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Effect of peristaltic dysfunction on esophageal volume clearance
GASTROENTEROLOGY
1988;94:73-80
Effect of Peristaltic I?ysfunction on Esophageal Volume Clearance P. J. KAHRILAS,
W. J. DODDS, and W. J. HOGAN
Department of Medicine, Northwestern University Medical School and Veterans Administration Lakeside Medical Center, Chicago, Illinois; Departments of Radiology and Medicine, The Medical College of Wisconsin, Milwaukee, Wisconsin
Prolonged esophageal acid clearance, found in some patients with esophagitis, can be attributed in part to the peristaltic dysfunction observed in this population. In this study, we undertook to define the effect of commonly observed peristaltic dysfunction on volume clearance by obtainjng concurrent videofluoroscopic and manometric recordings in patients with nonobstructive dysphagia or heartburn. Excellent correlation existed between the findings from the two studies. A single normal peristaltic wave resulted in 100% clearance of a barium bolus from the esophagus. At each recording site, luminal closure, as demonstrated by videofluoroscopy, coincided with the upstroke of the peri#altic pressure complex. Absent or incomplete perista!tic c&tractions invariably resulted in little or no volume clearance from the involved segment. Regional hypotensive peristalsis was associated with incomplete volume clearance by the mechanism of retrograde escape of barium through the region of hypotensive contraction. The regional peristaltic amplitude required to prevent retrograde escape of barium was greater in the distal compared with the proximal esophagus. The mean peristaltic amplitude associated with instances of retrograde escape was 25 mmHg in the distal esophagus compared with 12 mmHg in the proximal esophageal segments. Thus, the peristaltic dysfunction commonly seen in patients with esophagitis (failed and hypotensive peristalsis) likely leads to impaired volume clearance. sophageal peristaltic function is compromised in a significant minority of patients with peptic esophagitis (12). Such patients have been found to have a high incidence of failed peristalsis and hypotensive peristaltic foci in the esophagus relative to control populations. The incidence of these motor abnormalities has been found to increase with the severity of gastroesophageal reflux disease. Esopha-
E
geal acid clearance is prolonged in a significant fraction of patients with gastroesophageal reflux disease (3-5). Normally, esophageal acid clearance depends on two processes: first, successful volume clearance by primary or secondary peristalsis, and second, neutralization of the residual acid by swallowed saliva (6,7). Defective peristaltic function may reduce the efficacy of esophageal volume clearance. We undertook to test this hypothesis by the concurrent analysis of esophageai motor function by manometry and volume clearance by videofluoroscopy during barium swallows. Methods Concurrent manometric and videofluoroscopic recordings were obtained in 11 patients with nonobstructive dysphagia (n = 4) or heartburn (n = 9), or both. The patients had been scheduled for both studies as part of their clinical evaluation; therefore, doing the studies concurrently rather than individually expedited the patients’ clinical evaluation. The study protocol was approved by the Human Research Review Committee of the Medical College of Wisconsin in January 1986. The mean age of the patients was 41 yr (range 26-73 yr). None of the patients had an esophageal stricture or other morphologic abnormality to account for their dysphagia. Six patients had endoscopic findings of esophagitis. Seven of the patients had a small- to moderate-sized sliding hiatal hernia: none had a large hiatal hernia. Intraluminal manometry was done with a round, 4.5 mm-diameter, 8-lumen recording assembly that had metallic markers at each recording site. The recording sites were located at the distal end of the assembly and at s-cm intervals proximal to that. The assembly was passed via the nose and positioned with the distal recording site 1 cm proximal to the lower esophageal sphincter so that the assembly did not traverse the lower esophageal sphincter. During swallow sequences, each recording orifice was perfused with sterile water at 0.5 ml/min by a low0 1988 by the American
Gastroenterological 0018.5085/88/$3.50
Association
74 KAHRfLAS ET AL.
GASTROENTEROLOGY Vol. 94,No. 1
compliance pneumohydraulic pump (8). Each lumen of the catheter assembly was connected to a pressure transducer (model 33db; Gould Inc., Oxnard, Calif.). Transducer output was displayed on an 8-channel polygraph recorder (Sensormedics Corp., Anaheim, Calif.). The paper speed of the recorder was set at 10 mm/s during swallow sequences. Seven polygraph channels were used for pressure recording. After placement of the manometric assembly, the patient lay supine in an oblique position on a fluoroscopy table so that the esophagus was well imaged without vertebral interference. The video output of the fluoroscope was connected to a resettable counter/timer (model K-436; Thalner Electronics Laboratories Inc., Ann Arbor, Mich.) that encoded an analog time display on the video image in hours, minutes, seconds, and hundredths of a second. The modified image was then recorded on videotape with a Betamax (Sony model SL HF 900) recorder. In addition to encoding the video signal, the timer also delivered a 5-ms pulse to the eighth channel of the polygraph recorder at l-s intervals (corresponding to whole seconds on tbe analog display). Thus, the manometric record was precisely correlated in time with the video image derived from fluorosCOPY. A total of 10-15 swallow sequences were recorded from each subject. For each sequence, 6 ml of barium suspen-
UESX
sion was injected into the mouth by syringe after which the patient was instructed to take a single swallow. The fluoroscope was first panned over the length of the esophagus and then centered on the advancing edge of the peristaltic stripping wave. The timer was reset to zero after each sequence. The swallow sequence number was indicated by the hour notation on ‘the video image and by notation on the manometric record. Data analysis was initiated by slow motion playback of the videotapes without referring to the manometric record. Each barium swallow was classified as to the degree of barium clearance: complete, partial, or absent. In instances of complete volume clearance, the instant that the tail of the stripping wave arrived at each recording orifice was determined. In instances of absent or partial volume clearance, the time of failure and the location of residual barium were additionally noted. Failed peristaltic sequences were further described by the site of peristaltic failure and whether or not failure was accompanied by a simultaneous contraction in the distal esophagus. The manometric record was then analyzed. After the swallow sequences were first judged to be peristaltic or nonperistaltic, the tracings were analyzed for the onset and peak amplitude of contractile activity at each of the seven recording sites. The occurrence of repetitive contractions and simultaneous pressure events was noted. Data from
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1. Concurrent manometric and video recording of a 5-ml barium swallow. The tracings from the video images on the right show the distribution of the barium column at the times indicated above the individual tracings and by arrows on the manometric record. In this example, a single peristaltic sequence completely cleared the barium bolus from the esophagus, resulting in 100% volume clearance. Pharyngeal injection of barium into the esophagus occurs at the 1.0-smark. The entry of barium causes distention and a slightly increased intraluminal pressure, as indicated by the downward-pointing arrows marked "1 s." Shortly thereafter, esophageal peristalsis is initiated. During esophageal peristalsis, luminal closure and hence the tail of the barium bolus passed each recording site concurrent with the onset of the manometric pressure wave. Hence, at 1.5 s, the peristaltic contraction had just reached the proximal recording site and barium had been stripped from the esophagus proximal to that point. Similarly, at 4.2 s, the peristaltic contraction was beginning at the third recording site and, correspondingly, the tail of the barium bolus was located at the third recording site. Finally, after completion of the peristaltic contraction (time 13.8 s), all of the barium had been cleared into the stomach.
PERISTALTIC DYSFUNCTION VS. VOLUME CLEARANCE 75
January 1988
the videofluoroscopic and manometric records were then correlated. The esophagus was divided into four anatomic regions (distal or ampullary, retrocardiac, aortic arch, and cervical) to normalize regional data among individuals of different height. Peristaltic amplitudes associated with incomplete barium clearance were expressed as mean * 1 SD. Comparison of data among anatomic locations was accomplished by a one-way analysis of variance.
jection of barium. This minor elevation, caused by intrabolus pressure, was eliminated with the passage of a peristaltic stripping wave. In 12 instances, double- or triple-peaked contractions were recorded manometrically during passage of peristaltic pressure waves that were clearly progressive between adjacent recording sites. Multipeaked peristaltic contractions were not associated with any abnormality of volume clearance. The stripping wave corresponded to the upstroke of the manometrically recorded pressure wave. Were it not for the manometric record, there would have been no evidence that a multipeaked contraction had occurred.
Results Complete
Volume Clearance
In 61 of 152 recorded swallows, a single peristaltic sequence completely cleared the entire barium bolus from the esophagus (Figure 1). At each manometric recording site, luminal closure, effected by passage of the leading edge of the stripping wave, invariably occurred within 0.2 s of the upstroke of the peristaltic pressure wave. The minor increase in intraesophageal pressure that occurred coincident with the swallow itself (indicated by the downwardpointing arrows in Figure 1) corresponded to the area of esophagus distended by the pharyngeal in-
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peristalsis failed to traverse the entire length of the esophagus. In the 12 instances of absent peristalsis, a stripping wave did not develop in the esophagus and virtually the entire swallowed bolus remained in the esophageal body. The manometric record of such
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Little or no volume clearance occurred during the 28 recorded sequences in which esophageal
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Figure 2. As in Figure 1, the tracings from the video images on the right depict the distribution of the barium bolus at the times indicated by arrows on the manometric record. In this example, minimal volume clearance occurs due to a failed peristaltic contraction, The peristaltic stripping wave progressed beyond the aortic arch to the middle of the esophagus and failed to propagate further, thereby leaving most of the barium bolus in the distal esophagus. The manometric correlate of this event is shown on the left. The initial esophageal stripping action is associated with a feeble peristaltic contraction that progressed only as far as had the stripping wave. After the failure of the sequential peristaltic contraction, indicated by the 11.8-s mark, simultaneous waves were recorded from within the common cavity of the barium-distended esophagus. The simultaneous waves, recorded from the distal three recording sites, were of low amplitude and nearly identical waveform. These could represent either a pressure wave transmitted through the barium column or a non-lumen-obliterating contraction in the open esophageal segment. After the termination of contractile activity (15 s) some barium was redistributed into the thoracic esophagus. This retrograde movement could be passive or, again, the result of the non-lumen-obliterating contraction of the distal esophageal segment.
76
KAHRILAS ET AL.
GASTROENTRROLOGY Vol. 94, No. 1
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-_t--_ ‘yp Manametry / Figure 3. The tracings from the video recording on the right depict the distribution of the barium bolus at the times indicated by arrows on the manometric record. This example is another variant of a failed peristaltic contraction resulting in impaired barium clearance. As in Figure 2, the stripping wave progressed to beyond the aortic arch. However, in this example the peristaltic sequence terminated with a simultaneous contraction rather than as simultaneous waves in the distal esophagus. On videofluoroscopy, the simultaneous contraction was seen as a tertiary contraction that trapped small collections of barium in the distal esophageal body, while forcing the remainder either distally into the stomach or retrograde up the esophagus (9.3-s image]. Manometrically, the simultaneous contraction was distinguishable from the simultaneous pressure wave in Figure 2 in that the waveforms were dissimilar at recording sites 5-7 and the instantaneous pressure recorded within the contracted segment exceeded that recorded proximally (recording sites 14). The distinction between a simultaneous wave and a simultaneous contraction, however, was most evident on videofluoroscopy. The simultaneous wave occurred over a length of distended, open esophagus, as in Figure 2, whereas the simultaneous contraction occurred over a length of contracted, closed esophagus, as in this example.
instances revealed only a slight, abrupt increase in intraluminal pressure occurring coincident viriththe pharyngeal injection of barium and recorded from the segment of esophageal body distended by the swallowed barium. In the remaining 16 instances, the stripping wave progressed part way down the esophagus and then failed to progress further. Most commonly, the site of failure was at, or immediately distal to, the aortic arch. Figure 2 depicts the manometric and videofluoroscopic record of a failed peristaltic sequence. As in Figure 1, the swallow results in the distention of a significant length of the esophageal body. Barium entry is followed by a feeble peristaltic contraction recorded only from the recording orifices in the proximal esophagus. Beyond
the termination site of peristalsis, simultaneous pressure waves were recorded from the distal manometric recording sites situated within the common cavity of the barium-distended esophagus. The simultaneous pressure waves were of low amplitude and nearly identical waveform and were not associated with luminal closure. These pressure waves could result from either non-lumen-obliterating contraction of the involved esophageal segment or from a transmitted pressure wave from the proximal esophagus. Intraluminal manometry cannot distinguish between these possible explanations. Another variant of failed peristalsis is illustrated in Figure 3. In this instance, a peristaltic contraction progressed part way down the esophagus and then
PERISTALTIC DYSFUNCTION VS. VOLUME CLEARANCE
January 1988
77
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Figure 4. The tracings from the video images on the right depict the distribution of the barium bolus at the times indicated by arrows on the manometric record. In this example, a single swallow transported the majority of barium to the stomach but left a residual collection in the esophagus. Retrograde escape of barium through the peristaltic contraction was evident at the 8-s mark in the region of the aortic arch. The peristaltic amplitude associated with this escape phenomenon was 13 mmHg, inscribed from the second most orad recording site. Incidentally, three of the distal recording sites in this example inscribed multipeaked contractions after a normally conducted initiation of contraction. Were it not for the manometric record, there would be no hint of these repetitive contractions because the videofluoroscopy only yields information on esophageal closure and provides no further imaging of contractile activity in the collapsed segment.
terminated with a simultaneous contraction of the distal esophagus. On videofluoroscopy, the simultaneous contraction was seen as a tertiary contraction, trapping a small amount of barium in the involved segment while forcing the remainder either distally into the stomach or retrograde up the esophagus. The manometric correlate of this simultaneous contraction was similar to the simultaneous waves in the distal recording site of Figure 2. However, in the case of the lumen-obliterating contraction (Figure 3), the waveforms among recording sites were less similar and the instantaneous pressure recorded within the contracted segment slightly exceeded that recorded proximal to the contracted segment. The distinction between a simultaneous wave and a simultaneous contraction, however, was most evident on the videofluoroscopic correlate of the manometric record. A simultaneous wave occurred over a length of
distended, open-lumened esophagus, as in Figure 2, while a simultaneous contraction occurred over a length of contracted, closed esophagus, as in Figure 3.
Partial Volume Clearance In 63 instances, a single swallow transported most of the swallowed barium to the stomach, but a small residual collection of barium remained in the esophagus. Fluoroscopically, partial volume clearance occurred in one of two ways. In some instances, the stripping wave ceased to be lumen-obliterating over a short segment of the esophagus, despite being effective proximal and distal to that segment. In other instances, the barium bolus squirted retrograde through the advancing stripping wave. A common site of partial volume clearance, or retrograde escape
78
KAHRILAS ETAL.
GASTROENTEROLOGY Vol. 94, No. 1
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Figure 5. The tracings from the video images on the right depict the distribution of the barium bolus at the times indicated by arrows on the manometric record. In this example, a small amount of barium escaped retrograde through the peristaltic contraction in the distal esophagus and left a small residual pool in the esophageal ampulla after the passage of the peristaltic contraction. The amplitude of the peristaltic contraction associated with the bolus escape was 22 mmHg, inscribed from the most distal recording site.
of the barium bolus, was in the region of the aortic arch, as illustrated in Figure 4. In this example, the peristaltic amplitude associated with the escape phenomenon was 13 mmHg, inscribed from the second most orad manometric recording site. In other instances, such as in Figure 5, retrograde escape of barium occurred in the distal esophagus. The peristaltic amplitude associated with the escape shown in Figure 5 was 22 mmHg, inscribed from the most distal manometric recording site. Figure 6 illustrates the relative efficacy of all observed peristaltic contraction amplitudes in each esophageal region in terms of volume clearance. The peristaltic amplitudes associated with retrograde escape of barium were significantly different among the esophageal segments (p < O.OOl),such that the mean amplitudes were higher in the distal compared with the proximal esophageal segments (cervical 12 + 4 mmHg, aortic arch 11 rf: 6 mmHg, retrocardiac 19 + 6 mmHg, ampulla 25 f 6 mmHg). Similarly, the
peristaltic amplitude necessary to ensure against any instances of escape was greater distally (cervical 18 mmHg, aortic arch 25 mmHg, retrocardiac 30 mmHg, ampullary 43 mmHg). Barium escape never occurred in the proximal esophageal segments when the peristaltic amplitude was ~20 mmHg. On the other hand, barium escape invariably occurred in the distal esophagus when the peristaltic amplitude was ~20 mmHg. Additionally, barium escape was likely in the distal esophagus when peristaltic amplitude was 21-30 mmHg (19 of 32 instances), but occurred infrequently (3 of 37 instances) when peristaltic amplitude was 31-45 mmHg. Discussion Esophageal volume clearance, accomplished by primary or secondary esophageal peristalsis, is the initial step in the process of esophageal acid clearance. Because peristaltic function is frequently
PERISTALTIC DYSFUNCTION VS. VOLUME CLEARANCE
January 1968
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6. Summary
data on partial volume clearance categorized by esophageal region Each data point represents the peristaltic amplitude recorded in the indicated esophageal segment. Open circles indicate instances of retrograde escape and incomplete esophageal barium clearance. Closed circles indicate instances of complete esophageal barium clearance. The Iorge, closed circles in the ~50 mmHg row indicate that in numerous trials, there were no recorded instances of incomplete volume clearance. Inspection of the figure suggests that although negligible peristaltic amplitudes can effect complete esophageal volume clearance in the proximal esophagus, a value of about 30 mmHg is required in the distal esophageal segments to ensure against all but an occasional instance of escape.
impaired in patients with gastroesophageal reflux disease (l), we sought to identify the consequences of peristaltic dysfunction on volume clearance. This analysis was accomplished by obtaining synchronized, concurrent manometric and videofluoroscopic evaluations of swallowing in symptomatic supine individuals. In the process of doing these studies, we also gained information about the manometric determinants of successful volume clearance. Previous analyses of esophageal volume clearance (9-12) have used a radionuclide-labeled bolus and serial scanning with a y-camera to assess esophageal transit time. The radionuclide method works well to identify patients with extreme prolongations of esophageal transit, as is the case with achalasia, esophageal spasm, and scleroderma (10,ll). However, in the case of patients with gastroesophageal reflux disease, the mean transit time for a radiolabeled bolus is typically normal, indicating that, on
79
the average, a single peristaltic sequence results in virtually complete clearance. Only a rough subdivision of the esophagus is possible with the radionuelide imaging technique. Therefore, we used concurrent fluoroscopy and manometry to perform a discrete, focal analysis of the efficacy of single peristaltic sequences on esophageal volume clearance. This methodology provides a high temporal and spatial resolution not possible with radionuclide imaging. A provocative finding of this study pertains to the minimal peristaltic pressure amplitude required for regional esophageal volume clearance in supine subjects. Some data relevant to this issue were reported recently by Richter and coworkers, who found three instances (two after atropine administration) in which peristaltic contractions of 530 mmHg amplitude were ineffective in promoting complete isotope clearance in the distal esophagus (12). We recorded 63 instances of partial volume clearance and were able to do a regional analysis of peristaltic efficacy. The analysis showed that, although negligible peristaltic amplitude was effective for volume clearance in the proximal esophagus, more forceful contraction strength was required distally. This difference is probably related to the compliance of the esophageal segments distal to the advancing bolus. For the proximal esophagus, the distal esophageal segment is highly compliant because it has negligible resting tone, is subject to descending inhibition ahead of the contraction wave, and is situated in the negative pressure zone of the thoracic cavity. However, as the peristaltic contraction progresses distally, the segment distal to the contraction wave becomes less compliant because the lower esophageal sphincter must be opened by the bolus and the bolus pushed against a pressure gradient into the stomach. The findings of this study suggest that the minimum effective contraction strength for clearance in the distal esophagus is 20 mmHg, whereas in the proximal esophagus, virtually any propagated contraction will effectively empty the esophagus, The peristaltic amplitudes required for invariable bolus clearance were 16 mmHg in the proximal esophagus and 30-40 mmHg in the distal esophagus (Figure 6). In a previous analysis of peristaltic dysfunction among patients with gastroesophageal reflux disease, we used a statistical analysis of data from normal volunteers and patient controls to determine a value of 27 mmHg as the lower limit of normal peristaltic amplitude in the distal esophagus (1). The findings from the present study provide an additional rationale for a threshold value of about 30 mmHg and serve to strengthen the previous analysis. Our main intent in this study was to define the relationship between the manometric and fluoro-
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KAHRILAS ET AL.
scopic evaluations of peristalsis. As suggested previously, excellent correlation exists between the manometric and fluoroscopic evaluations of esophageal peristalsis (13). On the other hand, the two studies are complementary to one another, with each providing unique information. Fluoroscopy details anatomic aspects of the esophagus as well as motor function, whereas manometry quantifies the variables of peristaltic contractions. In this study, peristaltic sequences that were normal manometrically were normal on videofluoroscopy. The progression of the esophageal stripping wave coincided precisely with the progression. of the peristaltic contraction, such that luminal closure at each esophageal locus occurred concurrent with the upstroke of the peristaltic contraction. In contrast, failed peristaltic sequences, with or without accompanying simultaneous contractions, resulted in minimal esophageal volume clearance. Hypotensive peristaltic sequences achieved varying degrees of partial volume clearance depending on the severity of retrograde escape through the hypotensive peristaltic segment. The correlation between videofluoroscopy and manometry shown in this study infers that the abnormalities found in a significant proportion of patients with esophagitis (failed and hypotensive peristalsis) would be expected to prolong the process of esophageal volume clearance when the patients were recumbent (1). Thus, esophageal peristaltic dysfunction, along with occasional abnormalities of salivation (14) and in some cases repeated instances of re-reflux that occur during the process of acid clearance (IS), may all act to prolong the process of normal esophageal acid clearance in some patients with gastroesophageal reflux disease.
References 1.
2.
Kahrilas PJ, Dodds WJ, Hogan WJ, Kern M, Arndorfer RC, Reece A. Esophageal peristaltic dysfunction in peptic esophagitis. Gastroenterology 1986;91:897-904. Gill RC, Bowes KL, Murphy PD, Kingma YJ. Esophageal motor abnormalities in gastroesophageal reflux and the effects of fundoplication. Gastroenterology 1986;91:364-9.
GASTROENTEROLOGY Vol. 94, No. 1
3. Stanciu C, Bennett JR. Oesophageal 4. 5. 6.
7.
8.
9.
10.
11.
12.
acid clearing: one factor in the production of reflux esophagitis. Gut 1974;15:852-7. Booth DJ, Kemmerer WT, Skinner DB. Acid clearing from the distal esophagus. Arch Surg 1968;96:731-4. Dodds WJ, Hogan WJ, Miller WN. Reflux esophagitis. Am J Dig Dis 1976;21:49-67. Helm JF, Dodds WJ, Pelt LR, Palmer DW, Hogan WJ, Teeter BC. Effect of esophageal emptying and saliva on clearance of acid from the esophagus. N Engl J Med 1984;310:284-8. Helm JF, Dodds WJ, Riedel DR, Teeter BC, Hogan WJ, Arndorfer RC. Determinants of esophageal acid clearance in normal subjects. Gastroenterology 1983;85:607-12. Arndorfer RC, Stef JJ, Dodds WJ, Linehan JH, Hogan WJ. Improved infusion system for intraluminal esophageal manometry. Gastroenterology 1977;73:23-7. Phaosawasdi K, Malmud LS, Tolin SD, Stelzer F, Applegate G, Fisher RS. Cholinergic effects on esophageal transit and clearance. Gastroenterology 1981;81:915-20. Tolin RD, Malmud LS, Reilley J, Fisher RS. Esophageal scintigraphy to quantitate esophageal transit (quantitation of esophageal transit). Gastroenterology 1979;76:1402-8. Russel COH, Hill LD, Holmes ER, Hull DA, Gannon R, Pope CE. Radionuclide transit: a sensitive screening test for esophageal dysfunction. Gastroenterology 1981;80:887-92. Richter JE, Blackwell JN, Wu WC, Johns DN, Cowan RJ, Caste11 DO. Relationship of radionuclide liquid bolus transport and esophageal manometry. J Lab Clin Med 1987;109:
217-24. 13. Dodds WJ. 1976 Walter B. Cannon lecture: current concepts
of esophageal motor function: clinical implications for radiology. Am J Roentgen01 1977;128:549-61. M, Dodds WJ, Hogan WJ, Lipman S. 14. Helm JF, Allendorph Loss of the salivary response to esophageal acid perfusion in patients with peptic stricture (abstr). Gastroenterology 1986; 90:1456. 15. Mittal RK, Lange RC, McCallum RW. Identification and mechanism of delayed esophageal acid clearance in subjects with hiatus hernia. Gastroenterology 1987;92:130-5.
Received April 27, 1987. Accepted July 29, 1987. Address requests for reprints to: P. J. Kahrilas, M.D., Northwestern University Medical School, GI Section, Department of Medicine, 1526 Wesley Pavilion, Chicago, Illinois 60611. This work was presented at the biannual meeting of the American Motility Society in Houston, Texas on October 29, 1986 and was published in abstract form in Gastroenterology 1986;91:1057. This work was supported by a fellowship from the Schweppe Foundation (P.J.K.), grant NIH-BRSG RR-05370 from the U.S. Public Health Service (P.J.K.), and grant AM 25731 from the National Institutes of Health (W.J.D.).
1988;94:73-80
Effect of Peristaltic I?ysfunction on Esophageal Volume Clearance P. J. KAHRILAS,
W. J. DODDS, and W. J. HOGAN
Department of Medicine, Northwestern University Medical School and Veterans Administration Lakeside Medical Center, Chicago, Illinois; Departments of Radiology and Medicine, The Medical College of Wisconsin, Milwaukee, Wisconsin
Prolonged esophageal acid clearance, found in some patients with esophagitis, can be attributed in part to the peristaltic dysfunction observed in this population. In this study, we undertook to define the effect of commonly observed peristaltic dysfunction on volume clearance by obtainjng concurrent videofluoroscopic and manometric recordings in patients with nonobstructive dysphagia or heartburn. Excellent correlation existed between the findings from the two studies. A single normal peristaltic wave resulted in 100% clearance of a barium bolus from the esophagus. At each recording site, luminal closure, as demonstrated by videofluoroscopy, coincided with the upstroke of the peri#altic pressure complex. Absent or incomplete perista!tic c&tractions invariably resulted in little or no volume clearance from the involved segment. Regional hypotensive peristalsis was associated with incomplete volume clearance by the mechanism of retrograde escape of barium through the region of hypotensive contraction. The regional peristaltic amplitude required to prevent retrograde escape of barium was greater in the distal compared with the proximal esophagus. The mean peristaltic amplitude associated with instances of retrograde escape was 25 mmHg in the distal esophagus compared with 12 mmHg in the proximal esophageal segments. Thus, the peristaltic dysfunction commonly seen in patients with esophagitis (failed and hypotensive peristalsis) likely leads to impaired volume clearance. sophageal peristaltic function is compromised in a significant minority of patients with peptic esophagitis (12). Such patients have been found to have a high incidence of failed peristalsis and hypotensive peristaltic foci in the esophagus relative to control populations. The incidence of these motor abnormalities has been found to increase with the severity of gastroesophageal reflux disease. Esopha-
E
geal acid clearance is prolonged in a significant fraction of patients with gastroesophageal reflux disease (3-5). Normally, esophageal acid clearance depends on two processes: first, successful volume clearance by primary or secondary peristalsis, and second, neutralization of the residual acid by swallowed saliva (6,7). Defective peristaltic function may reduce the efficacy of esophageal volume clearance. We undertook to test this hypothesis by the concurrent analysis of esophageai motor function by manometry and volume clearance by videofluoroscopy during barium swallows. Methods Concurrent manometric and videofluoroscopic recordings were obtained in 11 patients with nonobstructive dysphagia (n = 4) or heartburn (n = 9), or both. The patients had been scheduled for both studies as part of their clinical evaluation; therefore, doing the studies concurrently rather than individually expedited the patients’ clinical evaluation. The study protocol was approved by the Human Research Review Committee of the Medical College of Wisconsin in January 1986. The mean age of the patients was 41 yr (range 26-73 yr). None of the patients had an esophageal stricture or other morphologic abnormality to account for their dysphagia. Six patients had endoscopic findings of esophagitis. Seven of the patients had a small- to moderate-sized sliding hiatal hernia: none had a large hiatal hernia. Intraluminal manometry was done with a round, 4.5 mm-diameter, 8-lumen recording assembly that had metallic markers at each recording site. The recording sites were located at the distal end of the assembly and at s-cm intervals proximal to that. The assembly was passed via the nose and positioned with the distal recording site 1 cm proximal to the lower esophageal sphincter so that the assembly did not traverse the lower esophageal sphincter. During swallow sequences, each recording orifice was perfused with sterile water at 0.5 ml/min by a low0 1988 by the American
Gastroenterological 0018.5085/88/$3.50
Association
74 KAHRfLAS ET AL.
GASTROENTEROLOGY Vol. 94,No. 1
compliance pneumohydraulic pump (8). Each lumen of the catheter assembly was connected to a pressure transducer (model 33db; Gould Inc., Oxnard, Calif.). Transducer output was displayed on an 8-channel polygraph recorder (Sensormedics Corp., Anaheim, Calif.). The paper speed of the recorder was set at 10 mm/s during swallow sequences. Seven polygraph channels were used for pressure recording. After placement of the manometric assembly, the patient lay supine in an oblique position on a fluoroscopy table so that the esophagus was well imaged without vertebral interference. The video output of the fluoroscope was connected to a resettable counter/timer (model K-436; Thalner Electronics Laboratories Inc., Ann Arbor, Mich.) that encoded an analog time display on the video image in hours, minutes, seconds, and hundredths of a second. The modified image was then recorded on videotape with a Betamax (Sony model SL HF 900) recorder. In addition to encoding the video signal, the timer also delivered a 5-ms pulse to the eighth channel of the polygraph recorder at l-s intervals (corresponding to whole seconds on tbe analog display). Thus, the manometric record was precisely correlated in time with the video image derived from fluorosCOPY. A total of 10-15 swallow sequences were recorded from each subject. For each sequence, 6 ml of barium suspen-
UESX
sion was injected into the mouth by syringe after which the patient was instructed to take a single swallow. The fluoroscope was first panned over the length of the esophagus and then centered on the advancing edge of the peristaltic stripping wave. The timer was reset to zero after each sequence. The swallow sequence number was indicated by the hour notation on ‘the video image and by notation on the manometric record. Data analysis was initiated by slow motion playback of the videotapes without referring to the manometric record. Each barium swallow was classified as to the degree of barium clearance: complete, partial, or absent. In instances of complete volume clearance, the instant that the tail of the stripping wave arrived at each recording orifice was determined. In instances of absent or partial volume clearance, the time of failure and the location of residual barium were additionally noted. Failed peristaltic sequences were further described by the site of peristaltic failure and whether or not failure was accompanied by a simultaneous contraction in the distal esophagus. The manometric record was then analyzed. After the swallow sequences were first judged to be peristaltic or nonperistaltic, the tracings were analyzed for the onset and peak amplitude of contractile activity at each of the seven recording sites. The occurrence of repetitive contractions and simultaneous pressure events was noted. Data from
__*----.
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Figure
1. Concurrent manometric and video recording of a 5-ml barium swallow. The tracings from the video images on the right show the distribution of the barium column at the times indicated above the individual tracings and by arrows on the manometric record. In this example, a single peristaltic sequence completely cleared the barium bolus from the esophagus, resulting in 100% volume clearance. Pharyngeal injection of barium into the esophagus occurs at the 1.0-smark. The entry of barium causes distention and a slightly increased intraluminal pressure, as indicated by the downward-pointing arrows marked "1 s." Shortly thereafter, esophageal peristalsis is initiated. During esophageal peristalsis, luminal closure and hence the tail of the barium bolus passed each recording site concurrent with the onset of the manometric pressure wave. Hence, at 1.5 s, the peristaltic contraction had just reached the proximal recording site and barium had been stripped from the esophagus proximal to that point. Similarly, at 4.2 s, the peristaltic contraction was beginning at the third recording site and, correspondingly, the tail of the barium bolus was located at the third recording site. Finally, after completion of the peristaltic contraction (time 13.8 s), all of the barium had been cleared into the stomach.
PERISTALTIC DYSFUNCTION VS. VOLUME CLEARANCE 75
January 1988
the videofluoroscopic and manometric records were then correlated. The esophagus was divided into four anatomic regions (distal or ampullary, retrocardiac, aortic arch, and cervical) to normalize regional data among individuals of different height. Peristaltic amplitudes associated with incomplete barium clearance were expressed as mean * 1 SD. Comparison of data among anatomic locations was accomplished by a one-way analysis of variance.
jection of barium. This minor elevation, caused by intrabolus pressure, was eliminated with the passage of a peristaltic stripping wave. In 12 instances, double- or triple-peaked contractions were recorded manometrically during passage of peristaltic pressure waves that were clearly progressive between adjacent recording sites. Multipeaked peristaltic contractions were not associated with any abnormality of volume clearance. The stripping wave corresponded to the upstroke of the manometrically recorded pressure wave. Were it not for the manometric record, there would have been no evidence that a multipeaked contraction had occurred.
Results Complete
Volume Clearance
In 61 of 152 recorded swallows, a single peristaltic sequence completely cleared the entire barium bolus from the esophagus (Figure 1). At each manometric recording site, luminal closure, effected by passage of the leading edge of the stripping wave, invariably occurred within 0.2 s of the upstroke of the peristaltic pressure wave. The minor increase in intraesophageal pressure that occurred coincident with the swallow itself (indicated by the downwardpointing arrows in Figure 1) corresponded to the area of esophagus distended by the pharyngeal in-
d
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peristalsis failed to traverse the entire length of the esophagus. In the 12 instances of absent peristalsis, a stripping wave did not develop in the esophagus and virtually the entire swallowed bolus remained in the esophageal body. The manometric record of such
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Little or no volume clearance occurred during the 28 recorded sequences in which esophageal
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Minimal Volume Clearance
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Figure 2. As in Figure 1, the tracings from the video images on the right depict the distribution of the barium bolus at the times indicated by arrows on the manometric record. In this example, minimal volume clearance occurs due to a failed peristaltic contraction, The peristaltic stripping wave progressed beyond the aortic arch to the middle of the esophagus and failed to propagate further, thereby leaving most of the barium bolus in the distal esophagus. The manometric correlate of this event is shown on the left. The initial esophageal stripping action is associated with a feeble peristaltic contraction that progressed only as far as had the stripping wave. After the failure of the sequential peristaltic contraction, indicated by the 11.8-s mark, simultaneous waves were recorded from within the common cavity of the barium-distended esophagus. The simultaneous waves, recorded from the distal three recording sites, were of low amplitude and nearly identical waveform. These could represent either a pressure wave transmitted through the barium column or a non-lumen-obliterating contraction in the open esophageal segment. After the termination of contractile activity (15 s) some barium was redistributed into the thoracic esophagus. This retrograde movement could be passive or, again, the result of the non-lumen-obliterating contraction of the distal esophageal segment.
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KAHRILAS ET AL.
GASTROENTRROLOGY Vol. 94, No. 1
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15
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-_t--_ ‘yp Manametry / Figure 3. The tracings from the video recording on the right depict the distribution of the barium bolus at the times indicated by arrows on the manometric record. This example is another variant of a failed peristaltic contraction resulting in impaired barium clearance. As in Figure 2, the stripping wave progressed to beyond the aortic arch. However, in this example the peristaltic sequence terminated with a simultaneous contraction rather than as simultaneous waves in the distal esophagus. On videofluoroscopy, the simultaneous contraction was seen as a tertiary contraction that trapped small collections of barium in the distal esophageal body, while forcing the remainder either distally into the stomach or retrograde up the esophagus (9.3-s image]. Manometrically, the simultaneous contraction was distinguishable from the simultaneous pressure wave in Figure 2 in that the waveforms were dissimilar at recording sites 5-7 and the instantaneous pressure recorded within the contracted segment exceeded that recorded proximally (recording sites 14). The distinction between a simultaneous wave and a simultaneous contraction, however, was most evident on videofluoroscopy. The simultaneous wave occurred over a length of distended, open esophagus, as in Figure 2, whereas the simultaneous contraction occurred over a length of contracted, closed esophagus, as in this example.
instances revealed only a slight, abrupt increase in intraluminal pressure occurring coincident viriththe pharyngeal injection of barium and recorded from the segment of esophageal body distended by the swallowed barium. In the remaining 16 instances, the stripping wave progressed part way down the esophagus and then failed to progress further. Most commonly, the site of failure was at, or immediately distal to, the aortic arch. Figure 2 depicts the manometric and videofluoroscopic record of a failed peristaltic sequence. As in Figure 1, the swallow results in the distention of a significant length of the esophageal body. Barium entry is followed by a feeble peristaltic contraction recorded only from the recording orifices in the proximal esophagus. Beyond
the termination site of peristalsis, simultaneous pressure waves were recorded from the distal manometric recording sites situated within the common cavity of the barium-distended esophagus. The simultaneous pressure waves were of low amplitude and nearly identical waveform and were not associated with luminal closure. These pressure waves could result from either non-lumen-obliterating contraction of the involved esophageal segment or from a transmitted pressure wave from the proximal esophagus. Intraluminal manometry cannot distinguish between these possible explanations. Another variant of failed peristalsis is illustrated in Figure 3. In this instance, a peristaltic contraction progressed part way down the esophagus and then
PERISTALTIC DYSFUNCTION VS. VOLUME CLEARANCE
January 1988
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Figure 4. The tracings from the video images on the right depict the distribution of the barium bolus at the times indicated by arrows on the manometric record. In this example, a single swallow transported the majority of barium to the stomach but left a residual collection in the esophagus. Retrograde escape of barium through the peristaltic contraction was evident at the 8-s mark in the region of the aortic arch. The peristaltic amplitude associated with this escape phenomenon was 13 mmHg, inscribed from the second most orad recording site. Incidentally, three of the distal recording sites in this example inscribed multipeaked contractions after a normally conducted initiation of contraction. Were it not for the manometric record, there would be no hint of these repetitive contractions because the videofluoroscopy only yields information on esophageal closure and provides no further imaging of contractile activity in the collapsed segment.
terminated with a simultaneous contraction of the distal esophagus. On videofluoroscopy, the simultaneous contraction was seen as a tertiary contraction, trapping a small amount of barium in the involved segment while forcing the remainder either distally into the stomach or retrograde up the esophagus. The manometric correlate of this simultaneous contraction was similar to the simultaneous waves in the distal recording site of Figure 2. However, in the case of the lumen-obliterating contraction (Figure 3), the waveforms among recording sites were less similar and the instantaneous pressure recorded within the contracted segment slightly exceeded that recorded proximal to the contracted segment. The distinction between a simultaneous wave and a simultaneous contraction, however, was most evident on the videofluoroscopic correlate of the manometric record. A simultaneous wave occurred over a length of
distended, open-lumened esophagus, as in Figure 2, while a simultaneous contraction occurred over a length of contracted, closed esophagus, as in Figure 3.
Partial Volume Clearance In 63 instances, a single swallow transported most of the swallowed barium to the stomach, but a small residual collection of barium remained in the esophagus. Fluoroscopically, partial volume clearance occurred in one of two ways. In some instances, the stripping wave ceased to be lumen-obliterating over a short segment of the esophagus, despite being effective proximal and distal to that segment. In other instances, the barium bolus squirted retrograde through the advancing stripping wave. A common site of partial volume clearance, or retrograde escape
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KAHRILAS ETAL.
GASTROENTEROLOGY Vol. 94, No. 1
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1
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Figure 5. The tracings from the video images on the right depict the distribution of the barium bolus at the times indicated by arrows on the manometric record. In this example, a small amount of barium escaped retrograde through the peristaltic contraction in the distal esophagus and left a small residual pool in the esophageal ampulla after the passage of the peristaltic contraction. The amplitude of the peristaltic contraction associated with the bolus escape was 22 mmHg, inscribed from the most distal recording site.
of the barium bolus, was in the region of the aortic arch, as illustrated in Figure 4. In this example, the peristaltic amplitude associated with the escape phenomenon was 13 mmHg, inscribed from the second most orad manometric recording site. In other instances, such as in Figure 5, retrograde escape of barium occurred in the distal esophagus. The peristaltic amplitude associated with the escape shown in Figure 5 was 22 mmHg, inscribed from the most distal manometric recording site. Figure 6 illustrates the relative efficacy of all observed peristaltic contraction amplitudes in each esophageal region in terms of volume clearance. The peristaltic amplitudes associated with retrograde escape of barium were significantly different among the esophageal segments (p < O.OOl),such that the mean amplitudes were higher in the distal compared with the proximal esophageal segments (cervical 12 + 4 mmHg, aortic arch 11 rf: 6 mmHg, retrocardiac 19 + 6 mmHg, ampulla 25 f 6 mmHg). Similarly, the
peristaltic amplitude necessary to ensure against any instances of escape was greater distally (cervical 18 mmHg, aortic arch 25 mmHg, retrocardiac 30 mmHg, ampullary 43 mmHg). Barium escape never occurred in the proximal esophageal segments when the peristaltic amplitude was ~20 mmHg. On the other hand, barium escape invariably occurred in the distal esophagus when the peristaltic amplitude was ~20 mmHg. Additionally, barium escape was likely in the distal esophagus when peristaltic amplitude was 21-30 mmHg (19 of 32 instances), but occurred infrequently (3 of 37 instances) when peristaltic amplitude was 31-45 mmHg. Discussion Esophageal volume clearance, accomplished by primary or secondary esophageal peristalsis, is the initial step in the process of esophageal acid clearance. Because peristaltic function is frequently
PERISTALTIC DYSFUNCTION VS. VOLUME CLEARANCE
January 1968
______ ---,__ ___-_--.;__
Arch Esophageal Figure
--_----,
--
cardiac Region
6. Summary
data on partial volume clearance categorized by esophageal region Each data point represents the peristaltic amplitude recorded in the indicated esophageal segment. Open circles indicate instances of retrograde escape and incomplete esophageal barium clearance. Closed circles indicate instances of complete esophageal barium clearance. The Iorge, closed circles in the ~50 mmHg row indicate that in numerous trials, there were no recorded instances of incomplete volume clearance. Inspection of the figure suggests that although negligible peristaltic amplitudes can effect complete esophageal volume clearance in the proximal esophagus, a value of about 30 mmHg is required in the distal esophageal segments to ensure against all but an occasional instance of escape.
impaired in patients with gastroesophageal reflux disease (l), we sought to identify the consequences of peristaltic dysfunction on volume clearance. This analysis was accomplished by obtaining synchronized, concurrent manometric and videofluoroscopic evaluations of swallowing in symptomatic supine individuals. In the process of doing these studies, we also gained information about the manometric determinants of successful volume clearance. Previous analyses of esophageal volume clearance (9-12) have used a radionuclide-labeled bolus and serial scanning with a y-camera to assess esophageal transit time. The radionuclide method works well to identify patients with extreme prolongations of esophageal transit, as is the case with achalasia, esophageal spasm, and scleroderma (10,ll). However, in the case of patients with gastroesophageal reflux disease, the mean transit time for a radiolabeled bolus is typically normal, indicating that, on
79
the average, a single peristaltic sequence results in virtually complete clearance. Only a rough subdivision of the esophagus is possible with the radionuelide imaging technique. Therefore, we used concurrent fluoroscopy and manometry to perform a discrete, focal analysis of the efficacy of single peristaltic sequences on esophageal volume clearance. This methodology provides a high temporal and spatial resolution not possible with radionuclide imaging. A provocative finding of this study pertains to the minimal peristaltic pressure amplitude required for regional esophageal volume clearance in supine subjects. Some data relevant to this issue were reported recently by Richter and coworkers, who found three instances (two after atropine administration) in which peristaltic contractions of 530 mmHg amplitude were ineffective in promoting complete isotope clearance in the distal esophagus (12). We recorded 63 instances of partial volume clearance and were able to do a regional analysis of peristaltic efficacy. The analysis showed that, although negligible peristaltic amplitude was effective for volume clearance in the proximal esophagus, more forceful contraction strength was required distally. This difference is probably related to the compliance of the esophageal segments distal to the advancing bolus. For the proximal esophagus, the distal esophageal segment is highly compliant because it has negligible resting tone, is subject to descending inhibition ahead of the contraction wave, and is situated in the negative pressure zone of the thoracic cavity. However, as the peristaltic contraction progresses distally, the segment distal to the contraction wave becomes less compliant because the lower esophageal sphincter must be opened by the bolus and the bolus pushed against a pressure gradient into the stomach. The findings of this study suggest that the minimum effective contraction strength for clearance in the distal esophagus is 20 mmHg, whereas in the proximal esophagus, virtually any propagated contraction will effectively empty the esophagus, The peristaltic amplitudes required for invariable bolus clearance were 16 mmHg in the proximal esophagus and 30-40 mmHg in the distal esophagus (Figure 6). In a previous analysis of peristaltic dysfunction among patients with gastroesophageal reflux disease, we used a statistical analysis of data from normal volunteers and patient controls to determine a value of 27 mmHg as the lower limit of normal peristaltic amplitude in the distal esophagus (1). The findings from the present study provide an additional rationale for a threshold value of about 30 mmHg and serve to strengthen the previous analysis. Our main intent in this study was to define the relationship between the manometric and fluoro-
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KAHRILAS ET AL.
scopic evaluations of peristalsis. As suggested previously, excellent correlation exists between the manometric and fluoroscopic evaluations of esophageal peristalsis (13). On the other hand, the two studies are complementary to one another, with each providing unique information. Fluoroscopy details anatomic aspects of the esophagus as well as motor function, whereas manometry quantifies the variables of peristaltic contractions. In this study, peristaltic sequences that were normal manometrically were normal on videofluoroscopy. The progression of the esophageal stripping wave coincided precisely with the progression. of the peristaltic contraction, such that luminal closure at each esophageal locus occurred concurrent with the upstroke of the peristaltic contraction. In contrast, failed peristaltic sequences, with or without accompanying simultaneous contractions, resulted in minimal esophageal volume clearance. Hypotensive peristaltic sequences achieved varying degrees of partial volume clearance depending on the severity of retrograde escape through the hypotensive peristaltic segment. The correlation between videofluoroscopy and manometry shown in this study infers that the abnormalities found in a significant proportion of patients with esophagitis (failed and hypotensive peristalsis) would be expected to prolong the process of esophageal volume clearance when the patients were recumbent (1). Thus, esophageal peristaltic dysfunction, along with occasional abnormalities of salivation (14) and in some cases repeated instances of re-reflux that occur during the process of acid clearance (IS), may all act to prolong the process of normal esophageal acid clearance in some patients with gastroesophageal reflux disease.
References 1.
2.
Kahrilas PJ, Dodds WJ, Hogan WJ, Kern M, Arndorfer RC, Reece A. Esophageal peristaltic dysfunction in peptic esophagitis. Gastroenterology 1986;91:897-904. Gill RC, Bowes KL, Murphy PD, Kingma YJ. Esophageal motor abnormalities in gastroesophageal reflux and the effects of fundoplication. Gastroenterology 1986;91:364-9.
GASTROENTEROLOGY Vol. 94, No. 1
3. Stanciu C, Bennett JR. Oesophageal 4. 5. 6.
7.
8.
9.
10.
11.
12.
acid clearing: one factor in the production of reflux esophagitis. Gut 1974;15:852-7. Booth DJ, Kemmerer WT, Skinner DB. Acid clearing from the distal esophagus. Arch Surg 1968;96:731-4. Dodds WJ, Hogan WJ, Miller WN. Reflux esophagitis. Am J Dig Dis 1976;21:49-67. Helm JF, Dodds WJ, Pelt LR, Palmer DW, Hogan WJ, Teeter BC. Effect of esophageal emptying and saliva on clearance of acid from the esophagus. N Engl J Med 1984;310:284-8. Helm JF, Dodds WJ, Riedel DR, Teeter BC, Hogan WJ, Arndorfer RC. Determinants of esophageal acid clearance in normal subjects. Gastroenterology 1983;85:607-12. Arndorfer RC, Stef JJ, Dodds WJ, Linehan JH, Hogan WJ. Improved infusion system for intraluminal esophageal manometry. Gastroenterology 1977;73:23-7. Phaosawasdi K, Malmud LS, Tolin SD, Stelzer F, Applegate G, Fisher RS. Cholinergic effects on esophageal transit and clearance. Gastroenterology 1981;81:915-20. Tolin RD, Malmud LS, Reilley J, Fisher RS. Esophageal scintigraphy to quantitate esophageal transit (quantitation of esophageal transit). Gastroenterology 1979;76:1402-8. Russel COH, Hill LD, Holmes ER, Hull DA, Gannon R, Pope CE. Radionuclide transit: a sensitive screening test for esophageal dysfunction. Gastroenterology 1981;80:887-92. Richter JE, Blackwell JN, Wu WC, Johns DN, Cowan RJ, Caste11 DO. Relationship of radionuclide liquid bolus transport and esophageal manometry. J Lab Clin Med 1987;109:
217-24. 13. Dodds WJ. 1976 Walter B. Cannon lecture: current concepts
of esophageal motor function: clinical implications for radiology. Am J Roentgen01 1977;128:549-61. M, Dodds WJ, Hogan WJ, Lipman S. 14. Helm JF, Allendorph Loss of the salivary response to esophageal acid perfusion in patients with peptic stricture (abstr). Gastroenterology 1986; 90:1456. 15. Mittal RK, Lange RC, McCallum RW. Identification and mechanism of delayed esophageal acid clearance in subjects with hiatus hernia. Gastroenterology 1987;92:130-5.
Received April 27, 1987. Accepted July 29, 1987. Address requests for reprints to: P. J. Kahrilas, M.D., Northwestern University Medical School, GI Section, Department of Medicine, 1526 Wesley Pavilion, Chicago, Illinois 60611. This work was presented at the biannual meeting of the American Motility Society in Houston, Texas on October 29, 1986 and was published in abstract form in Gastroenterology 1986;91:1057. This work was supported by a fellowship from the Schweppe Foundation (P.J.K.), grant NIH-BRSG RR-05370 from the U.S. Public Health Service (P.J.K.), and grant AM 25731 from the National Institutes of Health (W.J.D.).