Pharyngeal manometry

and upper esophageal sphincter in humans

JUNE A. CASTELL, CHRISTINE BOAG DALTON, AND DONALD 0. CASTELL Gastroenterology Section, Bowman Gray School of Medicine, Wake Forest University, Winston-Salem, North Carolina 27103

CASTELL,JUNE A., CHRISTINE BOAGDALTON,ANDDONALD 0. CASTELL. Pharyngeal and upper esophageal sphincter manometry in humans. Am. J. Physiol. 258 (Gastrointest. Liver Physiol. 21): G173-G178, 1990.-Manometric studies of pharyngeal-upper esophageal sphincter (UES) coordination during swallowing have proven difficult. Asymmetry of the UES makes pressure measurements with a single, unoriented transducer suspect. Perfused systems lack the necessary response rate for measuring peak pharyngeal contraction pressures. Precise quantification of the coordination of pharyngeal contractions and UES relaxations during swallowing is difficult because of rapid pressure changes. We tested a modified solid-state transducer that measures pressures over 360”. This transducer was placed in the proximal UES with a second, single transducer 5 cm proximal. Data were collected and analyzed with an Apple IIe microcomputer. A computer program was developed to measure nine timing sequences, UES resting pressure, nadir of UES relaxation, and pharyngeal contraction pressures. We studied 21 volunteers with six swallows each for dry, 5, 10, and 20 ml of water. Dry swallows differed significantly (P c 0.05) from wet (5 ml). All timing sequences became progressively longer with increasing bolus size. Residual pressures were unchanged. Timing sequences were also measured for wet (5 ml) and dry swallows in seven volunteers using a Dent sleeve and single perfused orifice in the UES; no differences were seen. swallow

coordination;

computer

analysis;

bolus effect

SWALLOWING, the transfer of food or liquid from the oral cavity to the upper esophagus is achieved by centrally controlled reflex muscle activity of the tongue, pharynx, and larynx and involves both voluntary and involuntary skeletal muscle activity. The so-called pharyngeal phase of swallowing involves reflex (involuntary) actions of swallowing. It is during this phase of swallowing that the bolus is transferred from the back of the tongue through the upper esophageal sphincter (UES) to the upper esophagus. This action takes approximately 1 s (1). These actions have been shown recently to result in orad movement of the UES during swallowing (6) Specific characteristics of the pressure phenomena of the human pharynx and UES remain somewhat of a mystery. Isolated reports of the UES and pharyngeal pressures have appeared, but these have been hampered by problems with equipment design and studies with limited numbers of normal individuals. Many conclusions have been drawn regarding potential abnormalities IN NORMAL

0193-1857/90

$1.50 Copyright

of the pharyngeal-UES contraction profile based on these inadequate data. There are a number of reasons for the deficiency in studies of the manometric characteristics of this area including 1) the unique anatomic configuration of the UES, 2) questions about proper catheter design related to this anatomic configuration, 3) inadequacy of perfused catheters to provide quantitative measures of pharyngeal contractions, 4) concerns about axial movement of the UES during swallowing, 5) discrepancies in UES pressure due to the speed of catheter withdrawal, and 6) the difficulty of assessingsmall changes due to the speed with which the events take place. The purpose of the present study was to address these deficiencies and develop a system for the accurate recording and objective analysis of manometric studies of the pharyngeal-UES complex. MATERIALS

AND METHODS

Subjects. Manometric studies with intraluminal, solidstate transducers were performed in 21 normal volunteers (16 males, 5 females; mean age 32.8 yr). Dent sleeve and single orifice perfused catheter studies were performed in seven human volunteers (5 males, 2 females; mean age 39 yr). After informed consent was obtained, subjects were studied after a 6-h fast as described below. Esophageal manometry. Esophageal manometry was performed with a complete intraluminal transducer system. In the system used, the catheter is round and contains two transducer assemblies as shown in Fig. 1. The more proximal transducer is a standard Konigsberg microtransducer with a single recording site. A proximal portion of the tube is marked so the orientation of the transducer can be identified. Five centimeters distal to this transducer is a second transducer assembly consisting of a glycerin-filled Silastic circumferential annulus, which surrounds a single miniature titanium strain gauge in contact with the glycerin. The chamber surrounding the transducer is filled with 0.025 ml of glycerin, producing an extremely noncompliant system. Studies by the manufacturer (Konigsberg Instruments, Pasadena, CA) reveal low hysteresis (0.40% of full scale) and low volumetric compliance (7 x lo-" mm”/mmHg). In our laboratory, this transducer had a pressure rise rate ~2,000 mmHg/s. This transducer assembly provided a measure of circumferential sphincter squeeze. The unique design of

0 1990 the American

Physiological

Society

G173

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on October 23, 2018. Copyright © 1990 American Physiological Society. All rights reserved.

G174

PHARYNGEAL-UES

this transducer permits accurate measurement of average sphincter pressure regardless of orientation and eliminates concerns about the radial asymmetry of the UES (9). This was accomplished by exposing the transducer’s pressure-sensing diaphragm to the fluid-filled annulus whose silicon rubber membrane made direct contact with the sphincter wall. The pressure exerted by the sphincter was transmitted through the contained fluid to the transducer. The outer silicon sleeve, which acted as the pressure-sensing portion transmitting pressures to the transducer, had an active length of 3.1 mm. The overall probe diameter was 4.6 mm, and the sphincter transducer had a diameter of 5.2 mm. In prior studies of UES pressure, a similar transducer has been shown to record the same maximal pressure as a posterior oriented orifice (8). Computer system. The computer system consisted of an Apple IIe microcomputer with 128 K memory, dual disk drives, and an Epson printer augmented with an ADALAB data acquisition system and an AI13 fast analog-to-digital multiplexer (Interactive Microware, State College, PA). P-UESCOORD (version 1) was developed at the Bowman Gray School of Medicine. The software is written in Applesoft FP BASIC with calls to a commercially available assembly language sub-routine (Interactive Microware, QUICKER I/O) for the data collection routines. The program sets up a dialogue with the investigator that allows for the interactive determination of the system parameters. The pressure signals are collected from the voltage output of the recorder. This output was initially calibrated with the ADALAB card using a mercury manometer applied to external transducers. The signal is collected at a rate of 30 points/s from each of the two channels for base-line measurements and at a rate of 100 points/s from each of the two channels for swallow measurements. These data points are then converted to the corresponding values in millimeters of mercury as determined by the calibration. This

MANOMETRY

system has been previously described in detail as used in our studies on esophageal peristalsis and lower esophageal sphincter dynamics (2, 3). Study design. The manometry catheter was introduced through the nose and passed until both transducers were recording esophageal pressure. All studies were performed in a supine position. The catheter was then withdrawn rapidly until the proximal transducer passed through the UES and the distal (sphincter) transducer began to record UES pressures. Resting UES base-line pressure was calculated as the mean of pressures generated over a 2-s period minus the esophageal base-line pressure. This resting pressure was measured during a slow pull-through of at least four locations. After each l-cm movement of the transducer, the UES pressure was allowed to stabilize for at least 15 s before computer measurements were made (Fig. 2). A profile of pharyngeal pressures was obtained by moving the proximal transducer in l-cm increments from the area just proximal to the UES until a swallow failed to produce a pharyngeal pressure wave. Pharyngeal pressures were measured during swallows at each l-cm interval, and the highest pressure generated was identified (Fig. 3). This unidirectional transducer was oriented posteriorly in the pharynx. The sphincter transducer was then anchored in the most proximal segment of the UES with the single transducer 5 cm above in the pharynx. This positioning of the sphincter transducer was critical to record accurate UES relaxation without potential artifact produced by orad movement of the UES during swallowing (6). When properly positioned, the recording shows an “M”-shaped configuration (Fig. 4). This configuration showed 1) an increase in pressure as the high pressure zone moved orad onto the transducer; 2) a fall in pressure as the UES relaxed; 3) an increase in pressure as the UES closed; and 4) a decrease in pressure as the UES returned to its initial position, leaving the trans-

FIG. 1. Photograph of the solid-state transducer catheter used in these studies compared with a standard 8-lumen infused catheter. Annular sphincter transducer is shown near distal end of tube.

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on October 23, 2018. Copyright © 1990 American Physiological Society. All rights reserved.

PHARYNGEAL-UES

G175

MANOMETRY

FIG. 2. Tracing of a station pullthrough across the UES with solid-state sphincter transducer. Each large division represents 2 s. UES pressure was measured at each station after a 15-s equilibration period.

FIG. 3. Tracing of a station pullthrough of hypopharynx with swallow performed at each centimeter. Distance between pharyngeal transducer and sphincter transducer is 5 cm. Note that maximal pressure obtained in the pharynx is just proximal to the UES with a second high-pressure zone at -6-7 cm above proximal portion of UES in this patient. Each large division indicates 2 S.

FIG. 4. Tracing of 3 swallows with transducers placed to allow accurate recording of pharyngeal-UES pressure dynamics. Sphincter transducer is positioned in the proximal extent of the UES before a swallow. Note “M” configuration seen at UES as sphincter moves upward onto transducer before relaxation.

:-_L ‘-

I

E

i

T, T2 T3 T4 T5 T6 T7 T8 T9 A B C D E

= = = = = = = = = = = = = =

l-4 2-4 3-4 6-4 2-5 6-3 5-l 6-l 3-l Phatyngeal basellne UESP Esophageal basellne Nadir UES relaxation Phatyngeal Maxrnai

P P P

Time (millisec)

5. Schematic representation of 5 pressures and 6 time intervals that are measured by computer with each swallow. Resultant 9 time intervals utilized in this study for analysis of swallow dynamics are defined. FIG.

ducer proximal to the high pressure zone. Radiographic studies have confirmed this series of events (7). For each swallow, the computer program recognizes five pressures and calculates nine timing intervals (Fig. 5). The pressures identified were the pharyngeal base line (A); the pharyngeal peak pressure (E); the UES resting pressure (B); the nadir of the UES pressure during a swallow (D): and the esophageal base-line pressure (C). The residual pressure is then calculated as D - C. Six specific times were identified, and the nine timing intervals were calculated from these six times. The six times were 1) when the pharyngeal pressure exceeded pharyngeal base line

by 5 mmHg, 2) the time of the peak pharyngeal pressure, 3) the time that the pharyngeal pressure falls to within 5 mmHg of the pharyngeal base line, 4) the time that the UES pressure falls below the lowest pressure measured during the UES resting base-line period, 5) the time of the nadir of the UES pressure during a swallow, and 6) the time that the UES pressure exceeded the highest pressure measured during the resting UES base-line period. The nine resulting timing intervals included four measured from the beginning of the UES relaxation. These were Tl, the time from the beginning of UES relaxation to the beginning of the pharyngeal contraction; T2, to the peak of the pharyngeal contraction; T3, to the end of the pharyngeal contraction; and T4, the duration of the UES relaxation. The time from the nadir of the relaxation to the peak of the contraction was T5, and T6 was the time from the end of the contraction to the end of the relaxation. There were three timing intervals related to the beginning of the pharyngeal contraction: T7, the time from the beginning of the pharyngeal contraction to the nadir of the UES relaxation; T8, to the end of the relaxation; and 1‘9, the duration of the pharyngeal contraction. After the completion of the chosen number of swallows, the system produced a printed report of all determined values for each swallow and mean parameter values for all swallows. The investigator could then choose to do another set of swallows or exit from the program. Each swallow sequence was studied through a series of six dry swallows and six swallows each of 5-, lo-, and 20ml water boluses placed in the posterior pharynx. We also studied wet (5 ml) and dry swallows in seven subjects using both an eight-lumen polyvinyl esophageal manometry catheter and a Dent sleeve. Both assemblies were constantly perfused by a low-compliance luminal pneumohydraulic capillary infusion pump (Arndorfer Specialties) at a rate of 0.5 ml/min using distilled water driven by a nitrogen pressure head of 16 pounds/square in. The pump and catheter system record rise rates in the range of 400 mmHg/s. One orifice was placed in the most proximal segment of the UES with a second orifice located 5 cm proximal. The study was repeated on a subsequent day with a Dent sleeve spanning the UES

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on October 23, 2018. Copyright © 1990 American Physiological Society. All rights reserved.

G176

PHARYNGEAL-UES

MANOMETRY

and a single perfused orifice 5 cm proximal to the Dent sleeve. Statistical analysis. Data were analyzed using paired ttests, one-way analysis of variance, two-way analysis of variance, and least-squares regression analysis where applicable.

90 80 70 60

RESULTS

For these 21 healthy volunteers, mean peak UES resting pressure using the station pull-through technique was 84 t 38 (MD) mmHg with a range of 30-175 mmHg. The mean peak pharyngeal contraction pressure was 154 t 34 mmHg with a range of 80-190 mmHg. All timing intervals measured showed a distinct bolus effect as the bolus size increased from 5 to 20 ml. The results of the regression analyses are shown in Table 1. 1.

TABLE

t

Water

Bolus

\

10

_:

20 ml

-3 407 652 755 204 118 205 760 650

-31 415 672 818 229 139 219 842 710

-54 446 740 901 264 152 237 955 802

All values are in milliseconds and represent UES, upper esophageal sphincter. 90% 1’4: \‘\

70 -

,y I,;/’

60 -

\

‘\.\ \ \

40 -

20 lo,

1111

Ill

-100

100

1

0

100

-

Dry

+-a

Wet

I

300 Time

I

@ml)

I

500 (msec)

II

700

900

Pharynx

: \

1

Time

500

____------

/,/\\

\\

\

I

300

\\ \\ \\

UES

‘\

‘, i ‘\ \‘\ \ 1. \ \\ ’ ‘\\ \ \ i ‘\ Ah x I II 11

1111

0

Y

/

----7 \\\

\./// 1,

\\

\\

\\ / 1’ ,

,

/ //

//

//

,

1

I,

,J

FIG. 8. Stylized representation of mean values for pharyngeal and UES time intervals comparing use of a single-orifice infused catheter and a Dent sleeve infused catheter. Time intervals are set relative to onset of UES relaxation.

III

700

,

\\

0 1002003004005006007008009001000 Milliseconds

UES

60-

/

/

/

/,

7. Stylized representation of mean pharyngeal and UES time for dry and 5-ml water swallows in 21 volunteers. All time are set relative to onset of pharyngeal contraction.

‘1 \



30 -

L 2 z $ ii

\

/

/

/

/

the mean for 21 subjects.

\\,\

1).

50 -

s ;

FIG.

\

IllI

-100

intervals intervals

\

/

/

/

/

I’q \\

Pharynx

80 -

0.92 0.98 0.99 0.99 0.99 0.99 0.90 0.99 0.99

\

: I

Tl T2 T3 T4 T5 T6 T7 T8 T9

\

20

Size

10 ml

\

30

r2 5 ml

\ \

40

Bolus effect on pharyngeal- UES timings

Pharyngeal-UES Timings

UES

60

900

(msec)

FIG. 6. Stylized representation of mean values for pharyngeal contraction and UES relaxation in 21 normal volunteers with 5-, lo-, and 2O-ml water swallows. All time intervals are set relative to the beginning of pharvngeal contraction.

Figure 6 is a stylized drawing of the effect of bolus size on pharyngeal-UES coordinations. All times are set relative to the beginning of the pharyngeal contraction. The effect of bolus size on the pharynx is to increase both the duration of the contraction and the time to the peak of the contraction. The duration of UES relaxation is also increased. Figure 7 is a stylized drawing showing the relationship between dry and 5-ml wet swallows on pharyngeal-UES coordination. The most obvious difference is the change in the dP/dt of the upstroke of pharyngeal contraction (dry, 322 t 37 mmHg/s; wet, 203 t 18 mmHg/s; P < 0.01).

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on October 23, 2018. Copyright © 1990 American Physiological Society. All rights reserved.

PHARYNGEAL-UES

Figure 8 shows the comparison of the Dent sleeve to the single-orifice perfused catheter in the UES. In this representation, all times are set relative to the beginning of the UES relaxation to more closely compare UES relaxation. A perfused single-orifice catheter was positioned in the pharynx in both experiments. No differences in the UES relaxation profile were seen with these two recording systems. DISCUSSION

Accurate manometric assessment of pharyngeal and UES pressure dynamics has suffered from problems in both adequate catheter design and accurate quantitation of the rapid pressure sequences occurring during the pharyngeal swallow (4). Because of axial movement of the UES during deglutition, there has been some controversy about the use of a single recording device to measure UES pressures during relaxation. We have shown that there is no difference in the UES relaxation profile as measured by a single-orifice catheter positioned in the proximal segment of the UES or a Dent sleeve spanning the UES. In addition, a recent comparison by Kahrilas et al. of manometric techniques and simultaneous radiographic studies has shown that reliable estimates of UES relaxation (compared with sphincter opening radiographically) can be obtained with either a sleeve device spanning the UES or a single sensor placed in the proximal portion of this sphincter (7). Accurate measurement of the rapidly changing pressures in the hypopharynx, which surpass the pressure rise rate of perfused symptoms, require the fidelity of a solid-state intraluminal transducer. We have previously shown that a standard computer can be used for on-line recording of peristaltic sequences in the esophageal body and also relaxation dynamics of the lower esophageal sphincter (23). Using similar technology, we are able to measure an array of timing sequences between the pharyngeal contraction and the UES relaxation that should better characterize the dynamics of the pharyngeal swallow. While it would be possible to measure these timing sequences manually if the recording system has an adequate frequency response and a high paper speed is used for writing hard copy, we do not feel it would be practical. The effort involved in analyzing over 500 individual swallows for such a large number of parameters as we did in this study would be time consuming and tedious. Computer analysis is not only much faster, but it also avoids a possible source of error and subjectivity. In this manuscript, we report our experience with the initial studies combining solid-state manometric techniques and computer analysis for the study of pharyngeal swallows in a group of normal individuals. In the evaluation of pharyngeal-UES pressure dynamics, there are three components that may provide important information. These include the resting pressure or tone of the UES, the contraction potential (pressure) of the hypopharynx, and the interaction between pharyngeal contraction and UES relaxation, i.e., the coordination sequence of these events. To record the maximal

G177

MANOMETRY

contractile potential in either the pharynx or the UES, we feel that the station pull-through technique is appropriate. This allows assessment of UES closing pressures throughout the full range of the high-pressure zone and avoids the artifactually increased UES pressures obtained with rapid pull-through due to movement of the catheter through the sphincter (5). It also allows similar measurement of pharyngeal contraction pressures throughout the distance between the UES and the nasopharynx in each individual. These two parameters are difficult to measure simultaneously with the assessment of pharyngeal-UES coordination dynamics because of the restrictions on transducer placement when accurately recording events occurring during the pharyngeal swallow. In our studies of this small group of normal volunteers, maximal pharyngeal pressures ranged from 80 to 190 mmHg, and resting UES pressures ranged from 30 to 175 mmHg. These values should be considered only preliminary estimates of possible normal pressures for these areas until larger numbers of subjects in all age ranges are studied with appropriate recording techniques. The pharyngeal-UES dynamics were studied during a series of wet and dry swallows and with wet swallows of variable bolus size. These studies indicate that distinct changes can be recorded in all of the timing sequences and that a linear relationship occurs with increases in bolus size. The computer evaluation of the rapid timing sequences would thus appear to provide a sufficiently accurate measurement to identify physiological changes dependent on bolus volume in the pharynx and UES. In a comparison of the effect of dry vs. wet (5 ml water) swallows, the major difference was the slower and more sustained pharyngeal contractions seen with the wet swallow. This effect was also shown proportionally with each increase in bolus size of water swallows from 5 through 20 ml as the other timing indexes were also proportionally increased. Similar effects, although not evaluated with the detailed analysis provided by one-line computer measurement, have recently been shown by Kahrilas et al. (7) with a Dent sleeve in the UES. These initial observations indicate that the potential for accurate recording of pharyngeal-UES manometry is possible with proper application of newer solid-state intraluminal transducers and on-line computer measurement of the rapidly changing pressure dynamics of the pharyngeal swallow. Further application of these techniques should clarify other physiologic changes and may be applicable to alterations in the swallowing apparatus secondary to various diseases. Address for reprint requests: D. 0. Castell, Div. of Gastroenterology, Jefferson Medical College, 1025 Walnut St., Philadelphia, PA 19107. Received

27 October

1988; accepted

in final

form

10 July

1989.

REFERENCES 1. BOSMA, J. F. Deglutition: pharyngeal state. Physiol. Reu. 37: 275300, 1967. 2. CASTELL, J. A., AND D. 0. CASTELL. Computer analysis of human esophageal peristalsis and lower esophageal sphincter pressure. II. An interactive system for on-line data collection and analysis. Dig. Dis. Sci. 31: 121-126, 1986.

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on October 23, 2018. Copyright © 1990 American Physiological Society. All rights reserved.

G178

PHARYNGEAL-UES

3. CASTELL, J. A., C. B. DALTON, AND D. 0. CASTELL. On-line computer analysis of human lower esophageal sphincter relaxation. Am. J. Physiol. 255 (Gastrointest. Liver Physiol. 18): G794-G799, 1988. 4. DODDS, W. J., W. J. HOGAN, S. B. LYDON, E. T. STEWART, J. J. STEF, AND R. C. ARNDORFER. Quantitation of pharyngeal motor function in normal human subjects. J. Appl. Physiol. 39: 692-696, 1975. 5. GREEN, W. E., J. A. CASTELL, AND D. 0. CASTELL. Upper esophageal sphincter pressure recording. Is an oval manometry catheter necessary? Dysphagia 2: 162-165, 1988.

MANOMETRY 6. ISBERG, A., M. E. NILSSON, AND H. SCHIRATZKI. Movement of the upper esophageal sphincter and a manometric device during deglutition. Acta. Radial. Diag. 86: 381-388, 1985. 7. KAHRILAS, P. J., W. J. DODDS, J. DENT, J. A. LOGEMANN, AND R. SHAKER. Upper esophageal sphincter function during deglutition. Gastroenterology 95: 52-62, 1988. 8. WELCH, R. W., K. LUCKMANN, P. M. RICKS, S. T. DRAKE, AND G. A. GATES. Manometry of the normal upper esophageal sphincter and its alteration in laryngectomy. J. Clin. Invest. 63: 1036-1041, 1979. 9. WINANS, C. S. The pharyngoesophageal closure mechanism: a manometric study. Gastroenterology 63: 768-777, 1972.

Downloaded from www.physiology.org/journal/ajpgi by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on October 23, 2018. Copyright © 1990 American Physiological Society. All rights reserved.

Pharyngeal and upper esophageal sphincter manometry in humans.

Manometric studies of pharyngeal-upper esophageal sphincter (UES) coordination during swallowing have proven difficult. Asymmetry of the UES makes pre...
2MB Sizes 0 Downloads 0 Views