Volitional augmentation of upper esophageal sphincter opening during swallowing P. J. KAHRILAS, J. A. LOGEMANN, C. KRUGLER, AND E. FLANAGAN Departments of Medicine and Communication Sciences and Disorders, Northwestern University and Veterans Administration Lakeside Medical Center, Chicago, Illinois 6061 I

P. J., J. A. LOGEMANN, C. KRUGLER, AND E. Volitional augmentation of upper esophageal sphincter opening during swallowing. Am. J. Physiol. 260 (Gastrointest. Liver Physiol. 23): G450-G456, 1991.-Studies were done on eight normal subjects with synchronized videofluoroscopy and manometry to facilitate a biomechanical analysis of the extent and mechanism of voluntary augmentation of upper esophageal sphincter (UES) opening during swallowing. Movements of the hyoid and larynx, dimensions of sphincter opening, and intraluminal pressure events were determined at 1/30-s intervals during swallows of 1 and 10 ml of liquid barium. Swallows of each volume were obtained both before and after subjects were taught a maneuver designed to augment UES opening, the Mendelsohn maneuver (voluntary prolongation of laryngeal excursion at the midpoint of the swallow). At either volume, use of the maneuver increased the duration of the anterior-superior excursion of the larynx and hyoid and consequently delayed sphincter closure by maintaining traction on the anterior sphincter wall. The onset of the pharyngeal contraction (the event normally culminating in sphincter closure) was not affected by the maneuver. We conclude that swallowrelated hyoid motion, laryngeal motion, and UES opening are subject to volitional augmentation, supporting the notion that biofeedback techniques can be used to modify impaired swallowing. KAHRILAS, FLANAGAN.

cricopharyngeus; maneuver

videofluoroscopy;

manometry;

Mendelsohn

UPPER ESOPHAGEAL SPHINCTER (UES) is a complex musculoskeletal structure that opens during swallowing in conjunction with laryngeal closure to facilitate bolus transfer from the pharynx to the esophagus. Both the duration and the diameter of UES opening during swallowing increase with increased swallow bolus volume (2, 4, 5). A recent study analyzing the mechanism of UES opening and volume-dependent modulation during swallowing suggested that sphincter opening could be divided into five phases (4): 1) relaxation, 2) opening, 3) distension, 4) collapse, and 5) closure. Sphincter relaxation occurred during laryngeal elevation and preceded opening by a mean period of 0.1 s. Sphincter opening was a consequence of the sphincter being pulled apart via muscular attachments to the hyoid such that the hyoid position at which opening occurred was similar among bolus volumes. The degree of sphincter distension achieved after opening was modulated by intrabolus pressure. The period of sphincter collapse was, in essence, the period between distension and the final phase of THE

G450

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$1.50

Copyright

sphincter activity, sphincter closure, which occurred as the propagated pharyngeal contraction reached the UES. Volume-dependent increases of sphincter diameter observed with increased bolus volumes were achieved primarily by increased intrabolus pressures. Modulation of the overall interval of sphincter opening was achieved by prolonging the interval between sphincter opening and the initiation of the pharyngeal contraction. Oropharyngeal dysphagia with impaired UES opening is a frequent clinical problem in brain stem stroke victims and in other neurologically impaired patients. In the past, this has often been attributed to “cricopharyngeal dysfunction,” implying that failed relaxation of this muscle was responsible for the absent or diminished UES opening. The concepts of UES opening outlined above, however, would suggest that impairment of the sphincter opening mechanism is an alternative explanation. Supporting this notion, a stroke victim has recently been reported to achieve improved swallowing function using modified biofeedback to volitionally augment the UES opening mechanism (6). Specifically, use of the Mendelsohn maneuver (purposeful prolongation of the superior and anterior displacement of the larynx at midswallow) accentuated UES opening and transformed a tube-fed patient into an oral feeder. This clinical observation suggests that UES function during swallowing is modifiable by volitional control in addition to the previously described volume regulation. The present study was undertaken to examine the mechanical effects of the Mendelsohn maneuver compared with those of increased bolus volume and to explore the degree to which normal subjects can use the Mendelsohn maneuver to modify UES function during swallowing. METHODS

Concurrent videofluoroscopic and manometric studies of swallowing were obtained in eight healthy male volunteers, 22-28 years of age, without past or current swallowing problems. Studies were done in the late afternoon, at least 4 h after a meal. The study protocol was approved by the Northwestern University Institutional Review Board. During recording sessions, subjects were seated in a chair fitted with a headrest, and lateral videofluoroscopic studies were done according to a method previously described that allowed for subsequent digitization of the video images with coordinate analysis of anatomic struc-

0 1991 the American

Physiological

Society

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CONTROL

TABLE

OF

UES

G451

OPENING

1. Effect of Mendelsohn maneuver on parameters of UES opening Bolus 1 ml

Opening duration, s Maximal diameter, mm Integral of opening diameter, AP closing coordinate, mm

0.36kO.02 7.7t0.7 2.44t0.24 0.85kO.37

mm/s

Values are means t SE. UES, upper vs. 1 ml same condition (with or without

esophageal maneuver).

sphincter;

Volume

1 ml Maneuver

0.56t0.06* 8.5t0.6 3.59t0.57 -0.08kO.32* AP, anterior-posterior.

and

Swallow

Condition 10 ml

10 ml Maneuver

0.58+0.02t 10.9+0.6”f 5.0+0.44t 0.88kO.37

0.75+0.06*t 12.2kO.97 6.2+0.62*-t -0.41&0.52*

* P < 0.05 vs. same volume

without

maneuver.

j- P < 0.05

swallow it as a single bolus. The subjects were then taught the Mendelsohn maneuver. First, with their fingers on their larynx, they felt the movement of their 1 ml with Maneuver larynx during swallowing. Then, they were instructed to 1 ml without Maneuver use the muscles under the chin and in then neck to maximally prolong the superior and anterior displacement of the larynx at midswallow. After trying the maneuver several times, they were observed fluoroscopically three times and given further instruction as necessary. Three test swallows were then obtained using the maneuver for l- and lo-ml boluses. Intraluminal manometry was done with a miniature strain-gauge assembly that was ovoid in cross section (3 x 5 mm) and incorporated three pressure sensors on one of the flat sides, spaced 3 cm apart with identical radial -0.2 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 orientation (Medical Measurements, Hackensack, NJ). Time in Seconds The manometric assembly was passed nasally and positioned with the sensors facing posteriorly so that the middle sensor was 5 mm proximal to the subglottic air column. This position enabled recording of intraluminal ,10 ml with Maneuver UES pressure during normal swallows by the middle __t_ 10 ml without Maneuver sensor (5). Pressure tracings were displayed on a polygraph (model R-611, Beckman, Oxnard, CA) with the sensitivity set at 10 mmHg/cm and the chart speed at 50 mm/s during swallows. Data analysis encompassed both temporal and spatial analysis of the videofluoroscopic images. For all analyses, the time base for each swallow was defined such that the first video frame showing UES opening (either barium or air within the UES) was time zero. This adjustment of the time base facilitated comparison of events among -5 swallows with specific attention to the relationship of -0.2 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 those events to UES opening. Without this time adjustTime in Seconds ment, events appeared staggered in time among swallows, FIG. 1. Upper esophageal sphincter (UES) opening as a function of since they occurred at variable intervals from an earlier bolus volume. A: data from l-ml swallows. B: data from lo-ml swallows. time reference such as the onset of bolus movement in Time 0 represents 1st video frame showing opening and distance 0 the mouth or the initiation of hyoid elevation. represents initial horizontal coordinate of sphincter relative to anchor point before sphincter opening. Anterior opening occurred as horizontal Manometric tracings were analyzed by visual inspecdistance between anterior sphincter wall and anchor point increased, tion, and intrabolus pressure was determined within the while posterior opening occurred as horizontal distance between posUES at the instant of maximal sphincter distension as terior sphincter wall and anchor point diminished. At either volume, determined fluoroscopically. Videofluoroscopic images of use of the Mendelsohn maneuver was associated with prolonging the tail of the opening envelope but had no significant effect on the profile each swallow were temporally analyzed during slow-moof the opening event or the maximal extent of opening achieved. Error tion playback to determine 1) the arrival time of the bars shown are representative. bolus head (leading edge) at the valleculae, 2) the time tures and temporal correlation with simultaneously ob- of arrival of the head and the tail (trailing edge) of the tained manometric recordings (4,7). Three swallows each barium bolus at each pressure sensor, and 3) the timing of swallow-related tongue movements (onset and attainof 1 and 10 ml liquid barium were obtained. Liquid barium was placed in the mouth with a syringe and ment of the ramp configuration seen early in the pharynsubjects instructed to hold the barium over the tongue geal swallow as well as the onset of the subsequent until the swallow command at which time they should posterior movement of the tongue base that terminated Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (130.070.008.131) on October 10, 2018. Copyright © 1991 American Physiological Society. All rights reserved.

CONTROL

OF

UES

OPENING -

__f__ __f_

T T

-0.5

0.0

0.5

1.0

1.5

1 ml With Maneuver 10 ml With Maneuver

2.0

2.5

-0.5

0.0

0.5

1.0

1 ml With Maneuver -

10 ml With Maneuver

-

1 ml Without 10 ml Without

1.5

2.0

Maneuver Maneuver

2.5

Time in Seconds

FIG. 2. Anterior vector of hyoid movement relative to the resting anterior-posterior coordinate during l- and lo-ml swallows with and without use of the Mendelsohn maneuver. Hyoid position at time of sphincter opening is shown by vertical line at time 0. Position 0 on vertical axis for each subject was the most posterior hyoid position observed in that subject during the entire study. As evidenced from extensive overlap among these tracings, anterior vector of hyoid movement was very similar among volumes with or without use of the maneuver and achieved nearly identical maximal excursion values (15 16 mm). The main modification in the anterior hyoid movement profile that occurred with the maneuver was after the peak excursion such that a plateau of intermediate value between the extreme excursion and the resting coordinates was maintained. Error bars shown are representative.

with contact of the tongue base to the pharyngeal wall) (10) Spatial analysis of the videofluoroscopic swallowing sequences was accomplished using an interactive computer program written to enable x-y coordinate determination of selected structures on each video frame (7). For each swallow, 30-90 sequential frames (at 1/30-s intervals) were analyzed and the following anatomic points marked: 1) the anterior-superior corner of hyoid bone, 2) the posterior-superior corner of the subglottic air column, and 3) the anterior and posterior walls of the UES. When the manometric catheter was against the posterior wall of the sphincter, the inside margin of the catheter rather than the outside margin was marked to minimize the effect of the catheter on the sphincter diameter measurement and to allow for the sphincter opening diameter to be zero. The axial position of the UES was uniformly marked 1 cm distal to the subglottic air column corresponding to the typical location of the center of the UES high-pressure zone (5). After the marking of data points on the digitized images, coordinate calculations were computed. The y-axis used in the coordinate analysis was the axis defined by the proximal two manometric sensors. Fluoroscopic magnification was corrected for by using the known distance of 3 cm between the first and second manometric sensors as a ruler positioned within the sagittal plane. Thus this analysis yielded the x and y coordinates of each data point (in mm) on each digitized frame of the swallow sequence corrected for magnification and for the axis of the prox-

Time in Seconds

FIG. 3. Vertical vector of hyoid movement during l- and lo-ml swallows with and without use of the Mendelsohn maneuver. Hyoid position at time of sphincter opening is shown by vertical line at time 0. Position 0 on the vertical axis for each subject was the most inferior hyoid position observed in that subject during the entire study. Vertical hyoid excursion was significantly augmented at either volume by use of the maneuver. Effects of volitional effort and increased volume were additive in the sense that lo-ml swallows with the maneuver exhibited greater superior hyoid excursion than seen with lo-ml swallows without the maneuver, which were greater than l-ml swallows without the maneuver. Maximal hyoid elevation was significantly prolonged both by increasing volume of the swallow or by use of the maneuver. In fact, all individuals were able to prolong persistence of hyoid near the peak of its excursion well past the time of UES closure at either volume using the maneuver. Error bars shown are representative.

imal esophagus. Numerical data among swallows were averaged and expressed as a mean. Comparison among individuals was accomplished by transposing all x-y coordinates so that the minimum superior-inferior and anterior-posterior position achieved by the hyoid in the course of the entire study became position 0,O. Mean values among subjects were averaged and expressed as means t SE unless otherwise specified. Data between volumes or conditions were compared by paired testing and P values ~0.05 were regarded as significant. t

RESULTS

UES opening profile. As summarized in Table 1, the main effect of the Mendelsohn maneuver on the UES opening profile was to prolong the duration of sphincter opening. No significant effect was seen on the maximal sphincter diameter achieved. The integral of the opening diameter was significantly increased only at the lo-ml volume. Figure 1 depicts the timing and extent of UES opening during swallows of 1 and 10 ml with and without the Mendelsohn maneuver. Figure 1 subdivides sphincter opening into a component achieved as the horizontal coordinate of the anterior sphincter wall moved away from the horizontal coordinate of the anchor point (anterior opening), and a component achieved as the horizontal coordinate of the posterior sphincter wall moved closer to that of the anchor point (posterior opening). At

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CONTROL

TABLE

OF

UES

2. Effect of bolus volume and Mendelsohn maneuver on anterior hyoid excursion Bolus 1 ml

Maximal Anterior

G453

OPENING

anterior excursion, persistence, s

mm

15.6t1.4 0.40~0.04

Values are means t SE. Anterior persistence, time that 0.05 vs. 1 ml same condition (with or without maneuver).

Volume

and

Swallow

Condition 10 ml

1 ml Maneuver

16.8k1.6 0.54kO.09 the hyoid

remained

10 ml Maneuver

16.4k1.5 0.61t0.05* anterior

16.6t2.1 0.67&0.09*

to the coordinate

at which

UES

opening

occurred.

* P

Volitional augmentation of upper esophageal sphincter opening during swallowing.

Studies were done on eight normal subjects with synchronized videofluoroscopy and manometry to facilitate a biomechanical analysis of the extent and m...
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