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British Journal of Anaesthesia 109 (4): 578–83 (2012)

Advance Access publication 26 June 2012 . doi:10.1093/bja/aes210

CRITICAL CARE

Influence of the cuff pressure on the swallowing reflex


in tracheostomized intensive care unit patients
R. Amathieu 1,2, S. Sauvat1,2, P. Reynaud 1,2, V. Slavov 1,2, D. Luis 1,2, A. Dinca1,2, L. Tual1,2, S. Bloc1,2
and G. Dhonneur 1,2*
1
Anaesthesia and Intensive Care Unit Department, Jean Verdier University Hospital of Paris, Av du 14 Juillet, 93143 Bondy, France
2
Paris 13 University School of Medicine, Bobigny, France
* Corresponding author. E-mail: gilles.dhonneur@jvr.aphp.fr

Background. Because recovery of an efficient swallowing reflex is a determining factor for

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Editor’s key points the recovery of airway protective reflexes, we have studied the influence of the
† The recovery of the tracheostomy tube cuff pressure (CP) on the swallowing reflex in tracheotomized patients.
swallowing reflex is key to Methods. Twelve conscious adult intensive care unit (ICU) patients who had been weaned
weaning from from mechanical ventilation were studied. Simultaneous EMG of the submental muscles
tracheostomy. with measurement of peak activity (EMGp) and amplitude of laryngeal acceleration (ALA)
† A cuffed tracheostomy tube were performed during reflex swallows elicited by pharyngeal injection of distilled water
anchors the tracheal to the boluses during end expiration. After cuff deflation, characteristics of the swallowing reflex
anterior neck tissues and (latency time: LaT, EMGp, and ALA) were measured at CPs of 5, 10, 15, 20, 25, 30, 40, 50,
interferes with swallowing. and 60 cm H2O.
† This study in intensive care Results. LaT and CP were linearly related (P,0.01). CP was inversely correlated (P,0.01) to
patients demonstrated that both ALA and EMGp.
the presence of a cuffed
Conclusions. We demonstrated that LaT, EMGp, and ALA of the swallowing reflex were
tube interferes with both
influenced by tracheostomy tube CP. The swallowing reflex was progressively more
the latency and magnitude
difficult to elicit with increasing CP and when activated, the resulting motor swallowing
of the swallowing reflex.
activity and efficiency at elevating the larynx were depressed.
† The effect increased with
Keywords: acceleromyography; airway protection; cuff pressure; electromyography;
greater cuff pressures,
swallowing reflex; tracheostomy
especially above 25 cm H2O.
Accepted for publication: 21 February 2012

The presence of a cuffed tracheostomy tube alters the pha- Methods


ryngeal stage of swallowing. This is believed to be the
After the local ethics committee approved the protocol and
result of the anchoring of the trachea to the anterior neck
informed consent had been obtained from the patient or
tissues, resulting in a reduction in elevation and anterior
relatives, 12 consecutive tracheostomized adult patients
movement of the larynx, uncoordinated laryngeal closure,
who had been weaned from mechanical ventilation were en-
and oesophageal obstruction by the cuff in the proximal oe-
rolled in the present study.
sophagus and hypopharynx.1 – 3 Other reasons including oro-
We studied patients who required intensive care after
motor dysfunction and impaired sensation may contribute to
severe blunt chest trauma. After resolution of the initial path-
disordered deglutition in tracheostomized patients.4 During
ology, sedation (sufentanil and midazolam titrated on the
the weaning process from the tracheostomy tube, continu-
Ramsay sedation scale) was discontinued and the patients
ous scoring of swallowing performance is recommended.5 were allowed to recover consciousness. After awaking
When the patient appears to be able to tolerate secretions (Glasgow coma scale of 13–15), dysphagia assessment was
without difficulties, the cuff is deflated and a swallowing as- undertaken in the intensive care unit (ICU). This included
sessment of food and fluid of varying consistencies is under- an assessment of the level of consciousness; cranial nerve
taken. If any sign of frank aspiration is observed, the cuff is function; cough capability, oromusculature efficiency; and
immediately re-inflated. We hypothesized that cuff pressure volitional swallows. A multidisciplinary team including phy-
(CP) in the tracheostomy tube may influence recovery of siotherapists and medical staff decided that patients were
swallowing. We studied the influence of the CP on the swal- fit for inclusion in the study when the patients tolerated
lowing reflex elicited in tracheostomized patients.

& The Author [2012]. Published by Oxford University Press on behalf of the British Journal of Anaesthesia. All rights reserved.
For Permissions, please email: journals.permissions@oup.com
Swallowing with a tracheostomy tube BJA
cuff deflation with a stable respiratory rate, arterial oxygen and 1.5 cm above the hyoid arch. The EMG was amplified
saturation, and expired carbon dioxide expiratory partial and band-pass filtered from 30 to 300 Hz, and then rectified
pressure. In order to be included, the patients had to demon- and integrated (100 ms time constant), and the peak electro-
strate they were co-operative and able to respond on myographic activity was measured (EMGp).
command simple orders such as ‘swallow your saliva’ and The quality of laryngeal elevation was measured by accel-
‘raise your right hand’. erometry with the use of a piezoelectric probe measuring
Once recruited, the stomach content of the patient was 2×2×4 mm (Entran; Garston, Watford, UK), which was
suctioned and the nasogastric feeding tube was removed. fixed in the mid-line with an adhesive tape 0.5 cm above
The patients were then requested to fast for a minimum of the tip of the thyroid cartilage. This probe measured acceler-
6 h. The studies were conducted with the patient sat up at ation values ranging from 5 to 25 G. The probe was orien-
458. Before measurement of the swallowing reflex character- tated to measure the amplitude of laryngeal acceleration
istics, oropharyngeal secretions were suctioned. After trache- (ALA) generated by the contraction of the submental swal-
ostomy tube cuff deflation (TRACOE VARIOTM , high-volume lowing muscles.
and low-pressure cuff, POURET Medical, Clichy, France), In order to synchronize pharyngeal stimuli with respir-
suction was performed through the tracheostomy tube to ation, ventilatory flows were monitored at the T-piece of
remove secretions that had been sitting on the top of the the tracheostomy tube with a pneumotachograph (Fleish 2)

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cuff. Figure 1 shows details of the electrophysiological mea- and a differential pressure transducer (Validyne MP 45,
surements. A 0.8 mm ID, polyvinyl catheter was placed Northridge, CA, USA). Reflex swallows were systematically eli-
through the nostril into the oropharynx using water lubricant cited with boluses of distilled cold water (38C) injected
gel without local anaesthetic. The tip of the catheter was through the pharyngeal catheter at the end of expiration.
positioned at the inferior limit of the oropharynx. This was The latency time of the swallowing reflex (LaT) was defined
checked visually and the catheter secured. Surface elec- as the time elapsing between the moment of bolus injection
trodes, used to measure EMG activity of the submental swal- of distilled water in the hypopharynx (a double-piston syringe
lowing muscles, were placed 2 cm away from the mid-line allowed simultaneous injection of distilled cold water into
the pharynx and 1 ml of air into the ventilatory circuit) and
the beginning of the evoked EMG signal (Fig. 2).
Patients were included in the study, if reflex swallows
could be elicited and if the characteristics of the swallowing
reflex could be measured accurately. In order to evaluate
pharyngeal sensory perception, we first determined in each
EMG tracheostomized patient the pharyngeal sensory threshold
(PST). After cuff deflation (CP¼0 cmH2O), patients received
LA
in a random order 0.3, 0.5, 0.8, 1, 3, 5, or 10 ml boluses of
cold (38C) distilled water through the pharyngeal catheter.
DPS
PST was arbitrary defined as the lowest (stimulation)
volume of distilled water systematically triggering three suc-
cessive end-expiratory reflexively activated swallows with an
LaT of below 10 s. The following variables, LaT, EMGp, and
ALA elicited with PST, were considered as the control
values for the swallowing reflex in that patient.
CP Controller
If a 10 ml cold water bolus did not systematically elicit a
reflex swallow or a PST of .5 ml was associated with frank
tracheal aspiration signs, or if only poor-quality recordings
of LaT, EMGp, or ALA could be obtained during elicited
PnT reflex swallows, the patient was excluded from the study.
All signals were recorded simultaneously and stored on a
personal computer.
Fig 1 Schematic illustration of the method used to evaluate the
The control values of the swallowing reflex were com-
influence of CP increase on the swallowing reflex in tracheosto-
mized patients. EMG and laryngeal acceleration (LA) were mea- pared with those obtained with the tracheostomy cuff
sured during reflexively elicited swallows at different values of inflated with air to different pressures: 5, 10, 15, 20, 25, 30,
CP measured using a CP controller (CPC). A pneumotachograph 40, 50, and 60 cm H2O (Endotest manometer, Pressure
and a differential pressure transducer (PnT) were used to syn- Cuffs, Rusch, Betschdorf, France), applied in a random order
chronize hypopharyngeal stimulations with the end-expiratory determined by a computer-generated randomization list. At
phase. A double-piston syringe (DPS) was used to simultaneously
each CP and for each variable (LaT, EMGp, and ALA), a
inject the pharyngeal stimulus (predefined: 0.3 –5 ml volume,
mean value of a set of three consecutive measures per-
cold 38C, distilled water bolus), and flush 1 ml of air within the
ventilatory circuit. formed over 1 min was normalized to the control value. An
interval of at least 1 min was allowed between each

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BJA Amathieu et al.

LaT

EMGp
EMG

ALA
LA

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Flow Expiration
Inspiration
300 ms
Pharyngeal
stimulation

Fig 2 Typical recording from one patient showing the characteristics of the swallowing reflex. EMG, electromyography; LA, laryngeal acceler-
ation. The peak EMG (EMGp) and ALA were measured. For each reflexively elicited swallow, EMGp and ALA were computed. Reflex swallows
were elicited during the end-expiratory phase using a continuous ventilatory flow monitoring. The latency time (LaT) of the swallowing
reflex was calculated as the time elapsing between the onset of the pharyngeal stimulation artifact (respiratory flow trace) and that of
the integrated EMG signal.

measurement and return to the basal respiratory rate was consent at the time of the trial. For these patients, consent
required before the next measurement was performed. to enter the study was given by family members. Retrospect-
After each set of three tests, CP was reset to 0 cm H2O. ively, we obtained signed consent from all the patients.
When all the measurements were completed, patients Six patients were excluded. Reasons for exclusion were a
were asked to swallow 10 ml of water gel coloured with a low amplitude of ALA measures (n¼2), poor pharyngeal sen-
white dye given orally with the cuff deflated. A flexible bron- sation as confirmed by the impossibility to trigger reflex
choscope was passed through the tracheostomy to identify swallows (n¼2), and because of frank tracheal aspiration
pulmonary aspiration manifest as coloured liquid seen on signs (n¼2) during PST determination.
the tracheal wall. The mean age of patients studied was 37 (range: 19–54) yr.
The overall impact of CP increase upon the swallowing Most of the patients were admitted in the ICU because of
reflex variables was evaluated using a Friedman test. Then, severe thoracic and abdominal trauma. Percutaneous trache-
a Wilcoxon non-parametric test for repeated measures was ostomy was performed 10 days after ICU admission (range;
performed to evaluate the impact of a specific level of CP 7–18). All the patients were fully conscious at the time of
upon each variable. swallowing reflex evaluation performed 14 (range: 5–20)
Regression lines obtained by the method of least squares days after cuffed tracheostomy tube placement.
and the Spearman correlation coefficients were calculated to The mean (SD) PST volume and control LaT were 1.5 (1.3)
assess the relationship between CP and the three variables ml and 1.5 (0.8) s, respectively. A significant linear relation-
LaT, EMGp, and ALA. Values are mean [standard deviation ship (P,0.05) was observed between PST and control LaT
(SD)] unless specified. A P-value of ,0.05 was considered [LaT¼0.4 (PST)+0.8; r 2 ¼0.726, P,0.05].
statistically significant. We observed that CP and LaT were significantly correlated
(Fig. 3). An inverse correlation was identified between CP and
both ALA and EMGp (Figs 4 and 5, respectively). The charac-
Results teristics of the swallowing reflex deteriorated with increasing
Eighteen patients were recruited and 12 completed the trial. CP. ALA and LaT were the most sensitive variables to CP in-
Among the recruited patients, four lacked capacity to give crease. ALA and LaT significantly deteriorated with a CP of

580
Swallowing with a tracheostomy tube BJA
25 and 30 cm H2O, respectively. When compared with the
Latency Time (% of Control) control value, the mean LaT was increased by 2.3-fold
350
Latency Time = 2.7(Cuff Pressure) + 70.3, when CP was 60 cm H2O.
300 *
r2 = 0.91, p <0.01 The mean changes in respiratory rate and SaO2 over the
250 * time period elapsing between the first and last CP tests
* were 1.5 (3.0) bpm and 21.9 (0.6)%, respectively. Four
200
* patients experienced pulmonary aspiration when attempting
150
to swallow 10 ml of coloured thin liquid.
100
50
0 10 20 30 40 50 60 Discussion
Cuff Pressure (cmH20) In this study, the sensory component of the swallowing
reflex was evaluated by LaT and the motor component was
Fig 3 Influence of CP (cm H2O) increase on the latency times of reflected by submental EMGp and resulting ALA. We demon-
the swallowing reflex expressed in the percentage of control strated that increasing tracheostomy tube CP influenced
measures. Values are means (blue diamonds) and SD (vertical both sensory and motor components of the swallowing

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bars), *P,0.05 when compared with control values. reflex. The swallowing reflex was progressively more difficult
to elicit with increasing CP and when activated, the resulting
motor swallowing activity was depressed. These findings
suggest that peripheral mechanical constraints and centrally
125 controlled inhibition may be involved in CP increase-induced
deterioration of instrumental characteristics of the swallow-
ALA (% of Control)

ing reflex.
100 * * We have used the method described by Nishino and col-
leagues6 7 using submental EMG to study the swallowing
75 * * * reflex. The method is easy to perform and to repeat in the
same patient and allows for evaluation of the pharyngeal
ALA= –0.8 (Cuff Pressure)
+102.1, r2 = 0.87, p < 0.01 reflex components of swallowing. We have improved the ac-
50 curacy of latency time calculation. Instead of visual observa-
0 10 20 30 40 50 60 tion of laryngeal movements, we identified precisely on
Cuff Pressure (cmH20) signal recordings both the time of pharyngeal stimulus and
the beginning of evoked EMG response. Moreover, we
Fig 4 Influence of CP (cm H2O) increase on swallowing-induced recorded the average values generated by repeated stimuli
laryngeal elevation accelerometry amplitude (ALA) expressed over 1 min. These methodological improvements prevented
as the percentage of control values. Values are means (blue dia- non-stimulated swallows interfering with our results. Al-
monds) and SD (vertical bars). *P,0.05 when compared with
though superficial submental EMG recording was shown to
control values.
be a valuable means of identifying swallowing activity, this
method does not allow precise quantification of pharyngeal
muscular activity.
In order to better quantify the motor component of the
125
swallowing reflex, we performed simultaneous measure-
EMGp (% of Control)

ments of submental EMG in combination with the resulting


* acceleration of laryngeal elevation. It has been demon-
100 *
* strated that the pattern of laryngeal elevation acceleration
characterizes pharyngeal subhyoid muscle function and the
75 resulting acceleration signal peak amplitude correlates with
the amount of laryngeal elevation.8 9
EMGp = –0.5 (Cuff Pressure) + 104.7,
r2 = 0.88, p < 0.01
When compared with healthy volunteers placed in the
50 same experimental conditions (personal unpublished data),
0 10 20 30 40 50 60 reflex swallows in tracheostomized conscious young patients
Cuff Pressure (cmH20) required a more intense afferent input to be elicited and
demonstrated a longer activation time. A number of factors
Fig 5 Influence of CP (cm H2O) increase on the integrated peak may explain this fact. Although we did not examine directly
electromyography (EMGp) of the submental swallowing muscles the mucosal lesions caused by prolonged contact of upper
expressed as the percentage of control measures. Values are airway tubes (nasogatric and orotracheal), the alteration of
means (blue diamonds) and SD (vertical bars). *P,0.05 when chemoreceptors or mechanoreceptors located in pharyngeal
compared with control values.
mucosa may have impaired sensation, resulting in an

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BJA Amathieu et al.

increased PST. It has been demonstrated that residual effects patients we studied had normal hyoid bone displacement,
of sedation influence the swallowing reflex and such cannot but this displacement was performed with reduced accelera-
be excluded as a cause for the prolonged swallowing reflex tion when tracheostomy CP increased.
latency time.10 The influence of other factors such as hypox- The results we report on the effect of CP on the swallowing
aemia and hypercabia that have been demonstrated to have clinical implications for intensive care daily practice. Al-
impair the swallowing reflex appear unlikely in the present though all patients we have included in the present trial were
study.11 All of our patients were weaned from mechanical capable of swallowing on command, most of them had ab-
ventilation assistance before entering the protocol and SpO2 normal airway protective mechanisms. The present results
did not vary during the tests. Since respiratory rate we have emphasize for strict monitoring of CP in ICU tracheostomized
measured remained stable during CP increase challenge, it patients. Inflation of tracheostomy cuff is mandatory but po-
is unlikely that large arterial CO2 changes may have occurred. tentially a harmful procedure. Excessive CP may not only ser-
Although tracheal cuff-induced dysphagia in tracheosto- iously damage tracheal wall with the risk of tracheal
mized patients has been discussed in many publications, ulceration, dilatation, and perforation, but also impair spon-
only few have investigated the influence of CP on airway pro- taneous rehabilitation and efficiency of protective reflexes
tection mechanisms.12 – 14 No study has evaluated the such as the swallowing reflex. We demonstrated that when
impact of tracheostomy CP upon swallowing physiology. CP exceeds 20–25 cm H2O, reflex swallows were elicited

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The frequency of reduced laryngeal elevation and silent as- with difficulty and the efficiency of submental muscles was
piration has been shown to be greater when the cuff is depressed. Impeded laryngeal elevation during swallowing
inflated.12 13 Deflation of the tracheostomy cuff was shown was associated with imperfect closure of the larynx, resulting
to reduce the aspiration risk for liquid boluses and improve in possible aspiration of pharyngeal content.20 With a
the laryngeal excursion during swallows.12 We did not CP-induced reduction in spontaneous swallows and an
study the efficiency of airway protective mechanisms, but open larynx, pharyngeal secretions may flow into the
rather analysed the impact of tracheostomy CP on physio- trachea and accumulate above the cuff with the risk of pul-
logical mechanisms controlling the swallowing reflex. Our monary aspiration. Moreover, maintaining an efficient swal-
observations suggest that central inhibition of the swallow- lowing reflex may favour high spontaneous swallowing
ing centre is probably involved in CP increase-induced deteri- rates, which probably contribute to swallowing effectiveness.
oration of the characteristics of the swallowing reflex. The In the case of dysphagia, swallowing function should be
swallowing reflex was progressively more difficult to elicit evaluated and re-educated with a CP controlled at 20–25
with increasing CP. This observation agrees with physiological cm H2O.
studies demonstrating that sensory inputs from peripheral Our study has limitations. First, we tested the effect of CPs
receptors affect the control of swallowing.15 EMG data and exceeding 30 cm H2O, that is, higher than the commonly
recordings of vagal motor fibres show reversible inhibition recommended CP. Moreover, we showed that the greatest
of swallowing during distension of the cervical oesophagus.16 impact of CP upon swallowing reflex occurred at the
Using an intra-oesophageal balloon, Jean17 demonstrated highest CPs. However, we demonstrated that LaT and ALA,
that the neuronal swallowing activity was delayed and wea- both important determining factors for airway protective
kened by slight distension of cervical oesophagus and sup- swallowing reflex efficiency, were significantly altered for
pressed when the distension was increased. The authors CP situated in the upper limit of the normal range. Secondly,
also demonstrated that after balloon deflation, neuronal we have excluded from the present study patients showing
swallowing activity returned to normal. Increasing the poor pharyngeal perception and aspiration signs suggesting
tracheostomy tube CP was shown to increase intraluminal severe dysphagia. Then, it is questionable whether our find-
proximal oesophageal pressure.18 These observations ings could be applicable to patients with severe swallowing
mimic our data in tracheostomized patients. Inflation of difficulties. We believe that the more the airway protective
the cuff induced-oesophageal anterior mucous membrane reflexes are altered, the more the impact of strict CP
distension may have stimulated oesophageal mecano/ control during ICU stay is crucial for patient’s recovery of ef-
stretch receptors, resulting in an inhibition of the central ficient swallowing reflex. Finally, we demonstrated significant
control of swallowing causing both a delayed swallowing correlations between CP and instrumental characteristics of
reflex and impaired muscular activity of submental muscles. the swallowing reflex, but it does not mean that these rela-
The most marked effect of CP increase was lengthening of tions are strictly linear. Indeed, a non-linear relationship
the swallowing reflex latency time by 2.3-fold when com- between CP and the measured parameters we have studied
pared with the control. The magnitude of the decrease in la- may better explain our results. Moreover, non-linear relation-
ryngeal acceleration was less marked with a maximum ship analysis may permit identification of a critical pressure
reduction to 42% of control values at 60 cm H2O CP. Our range for each variable, resulting at the point of deviation
results do not contradict a recent pharyngeal swallow bio- from linearity. Careful observation of Figures 3–5 suggests
mechanics trial which concluded that tracheostomy tubes such a critical CP in the range of 25– 40 cm H2O, above
do not affect laryngeal movement.19 The authors did not which the impact of CP increase upon the swallowing reflex
measure tracheostomy CP, but rather inflated the cuff with seems to be marked. Above this critical CP range, the swal-
a standard volume for all patients.19 It is possible that the lowing reflex is more difficult to elicit, the activity of

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Swallowing with a tracheostomy tube BJA
swallowing muscles is depressed, resulting in severe impair- 6 Nishino T, Takizawa K, Yokokawa N, Hiraga K. Depression of the
ment of their efficiency at elevating the larynx as illustrated swallowing reflex during sedation and/or relative analgesia pro-
by intense reduction of laryngeal elevation acceleration. duced by inhalation of 50% nitrous oxide in oxygen. Anesthesi-
ology 1987; 67: 995– 8
Interestingly, this critical CP range is situated within the
7 Nishino T, Hiraga K. Coordination of swallowing and respiration in
clinical range of pressure commonly measured in ICU
unconscious subjects. J Appl Physiol 1991; 70: 988–93
tracheostomized patients. Thus, although our results are
8 Reddy NP, Katakam A, Gupta V, Unnikrishnan R, Narayanan J,
statistically relevant, possible non-linear relationship analysis Canilang EP. Measurements of acceleration during videofluoro-
between tracheostomy tube CP and electrophysiological graphic evaluation of dysphagic patients. Med Eng Phys 2000;
parameters of the swallowing reflex may be more clinically 22: 405– 12
pertinent. 9 Reddy NP, Simcox DL, Gupta V, et al. Biofeedback therapy using
In conclusion, CP in the tracheostomy tube influences the accelerometry for treating dysphagic patients with poor laryngeal
characteristics of the swallowing reflex in conscious tra- elevation: case studies. J Rehabil Res Dev 2000; 37: 361–72
cheostomized patients. Excessive CP alters electrophysio- 10 Dhonneur G, Rimaniol JM, el Sayed A, Lambert Y, Duvaldestin P.
Midazolam/propofol but not propofol reversibly depress the swal-
logical characteristics of the swallowing reflex.
lowing reflex. Acta Anaesthesiol Scand 1994; 38: 244
11 Nishino T, Kohchi T, Honda Y, Shirahata M, Yonezawa T. Differ-
Acknowledgements

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very helpful respective contribution to the editing process
physiology. Dysphagia 2003; 18: 284– 92
and statistical assistance.
13 Conway DH, Mackie C. The effects of tracheostomy cuff deflation
during continuous positive airway pressure. Anaesthesia 2004;
Declaration of interest 59: 652–7
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cuff inflated or deflated: a retrospective study. Head Neck 2005;
27: 809–13
Funding 15 Jean A. Brain stem control of swallowing: neuronal network and
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16 Jean A. Control of the central swallowing program by inputs from
the peripheral receptors. A review. J Auton Nerv Syst 1984; 10:
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