Abstract
Intramuscular
stimulation can aid laryngeal elevation and could augment airway protection in
dysphagia. Swallowing is complex , involving multiple
sensory and motor events prior to the
pharyngeal phase, making automatic triggering
difficult. Our purpose was to determine if patients with severe dysphagia could
improve airway protection during swallowing after training to coordinate
swallowing onset during the pharyngeal phase with intramuscular stimulation.
Comparisons were made between: a) airway protection during baseline swallowing without
intramuscular stimulation before training versus swallowing coordinated with
stimulation after training; b) airway protection during swallow without
intramuscular stimulation before versus after training; and c) airway
protection with and without stimulation after training. Percutaneous hooked
wire electrodes were inserted into submental and extrinsic laryngeal muscles
and stimulation onset was controlled by a button press. The resulting swallows were
recorded during videofluorography. The degree of airway protection was scored
by judges blinded to condition and patient identity. Significant improvements in swallowing
performance occurred between baseline pre-training to post-training with
stimulation (p=.002 ) and between post-training sham and stimulated swallows
(p=.045). By training patients to coordinate intramuscular stimulation with
swallowing, they can improve their airway protection with intramuscular
stimulation, and may also augment their volitional swallowing control through
practice.
1.
INTRODUCTION
Previous muscle
stimulation approaches during swallowing have either used continuous
stimulation for prolonged periods during swallowing training, which can lead to muscle fatigue [1], or have attempted to use
surface electromyography (EMG) of the submental muscles to detect activity [2]. Submental EMG signals,
however, are often confounded by chewing activity that takes place during the
oral phase of swallowing. We have
previously demonstrated in normal volunteers that intramuscular stimulation can
provide elevation of the hyo-laryngeal complex [3], and that normal volunteers
can easily learn to accurately synchronize a button press to trigger
intramuscular stimulation coincident with the onset of the pharyngeal phase of
swallowing [4].
Severe pharyngeal
dysphagia reflects problems with volitional control of swallowing. Often aspiration (the entry of a bolus into
the trachea) occurs because of either a delay in the initiation of the
pharyngeal phase of swallowing, reduced elevation of the hyolaryngeal complex
to provide airway protection, or incomplete clearance of the bolus from the
pharynx. Our aim is to improve a
patient’s volitional control of the onset of the pharyngeal phase of swallowing
and augment hyolaryngeal elevation by training patients to press a button to
trigger intramuscular stimulation during the pharyngeal phase of swallowing.
This study tested the following hypotheses:
a) airway protection would improve with intramuscular stimulation during
swallowing following training; b) swallowing training would improve a patient's
airway protection during swallowing without stimulation; and, c) airway protection
would be improved during stimulated swallows over sham stimulation swallows
post training.
2.
METHODS
2.1.
Subjects
Ten patients with severe chronic dysphagia
who were unable to feed orally were selected for a feasibility study of the
effects of intramuscular stimulation on airway penetration and aspiration
during swallowing. Prior to
participation in the study, the patients underwent testing to determine if they
could press a button or signal the time of onset of the pharyngeal phase while
attempting to swallow a small (2-3 ml) amount of water from a syringe.
2.2. Experimental Methods
During the study, hooked wire electrodes
were inserted into submental and extrinsic laryngeal muscles (mylohyoid,
geniohyoid, hyoglossus and thyrohyoid).
The accuracy of the location of the electrodes was verified by observing
the movement induced during monopolar electrical stimulation 3-7 mA at 30 Hz
using 200 µs biphasic pulses for 4 s.
Videofluorographic images during stimulation at rest determined which
combination of muscle stimulation was most effective for inducing hyolaryngeal
elevation without swallowing.
A bolus of 3-10 ml of liquid barium was
administered to obtain a sample of swallowing without any training or
intramuscular stimulation. Following this,
the patient underwent five (5) trials of training to coordinate their onset of
the pharyngeal phase of swallowing with stimulation onset. The patient attempted to swallow 3 ml of
water at the same time as stimulation.
After training, videoflourography was used to record trials of
intramuscular stimulation (stimulated trials) randomly ordered with trials
without stimulation (sham trials) while swallowing 3-10 mls of liquid barium.
2.3. Data Analyses
Four speech pathologists used a scoring
system to measure the number of occurrences of aspiration of liquid passing
through the vocal folds into the trachea, and whether there was pooling in the
vallecula, penetration of liquid into the laryngeal vestibule either from the
oral or hypo-pharynx, pooling in the pyriform sinuses and entry of food through
the upper esophageal sphincter on each trial.
All scoring was done with the speech pathologists blinded to subject
identity and condition (baseline, stimulated or sham trials before and after
training). A total score was derived to represent risk of aspiration during
swallowing for each trial; a lower score represented less risk of aspiration.
A Mean Total Score was derived for each
patient for pre-training baseline swallows, and post-training stimulation and sham
trials. Repeated ANOVAs tested each directional hypothesis: 1) that a reduction
occurred in the Total Score between baseline and post training stimulation; 2)
that a reduction occurred in the Total Score between baseline pre-training and
post-training sham trials, and that 3) a reduction occurred between stimulated
and sham swallows post training.
3.
RESULTS
3.1. Pre-Experimental
Training
All of the patients with chronic pharyngeal dysphagia
were able to meet the pre-experimental criterion of accurately synchronizing a
button press with their attempts to initiate the pharyngeal phase of swallowing
on at least 5 consecutive trials and had an 80% overall accuracy during 20
training trials.
3.2. Comparison of Baseline
Non-stimulation Pre-training with Post-training Stimulation.
The repeated ANOVA demonstrated a significant
reduction in Total Score between pre-training baseline and post training
stimulation swallows (F=11.36; df=1,9, p=0.002). The Total Score was reduced in
all but one of the ten patients; only the least affected patient did not reduce
his risk of aspiration during swallowing on his Total Score (Figure 1).
Figure 1. Individual patient pre-training baseline
Total Score representing degree of risk of aspiration during swallowing and
post-training Total Score during coordination of intramuscular stimulation with
swallowing.
3.2. Comparison of
Pre-training Baseline Non-stimulated Swallowing with Post-training Swallowing
with Sham Stimulation.
Repeated ANOVAs between baseline pre-training and post-training
sham trials were available for comparison in 8 patients and were not
statistically significant (F=1.783, df=1,7, p=0.112) but showed modest
improvement in 5 patients. (Figure 2).
Figure 2. Individual
patient pre-training baseline Total Score representing degree of risk of
aspiration during swallowing and post-training Total Score during coordinating
swallowing without intramuscular stimulation.
3.3.
Comparison of Post-training Swallowing with and without Stimulation
When post-training sham and stimulated
swallows were compared, a significant reduction in aspiration risk was found
with stimulation (F=3.718, df=1,8, p=.045).
4.
DISCUSSION AND CONCLUSIONS
Although these results are preliminary,
they indicate that training patients to coordinate intramuscular stimulation
with their own swallowing provides improved airway protection during swallowing
in severe chronic dysphagia. Each of
these patients had previously undergone extensive therapy for dysphagia
immediately following the onset of their dysphagia (post stroke, in Parkinson
disease, traumatic brain injury or following surgery for a brain tumour). In spite of early intervention, each patient
had remained at significant risk of aspiration six months post onset and had
continued to require enteric feeding.
Most could not handle their own saliva and some required suctioning for
saliva control. The improvement in airway protection with intramuscular
stimulation in comparison with baseline swallowing was encouraging in all but
the mildest patient improved. What was unexpected was the modest improvement in
swallowing without stimulation post training in comparison with measures of
baseline swallow. This suggested that
with five training trials to improve the coordination between stimulation and
the patients’ attempts at volitional control of the pharyngeal phase of
swallowing, some degree of therapeutic benefit may have occurred besides the
augmentation of hyolaryngeal movement improvement by intramuscular stimulation
in persons with chronic pharyngeal dysphagia.
These patients have brain injury that may
either disrupt the central pattern generator for swallowing in the medulla or
produce a disconnection between cortically based volitional control of
swallowing and their swallowing pattern generator in the medulla. These
preliminary results suggest that by training a patient to coordinate their own
swallowing with intramuscular stimulation, their central volitional control
might also be improved.
Because many patients have expressed a desire
for control over their own movement in spite of their difficulties, provision
of a patient controlled device to onset electrical stimulation for movement may
serve to both augment airway protection and improve volitional control of
swallowing.
References
1. Freed ML, Freed L, Chatburn RL, et al. Electrical stimulation for swallowing disorders caused by stroke. Respir Care, 46: 466-474, 2001.
2. Leelamanit V, Limsakul C and Geater A. Synchronized electrical stimulation in treating pharyngeal dysphagia. Laryngoscope, 112: 2204-2210, 2002.
3. Burnett TA, Mann EA, Cornell SA, et al. Laryngeal elevation achieved by neuromuscular stimulation at rest. J Appl Physiol, 94: 128-134, 2003.
4. Burnett TA, Mann EA, Stoklosa JB, et al. Self-triggered functional electrical stimulation during swallowing. under review.
Acknowledgements
The research was supported by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health, project number Z01 NS 02980.