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1 Department of Speech and Hearing Science, University of Illinois at Urbana-Champaign, Champaign, Illinois 61820; 2 Center for Digestive Disease, Farmington, New Mexico 87401; and 3 Department of Otolaryngology-Head and Neck Surgery, University of Iowa Hospitals and Clinics, Iowa City, Iowa 52240
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The durations and temporal relationships of electromyographic activity from the submental complex, superior pharyngeal constrictor, cricopharyngeus, thyroarytenoid, and interarytenoid muscles were examined during swallowing of saliva and of 5- and 10-ml water boluses. Bipolar, hooked-wire electrodes were inserted into all muscles except for the submental complex, which was studied with bipolar surface electrodes. Eight healthy, normal, subjects produced five swallows of each of three bolus volumes for a total of 120 swallows. The total duration of electromyographic activity during the pharyngeal stage of the swallow did not alter with bolus condition; however, specific muscles did show a volume-dependent change in electromyograph duration and time of firing. Submental muscle activity was longest for saliva swallows. The interarytenoid muscle showed a significant difference in duration between the saliva and 10-ml water bolus. Finally, the interval between the onset of laryngeal muscle activity (thyroarytenoid, interarytenoid) and of pharyngeal muscle firing patterns (superior pharyngeal constrictor onset, cricopharyngeus offset) decreased as bolus volume increased. The pattern of muscle activity associated with the swallow showed a high level of intrasubject agreement; the presence of somewhat different patterns among subjects indicated a degree of population variance.
deglutition; electromyography; pharynx; larynx
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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VARIOUS TECHNIQUES have been used to study physiological and biomechanical aspects of the oral and pharyngeal stages of deglutition. The two most commonly used techniques, videofluoroscopy and videoendoscopy, provide information on the movement of anatomic structures during deglutition. A third technique, pharyngeal manometry, is used to study the pressures generated during the pharyngeal stage of swallowing. Each of these three techniques provides only inferential information about muscle activation. The determination of muscle activation patterns is best achieved with electromyography (EMG). Both animal and human experiments in which EMG was used have contributed to the corpus of knowledge on deglutition. Unfortunately, there have been a limited number of such experiments reported over the past 40 years, and only two major attempts at compiling a review of that literature on the oral and pharyngeal stages have been published in the past 25 years (1, 3).
One of the early and most frequently cited studies on the pharyngeal stage of the swallow is that by Doty and Bosma (5). In that investigation, the researchers used needle electrodes to record intramuscular EMG activity during swallowing from a large complex of oral, pharyngeal, and laryngeal muscles in anesthetized monkeys, cats, and dogs. Direct nerve stimulation was performed in anesthetized animals, and the investigators concluded that there is an organized and relatively invariant sequence of muscle activation during swallowing. Although highly descriptive, the use of different animal species precluded quantification of their findings. Additional EMG investigations of the oral and pharyngeal stages of swallowing in nonhuman species have been reported (10, 17, 18, 20, 21, 30, 34). Generally, data from those studies support the conclusion that had been stated earlier by Doty and Bosma that the nonvoluntary portion of the swallow is controlled by a central program generator (16). Some quantitative information was reported by Miller (21), who found that the total duration of the canine swallow from first EMG onset to last EMG offset was in the range of 700-900 ms.
Most of the human studies in which intramuscular EMG of various aspects of the pharyngeal stage of swallowing was performed have concentrated on the activity of a single muscle or muscle pair (2, 23, 25, 28, 32, 33). The study of a single muscle or muscle pair can provide valuable information about the properties of the muscle of interest. However, it does not provide information about the dynamics of swallowing, and a competent swallow requires a complex sequence of oral and pharyngeal events that result in the passage of a bolus into the esophagus. Those studies that did examine EMG activity among more that one pair of muscles in humans (6, 8, 9, 11, 19, 29) have been somewhat limited in their scope and did not quantify their temporal relationships. Quantitative surface EMG investigations of the submental complex (SM) and of suprahyoid muscle firing during swallowing reported that the duration of SM activity was viscosity dependent and that EMG duration was longer for paste than for liquid (4, 27).
A breakdown in the efficiency of the swallow can occur as a result of physiological or biomechanical changes in the anatomic structures involved in performing a swallow. Therefore, it is imperative that we develop an understanding of the muscle firing pattern that occurs with a normal swallow. The purpose of the present investigation was to record EMG activity from a select group of muscles that have been identified as participants in nonhuman mammalian swallowing and to quantify the temporal relationships of those muscles during the human swallow.
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METHODS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects
Six male and two female subjects ranging from 23 to 25 yr of age participated in this investigation. All subjects were healthy, and each denied any history of velopharyngeal insufficiency; palatal, pharyngeal, or laryngeal surgery; neuromuscular disease; or speech or swallowing problems. All subjects had a normal physical examination of the neck, pharynx, and larynx as performed by an otolaryngologist (T. M. McCulloch), and no subjects wore a dental plate. All subjects were advised of the risks of this investigation, and each signed the necessary Human Subject Consent Forms.The safety of laryngeal EMG is emphasized by an article by Mu and Yang (22) in which 1,200 patients with laryngeal motor disorders underwent ~3,200 laryngeal EMG examinations. The examiners reported no complications resulting from the EMG procedures.
Electrode Preparation
Bipolar, 0.003-gauge, silver-coated, hooked wire electrodes (Medwire, Mt. Vernon, NY) were prepared by using techniques similar to those described by Hirano and Ohala (12). Electrodes to be inserted transorally were prepared with 0.5-in. 25-gauge needles to which a retrieval line was connected to the needle hub (Fig. 1A). To ensure accurate depth of placement, the transoral electrodes prepared for insertion into the superior pharyngeal constrictor (SPC) were constructed by threading all but the distal 2 mm of the needle through polyethylene tubing (25) (Fig. 1B). Transcutaneous electrodes were prepared with 0.5- and 1.5-in. 25-gauge needles (Fig. 1C). Surface electrodes to be placed in the SM region were commercially available.
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Electrode Placement
SPC. Electrodes were inserted into SPC by using the technique described by Perlman et al. (24, 25). Topical anesthesia, (Hurricaine Spray, 20% benzocaine) was applied to the posterior pharyngeal wall, and the electrodes were inserted just lateral to the median raphe of the posterior pharyngeal wall, below the level of the soft palate. Placement was verified by observing increased activity during the swallow and the absence of activity with head movement.
Interarytenoid (IA). Subjects were instructed to gargle with 0.5% dyclonine HCl (Dyclone). A rigid endoscope connected to a camera provided videoendoscopic images of the larynx. While using Fraenkel laryngeal forceps, the otolaryngologist (T. M. McCulloch) inserted electrodes into the IA muscle and observed placement on the video image; the technique was similar to the transoral technique reported by Thumfart (31). Placement was verified by visual inspection, by the presence of activity during sustained phonation tasks at normal and higher pitches, and by the absence of respiratory specific activity.
Thyroarytenoid (TA). Local anesthesia (1.0% lidocaine) was applied subcutaneously over the midline region of the cricothyroid membrane. Electrodes were inserted transcutaneously into the TA muscle. TA was approached from the midline beginning at the level of the cricothyroid membrane as described by Hirano and Ohala (12). Subjects were asked to phonate, and TA was approached at an angle 30° superior and 30° medial to the normal plane. Placement was verified with sustained phonation tasks at normal and higher pitches and the absence of EMG during chin press.
Cricopharyngeus (CP). Electrodes were inserted into the CP muscle by using a technique similar to that of Elidan et al. (7). Insertion was performed at the level of the cricothyroid membrane just lateral to midline. The needle was then advanced in a posterior and inferior direction. Placement was confirmed by a cessation of tonic activity during a swallow followed by reactivation on completion of the swallow, an absence of respiratory specific activity, and no activity with head motion.
SM. Contraction of the muscles of the floor of the mouth (mylohyoid, geniohyoid, and, possibly, the anterior belly of the digastric) was measured via bipolar surface electrodes placed in the midline of the SM region just posterior to the genium.
Data Acquisition
Electrodes were connected to an optically isolated preamplifier (model 310A, Biocommunication Electronics) that provided a fixed gain of 100 times. Additional amplification was provided by a four-channel variable-gain amplifier (model 205, Biocommunication Electronics). Signals were low-pass filtered at 5,000 Hz, recorded onto a DAT recorder (TEAC model RD-111T PCM), and input to a microcomputer. Signals were monitored by using the CODAS System (Computer-based Oscillograph and Data Acquisition System). A chatter channel and written event log were utilized to mark events on the DAT recording. A speaker permitted monitoring of the individual channels throughout the acquisition session.Data-Acquisition Protocol
The subjects were seated in a comfortable chair and the electrodes were placed. Sufficient time was allowed for the effect of local anesthesia to wane before the experimental protocol began. Because we were limited to four channels of amplification, the muscles selected for individual evaluations always included SPC, but others varied. Amplifier gains were established during verification tasks. In a random order, subjects performed seven each of saliva, 5- and 10-ml water swallows. Water volumes were verified with a calibrated syringe. For water swallows, the subjects held the bolus in the oral cavity until the EMG activity returned to a baseline level at which time they were instructed to swallow. Saliva swallows were performed following the same instructions as those presented with the 5- and 10-ml volumes: "When you are ready, please swallow." After data collection, electrodes were removed and the subjects were observed for 30 min. There were no complications.Data Analysis
For each subject and each task, the first five tokens where activity was visualized in all the recorded muscles with no evidence of signal clipping were used for analysis. This resulted in a total of 40 tokens per task (saliva, 5 ml, 10 ml). That is to say, each of the eight subjects performed five swallows each of three bolus volumes, for a grand total of 120 swallows. Data were transferred from the DAT tape to the CODAS system by using the ACODAS program at a sampling rate of 10 kHz per channel and were analyzed by using the ADVPOST program.Relative EMG onset and offset times for swallows were established by
computer-assisted visual inspection of the signal. The ADVPOST program
allows the investigator to change the visual parameters (time
compression or expansion, amplitude magnification or reduction) without
influencing the raw data. For purposes of this investigation, onset was
defined as the point where signal activity began a sustained increase
from baseline. Offset was defined as the point where the signal
activity returned to a baseline or to a reduced, relatively steady-state pattern. To obtain the duration of EMG activity for each
muscle, with the exception of the CP, the time of offset was subtracted
from the time of onset. For the CP muscle, it was the total duration of
reduced EMG activity that was of importance. Figure
2 provides an example of an EMG record
during a 5-ml swallow task. In this figure, EMG onsets and offsets of
the SPC muscle are marked on the signal with a medium level of
compression (A), and only the onset
is marked on the signal that is fully decompressed (B).
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Once the onset and offset for each muscle during each swallow were determined, each swallow was then identified with a muscular pattern of activation in qualitative terms. The frequency of occurrence for each pattern of muscle activation was determined for each subject and for each swallow type. Because both TA and IA were not recorded simultaneously in all subjects, when TA was recorded alone, it was assumed that IA followed the modal pattern. A similar assumption was held for the activation of SPC and CP.
For quantification of temporal events, SPC onset was defined as time 0. This muscle was chosen because the muscle has a characteristic EMG signal associated with the swallow (25), is easy to access, and is outside voluntary control.
Because intrasubject agreement was high, as will be discussed in RESULTS, analysis for each muscle by subject and by task were averaged. Those averages were then used to generate a grand mean and SE for each muscle across subjects.
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RESULTS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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The gender and the muscles tested for each of the eight subjects are
shown in Table 1. Although four electrode
pairs were inserted into subject 3, the insertion of one electrode pair, which was intended for
cricothyroid placement, resulted in severe movement artifact and poor
signal-to-noise ratio; therefore, the data were not included in the
analysis.
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Qualitative Patterns of EMG Activity
A dominant pattern of EMG activity was identified across the three bolus types tested (saliva, 5 ml water, 10 ml water). That pattern was characterized by SM onset, SPC onset, CP offset, IA onset, and TA onset. Across subjects, the dominant pattern occurred in 41% of the 120 swallows tested. Within the saliva swallow group, 23 of the 40 swallows (58%) followed the dominant pattern. Within the 5- and 10-ml water swallow groups, that pattern was present in 38 and 28% of the swallows, respectively. The patterns of activation and frequency of occurrence for each pattern are shown in Table 2. When the SM musculature was excluded from the determination of the temporal pattern of activation, the pattern agreement increased to 28 of 40 (70%) for saliva swallows, 22 of 40 (55%) for 5-ml liquid swallows, and 18 of 40 (45%) for 10-ml swallows.
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When EMG onsets for SPC and TA were examined, it was ascertained that SPC preceded TA for all but 3 of the 120 swallows (97.5%). When the pattern for the two pharyngeal muscles (SPC, CP) was examined, we noted that in 68% of the swallows SPC activation preceded CP deactivation. A temporal relationship for the initiation pattern of the two intrinsic laryngeal muscles (TA, IA) was not discernible. That is to say, the IA muscle was activated before the TA 53% of the time.
Intrasubject pattern agreement occurred for 29 of 40 saliva swallows (73%), 31 of 40 (78%) 5-ml swallows, and 26 of 40 (65%) 10-ml swallows. Overall, intrasubject agreement was 72%. The highest intrasubject agreement came from subjects 1 and 8, with each demonstrating 87% intrasubject agreement. The lowest intrasubject agreement was from subject 2 with 47%; this was followed by subject 4 with 60% intrasubject agreement.
Quantitative Patterns of EMG Activity
The average duration, SD, and SE of activation for the SM, SPC, TA, and IA muscles and of deactivation for the CP muscle are listed in Table 3.
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In Fig. 3, the average duration and SE
of activation are displayed graphically. The SE for each mean is
indicative of the deviations from the dominant pattern of activation
for each muscle and each bolus type. Because the means and SE range of
the offsets of SM, SPC, TA, and IA and the onset of CP overlapped for
each bolus type (Table 3), an analysis of the detailed pattern of muscle activity after bolus transit was determined to be of no importance and was therefore not performed.
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The SM region displayed the longest duration of EMG activity. This was closely followed by the SPC. Overall, TA and IA had the shortest duration of EMG activity. The duration of CP quiesence was in the range of the duration of EMG activity for the TA and the IA muscles.
Both of the intrinsic laryngeal muscles that were examined in this study (TA and IA) showed a trend toward bolus-volume-dependent increases in the duration of activity, and IA showed a significant difference between the saliva and 10-ml water swallows. None of the other muscles tested showed any relationship between volume and duration.
Relative to the onset of SPC activity, the mean time of offset of muscle activity for SM, SPC, TA, and IA, for all subjects during all bolus conditions, ranged from 651 to 782 ms. Onsets and offsets of muscle activation relative to the time of onset of EMG activity in the SPC are listed in Table 3.
The average of the onset and of offset activity, relative to the CPS
onset for each bolus condition is also displayed graphically in Fig.
4. From that figure it is clear that there
is great similarity in performance regardless of bolus type. Although
not statistically significant, with 5- and 10-ml water swallows there
was a tendency for activation of the intrinsic laryngeal muscles to
occur earlier than with saliva swallows.
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DISCUSSION |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The purpose of this investigation was to observe and to quantify the EMG pattern of specific muscle activity during voluntary swallowing in humans. We examined the durations and temporal relationships of the SM complex, SPC, CP, TA, and IA muscles during swallowing of saliva and of a 5- and 10-ml water bolus. Overall, the total duration of the pharyngeal stage of the swallow did not alter with bolus condition. Furthermore, a common sequential firing pattern was generally consistent across the bolus conditions. That is to say, for all muscles, intrasubject pattern agreement occurred in 73% of the saliva swallows, 78% of the 5-ml swallows, and 65% of the 10-ml swallows for an overall intrasubject agreement of 72%. This high level of intrasubject agreement supports the concept of a central pattern generator. However, the somewhat lower level of agreement that we observed between subjects indicates that there is a degree of population variance.
The tendency toward a more consistent intrasubject firing pattern was compatible with the reports on the swallowing patterns from animal studies. Furthermore, the duration of the pharyngeal stage, as measured from the onset of SPC firing to the offset of IA firing, was in complete agreement with the values reported by Miller (21).
The phase relationship across muscles was sensitive to the change from a saliva to a water bolus. The duration of SM EMG activity, which reflects oral muscle activity, began earlier and was significantly longer for saliva swallows than for 5- and 10-ml water swallows. This agrees with the data of Hrycyshyn and Basmajian (13), who also showed longer durations of EMG activity for SM muscles during saliva swallows, and with the findings of Perlman et al. (26), in which solid-state pressure measurements within the oropharynx demonstrated longer duration for saliva swallows than for bolus swallows. Despite the similarity of our data with previous findings, careful interpretation is warranted. A longer duration of SM muscle activity during saliva swallows may well indicate a bolus-volume effect, yet it may also be an artifact of the methodology. Salivary secretion is controlled, in part, by contraction of the muscles of the floor of the mouth. When a subject with a dry mouth was asked to swallow, that subject may have performed various oral manipulations to express saliva from the submaxillary and sublingual glands. Such manipulations would result in an increased duration of muscle activity for saliva swallows. Although our subjects were instructed to "swallow when ready," an increased duration of muscle activity may have been required to generate sufficient saliva for the production of a swallow. Differences between spontaneous and saliva swallows on command have not been investigated.
The TA muscle showed a nonstatistically significant volume-dependent increase in duration. The IA muscle showed a statistically significant difference in duration between the saliva and 10-ml water bolus. Such changes in duration complement a simultaneous manometric and videofluorographic study by Kahrilas et al. (15), which showed a volume-dependent increase in the duration of cricopharyngeal opening. When considered collectively, the data obtained from the present study and those obtained by Kahrilas et al. provide strong support for the concept that swallowing increasingly larger volumes results in an increasingly longer time during which the airway is protected. Such an increase, although not statistically significant between 5- and 10-ml swallows, may be indicative of peripheral feedback to the central pattern generator. To understand the effect of peripheral feedback on the durations of EMG activity, investigations using greater differences in bolus volume and differences in viscosity should be considered.
In previously reported videofluorographic and manometric studies, the upper esophageal sphincter (UES), of which the CP muscle is a major component, has shown a volume-dependent increase in the duration of opening (14). In the present investigation, the duration of CP relaxation did not increase with changes from saliva to 5- and 10-ml water swallows. Given that UES opening is achieved through a combination of laryngeal elevation (34) and CP relaxation, these studies are not contradictory. Our finding of an invariate duration of CP relaxation supports the hypothesis that the duration of UES opening is a combined function of laryngeal elevation as well as of CP relaxation.
Despite the consistent duration of the period of CP relaxation, with increased bolus volume, there was a reduction in the time between the offset of CP activity and the onset of EMG activity in the laryngeal muscles. This effect was due to an earlier onset of laryngeal activity. Thus the total duration of the EMG activity during swallow did not increase with bolus volume increase, but the temporal relationships did alter.
With 5- and 10-ml bolus volumes, this investigation found that the onset of SM EMG activity was <45 ms preceding the onset of SPC firing. This would agree with the findings reported by Doty and Bosma (5). In the present investigation, it was also found that the onset of EMG activity occurred earlier with saliva swallows than with water bolus swallows. To correct for the possibility that this time difference is related to a longer duration of oral maneuvers with small bolus volumes or with saliva alone, future analysis of the relationship of SM activity to the onset of the pharyngeal stage of the swallow should include analysis of the peak of the SM activity.
In conclusion, our data indicate that the pattern of muscle activity associated with swallowing is produced with a high level of consistency. Although noteworthy within as well as between subjects, this reproducibility was more pronounced within than between subjects. Laryngeal muscles showed an increased duration of activity with increased bolus volumes, and SM muscles showed an increased duration of activity for saliva swallows. Finally, the interval between the onset of laryngeal muscle activitiy (TA onset, IA onset) and pharyngeal muscle firing patterns (SPC onset, CP offset) decreased as bolus volume increased.
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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. §1734 solely to indicate this fact.
Address for reprint requests: A. L. Perlman, Dept. of Speech and Hearing Science, Univ. of Illinois at Urbana-Champaign, 901 So. Sixth St., Champaign, IL 61820 (E-mail: aperlman{at}uiuc.edu).
Received 27 April 1998; accepted in final form 11 January 1999.
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METHODS
RESULTS
DISCUSSION
REFERENCES
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