- Email: [email protected]
Alteration of Lower Esophageal Sphincter Characteristics with Respiration and Proximal Esophageal Balloon Distention
Vol. 62. No. 3
GASTROENTEROLOGY
Printed in U.S.A.
Copyright © 1972 by The Williams & Wilkins Co.
ALTERATION OF LOWER ESOPHAGEAL SPHINCTER CHARACTERISTICS WITH RESpmATION AND PROXIMAL ESOPHAGEAL BALLOON DISTENTION CHARLES
S.
WINANS,
M.D.
The Pritzker School of Medicine, The University of Chicago, Chicago, Illinois
By using the manometric recording catheter as both a measuring stick and a pressure detecting device, the location, length, and magnitude of the lower esophageal high pressure zone (HPZ) were studied in healthy human subjects. The HPZ was found to be located 1 to 3 cm more distal at end-inspiration than at end-expiration. In both phases of respiration the mean length (3 cm) and magnitude (22 mm Hg) of the resting HPZ were similar. An upward movement of the HPZ followed distention of the proximal esophagus by a balloon, accompanied by a 40% shortening of the HPZ and a 65% decrease in its magnitude. Whereas the movement of a sphincter segment relative to the recording orifice during the respiratory cycle can explain the pressure fluctuations within the resting HPZ, a combination of positional change and diminished sphincter tone best explains the fall in pressure within the HPZ after balloon distention and, probably, after swallowing. In addition, it is possible that sphincter length, as well as sphincter magnitude, is an important determinant of sphincter competence. The existence of a manometric high pressure zone (HPZ) at the gastroesophageal junction, first demonstrated with the aid of a miniature electromagnetic pressure transducer by Fyke et al. 1 in 1956, has been accepted by many as strong evidence for the presence of a sphincter mechanism in the distal esophagus. This band of elevated pressure, varying from 2 to 5 cm in length,2 is believed to be due to the tonic contraction of a sphincter muscle and constitutes a segment within which, under resting conditions, a barrier pressure always exceeds the simultaneously present intragastric pressure. Received April 13, 1971. Accepted October 27, 1971. Address requests for reprints to: Dr. C. S. Winans, The University of Chicago Hospitals, Box 400, 950 East 59th Street, Chicago, Illinois 60637. This work was supported in part by the National Institutes of Health Research Grant AM-2133-14. 380
Within this HPZ a point of respiratory reversal (PRR) usually can be identified below which a rise in pressure is recorded with inspiration and above which the converse is true. Many investigators 1 - S have believed that the PRR identifies the location of the diaphragmatic hiatus and have used it as a central reference point for the tabulation of manometric data. Little comment has been made in the literature concerning the genesis of the respiratory pressure fluctuations within the HPZ which often are of greater amplitude than those simultaneously observed in the adjacent stomach or esophagus. By inference, they have been regarded as intraabdominal or intrathoracic pressures superimposed upon the pressure due to the resting sphincter tone. The pressure profile of the resting HPZ is altered by deglutition. Within 1.5 to 2.5 sec following a swallow, Fyke et al. 1
March 1972
ALTERATION OF LOWER ESOPHAGEAL SPHINCTER CHARACTERISTICS
observed an obliteration of the band of elevated pressure. This fall in pressure, which persists only until the esophageal peristaltic wave reaches the gastroesophageal junction, is commonly believed to represent reflex relaxation of the lower esophageal sphincter. 1, 2 These conventional explanations concerning the cause of these pressure fluctuations within the HPZ involve the tacit assumption that neither the recording device nor the distal esophagus move significantly relative to one another and that, therefore, pressure changes at a constant location are being monitored. Not only has the validity of this assumption not been proved, but the cineradiographic studies of Johnson 6 suggest that considerable movement of the gastroesophageal junction occurs with both respiration and swallowing. The purpose of this study was to investigate, by manometric techniques, the location and the axial movements of the lower esophageal sphincter with respiration and swallowing and to clarify the genesis and significance of the observed pressure changes within the HPZ with these activities.
Methods The essential features of the recording system used in these studies have been previously described. 7 The recording assembly consisted of three polyvinyl tubes (outside diameter 2.4 mm, inside diameter 1.4 mm) cemented together to form a single catheter. The three lateral recording orifices (l.2 mm diameter) were located at 5-cm intervals with the most distal being placed 5 cm from the catheter tip. The completed catheter assembly had an over-all diameter of 5 mm and, although flexible, could not be stretched by the minimal pull necessary to withdraw it through the esophagus. Beginning at the distal orifice, the shaft of the completed catheter was marked with circumferential bands at I-cm intervals. The catheter, thus, became a measuring stick by which the position of each of the three recording orifices could be accurately localized at all times relative to a fixed external point, usually the margin of the subject's nostril from which the catheter emerged. The proximal end of each tube was attached to an external pressure transd~cer (Sanborn 267 series). Each of the
381
three water-filled recording systems was infused with fluid from an external source at a constant rate of approximately 12 /lliters per sec. Pressures measured from closed (sphincter) segments of the gastrointestinal tract by the infusion technique are believed to assess the resistance of that segment to forceful opening by a radial force acting from within the lumen,7. 8 and have been shown to correlate with the competence of the sphincter as judged by a variety of other criteria. 7-. Studies were conducted in a group of 11 volunteer medical student or physician subjects. Although none was subjected to radiographic examination, all were free of symptoms of gastroesophageal disease. Subjects were intubated in the sitting position and the catheter passed so that the most proximal recording orifice was more than 5 cm beyond the gastroesophageal junction. The subject then lay in the supine position during the study. A tube pneumograph around the subject's lower chest monitored respiration, and swallows were detected and recorded with the aid of either electromyograph electrodes placed over the laryngeal muscles or by an additional fluid-filled uninfused catheter passed by nose so that its open tip lay in the oropharynx. For the studies discussed under part 2, an additional catheter (outside diameter 3.5 mm, inside diameter 2.5 mm) tipped with a latex balloon of 40 cc capacity was passed by mouth so that the balloon tip lay 30 cm from the incisors. This catheter was firmly taped to the subject's chin so that the propulsive force elicited by distention of this balloon with 10 to 20 cc of air did not displace it. Part I-respiratory studies. To determine the effect of respiratory phase on the position and magnitude of the resting lower esophageal HPZ, studies were performed on seven individuals. With the subject breathing quietly, the catheter was slowly withdrawn until one of its recording orifices was about 2 cm beyond the distal margin of the HPZ as determined by a preliminary pull-through measurement. The subject was then asked to suspend his respiration at the end of either a normal tidal inspiration or expiration and to maintain breath-holding while the catheter was withdrawn by I-cm increments for a total distance of 6 to 8 cm. The recording point remained at each station only until a stable pressure was recorded, a period of 2 to 4 sec. After the initial pull-through the recording orifice was carefully repositioned in the stomach and the procedure repeated with breath held in the
382
WINANS
opposite phase of respiration. Only pullthroughs accomplished without swallowing and without evidence of Valsalva maneuver (as judged by constancy of simultaneously recorded gastric or esophageal pressure) were considered in the tabulation of the results. The zone of eleva ted pressure detected by pull-throughs during suspended respiration was termed the static HPZ, to differentiate it from the phasic HPZ profile obtained with pullthroughs during quiet breathing. The static HPZ's during inspiration and expiration for each subject were inspected to determine their length and the maximal pressure gradient between static HPZ and gastric fundus. In addition, the relative positions (as measured from the nares) of the proximal and the distal ends of the static HPZ's during inspiration and expiration were compared. Comparisons were made only between static HPZ's recorded from the same recording orifice. A total of 38 successful pull-throughs were performed in the 7 subjects. Twenty-two were performed in expiration and 16 in inspiration, the difference reflecting the difficulty some subjects experienced in holding their breath at end-inspiration without performing a Valsalva maneuver. Part 2-balloon distention studies. Ideally, changes in the position and magnitude of the HPZ following deglutition should be studied by pull-through pressure measurements performed during the period of "relaxation" of the HPZ which follows a swallow. Unfortunately, the short (6 to 10 sec) duration of this phenomenon makes this impractical. Advantage was taken, therefore, of an observation made by Creamer and Schlegel 10 and confirmed by others 11 that prolonged balloon distention of the proximal esophagus results in a sustained fall in pressure within the HPZ. The lowered pressure persists until the balloon is deflated, after which it returns to its previous resting level. Studies were performed in 4 subjects. Initially the recording tip was withdrawn from stomach to esophagus by l-cm increments as the subject respired quietly. The catheter tip then was advanced so that the recording orifice again lay distal to the gastroesophageal junction and a second pull-through was performed during quiet breathing after the balloon, positioned in the proximal esophagus, had been inflated with 10 to 20 cc of air. If the subject swallowed during a balloon distention pull-through, the study was discarded. In every instance deflation of the balloon resulted
Vol. 62, No.3
in a peristaltic contraction of the body of the esophagus. A total of nine successful paired studies were performed in the 4 subjects. From the phasic HPZ's recorded before and during balloon distention, static HPZ's during inspiration and expiration were calculated by inspecting the record and determining the length and magnitude of the end-inspiratory and end-expiratory pressure elevations at the gastroesophageal junction.
Results Part I-respiratory studies. Figure 1, A
and B, illustrates the type of pressure profile obtained during pull-throughs with suspended respiration. In figure lA a 3-cm segment of pressure elevation (at points 44, 43, and 42 cm from the naris) constitutes the static HPZ during expiration, while the inspiratory static HPZ (fig. IB) was 4 cm long (elevation of pressures at points 46, .45, 44, and 43 cm from the naris). Among the 38 measurements taken in the 7 subjects, the static HPZ varied from 2 to 4 cm in length. The mean length (fig. 2) of the static HPZ during inspiration (2.8 cm) did not differ significantly from its length during expiration (3.2 cm) (p> 0.1). Also evident from figure 1, A and B, is the fact that the static HPZ was located more distally during inspiration than during expiration. In this example the distal margin of the static HPZ moved 2 cm with the tidal inspiration (from a point 44 cm to a point 46 cm from the naris) while the proximal margin moved downward 1 cm (from a point 42 cm to a point 43 cm from the naris). This downward movement occurred in every study in every subject and varied from 1 to 3 cm with a normal tidal inspiration. Deep inspiration caused an even greater (up to 5 cm) movement. The mean downward movement of the proximal margin of the static HPZ for the 7 subjects was 1.4 cm, and did not differ significantly (P > 0.5) from the mean downward movement of the distal margin of 1.5 cm. The degree of pressure elevation was not uniform throughout the length of the static HPZ. Rather, the greatest pressure
March 1972
ALTERATION OF LOWER ESOPHAGEAL SPHINCTER CHARACTERISTICS
STATIC HPZ
STATIC HPZ
EXPIRATION
383
INSPIRAliON
FIG. 1. Upper tracings, recording orifice pulled from stomach into esophagus with breath held in expiration (A) or inspiration (B). Lower tracings, distal recording orifice in stomach. Heavy vertical lines indicate I-cm withdrawals of catheter. Numbers indicate distance in centimeters of recording orifice from nostril. Note shift of static high pressure zone (HPZ) location in an aboral direction with inspiration. Low amplitude pressure fluctuations with rate of about 78 per min seen in some segments are artifacts due to pulsation of an adjacent vascular structure.
GRAD lENT PRESSURE 25-
LENGTH 20-
-4
15-
-3
MM HG
eM
10-
-2
5-
-1
0-
E
E
-0
FIG. 2. Mean length of static high pressure zone (HPZ) and mean maximal pressure gradient between static HPZ and gastric fundus at end-inspiration (l) and end-expiration (E) . Brackets enclose ± 1 SEM.
was invariably found near the center of the static HPZ, with lesser pressures being recorded near its proximal and distal margins. The maximal pressure gradient between the static HPZ and gastric fundus was similar during expiration and inspiration. As shown in figure 2, the mean maximal pressure gradient in inspiration was 21.4 mm Hg and in expiration was 22.7 mm Hg. These values are not significantly different (P > 0.7). Similarly, the mean maximal gradient pressure was not significantly different whether the static HPZ was 2, 3, or 4 cm in length. Gastric and esophageal pressures as measured during suspended respiration varied in the anticipated manner. Part 2-balloon distention studies. Figure 3A demonstrates the appearance of the control phasic HPZ of 1 of the 4 subjects. In both inspiration and expiration an elevated pressure was recorded over a distance of 3 cm. The location of this segment (the calculated static HPZ) was 1 cm more distal at end-inspiration than at endexpiration. Figure 3B, a tracing recorded from the same subject several minutes later during balloon distention, demon-
384
WINANS
CONTROL
BALLOON
Vol. 62, No.3
PHASIC
DISTENTION
H PZ
PHASIC
HP~
FIG. 3. A, control phasic high pressure zone (HPZ) profile as recording orifice is pulled through sphincter by l-cm increments (heavy vertical lines) . Numbers indicate distance in centimeters of recording orifice from nostril. Orifice is in gastric fundus at 53 and 52 cm, and in esophagus at 47 cm . End-inspiratory pressure elevations are present at 51 through 49 cm, indicated by upper bar (calculated inspiratory static HPZ). End-expiratory pressure elevations are present at 50 through 48 cm, indicated by lower bar (calculated expiratory static HPZ) . B, Phasic HPZ profile with balloon distention. Recording orifice is in gastric fundus at 52, 51, and 50 cm, and in esophagus at 47 cm and above. End-inspiratory and end-expiratory pressure elevations are present at 49 and 48 cm, respectively. The calculated static HPZ's, indicated by upper bars, are only 1 cm in length. A peristaltic wave traverses the esophagus following deflation of the balloon.
March 1972
ALTERATION OF LOWER ESOPHAGEAL SPHINCTER CHARACTERISTICS
strates that the calculated static HPZ was now only 1 cm in length at the end of both inspiration and expiration. The location of the static HPZ still shifted distally 1 cm with inspiration. Also evident from comparison of figure 3, A and B, is the fact that the maximal inspiratory and expiratory pressure gradients between HPZ and stomach were markedly reduced following balloon distention, and that the distal margin of the HPZ is 2 cm more proximal after balloon distention. From each phasic HPZ (both before and during balloon distention) an inspiratory and expiratory static HPZ were calculated. Thus, from the nine paired studies there resulted 18 control static HPZ's and 18 static HPZ's following balloon distention. The strength and length characteristics of these two groups of static HPZ's are compared in figure 4. The mean length (3.2 cm) and magnitude (22.3 mm Hg) of the static HPZ's without balloon distention agree closely with those measurements made in part 1. However, following balloon distention the mean length of the static HPZ decreased to 1.9 cm and the mean maximal pressure within the static HPZ fell to 7.8 mm Hg. Both of these values differ significantly from the control measurements (P < 0.001). Balloon distention resulted in a mean upward movement of the distal margin of the static HPZ of 1.8 cm ± 0.17 cm (SEM). Indeed, at least 1- and as much as 3-cm upward movement of the distal margin occurred in every study on every subject.
Discussion This study confirms that in the distal resting esophagus there is a segment from which a zone of elevated pressure can be recorded by manometric techniques. This segment is about 3 cm in length and, relative to the recording catheter, moves down with inspiration and up with expiration and balloon distention. Could these movements be only apparent and, in fact, caused by an upward movement ofthe catheter with inspiration and a downward movement of the catheter with bal-
385
GRAD lENT PRESSURE 25-
LENGTH 20-
-4
15-
-3
MM HG
eM
10-
-2
5-
-1
0-
c
BD
c
BD
-0
FIG. 4. Mean length of calculated static high pressure zone (HPZ) and mean maximal pressure gradient between static HPZ and gastric fundus during control (C) pull-through measurements and following balloon distention (BD). Brackets enclose ± 1 SEM .
loon distention? As the catheter was held firmly at the point that it emerged from the nose during the studies and because the catheter thickness was such as to make buckling in the pharynx or esophagus difficult, this alternate explanation seems unlikely. However, to check on this possibility fluoroscopic observations were made in several subjects. Neither inspiration nor balloon distention caused movement of the radio-opaque catheter tip relative to adjacent vertebral bodies. That the distal esophagus itself actually moves in the fashion stated in this report is supported by the cineradiographic studies of Johnson 6 who demonstrated that metal washers sewn to the serosal gastroesophageal junction or placed within the muscularis propria of the distal esophagus of dogs moved downward with inspiration and up with swallowing. More recently, Clark et al. 12 similarly observed that a
386
WINANS
small barium-filled diverticulum of the distal esophagus of 2 human subjects moved upward with swallowing. Although the extent of the downward movement of the static HPZ does seem related to the depth of inspiration, the mechanism by which this movement occurs is not revealed by this study. It seems likely that the mechanism is a passive one and does not involve alteration of the tone of the distal esophageal muscle as neither the length nor magnitude of the static HPZ is altered during the movement. Perhaps the stomach, displaced downward by the descent of the diaphragm, or the phrenoesophageal attachments cause traction on the esophagus and result in the observed movement. Most investigators have attributed the HPZ to the squeeze of a sphincter mechanism intrinsic to the circular muscle of the distal esophagus. The marked decrease in magnitude of the HPZ with balloon distention found in this study is consistent with the assumption that the HPZ is a manifestation of such a physiological sphincter. However, because an anatomical sphincter has not been convincingly demonstrated and because any force, intrinsic or extrinsic, which compresses the distal esophagus could cause an HPZ to be recorded, attributing the HPZ to the action of an intrinsic sphincter remains only a reasonable assumption. To what extent external compression of the distal esophagus at the hiatus by the diaphragm contributes to the manometric high pressure zone is unsettled. It is theoretically possible that the static HPZ is substantially due to such compression and that the downward movement of the hiatal ring with inspiration is directly responsible for the movement of the static HPZ. However, manometric studies of patients with hiatus hernia by the infusion technique generally reveal only a minimal plateau of pressure at the hiatus with a much greater, more proximal pressure elevation due to the sphincter. The magnitude of the static HPZ in this study argues against the idea that it and its movement are the result of compression by the descending diaphragm.
Vol. 62, No.3
Movement of a lower esophageal sphincter up and down with the respiratory cycle provides a ready explanation for the sometimes large pressure fluctuations, phasic with respiration, seen at either end of the phasic HPZ. Figure 5 demonstrates sche-
------------ 6
-.
t
'0 """G ./"'../
-
0 1
"\
\ ./
f\ l ""\ 1 ~
~
~
,\
: I
\,
2
3
4
I N SPI RATI O N
L
V!:'\, ' I VI' I' PNE U M O GRAM -
I,l\'l
,"1
\
l
5
n
.-
.0"""G
r-,,'- V '
0 --
6
FIG. 5. Illustration of the role of axial sphincter movement in the genesis of the phasic high pressure zone profile, assuming a 3·cm sphincter with static high pressure zone profile similar to that in figure 1A with greatest pressure at the midpoint and lesser pressures at the margins, Horizontally lined area and solid arc (E) represent end-expiratory positions of sphincter and gastric fundus, whereas dotted area and broken arc represent positions of these structures after i-cm distal movement at end-inspiration, Numbers relate positions of catheter recording orifice to segment of profile below, At positions 1 and 6 the recording orifice monitors pressure from stomach and esophagus, respectively, during all phases of the respiratory cycle. At position 2 the orifice is in the stomach at end-expiration but under the distal margin of the sphincter at end-inspiration, Hence, only an end-inspiratory pressure elevation is present in segment 2 of the pressure profile. At position 5 the situation is reversed, with pressure elevation only at end-expiration when the proximal margin of the sphincter covers the recording orifice. At positions 3 and 4 the orifice is in contact with the sphincter throughout the respiratory cycle, but records the highest pressure only when it is covered by the center of the sphincter (end-inspiration at position 3; endexpiration at position 4) . The point of respiratory reversal occurs at position 4 where the center of the sphincter first lies below the orifice at end-inspiration, thus recording a lower end-inspiratory than end-expiratory pressure,
m
March 1972
ALTERATION OF LOWER ESOPHAGEAL SPHINCTER CHARACTERISTICS
mati cally how movement of the gastroesophageal junction and sphincter relative to the stationary recording orifice could cause these pressure fluctuations to be recorded. In fact, all pressure fluctuations within the phasic HPZ are best explained not as superimposed abdominal and thoracic pressure variations, but as the result of successive exposure of the recording orifice to different anatomical points with differing pressures during the respiratory cycle. Harris and Pope 13 have shown that the PRR as detected by an uninfused manometric system is due to the sealing of the recording orifice by the sphincter and that it does not reliably indicate the location of the diaphragmatic hiatus. Similarly, with the infused manometric recording system, the PRR would be predicted to occur at that point where the recording orifice at end-inspiration is first exposed to a site of lower pressure than at end-expiration. As pressures rise progressively from gastric fundus to the midpoint of the static HPZ and decline progressively above the midpoint of the static HPZ to the esophagus, the PRR will be found when the midpoint of the static HPZ lies somewhere below the recording orifice at end-inspiration. In studies dealing with the correlation between the competence of the lower esophageal sphincter and the magnitude of the pressure recorded from within the HPZ, there has been a lack of uniformity in the manner of calculating the magnitude of the HPZ. Some 7 • 8 have taken the highest mean pressure within the phasic HPZ, while others 9 have tabulated the end-expiratory pressure gradient between HPZ and stomach. Recognition that the static HPZ changes position during the respiratory cycle suggests that the former method of pressure measurement does not assess the true maximal sphincter pressure because the recording orifice will be monitoring a sub maximal portion of the static HPZ during at least half of the respiratory cycle. Perhaps the best measurement of maximal sphincter pressure would be the highest end-inspiratory or end-expiratory pressure found within the phasic HPZ.
387
Because the maximum pressure within the static HPZ was the same regardless of its length, it is unlikely that length of the static HPZ is simply a function of the force of closure of the sphincter mechanism. Although heretofore the literature has stressed only sphincter pressure as a measure of sphincter competence, it is possible that sphincter length (as measured by the static HPZ) is also important in determining the effectiveness of the sphincter as a barrier against gastroesophageal reflux. Christensen and Lund 14 have studied the response of mammalian (opossum) esophageal smooth muscle in vivo and in vitro to balloon distention. They have demonstrated a localized contraction of the longitudinal muscle in the vicinity of the distending stimulus, termed the " duration response," which persists as long as the proximal esophagus is distended and results in a shortening of the entire organ and elevation of the cardia. Such a contraction of esophageal longitudinal muscle may well have accounted for the elevation of the gastroesophageal junction with balloon distention in man observed in this study. In addition to elevation, a previously unrecognized change in the lower esophageal sphincter-shortening-was shown by this study to occur with balloon distention. This shortening averaged 40% of resting sphincter length and was accompanied by an average fall in sphincter pressure of 65%. Further studies of the relationship of these changes to the location and volume of the distending balloon and of their alteration by autonomic drugs are necessary to clarify the mechanism of these potentially important aspects of sphincter physiology. The manner in which the manometric HPZ shortens following balloon distention is not explained by this study. It is possible that the sphincter is actually compressed into a shorter length, for instance, by a local contraction of the longitudinal muscle in the region of the sphincter. In their studies of the isolated opossum esophagus, however, Christensen and Lund 14 observed such a contraction only
388
Vol. 62, No.3
WINANS
adjacent to the distending balloon and not in the distal esophagus. A more likely explanation for the shortening of the static HPZ with balloon distention is that a generalized decrease in tone occurs along the length of the sphincter, resulting in the disappearance of measurable tone at the margins where the pressure is already lowest in the resting state. In this study proximal esophageal balloon distention was used to prolong the effect normally produced by swallowing on the lower esophageal high pressure zone. Although it is not possible to state with certainty that this maneuver alters the lower esophageal sphincter in the same way or to the same extent as deglutition, this study does indicate that the sphincter's location and length, as well as its magnitude, are capable of alteration, and this fact should be considered in interpreting the fall in pressure within the phasic HPZ following swallowing. Rinaldo and Clark,15 using a combined cineradiographic and manometric technique, previously recognized that this "relaxation" may, in fact, be due to proximal movement of the sphincter. This study confirms their contention but demonstrates that a genuine decrease in sphincter tone occurs as well. The observed pressure changes within the phasic HPZ with swallowing would seem to represent a combination of the two effects. Thus, at the distal end of the phasic HPZ (at positions as shown at recording points 2 and 3 in fig. 5) a 2-cm elevation of the distal margin of the sphincter would leave the recording orifice exposed to intragastric pressures throughout the entire respiratory cycle. A decrease in pressure recorded from either of these two orifices after a swallow would, therefore, be solely a result of change in position of the sphincter and not reflect a change in sphincter tone. On the other hand, at points higher in the phasic HPZ (for example, at orifice 4 in fig. 5) the orifice would remain within the sphincter even after a 2-cm elevation, and the fall in recorded pressure following deglutition would, therefore,
result from a change in sphincter tone as well as position. REFERENCES 1. Fyke FE, Code CF, Schlegel JF: The gastroesoph-
ageal sphincter in healthy human beings. Gastroenterologia 86: 135- 150, 1956 2. Pert JH, Davidson M, Almy TP, et al: Esophageal catheterization studies. I. The mechanism of swallowing in normal subjects with particular reference to the vestibule. J Clin Invest 38:397406, 1959
3. Nagler R, Spiro HM: Serial esophageal motility studies in asymptomatic young subjects. Gastroenterology 41 :371-379, 1961 4. Atkinson M, Edwards DA W, Honour AJ, et al: Comparison of cardiac and pyloric sphincters. Lancet 2:918- 922, 1957 5. Kelley ML, Wilbur DL, Schlegel JF, et al : Deglutitive responses in the gastroesophageal sphincter of healthy human beings. J Appl Physiol 15:483- 488, 1960 6. Johnson HD: The cardia and hiatus hernia. Springfield, Illinois, Charles C Thomas, 1968, p 17-30
7. Winans CS, Harris LD: Quantitation of lower esophageal sphincter competence. Gastroenterology 52:773- 778, 1967 8. Pope CE: A dynamic test of sphincter strength: its application to the lower esophageal sphincter. Gastroenterology 52:779- 786, 1967 9. Haddad JK: Relation of gastroesophageal reflux to yield sphincter pressures. Gastroenterology 58: 175- 184, 1970 10. Creamer B, Schlegel JF: Motor responses of the esophagus to distention. J Appl Physiol 10:498504, 1957 11. Fleshier B, Hendrix TR, Kramer P, et al : The
12.
13.
14.
15.
characteristics and similarity of primary and secondary peristalsis of the esophagus. J Clin Invest 38: 110- 116, 1959 Clark MD, Rinaldo JA, Eyler WR: Correlation of manometric and radiologic data from the esophagogastric area. Radiology 94:261- 270, 1970 Harris LD, Pope CE: The pressure inversion point; its genesis and reliability. Gastroenterology 51 :641- 648, 1966 Christensen J, Lund GF: Esophageal responses to deglutition and electrical stimulation. J Clin Invest 48:408- 419, 1969 Rinaldo JA, Clark MD: Manometric consequences of movement of the inferior esophageal sphincter during swallowing (abstr.). Gastroenterology 48:842, 1965
GASTROENTEROLOGY
Printed in U.S.A.
Copyright © 1972 by The Williams & Wilkins Co.
ALTERATION OF LOWER ESOPHAGEAL SPHINCTER CHARACTERISTICS WITH RESpmATION AND PROXIMAL ESOPHAGEAL BALLOON DISTENTION CHARLES
S.
WINANS,
M.D.
The Pritzker School of Medicine, The University of Chicago, Chicago, Illinois
By using the manometric recording catheter as both a measuring stick and a pressure detecting device, the location, length, and magnitude of the lower esophageal high pressure zone (HPZ) were studied in healthy human subjects. The HPZ was found to be located 1 to 3 cm more distal at end-inspiration than at end-expiration. In both phases of respiration the mean length (3 cm) and magnitude (22 mm Hg) of the resting HPZ were similar. An upward movement of the HPZ followed distention of the proximal esophagus by a balloon, accompanied by a 40% shortening of the HPZ and a 65% decrease in its magnitude. Whereas the movement of a sphincter segment relative to the recording orifice during the respiratory cycle can explain the pressure fluctuations within the resting HPZ, a combination of positional change and diminished sphincter tone best explains the fall in pressure within the HPZ after balloon distention and, probably, after swallowing. In addition, it is possible that sphincter length, as well as sphincter magnitude, is an important determinant of sphincter competence. The existence of a manometric high pressure zone (HPZ) at the gastroesophageal junction, first demonstrated with the aid of a miniature electromagnetic pressure transducer by Fyke et al. 1 in 1956, has been accepted by many as strong evidence for the presence of a sphincter mechanism in the distal esophagus. This band of elevated pressure, varying from 2 to 5 cm in length,2 is believed to be due to the tonic contraction of a sphincter muscle and constitutes a segment within which, under resting conditions, a barrier pressure always exceeds the simultaneously present intragastric pressure. Received April 13, 1971. Accepted October 27, 1971. Address requests for reprints to: Dr. C. S. Winans, The University of Chicago Hospitals, Box 400, 950 East 59th Street, Chicago, Illinois 60637. This work was supported in part by the National Institutes of Health Research Grant AM-2133-14. 380
Within this HPZ a point of respiratory reversal (PRR) usually can be identified below which a rise in pressure is recorded with inspiration and above which the converse is true. Many investigators 1 - S have believed that the PRR identifies the location of the diaphragmatic hiatus and have used it as a central reference point for the tabulation of manometric data. Little comment has been made in the literature concerning the genesis of the respiratory pressure fluctuations within the HPZ which often are of greater amplitude than those simultaneously observed in the adjacent stomach or esophagus. By inference, they have been regarded as intraabdominal or intrathoracic pressures superimposed upon the pressure due to the resting sphincter tone. The pressure profile of the resting HPZ is altered by deglutition. Within 1.5 to 2.5 sec following a swallow, Fyke et al. 1
March 1972
ALTERATION OF LOWER ESOPHAGEAL SPHINCTER CHARACTERISTICS
observed an obliteration of the band of elevated pressure. This fall in pressure, which persists only until the esophageal peristaltic wave reaches the gastroesophageal junction, is commonly believed to represent reflex relaxation of the lower esophageal sphincter. 1, 2 These conventional explanations concerning the cause of these pressure fluctuations within the HPZ involve the tacit assumption that neither the recording device nor the distal esophagus move significantly relative to one another and that, therefore, pressure changes at a constant location are being monitored. Not only has the validity of this assumption not been proved, but the cineradiographic studies of Johnson 6 suggest that considerable movement of the gastroesophageal junction occurs with both respiration and swallowing. The purpose of this study was to investigate, by manometric techniques, the location and the axial movements of the lower esophageal sphincter with respiration and swallowing and to clarify the genesis and significance of the observed pressure changes within the HPZ with these activities.
Methods The essential features of the recording system used in these studies have been previously described. 7 The recording assembly consisted of three polyvinyl tubes (outside diameter 2.4 mm, inside diameter 1.4 mm) cemented together to form a single catheter. The three lateral recording orifices (l.2 mm diameter) were located at 5-cm intervals with the most distal being placed 5 cm from the catheter tip. The completed catheter assembly had an over-all diameter of 5 mm and, although flexible, could not be stretched by the minimal pull necessary to withdraw it through the esophagus. Beginning at the distal orifice, the shaft of the completed catheter was marked with circumferential bands at I-cm intervals. The catheter, thus, became a measuring stick by which the position of each of the three recording orifices could be accurately localized at all times relative to a fixed external point, usually the margin of the subject's nostril from which the catheter emerged. The proximal end of each tube was attached to an external pressure transd~cer (Sanborn 267 series). Each of the
381
three water-filled recording systems was infused with fluid from an external source at a constant rate of approximately 12 /lliters per sec. Pressures measured from closed (sphincter) segments of the gastrointestinal tract by the infusion technique are believed to assess the resistance of that segment to forceful opening by a radial force acting from within the lumen,7. 8 and have been shown to correlate with the competence of the sphincter as judged by a variety of other criteria. 7-. Studies were conducted in a group of 11 volunteer medical student or physician subjects. Although none was subjected to radiographic examination, all were free of symptoms of gastroesophageal disease. Subjects were intubated in the sitting position and the catheter passed so that the most proximal recording orifice was more than 5 cm beyond the gastroesophageal junction. The subject then lay in the supine position during the study. A tube pneumograph around the subject's lower chest monitored respiration, and swallows were detected and recorded with the aid of either electromyograph electrodes placed over the laryngeal muscles or by an additional fluid-filled uninfused catheter passed by nose so that its open tip lay in the oropharynx. For the studies discussed under part 2, an additional catheter (outside diameter 3.5 mm, inside diameter 2.5 mm) tipped with a latex balloon of 40 cc capacity was passed by mouth so that the balloon tip lay 30 cm from the incisors. This catheter was firmly taped to the subject's chin so that the propulsive force elicited by distention of this balloon with 10 to 20 cc of air did not displace it. Part I-respiratory studies. To determine the effect of respiratory phase on the position and magnitude of the resting lower esophageal HPZ, studies were performed on seven individuals. With the subject breathing quietly, the catheter was slowly withdrawn until one of its recording orifices was about 2 cm beyond the distal margin of the HPZ as determined by a preliminary pull-through measurement. The subject was then asked to suspend his respiration at the end of either a normal tidal inspiration or expiration and to maintain breath-holding while the catheter was withdrawn by I-cm increments for a total distance of 6 to 8 cm. The recording point remained at each station only until a stable pressure was recorded, a period of 2 to 4 sec. After the initial pull-through the recording orifice was carefully repositioned in the stomach and the procedure repeated with breath held in the
382
WINANS
opposite phase of respiration. Only pullthroughs accomplished without swallowing and without evidence of Valsalva maneuver (as judged by constancy of simultaneously recorded gastric or esophageal pressure) were considered in the tabulation of the results. The zone of eleva ted pressure detected by pull-throughs during suspended respiration was termed the static HPZ, to differentiate it from the phasic HPZ profile obtained with pullthroughs during quiet breathing. The static HPZ's during inspiration and expiration for each subject were inspected to determine their length and the maximal pressure gradient between static HPZ and gastric fundus. In addition, the relative positions (as measured from the nares) of the proximal and the distal ends of the static HPZ's during inspiration and expiration were compared. Comparisons were made only between static HPZ's recorded from the same recording orifice. A total of 38 successful pull-throughs were performed in the 7 subjects. Twenty-two were performed in expiration and 16 in inspiration, the difference reflecting the difficulty some subjects experienced in holding their breath at end-inspiration without performing a Valsalva maneuver. Part 2-balloon distention studies. Ideally, changes in the position and magnitude of the HPZ following deglutition should be studied by pull-through pressure measurements performed during the period of "relaxation" of the HPZ which follows a swallow. Unfortunately, the short (6 to 10 sec) duration of this phenomenon makes this impractical. Advantage was taken, therefore, of an observation made by Creamer and Schlegel 10 and confirmed by others 11 that prolonged balloon distention of the proximal esophagus results in a sustained fall in pressure within the HPZ. The lowered pressure persists until the balloon is deflated, after which it returns to its previous resting level. Studies were performed in 4 subjects. Initially the recording tip was withdrawn from stomach to esophagus by l-cm increments as the subject respired quietly. The catheter tip then was advanced so that the recording orifice again lay distal to the gastroesophageal junction and a second pull-through was performed during quiet breathing after the balloon, positioned in the proximal esophagus, had been inflated with 10 to 20 cc of air. If the subject swallowed during a balloon distention pull-through, the study was discarded. In every instance deflation of the balloon resulted
Vol. 62, No.3
in a peristaltic contraction of the body of the esophagus. A total of nine successful paired studies were performed in the 4 subjects. From the phasic HPZ's recorded before and during balloon distention, static HPZ's during inspiration and expiration were calculated by inspecting the record and determining the length and magnitude of the end-inspiratory and end-expiratory pressure elevations at the gastroesophageal junction.
Results Part I-respiratory studies. Figure 1, A
and B, illustrates the type of pressure profile obtained during pull-throughs with suspended respiration. In figure lA a 3-cm segment of pressure elevation (at points 44, 43, and 42 cm from the naris) constitutes the static HPZ during expiration, while the inspiratory static HPZ (fig. IB) was 4 cm long (elevation of pressures at points 46, .45, 44, and 43 cm from the naris). Among the 38 measurements taken in the 7 subjects, the static HPZ varied from 2 to 4 cm in length. The mean length (fig. 2) of the static HPZ during inspiration (2.8 cm) did not differ significantly from its length during expiration (3.2 cm) (p> 0.1). Also evident from figure 1, A and B, is the fact that the static HPZ was located more distally during inspiration than during expiration. In this example the distal margin of the static HPZ moved 2 cm with the tidal inspiration (from a point 44 cm to a point 46 cm from the naris) while the proximal margin moved downward 1 cm (from a point 42 cm to a point 43 cm from the naris). This downward movement occurred in every study in every subject and varied from 1 to 3 cm with a normal tidal inspiration. Deep inspiration caused an even greater (up to 5 cm) movement. The mean downward movement of the proximal margin of the static HPZ for the 7 subjects was 1.4 cm, and did not differ significantly (P > 0.5) from the mean downward movement of the distal margin of 1.5 cm. The degree of pressure elevation was not uniform throughout the length of the static HPZ. Rather, the greatest pressure
March 1972
ALTERATION OF LOWER ESOPHAGEAL SPHINCTER CHARACTERISTICS
STATIC HPZ
STATIC HPZ
EXPIRATION
383
INSPIRAliON
FIG. 1. Upper tracings, recording orifice pulled from stomach into esophagus with breath held in expiration (A) or inspiration (B). Lower tracings, distal recording orifice in stomach. Heavy vertical lines indicate I-cm withdrawals of catheter. Numbers indicate distance in centimeters of recording orifice from nostril. Note shift of static high pressure zone (HPZ) location in an aboral direction with inspiration. Low amplitude pressure fluctuations with rate of about 78 per min seen in some segments are artifacts due to pulsation of an adjacent vascular structure.
GRAD lENT PRESSURE 25-
LENGTH 20-
-4
15-
-3
MM HG
eM
10-
-2
5-
-1
0-
E
E
-0
FIG. 2. Mean length of static high pressure zone (HPZ) and mean maximal pressure gradient between static HPZ and gastric fundus at end-inspiration (l) and end-expiration (E) . Brackets enclose ± 1 SEM.
was invariably found near the center of the static HPZ, with lesser pressures being recorded near its proximal and distal margins. The maximal pressure gradient between the static HPZ and gastric fundus was similar during expiration and inspiration. As shown in figure 2, the mean maximal pressure gradient in inspiration was 21.4 mm Hg and in expiration was 22.7 mm Hg. These values are not significantly different (P > 0.7). Similarly, the mean maximal gradient pressure was not significantly different whether the static HPZ was 2, 3, or 4 cm in length. Gastric and esophageal pressures as measured during suspended respiration varied in the anticipated manner. Part 2-balloon distention studies. Figure 3A demonstrates the appearance of the control phasic HPZ of 1 of the 4 subjects. In both inspiration and expiration an elevated pressure was recorded over a distance of 3 cm. The location of this segment (the calculated static HPZ) was 1 cm more distal at end-inspiration than at endexpiration. Figure 3B, a tracing recorded from the same subject several minutes later during balloon distention, demon-
384
WINANS
CONTROL
BALLOON
Vol. 62, No.3
PHASIC
DISTENTION
H PZ
PHASIC
HP~
FIG. 3. A, control phasic high pressure zone (HPZ) profile as recording orifice is pulled through sphincter by l-cm increments (heavy vertical lines) . Numbers indicate distance in centimeters of recording orifice from nostril. Orifice is in gastric fundus at 53 and 52 cm, and in esophagus at 47 cm . End-inspiratory pressure elevations are present at 51 through 49 cm, indicated by upper bar (calculated inspiratory static HPZ). End-expiratory pressure elevations are present at 50 through 48 cm, indicated by lower bar (calculated expiratory static HPZ) . B, Phasic HPZ profile with balloon distention. Recording orifice is in gastric fundus at 52, 51, and 50 cm, and in esophagus at 47 cm and above. End-inspiratory and end-expiratory pressure elevations are present at 49 and 48 cm, respectively. The calculated static HPZ's, indicated by upper bars, are only 1 cm in length. A peristaltic wave traverses the esophagus following deflation of the balloon.
March 1972
ALTERATION OF LOWER ESOPHAGEAL SPHINCTER CHARACTERISTICS
strates that the calculated static HPZ was now only 1 cm in length at the end of both inspiration and expiration. The location of the static HPZ still shifted distally 1 cm with inspiration. Also evident from comparison of figure 3, A and B, is the fact that the maximal inspiratory and expiratory pressure gradients between HPZ and stomach were markedly reduced following balloon distention, and that the distal margin of the HPZ is 2 cm more proximal after balloon distention. From each phasic HPZ (both before and during balloon distention) an inspiratory and expiratory static HPZ were calculated. Thus, from the nine paired studies there resulted 18 control static HPZ's and 18 static HPZ's following balloon distention. The strength and length characteristics of these two groups of static HPZ's are compared in figure 4. The mean length (3.2 cm) and magnitude (22.3 mm Hg) of the static HPZ's without balloon distention agree closely with those measurements made in part 1. However, following balloon distention the mean length of the static HPZ decreased to 1.9 cm and the mean maximal pressure within the static HPZ fell to 7.8 mm Hg. Both of these values differ significantly from the control measurements (P < 0.001). Balloon distention resulted in a mean upward movement of the distal margin of the static HPZ of 1.8 cm ± 0.17 cm (SEM). Indeed, at least 1- and as much as 3-cm upward movement of the distal margin occurred in every study on every subject.
Discussion This study confirms that in the distal resting esophagus there is a segment from which a zone of elevated pressure can be recorded by manometric techniques. This segment is about 3 cm in length and, relative to the recording catheter, moves down with inspiration and up with expiration and balloon distention. Could these movements be only apparent and, in fact, caused by an upward movement ofthe catheter with inspiration and a downward movement of the catheter with bal-
385
GRAD lENT PRESSURE 25-
LENGTH 20-
-4
15-
-3
MM HG
eM
10-
-2
5-
-1
0-
c
BD
c
BD
-0
FIG. 4. Mean length of calculated static high pressure zone (HPZ) and mean maximal pressure gradient between static HPZ and gastric fundus during control (C) pull-through measurements and following balloon distention (BD). Brackets enclose ± 1 SEM .
loon distention? As the catheter was held firmly at the point that it emerged from the nose during the studies and because the catheter thickness was such as to make buckling in the pharynx or esophagus difficult, this alternate explanation seems unlikely. However, to check on this possibility fluoroscopic observations were made in several subjects. Neither inspiration nor balloon distention caused movement of the radio-opaque catheter tip relative to adjacent vertebral bodies. That the distal esophagus itself actually moves in the fashion stated in this report is supported by the cineradiographic studies of Johnson 6 who demonstrated that metal washers sewn to the serosal gastroesophageal junction or placed within the muscularis propria of the distal esophagus of dogs moved downward with inspiration and up with swallowing. More recently, Clark et al. 12 similarly observed that a
386
WINANS
small barium-filled diverticulum of the distal esophagus of 2 human subjects moved upward with swallowing. Although the extent of the downward movement of the static HPZ does seem related to the depth of inspiration, the mechanism by which this movement occurs is not revealed by this study. It seems likely that the mechanism is a passive one and does not involve alteration of the tone of the distal esophageal muscle as neither the length nor magnitude of the static HPZ is altered during the movement. Perhaps the stomach, displaced downward by the descent of the diaphragm, or the phrenoesophageal attachments cause traction on the esophagus and result in the observed movement. Most investigators have attributed the HPZ to the squeeze of a sphincter mechanism intrinsic to the circular muscle of the distal esophagus. The marked decrease in magnitude of the HPZ with balloon distention found in this study is consistent with the assumption that the HPZ is a manifestation of such a physiological sphincter. However, because an anatomical sphincter has not been convincingly demonstrated and because any force, intrinsic or extrinsic, which compresses the distal esophagus could cause an HPZ to be recorded, attributing the HPZ to the action of an intrinsic sphincter remains only a reasonable assumption. To what extent external compression of the distal esophagus at the hiatus by the diaphragm contributes to the manometric high pressure zone is unsettled. It is theoretically possible that the static HPZ is substantially due to such compression and that the downward movement of the hiatal ring with inspiration is directly responsible for the movement of the static HPZ. However, manometric studies of patients with hiatus hernia by the infusion technique generally reveal only a minimal plateau of pressure at the hiatus with a much greater, more proximal pressure elevation due to the sphincter. The magnitude of the static HPZ in this study argues against the idea that it and its movement are the result of compression by the descending diaphragm.
Vol. 62, No.3
Movement of a lower esophageal sphincter up and down with the respiratory cycle provides a ready explanation for the sometimes large pressure fluctuations, phasic with respiration, seen at either end of the phasic HPZ. Figure 5 demonstrates sche-
------------ 6
-.
t
'0 """G ./"'../
-
0 1
"\
\ ./
f\ l ""\ 1 ~
~
~
,\
: I
\,
2
3
4
I N SPI RATI O N
L
V!:'\, ' I VI' I' PNE U M O GRAM -
I,l\'l
,"1
\
l
5
n
.-
.0"""G
r-,,'- V '
0 --
6
FIG. 5. Illustration of the role of axial sphincter movement in the genesis of the phasic high pressure zone profile, assuming a 3·cm sphincter with static high pressure zone profile similar to that in figure 1A with greatest pressure at the midpoint and lesser pressures at the margins, Horizontally lined area and solid arc (E) represent end-expiratory positions of sphincter and gastric fundus, whereas dotted area and broken arc represent positions of these structures after i-cm distal movement at end-inspiration, Numbers relate positions of catheter recording orifice to segment of profile below, At positions 1 and 6 the recording orifice monitors pressure from stomach and esophagus, respectively, during all phases of the respiratory cycle. At position 2 the orifice is in the stomach at end-expiration but under the distal margin of the sphincter at end-inspiration, Hence, only an end-inspiratory pressure elevation is present in segment 2 of the pressure profile. At position 5 the situation is reversed, with pressure elevation only at end-expiration when the proximal margin of the sphincter covers the recording orifice. At positions 3 and 4 the orifice is in contact with the sphincter throughout the respiratory cycle, but records the highest pressure only when it is covered by the center of the sphincter (end-inspiration at position 3; endexpiration at position 4) . The point of respiratory reversal occurs at position 4 where the center of the sphincter first lies below the orifice at end-inspiration, thus recording a lower end-inspiratory than end-expiratory pressure,
m
March 1972
ALTERATION OF LOWER ESOPHAGEAL SPHINCTER CHARACTERISTICS
mati cally how movement of the gastroesophageal junction and sphincter relative to the stationary recording orifice could cause these pressure fluctuations to be recorded. In fact, all pressure fluctuations within the phasic HPZ are best explained not as superimposed abdominal and thoracic pressure variations, but as the result of successive exposure of the recording orifice to different anatomical points with differing pressures during the respiratory cycle. Harris and Pope 13 have shown that the PRR as detected by an uninfused manometric system is due to the sealing of the recording orifice by the sphincter and that it does not reliably indicate the location of the diaphragmatic hiatus. Similarly, with the infused manometric recording system, the PRR would be predicted to occur at that point where the recording orifice at end-inspiration is first exposed to a site of lower pressure than at end-expiration. As pressures rise progressively from gastric fundus to the midpoint of the static HPZ and decline progressively above the midpoint of the static HPZ to the esophagus, the PRR will be found when the midpoint of the static HPZ lies somewhere below the recording orifice at end-inspiration. In studies dealing with the correlation between the competence of the lower esophageal sphincter and the magnitude of the pressure recorded from within the HPZ, there has been a lack of uniformity in the manner of calculating the magnitude of the HPZ. Some 7 • 8 have taken the highest mean pressure within the phasic HPZ, while others 9 have tabulated the end-expiratory pressure gradient between HPZ and stomach. Recognition that the static HPZ changes position during the respiratory cycle suggests that the former method of pressure measurement does not assess the true maximal sphincter pressure because the recording orifice will be monitoring a sub maximal portion of the static HPZ during at least half of the respiratory cycle. Perhaps the best measurement of maximal sphincter pressure would be the highest end-inspiratory or end-expiratory pressure found within the phasic HPZ.
387
Because the maximum pressure within the static HPZ was the same regardless of its length, it is unlikely that length of the static HPZ is simply a function of the force of closure of the sphincter mechanism. Although heretofore the literature has stressed only sphincter pressure as a measure of sphincter competence, it is possible that sphincter length (as measured by the static HPZ) is also important in determining the effectiveness of the sphincter as a barrier against gastroesophageal reflux. Christensen and Lund 14 have studied the response of mammalian (opossum) esophageal smooth muscle in vivo and in vitro to balloon distention. They have demonstrated a localized contraction of the longitudinal muscle in the vicinity of the distending stimulus, termed the " duration response," which persists as long as the proximal esophagus is distended and results in a shortening of the entire organ and elevation of the cardia. Such a contraction of esophageal longitudinal muscle may well have accounted for the elevation of the gastroesophageal junction with balloon distention in man observed in this study. In addition to elevation, a previously unrecognized change in the lower esophageal sphincter-shortening-was shown by this study to occur with balloon distention. This shortening averaged 40% of resting sphincter length and was accompanied by an average fall in sphincter pressure of 65%. Further studies of the relationship of these changes to the location and volume of the distending balloon and of their alteration by autonomic drugs are necessary to clarify the mechanism of these potentially important aspects of sphincter physiology. The manner in which the manometric HPZ shortens following balloon distention is not explained by this study. It is possible that the sphincter is actually compressed into a shorter length, for instance, by a local contraction of the longitudinal muscle in the region of the sphincter. In their studies of the isolated opossum esophagus, however, Christensen and Lund 14 observed such a contraction only
388
Vol. 62, No.3
WINANS
adjacent to the distending balloon and not in the distal esophagus. A more likely explanation for the shortening of the static HPZ with balloon distention is that a generalized decrease in tone occurs along the length of the sphincter, resulting in the disappearance of measurable tone at the margins where the pressure is already lowest in the resting state. In this study proximal esophageal balloon distention was used to prolong the effect normally produced by swallowing on the lower esophageal high pressure zone. Although it is not possible to state with certainty that this maneuver alters the lower esophageal sphincter in the same way or to the same extent as deglutition, this study does indicate that the sphincter's location and length, as well as its magnitude, are capable of alteration, and this fact should be considered in interpreting the fall in pressure within the phasic HPZ following swallowing. Rinaldo and Clark,15 using a combined cineradiographic and manometric technique, previously recognized that this "relaxation" may, in fact, be due to proximal movement of the sphincter. This study confirms their contention but demonstrates that a genuine decrease in sphincter tone occurs as well. The observed pressure changes within the phasic HPZ with swallowing would seem to represent a combination of the two effects. Thus, at the distal end of the phasic HPZ (at positions as shown at recording points 2 and 3 in fig. 5) a 2-cm elevation of the distal margin of the sphincter would leave the recording orifice exposed to intragastric pressures throughout the entire respiratory cycle. A decrease in pressure recorded from either of these two orifices after a swallow would, therefore, be solely a result of change in position of the sphincter and not reflect a change in sphincter tone. On the other hand, at points higher in the phasic HPZ (for example, at orifice 4 in fig. 5) the orifice would remain within the sphincter even after a 2-cm elevation, and the fall in recorded pressure following deglutition would, therefore,
result from a change in sphincter tone as well as position. REFERENCES 1. Fyke FE, Code CF, Schlegel JF: The gastroesoph-
ageal sphincter in healthy human beings. Gastroenterologia 86: 135- 150, 1956 2. Pert JH, Davidson M, Almy TP, et al: Esophageal catheterization studies. I. The mechanism of swallowing in normal subjects with particular reference to the vestibule. J Clin Invest 38:397406, 1959
3. Nagler R, Spiro HM: Serial esophageal motility studies in asymptomatic young subjects. Gastroenterology 41 :371-379, 1961 4. Atkinson M, Edwards DA W, Honour AJ, et al: Comparison of cardiac and pyloric sphincters. Lancet 2:918- 922, 1957 5. Kelley ML, Wilbur DL, Schlegel JF, et al : Deglutitive responses in the gastroesophageal sphincter of healthy human beings. J Appl Physiol 15:483- 488, 1960 6. Johnson HD: The cardia and hiatus hernia. Springfield, Illinois, Charles C Thomas, 1968, p 17-30
7. Winans CS, Harris LD: Quantitation of lower esophageal sphincter competence. Gastroenterology 52:773- 778, 1967 8. Pope CE: A dynamic test of sphincter strength: its application to the lower esophageal sphincter. Gastroenterology 52:779- 786, 1967 9. Haddad JK: Relation of gastroesophageal reflux to yield sphincter pressures. Gastroenterology 58: 175- 184, 1970 10. Creamer B, Schlegel JF: Motor responses of the esophagus to distention. J Appl Physiol 10:498504, 1957 11. Fleshier B, Hendrix TR, Kramer P, et al : The
12.
13.
14.
15.
characteristics and similarity of primary and secondary peristalsis of the esophagus. J Clin Invest 38: 110- 116, 1959 Clark MD, Rinaldo JA, Eyler WR: Correlation of manometric and radiologic data from the esophagogastric area. Radiology 94:261- 270, 1970 Harris LD, Pope CE: The pressure inversion point; its genesis and reliability. Gastroenterology 51 :641- 648, 1966 Christensen J, Lund GF: Esophageal responses to deglutition and electrical stimulation. J Clin Invest 48:408- 419, 1969 Rinaldo JA, Clark MD: Manometric consequences of movement of the inferior esophageal sphincter during swallowing (abstr.). Gastroenterology 48:842, 1965