failure in Brain-injured Patients
Hypersecretion was the main reported reason accounting for Starting from this model, we created a score with weight-
67% of extubation failure. Stridor was the cause in 14%. ing related to ORs and ranging from 1 to 14 (table5). Boot-
No patient was reintubated due to any acute neurologic strap validation was performed for the construction of ROC
complication. curve presented in figure2. AUC was 0.82 (95% CI, 0.73 to
Extubation failure rates associated with total GCS and 0.91) for CRS-R visual subscale-based multivariate model.
eye and motor subscales are presented in Figure E1 (Supple- In our cohort, at the cutoff point of 9 determined by ROC
mental Digital Content, http://links.lww.com/ALN/B322, analysis, positive and negative predictive values for extuba-
presenting extubation failure rates associated with total and tion failure were 89 and 66% with a sensitivity of 84% and
eye and motor subscales of GCS). Some patients with GCS a specificity of 75%, respectively (table6).
as low as 3 could be extubated with success. Extubation failure rates across the original cohort are pre-
In univariate analysis, as shown in table3, assessment of sented in figure3. Scores beyond presented cutoff of 9 show
ocular functions in FOUR and CRS-R scores significantly low extubation failure incidences. Patients presenting with at
differentiated success and failure. None of the motor least two operating airway components succeeded extubation
responses was significant irrespective to scores. Communica- in 90 versus 10% if less (fig.4A). In each subgroup of operat-
tion and oromotor responses from CRS-R did not appear ing airway functions (0, 1, 2, or 3), extubation success rates
discriminative. Brainstem and arousal capabilities assessed by were 38, 32, 67, and 90%, respectively, independent of the
FOUR, GCS, and CRS-R were associated with extubation type of operating function: gag reflex, cough, or deglutition
failure. Agitation and pain assessed by Richmond Agitation (fig.4B).
and Sedation Scale and Behavioral Pain Scale, respectively, ROC curve of model including only airways function
did not accurately predict extubation outcome. Confusion of has an AUC of 0.79 and was not significantly different from
patients, as assessed by confusion assessment method for the ROC curve of model integrating neurologic status (AUC,
intensive care unit, was significantly associated with extuba- 0.82). Notwithstanding, this last model is more parsimoni-
tion failure. Classical respiratory and general parameters like ous with lower log-likelihood (55 vs. 60). When consider-
respiratory rate, rapid shallow breathing index, weight varia- ing patients with low consciousness levels (CRS-R visual
tion, and heart rate were not significant. Assessment of airway scores 0, 1, and 2), predictions of extubation success were 38
management criteria, illustrated by the capability to cough, versus 85% when considering operating airways functions
the deglutition ability, and the gag reflex, were strongly asso- (fig. 5). No extubation delays or erroneous primary trache-
ciated with extubation failure when absent. ostomy indications were revealed by retrospective analysis of
In multivariate analyses, GCS and FOUR as total scores electronic patient records.
or as their different components, as well as alcohol consump-
tion history, were not significant. CRS-R subscales were col- Discussion
linear. Related to practical ability in intubated patients, the This study identified risk factors associated with extubation
decision was made to keep CRS-R visual. Multivariate failure in a cohort of neurocritical care patients with severe
analysis was computed, and results are presented in table4. brain injuries. A pragmatic predictive clinical score, easy to
According to statistical distribution and clinical relevance, perform at the bedside, was elaborated and validated.
CRS-R visual subscore was dichotomized as presented Weaning of MV requires two successive steps: weaning
in Figure E2 (Supplemental Digital Content, http://links. of pressure support (ventilator) and liberation of the airway
lww.com/ALN/B322, presenting CRS-R visual subscore from the endotracheal tube. Brain-injured patients, usually
dichotomization). not affected by cardiopulmonary incompetency as a cause of
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
CRITICAL CARE MEDICINE
Criteria associated with extubation failure. Data are presented as mean SD unless otherwise noted. Score items are presented as mean SD to be more
illustrative of differences. FOUR-item respiratory equals 1 for all patients according to the definition in intubated patients.
BPS = behavioral pain scale; CAM-ICU = confusion assessment method for the intensive care unit; CRS-R = Coma Recovery Scale-Revised; FOUR = full
outline of unresponsiveness; GCS = Glasgow Coma Scale; HR = heart rate; IQR = interquartile range; RASS = Richmond Agitation and Sedation Scale;
RR = respiratory rate; RSBI = rapid shallow breathing index; Vt = tidal volume.
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Extubation Failure in Brain-injured Patients
Fig. 2. Receiver operating characteristic (ROC) curve of multivariate model based on Coma Recovery Scale-Revised item
visual and airways items. Area under the curve = 0.82 (95% CI, 0.73 to 0.91).
Table 6. Diagnostic Performances of Predictive Score of patients unable to tolerate multiple weaning trials related to
Extubation Failure infratentorial ischemic stroke, with bulbar respiratory drive
Score
palsy in three patients and prolonged neuromuscular weak-
ness in one patient.
CRS-R Item Visual In this population, from extended epidemiologic, clinical,
Cutoff 9 and biologic criteria concerning neurologic, hemodynamic,
Sensitivity 84% (95% CI, 0.750.91) and ventilatory functions, we identified few independently
Specificity 75% (95% CI, 0.580.88) associated with extubation failure: predominantly loss of
Positive predictive value 89% (95% CI, 0.800.95) upper-airway protective reflexes and to a lesser extent loss of
Negative predictive value 66% (95% CI, 0.490.80) minimal behavioral clinical evidence of consciousness.
CRS-R = Coma Recovery Scale-Revised. Coplin et al.9 demonstrated that brain-injured patients
meeting standard weaning criteria could be extubated irre-
spective of their upper-airway function and their mental sta-
tus could be evaluated with the GCS. In their cohort, some
patients with a GCS as low as 4 tolerated extubation. Extu-
bations delay was associated with increased risk of pneu-
monia and prolonged length of stay. In our cohort, patients
with low GCS could also sustain extubation.
Nevertheless, Namen et al.8 identified GCS to be the best
independent factor associated with extubation failure. ROC
curve analysis identified a cutoff beyond GCS greater than
or equal to 8 for extubation success (AUC, 0.681; OR, 4.9;
95% CI, 2.8 to 8.3; P < 0.001). Other studies found GCS
with a threshold value of 8 to be a good indicator of extuba-
Fig. 3. Percentages of extubation failure according to predic- tion tolerance,3234 and American guidelines suggest wean-
tive score. N = number of patients in the cohort with a par- ing when adequate mentation defined as GCS greater than
ticular score range. or equal to 13 is present.5 However, other studies did not
recognize GCS as a predictor,13,35 and in our cohort, GCS
in extubation failure.10,13 It could be related to population was not independently associated with extubation failure.
disparities, for example, elective neurosurgical patients with Indeed, GCS lacks information to differentiate subtle dis-
short duration of MV or exclusions of tracheostomy without orders of consciousness, does not assess brainstem reflexes,
any extubation attempt for severe patients in some studies. In and is not evaluable in intubated patients.15 Identical GCS
our cohort, no tracheostomy was performed unless the patient with total sum of scale components could indicate very dif-
was not able to sustain SBT. It happened in four nonincluded ferent neurologic conditions.18 Therefore, results based on
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
CRITICAL CARE MEDICINE
A B
Fig. 4. (A) Percentages of extubation success according to the number of operating airways functions in the whole popula-
tion. The presence of at least two operating airways functions (cough, deglutition, or gag reflex) allow the prediction of 90%
of extubation success. (B) Percentages of extubation success according to the number of operating airways function in each
subgroup of functioning airway. NS = number of patients presenting with extubation success; NT = total number of patients in
each subgroup of operating airways function.
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Extubation Failure in Brain-injured Patients
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
CRITICAL CARE MEDICINE
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Extubation Failure in Brain-injured Patients
C, Gergaud S, Plaud B, Constantin JM, Malledant Y, Flet L, 43. Thille AW, Corts-Puch I, Esteban A: Weaning from the ventila-
Sebille V, Roquilly A; Corti-TC Study Group: Hydrocortisone tor and extubation in ICU. Curr Opin Crit Care 2013; 19:5764
and fludrocortisone for prevention of hospital-acquired 44. Mackay LE, Morgan AS, Bernstein BA: Swallowing disorders
pneumonia in patients with severe traumatic brain injury in severe brain injury: Risk factors affecting return to oral
(Corti-TC): A double-blind, multicentre phase 3, randomised intake. Arch Phys Med Rehabil 1999; 80:36571
placebo-controlled trial. Lancet Respir Med 2014; 2:70616 45. Ponfick M, Linden R, Nowak DA: DysphagiaA common,
32. Vidotto MC, Sogame LC, Gazzotti MR, Prandini MN, Jardim transient symptom in critical illness polyneuropathy: A fiber-
JR: Analysis of risk factors for extubation failure in subjects optic endoscopic evaluation of swallowing study. Crit Care
submitted to non-emergency elective intracranial surgery. Med 2015; 43:36572
Respir Care 2012; 57:205966 46. Skoretz SA, Flowers HL, Martino R: The incidence of dyspha-
33. Wang S, Zhang L, Huang K, Lin Z, Qiao W, Pan S: Predictors gia following endotracheal intubation: A systematic review.
of extubation failure in neurocritical patients identified by Chest 2010; 137:66573
a systematic review and meta-analysis. PLoS One 2014; 47. Chan LY, Jones AY, Chung RC, Hung KN: Peak flow rate dur-
9:e112198 ing induced cough: A predictor of successful decannulation
34. Wendell LC, Raser J, Kasner S, Park S: Predictors of extuba- of a tracheotomy tube in neurosurgical patients. Am J Crit
tion success in patients with middle cerebral artery acute Care 2010; 19:27884
ischemic stroke. Stroke Res Treat 2011; 2011:248789 48. Salam A, Tilluckdharry L, Amoateng-Adjepong Y, Manthous
35. Koh WY, Lew TW, Chin NM, Wong MF: Tracheostomy in a CA: Neurologic status, cough, secretions and extubation out-
comes. Intensive Care Med 2004; 30:13349
neuro-intensive care setting: Indications and timing. Anaesth
Intensive Care 1997; 25:3658 49. Crary MA, Carnaby GD, Sia I, Khanna A, Waters MF:
Spontaneous swallowing frequency has potential to identify
36. American Congress of Rehabilitation Medicine BI-ISIGDoCTF,
dysphagia in acute stroke. Stroke 2013; 44:34527
Seel RT, Sherer M, Whyte J, Katz DI, Giacino JT, Rosenbaum
AM, Hammond FM, Kalmar K, Pape TL, Zafonte R, Biester 50. Moulton C, Pennycook A, Makower R: Relation between
RC, Kaelin D, Kean J, Zasler N: Assessment scales for disor- Glasgow coma scale and the gag reflex. BMJ 1991; 303:12401
ders of consciousness: Evidence-based recommendations for 51. Davies AE, Kidd D, Stone SP, MacMahon J: Pharyngeal
clinical practice and research. Arch Phys Med Rehabil 2010; sensation and gag reflex in healthy subjects. Lancet 1995;
91: 1795813 345:4878
37. Schnakers C, Giacino J, Kalmar K, Piret S, Lopez E, Boly M, 52. Manno EM, Rabinstein AA, Wijdicks EF, Brown AW, Freeman
Malone R, Laureys S: Does the FOUR score correctly diag- WD, Lee VH, Weigand SD, Keegan MT, Brown DR, Whalen
nose the vegetative and minimally conscious states? Ann FX, Roy TK, Hubmayr RD: A prospective trial of elective
extubation in brain injured patients meeting extubation crite-
Neurol 2006; 60:7445; author reply 745
ria for ventilatory support: A feasibility study. Crit Care 2008;
38. Schnakers C, Majerus S, Giacino J, Vanhaudenhuyse A, Bruno 12:R138
MA, Boly M, Moonen G, Damas P, Lambermont B, Lamy M,
53. Blackwood B, Clarke M, McAuley DF, McGuigan PJ, Marshall
Damas F, Ventura M, Laureys S: A French validation study of JC, Rose L: How outcomes are defined in clinical trials of
the Coma Recovery Scale-Revised (CRS-R). Brain Inj 2008; mechanically ventilated adults and children. Am J Respir Crit
22:78692 Care Med 2014; 189:88693
39. Schnakers C, Vanhaudenhuyse A, Giacino J, Ventura M, Boly 54. Cheng KC, Hou CC, Huang HC, Lin SC, Zhang H: Intravenous
M, Majerus S, Moonen G, Laureys S: Diagnostic accuracy of injection of methylprednisolone reduces the incidence of
the vegetative and minimally conscious state: Clinical con- postextubation stridor in intensive care unit patients. Crit
sensus versus standardized neurobehavioral assessment. Care Med 2006; 34:134550
BMC Neurol 2009; 9:35 55. Karanjia N, Nordquist D, Stevens R, Nyquist P: A clinical
40. Estraneo A, Moretta P, De Tanti A, Gatta G, Giacino JT, Trojano description of extubation failure in patients with primary
L; Italian Crs-R Multicentre Validation Group: An Italian mul- brain injury. Neurocrit Care 2011; 15:412
ticentre validation study of the coma recovery scale-revised. 56. Efron BT, Tibshirani R: An introduction to the bootstrap,
Eur J Phys Rehabil Med 2015; 51:62734 Bootstrap Methods and Their Applications. Edited by
41. Majerus S, Gill-Thwaites H, Andrews K, Laureys S: Behavioral Davison ACH, Hinkley DV. Cambridge, Cambridge University
evaluation of consciousness in severe brain damage. Prog Press, 1997
Brain Res 2005; 150:397413 57. Giacino JT, Fins JJ, Laureys S, Schiff ND: Disorders of con-
42. Bruno MA, Vanhaudenhuyse A, Schnakers C, Boly M,
sciousness after acquired brain injury: The state of the sci-
Gosseries O, Demertzi A, Majerus S, Moonen G, Hustinx R, ence. Nat Rev Neurol 2014; 10:99114
Laureys S: Visual fixation in the vegetative state: An observa- 58. Nava S, Hill N: Non-invasive ventilation in acute respiratory
tional case series PET study. BMC Neurol 2010; 10:35 failure. Lancet 2009; 374:2509
Copyright 2016, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.