Clinical Rehabilitation 2007; 21: 41
46

Pre-emptive swallowing stimulation in long-term

intubated patients
Chang Ho Hwang Department of Physical Medicine and Rehabilitation Medicine, Ulsan University Hospital, Ulsan and
Kyoung Hyo Choi Department of Physical Medicine and Rehabilitation Medicine, Yoon Suk Ko and Chae Man Leem
Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea

Received 4th October 2005; returned for revisions 25th March 2006; revised manuscript accepted 12th May 2006.

Objective: To evaluate the effect of pre-emptive swallowing stimulation on the

recovery of swallowing function in long-term intubated patients.
Design and subjects: Patients in the intensive care unit intubated for at least
48 hours due to respiratory distress from March to August 2004 were randomly
divided into two groups. Fifteen patients of mean age 55.39/17.9 years were
stimulated (experimental group) and 18 patients of mean age 61.39/13.5 years were
not stimulated (control group). The duration of intubation was 15.59/6.7 days in the
experimental group and 15.79/6.5 days in the control group. Duration of stimulation
in the experimental group was 7.39/3.6 days. After extubation, we compared the
severity of dysphagia via video-fluoroscopic swallow study.
Results: There were no statistically significant differences in the percentage of
aspiration and the swallowed volume between the two groups. However, oral transit
time in the experimental group (0.379/0.07 seconds) was significantly shorter than
that of the control group (0.839/0.10 seconds), and the oropharyngeal swallowing
efficiency of the experimental group (73.39/17.4%/s) was significantly higher than
that of the control group (50.19/13.0%/s).
Conclusion: Pre-emptive swallowing stimulation during intubation assists in the
recovery of swallowing function in long-term intubated patients.

Introduction aspiration pneumonia, prolonging hospital stay

Patients intubated over a long period of time have
a significantly increased risk of aspiration, with
dysphagia being common in patients intubated for
at least 48 hours.1
3 Aspiration after intubation
may be due to the slow resolution of laryngeal
lesions for three months after extubation,4 or to
the slow recovery of a decreased gag reflex after
one week in patients intubated for at least 24
hours.5 Intubation also increases the risk of
Address for correspondence: Chang Ho Hwang, Department of
Physical Medicine and Rehabilitation Medicine, Ulsan Uni-
versity Hospital, 290-3 Jeonha-dong, Dong-gu, Ulsan 682-714,
Korea. e-mail: chhwang1220ciba@yahoo.co.kr
# 2007 SAGE Publications
and increasing mortality. Although prolonged
intubation is associated with the possibility of
these complications, it has not received enough
attention in the broader context of critical care.
There has been no published research to investi-
gate the use of modalities with the specific goal of
improving swallowing function and therefore pos-
sibly preventing some of these complications.
Laryngotracheal sequelae, including traumatic
injury, decreased gag reflex and mucosal ulcera-
tion, are also very common after prolonged
intubation and may add to swallowing diffi-
culties.4
8 The exact mechanism, however, has
not yet been proven. De Larminant et al. proposed
10.1177/0269215506071286

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42 CH Hwang et al.
that the presence of an orotracheal tube has been
shown to alter the mechanoreceptors and chemo-
receptors of the pharyngeal and laryngeal muco-
sae.5 Recently Barquist et al. reported that non-use
of laryngopharyngeal muscles during intubation
causes both the freezing of muscles and mucosal
lesions, making loss of proprioception a mechan-
ism of dysphagia.2
Our hypothesis is that regular pre-emptive
swallowing stimulation could potentially prevent
or decrease loss of proprioception, muscle atrophy,
and changes of mechanoreceptors or chemorecep-
tors in the oropharynx, thus assisting in the
recovery of swallowing function following extuba-
tion. We therefore investigated swallowing function
following extubation using video-fluoroscopic
swallow study.
Methods
Pre-emptive swallowing stimulation
A routine of pre-emptive swallowing stimulation
was designed for this study in the Department of
Physical Medicine and Rehabilitation Medicine.
Pre-emptive swallowing stimulation consisted of
thermal
tactile stimulation, oral stimulation, oral
massage, digital manipulation and a cervical range
of motion exercise (see Appendix). Patients in the
experimental group received this pre-emptive swal-
lowing stimulation for 15 minutes twice daily, six
days per week, in a semi-fowler position with the
back rest at 30
45 degrees from the third day after
intubation until video-fluoroscopy. Only one occu-
pational therapist performed the pre-emptive swal-
lowing stimulation.
Both the experimental and the control group
received general oral hygiene such as tooth brush-
ing or clearing of mouth secretions with cotton
gauze as required.
Video-fluoroscopic swallow study
Sedatives and neuromuscular blockers were
withheld for 24 hours prior to video-fluoroscopy
swallow study.5 Immediately before the study,
nasogastric tube and any materials adhering to
the oral cavity were removed, and for patients with
tracheostomies, the cuffs/balloons were deflated.
During video-fluoroscopic swallow study arter-
ial oxygen saturation was monitored using pulse
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oxymetry and maintained above 94%. Oxygen was
administered via nasal prong if required. Respira-
tory rate was monitored and maintained below
24 breaths per minute. Patients were fed the five
kinds consistency diet, consisting of 80 g each of
yogurt, pureed fruit and pudding mixed with 10 g
liquid barium sulfate (Solotop suspension 140;
Taejoon Inc, Seoul, Korea), 5 mL of thin liquid
composed of 140 g/mL liquid barium sulfate mixed
with 300 mL of normal saline down to 35%/v
(thin-consistency test liquid), and 5 mL thick
liquid composed of 140 g/mL of liquid barium
sulfate mixed with 100 mL of normal saline down
to 70%/v (thick-consistency test liquid) as study
materials.9
The video-fluoroscopic swallow study was per-
formed using digitalized fluoroscopy (IRF-
850
150; Philips, Eindhoven, Noord Brabant,
Netherlands) and a dynamic storing method.
Parameters measured and calculated were aspira-
tion, silent aspiration, swallowed volume, oral
transit time (OTT), pharyngeal transit time
(PTT), oropharyngeal transit time (OPTT), and
oropharyngeal swallowing efficiency (OPSE) after
extubation. Aspiration was defined as the entry of
a material into the airway below the level of the
true vocal folds, with silent aspiration occurring in
the absence of any external behavioural signs such
as coughing or choking.3
Oropharyngeal swallowing efficiency, the ratio
of the percentage swallowed to the total swallow-
ing time in the oral and pharyngeal stages, was
measured by Peta-Motion for Clinics (AMC,
Seoul, Korea) and Adobe Premiere 6.0. Oral
transit time is the time (in seconds) from the
onset of bolus movement in the mouth until
the head of the bolus reaches the point where the
lower rim of the mandible crosses the base of the
tongue base. Pharyngeal delay time (PDT) is
the time (in seconds) from the arrival of the
bolus head at the point where the lower rim of
the mandible crosses the base of the tongue until
the first laryngeal elevation. Pharyngeal response
time (PRT) is the time (in seconds) from the first
laryngeal elevation until the bolus tail passes
through the cricopharyngeal region. Pharyngeal
transit time is the sum of pharyngeal delay time
and pharyngeal response time. Residue is the
approximate percentage of the bolus remaining
in the oral cavity (ORES) and pharynx (PRES)
 Pre-emptive swallowing stimulation 43

after completion of the first swallow of a bolus, tory disease, 14 for infectious disease, 2 for gastro-
and aspiration is the approximate percentage of intestinal disease, and 1 for cancer.
the bolus aspirated before (ASPB) and during The patients were assigned randomly to two
(ASPD) a swallow.10 groups. There were no significant differences
between the groups in age, sex, number of
100  (ORES  PRES  ASPB  ASPD) tracheostomies, time until video-fluoroscopic swal-
OPSE
OTT  PTT low study, and duration of intubation (Table 1).

The study was performed in a double-blind Clinical evaluation

manner, in which the patient, video-fluoroscopic There were no statistically significant differences
swallow study examiner and assessor did not between the experimental and control groups in
know whether a patient was assigned into the occurrence of aspiration pneumonia, length of stay
experimental or the control group. All patients of in the medical intensive care unit, days to oral
both groups took video-fluoroscopic swallow intake, and days to discharge (Table 2).
study after extubation routinely. None of the
patients could see the pre-emptive swallowing
Evaluation of swallowing function
stimulation done to other patients because of
There were no statistically significant differences
temporal screening. Randomization and alloca-
between the experimental and control groups in
tion was done using a random assignments
measures of aspiration, silent aspiration, swal-
generator (Medusa, solution@randombots.com,
lowed volume, and pharyngeal transit time.
Long Beach, CA, USA). Only the one occupa-
There were, however, statistically significant
tional therapist who performed pre-emptive swal-
differences between the groups in measures of
lowing stimulation knew these assignments.
oral transit time, oropharyngeal transit time, and
The Fisher’s exact test was used to evaluate the
oropharyngeal swallowing efficiency (Table 3).
effect of sex and presence of tracheostomy, aspira-
Each of these measures were significantly faster
tion pneumonia, subglottic aspiration, silent sub-
in the experimental group.
glottic aspiration, and discharge to home. The
Wilcoxon rank sum test was used to evaluate the
effect of age, days to video-fluoroscopic swallow
study, duration of intubation, stay in intensive care Discussion
unit, days to oral intake, swallowed volume, oral
transit time, pharyngeal transit time, oropharyn- In this study a statistically significant improvement
geal transit time, and oropharyngeal swallowing in mathematical variables of oral transit time,
efficiency. Windows SPSS version 10.0 was used oropharyngeal transit time, and oropharyngeal
for all mathematic evaluations. A P-value below swallowing efficiency was demonstrated by use
0.05 was defined as statistically significant.
Table 1 Descriptive data

Case Control P-value

Number 15 18
Results M/F 8/7 9/9 1.000
Age (years) 55.39/17.9 61.39/13.5 0.361
Subjects Extubation to VFSS 4.99/3.2 4.79/3.0 0.873
Thirty-three patients who required intuba- (days)
tion for at least 48 hours because of respiratory Duration of 15.59/6.7 15.79/6.5 0.656
intubation (days)
difficulty in the medical intensive care unit from Tracheostomy (%) 8 (53%) 8 (44%) 0.732
March to August 2003 were studied prospectively. Duration of training 7.39/3.6 0
Patients were excluded if they had a history of (days)
intubation or dysphagia, traumatic brain injury,
injury of cranial nerves, or neuromuscular disease. Values are mean9/standard deviation.
Sixteen of these patients were admitted for respira- VFSS, Video-fluoroscopic swallow study.

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44 CH Hwang et al.

Table 2 Clinical data

Clinical messages
Case Control P-value

Number 15 18 . In patients with endotracheal intubation,

Pneumonia (%) 0 (0%) 2 (11%) 0.489 pre-emptive swallowing stimulation for
ICU stay (days) 29.29/16.9 22.49/10.0 0.166 15 minutes twice daily while intubated
To oral intake (days) 7.49/7.4 11.99/10.5 0.166
Discharge to home (%) 10 (66%) 10 (55%) 0.722
improved oropharyngeal swallowing effi-
ciency when extubated.
Values are mean9/standard deviation. . There was no difference in major clinical
ICU, intensive care unit. outcomes, but the numbers were too small to
detect any.
of video-fluoroscopic swallow study in long-
term intubated patient who received pre-emptive
transit time in patients with mild dysphagia so this
swallowing stimulation. To our knowledge, this is
significant intergroup difference was observed.10
the first trial to investigate the effectiveness of
It has been claimed that intermittent aspiration
stimulation through the mouth during intubation. is likely to occur due to pooling of material in the
However, a clinical improvement of statistical vallecular pouch and pyriform sinuses.11 Although
significance was not found in variables such as in this study we noted increased pharyngeal
stay in intensive care unit, occurrence of pneumo- residue during pharyngeal phage of swallowing in
nia, days to oral intake, and number of patients both groups, we could not report the findings and
discharged to home. degree of vallecular stasis or pyriform sinus stasis
The results of this study suggest that pre- that may in fact be found out to be statistically
emptive swallowing training may have prevented significant.
or decreased loss of proprioception, muscle atro- Several variables correlated with dysphagia
phy and changes in mechano- or chemoreceptors require correction in a case
control study. The
in the oropharyngeal cavity by consistent stimula- Glasgow Coma Scale (GCS) during admission or
tion. Although we were able to objectively measure intubation has been found to affect dysphagia in
specific changes of this nature, this consequence trauma patients,2 therefore trauma patients were
was suggested by the statistically significant inter- excluded from this study. There is controversy
group differences in oral transit time, oropharyn- regarding nasogastric tubes, therefore these were
geal transit time and oropharyngeal swallowing removed prior to video-fluoroscopic swallow study.
efficiency. Even though there were no statistically Even though an increased incidence of aspiration
significant differences in swallowed volumes and has been reported in patients older than 65 years
pharyngeal transit time, oropharyngeal swallowing with tracheostomy,12 the mean ages in the two
efficiency is strongly correlated with oropharyngeal group were 55.39/17.9 years and 61.39/13.5 years.
We could not correct for predisposing medical
Table 3 Oropharyngeal swallowing efficiency conditions, however, including gastroesophageal
Case Control P-value reflux, oropharyngeal colonization of pathologic
bacteria and immunocompromised patients, and
Aspiration (%) 3 (20%) 4 (22%) 1.000 we could not compare the two groups relative to
Silent aspiration (%) 2 (66%) 2 (50%) 1.000 the presence of a tracheostomy.
Swallowed volume (%) 88.49/12.5 85.49/19.2 0.929
OTT (seconds) 0.379/0.07 0.839/0.10 B/0.001 The practical flaw in the method was the lack
PTT (seconds) 0.879/0.11 0.909/0.07 0.708 of use of a sham form of stimulation to investi-
OPTT (seconds) 1.249/0.18 1.739/0.16 B/0.001 gate whether a sham form of stimulation would
OPSE (%/s) 73.39/17.4 50.19/13.0 B/0.001 result in the same changes as the form of stimu-
lation used in this study. For example, tooth
Values are mean9/standard deviation.
OTT, oral transit time; PTT, pharyngeal transit time; OPTT, brushing could have been used as a sham form
oropharyngeal transit time; OPSE, oropharyngeal swallowing of stimulation to determine if this generalized
efficiency. oral stimulation would results in the same changes

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as those found with the stimulation used in this
study. Furthermore, the pre-emptive swallowing
stimulation used consisted of five interventions of
thermal
tactile stimulation: oral stimulation, oral
massage, digital manipulation and cervical range
of motion exercise. All five interventions were
performed on all subjects in the experimental
group so we are unable to determine whether
one, a combination, or all of these interventions
are needed to obtain the results.
Other limitations of this study included the
difficulty encountered in performing video-fluoro-
scopic swallow studies due to severity of illness, and
our inability to determine the baseline state of the
swallowing function of each patient prior to intuba-
tion. Although sedatives and neuromuscular block-
ers were withheld for 24 hours prior to video-
fluoroscopic swallow study, the possibility of re-
maining effects should be evaluated or ruled out.
In addition, no long-term follow-up of patients
was carried out in this study. Thus it is not possible
to determine with certainty whether the results are
representative of the general course of dysphagia in
long-term intubated patients.
We would like to propose that this study is a
positive trial that provides good information for
further, more advanced and extended research into
the clinical advantage and significance of pre-
emptive swallowing stimulation. Further research
should be carried out in consideration of and, if
possible, eliminating the limitations cited above.
In conclusion, objective parameters of dyspha-
gia, especially oral transit time were improved via
pre-emptive swallowing stimulation in long-term
intubated patients. Comprehensive swallowing
stimulation during long-term intubation may be
beneficial to the patient.
Acknowledgements
We thank Mrs Emily Holt from Australia for
editing.
Conflicts of interest
No commercial party having a direct financial
interest in the results of the research supporting
this article has or will confer a benefit upon the
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Pre-emptive swallowing stimulation 45
authors or upon any organization with which the
authors are associated.
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46 CH Hwang et al.

Appendix
Methods of pre-emptive swallowing stimulation

Thermal tactile stimulation
1) Chill laryngoscope
2) Open patient’s mouth wide and stroke the right side of the anterior palatal arch five times with the
laryngoscope
3) Similarly, stroke the left side of the anterior palatal arch five times with the laryngoscope.

Oral stimulation
1) Stimulate the tongue gently with a gauze or brush
2) Stroke the middle and both sides of the tongue
3) Stroke the roof of the oral cavity gently
4) Repeat for 1 minute.

Oral massage
1) After donning gloves, place the second finger into the oral cavity, with the thumb outside
2) Massage both lips with traction
3) Massage both cheeks similarly
4) Repeat for 1minute.

Digital manipulation
1) Place the thumb and second finger around the thyroid
2) Stroke the upper portion of hyoid bone to below the thyroid cartilage up and down forcefully
3) Repeat five times
4) Stroke the muscles around neck downward 10 times.

Cervical range of motion exercise

1) Flex the neck of the patient toward the chest and then extend the neck
2) Bend the neck of the patient to the right side until the patient’s ear is in contact with the shoulder
3) Repeat on the left side
4) Rotate the neck of the patient to fully to the right and then to the left
5) Open the patient’s mouth as wide as possible and massage the tympano-mandibular joints
6) Repeat this five times.

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