Dysphagia (2008) 23:302309
DOI 10.1007/s00455-007-9145-9
ORIGINAL ARTICLE
Neuromuscular Electrical Stimulation (NMES) in Stroke Patients
with Oral and Pharyngeal Dysfunction
Margareta Bulow Renee Speyer Laura Baijens
Virginie Woisard Olle Ekberg
Published online: 25 April 2008
Springer Science+Business Media, LLC 2008
Abstract Neuromuscular electrical stimulation (NMES)
technique is a dual-channel electrotherapy system designed
specifically for the treatment of pharyngeal dysfunction.
The purpose of this study was to evaluate and compare the
outcome of NMES versus traditional swallowing therapy
(TT) in stroke patients. Three European swallowing centers
participated in this randomized trial. Twenty-five patients
(16 men and 9 women) were included. Twelve patients
were randomized for NMES and 13 for TT. Mean age was
70 years for the NMES group and 71 years for the TT
group. Inclusion criteria were (1) patients 5080 years old
with cerebrovascular disease (stroke) for more than
3 months before the study, (2) only patients with hemi-
spheric stroke, (3) no brainstem involvement, (4) ability to
swallow, and (5) ability to communicate. Pre- and post-trial
measurements were videoradiographic swallowing evalu-
ation, nutritional status, oral motor function test, and a
visual analog scale (VAS) for self-evaluation of com-
plaints. All subjects received 15 therapy sessions.
Statistically significant positive therapy effects for both
NMES and TT combined were found, but there was no
statistically significant difference in therapy effect between
the groups. The correlations between measurements were
M. Bulow (&)
O. Ekberg
Diagnostic Centre of Imaging and Functional Medicine,
Malmo University Hospital, Malmo, Sweden
e-mail: margareta.bulow@med.lu.se
R. Speyer
L. Baijens
Audiology/ENT Department, University Hospital Maastricht,
Maastricht, The Netherlands
V. Woisard
Unite de la voix et de la deglutition, Service ORL,
Hopital Larrey, Toulouse, France
123
low. The patients subjective experience of improvement
had low correlation with the outcome from the objective
evaluation.
Keywords Neuromuscular electrical stimulation
(NMES)
Traditional swallowing therapy
Dysphagia

Oropharyngeal swallowing dysfunction
Stroke

Deglutition
Deglutition disorders
Oral, pharyngeal, and esophageal swallowing is a sequen-
tial event that transports saliva, ingested solids, and fluid
from the mouth to the stomach and protects the airways
during swallowing [1, 2]. Pharyngeal function involves
numerous interacting control mechanisms that ultimately
link pharyngeal contraction patterns to the adjacent oral
cavity and esophagus. From a functional point of view, the
pharynx can be divided into two parts: the muscle and
nerves. Contraction of swallowing muscles occurs as a
result of depolarization after acetylcholine release at the
endplates. However, contraction of muscles can also occur
after direct electrical stimulation. Neuromuscular electric
stimulation (NMES) is a special form of neuromuscular
stimulation used to re-educate patients to use their pha-
ryngeal muscles in the throat for patterned activity to
initiate or re-establish swallowing. NMES is a dual-channel
electrotherapy system designed specifically for the treat-
ment of pharyngeal dysfunction from any etiology. NMES
electrodes are placed at one or several sites on the throat
for stimulation of the underlying musculature. Prior studies
have shown the beneficial effect of NMES on the symp-
toms of dysphagia [3, 4]. Studies have also shown that oral
and pharyngeal stimulation may cause reorganization of
the human adult motor cortex [511]. However, no prior
M. Bulow et al.: NMES in Stroke Patients
study has addressed objectively how pharyngeal function is
affected by NMES.
The purpose of this study was to evaluate and compare
the outcome of NMES versus traditional swallowing ther-
apy (TT) in stroke patients using diverse measurements:
videoradiographic swallowing evaluation, nutritional sta-
tus, oral motor function test, and a visual analog scale
(VAS) for the patients subjective self-evaluation of
complaints.
Materials
Subjects
Three different European swallowing centers participated
in this randomized trial: Malmo University Hospital,
Malmo, Sweden (where the principal investigators are
located); University Hospital Maastricht, Maastricht,
Netherlands; and University Hospital Toulouse, Toulouse,
France. Twenty-five patients (16 men and 9 women) were
included in the trial. Twelve patients were randomized for
NMES and 13 for TT. Mean age was 70 years for the
NMES group and 71 years for the TT group. Four patients
in the NMES group were on tube feeding and 7 patients in
the TT group.
Inclusion criteria for the trial were as follows: (1) patients
had to be 5080 years old and had cerebrovascular disease
(stroke) more than 3 months prior to the study. (2) Patients
with hemispheric stroke and without neurologic signs typical
for brainstem involvement. (3) Patients could not have
nasogastric tubes but could have PEG. (4) Patients had to be
able to elicit some pharyngeal swallow as revealed during
videoradiographic swallowing evaluation and seen as ante-
rior movement of the hyoid bone and constrictor activity in
the pharyngeal wall. (5) They had to be able to communicate.
Computed tomography (CT) or magnetic resonance (MR)
findings were not used for inclusion or exclusion. A MR
examination was not done. The disease process should have
been stable. The stroke could have been a first-time stroke or
a recurrence. Patients could be on a modified diet and may
practice swallowing maneuvers.
Exclusion criteria for the trial were as follows: (1)
patients with progressive cerebrovascular disease; (2)
patients with other neurologic diseases such as ALS, MS,
or Parkinsons disease; (3) patients with tumors or neo-
plastic disease of the swallowing apparatus and who had
undergone radiotherapy to the neck; (4) patients who had
undergone surgery to the swallowing apparatus; (5)
patients who were not able to elicit pharyngeal swallow (as
described above); (6) patients with a nasogastric tube.
The trial was approved by the ethical committees in
Sweden, the Netherlands, and France.
303
Methods
Randomization
A randomization table was designed and used as an online
randomization tool, assigning patients to treatment A or B
with a chance of 50% to be assigned to either treatment.
This table was used in the online database for the trial in
which each patient had a preassigned treatment number
that appeared once the eligibility criteria were checked and
basic patient information was entered.
Evaluation Measurements
Pre- and Post-treatment Evaluation
Clinical evaluation A qualitative clinical swallowing
assessment was performed and included a visual analog
scale (VAS) for the patients subjective self-evaluation of
complaints (see below), actual nutrition status (Table 1),
and oral motor status (Table 2). Also, a quantitative mea-
surement was used, namely, videoradiographic swallowing
evaluation (Table 3). The post-treatment evaluation should
be performed the same day after the last treatment.
Visual analog scale (VAS) The VAS was used to compare
differences between pre- and post-treatment. The number of
points before and after treatment was also compared; 0
points = no difficulties at all and 10 points = maximum/
unable to swallow. A comparison was made between the
patients subjective feeling (i.e., the VAS) and the objective
pharyngeal function (videoradiography). A comparison was
also made with the clinical evaluation.
Radiologic Evaluation: Videofluoroscopy
Endpoints The radiologic evaluation/examination was
documented on video or in a digital modality. The frame
Table 1 Scores for Actual Nutrition Status (ANS)
Score Activity limitation
0 Full oral, no limitations
1 Full oral, with compensation
2 Full oral, with consistency restriction
3 Full oral, with compensation and consistency restriction
4 Partial oral
5 Partial oral, with compensation
6 Tube feeding
123
304 M. Bulow et al.: NMES in Stroke Patients

Table 2 Oral motor function test (OMFT) suspension. Thickened liquid was prepared according to
1. Open and close the mouth.
the following recipe: 110 g Fortifresh (Nutricia) raspberry.
2. Blow up the cheeks with the mouth closed. Then press a finger
Add 40 g barium powder. Mix well. Then add 4 g Thicken
against the left cheek and the right cheek a couple of times, Up (Resource, Novartis Consumer Health UK, Ltd). Mix it
while keeping the mouth closed. (No air may leak out of the well. Use at room temperature within 10 min.
mouth.) The patient was given 5-ml boluses. The patient per-
3. Stretch the tongue out of the mouth as far as possible. formed five swallows of 5 ml thin liquid and five swallows
4. Open your mouth and move the tongue as far as possible to the of 5 ml thick liquid. Three swallows were also performed
right.
in an AP view (thin liquid).
5. Open your mouth and move the tongue as far as possible to the
To measure distances, a coin (5 eurocent) with a known
left.
diameter was placed in the midline of the anterior neck
6. With the tip of the tongue, push out left cheek and press a finger
against the tongue. when the patient was imaged in lateral projection. This
7. With the tip of the tongue, push out right cheek and press a finger coin was included in the X-ray field. The assessment
against the tongue. (If there is normal tongue strength, it should focused on (1) dissociation between oral and pharyngeal
be possible to resist finger pressure.) stage, (2) misdirected swallowing, (3) pharyngeal reten-
The test should be evaluated according to the scale below. tion, and (4) width of PES (Table 3).
0 Normal Dissociation between oral and pharyngeal stage was
1 Mild dysfunction measured as the start of the anterior movement of the hyoid
2 Moderate dysfunction bone. This correlated with the position of the apex of the
3 Severe dysfunction bolus. In normal patients the apex of the bolus should not
4 Impossible to perform the exercise pass beyond the faucial isthmus by more than 0.5 s before
the hyoid starts to move anteriorly. This timing was given
in milliseconds (Table 3). Leakage was also registered.
Table 3 Scores for Videofluoroscopic Examination Misdirected swallowing was classified as either barium
Videofluoroscopic examination Scoringb reaching into the laryngeal vestibule or beyond the vocal
folds into the trachea (Table 3).
Dissociation 0 = \0.5 s Retention was classified as either minor or major. In the
1 = 0.51.0 s AP or the lateral view, the height of the air fluid level was
2 = 1.02.0 s measured and compared with the 5-eurocent coin (Table 3).
3 = [2.0 s The maximum width of the PES was measured in either
Misdirected swallowa 0 = normal swallow the AP or the lateral view (Table 3).
1 = into the laryngeal vestibule The radiologist was blinded for whether the videora-
but not into the trachea
diographic examination was performed before or after
3 = into the trachea
treatment.
Retention (fluid level) 0 = \6 mm
1 = 710 mm
2 = 11 mm Intervention-Procedure
PES width (maximal width of the 3 = \5 mm
PE segment in AP or lateral 1 = 510 mm
projection)
NMES and TT were administered by a speech-language
0 = [10 mm pathologist trained in dysphagia management. The SLPs
a
In Malmo a more detailed scale is used and therefore two points are involved in this study have all attended the VitalStim
missing. The scaling/scoring is arbitrary and reflects only the inves- Certification Program and completed all requirements for
tigators appreciation of the weight of each dysfunction certification as a VitalStimTM Therapy Provider [12].
b
In lateral and anterior projection (AP), respectively, ten and three The patients were randomized for either NMES or the
swallows are registered. The AP swallows are scored only on reten-
tion and PES width (if applicable)
control group (TT). Patients referred to the NMES (Vital-
Stim) group were given the following treatment: (1)
rate (or equivalent) was 25 frames/s or more. Radiologic Placement 3 B; two sets of electrodes were used and
evaluation was done within one week before entering the located on each side of the midline of the throat. Two
study. The examination covered the oral cavity, including electrodes were placed just at or above the level of the
tongue, pharynx, and pharyngoesophageal segment (PES). thyroid notch over the thyrohyoid muscle. The typical level
Patients were examined while they were in a sitting posi- ranged from 4.5 to 25 mA with a mean level of around
tion and thin and thickened liquids were used. The 13 mA. (2) One 60-min session every day. (3) Patients
following recipe was used: Thin liquids: 40% w/v barium were treated 5 days a week over 3 weeks, i.e., 15 treatment

123
M. Bulow et al.: NMES in Stroke Patients 305

Table 4 Visual analog scale (VAS), comparisons pre- and post- Mann-Whitney test for each parameter of the videoradi-
treatment ography of swallowing, the Actual Nutrition Scale (ANS),
VAS Pretreatment Post pretreatment pa and the total score of the Oral Motor Function Test
(OMFT). The data of the VAS scale were sufficiently
Median 25th; 75th N Median 25th; 75th N
normally distributed to allow an independent-samples t
NMES 7.4 4.8; 9.5 12 -2.9 -4.8; 12 0.40 test. Differences in effect data between the NMES group
-1.7 (ns) and the TT group were tested for significance by a Wil-
TT 5.7 4.0; 8.2 13 -2.5 -3.6; 12 coxon signed rank test, except for the VAS scale for which
-1.2
data distribution allowed the use of a paired-samples t test.
NMES 6.5 4.6; 8.6 25 -2.6 -4.1; 24 0.000
The relationship between the baseline data and the therapy
and TT -1.6
effects on all evaluation tools was studied by nonpara-
ns = not significant; TT = traditional therapy metric Spearmans correlation coefficients. A Bonferroni
Descriptive statistics of baseline data and effect data (difference correction has been applied (p \ 0.05/18). All computa-
between post-therapy minus pretherapy data). The maximum score of
tions were performed using SPSS v12.0.1 (SPSS Inc.,
the scale is 10
a Chicago, IL).
Level of significance (p) of the difference in effect data between
both groups (independent-samples t test) and of the difference
between post-therapy data compared to baseline data for both groups
combined (paired-samples t test). A Bonferroni correction has been Results
applied (p \ 0.05/18)

sessions. (4) NMES patients could have their diets modi-
fied if they were modified when the patient was included in
the study. (5) Only spontaneous maneuvers were allowed.
No other maneuvers or treatments were added or included.
(6) The SLP instructed the patient to swallow hard and fast.
The control group (TT) underwent the following: (1)
Diet modification if applicable. (2) A clinician determined
appropriate maneuvers or other treatment techniques. (3)
Analogous to the NMES group, they were treated for
60 min 5 days a week over 3 weeks, i.e., 15 sessions. If the
patient could not participate for 60 min, he/she was told to
do a training session on his/her own at home. (4) They
received exercise sheets for the specific exercises that they
had to perform, equal for all participating clinics.
Statistical Analyses
Combined group differences between post-therapy and
baseline data (effect data) were tested for significance by a
Effects of Therapy
Visual Analog Scale (VAS)
Table 4 presents the median and the 25th and 75th per-
centiles of the patients self-evaluation of dysphagia. Using
a paired-samples t test, statistically significant therapy
effects were found for the total group of patients. No sta-
tistically significant differences were found between
NMES and TT (independent-samples t test).
Actual Nutrition Scale (ANS)
Table 5 contains descriptive statistics of the pretherapy
data and the effect data for the ANS. A Wiloxon signed
rank test was used to test for significant changes between
baseline and post-therapy data. When combining both
groups, a statistically significant group change after therapy
could be demonstrated. No statistically significant

Table 5 Actual nutrition scale (ANS), comparisons pre- and post-treatment

ANS Pretreatment Post minus pretreatment pa
Median 25th; 75th N Median 25th; 75th N

NMES 2.5 0.5; 5.8 12 -1.0 -2.0; 0 12 0.189 (ns)

TT 3.0 0; 5,0 13 0 -1.0; 0 13
NMES and TT 3.0 0; 5.0 25 0 -1.0; 0 25 0.002
ns = not significant; TT = traditional therapy
Descriptive statistics of baseline data and effect data (difference between post-therapy minus pretherapy data). The maximum score of the scale is
6
a
Level of significance (p) of the difference in effect data between both groups (Mann-Whitney Test) and of the difference between post-therapy
data compared to baseline data for both groups combined (Wilcoxon signed rank test). A Bonferroni correction has been applied (p \ 0.05/18)

123
306 M. Bulow et al.: NMES in Stroke Patients

differences were found between NMES and TT (Mann- tools, no statistically significant therapy effects are found
Whitney test). for any of the variables of videoradiography. In particular,
the width of the PES and the amount of retention were
unchanged. No statistically significant differences were
Oral Motor Function Test (OMFT) found between NMES and TT (Mann-Whitney test).

Table 6 shows descriptive baseline and effect data for each

item. The results of a Wilcoxon signed rank test indicate
that positive significant therapy effects are present for the
total score of the OMFT. No statistically significant dif-
ferences were found between NMES and TT (Mann-
Whitney test).
Videoradiographic Evaluation of Swallowing
Table 7 shows the results of Wilcoxon signed rank tests per
variable. In contrast to the results of the other evaluation
Relationship Among Evaluation Tools
The relationship among the evaluation parameters was
studied by nonparametric Spearmans correlation coeffi-
cients (Table 8). The correlations between the baseline
data were low. The mean correlation was -0.06
(range = -0.30 \ R \ 0.16). The correlations between
the effect data were low also, except for the correlation
between the effect data of the total score of the videora-
diography and the patients self-evaluation (R = 0.72).
The mean correlation of the effect data was 0.10

Table 6 Oral motor function test (OMFT), comparisons pre- and post-treatment
OMFT Pretreatment Post minus pretreatment pa
Item Group Median 25th; 75th N Median 25th; 75th N

1 NMES 0 0; 1 10 0 -1; 0 10
TT 0 0; 0 12 0 0; 0 12
NMES and TT 0 0; 0.25 22 0 0; 0 22
2 NMES 1 0; 2 10 -0.5 -1; 0 10
TT 1 0; 1.75 12 0 -1; 0 12
NMES and TT 1 0; 2 22 0 0; 0 22
3 NMES 0.5 0; 1 10 -0.5 -1; 0 10
TT 1 0; 1 12 0 -1; 0 12
NMES and TT 1 0; 1 22 0 0; 0 22
4 NMES 0.5 0; 1 10 -0.5 -1; 0.25 10
TT 1 0; 1.75 12 0 -1; 0 12
NMES and TT 1 0; 1 22 0 0; 0 22
5 NMES 0 0; 1 10 0 -1; 0 10
TT 1 0; 1.75 12 0 -1; 0 12
NMES and TT 1 0; 1 22 0 0; 0 22
6 NMES 1.5 0.75; 2.25 10 0 -1.25; 0 10
TT 2 0; 3.5 12 0 -1; 0 12
NMES and TT 2 0; 2.25 22 0 0; 0 22
7 NMES 1.5 0; 2.25 10 0 -1; 0 10
TT 2 0.25; 3.75 12 0 -1; 0 12
NMES and TT 2 0; 3 22 0 0; 0 22
Total NMES 6.5 2.25; 7.75 10 -2 -7; 0 10 0.506 (ns)
TT 8 2.25; 10.5 12 -2 -5; 0.75 12
NMES and TT 7 2.75; 9.25 22 -2 -5.25; 0 22 0.014
ns = not significant; TT = traditional therapy
Descriptive statistics of baseline data and effect data (difference between post-therapy minus pretherapy data). The maximum score per item is 4
and the maximum total score is 28
Level of significance (p) of the difference in effect data between both groups (Mann-Whitney Test) and of the difference between post-therapy
data compared to baseline data for both groups combined (Wilcoxon signed rank test). A Bonferroni correction has been applied (p \ 0.05/18)

123
M. Bulow et al.: NMES in Stroke Patients 307

Table 7 Videofluoroscopy (VFS), comparisons pre- and post-treatment

Videoradiography Pretreatment Post minus pretreatment pa
Item Group Median 25th; 75th N Median 25th; 75th N

1 Dissociation NMES 12 0; 24.5 12 0 -6; 0.75 12 0.528 (ns)

TT 4 0; 22 13 0 0; 0 11
NMES and TT 10 0; 22 25 0 -1; 0 23 0.824 (ns)
2 Misdirection NMES 4.5 1.5; 10.25 12 -0.5 -2; 0.75 12 0.900 (ns)
TT 6 1.5; 11.5 13 0 -3; 0 11
NMES and TT 6 2; 10 25 0 -2; 1 23 0.212 (ns)
3 Retention NMES 0 0; 7.25 12 0 0; 0 12 0.051 (ns)
TT 0 0; 0 13 0 0; 0 11
NMES and TT 0 0; 1.5 25 0 0; 0 23 1.000 (ns)
4 PES width NMES 0 0; 0 12 Constant = 0 12 1.000 (ns)
TT Constant = 0 13 Constant = 0 11
NMES and TT 0 0; 0 25 Constant = 0 23 1.000 (ns)
5 Total NMES 25 1.5; 36.5 12 0 -8.75; 3 12 0.514 (ns)
TT 6 4.5; 37 13 0 -2; 5 11
NMES and TT 13 4; 37 25 0 -3; 3 23 0.722 (ns)
ns = not significant; TT = traditional therapy
Descriptive statistics of baseline data and effect data (difference between post-therapy minus pretherapy data). Minimum and maximum scores
are presented in Table 3
a
Level of significance (p) of the difference in effect data between both groups (Mann-Whitney test) and of the difference between post-therapy
data compared to baseline data for both groups combined (Wilcoxon signed rank test)

Table 8 Correlation between measurement instruments further research is needed [13]. The goal of this random-
ANS VAS OMFT total VFS Total ized trial was to compare differences in outcome between
ANS -0.07 (25) 0.05 (23)
a
0.72 (25) NMES (VitalStimTM) and traditional swallowing therapy,
VAS -0.13 (24) 0.02 (23) -0.12 (25)
OMFT total 0.14 (22) -0.12 (22) 0.02 (23)
and also to compare differences between oral and pha-
VFS Total -0.08 (23) -0.30 (23) 0.16 (21) ryngeal function and the patients symptoms. Our results
show that there were no differences in outcome between
Nonparametric Spearmans correlation coefficients. Pretreatment
data compared between instruments: association between measure- NMES and TT, which is in accordance with another newly
ment instruments. Post minus pretreatment data (= effect data) published study on this topic [14]. Ludlow et al. [15]
compared between instruments: association between effect scores concluded that surface electrical stimulation in some dys-
(therapy effects) phagic patients could interfere with hyolaryngeal elevation
The entries in the white background refer to correlations between which is required for airway protection during swallowing.
baseline data. The values in the gray background refer to correla-
tions between effect scores (post-therapy minus pretherapy data). Shaw et al. [16] found that VitalStim therapy helped
The numbers of patients are in parentheses patients with mild to moderate dysphagia. Therefore, they
a
Correlation is significant at the 0.01 level (2-tailed) concluded that VitalStim therapy has a place in the man-
agement of dysphagia but that the most severely injured
patients did not improve. Referring to Logemann [17]:
(range = -0.12 \ R \ 0.72). These poor correlations We still need much more research to determine whether
between the baseline data and between the effect data VitalStim or other methods of neuromuscular electrical
imply that the outcome of the diverse evaluation tools stimulation have any role to play in the management of
represents independent aspects of swallowing. oro-pharyngeal swallowing difficulties.

Discussion Subjects

Neuromuscular electrical stimulation (NMES) is widely The experiences from all three centers involved in this
used in the United States but not known in Europe until study revealed great difficulties in identifying patients who
lately. The scientific evidence of its efficacy is unclear and met the inclusion criteria. Several potential subjects had a

123
308
spontaneous recovery within the inclusion time of
3 months or were so severely injured that it was impossible
for them to participate in the trial. Some of them could not
initiate a pharyngeal swallow. Therefore, we had to close
the study after 2 years.
One of the inclusion criteria was hemispheric stroke,
while patients with brainstem lesions were excluded. The
rationale for this was that the NMES is supposed to stim-
ulate efferent nerves in the neck. In patients with brainstem
lesions, the lower motor neuron is supposed to be non-
functioning or degenerated. Therefore, we assumed that
this type of patient would not be suitable for NMES.
The patients for this trial were not stratified by hemi-
spheric lesions, severity of CVA, or time post-onset. The
participants were specifically not identified by lesion or
severity of CVA because this was a preliminary study with
small numbers. To stratify by lesion or isolate just one
particular type of lesion would have lengthened participant
enrolment past what was of interest for this study. Larger,
more controlled studies have to stratify their participants
according to these variables. Future studies may also
stratify individuals with CVA by lesion location, time post-
onset, and severity to determine the effectiveness of NMES
as a function of CVA-related variables as well.
Evaluation Measurements
VAS
The outcome from the VAS showed that baseline data of the
NMES group were more severe than those of the TT group. It
must be considered an accident that the subjects in the NMES
group seemed to be more severely impaired by their swal-
lowing disorders than the subjects in the TT group.
Actual Nutrition
When combining both groups, statistically significant
group changes in actual nutrition status after therapy were
demonstrated. Also, an improvement in nutrition for both
groups combined was found. We may conclude that
swallowing treatment will improve the awareness of how
to eat and drink. From earlier studies we have learned that
the traditional swallowing techniques and diet modification
could decrease misdirected swallowing to the trachea and
pharyngeal retention [18].
Oral Motor Function
Positive significant therapy effects were present for the
total score of the OMFT. Oral motor range-of-motion
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M. Bulow et al.: NMES in Stroke Patients
exercises in some cases are an option for dysphagic
patients [19], and in this study the individually recom-
mended oral motor exercises seem to have improved the
actual swallowing dysfunction.
Videofluoroscopy
In contrast to the results of the other evaluation tools, no
statistically significant therapy effects were found for any
of the variables of videoradiography. In particular, the
width of the PES and the amount of retention were rather
unchanging variables in this study. However, clinically we
often experience obvious differences in follow-up patients.
Based on the literature, videoradiography is considered to
be the most objective and reliable measurement in the
evaluation of swallowing [20]. Perhaps when using larger
numbers of subjects or defining parameters used for the
evaluation of videoradiography that are robust and more
sensitive to changes resulting from therapy, statistically
significant therapy effects might be found in future studies.
Correlation Between Measurement Instruments
Statistically significant positive therapy effects for both
groups (NMES and TT) combined were found but there
was no statistically significant difference in therapy effect
between the groups. The correlations between the different
measurements were low. Therefore, the patients subjective
experience of improvement did not correlate with the
objective videoradiography. A false-positive experience of
improvement may lead to serious swallowing complica-
tions such as choking attacks. At least two of the patients
included in this study (randomized for NMES) were a
couple of months after they had completed the trial treated
for severe aspiration pneumonia. Because they had a very
positive post-treatment VAS score and felt that they had
recovered from their swallowing difficulties, they did not
follow the recommendations regarding diet modification.
Elmstahl et al. [21] concluded that assessment of sub-
jective swallowing complaints is not sufficient to evaluate
the clinical course. A quality of life measurement such as
SWAL-QOL would probably have been a better tool to
estimate how the patients experienced quality of life after
swallowing treatment.
Conclusion
In this study no statistically significant differences were
found in therapy effect between the NMES group and the
TT group. The correlations between the different
M. Bulow et al.: NMES in Stroke Patients
measurements were low. The subjective improvement
(VAS) experienced by several patients did not correlate
with the objective videoradiographic outcome. We still
need to know more before we can claim that NMES is
valuable as a treatment option for dysphagic patients.
Acknowledgments The authors thank Corina van As and Stella
Ramette, Atos Medical Sweden, for their assistance in this study.
References
1. Martin RE, Sessle BJ. The role of the cerebral cortex in swal-
lowing. Dysphagia 1993;8:195202.
2. Miller AJ. Deglutition. Physiol Rev 1982;62:129184.
3. Park CL, ONeill PA, Martin DF. A pilot exploratory study of
oral electrical stimulation on swallow function following stroke:
an innovative technique. Dysphagia 1997;12:161166.
4. Leelamanit V, Limsakul C, Geater A. Synchronized electrical
stimulation in treating pharyngeal dysphagia. Laryngoscope
2002;112:22042210.
5. Hamdy S, Jilani S, Price V, Parker C, Hall N, Power M. Mod-
ulation of human swallowing behaviour by thermal and chemical
stimulation in health and after brain injury. Neurogastroenterol
Motil 2003;15:6977.
6. Hamdy S, Rothwell JC, Aziz Q, Thompson DG. Organization and
reorganization of human swallowing motor cortex: implications
for recovery after stroke. Clin Sci 2000;99:151157.
7. Fraser C, Power M, Hamdy S, Rothwell J, Hobday D, Hollander
I, Tyrell P, Hobson A, Williams S, Thompson D. Driving plas-
ticity in human adult motor cortex is associated with improved
motor function after brain injury. Neuron 2002;34:831840.
8. Hamdy S, Rothwell JC, Fraser C, Power M, Gow D, Thompson
DG. Patterns of excitability in human oesophageal sensorimotor
cortex to painful and nonpainful visceral stimulation. Am J
Physiol Gastrointest Liver Physiol 2002;282:G332G337.
9. Fraser C, Rothwell J, Power M, Hobson A, Thompson D, Hamdy
S. Differential changes in human pharyngoesophageal motor
excitability induced by swallowing, pharyngeal stimulation, and
anaesthesia. Am J Physiol Gastrointest Liver Physiol
2003;285:G137G144.
10. Ertekin C, Turman B, Tarlaci S, Celik M, Aydogdu I, Secil Y,
Kiylioglu N. Cricopharyngeal sphincter muscle responses to
transcranial magnetic stimulation in normal subjects and in
patients with dysphagia. Clin Neurophysiol 2001;112:8694.
309
11. Mattioli S, Lugaresi M, Zannoli R, Brusori S, dOvidio F,
Braccaioli L. Pharyngoesophageal manometry with an original
balloon sensor probe for the study of oropharyngeal dysphagia.
Dysphagia 2003;18:242248.
12. Freed M, Wijting Y. VitalStim Certification Program. Training
manual for patient assessment, treatment using VitalStim elec-
trical stimulation. Hixson TN: Chattanooga Group; 2003.
13. Suiter DM, Leder SB, Ruark JL. Effects of neuromuscular elec-
trical stimulation on submental muscle activity. Dysphagia
2006;21:5660.
14. Kiger M, Brown CS, Watkins L. Dysphagia management: An
analysis of patient outcomes using VitalStimTM therapy com-
pared to traditional swallow therapy. Dysphagia 2006;21:243
253.
15. Ludlow CL, Humbert I, Saxon K, Poletto C, Sonies B, Crujido L.
Effects of surface electrical stimulation both at rest and during
swallowing in chronic pharyngeal dysphagia. Dysphagia
2007;22:110.
16. Shaw GY, Sechtem PR, Searl J, Keller K, Rawi TA, Dowdy E.
Transcutaneous neuromuscular electrical stimulation (VitalStim)
curative therapy for severe dysphagia: myth or reality? Ann Otol
Rhinol Laryngol 2007;116:3644.
17. Logemann JA. The effects of VitalStim on clinical and research
thinking in dysphagia. Dysphagia 2007;22:1112.
18. Bulow M. Therapeutic aspects of oral and pharyngeal swallowing
dysfunction. Videoradiographic and videomanometric analyses of
adult healthy volunteers and dysphagic patients. Thesis, Faculty
of Medicine, Lund University, 2003.
19. Gerek M, Ciyiltepe M. The management of swallowing disorders
through rehabilitation methods. Kulak Burun Bogaz Ithis Derg
2005;14:1017.
20. Zammit-Maempel I, Chapple C-L, Leslie P. Radiation dose in
videofluoroscopic swallow studies. Dysphagia 2007;22:1315.
21. Elmstahl S, Bulow M, Ekberg O, Pettersson M, Tegner H.
Treatment of dysphagia improves nutritional conditions in stroke
patients. Dysphagia 1999;14:6166.
Margareta Bulow SLP, PhD
Renee Speyer SLP, PhD
Laura Baijens MD
Virginie Woisard MD, PhD
Olle Ekberg MD, PhD
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