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1Laryngeal and Speech Section, National Institutes of Neurological Disorders and Stroke, Bethesda, Maryland; 2Department of Communication Sciences and Disorders, Howard University, Washington, District of Columbia; 3Office of the Clinical Director, National Institutes of Neurological Disorders and Stroke, Bethesda, Maryland; and 4Department of Rehabilitation of the Clinical Center, National Institutes of Health, Bethesda, Maryland
Submitted 23 March 2006 ; accepted in final form 18 July 2006
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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0.01) reductions in both the larynx and hyoid bone peak elevation occurred during stimulated swallows. The stimulated swallows were also judged less safe than nonstimulated swallows using the National Institutes of Health-Swallowing Safety Scale (P = 0.0275). Because surface electrical stimulation reduced hyolaryngeal elevation during swallowing in normal volunteers, our findings suggest that surface electrical stimulation will reduce elevation during swallowing therapy for dysphagia. dysphagia; videofluoroscopy; neuromuscular stimulation; neck muscles
50% of normal laryngeal elevation when applied in normal volunteers at rest (4). In the last 5 years, surface electrical stimulation has been gaining attention as an aid for treatment of dysphagia (7, 10) and is now used by therapists during treatment of dysphagia. The surface electrodes are placed on the neck using one of four different placements provided by the developers of this technique (18). When applied, the current intensity level is increased until the patient reports the sensation of "muscles grabbing," referred to as "motor" levels of stimulation. The stimulator then remains on, cycling off for 1 s every minute throughout 1 h of therapy while the patient is encouraged to repeatedly "swallow hard," beginning with his or her own saliva. Over time, the patient is progressively moved from swallowing saliva to ice chips and later to solids. The developers of this device claim that "most patients should demonstrate increased laryngeal elevation with stimulation during the first session" (18). If these claims are correct, then surface stimulation might be preferred to intramuscular stimulation, because surface stimulation is noninvasive and could be easier to use than intramuscular implantation.
We recently studied the physiological effects of surface stimulation using one electrode placement in patients with severe pharyngeal dysphagia (13). Stimulation induced a descent of the hyoid bone when presented at rest. When the same stimulation was applied during swallowing in these patients, no significant change was noted in swallowing safety. However, a relationship was found between the extent of hyoid depression during stimulation at rest and the amount of reduction in aspiration and penetration during stimulated swallows compared with nonstimulated swallows. This relationship suggested that, in some patients, the stimulation may have served as a resistance to hyoid elevation and might have increased their effort during swallowing, accounting for their reduced aspiration and penetration with stimulation. This raised the issue of whether the stimulation-induced hyoid descent can be overcome during swallowing. If normal volunteers cannot overcome stimulation-induced hyoid descent during swallowing, then patients might be placed at risk by using surface stimulation during swallowing.
The first purpose of this study was to examine whether different surface electrode placements vary in their effects on hyolaryngeal position when applied at rest. When surface electrical stimulation is applied to the skin, depolarization will first activate sensory fibers in the skin and, with high enough intensity, will activate nerve endings in muscles that lie immediately below the skin surface. In the laryngeal region, the platysma is the most superficial muscle and overlies the omohyoid and sternohyoid muscles, which pull the hyoid downward, and could resist hyoid elevation during swallowing. The thyrohyoid muscle, which elevates the larynx to the hyoid, lies deep beneath the sternohyoid and omohyoid and is less likely to be activated by electrical stimulation on the skin surface. On the other hand, if surface stimulation were applied under the chin in the submental region, the mylohyoid and geniohyoid may be activated. The activation of these muscles may vary, however, depending upon the location of the stimulating electrodes and the amount of adipose tissue in this region.
This study determined whether using various placements of surface electrodes differed in the resultant movement of the hyoid bone and larynx when applied at rest in healthy individuals. It also examined whether or not surface electrical stimulation-induced hyolaryngeal descent could be overcome by normal volunteers during swallowing. If healthy volunteers could not overcome the effects of hyolaryngeal descent induced by surface stimulation during swallowing, then patients with dysphagia would be less likely to overcome hyolaryngeal descent during swallowing with stimulation. We measured both the duration of movement of a liquid bolus from the back of the pharynx into the esophagus (the pharyngeal transit time) and the peak hyolaryngeal elevation during stimulation and nonstimulated swallows.
We hypothesized 1) that different arrangements of surface electrodes might differ in the degree to which they caused: descent of the hyolaryngeal complex when applied at rest, and 2) that healthy volunteers might not be able to overcome the effects of stimulation-induced hyolaryngeal lowering on measures of peak hyolaryngeal elevation and pharyngeal transit time when stimulation was applied during swallowing. Finally, blind ratings of the videofluoroscopy recordings of swallowing were performed to determine whether swallowing safety was altered by the application of stimulation in healthy volunteers.
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METHODS |
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Procedures. Measures of participants’ adipose tissue thickness in the submental and laryngeal regions were obtained using a caliper (Lange Skinfold Caliper, Beta Technology, Santa Cruz, CA). Each participant was familiarized with the sensations to expect with use of the surface electrical stimulation unit (VitalStim, Chattanooga Group, Chattanooga, TN). The electrical stimulation unit provided two channels of bipolar electrical stimulation at a fixed 80-Hz pulse rate and a fixed biphasic pulse duration of 700 µs. Each channel can be independently adjusted between 0 and 25 µA of stimulation intensity.
The skin in the submental and laryngeal regions was cleaned with alcohol and wiped with a TENS Clean-Cote Skin Wipe to increase the adherence of the electrodes to the skin (Tyco Uni-Patch Model UP220). All male participants were clean-shaven to allow the electrodes to adhere to the skin. Adult-sized electrodes (VitalStim, REF 59000) with a 2.1-cm round active area were used. A chin-neck bandage (Caromed model 1–8006) was fitted over the electrodes to maintain good contact.
A total of 10 different electrode placements was used (Fig. 1). Before data recording, each electrode pair was placed on the skin, and the stimulation intensity was raised gradually in 0.5-mA steps until the participant could first feel a tingling sensation. Then the stimulation level was gradually increased until the participant reported a tugging sensation. The level was then increased further until the participant indicated that any further increase would become uncomfortable, yielding the maximum tolerance level. The maximum tolerance level was determined and recorded for all electrode pairs in a placement simultaneously.
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Three placement groups (A, B, and C) grouped electrode placements that shared some of the same electrode locations. Group A included placement 1, 1 superior, 2, 2 superior, and 2 inferior. Group B included placements 3B and 3B superior. Group C included placements 3A, 3A right, and the submental-only placement. The placements were randomized separately within the group they were assigned to (A, B, or C). Two group orders were randomly used among participants (A, B, then C; and C, B, then A). Group B always occurred between groups A and C, because it shared more electrodes among the groups.
Two swallowing trials were always administered immediately following the group B placements. The subject was given 5 ml of liquid barium to swallow, both with and without stimulation using only placement 3B, the placement previously found to produce extensive hyoid descent in patients with dysphagia (13). Thus 12 pseudorandomized trials were recorded (10 at rest stimulations and two swallows, one without stimulation and the other with stimulation). The stimulation level was set at a participant’s maximum stimulation tolerance level for each placement where the subject reported a "grabbing" sensation, as instructed in the Training Manual for VitalStim Therapy (18).
Surface electromyography electrodes, placed on the neck lateral to the stimulating electrodes, recorded the stimulus artifact for determining stimulation onset and offset times. A metal sphere, 19 mm in diameter, was taped to the neck for distance calibration (Fig. 2).
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3 s at rest during videofluoroscopy to visualize whether any movement occurred with stimulation. The videofluoroscopic image was recorded on a Super VHS videocassette recorder (Panasonic) at 60 frames/s. A time stamp in hundredths of a second was recorded on each frame. For stimulation at rest trials, participants were instructed not to move and to keep their jaws closed. This was to prevent any jaw opening because of the proximity of the surface electrodes to the anterior belly of the digastric, which overlies the mylohyoid in the submental region and could be invoked with surface stimulation, although jaw closing was not necessary during intramuscular stimulation using hooked wires placed directly into the mylohyoid or thyrohyoid muscles (4). It was important to prevent mouth opening, which might interfere with swallowing (5) and cause spillage of the liquid from the mouth during the swallowing trials. Before the study, participants were familiarized with the sensation of stimulation to reduce extraneous movement in response to stimulation onset. For swallowing trials, participants were instructed to hold the 5-ml bolus in their mouths until told to swallow and to avoid multiple swallows. Stimulation was initiated and remained on before, during, and after the swallow (3 s). Electrodes were kept on the subject during nonstimulated swallows so that the investigators could be blinded during data analysis of the videotaped swallow samples. The stimulator contained two sets of bipolar electrodes and automatically cycled on for 59 s and off for 1 s. To prevent muscle fatigue and coordinate stimulation onset with videofluoroscopic recording, a switch box was used to interrupt the flow of current between the controller box and the pairs of electrodes, except when the button was pressed.
Data analysis. The videofluroscopic recordings were used to locate the hyoid, larynx (subglottal air column), and bolus during stimulation and swallowing (Fig. 2). All videofluoroscopic recordings were digitized using a frame grabber board and Peak Performance Image Processing (ViconPeak, Centennial, CO 80112), version 8.2, for kinematic analysis. The stimulation onset and offset frame counter times were noted for each trial. The lower anterior corner of the second and fourth cervical vertebrae was marked, and a line drawn through these two points served as the y-axis. The x-axis was drawn at a 90° angle to y-axis through the point on the fourth cervical vertebra. The following points were marked on each frame: the superior/posterior aspect of the subglottal air column measured the laryngeal position on the y-axis, and the anterior/inferior most point of the hyoid bone measured the position on the x- and y-axes (Fig. 2). On swallowing trials, the position of the bolus head and tail was marked on each frame. When either the second or fourth cervical vertebra was obscured by a radiopaque structure (i.e., the calibration sphere or electrodes), other vertebrae were marked as reference points (i.e., the third and fifth vertebrae).
For stimulation at rest, we computed the mean position of the subglottal air column (larynx) and the hyoid for 400 ms or 25 frames before stimulation onset (nonstimulation period mean) and during the stimulation period (stimulation period mean). Position change scores for the hyoid on the x- and y-axes and the larynx on the y-axis were computed by subtracting the nonstimulation period mean from the stimulation period mean. A negative score indicated laryngeal or hyoid descent on the y-axis or posterior movement of the hyoid on the x-axis. Fifty-nine stimulation-at-rest trials, evenly distributed across the 10 different placements, were selected and reanalyzed for intrarater reliability.
For swallowing trials, the peak elevation of the hyoid and larynx and pharyngeal transit times was measured for nonstimulated and stimulated trials. The investigator was blinded to the presence or absence of stimulation. Pharyngeal transit time was defined as the time between when the front edge of the bolus head passed the ramus of the mandible (time 1) and when the tip of the bolus tail (that remained part of the bolus) reached the upper esophageal sphincter (time 2). The peak elevation for the hyoid and larynx on the y-axis was determined for nonstimulated and stimulated swallows for each subject. Subtracting the nonstimulated swallow peak from the stimulated swallow peak derived a swallowing peak difference with stimulation. Negative scores indicated that less elevation occurred on the stimulated swallow.
Swallowing trials were also assessed for safety by four speech-language pathologists using the National Institutes of Health Swallowing Safety Scale (NIH-SSS). When scoring a swallow, a score of 1 was assigned for the occurrence of each of the following abnormalities: pooling in the vallecula, pooling in the pyriform, penetration into the vestibule from the hypopharynx, and backup penetration from the pyriform into the laryngeal vestibule. The number of aspirations was counted, and the amount of the bolus material entering the esophagus (without returning to the pharynx) was rated for each swallow, either as all (0), some (1), minimal (2), or none (3). Only normal swallows received a total of 0 on this scale, and the maximum score depended upon the number of abnormalities in bolus flow that occurred in a single swallow.
All four speech-language pathologists viewed each videofluoroscopic recording without knowledge of the presence or absence of stimulation and came to a consensus on all noted behaviors before assigning ratings. Additional swallows were randomly selected and rated a second time for judging reliability.
Statistical analysis. To determine measurement reliability, 59 stimulation-at-rest trials, evenly distributed across placements, were reanalyzed. Intraclass correlation coefficients (ICC) were computed for each placement for hyoid measures on the x- and y-axes and for laryngeal measures on the y-axis using only the repeated sets of 59 ratings for measuring intrarater reliability. The ICC represents the proportion of total variation (between-subject variability and measurement variability) that may be attributed to between-subject variability. Values near 1 suggest nearly all variability is essentially biological variance and not related to measurement, whereas values near 0 indicate that variability is primarily a result of measurement problems (6).
The primary goal of the study was to assess how stimulation placements differed in their effects on hyoid and larynx position with stimulation. A mixed-effects model (similar to a repeated-measures ANOVA with covariates but with fewer restrictive assumptions) was used to address these questions [see Pinheiro and Bates (16) for a discussion of such models]. To test the hypothesis that surface electrical stimulation at rest would cause hyolaryngeal descent, the changes in position (for example, the changes in hyoid position along the y-axis) were compared across the 10 different electrode placements using a mixed-effects model with electrode position as the fixed factor of interest and participants as random effects. Other covariates were included as fixed effects to account for some participant-to-participant variability. The covariates considered were sex, age, submental and laryngeal region fat caliper readings, and stimulation intensity level. Three such models were fit to measure position change of the hyoid on the y-axis, the larynx on the y-axis, and the hyoid on the x-axis.
When placement differences were significant (as evidenced by a significant effect corresponding to the electrode placement factor), post hoc pairwise comparisons of the mean changes between different positions were conducted with Bonferroni corrected 
values; the original P values were multiplied by 45 to obtain the corrected P values that reflect the number of pairwise comparisons.
We also hypothesized that stimulation-induced hyoid descent during swallowing would reduce the peak hyoid and laryngeal elevations and increase pharyngeal transit time. A paired t-test was used to compare pharyngeal transit times between nonstimulated and stimulated swallows. The participants’ differences in peak hyoid and laryngeal elevation between stimulated and nonstimulated swallows were compared with zero using one-sample t-tests.
A one-sample directional t-test was used to compare the scores on the NIH-SSS for stimulated and nonstimulated swallows. For judging reliability, percent agreement was derived for each scoring category (e.g., vallecular pooling, esophageal entry).
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RESULTS |
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values < 0.05). Placement 3B showed the greatest laryngeal descent during stimulation at rest, while the submental-only placement showed no change in laryngeal position with stimulation at rest (Fig. 3). For hyoid movement on the y-axis, post hoc comparisons between placements showed the greatest differences between placements 2 superior, 3B superior, and submental-only and all other placements during stimulation at rest. These three placements did not produce any hyoid descent, while all other placements produced descent of the hyoid bone. Differences in laryngeal and hyoid vertical positions with stimulation at rest occurred between placements 3B and 3B superior (P < 0.0001). Movement change for the hyoid bone on the y-axis also differed significantly between placements 2 and 2 superior (P < 0.0001) and between placements 2 superior and 2 inferior (P < 0.0001).
During swallowing, a one-tailed t-test revealed a significant difference from zero for change in peak elevation for the larynx (P = 0.012) and hyoid (P < 0.0005), demonstrating reduced laryngeal and hyoid peak elevation during stimulated swallows compared with nonstimulated swallows (Fig. 4). No significant difference in pharyngeal transit times occurred between stimulated and nonstimulated swallows (P = 0.116).
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When judging swallowing safety using the NIH-SSS, judges had >80% agreement on each swallowing feature that was rated. The risk for aspiration and swallowing safety worsened during stimulation. A one-sample directional t-test compared nonstimulated swallows with stimulated swallows within participants and revealed that stimulated swallows were judged to be significantly less safe than nonstimulated swallows using the NIH-SSS (P = 0.0275).
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DISCUSSION |
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During normal swallowing, the hyoid bone and larynx elevate 20 mm, and the hyoid bone moves anteriorly 5 mm in healthy young men (8). Stimulation using placement 3B at rest caused the greatest hyoid descent (10 mm) in the opposite direction from movement during swallowing. Stimulation with electrodes placed on the neck over the larynx (placements 1, 1 superior, 2, 2 inferior, 3A, 3A right, and 3B) produced greater descent of the hyoid and larynx than when electrodes were only in the submental region (2 superior, 3B superior, and submental-only) (Fig. 3). Placements over the larynx caused descent, most likely due to activation of the omohyoid, sternohyoid, and sternothyroid muscles, which are large, close to the neck surface, and superficial to the thyrohyoid muscle (19). Although the thyrohyoid muscle pulls the larynx upwards and toward the hyoid bone, it lies deep beneath the sternohyoid and omohyoid and was less likely to have been stimulated.
Placements that used two electrode pairs to target both the submental and laryngeal regions, such as placements 2 and 3B, may have simultaneously activated opposing muscles. In other words, electrodes on the submental region likely activated the mylohyoid and geniohyoid, which raise the hyoid bone, whereas electrodes over the larynx may have activated the sternohyoid and omohyoid, which lower the hyoid bone. Yet hyoid descent occurred with both of the aforementioned combined electrode placements and had descent comparable to that observed in placement 2 inferior, a placement where only the regions below the hyoid were stimulated (Fig. 3). This suggests that the muscles below the hyoid (sternohyoid and omohyoid) overpowered any elevation effects due to geniohyoid and mylohyoid contraction induced by the upper electrodes in placements 2 and 3B. Because the sternohyoid and omohyoid are large, they may be more powerful than the geniohyoid and mylohyoid muscles. Moreover, submental fat measures were an average of 4.4 mm greater than laryngeal fat measures (Table 1), possibly contributing increased resistance to muscle stimulation in the submental region.
Limited laryngeal movement occurred with each of the placements. No elevation was observed, and the descent was limited to a couple of millimeters. Possibly laryngeal descent might have occurred secondary to the hyoid bone pushing the larynx downward due to contraction of the sternohyoid and omohyoid muscles.
Stimulation did not produce significant horizontal movement of the hyoid bone. The submental-only placement had both sets of electrodes placed bilaterally over the region of the mylohyoid and geniohyoid muscles and the anterior belly of the digastric. By asking the participants to close their mouth during stimulation both at rest and during swallowing, the effect of surface electrical stimulation activating the anterior belly of the digastric, which has a jaw-opening action, was prevented. This may have also enhanced swallowing to some degree, in that trigeminal afferents from the masseter and the periodontal receptors have recently been shown to have excitatory terminations in the nucleus ambiguus, the region of laryngeal and pharyngeal motor neurons (20). Despite jaw stabilization, however, submental stimulation alone on the surface of the skin produced no elevation of the hyoid, with only some anterior movement compared with all other placements, although these results were not significant. This is in contrast with intramuscular stimulation using hooked wires placed in the mylohyoid muscles at rest, which produced 50% of the extent of laryngeal elevation that occurs during swallowing (4).
Significant decreases in both laryngeal and hyoid peak elevation occurred during the surface stimulated swallows using placement 3B (Fig. 4). Stimulation temporarily modified a normal swallow in these healthy participants, despite the fact that they had intact musculature and normal coordination. The results suggest that these normal participants were not able to overcome the stimulation effects and that their hyolaryngeal elevation did not achieve the same level as during nonstimulated swallows. Thus patients with dysphagia, who are likely to have compromised hyolaryngeal elevation (9), could experience detrimental effects on their hyolaryngeal elevation during swallowing with most surface stimulation placements. Furthermore, the three positions that did not produce hyoid descent, placements 2 superior, 3B superior, and submental only, also did not raise either the hyoid or the larynx during stimulation at rest. Therefore, none of the electrode positions used in this study could be expected to augment hyolaryngeal elevation in patients with dysphagia, and most would be detrimental to patients’ hyolaryngeal elevation.
We only evaluated the effects of placement 3B on swallowing in these healthy volunteers. This was the placement, along with placement 2 inferior, that induced the greatest hyoid descent when presented at rest. The only stimulation placements that did not lower the hyoid were placement 2 superior, 3B superior, and the submental only. The submental-only placement raised the larynx by 1 mm (Fig. 3). Because healthy volunteers usually raise their hyolaryngeal complex by 20 mm during swallowing, the amount of hyoid elevation induced by surface stimulation, between 1 and 2 mm, would be of no consequence in normal volunteers. In patients with no or limited hyolaryngeal elevation, this small amount of elevation of only 1–2 mm of hyoid and/or laryngeal elevation would not be adequate to achieve the normal range of 20 mm of elevation.
None of the previous studies employing surface electrical stimulation have examined the physiological effects of stimulation on swallowing. Freed et al. (7) compared the effects of therapy using surface electrical stimulation, similar to that used in this study, with thermal pharyngeal sensory stimulation in two groups of poststroke patients. Results indicated that surface electrical stimulation improved swallow function compared with sensory stimulation with longer maintenance of the improved swallow outcomes. Leelamanit et al. (10) also used surface stimulation in patients with dysphagia and assumed that surface electrical stimulation to the laryngeal region would activate the thyrohyoid muscle and raise the larynx. Our results suggest that increases with surface electrical stimulation reported by the previous studies (7, 10) cannot be assumed to result from augmentation of hyolaryngeal elevation. Rather, our results indicate that the motor effects of stimulation would cause hyolaryngeal lowering, particularly in patients with dysphagia.
Others have studied the effects of sensory stimulation using a 2-Hz stimulation rate in the oral region during swallowing. Park et al. (15) used this slow rate of electrical stimulation to the soft palate as a sensory stimulus to elicit an involuntary swallow in four chronically dysphagic patients poststroke. Involuntary swallows were not elicited, but partial laryngeal elevation was observed in one patient while he was attempting to swallow. Stimulation decreased total transit time (duration of oral and pharyngeal phases) in each patient. Electrical stimulation to the skin surface may also have sensory stimulation effects besides the motor effects of reducing hyolaryngeal elevation. Recently, low levels of surface electrical stimulation to the skin at the sensory threshold level were shown to reduce aspiration and pooling in severe dysphagia (13).
Ten different electrode placements were investigated in the present study to determine whether placement of electrodes changed the movement outcome. Individual differences in maximum tolerance levels resulted in highly variable results for some measures but give a realistic account of the variability that likely exists in the normal population. It must be recognized, however, that persons with severe dysphagia may be highly motivated and would likely tolerate higher levels of stimulation than did the normal participants in this study. Furthermore, the normal participants were younger than 60 yr old and did not have possible denervation, which can occur in individuals >60 yr old (17).
In conclusion, this study showed that surface electrical stimulation to the laryngeal regions caused significant hyoid and laryngeal descent at rest and reduced hyoid and laryngeal peak elevation during swallowing in healthy adults. Only submental placements alone did not produce hyoid descent, but these electrode placements did not provide the expected hyolaryngeal elevation or anterior movement. These findings are in contrast with results using intramuscular stimulation of the thyrohyoid and mylohyoid muscles, which has been shown to induce laryngeal elevation comparable to 50% of elevation that occurs during swallowing (4). Surface stimulation, therefore, would not be an acceptable alternative to the more invasive intramuscular stimulation for enhancing hyolaryngeal elevation in dysphagia. In fact, the results of this study and our laboratory’s previous study in dysphagic patients (13) suggest that surface stimulation would be detrimental to hyolaryngeal elevation in dysphagic individuals, particularly in those with already reduced volitional hyolaryngeal elevation.
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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