Intensive Care Med (2012) 38:85–90

DOI 10.1007/s00134-011-2417-8 ORIGINAL

Hélène Prigent
Michèle Lejaille
Effect of a tracheostomy speaking valve
Nicolas Terzi on breathing–swallowing interaction
Djillali Annane
Marjorie Figere
David Orlikowski
Frédéric Lofaso

H. Prigent
M. Lejaille
M. Figere
electromyography, cervical piezo-

Received: 14 June 2011 D. Orlikowski
F. Lofaso
Accepted: 21 October 2011 electric sensor, and nasal and tracheal
EA 4497, Université de Versailles flow recording. Three water-bolus
Published online: 24 November 2011
Ó Copyright jointly held by Springer and Saint-Quentin-en-Yvelines,
78035 Guyancourt, France sizes (5, 10, and 15 mL) were tested
ESICM 2011 in random order. Results: Swallow-
ing characteristics and breathing–
Abstract Purpose: Expiratory swallowing synchronisation were not
flow towards the upper airway after influenced by SV use. However,
swallowing serves to expel liquid or expiratory flow towards the upper
H. Prigent
M. Lejaille
D. Annane
food particles misdirected towards the airway after swallowing was negligi-
M. Figere
D. Orlikowski
F. Lofaso ()) trachea during swallowing. However, ble without the SV and was restored
Hôpital Raymond Poincaré, Services de expiration may not occur consistently by adding the SV. Conclusion: In
Physiologie-Explorations Fonctionnelles, after swallowing in tracheostomised tracheostomised patients, protective
Réanimation Médicale, Centre patients with an open tracheostomy expiration towards the upper airway
d’Investigation Clinique et d’Innovation tube. We investigated the effect of a after swallowing is restored by the
Technologique (INSERM Unit 805), APHP,
92380 Garches, France speaking valve (SV) on breathing– use of an SV.
e-mail: f.lofaso@rpc.ap-hop-paris.fr swallowing interactions and on the
Tel.: ?33-1-47107941 volume expelled through the upper Keywords Tracheostomy

Fax: ?33-1-47107943 airway after swallowing. Speaking valve
Deglutition

Methods: Eight tracheostomised Aspiration
Subglottic air pressure
N. Terzi neuromuscular patients who were
INSERM, ERI27, Service de Réanimation able to breathe spontaneously were
Médicale, CHRU Caen, 14000 Caen, France
studied with and without an SV.
F. Lofaso Breathing–swallowing interactions
INSERMU 955, Créteil, France were investigated by chin

Introduction impairment of the vocal-cord closure reflex [3], disuse

In patients with acute respiratory failure, the nature or
seriousness of the underlying disease may require a tra-
cheostomy after the initial phase of intensive care, to allow
either prolonged weaning or ventilation. One crucial
decision in tracheostomised patients is whether to resume
oral feeding. It has been demonstrated that the presence of
a tracheostomy tube often induces or increases aspiration.
Mechanisms that may explain this effect include tethering
of the larynx [1], desensitisation of the upper airway [2],
atrophy of the laryngeal muscles [4], oesophageal com-
pression by the inflated cuff [5], and loss of subglottic air
pressure during swallowing [6]. These last two factors can
easily be avoided by using a cuffless tracheostomy tube
and a speaking valve (SV), respectively [6–10].
Another potential advantage of SV use may be
improved breathing–swallowing coordination. A study in
healthy individuals showed that swallowing often occurred
after expiration initiation, coincided with a period of
apnoea, and was usually followed by further expiration
86

[11]. Other studies [12–16] confirmed these findings and
established that the expiratory activity surrounding swal-
lowing helped to prevent the passage of noxious chemicals
and microbes from the mouth to the lungs. However, tra-
cheostomised patients expire at least in part through the
tracheostomy tube [6], which may eliminate the protection
afforded by expiration to the upper airways, unless the
expired gas is directed towards the upper airways by an SV.
The aim of this study was to investigate upper airway and
tracheostomy tube flows during swallowing and to assess
breathing–swallowing interactions with and without an SV
in a selected population of stable tracheotomised patients.
patients were tested with (SV?) and without (SV-) a
Passy-Muir speaking valve (Passy-Muir Inc, Irvine, CA,
USA), in random order. A syringe was used to place water
boluses in the mouth. In each condition, three bolus sizes
(5, 10, and 15 mL) were administered in random order.
Four sets of three boluses were studied, taking care not to
use the same bolus size twice consecutively. The study
participants were blinded to bolus size. They were
instructed to swallow normally while trying to be as
efficient as possible.
Data analysis

Swallowing onset was defined as the onset of phasic

Methods
Study population
We conducted a prospective observational study from
February 2010 to February 2011. The patients were
recruited during routine follow-up visits for home-venti-
lation management at the Raymond Poincaré Teaching
Hospital, Garches, France. Patients were eligible if they
had had a tracheostomy with a cuffless tube for at least
6 months, usually ate without ventilatory assistance, used
an SV, and were in stable clinical condition. All study
patients provided written informed consent. The study
was approved by the relevant ethics committee (Ambroise
Paré Teaching Hospital, Boulogne, France).
submental electromyographic activity and swallowing
termination as the beginning of the downward laryngeal
movement detected by the piezoelectric sensor [18, 19].
For each bolus size, we recorded the duration of swal-
lowing, number of swallows, and number of ventilatory
cycles. The percentages of swallows preceded and fol-
lowed by expiration were calculated. In addition, when
the swallows were followed by expiration, the post-
swallowing nasal expiratory volume was routinely mea-
sured; and in the SV- condition, the expiratory volume
leaking through the tracheostomy tube during and after
swallowing was measured.
Statistical analysis

All results are described as mean ± standard deviations

Study procedures in the text and as mean ± standard error of the mean in
the figures. Statistical tests were run using the StatView 5
Tracheal and nasal flows were measured using pneumota- package (SAS Institute, Grenoble, France).
chographs (Fleisch no. 2, Lausanne, Switzerland). Patients Two-way (SV effect and bolus-size effect) analysis of
wore a nasal mask (Flexifit 407, Fisher & Paykel Healthcare variance (ANOVA) with repeated measures was used.
Ltd, Auckland, New Zealand) connected to the pneu- Values of p below 0.05 were considered statistically
motacograph. With the SV in place, tracheal pressure was significant.
measured at the proximal end of the tracheostomy tube
using a differential pressure transducer (Validyne MP
45 ± 100 cmH2O, Northridge, CA, USA). Swallowing
was monitored non-invasively, using electromyography to
detect submental muscle activity via skin-surface elec-
Results
trodes on the chin and a piezoelectric sensor placed between Patients
the cricoid and thyroid cartilages, as described elsewhere
[17–19]. All signals were digitised and recorded directly on
The demographic and ventilatory characteristics of the
a personal computer. During the recording, we checked that
eight study participants are reported in Table 1. Mean age
the mouth was closed, although this behaviour was not was 37.5 ± 12.2 years. Except for one patient (no. 4)
suggested to the patients. who had fluctuating respiratory function and remained
tracheostomised until the underlying disease (myasthenia
gravis) was stabilised under treatment, all patients had
Experimental protocol severe neuromuscular respiratory failure (vital capacity
B60%). All patients had been tracheostomised after an
Each patient was seated comfortably with the head and episode of acute respiratory failure with weaning failure;
neck maintained in the patient’s preferred position. All they were ventilated intermittently but remained
 87

Table 1 Baseline patient characteristics

No. Diagnosis Age Height Weight Duration of VC MEP MIP VT Duration

(years) (cm) (kg) tracheostomy sitting (cmH2O) (cmH2O) during of
(years) (%) SB mechanical
(mL) ventilation
(h/day)

1 Becker muscular dystrophy 43 191 88 10 11 65 54 165 13

2 Facioscapulohumeral muscular 62 180 56 11 36 10 19 330 11
dystrophy
3 Pompe disease 53 169 66 8 26 20 11 260 12
4 Myasthenia gravis 57 159 64 0.5 90 41 45 245 9
5 Congenital muscular dystrophy 35 153 43 5 29 42 12 490 15
6 Spinal amyotrophy 29 163 50 12 25 14 27 330 0
7 MERRF syndrome 29 172 56 3 60 11 31 510 8.5
8 Selenoprotein N muscular 46 150 31 5 21 37 26 168 15
dystrophy
VC vital capacity, MIP maximal inspiratory pressure, MEP maximal expiratory pressure, VT tidal volume, SB spontaneous breathing, SDs
standard deviations, MERRF myoclonic epilepsy with ragged red fibres

tracheostomised because of either severe progressive
respiratory failure or patient refusal to use an alternative
interface (nos. 2, 3, and 7). Patient 6 met criteria for
ventilatory assistance (severe respiratory failure, hyper-
capnia, and nocturnal hypoventilation) but refused to be
ventilated. Mean duration of invasive ventilation per day
was 15 ± 6 h.
In the SV? condition, the peak positive pressure in the
tracheostomy tube occurred during swallowing and the
mean pressure value ranged from 1.4 to 8.6 cmH2O. The
volume swallowed did not influence tracheostomy tube
pressure (ANOVA, p = 0.23). An example is shown in
Fig. 1b.

Swallowing description Coordination between swallowing and respiration

Piecemeal deglutition occurred in all patients, with each
bolus often requiring several swallows over several
breathing cycles. However, the duration of swallowing,
the number of swallows per bolus, and the number of
ventilatory cycles per bolus did not differ significantly
between SV- and SV? (Table 2). In contrast, increasing
the bolus size significantly increased the total bolus
swallowing time, number of swallows per bolus, and
number of breathing cycles per swallow (Table 2).
In the SV- condition, leaks occurred through the
tracheostomy tube during all expirations. In addition,
during expirations bracketing swallowing, leakage
through the tube continued before, during, and after the
swallowing period, as shown in the example in Fig. 1a.
The percentage of swallows followed by expiration was
not significantly different between SV- and SV?
(Table 2) and was not influenced by bolus size (Table 2).
However, when swallows were followed by expiration,
the volume expired through the upper airway after expi-
ration was considerably lower in SV- (mean values
below 20 mL) compared with SV? (ANOVA, valve
effect p = 0.0003, Fig. 2), although the total expired
volume during and after swallowing was higher (but not
significantly) in SV- than in SV? (5 mL bolus size:
139 ± 80 vs. 124 ± 62 mL; 10 mL bolus size: 144 ± 63
vs. 104 ± 56 mL; and 15 mL bolus size: 151 ± 60 vs.
112 ± 59 mL, respectively; ANOVA, valve effect:
p = 0.12)

Table 2 Swallowing variables per bolus according to bolus size (5, 10, or 15 mL) and test condition: without (SV-) and with (SV?) a
tracheostomy valve

5 mL 10 mL 15 mL ANOVA (p value)
SV- SV? SV- SV? SV- SV? SV effect Volume effect

Duration of swallowing (s) 2.5 ± 2.4 2.9 ± 3.8 3.8 ± 2.7 4.4 ± 4.4 4.5 ± 3.2 4.6 ± 4.8 0.62 0.001
Number of swallows per bolus 1.6 ± 1.0 1.6 ± 1.1 2.2 ± 1.2 2.1 ± 1.4 2.6 ± 1.3 2.3 ± 1.7 0.37 0.001
Number of ventilatory cycles per bolus 1.0 ± 0.0 1.2 ± 0.4 1.3 ± 0.6 1.7 ± 1.0 1.3 ± 0.6 1.6 ± 1.1 0.44 0.006
% of swallows followed by expiration 65 ± 34 82 ± 24 72 ± 28 78 ± 21 62 ± 30 74 ± 28 0.37 0.51
88

Fig. 1 Breathing–swallowing
interaction in a tracheostomised
patient without (a) and with
(b) a speaking valve. The
upper-airway zero-flow periods
within the swallowing periods
are shaded in grey. Panel
a without the SV, the persistent
expiratory leak through the
tracheostomy tube during
swallowing apnoea resulted in
the lack of upper airway flow
(arrows). Panel b with the SV,
no leakage occurred through the
tracheostomy during
swallowing apnoea but a small
inspiratory spike (hollow
arrow) coinciding with the end
of the apnoea occurred, at a
time when tracheal pressure
was positive (solid arrow),
excluding a concomitant
inspiratory effort as the cause of
this spike

Discussion
This study showed that, without an SV, a significant part
of the expiratory flow leaked through the tracheostomy
tube. Leakage also occurred during upper airway occlu-
sion due to swallowing. Adding an SV to prevent leakage
through the tube did not significantly change the per-
centages of expirations occurring before and after
swallowing. However, the SV increased the expired vol-
ume through the upper airway after swallowing, which
was negligible without the SV.
Other findings were as follows. In both the SV? and
the SV- conditions, an inspiratory nasal flow spike
occurred nearly consistently at the end of the nasal zero Fig. 2 Comparison of expiratory volume through the upper airway
after swallowing each bolus size with (black columns) and without
flow curve (Fig. 1a, b), as previously described [12, 15]. (striped column) a speaking valve (ANOVA; valve effect
This spike coincided with the airway reopening during p = 0.0003; volume effect p = 0.54)
descent of the hyolaryngeal complex [15] and with a
slight negative pharyngeal pressure dip occurring with the as indicated by the finding in our study and an earlier
offset of pharyngeal contraction [12]. Accordingly, we study [6] of significant and continuous expiratory leakage
observed a concomitant peak of positive tracheal pressure through the tracheostomy tube during swallowing brack-
(Fig. 1b), confirming that the inspiratory spike was not eted by expiration.
related to an inspiratory effort. This spike was not taken Swallowing during expiration produces several bene-
into account in our measurements. fits. Expiration facilitates vocal cord adduction, thus
A study in healthy volunteers showed the occurrence affording a protective set point for further laryngeal clo-
of diaphragmatic activity consistent with active breath- sure as the swallow progresses [21]. In addition, the
holding that preserved the expiratory volume just before positive tracheal pressure facilitated by expiration plays a
swallowing, thereby allowing expiration at the end of the pivotal role in maintaining the glottis closure reflex [6,
swallowing apnoea [20]. However, this activity was not 22]. Finally, expiratory flow towards the upper airway
sufficient to induce breath-holding during swallowing in after swallowing expels liquid or food particles misdi-
tracheostomised patients with open tracheostomy tubes, rected toward the trachea during swallowing [12–16].
 89

Study limitations We used water to assess swallowing. There is some

We studied a heterogeneous population of neuromuscular
patients. However, we excluded neuromuscular patients
with central nervous system involvement that might
influence upper airway muscle coordination during
swallowing [23, 24]. In addition, in a previous study with
a similar but larger population [19], the increases in
swallowing duration and swallowing fragmentation cor-
related negatively with several respiratory muscle
performance markers but not with general functional
disability or the dysphagia index. In our study, each
patient served as his or her own control, and the SV
restored protective expiration towards the upper airway
after swallowing in all patients. It might be argued that
our results do not apply to patients with other causes of
respiratory failure requiring tracheostomy, such as
chronic obstructive pulmonary disease (COPD). How-
ever, in COPD patients, the abnormalities in swallow
timing within the respiratory cycle [25] are similar to
those in neuromuscular patients [19]. In addition, studies
in healthy individuals established that the occurrence of
inspiration after swallows was increased by hypercapnia
[26] or the application of an inspiratory elastic load [27],
suggesting that poor breathing–swallowing coordination
might be a non-specific sign of respiratory difficulty.
Therefore, there is no reason our results would not apply Acknowledgments The study was supported by the Association
to other populations with respiratory failure.
evidence that choking may occur only with solids in some
neuromuscular patients [28]. However, water rather than
jelly was used in most of the previous studies [12, 13, 27,
29], which allowed us to compare our results with earlier
data. Furthermore, the use of solids requires chewing,
which may cause fatigue, thereby worsening the swal-
lowing impairments.
Finally, SV use has been reported to improve swal-
lowing in tracheostomised patients by restoring a positive
subglottic pressure during swallowing [6–8]. In addition,
the SV restores a significant expiratory volume through
the upper airway after swallowing, which is considered to
prevent the passage of noxious chemicals and microbes
from the mouth into the lungs [12–16].
In conclusion, our previous studies supported the use
of mechanical ventilation in tracheostomised patients
during meals [19, 30]. However, mechanical ventilation
during meals is not always available or accepted under
real-life conditions (outside the intensive care unit), for
various non-medical reasons. This study confirms that the
use of an SV should be offered routinely during periods
off mechanical ventilation, to facilitate expiration through
the upper airway after swallowing and to decrease the risk
of aspiration or laryngeal penetration.
d’Entraide des Polios et Handicapés (ADEP).

References
1. Bonanno PC (1971) Swallowing
dysfunction after tracheostomy. Ann
Surg 174:29–33
2. Feldman SA, Deal CW, Urquhart W
(1966) Disturbance of swallowing after
tracheostomy. Lancet 1:954–955
3. Buckwalter JA, Sasaki CT (1984)
Effect of tracheotomy on laryngeal
function. Otolaryngol Clin North Am
17:41–48
4. DeVita MA, Spierer-Rundback L
(1990) Swallowing disorders in patients
with prolonged orotracheal intubation
or tracheostomy tubes. Crit Care Med
18:1328–1330
5. Betts RH (1965) Post-tracheostomy
aspiration. N Engl J Med 273:155
6. Eibling DE, Gross RD (1996)
Subglottic air pressure: a key
component of swallowing efficiency.
Ann Otol Rhinol Laryngol
105:253–258
7. Suiter DM, McCullough GH, Powell
PW (2003) Effects of cuff deflation and
one-way tracheostomy speaking valve
placement on swallow physiology.
Dysphagia 18:284–292
8. Gross RD, Mahlmann J, Grayhack JP
(2003) Physiologic effects of open and
closed tracheostomy tubes on the
pharyngeal swallow. Ann Otol Rhinol
Laryngol 112:143–152
9. Elpern EH, Borkgren Okonek M, Bacon
M, Gerstung C, Skrzynski M (2000)
Effect of the Passy-Muir tracheostomy
speaking valve on pulmonary aspiration
in adults. Heart Lung 29:287–293
10. Stachler RJ, Hamlet SL, Choi J,
Fleming S (1996) Scintigraphic
quantification of aspiration reduction
with the Passy-Muir valve.
Laryngoscope 106:231–234
11. Smith J, Wolkove N, Colacone A,
Kreisman H (1989) Coordination of
eating, drinking and breathing in adults.
Chest 96:578–582
12. Martin BJ, Logemann JA, Shaker R,
Dodds WJ (1994) Coordination
between respiration and swallowing:
respiratory phase relationships and
temporal integration. J Appl Physiol
76:714–723
13. Nishino T, Yonezawa T, Honda Y
(1985) Effects of swallowing on the
pattern of continuous respiration in
human adults. Am Rev Respir Dis
132:1219–1222
14. Paydarfar D, Gilbert RJ, Poppel CS,
Nassab PF (1995) Respiratory phase
resetting and airflow changes induced
by swallowing in humans. J Physiol
483(Pt 1):273–288
15. Martin-Harris B, Brodsky MB, Price
CC, Michel Y, Walters B (2003)
Temporal coordination of pharyngeal
and laryngeal dynamics with breathing
during swallowing: single liquid
swallows. J Appl Physiol 94:1735–1743
16. Boden K, Cedborg AI, Eriksson LI,
Hedstrom HW, Kuylenstierna R,
Sundman E, Ekberg O (2009)
Swallowing and respiratory pattern in
young healthy individuals recorded
with high temporal resolution.
Neurogastroenterol Motil 21:1163
e1101
90
17. Cohn MA, Rao AS, Broudy M, Birch S,
Watson H, Atkins N, Davis B, Stott FD,
Sackner MA (1982) The respiratory
inductive plethysmograph: a new non-
invasive monitor of respiration. Bull
Eur Physiopathol Respir 18:643–658
18. Ertekin C, Pehlivan M, Aydogdu I,
Ertas M, Uludag B, Celebi G,
Colakoglu Z, Sagduyu A, Yuceyar N
(1995) An electrophysiological
investigation of deglutition in man.
Muscle Nerve 18:1177–1186
19. Terzi N, Orlikowski D, Aegerter P,
Lejaille M, Ruquet M, Zalcman G,
Fermanian C, Raphael JC, Lofaso F
(2007) Breathing–swallowing
interaction in neuromuscular patients: a
physiological evaluation. Am J Respir
Crit Care Med 175:269–276
20. Hardemark Cedborg AI, Sundman E,
Boden K, Hedstrom HW, Kuylenstierna
R, Ekberg O, Eriksson LI (2009) Co-
ordination of spontaneous swallowing
with respiratory airflow and
diaphragmatic and abdominal muscle
activity in healthy adult humans. Exp
Physiol 94:459–468
21. Martin-Harris B, Brodsky MB, Michel
Y, Ford CL, Walters B, Heffner J
(2005) Breathing and swallowing
dynamics across the adult lifespan.
Arch Otolaryngol Head Neck Surg
131:762–770
22. Ikari T, Sasaki CT (1980) Glottic
closure reflex: control mechanisms.
Ann Otol Rhinol Laryngol 89:220–224
23. Ertekin C, Aydogdu I, Yuceyar N,
Kiylioglu N, Tarlaci S, Uludag B
(2000) Pathophysiological mechanisms
of oropharyngeal dysphagia in
amyotrophic lateral sclerosis. Brain
123(Pt 1):125–140
24. Ertekin C, Yuceyar N, Aydogdu,
Karasoy H (2001) Electrophysiological
evaluation of oropharyngeal
swallowing in myotonic dystrophy.
J Neurol Neurosurg Psychiatry
70:363–371
25. Gross RD, Atwood CW Jr, Ross SB,
Olszewski JW, Eichhorn KA (2009)
The coordination of breathing and
swallowing in chronic obstructive
pulmonary disease. Am J Respir Crit
Care Med 179:559–565
26. Nishino T, Hasegawa R, Ide T, Isono S
(1998) Hypercapnia enhances the
development of coughing during
continuous infusion of water into the
pharynx. Am J Respir Crit Care Med
157:815–821
27. Kijima M, Isono S, Nishino T (1999)
Coordination of swallowing and phases
of respiration during added respiratory
loads in awake subjects. Am J Respir
Crit Care Med 159:1898–1902
28. Pane M, Vasta I, Messina S, Sorleti D,
Aloysius A, Sciarra F, Mangiola F,
Kinali M, Ricci E, Mercuri E (2006)
Feeding problems and weight gain in
Duchenne muscular dystrophy. Eur J
Paediatr Neurol 10:231–236
29. Hadjikoutis S, Pickersgill TP, Dawson
K, Wiles CM (2000) Abnormal patterns
of breathing during swallowing in
neurological disorders. Brain 123(Pt
9):1863–1873
30. Terzi N, Prigent H, Lejaille M, Falaize
L, Annane D, Orlikowski D, Lofaso F
(2010) Impact of tracheostomy on
swallowing performance in Duchenne
muscular dystrophy. Neuromuscul
Disord 20:493–498