Swallowing Disorders as a Predictor of Unsuccessful Extubation: A

Clinical Evaluation
Philippe Colonel, Marie Hélène Houzé, Hélène Vert, Joachim Mateo, Bruno Mégarbane, Dany
Goldgran-Tolédano, Françoise Bizouard, Martine Hedreul-Vittet, Frédéric J. Baud, Didier
Payen, Eric Vicaut and Alain P. Yelnik
Am J Crit Care 2008;17:504-510
© 2008 American Association of Critical-Care Nurses
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Pulmonary Critical Care

S WALLOWING DISORDERS
AS APREDICTOR OF
UNSUCCESSFUL EXTUBATION:
A CLINICAL EVALUATION
By Philippe Colonel, PT, Marie Hélène Houzé, PT, Hélène Vert, PT, Joachim
Mateo, MD, Bruno Mégarbane, MD, PhD, Dany Goldgran-Tolédano, MD,
Françoise Bizouard, PT, Martine Hedreul-Vittet, PT, Frédéric J. Baud, MD,
Didier Payen, MD, Eric Vicaut, MD, PhD, and Alain P. Yelnik, MD

Background Unsuccessful extubation may be due to swallowing

dysfunction that causes airway obstruction and impairs patients’
ability to cough and expectorate.
Objective To determine whether swallowing assessment before
extubation is helpful in predicting unsuccessful extubation due
to airway secretions.
Methods This prospective study included all patients intubated
orotracheally for more than 6 days. Before extubation, 3 tests
designed to assess (1) cervical, oral, labial, and lingual motility;
(2) gag reflex; and (3) swallowing were used at the bedside.
Causes of reintubation were identified, and their relationship to
patients’ swallowing function before extubation was evaluated.
Results Sixty-two patients were enrolled. Data on 55 patients
reintubated for swallowing dysfunction were analyzed. Nine
patients were reintubated because of obstruction related to upper
airway secretions. Evaluation before extubation enabled predic-
tion of 7 of those 9 unsuccessful extubations. Among the 23
patients with central nervous system disease, 3 of 4 unsuccess-
ful extubations were predicted. According to a multivariate
logistic regression model, motility and swallowing were inde-
pendent predictors of unsuccessful extubation (area under
receiver-operating-characteristic curve, 80%). The gag reflex was
the only significant predictor of the ability to cough (area under
curve, 73%) and excessive pulmonary secretion (area under curve,
67%). Swallowing was an independent predictor of the need for
suctioning (area under curve, 78%).
Conclusions Using simple bedside tests to evaluate swallowing
before extubation is helpful when deciding whether to extubate
patients who have been intubated for more than 6 days.
Involvement of nurses in these decisions would improve
patients’ management. (American Journal of Critical Care.
2008;17:504-510)

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P
atients in whom extubation is unsuccessful stay significantly longer in intensive care
units (ICUs) and have a higher mortality rate than do patients who are extubated
successfully.1,2 Tracheal reintubation can become necessary in several situations,
including mechanical ventilation, airway protection, airway obstruction, pul-
monary cleansing, and high-level continuous positive airway pressure.3 In most
of these situations, reintubation is associated with life-threatening complications and a
poor prognosis.

These many and varied causes of reintubation leads to aspiration is common, especially after pro-
necessitate a battery of tests for each indication. longed intubation, and accounts for up to 15% of
Results of functional respiratory tests are often used unsuccessful extubation cases.6 The incidence of
as weaning parameters (ie, to assess ability to main- swallowing dysfunction is underestimated, mainly
tain spontaneous breathing without ventilatory among patients whose intubation lasts longer than
assistance). However, such measurements are not 48 hours.13-15 Moreover, no guidelines are available
accurate enough to enable prediction of unsuccessful to predict extubation outcome in brain-injured
extubation (ie, the inability to tolerate removal of patients.2 Swallowing is usually evaluated after
the translaryngeal tube).4,5 Previous reports6-10 on extubation and requires specialized
these tests indicate that some respiratory measure- intervention and transportation of
ments are independent predictors of extubation patients. We therefore devised a scale Swallowing
outcomes. These measurements include peak expi-
ratory flow (as an evaluation of cough strength),
for bedside evaluation of swallow-
ing function before extubation. Our
dysfunction
score on the Glasgow Coma Scale, secretion volume, aim in the study reported here was accounts for
the cuff leak test, the ratio of PaO2 to fraction of to determine whether this scale is
inspired oxygen, maximum negative inspiratory useful to predict unsuccessful extu-
up to 15% of
pressure, and the ratio of respiratory rate to tidal bation related to airway secretions. extubation failure.
volume. However, the reliability of such measure-
ments remains debatable because the measurements Patients and Methods
may vary, depending on the study population and This research was done in accordance with the
the methods of evaluation.11 This concern is particu- appropriate institutional review body and was carried
larly important for patients with central nervous out in conformity with the ethical standards set forth
system (CNS) diseases; in these patients, swallowing in the Helsinki Declaration of 1975. All patients were
disabilities may result because of either their neuro- treated according to our standard clinical practice,
logical disease or their impaired mental status.12 so their specific informed consent was not required.
Unsuccessful extubation can be caused by upper
airway obstruction with consequent narrowing of Patients
the respiratory space or by inability to manage res- All successive patients admitted to the medical
piratory secretions. Swallowing dysfunction that or surgical ICU at l’Hôpital Lariboisière-Fernand
Widal, Paris, France, and intubated by
the orotracheal route for more than 6
About the Authors days were prospectively enrolled when Swallowing
Philippe Colonel, Marie Hélène Houzé, Hélène Vert,
Françoise Bizouard, and Martine Hedreul-Vittet are
extubation was planned. Patients with
nasotracheal intubation, previous
function was
physiotherapists and Alain P. Yelnik is a physician in the
Service de Médecine Physique et de Réadaptation;
swallowing disorders, ear-nose-throat based on cervi-
surgery, or chronic persistent vegeta-
Joachim Mateo and Didier Payen are physicians in the
Département d’Anesthésie et de Réanimation; Bruno tive status were not included. During
cal, oral, labial,
Mégarbane, Dany Goldgran-Tolédano, and Frédéric J.
Baud are physicians in Réanimation Médicale et Toxi-
the study period, all patients were and lingual motil-
cologique; and Eric Vicaut is a physician in the Unité de intubated with a low-pressure, high-
Recherche Clinique; all at l’Hôpital Lariboisière-Fernand volume tube cuff. Cuffs were routinely ity; gag reflex;
Widal, Université Paris VII, Paris, France.
Corresponding author: Bruno Mégarbane, MD, PhD, Réani-
checked, and pressure was kept at 25 and swallowing.
to 30 cm H2O. Treatments, weaning
mation Médicale et Toxicologique, Hôpital Lariboisière,
2 Rue Ambroise Paré, 75010 Paris, France (e-mail: protocols, and decisions to extubate or reintubate
bruno-megarbane@wanadoo.fr). were left to the discretion of the attending physicians.

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 Table 1
Bedside evaluation of swallowing
function before extubation
In both the medical and surgical ICUs, evaluations
Function Score were performed by 4 experienced physiotherapists,
with the patient’s tube cuff inflated. When the cuffs
Motilitya were deflated, however, tube mobility was excessive
Holding the head up Not able 1□
Able 2□ and an excessive coughing reflex occurred that
impaired the evaluation process despite suctioning
Opening the mouth Not able 1□
Able 2□ of pharyngeal secretions. The physicians were not
told the results of the swallowing tests.
Pursing the lips Not able 1□
The ability to cough and swallow, secretion
Able 2□
volume, and the need for suctioning were evaluated
Gritting the teeth Not able 1□
immediately (within 10 minutes) and at 24 and 48
Able 2□
hours after extubation (Figure 2). Cough was scored
Sticking the tongue out over the lower Not able 1□ as normal or abnormal according to the efficiency
teeth Able 2□
with which secretions were ejected. The ability to
Total (5-10) perform a complete swallow without coughing was
scored as possible or impossible. Increases in laryn-
Gag reflexb geal secretions after extubation were evaluated by
Right side None 1□ using suctioning and respiratory therapy.
Weak 2□
Normal 3□
Justification of the Evaluation Tests
Left side None 1□
The choice of evaluation criteria (Table 1) was
Weak 2□
Normal 3□ based on the physiology of swallowing in its buc-
colingual and oropharyngeal stages.17,18 Each item
Total (2-6)
was related to a simple order that was easy for the
Swallowingc Incomplete 0□ therapist to mimic. The testing of spontaneous cer-
Complete 1□ vical motility allowed even confused patients to be
Total (0-1) scored. Although the score on the Glasgow Coma
a Motility was scored 2 if a motor response to a request or the ability to move was Scale was not precisely determined at the time of
observed by the therapist, and 1 if no movement was observed. extubation, all the patients had a sufficient level of
b The left and right sides were scored separately, by triggering each lateral oropha- consciousness to allow examination of their motor
ryngeal side with the finger. A 10-mL syringe positioned between the molars was
used to protect therapists from biting.
functions. Ability to hold the head up is usually
c The complete motor scheme of swallowing was assessed, including pharyngo- considered before extubation is decided, because
laryngotracheal axis elevation, the anterior movement of the larynx and hyoid this ability indicates that sedative and neuromuscu-
bone, and the sound of pressure propelling the bolus down the esophagus.
lar blocking agents have worn off completely.
Weakness of muscles in the front of the neck may
All patients met institutionally sanctioned weaning cause swallowing dysfunction related to hyoid bone
criteria.16 Extubation was performed by trained nurses instability and nonphysiological positioning of the
and physiotherapists. (In France, physical and respi- head and neck. Therefore, the palpable muscles in
ratory therapies are performed by the same thera- the front of the neck, which appeared either sponta-
pist.) Before extubation, subglottal neously or after adequate postural stimulation, were
Using a bedside suctioning was performed. tested (a score of 1 of 5 on manual muscle testing
was required).19
preextubation Interventions Ability to open the mouth indicated normal
evaluation, 78% Before extubation, the different tonicity. Ability to purse the lips indicated facial
components of swallowing functions nerve integrity. Ability to grit the teeth, which is part
of extubation were evaluated at the bedside by of the swallowing process, was necessary to give a
using a scale to assess (1) cervical, fixation point for the suprahyoid muscles. Their
failures were oral, labial, and lingual motility; contraction allows the pharyngolaryngeal tracheal
predicted. (2) the gag reflex; and (3) swallow- axis to tighten and the hyoid bone and larynx to
ing (Table 1 and Figure 1). These elevate. Swallowing is usually difficult when the
tests do not require any specific equipment. A 10-mL mouth is open. Ability to stick out the tongue over
syringe was positioned between the patient’s molars the lower teeth indicated that the tongue was strong
to prevent biting when the operator introduced a enough to push the bolus being swallowed backward
finger into the patient’s mouth to test the gag reflex. down the esophagus.

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Data Collection and Analysis
The physiological variables measured at admis-
sion were used to calculate the Simplified Acute
Physiology Score II.20 Extubation was considered 1 2 3
unsuccessful if reintubation was required within
48 hours after extubation. The causes of unsuccess-
ful extubation were identified, and their relation-
ship to swallowing function before extubation was
evaluated. Some patients were reintubated for
reasons other than swallowing problems or airway 4 5
protection. Thus, the only patients included in the
analysis were patients who were successfully extu-
bated and patients in whom extubation was unsuc-
cessful because of upper airway secretions.

Statistical Analysis 6 7
Results were expressed as medians (10th-90th
percentiles). Comparisons were performed by using
the Mann-Whitney test (because of the nonnormal Figure 1 Steps in the clinical evaluation of swallowing disorders.
distribution of variables) or the Fisher exact test. Assessment of the patient’s ability to hold the head up (1), open
the mouth (2), purse the lips (3), grit the teeth (4), and stick the
The value of each test in predicting successful extu- tongue out over the lower teeth (5), and determination of the
bation was assessed by using multivariate logistic gag reflex score (6) and the swallowing score (7).
regression. When a quantitative parameter (or a

Extubation

Evaluation of the need for + 10 minutes + 24 hours + 48 hours

Weaning an orotracheal tube

Time

Evaluation before extubation

Evaluation after extubation
Intensivist Physiotherapist
Extubation criteria evaluation
Performed at extubation time + 10
including PaO2/fraction of Auscultation
minutes, + 24 hours, + 48 hours
inspired oxygen, Forced expectoration test
mental status, Cough strong enough to eject airway
comorbid diseases secretions?
Bedside evaluation of Increased volume of secretions?
swallowing function
Efficient swallowing?
(guidelines)
Need for subglottal suctioning?
Extubation
decision Blinded

Figure 2 Time and methods of data collection and evaluation.

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 Table 2
Patients’ demographic characteristics
Characteristic Value score combining several parameters) was identified
as a predictor of an event, the sensitivity and speci-
No. of patients enrolled 62
ficity of the predictor for different considered cutoff
No. of patients included in the analysis 55
points were determined. Then the true-positive rate
Age, median (10th-90th percentile), y 51 (26-79) (ie, sensitivity) was plotted against the false-positive
Sex, No. of patients rate (1 - specificity) for the different possible cutoff
Male 38 points of the parameter. This kind of graph is called
Female 17 a receiver-operating-characteristic (ROC) curve. Accu-
Intubation time, median (10th-90th 13 (7-27) racy of prediction was indicated by the area under
percentile), d the ROC curve. An area of 1 represented a perfect
Simplified Acute Physiology Score II, 50 (28-73) test; an area of 0.5 represented a worthless test. Areas
median (10th-90th percentile) larger than 0.9, 0.8, 0.7, or 0.6 were considered excel-
Primary disorders, No. (%) of patients lent, good, fair, or poor, respectively. ROC curves
Central nervous system diseases 23 (42)a show the trade-off between sensitivity and specificity:
Acute respiratory failure 14 (26) any increase in sensitivity results in a decrease in
Shock 7 (13) specificity. Values in predicting unsuccessful extuba-
Heart failure 6 (11)
tion were estimated by calculating the values of sen-
Acute poisoning 5 (9)
sitivity and specificity for the different cutoff points
a Including 10 with head trauma and 7 with brain ischemia.
that maximize the “sensitivity plus specificity” sum.
Similar methods were used to identify potential
predictors of cough, swallowing, greater volumes
of secretions, and the need for suctioning. All tests
were 2-sided, with a 5% significance level.
Table 3
Value of evaluation before extubation to predict
unsuccessful extubation due to excessive bronchial
Results
secretions: successful vs unsuccessful extubation A total of 62 patients were enrolled during 15
months, and 55 patients were included in the analysis
Extubation (Table 2). Patients admitted to the surgical and med-
Successful Unsuccessful ical ICUs differed in median age (40 years, 10th-90th
Characteristic (n = 46) (n = 9) P percentile, 23-64 vs 63 years, 10th-90th percentile,
39-84; P < .001) and median days of intubation (16,
Age, median (10th-90th 46 (25-79) 56 (36-75) .30
percentile), y 10th-90th percentile, 9-35 vs 10, 10th-90th percentile,
7-23; P = .002). Seven patients were reintubated
Sex, No. of patients .70
Male 30 8
within 24 hours of extubation for reasons other than
Female 16 1 swallowing dysfunction or airway protection, includ-
ing septic shock (n = 2), laryngeal edema (n = 1),
Intensive care unit, No. of patients .90
Surgical 24 5 bronchospasm (n = 1), respiratory problems (n = 1),
Medical 22 4 heart problems (n = 1), and kidney failure (n = 1).
Central nervous system diseases, % 41 44 .90
A total of 46 patients were successfully extubated;
the remaining 9 patients (16%) were reintubated for
Intubation duration, median 12 (7-26) 13 (7-23) .80
upper airway obstruction related to secretions (Table 3).
(10th-90th percentile), d
No other patients were reintubated once 48 hours had
Simplified Acute Physiology Score II, 47 (24-69) 60 (45-81) .005 elapsed after extubation. When the bedside evaluation
median (10th-90th percentile)
was done before extubation, 7 of 9 (78%) unsuccess-
Death in intensive care unit, % 0 33 <.001 ful extubations were predicted. Of the 23 patients
Evaluation before extubation with Central Nervous System (CNS) diseases, 19 were
Motility scores (scale, 5-10), 10 (9-10) 9 (6-10) .003 successfully extubated; the other 4 were reintubated.
median (10th-90th percentile) Among the patients with CNS disorders, 3 of the 4
Gag reflex scores (scale, 2-6), 5 (2-6) 5 (1-5) .30 (75%) unsuccessful extubations were predicted.
median (10th-90th percentile) On the basis of the logistic regression model
Swallowing process, No. of patients .005 coefficients, cervical motility and swallowing were
Complete 34 2 independent predictors of unsuccessful extubation
Incomplete 12 7 (area under ROC curve, 80%; sensitivity, 0.56;
specificity, 0.98; Figure 3). The gag reflex was the

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 1.0

only significant predictor of the ability to cough (area 0.9

under ROC curve, 73%; sensitivity, 0.59; specificity,
0.8
0.73) and of the presence of excessive pulmonary
secretions (area under ROC curve, 67%; sensitivity, 0.7
0.36; specificity, 0.93). Swallowing was an independ-
ent predictor of the need for suctioning (area under 0.6

Sensitivity
ROC curve, 78%; sensitivity, 0.43; specificity, 0.89). 0.5
No test was predictive of swallowing disorders.
0.4
Discussion
In this preliminary investigation, swallowing func- 0.3
tion before extubation was predictive of successful extu- 0.2
bation in patients intubated for more than 6 days. Of
the 3 tests used, the tests for cervical motility and swal- 0.1
lowing were independent predictors of reintubation.
0.0
To our knowledge, this study is the first assess-
ment of the reliability of standard criteria for physio- 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
therapeutic extubation. Although our evaluation 1 – Specificity
before extubation seemed easy to perform, one limita- Figure 3 Receiver-operating-characteristic curve based on the
tion of this study was that we did not evaluate interop- regression logistic model with the 2 variables (ie, cervical motility
erator reliability. Among the criteria of our bedside and swallowing) that were independent predictors of unsuccess-
guidelines, we chose to evaluate the gag reflex, because ful extubation.
it may be impaired by orotracheal intubation and the
sensitivity level of the corresponding oropharyngeal For the purpose of this study, the evaluation tests
side may increase. The gag reflex may be absent in sev- were performed only by physiotherapists. However,
eral CNS disorders, in cranial nerve impairments, or in we think that nurses in critical care could perform
elderly persons.21,22 The presence of this reflex does not these assessments, just as they do tests to determine
ensure protection against aspiration.23 whether patients are ready for weaning from
We were able to predict a patient’s ability to mechanical ventilation.16 Thus, our
cough and to eject bronchial secretions, but no reli- bedside evaluation guidelines for
able criteria were predictive of swallowing disorders. assessing swallowing function before
Swallowing
However, we think that the 9 patients who were extubation could be implemented evaluation before
reintubated for upper airway obstruction related to by several members of the ICU
excessive secretions had a primary swallowing prob- multi-disciplinary team.
extubation, using
lem, because their scores on the Glasgow Coma Scale simple bedside
were greater than 9 on extubation and their cough Conclusion
did not weaken. Indeed, we could not even distin- Our results indicate the useful- tests, is useful
guish major swallowing disorders from silent aspi- ness of evaluating swallowing disor- to predict extu-
ration. Mechanisms for swallowing impairment and ders before extubation and of
for the ability to cough and eliminate bronchial predicting unsuccessful extubations by bation failure.
secretions are different.12,17,24 Bedside clinical evalua- using simple bedside tests. Simultane-
tions done just after extubation always yield under- ous evaluation by physicians and physiotherapists may
estimates of the incidence of swallowing disorders be helpful for extubation decisions in patients intu-
when fiber-optic measuring devices are used.21,23,25 bated for long periods. However, our findings should
To date, no study has been done to evaluate be confirmed in further studies of larger cohorts by
swallowing before extubation. Swallowing mecha- extensive repetition of the current procedures.
nisms are complex and may be impaired in many
situations, including CNS diseases.13 In patients with FINANCIAL DISCLOSURES
None reported.
CNS diseases, the success of extubation is difficult
to predict.2 With our evaluation, 3 of 4 reintubations
eLetters
could be predicted in the patients with CNS diseases, Now that you’ve read the article, create or contribute to an
thus highlighting the value of our bedside evaluation online discussion on this topic. Visit www.ajcconline.org
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 13. Tolep K, Getch CL, Criner GJ. Swallowing dysfunction in
SEE ALSO patients receiving prolonged mechanical ventilation. Chest.
To learn more about reducing unsuccessful extuba- 1996;109(1):167-172.
tions in critical care, visit http://ajcc.online.org, and 14. Ajemian MS, Nirmul GB, Anderson MT, Zirlen DM, Kwasnik
read the article by McLean and colleagues, “Improv- EM. Routine fiberoptic endoscopic evaluation of swallowing
ing Adherence to a Mechanical Ventilation Weaning following prolonged intubation: implications for manage-
ment. Arch Surg. 2001;136(4):434-437.
Protocol for Critically Ill Adults: Outcomes After an
15. El Solh A, Okada M, Bhat A, Pietrantoni C. Swallowing dis-
Implementation Program” (American Journal of Criti- orders post orotracheal intubation in the elderly. Intensive
cal Care, May 2006). Care Med. 2003;29(9):1451-1455.
16. Richard C, Beydon L, Cantagrel S, et al. XXIe conférence de
consensus en réanimation et en médecine d’urgence.
Sevrage de la ventilation mécanique (à l’exclusion du nou-
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