Role of Laryngeal Movement and Effect of Aging on Swallowing Pressure in the Pharynx and Upper Esophageal Sphincter

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1 The Laryngoscope Lippincott Williams & Wilkins, Inc., Philadelphia 2000 The American Laryngological, Rhinological and Otological Society, Inc. Role of Laryngeal Movement and Effect of Aging on Swallowing Pressure in the Pharynx and Upper Esophageal Sphincter Masato Yokoyama, MD; Natsuhiko Mitomi, MD; Katsuhiko Tetsuka, MD; Niro Tayama, MD; Seiji Niimi, MD Objectives: Describe contribution of laryngeal movement to pressure changes at the upper esophageal sphincter (UES) and the effect of aging on the swallowing function. Study Design: Manofluorography on 56 nondysphagic adults divided into three age groups: the 21- to 31-year-old group (n 32), the 61- to 74-year-old group (n 12) and the 75- to 89-year-old group (n 12). Analyses of the bolus transit time, the amplitudes and durations of pharyngeal pressures, the timing of a pressure fall at the UES and the laryngeal movements. Methods: Intraluminal strain-gauge sensors recorded pressure changes in the oropharynx, hypopharynx and the UES. Motion pictures of the videotapes were fed into a personal computer, and movements of the hyoid bone were measured in both the horizontal and vertical directions as an indication of laryngeal movement. Results: In 26- and 70-year-old men with calcification of the thyroid cartilage, it was determined that the larynx and hyoid bone moved in consonance until the end of the rapid hyoid movements in both the superior and anterior directions. In the 21- to 31-year-old group, the magnitude of the pressure fall at the UES was maximal before or almost at the same time as the bolus arrival, in preparation for smooth passage of the bolus from the pharynx to the esophagus. The rapid superior movements of the hyoid bone started significantly early as compared with its anterior movements (P.0001). The rapid anterior movements of the hyoid bone started simultaneously with the pressure fall at the UES. In the elderly, all segmental transit times were significantly increased. The timing of the pressure fall at the UES was significantly delayed and the From the Department of Otolaryngology (M.Y.), Tokyo Metropolitan Bokutoh Hospital, the Department of Otolaryngology (N.M.), JR Tokyo Hospital, and the Departments of Otolaryngology (K.T., N.T.) and Speech Physiology (S.N.), Graduate School of Medicine, University of Tokyo, Tokyo, Japan. This study was done at the Department of Otolaryngology, Graduate School of Medicine, University of Tokyo, Tokyo, Japan. Editor s Note: This Manuscript was accepted for publication December 31, Send Correspondence to Masato Yokoyama, MD, Department of Otolaryngology, Tokyo Metropolitan Bokutoh Hospital, Kotobashi, Sumida-ku, Tokyo, Japan. 434 UES pressure reached its minimum value after arrival of the bolus at the UES. The minimum pressure at the UES increased to a significantly positive value. The rapid anterior movements of the hyoid were significantly delayed, suggesting that this delay causes the delay in the pressure fall at the UES. Conclusions: The rapid superior and anterior movements of the hyoid bone are considered to start at the same time as those of the larynx. In the young group, it is suggested that superior laryngeal movement protects the lower airway prior to the anterior laryngeal movement, causing the pressure fall at the UES to enable the passage of a bolus into the UES. In the elderly, smooth passage of the bolus from the pharynx to the esophagus is hindered and the system that prevents aspiration is rendered inefficient by changes in the swallowing pressures and laryngeal movements with aging. Key Words: Laryngeal movement, swallowing pressure, upper esophageal sphincter, aging, manofluorography. Laryngoscope, 110: , 2000 INTRODUCTION During normal swallowing, the pressures in the pharynx and upper esophageal sphincter (UES) change according to bolus transportation. 1,2 Pharyngeal pressure mostly consists of propagated pharyngeal contraction for facilitating pharyngeal clearance and minimizing the residue after swallowing. 3,4 At the UES, the resting pressure decreases rapidly before the arrival of a bolus to the piriform sinus prior to its entry into the esophagus. 1,2,5 The time course of pressure changes in the pharynx must be appropriate for smooth passage of a bolus without leaving pharyngeal residue or aspiration. Swallowing pressure is generated not only by the activities of the pharyngeal constrictor, UES, and esophageal muscles, but also by the condition of the surrounding structures. Laryngeal movement has been considered to induce a fall of UES pressure. 6,7 However, little information is available about the relationship between laryngeal movement and UES pressure during normal swallowing in human subjects. The physiological function of swallowing gradually deteriorates with aging, resulting in a high risk of swal-

2 lowing disorders in the elderly. 8,9 Given the high incidence and mortality of aspiration pneumonia in the elderly, 10 it is important to examine the effect of aging on the swallowing function. The purpose of this study was to evaluate the contribution of laryngeal movement to pressure changes at the UES and the effect of aging on the swallowing function, by manofluorography (simultaneous video recording of manometry and fluoroscopy). MATERIALS AND METHODS The study was performed in 56 nondysphagic adults divided into three age groups: 21- to 31-year-olds (n 32; 16 men, 16 women), 61- to 74-year-olds (n 12; 6 men, 6 women), 75- to 89-year-olds (n 12; 6 men, 6 women). All subjects gave informed consent before participation in the study. Recordings of swallowing movements were obtained with the subjects sitting or standing in a position comfortable for swallowing. Lateral fluoroscopic images of the oral cavity, pharynx, cervical esophagus, and bodies of the cervical vertebrae were obtained during one swallowing of 10 ml of liquid barium (140 weight/volume %) for each subject. The manometric probe used in this study had an outer diameter of 3 mm, and contained three intraluminal strain-gauge sensors (model CTO-3, Gealtec MMI, Hackensack, NJ) at 4-cm intervals. Light topical anesthesia was performed on the anterior area of the nasal cavity by an 8% lidocaine spray. The probe was inserted nasally and positioned in the pharynx and cervical esophagus so that the distal sensor was situated 0.5 cm proximal to the point of the peak resting pressure in the UES (Fig. 1). Because the UES high-pressure zone moves superiorly during swallowing, 11 the distal sensor reaches the center of the UES high-pressure zone at the onset of UES relaxation. The middle and proximal sensors were located in the hypopharynx and oropharynx, respectively. The sensing face of each sensor was oriented posteriorly. The output of the pressure transducers was transmitted through an amplifier (model 366, NEC Medical Systems, Tokyo, Japan) to a video converter (model EL , NEC Medical Systems), which superimposed the fluoroscopic images and information from a video timer (model VTG-33, FOR.A, Tokyo, Japan) onto a single video screen. The manometric recording with a timing pulse was also demonstrated as digital data at 2-millisecond intervals on a personal computer. All events were analyzed temporally relative to the moment at which the bolus head reached the bottom of the piriform sinus (top of the UES), considered as time zero, because it is important for the smooth passage of a bolus to achieve a reduction in pressure at the UES before bolus arrival at the UES. Motion pictures of the videotapes were fed into a personal computer and frame-by-frame analysis was performed using the NIH Image software. To measure the two-directional movements of the larynx, the vertical and horizontal axes were defined as shown in Figure 2. Because the larynx itself does not have a suitable landmark detectable in each frame of the computerassisted analysis, the hyoid bone was used instead as the representative landmark. The relationship between the movements of the larynx and hyoid bone was examined in 26- and 70-year-old men having nonpathological calcification of the thyroid cartilage. Coordinates of the body of the hyoid and the calcification of the thyroid cartilage were calculated in each frame. The starting point of the analysis was set at time 1 second (1 second before the bolus arrival at the bottom of the piriform sinus). For each subject, 60 sequential frames (at 1/30th of a second intervals for 2 seconds) were analyzed. Consequently, the reliability limit of the timing measurement was 1/30th of a second. Fluoroscopic magnification was corrected for the known 4-cm-length intervals between the manometric sensors. Figure 3 shows a record of swallowing obtained from a 26-year-old man. The parameters for analysis were defined as follows. Fig. 1. Position of the upper esophageal sphincter (UES) sensor. The sensor was situated at the point (star) that is 0.5 cm proximal to the point (circle) of the peak resting pressure in the UES. Fig. 2. A vertical (superoinferior) axis was drawn through the anterior and inferior corners of C3 and C5. The horizontal (anteroposterior) axis drawn through the anterior and inferior corner of C5 was defined as being perpendicular to the vertical axis. Manometric sensors were located at the oropharynx, hypopharynx, and UES at 4-cm intervals. 435

3 Fig. 3. Recording of swallowing movements was performed in a 26-year-old man. The upper three graphs show swallowing pressure (thin lines) and bolus transits (bars) in the oropharynx, hypopharynx, and UES. The bottom graph shows the superior (Sup) and anterior (Ant) movements of the hyoid bone. 1. Pharyngeal transit time: Duration from the moment the bolus head touches the oropharyngeal sensor to the moment the bolus tail leaves the UES sensor. 2. Segmental (oropharyngeal, hypopharyngeal, or UES) transit time: Duration from the moment the bolus head touches the respective sensor to the moment the bolus tail leaves the same sensor. 3. Oropharyngeal (or hypopharyngeal) Pmax: Maximum value of the oropharyngeal (or hypopharyngeal) pressure. 4. Oropharyngeal (or hypopharyngeal) pressure duration: Duration of the oropharyngeal (or hypopharyngeal) positive pressure. 5. Oropharyngeal (or hypopharyngeal) Pave: Average value of the oropharyngeal (or hypopharyngeal) positive pressure while the bolus is transiting the sensor. 6. UES Pmin: Minimum value of the UES pressure. 7. Time PF: The time at which the UES pressure begins to fall. 8. Time Pmin: The time at which the UES pressure becomes minimal. 9. UES relaxation duration: Duration from Pmin to the moment at which the UES pressure begins to rise with recontraction of the UES. 10. Time HS (or HA): The time at which the rapid superior (or anterior) movement of the hyoid bone starts. 11. PF-HS (or PF-HA) interval: Duration from the moment at which the UES pressure begins to fall to the moment at which the rapid superior (or anterior) movement of the hyoid bone starts. A paired Student t test was used to determine the difference between time HS and time HA in each of the age groups. To determine the differences between age groups, a one-way factorial ANOVA was used with a Fisher s post hoc test. Statistical significance was defined as P.05. Values in the text are expressed as means SEM. RESULTS Figures 4 and 5 show recordings of the movements of the larynx and hyoid bone obtained from 26- and 70-yearold men with calcification of the thyroid cartilage. The two structures moved in consonance until the end of the rapid hyoid movements in both the superior and anterior directions. Figures 6 through 9 show the results of comparison between age groups. All of the bolus transit times were significantly increased in the elderly (Fig. 6). No significant difference was shown in oropharyngeal/hypopharyngeal Pmax and Pave between age groups (Fig. 7). UES Pmin was significantly increased in the elderly. Oropharyngeal/hypopharyngeal pressure duration was significantly increased in the elderly (Fig. 8). However, UES relaxation duration showed no significant difference between age groups. Time HA, time PF, and time Pmin were significantly delayed in the elderly (Fig. 9). Figure 9 reveals the results of the comparison between time HS and time HA in each of the age groups. Time HA was significantly delayed compared with time HS in each age group. Table I shows the values of PF-HS and PF-HA intervals. In each of the age groups, the average PF-HA interval was within 0.03 seconds, the detection limit of the timing measurements. DISCUSSION Relationship Between Movements of Larynx and Hyoid Bone Laryngeal movement during swallowing is a result of activity of the suprahyoid (also called the leading complex) and extrinsic laryngeal muscles. Among these muscles, the geniohyoid and thyrohyoid play the predominant role. 12,13 Activity appears simultaneously in the respective suprahyoid muscles, much earlier than in the other muscles. 14 Simultaneous recording of the electromyogram and fluoroscopy revealed that the superior laryngeal move- Fig. 4. Superior (Sup) and anterior (Ant) movements of the larynx and hyoid bone during swallowing in a 26-year-old man. Laryngeal movements were traced by monitoring the movements of the calcified thyroid cartilage. 436

4 Fig. 5. Superior (Sup) and anterior (Ant) movements of the larynx and hyoid bone during swallowing in a 70-year-old man. Laryngeal movements were traced by monitoring the movements of the calcified thyroid cartilage. ment reached its peak in 0.76 seconds and that the activity of the thyrohyoid muscle appeared 0.49 seconds later than the onset of this movement. 13 Thus during the early two thirds of superior laryngeal movement, because the thyrohyoid muscle does not contract, the spacial relation between the hyoid bone and thyroid cartilage must be stable. This means that the larynx and hyoid bone move together by contraction of the suprahyoid muscles during this period. The hyoid bone is considered to be a useful landmark for monitoring laryngeal movements during swallowing because of its radiopacity. Cineradiographic studies revealed that the position of the rima glottis was closely related to the movement of the hyoid bone, but the former continued to rise even after the latter reached its peak. 15 Our study also shows that the larynx and hyoid bone move in consonance in both the superior and anterior directions Fig. 7. Values of swallowing pressure in the oropharynx (Oro), hypopharynx (Hypo), and UES. The minimum pressure at the UES was significantly increased in the elderly. * P.05 by one-way factorial ANOVA and Fisher s post hoc test. NS not statistically significant by ANOVA. until the end of the rapid hyoid movements (Fig. 4 and 5). As regards the timing of the rapid movements of the larynx and hyoid bone, it was reasonable to consider the hyoid bone as a representative structure of the whole larynx. Consequently, the rapid superior and anterior movements of the hyoid are thus considered to start at the same time as those of the larynx. Normal Swallowing in the Young Group Disappearance of the positive resting pressure enables smooth passage of a bolus through the UES. Thus the UES pressure must fall before the arrival of the bolus at the UES. Our study reveals that the UES pressure falls to its minimum value before or almost at the same time as the arrival of the bolus. That is, the pressure changes at the UES ensure smooth passage of the bolus from the pharynx to the esophagus. Fig. 6. Bolus transit time at each site. Each of the segmental transit times was significantly increased in the elderly. * P.05 by oneway factorial ANOVA and Fisher s post hoc test. Fig. 8. Duration of positive pressure in the pharynx and relaxation at the UES. The oropharyngeal (Oro) and hypopharyngeal (Hypo) pressure durations were significantly increased in the elderly. * P.05 by one-way factorial ANOVA and Fisher s post hoc test. NS not statistically significant by ANOVA. 437

5 suggests that superior laryngeal movement protects the lower airway prior to the decrease in the UES pressure by anterior laryngeal movement to enable the passage of a bolus into the UES. The timing of the laryngeal movements in the two directions ensures prevention of aspiration. Fig. 9. Timing of rapid hyoid movements and pressure changes at the UES. Time HA, time PF, and time Pmin were significantly delayed in the elderly. Time HA was significantly delayed compared with time HS in each age group. * P.05 by one-way factorial ANOVA and Fisher s post hoc test. NS not statistically significant by ANOVA. #1, #2, #3, P.05 by paired Student t test. The UES pressure falls to a minimum value (UES Pmin) of mm Hg. Cerenko et al. 3 reported that the negative pressure at the UES acts as a hypopharyngeal suction pump for the bolus head. Because the UES is located at the branching point of the respiratory and digestive tracts, a system to prevent aspiration is indispensable. It is important, for prevention of aspiration, not only to close the larynx by adduction of the vocal cords or tilting of the epiglottis, but also to guide the bolus into the esophagus by negative pressure suction. Laryngeal movement plays an important role in swallowing. Anterior laryngeal movement is thought to contribute to the pressure fall at the UES. Asoh and Goyal 6 reported, from studies on the opossum, that anterior laryngeal movement caused by contraction of the geniohyoid muscle caused a pressure fall at the UES, even when the cricopharyngeus and inferior pharyngeal constrictor muscles were kept contracted. Mendelsohn and McConnel 7 reported that manofluorography revealed no negative pressure formation at the UES in a patient without anterior laryngeal movement. In our study, since the average PF-HA interval was within 0.03 seconds, rapid anterior movements of the hyoid bone started almost simultaneously with the pressure fall at the UES. This finding indicates that anterior laryngeal movement causes the pressure fall at the UES in humans also. Superior laryngeal movement tilts the epiglottis, causing closure of the laryngeal introitus for airway protection. Our study shows that rapid superior movements of the hyoid bone started significantly early compared with its anterior movements (P.0001). This finding TABLE I. Intervals Between Beginnings of Pressure Fall at the Upper Esophageal Sphincter and Rapid Hyoid Movements. 21- to 31-Year-Old 61- to 74-Year-Old 75- to 89-Year-Old PF-HS interval (s) PF-HA interval (s) Effect of Aging on Swallowing Our study shows that the durations of positive pressure in both the oropharynx and the hypopharynx were significantly increased in the elderly (Fig. 8), whereas the maximum and average pressures were not significantly different among the different age groups (Fig. 7). These findings suggest that not higher pressures, but rather sustained positive pressures prevail in the pharynx in the elderly. The pharyngeal mucosa becomes less lubricated in the elderly owing to decreased salivation and degeneration of the mucosa itself. 8 The sustained positive pressures in the elderly could be considered to represent adaptation to the diminished lubrication of the pharynx. Oropharyngeal and hypopharyngeal transit times were significantly increased in the elderly (Fig. 6). A decrease in the tongue propelling force is considered to decrease the bolus speed in the pharynx. In addition to the diminished lubrication of the pharynx, the resistance to bolus entry into the UES, as described later, could be a factor that causes the bolus to remain in the pharynx. The pressure fall at the UES (time PF and time Pmin) was significantly delayed in the elderly (Fig. 9). It is noteworthy that the pressure fall at the UES reached its minimum value after the arrival of the bolus at the UES, in contrast to the observation in the young group. Thus the pressure at the UES is still positive at the time of entry of the bolus into the UES. In other words, the elderly have resistance to bolus entry into the UES. The minimum pressure at the UES was increased to a significantly positive value in the elderly. This finding suggests that the elderly have resistance to bolus passage through the UES owing to the existence of a positive pressure during relaxation. Resistance to entry and passage through the UES is considered to cause a significant increase in the UES transit time in the elderly. In each age group, the rapid superior movements of the hyoid bone started significantly early compared with its anterior ones. Thus, the interval between the laryngeal movements in the superior and anterior directions is considered to be well preserved in the elderly. The timing of laryngeal elevation is thought to be delayed in the elderly. Tracy et al. 16 reported that aging prolonged the interval between bolus arrival at the posterior edge of the ramus of the mandible and the onset of laryngeal elevation. In our study, the onset of rapid anterior movements of the hyoid was significantly delayed in the elderly. The rapid anterior movements of the hyoid started almost at the same time as the pressure fall at the UES. These findings suggest that the delay in anterior laryngeal movements causes the delay in the pressure fall at the UES and resistance to bolus entry into the UES in the elderly. 438

6 CONCLUSION Smooth passage of a bolus from the pharynx to the esophagus is hindered and the system that prevents aspiration is rendered inefficient by changes in the swallowing pressures and laryngeal movements with aging. ACKNOWLEDGMENT The authors thank Kimitaka Kaga, MD, for his encouragement and support of the project. This study was supported in part by a grant from the Ministry of Education, Science, Sports and Culture, Japan. BIBLIOGRAPHY 1. Sokol EM, Heitmann P, Wolf BS, Cohen BR. Simultaneous cineradiographic and manometric study of the pharynx, hypopharynx and cervical esophagus. Gastroenterology 1966;51: McConnel FMS. Analysis of pressure generation and bolus transit during pharyngeal swallowing. Laryngoscope 1988; 98: Cerenko D, McConnel FMS, Jackson RT. Quantitative assessment of pharyngeal bolus driving forces. Otolaryngol Head Neck Surg 1989;100: Kahrilas PJ, Logemann JA, Lin S, Ergun GA. Pharyngeal clearance during swallowing: a combined manometric and videofluorographic study. Gastroenterology 1992;103: Atkinson M, Kramer P, Wyman SM, Ingelfinger FJ. The dynamics of swallowing. I. Normal pharyngeal mechanisms. J Clin Invest 1957;36: Asoh R, Goyal RK. Manometry and electromyography of the upper esophageal sphincter in the opossum. Gastroenterology 1978;74: Mendelsohn MS, McConnel FMS. Function in the pharyngoesophageal segment. Laryngoscope 1987;97: Heeneman H, Brown DH. Senescent changes in and about the oral cavity and pharynx. J Otolaryngol 1986;15: Sheth N, Diner WC. Swallowing problems in the elderly. Dysphagia 1988;2: Elliott JL. Swallowing disorders in the elderly: a guide to diagnosis and treatment. Geriatrics 1988;43: Kahrilas PJ, Dodds WJ, Logemann JA, Shaker R. Upper esophageal sphincter function during deglutition. Gastroenterology 1988;95: Maeyama T. Experimental investigations of the function of the intrinsic and extrinsic laryngeal muscles during deglutition, especially for elevation of the larynx. Otologia Fukuoka 1975;21: Yoshida T. Electromyographic and X-ray investigations of normal deglutition. Otologia Fukuoka 1979;25: Doty RW, Bosma JF. An electromyographic analysis of reflex deglutition. J Neurophysiol 1955;19: Ekberg O. The normal movements of the hyoid bone during swallow. Invest Radiol 1986;21: Tracy JF, Logemann JA, Kahrilas PJ, Jacob P, Kobara M, Krugler C. Preliminary observations on the effects of age on oropharyngeal deglutition. Dysphagia 1989;4: