Opening mechanisms of the human upper esophageal sphincter

IAN J. COOK, WYLIE J. DODDS, ROBERTO 0. DANTAS, BENSON MASSEY,

MARK K. KERN, IVAN M. LANG, JAMES G. BRASSEUR, AND WALTER J. HOGAN
Departments of Radiology, Medicine and Surgery, the Medical College of Wisconsin,
Milwaukee, Wisconsin 53226

COOK, IAN J., WYLIE J. DODDS, ROBERTO 0. DANTAS, hyoid movement that pulls open a relaxed or partially
BENSON MASSEY,MARK K. KERN, IVAN M. LANG, JAMES G. relaxed sphincter (2, 11, 14). Another possible mecha-
BRASSEUR, AND WALTER J. HOGAN. Opening mechanisms of nism of UES opening is intrabolus pressure forces, me-
the human upper esophageal sphincter. Am. J. Physiol. 257 diated by an oncoming swallowed bolus (20). Our aims
(Gastrointest. Liver Physiol. 20): G748-G759,1989.-Our goals in this study were to 1) quantify the variables of UES
in this study were to evaluate the mechanisms operative in
opening associated with swallows of different bolus vol-
swallow-associated opening of the upper esophageal sphincter
ume and 2) analyze the specific mechanisms that govern
(UES) and to determine the dynamics of fluid flow across the
sphincter. For this purpose, we obtained concurrent videofluo-
UES opening and transsphincteric flow.
rographic and manometric studies of 2- to 30-ml barium swal-
lows in 15 normal subjects. We found that the resting UES METHODS
high-pressure zone corresponded closely with the location of
the cricopharyngeus. The findings indicated that manometric We obtained concurrent videofluoroscopic and mano-
UES relaxation and anterior hyoid traction on the larynx metric studies of UES function during barium swallows
invariably preceded UES opening. With graded increases in in 15 healthy male volunteers with an average age of 29
bolus volume, progressive increases occurred in UES diameter, t 5 (SD) yr, range 18-38 yr. The study was approved bY
cross-sectional area, flow duration, and transsphincteric flow the Human Research Review Committee of the Medical
rate. Intrabolus pressure upstream to the UES and within the College of Wisconsin.
UES at its opening during transsphincteric flow of barium The subjects were positioned sitting on a stool, turned
remained within a narrow physiological range of 40 mmHg laterally to a vertical X-ray table top and held their head
up to a bolus volume of IO ml. With increases in bolus volume,
in a neutral position. Swallow sequences were recorded
anterior hyoid movement, UES relaxation, and UES opening
at 30 frames/s on video tape with a O.&in. Beta video
occurred sooner in the swallow sequence to accommodate the
early entry of large boluses into the pharynx. We conclude that recorder (Sony SLHF 900). Using either a 6- or g-in.
during swallowing 1) normal UES opening involves sphincter intensifier magnificati .on mode, we obtained concurrent
relaxation, anterior laryngeal traction, and intrabolus pressure, videofluoroscopic and manometric recordings (4-6 s du-
2) volume-dependent adaptive changes in UES dimension ac- ration) of swallows of high-density barium (250% wt/
commodate large bolus volumes and flow rates with minimal vol; E-Z-hd barium sulfate, E-Z-EM, Westbury, NY).
requirement for increases in upstream, or intrasphincteric, Swallow sequences were recorded for barium volumes of
intrabolus pressure or UES opening duration, and 3) volume- 0,2, 5, 10, 20, and 30 ml. Each bolus was delivered to the
dependent changes in UES dimensions as well as timing of mouth by a syringe. For “dry swallows” of 0 ml barium,
UES relaxation and opening indicate a sensory feedback mech- small amounts of saliva and residual barium from prior
anism that modulates some components of the swallow re- swallows passed into the esophagus. For each swallowed
sponse generated by the brain stem swallow centers.
volume, recordings over the pharynx and UES were made
in duplicate for both the lateral and posterior-anterior
pharyngoesophageal sphincter; laryngeal motion; hyoid motion
(P -A) projection s. A ruler with metal markers 3 cm apart,
recorded in the plane of the UES for both the P-A and
lateral projections, enabled distance correction for mag-
THE UPPER ESOPHAGEAL SPHINCTER (UES) normally nification. Recording of each swallow lasted 4-6 s. Fluo-
relaxes and opens during swallowing to permit passage roscopy time was ~2.5 min.
of ingested material into the esophagus but otherwise Manometry was done using several different trans-
remains closed except during belching and vomiting. ducer probes (Gaeltec, Medical Measurements, Hacken-
Although observations of swallow-induced UES opening sack, NJ) of 1%mm OD that contained two or three
are made commonly during radiographic examination, individual transducers spaced at l.5- or 3-cm intervals,
minimal quantitative information exists about the spe- respectively. Before manometry, the transducers were
cific mechanisms of deglutitive UES opening in humans balanced and calibrated in a water bath at 37°C. Trans-
(16, 23). Some investigators emphasize that the major ducer signals were processed through an eight-channel
mechanism associated with deglutitive UES opening is Beckman polygraph (Sensor Medics, Anaheim, CA) run
transient cessation of cricopharyngeal electrical activity at a speed of 100 mm/s. The videofluoroscopic and man-
(12, 20, 22). Other workers stress that actual UES open- ometric recordings were synchronized using a clock timer
ing is caused mainly by traction generated by anterior (Thalner Electronics, Ann Arbor, MI) that indicates
G748 0193-l&57/89 $1.50 Copyright 0 1989. the American Physiological Society

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.
 UES OPENING G749

digital time in hundredths of a second on each video C-clamp. Pressure values among pullthroughs and
frame and event markers at l-s intervals on the poly- among subjects were normalized by indexing peak pullth-
graph paper. rough pressure as 100%. Peak posterior pressure was
Subjects were divided into two groups. In group 1 (8 located 1.6 t 0.2 (SE) cm distal to the level of the vocal
subjects), we obtained magnified images (6-in. mode) of cords. The region of UES pressure ~50% of peak aver-
the pharynx and UES to quantify the features of UES aged 1.3 cm in length. Peak pressure for the anterior
opening. In group 2 (7 subjects), we used a low-magnifi- axial pressure profile was located 3-4 mm proximal to
cation mode (g-in. mode) to record concurrently the oral that of the posterior pressure peak. These results were
and pharyngeal phases of swallowing in order to deter- similar to our previous observation that the major por-
mine the precise timing of UES opening during the oral- tion of the functional UES high-pressure zone corre-
pharyngeal peristaltic sequence. sponds to the cricopharyngeus (19).
In the eight group 1 subjects, a single probe with three Analysis of deglutitive UES opening and transsphinc-
transducers spaced at 1.5-cm intervals was passed trans- teric barium flow was done on the video sequences by
nasally. After a UES pullthrough, the distal transducer obtaining the time and sequential sphincter diameter
was positioned within the proximal part of the sphincter. from each video frame. Measured distances were cor-
The transducers were oriented anteriorly and the probe rected for magnification. We defined UES opening as the
taped to the subject’s nose. instant that the barium bolus head reached the central
In the seven group 2 subjects we used two pressure zone of the UES. In some sequences, barium or air
probes. A probe with two transducers 3 cm apart was entered the proximal few millimeters of the sphincter
passed transnasally and positioned with the proximal 0.03- 0.09 s before opening of the central sphincter zone
transducer in the oropharynx at the level of the valleculae of maximal resting pressure. Sagittal sphincter diameter
and the distal transducer in the hypopharynx. The trans- was measured -1.6 cm distal to the cords. Time of UES
ducers faced anteriorly. A second probe with two trans- closure was taken as the instant that the barium column
ducers 3 cm apart was passed transorally and positioned disappeared from the sphincter zone. Transverse diam-
so that the distal transducer was located at the posterior eter of the UES was measured at the junction of the
tonsillar arch while the proximal transducer was located funnel-shaped pharynx with the tubular esophagus on
at the middle of the tongue. Lateral video images of the the P-A video projections. The P-A dimensions of the
mouth and pharynx were recorded for barium swallows UES were measured from the lateral video projections.
of 0, 2, 5, 10, and 20 ml. For bolus volumes X0 ml, the barium column in the
In the group 2 subjects we also determined the resting UES tended to slightly overlap the cervical spine, thereby
axial and radial UES pressure profile using a four-lumen indicating that the maximal P-A sphincter diameters
catheter that was passed transnasally. This catheter were parasagittal rather than midline. Indeed, regional
measured 2 x 4 mm OD. Lateral recording orifices were UES anatomy suggests that UES opening in the midline
located at the same level, 5 cm proximal to the end of would be restricted by the cervical spine and posterior
the assembly. The catheter lumens distal to each orifice bulge of the cricoid plate (7). To estimate midline UES
were occluded with metal plugs of different lengths that opening, we measured the change in distance of the
permitted fluoroscopic determination of recording orifice posterior tracheal wall (1.6 cm distal to the vocal cords)
orientation. During recordings, each catheter lumen was to the spine. Maximal UES area during transsphincteric
perfused with water at 0.5 ml/min (1). In each subject, flow for a given barium volume was estimated from the
three UES pullthroughs were done at 0.5 cm/s during maximal values of transverse, parasagittal, and midline
concurrent videofluoroscopic and manometric recording sphincter diameter. Approximations of cross-sectional
while the subject refrained from swallowing. sphincter area were calculated using mathematical
We measured a large number of variables including models for 1) an ellipse, ignoring the potential midline
the following: 1) resting location and pressure profile of narrowing and 2) a “barbell” configuration that attempts
the UES, 2) dimensions and timing of swallow-induced to correct for midline narrowing (15).
UES opening, 3) timing and magnitude of deglutitive To determine the superior and anterior components of
movements of the hyoid, larynx, and tongue, and 4) deglutitive hyoid movement, we measured the sequential
pressure profile across the UES during swallowing. Du- coordinates of the anterior-inferior hyoid margin. To
plicate measurements were averaged. measure superior laryngeal movement, we used the vocal
We determined pressure at 2-mm increments across cords as a marker (Fig. 1). Superior movement of the
the resting posterior and anterior UES pressure profile larynx is caused by hyoid elevation plus shortening of
and related axial location of the pressure profile to the the thyrohyoid muscles (7). Thyrohyoid shortening was
under surface of the vocal cords. On the videofluoroscopic determined by subtracting superior hyoid movement
recordings, this landmark was readily seen as a horizon- from superior laryngeal movement. We determined the
tal air-tissue interface. As shown in Fig. 1, the vocal time of initial movement of the tongue tip against the
cords attach posteriorly to the vocal process of each posterior surface of the maxillary incisors, an event that
arytenoid and mark the superior margin of the cricoid represents the onset of lingual peristalsis (6). This event
lamina. The cricopharyngeus muscle is a horizontal band was used as the temporal reference for all other events.
of muscle without a midline raphe that loops posteriorly We also measured the timing and magnitude of tongue
around the pharyngoesophageal junction so that its arms base movement. The onset of tongue base movement was
attach to the lateral margins of the cricoid lamina like a taken as the initial forward or backward movement of

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.
G750 UES OPENING

FIG. 1. Relationship of axial UES

UES Pressure
20
I copharyngeus
the tongue base, at a point just apart and above the
vallecula. Generally, the initial movement was forward.
From the manometric tracings, we determined the
relationship between the barium bolus tail and the peri-
staltic pressure wave, as peristalsis swept the bolus
through the mouth (group 2 subjects) and pharynx krouP
1 subjects). Resting UES pressure and deglutitive pres-
sures above, within, and below the sphincter were refer-
enced to atmospheric pressure. Manometric UES relax-
ation does not corn.mence until after the sphincter aP-
proaches or reaches the apogee of its superior degluti .tive
excursion (17, 19). We observed radiographically in the
group I subjects that the middle transducer, positioned
1.5 cm proximal to the upper margin of the resting UES,
lay within the central zone of the sphincter during its
deglutitive orad excursion. Therefore, we used the pres-
sure tracing of the middle transducer to measure mano-
metric UES relaxation. Measurements were made of the
timing of relaxation onset, complete relaxation to at-
mosphere as zero, and termination of complete relaxa-
tion, coincident with the arrival of pharyngeal peristaltic
pressure wave. We then calculated the duration of com-
plete UES relaxation. Also measured were the absolute
pressures above, within, and below the UES, coincident
with the onset of sphincter opening (defined as opening
pressure) and during the interval of maximal UES open-
ing (defined as flow pressure). We also calculated the
pressure difference across the UES during maximal
sphincter opening. Upstream intrabolus pressure was
taken from the hypopharynx 1 cm above the open UES
while downstream intrabolus pressure was measured
from the cervical esophagus 1 cm below the UES. Intra-
sphincteric pressure was measured from within the UES.
Inferences regarding the statistical significance of
pressure obtained by continuous pull-
throughs to laryngeal anatomy. Mano-
metric pressures were obtained in 8
healthy volunteers. The schematic of the
larynx shows the relationship of the cri-
coid (l), thyroid (2), and arytenoid (3),
epiglottic (4), and hyoid (5) cartilages.
Each vocal cord stretches between the
anterior thyroid cartilage and the vocal
process of the ipsilateral arytenoid. This
level marks the upper margin of the cri-
coid cartilage and was used as a marker
of cricoid location on the videoradi-
40 60 80% ographs. The cricopharyngeus (CP)
muscle attaches to the base plate of the
cricoid cartilage. The posterior wall of
the trachea (closed arrow) was used to
measure the trachea to spine distance.
Increases in this distance during swal-
lowing were taken as an estimate of UES
opening in the midline sagittal plane.
The epiglottis demarcates the superior
margin of the laryngeal vestibule and is
attached to the hyoid by the thyrohyoid
muscles. The averaged normalized data
for axial UES pressure in the posterior
and anterior radial orientations is
shown. Pressure profile was indexed to
the level of the vocal cords, which cor-
responds to the upper margin of the cri-
muscle.
I I I
changes in the timing or magnitude of peristaltic events
associated with different swallowed bolus volumes were
tested by analysis of variance for repeated measures.
Composite data in the text is given as means t SD unless
designated otherwise.
RESULTS
The sequence of events during the oral and pharyngeal
phases of swallowing for a lo-ml barium bolus is shown
in Fig. 2. At swallow initiation the bolus is held in the
anterior mouth with the tongue tip positioned against
the upper incisors. The oral cavity is sealed off from the
oropharynx by compression of the palate against the
posterior-superior aspect of the tongue. With swallowing,
the tongue moves superiorly against the palate, first its
tip and then the base, to propel the bolus in a peristaltic
fashion into the pharynx. During lingual peristalsis, the
point of glossopalatal contact imparts a V-configuration
to the tail of the barium bolus. At the onset of oral
peristalsis, the tongue base moves forward to accommo-
date bolus entry into the pharynx, and the hyoid, larynx,
and UES begin a superior and anterior excursion that
widen the pharynx and shorten the axial distance that
the bolus must travel. The UES segment opens gener-
ously during flow of the bolus into the esophagus. Trans-
sphincteric flow is completed during laryngeal descent
toward its resting position. During swallowing the larynx
is sealed by action of its intrinsic muscles and inversion
of the epiglottis.
Maximal transverse and P-A dimensions of the UES
during transsphincteric flow of different swallow bolus
volumes are given in Table 1. The maximal transverse
and P-A diameters both showed a progressive increase
for graded increases in bolus volume (P c 0.01). Also

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.
 UES OPENING G751

FIG. 2. Sequential images obtained during swallowing of a lo-ml barium bolus in a normal subject. A: bolus position
at the initiation of swallowing (time = 0). B: oral phase of swallowing (time = 0.01 s). Posterior movement of the
tongue against the palate imparts a V-configuration to the bolus tail and propels the bolus into the pharynx. The
hyoid and larynx begin to move superiorly and then forward. C: pharyngeal phase of swallowing (time = 0.03 s). The
tongue base moves forward to accommodate bolus entry in the pharynx. The central zone of the sphincter is located
distal to the vocal cords. The larynx is starting to close. D: pharyngeal phase (time = 0.6 s). The pharyngeal contraction
wave is in the oropharynx. The hyoid and larynx have reached their maximal anterior position, The UES is maximally
open while barium flows freely into the esophagus.

TABLE 1. Maximal dimensions and calculated UES area during transsphincteric flow
of different volumes of swallowed barium

Volume of Swallowed Barium, ml

2 5 10 20 30

Upper sphincter diameter, mm

Transverse 18.9k3.5 20.7k3.7 21.Ok3.7 22.3k3.3 29.943.4
Parasagittal 8.Ok1.3 ll.Ok1.9 11.8zk1.6 13.3k2.0 14.1k1.9
Midline 4.8k1.2 7.3k2.2 8.1k2.1 9.3rt1.8 9.5*2.5

Area, mm*
Ellipse 118k31 181+59 195+45 23OIfr31 264k46
Barbell 115f37 205k60 235+44 297524 332k33
Values are means + SD in mm of 8 group 1 subjects. Values for midlir le were estimated by anterior tracheal movement.

shown in Table 1 are the values for estimated maximal
midline UES diameter during transsphincteric flow of
different bolus volumes. These values were determined
by the maximal change in the posterior trachea-to-spine
distance during sphincter opening. The estimated mid-
line diameter during maximal UES opening was invari-
ably less than the maximal P-A diameter for all bolus
volumes (P < 0.05). For graded increases in bolus volume,
maximal midline UES diameter increased progressively
to a bolus volume of 10 ml (P < 0.01) and then increased
minimally for larger boluses. Calculated approximations
of the maximal area of UES opening for different bolus
volumes are given for both the ellipse and “barbell”
mathematical models (Fig. 3). Although the calculated
barbell-shaped areas were somewhat greater than the
calculated ellipse areas, both sets of approximations
showed a significant progressive increase in cross-sec-
tional UES area for graded increases in swallowed vol-

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.
G752 UES OPENING

mm* 0.17 s for boluses ~10 ml. As seen in Fig. 4 and in Table
350 2, graded increases in bolus volume resulted in a pro-
gressive increase in the duration of transsphincteric bar-
BARBELL ium flow and in UES relaxation (P < 0.01). Duration of
ELLIPSE complete manometric UES relaxation and flow did not
differ significantly for any bolus volume (Table 2).
250 Mean flow rate during UES opening was calculated by
dividing the volume of swallowed barium by the interval
UES
Area 200
of transsphincteric flow. For the 2-, 5, lo-, 20-, and 30-
ml barium boluses, respectively, the average transsphinc-
teric flow rates were the following: 5 t 0.3, 10 t 0.6, 18
150
t 1.8, 32 t 1.9, and 46 t 1.9 ml/s. Thus, as bolus volume
was increased from 2 to 30 ml, mean transsphincteric
flow rate increased nearly lo-fold.
The initiation of swallowing was heralded by a leading
complex of three closely related events: movement of the
tongue tip and tongue base and superior movement of
Volume of Swallowed Barium [ml] the hyoid. These initial events were followed in order by
FIG. 3. UES area during transsphincteric flow for graded increases
superior movement of the larynx (vocal cords), anterior
in swallowed bolus volume. Calculations (15 ) are shown for both the movement of the hyoid, onset of manometric UES relax-
ellipse and barbell shapes. Data from 8 subjects are plotted as mean t ation, anterior movement of larynx (posterior tracheal
SE. For both models, significant increases in UES area occurred as a wall), and UES opening. UES closure occurred coinci-
function of increases in bolus volume (P < 0.01).
dent with the arrival of pharyngeal peristaltic wave at
mm the sphincter. The onset of UES relaxation and subse-
I quent UES opening occurred as the hyoid and larynx
30 ml approached or reached the apogee of their superior ex-
cursions (Fig. 5). UES opening occurred shortly after the
hyoid and larynx began to move anteriorly. In -20% of
swallows, detectable gas penetrated the UES 0.03-0.06 s
before the barium bolus. This phenomenon was not
UES dependent on bolus volume.
Diameter Increases in bolus volume were associated with pro-
gressive increases in maximal superior hyoid and laryn-
geal movement (P c 0.01) (Fig. 6). Superior laryngeal
movement exceeded that of the hyoid. The shaded area
4- indicates the magnitude of thyrohyoid shortening. Max-
imal anterior movement of both the hyoid and larynx
2- also increased with bolus volume (P < 0.05). For each
bolus volume, magnitude of anterior laryngeal movement
was less than anterior hyoid movement.
0 .l -7 With respect to the onset of swallow-induced lingual
Time From UES Opening [see] peristalsis, anterior hyoid and laryngeal movement, as
FIG. 4. Sequential changes in posterior-anterior parasagittal UES well as UES opening, all moved forward significantly in
diameter during transsphincteric flow of barium boluses, range from time (P < 0.05) with increases in bolus volume (Table 3)
2-30 ml in volume. Curves plotted from mean values derived from 8 (Fig. 7). UES opening invariably occurred during anterior
subjects. Time 0 corresponds to the onset of detectable UES opening
laryngeal movement while closure occurred as the larynx
identified as penetration of the sphincter by the barium bolus. Initially,
the sphincter pops open to a diameter of -7 mm, regardless of bolus returned to its initial resting position. As illustrated in
volume; however, both the magnitude of maximal anterior-posterior Fig. 8, the forward temporal migration of UES relaxation
UES diameter and the duration of sphincter opening increased with and opening with respect to the onset of oral peristalsis
bolus volume (P < 0.05).
accounted for the bolus-dependent increases in the du-
ume (P c 0.01). For each type of calculation, maximal ration of UES opening and transsphincteric flow. As
UES area more than doubled as bolus volume increased bolus volume increased, the bolus head arrived at the
from 2 to 30 ml. UES sooner as a consequence of an increase in bolus
The sequential changes of P-A parasagittal UES di- length. Figure 9 shows that for each bolus volume, the
ameter during transsphincteric flow of different barium onset of manometric UES relaxation began before the
volumes are shown in Fig. 4. For each bolus volume, onset of anterior laryngeal movement, whereas complete
UES opening showed an abrupt increase to 6-7 mm UES relaxation and UES opening occurred during an-
followed by a slower progressive increase to reach a terior movement of the hyoid and larynx.
maximal diameter. Maximal P-A values of UES diameter The transit times of oral and pharyngeal peristalsis
were reached at 0.07 s after initial UES opening for the measured by videofluorography and manometry were
2-ml barium bolus, at 0.14 s for the 5-ml bolus, and at nearly identical (Table 4). Whereas increases in bolus

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.
 UES OPENING G753
TABLE 2. Duration of transsphincteric flow and complete UES relaxation for different volumes of swallowed barium

Volume of Swallowed Barium, ml

2 5 10 20 30

Trans-UES barium flow 0.41t0.03 0.4820.05 0.55&0.05 0.62t0.07 0.65t0.04

Complete UES relaxation 0.4620.14 0.50t0.14 0.56~0.12 0.6520.12 0.64t0.18
Values are means ~fc SD in s for 8 group 1 subjects. For each volume, a significant difference did not exist between the duration of UES
relaxation and transsphincteric barium flow.

mm
30-
fl Larynx

Superior
Movement z”-

FIG. 5. Relationship among hyoid

and laryngeal movement (superior and
anterior), UES relaxation, and UES
15 p Hyoid opening for a s-ml barium swallow.
Shown are pooled data from 8 subjects.
Anterior 101 Stippled bar shows period of UES open-
,,,,,, pG+ \.,.,,,.,. o
Movement ing and interval of transsphincteric bar-
5-
ium flow. Note that superior relocation
0J 0’ of the larynx precedes UES penetration
by the bolus. Anterior movement of the
hyoid and larynx precede sphincter
mmHg
100 @-\ opening.
I/ \\

Trans-UES Flow
UES
Pressure 50

I I I I I I I I I I I

0.2 I8C

volume were inversely related to the rate of oral transit up was coincident with the arrival of the bolus head at
(P < 0.05), bolus volume did not affect transit time in the hypopharyngeal recording site. The low-pressure pla-
the pharynx. Although increases in bolus volume were teau of intrabolus pressure corresponded to the interval
associated with earlier UES closure, this trend did not during which the bolus flowed past the transducer.
reach statistical significance, except in group 2 (Table Upstream intrabolus pressure at the onset of UES
3) . opening was invariably low, e.g., 6 t 1.8 mmHg for a lo-
Swallowed bolus volume did not affect the interval ml swallowed bolus, but was directly dependent on bolus
between the onset of manometric UES relaxation (in- volume (Fig. 11). In contrast, at the instant of UES
stant the pressure turns downward) and complete opening, downstream pressure in the cervical esophagus
sphincter relaxation (decreases to zero pressure) or the was slightly negative at about 6-8 mmHg and was inde-
interval between complete UES relaxation and the onset pendent of bolus volume (Table 5). Upstream bolus pres-
of transsphincteric bolus flow (Figs. 8 and 9). For a &ml sure during transsphincteric flow was l-5 mmHg greater
bolus, these intervals were 0.13 t 0.01 s and 0.05 t 0.01 than opening pressure and was directly related to bolus
s, respectively, in the eight group 1 subjects. volume. Intrasphincteric pressure during flow also in-
Detailed analysis of manometric tracings established creased with bolus volume (Fig. 8; Table 5). During
the interrelationship between intraluminal pressure and transsphincteric flow, intrasphincter pressure was -3
transsphincteric flow during swallowing. Resting pres- mmHg less than upstream bolus pressure, while down-
sure in the pharynx was zero relative to atmosphere. stream bolus pressure in the cervical esophagus was 3-
With a dry swallow, a slightly negative pressure of 2-4 10 mmHg lower than hypopharyngeal pressure. The
mmHg commonly developed before the arrival of the downstream pressure was slightly negative for the Z-ml
peristaltic contraction wave. For wet swallows, a small bolus but increased to a value of 15.3 mmHg for the 30-
step up of positive hypopharyngeal pressure preceded the ml bolus. The upstream-to-downstream pressure differ-
peristaltic pressure wave (Fig. 10). The onset of this step ence across the UES during sphincter opening was al-

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.
G754 UES OPENING
mm
xl-
recordings of barium swallows of graded barium volumes.
Larynx
The study findings indicate that 1) the cricopharyngeus
is the major contractile element of the UES and exhibits
25 - manometric relaxation just prior to sphincter opening;
Thyrohyoid
2) UES traction by anterior deglutitive movement of the
Shortening
hyoid and larynx initiates normal sphincter opening and
is the predominant mechanism that determines UES
Superior zO- opening for dry swallows and wet swallows of low volume;
Movement Hyoid
3) for swallowed volumes 25 ml, pressure forces within
15- the bolus contribute substantially to the magnitude of
UES opening; 4) graded increases in swallowed bolus
volume cause adaptive increases of UES dimension that
decrease flow resistance, thereby allowing a substantial
increase in flow rate while maintaining a short duration
of transsphincteric flow with only minimal increases in
intrabolus pressure, and 5) modulation of swallowing by
change in bolus volume exhibits adaptive accommoda-
tion by the pharynx and UES, whereas peristaltic prop-
agation in the pharynx remains stereotyped and con-
,&--ii Hyoid stant.
For our study, we selected anatomical markers that
would satisfactorily identify UES location during deglu-
Larynx
tition. Manometric pullthroughs across the UES during
videofluoroscopic recordings confirmed previous obser-
vations that the central UES high-pressure zone corre-
sponds to the cricopharyngeus (18, 19). The inferior
aspect of the vocal cords serves as a reliable radiographic
marker for identifying the upper margin of the cricoid,
which is located about 1-2 cm cephalad to the peak
resting UES pressure. During swallowing, the hyoid and
Swallowed Bolus Volume (ml)
FIG. 6. Maximalhyoid and laryngeal movements during swallowing
larynx make a pronounced superior and anterior excur-
of 2- to 30-ml barium boluses. Composite data for 8 subjects is plotted sion. We quantified these movements with temporal
as mean values. Superior and anterior movement of the hyoid and plots of the location of the hyoid, vocal cords, and pos-
larynx all show significant increases with graded increases in bolus terior tracheal wall. Anterior tracheal movement was
volume (P < 0.05). Shaded area indicates the contribution of thyrohyoid
judged to approximate sagittal UES opening in the mid-
shortening to laryngeal elevation.
line. To measure manometric UES relaxation, we posi-
ways positive (Table 5) but decreased with increases in tioned a transducer 1.5 cm above the proximal margin of
bolus volume (P < 0.01). This latter finding was associ- the resting UES. During its deglutitive excursion, the
ated with a volume-dependent pressure increase within UES rose to the level of the transducer. Manometric
the cervical esophagus. UES relaxation and sphincter opening occur while the
sphincter approaches or reaches the apogee of its deglu-
DISCUSSION
titive orad excursion (17, 19).
Complete manometric sphincter relaxation as well as
The aim of this investigation was to determine and the onset of anterior hyoid laryngeal movement invari-
quantify the mechanisms that contribute to deglutitive ably preceded UES opening. UES opening was signaled
UES opening in normal subjects. For this purpose, we by penetration of the sphincter segment by the head of
utilized concurrent videofluoroscopic and manometric the barium column. Generally, the barium penetration

TABLE 3. Temporal relationship of onset of hyoid and laryngeal movement, UES opening,
and closure to initiation of swallow-induced oral peristalsis

Swallowed Interval From Onset of Lingual Peristalsis, s Duration of

Volume, Anterior Anterior UES UES UES
ml opening closure Opening
hyoid larynx

0 0.56t0.09 0.69t0.08 0.84t0.07 1.14t0.07 0.3OkO.02

2 0.45t0.09 0.65t0.08 0.73kO.07 1.08t0.07 0.38kO.01
5 0.35kO.06 0.54zkO.06 0.61t0.06 1.07&0,06 0.4620.02
10 0.20t0.05 0.36t0.04 0.44t0.04 0.93kO.04 0.49t0.02
20 0.18t0.03 0.29t0.04 0.36~10.03 0.91kO.03 0.55kO.02
Values are means -+ SE in s and are composite data from 7 group 2 subjects. All columns showed a direct correlation with bolus volume (P <
0.001).

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.
 UES OPENING G755

FIG. 7. Group mean data in group 1

patients showing the relationship be-
tween UES opening and anterior move-
Anterior 6- ment of the larynx for 2- to 20-ml bolus
Laryngeal volumes. UES opening is indicated by
Movement open circles; closure is indicated by the
closed circles. Plots demonstrate that
4- maximal anterior hyoid movement
creases in magnitude and moves leftward
in-

in time as bolus volume increases. For

all volumes, UES opening invariably oc-
curred after the onset of anterior laryn-
2- geal movement but before peak move-
ment.

I ,
0 -,
0 .2 .4 .6 .8 1.0 1.2 1.4
Time in Seconds

accurately defined the instant of UES opening, but oc-

casionally air preceded the bolus head by 0.03-0.06 s. In
either case, however, sphincter opening was always pre-
I ceded by complete manometric UES relaxation. We judge
mmHg
I that manometric UES relaxation likely reflects cessation
OS fr
of cricopharyngeal electromyogram activity, which is
transiently switched off during swallowing (2, 10). The
onset of manometric UES relaxation occurred prior to
appreciable anterior laryngeal movement and thus does
not appear to be caused by traction that might reduce
UES pressure without true sphincter relaxation (2). Our
data support the proposal that UES relaxation is a
prerequisite for normal sphincter opening (21).
The second event associated with normal deglutitive
UES opening is brisk anterior movement of the larynx.
This forward laryngeal movement is generated by ante-
rior movement of the hyoid during its superior excursion
and to a lesser degree by thyrohyoid shortening. The
timing of anterior hyoid and laryngeal movement support
the conclusion that anterior traction is the predominant
force responsible for the initiation of deglutitive UES
opening as the sphincter snaps open. This initial opening
of -7 mm was independent of bolus volume. Further,
FIG. 8. Example from a single normal group 1 subject of the effect sphincter opening elicited by anterior laryngeal move-
of increases in bolus volume on the timing of UES relaxation and ment occurs during a dry swallow when a fluid bolus is
opening during the swallowing sequence. DS, dry swallow. Initial pres- negligible. This conclusion is also supported by neural
sure hump on each tracing is caused by superior movement of the
unrelaxed UES to the level of the transducer positioned 1.5 cm proximal
stimulation studies of the geniohyoid muscle in the opos-
to the rest position of the sphincter. Onset of UES relaxation is defined sum (2) and dog (unpublished observations). During
as the instant the pressure hump turns downward. Arrows indicate the anterior distraction of the cricoid, the posterior portion
onset (*) and peak (+) of anterior laryngeal movement. Horizontal of the C-shaped cricopharyngeus is normally prevented
black bars indicate UES opening and interval of transsphincteric flow
of barium. Vertical dashed line indicates UES closure. The manometric
from moving forward by the prevertebral fascia (7). This
tracings of UES relaxations are aligned, or indexed, to the instant of fascia allows the pharyngeal musculature to move freely
UES closure because analysis of data from group 2 subjects indicated in the longitudinal direction while allowing negligible
that the timing of UES closure in relation to the onset of the oral phase anterior movement. During swallowing, shortening of
of swallowing was not significantly affected by bolus volume. In this
example, the onset of UES relaxation, anterior laryngeal movement,
the pharyngeal elevator muscles (e.g., stylopharyngeus)
and UES opening all migrate forward in the swallow sequence as a also elevate the larynx (7) and serve to widen transverse
function of increases in swallowed bolus volume. UES diameter. Transverse UES widening occurs because

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.
G756 UES OPENING
Tongue Tip
at Incisors [SL-P]*,[SH-P]*

FIG. 9. Composite data from 8 group 1 sub-

jects showing the effect of swallowed bolus vol-
ume on the timing of anterior hyoid and laryn-
geal movement, UES relaxation, and UES
opening within the swallow sequence. Data
2 ml from magnified images of the pharynx in group
1 subjects is plotted using the incisor to UES
opening intervals measured from group 2 sub-
jects in whom UES relaxation was not recorded.
Dotted curves represent manometric profile of
5 ml UES relaxation. With increases in bolus vol-
ume, the onset and peaks of anterior hyoid and
‘~-.............-...........~......~. laryngeal movement as well as UES relaxation
and opening shift to the left so that in effect
I
Tg St&~ fL-0 AH-0 AL-0 AL;P qH-P -56s ,/-“ ‘j, the sphincter opens earlier. TB, initial move-
I ,L.-t;y ,.‘..h: . ,.
I w.ma = 88. ment of tongue base; SH-0, superior hyoid
10 ml “‘-m ‘. ‘. ,I C ,@\s
‘. ‘. : movement; SL-0, onset superior laryngeal
movement; AH-O, onset anterior hyoid move-
ment; AL-O, onset anterior laryngeal move-
ment; AL-P, peak anterior laryngeal move-
ment; AH-P, peak anterior hyoid movement;
SL-P, peak superior laryngeal movement; SH-
P, peak superior hyoid movement. Horizontal
shaded bars indicate duration of UES opening
TB SH-0 SL-0 for liquid boluses. Duration of opening is shown
30 ml above the bar. Duration also judged for UES
opening for a dry swallow (DS). The later was
identified when a thin coating of barium out-
lined the mucosa of the pharynx and UES.
I I I I I I I I I I
-0.6 -0.4 -0.2 0 0.2 0.4 0.6 0.8 1.0 1.2
Time in Seconds

TABLE 4. Comparison of oral-pharyngeal peristaltic transit times measured

by videoradiography and intraluminal manometry

Swallowed Mid Tongue + Fauces Fauces + Hypopharynx Fauces -+ UES

Volume,
ml Video Manometry Video Manometry Video Manometry

2 0.20t0.05 0.26t0.06 0.56t0.04 0.53t0.05 0.73t0.06 0.74t0.06

5 0.12t0.02 0.18t0.03 0.56kO.03 0.52t0.01 0.60t0.02 0.70t0.06
10 0.12rto.02 0.13t0.03 0.50t0.01 0.53t0.02 0.60t0.02 0.64t0.04
20 0.10~0.01 0.10t0.02 0.46AO.01 0.50~0.04 0.58t0.03 0.60~0.06
Values are means t SE in s from 7 group 2 subjects.

the superior attachment of the stylopharyngeus is lateral maximal UES diameter. The contribution of intrabolus
to its insertion on the hypopharynx. Orad excursion of pressure to the magnitude of UES opening was particu-
the larynx during swallowing not only facilitates opening larly evident for bolus volumes of 10 and 20 ml, which
of the UES but also enlarges the pharynx to receive a are within the upper physiological range of normal. For
swallowed bolus, engulfs the bolus, shortens the distance such bolus volumes, traction and intrabolus pressure may
the bolus must travel, and protects the larynx against act in concert for 0.1-0.25 s to open the sphincter further
aspiration (11). The hyoid and larynx elevation achieved after its initial opening. After 0.1-0.2 s, when traction
during swallowing in adults transiently recapitulates the becomes maximal, however, further increases in UES
high resting position of these structures that exists dur- diameter are accounted for only by intrabolus pressure
ing infancy (22). alone, which acts as a radially distending force within
Pressure forces imparted by a swallowed bolus also the sphincter lumen.
contribute to UES opening. Although intrabolus pressure Intrabolus opening pressure 1 cm proximal to the UES
is not needed for the initiation of UES opening, it con- at the instant of sphincter opening and during transs-
tributes to the magnitude of sphincter opening for bolus phincter flow are normally within a low range of O-20
volumes >5 ml in size. For bolus volumes ~2 ml, intra- mmHg. The low deglutitive pressure difference between
luminal bolus pressure at the instant of UES opening the bolus and trachea has little tendency to cause aspi-
was virtually zero (Fig. 11)) and minimal increase in ration. An important distinction exists between intra-
sagittal UES diameter occurred after that of the initial bolus pressure, which is normally low, and the high
opening (Fig. 4). For bolus volumes >5 ml, however, contractile pressure of X00 mmHg (9) within the col-
modest progressive increases occurred in opening pres- lapsed segment of the hypopharyngeal peristaltic con-
sure, flow pressure (above and within the sphincter), and traction wave. Pressures within the bolus and trailing

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.
 UES OPENING G757

mmHg
a0

23-L I
FIG. 10. Example of intrabolus pres-
mmHg sure -1 cm upstream from the UES prior
to sphincter opening and during transs-
phincteric flow. Tracings shown for 2-,
above 5, lo-, 20- and 30-ml barium swallows.
:r: ,j _ mJ-/ Black horizontal bars indicate period of
0.1 t
\ UES opening and transsphincteric flow.

I
i
Hatched area under each pressure trac-
ing indicates interval during which the

d
I bolus flowed by the transducer. The up-
UES I stroke onset of the peristaltic pressure
I
wave corresponded to the disappearance
of the bolus tail.

UES Flow !
I

lntrabolus
Pressure
Proximal
to UES FIG. 11. Relationship of upstream opening pressure and
flow pressure to swallowed bolus volume. Composite data
from 8 group 1 subjects. Bars plotted as means; black bars
indicate SE. Mean value is given at top of each bar.

2 5 10 20 30
Swallowed Bolus Volume (ml)

TABLE 5. Intrabolus pressure and pressure across the UES associated

with sphincter opening for different volumes of swallowed barium

Bolus Vol- Pressure Onset UES Opening Bolus Pressure at Maximal UES Opening
ume, ml Upstream Downstream Upstream UES Downstream Difference

0 O.lrtl.0 -8.2k2.4 5.6t4.6 2.1t2.8 -4.722.0 10.3t5.8

2 0.5t0.6 -7.8t2.4 5.5t2.3 2.1t5.3 -2.lk2.2 7.6t3.9
5 4.4H.8 -6.6k2.2 7.9k2.1 3.8t4.4 2.6k2.5 5.3k4.3
10 6.Ok1.8 -7.2k3.3 7.8t2.1 5.1zk4.0 2.4t3.0 5.4t4.7
20 lO.Ok2.6 -8.4k3.1 13.8t2.1 13.8k5.2 11.3k2.1 2.5t2.8
30 17.0rt5.4 -7.8t3.4 18.1t3.5 18.1t7.7 15.3k2.6 2.826.5
Values are means t SE for 8’group 1 subjects. Upstream, 1 cm proximal to UES; downstream, 1 cm distal to UES.

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.
G758 UES OPENING

contracting segment are within two distinct domains measurements, however, merit further study.
(5a). The leading edge between these two domains is the With swallowing, transient negative subatmospheric
upstroke of the peristaltic pressure complex that imparts pressures occurred in the hypopharynx, UES and cervical
a V-configuration to the bolus tail (25, 26). Hence, peri- esophagus. We attribute these negative pressures to the
staltic transit time may be determined accurately by pharyngeal expansion and elongation of the cervical
either videofluoroscopy or intraluminal manometry. Our esophagus that occur during swallowing. Our observa-
data suggest that normally a swallowed barium bolus tions support the notion that the resultant suction forces
does not fall through the pharynx by gravity (5a, 8, 24) may assist bolus transport through the pharynx (3, 4)
but rather is mainly pushed by peristalsis. but only for a short interval early in the swallow se-
Approximations of maximal cross-sectional UES area quence. Transient-negative pressures in the hypophar-
for different bolus volumes were calculated for elliptical ynx were observed only for dry or 2-ml swallows, prob-
and barbell shapes. The barbell approximation of the ably because the arrival of a larger bolus masks the
open UES likely corresponds more closely to the actual phenomenon. The transient-negative deglutitive pres-
area because the central zone of the open UES is flat- sures in the cervical esophagus were bolus independent.
tened by the cricoid plate and cervical spine (7). For They occurred during superior movement of the closed
larger bolus volumes, increases in sphincter area seem to sphincter and disappeared with the onset of sphincter
occur mainly in the lateral lobes of the sphincter because opening. The transient-negative pressures within the
the sagittal trachea-to-spine distance reached a maxi- UES we attribute to hyoid traction on the sphincter.
mum value for a lo-ml bolus, whereas the maximum This negative pressure disappears concurrent with UES
parasagittal diameter of the barium column increased opening.
progressively for bolus volumes up to 30 ml. Cross- With increases in swallowed bolus volume, the onsets
sectional UES areas calculated by the ellipsoid method of anterior hyoid and laryngeal movement, manometric
showed a close correlation to those calculated by the UES relaxation, and UES opening all moved forward in
barbell method, thereby suggesting that the ellipsoid time with respect to the initiation of oral peristalsis. Oral
method gives a reasonable approximation. transit decreased with increases in bolus volume. In
When swallowed bolus volume was increased from 2 contrast, the timing and velocity of pharyngeal peristalsis
to 30 ml, mean flow rate through the pharynx and across and the relationship of pharyngeal peristalsis to UES
the sphincter increased -IO-fold, whereas the velocity of closure were not affected by bolus volume. Because larger
pharyngeal peristalsis remained unchanged. Flow dura- bolus volumes cause earlier laryngeal movement and
tion and intrabolus pressure showed only modest change. UES opening while having minimal effect on the timing
Thus the substantial increase in flow rate was achieved of sphincter closure, increases in bolus volume caused
primarily through an increase in UES cross-sectional increments in the duration of manometric UES relaxa-
area. The modest volume-dependent increase in intra- tion and opening.
bolus pressure immediately above and within the UES The finding that bolus volume affects the timing and
during transsphincteric bolus flow serves as a radially magnitude of many events associated with swallowing
distending force to increase the cross-sectional area of has implications about the control mechanism that exe-
the hypopharynx and UES. cutes swallowing. Some evidence from canine studies
The pressure difference between intrabolus pressure suggests that the pharyngeal and late oral phase of
in the hypopharynx (1 cm proximal to the UES) and in swallowing are a stereotyped patterned response, unaf-
the cervical esophagus (1 cm distal to the UES) was fected by the type of swallowing, programmed by the
found to decrease as bolus volume was increased from 2 medullary swallowing centers (13, 22). In contrast, data
to 30 ml (Table 5). The implications of this decrease from rabbits suggests that duration of pharyngeal con-
merit analysis. The pressure difference across a segment strictor responses is altered by the type of swallowing
such as the open UES is associated with two additive (5). Our data show that the timing, duration, and mag-
effects: 1) a decrease in pressure due to frictional losses nitude of many deglutitive events are modulated by the
(Poiseuille’s law) and 2) a difference in pressure associ- volume of a swallowed liquid bolus, albeit velocity of
ated with a difference in cross-sectional area at the two pharyngeal peristalsis was not affected. Bolus modula-
measurement ports (Bernoulli effect). Estimates of fric- tion of hyoid movement and other events begins while
tional loss in pressure account for negligible pressure the bolus is still in the mouth. At present, however, it is
drop across the UES because UES area increases so not clear whether bolus modulation of deglutitive events
substantially with increase in bolus volume. Therefore, occurs during swallowing or whether the central nervous
the measured decreases in pressure differences across the system modification of swallowing is modified before
UES as bolus volume was increased from 2 to 30 ml are swallow initiation. We speculate that modification orig-
likely due to changes in cross-sectional area in the hy- inates from mechanoreceptors in the tongue that are
popharynx and cervical esophagus such as that the rel- deformed by an intraoral bolus.
ative area of the hypopharynx increases more than that To summarize, our study findings indicate that normal
of the cervical esophagus. The dimensions of both these swallow-induced UES opening is governed by four fac-
areas increased with increases in bolus volume but were tors: 1) relaxation of resting UES tone, 2) traction caused
not quantified due to the problem of simulating hypo- by anterior laryngeal movement and pharyngeal short-
pharyngeal geometry, and the cervical esophagus was ening, 3) pressure forces generated within the oncoming
often cut off on the videofluoroscopic recordings. These swallowed bolus, and 4) low compliance of the relaxed

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.
 UES OPENING G759
UES that allows the cricopharyngeus to be easily 7. CURTIS, D. J. Laryngeal dynamics. CRC Crit. Rev. Diugn. Imug.
18: 29-80,1982.
stretched open by traction and low intrabolus pressure. 8. CURTIS, D. J., AND D. F. CRUESS. Videofluoroscopic identification
Although UES relaxation is determined by transient of two types of swallowing. Radiology 152: 305-308,1984.
central inhibition of resting central nervous system cri- 9. DODDS, W. J., W. J. HOGAN, S. B. LYDON, E. T. STEWART, J. J.
copharyngeal stimulation (IZ), physical opening of the STEF, AND R. C. ARNDORFER. Quantitation of pharyngeal motor
function in normal human subjects. J. Appl. Physiol. 39: 692-696,
sphincter occurs passively by traction and intrabolus 1975.
pressure that act on the relaxed sphincter. 10. DODDS, W. J., P. J. KAHRILAS, J. DENT, AND W. J. HOGAN.
Clinical abnormalities of UES opening may be related Considerations about pharyngeal manometry. Dysphugiu 1: 209-
to impaired UES relaxation, diminished traction caused 214,1987.
by feeble laryngeal movement, impaired pharyngeal per- 11. DODDS, W. J., K. M. MAN, I. J. COOK, P. J. KAHRILAS, E. T.
STEWART, AND M. K. KERN. Influence of bolus volume on swallow-
istalsis, or reduced compliance of the UES musculature. induced hyoid movement in normal subjects. Am. J. Roentgenol.
Functionally, these abnormalities, either singularly or in 150: 1307-1309,1988.
combination, may lead to absent or incomplete UES 12. DOTY, R. W., AND J. D. BOSMA. An electromyographic analysis of
opening, laryngeal aspiration, and increased residual in reflex deglutition. J. Neurophysiol. 19: 44-60, 1956.
13. DOTY, R. W. Neural organization of deglutition. In: Handbook of
the pharynx. Such patients generally complain of dys- Physiology. Alimentary Canal. Washington, DC: Am. Physiol. Sot.,
phagia or choking. sect. 6, vol. 4, 1968, p. 1861-1902.
14. EKBERG, 0. The normal movements of the hyoid bone during
This work was supported, in part, by National Institutes of Health swallow. Inuest. Rudiol. 21: 408-410, 1986.
15. EVES, H. Curves and surfaces. In: CRC Standard Muthemuticul
Grant ROl-DK-25731 and by the General Clinical Research Center
Tables, edited by W. H. Beyer. Boca Raton, FL: CRC, 1981, p. 271.
Grant RR-00058.
16. GOYAL, R. K. Disorders of the cricopharyngeus muscle. Otoluryngol.
Address for reprints requests: W. J. Dodds, Professor of Radiology
Clin. N. Am. 17: 115-130, 1984.
and Medicine, Medical College of Wisconsin, Dept. of Radiology,
17. ISBERG, A., M. E. NILSSON, AND H. SCHIRATZKI. The upper
Froedtert Memorial Lutheran Hospital, 9200 West Wisconsin Ave.,
esophageal sphincter during normal deglutition. Actu Rudiol. Diugn.
Milwaukee, WI 53226.
23: 563-568,1985.
Received 30 January 1989; accepted in final form 20 June 1989. 18. KAHRILAS, P. J., J. DENT, W. J. DODDS, W. J. HOGAN, AND R. C.
ARNDORFER. A method for continuous monitoring of upper esoph-
ageal sphincter pressure. Dig. Dis. Sci. 32: 121-128, 1987.
REFERENCES 19. KAHRILAS, P. J., W. J. DODDS, J. DENT, J. A. LOGEMANN, AND
R. SHAKER. Upper esophageal sphincter function during degluti-
1. ARNDORFER, R. C., J. J. STEF, W. J. DODDS, H. H. LINEHAN, AND tion. Gustroenterology 95: 52-62, 1988.
W. J. HOGAN. Improved infusion system for intraluminal esopha- 20. LARSON, C. Neurophysiology of speech and swallowing. Sem.
geal manometry. Gustroenterology 73: 23-27, 1977. Speech Language 6: 275-291,1985.
2. ASOH, R., AND R. K. GOYAL. Manometry and electromyography of 21. LUND, W. S. A study of the cricopharyngeal sphincter in man and
the upper esophageal sphincter in the opossum. Gustroenterology in the dog. Ann. R. Coll. Surg. Engl. 37: 225-246, 1965.
74: 514-520,1978. 22. MILLER, A. J. Deglutition. Physiol. Reu. 62: 129-184, 1982.
3. ATKINSON, M., P. KRAMER, S. M. WYMAN, AND F. J. INGELFIN- 23. MILLER, A. J. Neurophysiological basis of swallowing. Dysphugiu
GER. Dynamics of swallowing. I. Normal pharyngeal mechanisms. 1: 91-100,1986.
J. Clin. Inuest. 36: 581-595, 1957. 24. MOSHER, H. P. X-ray study of movements of the tongue, epiglottis
4. BARCLAY, A. E. The normal mechanism of swallowing. Br. J. and hyoid bone in swallowing, followed by a discussion of difficulty
Radiol. 3: 534-546, 1930. in swallowing caused by retropharyngeal diverticulum, post-cricoid
5. BASMAJIAN, J. V., AND C. R. DUTTA. Electromyography of the webs and exostoses of cervical vertebrae. Luryngoscope 37: 235- .
pharyngeal constrictors and soft palate in rabbits. Anut. Rec. 139: 262, 1927.
443-449,196l. 25. SHAKER, R., I. J. S. COOK, W. J. DODDS, AND W. J. HOGAN.
sa.BRASSEUR, J. G. A fluid mechanical perspective on esophageal Pressure-flow dynamics of the oral phase of swallowing. Dysphugiu
bolus transport. Dysphugia 2: 32-39, 1987. 3: 79-84,1988.
6. COOK, I. J., W. J. DODDS, R. 0. DANTAS, M. K. KERN, B. T. 26. SOKOL, E. M., P. HEITMANN, B. S. WOLF, AND B. R. COHEN.
MASSEY, R. SHAKER, AND W. J. HOGAN. Timing of videofluoros- Simultaneous cineradiographic and manometric study of the phar-
topic, manometric events and bolus transit during the oral and ynx, hypopharynx and cervical esophagus. Gustroenterology 51:
pharyngeal phases of swallowing. Dysphugia. In press. 960-974,1966.

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 1, 2018.

Copyright © 1989 American Physiological Society. All rights reserved.