Regional differences in oesophageal motor ... - Wiley Online Library

Neurogastroenterol Motil (2004) 16, 31–37

Regional differences in oesophageal motor function J. L. WISE, J. A. MURRAY & J. L. CONKLIN

Department of Gastroenterology and Hepatology, Mayo Clinic, Rochester, MN, USA

While the oesophagus may be thought of as a simple, muscular tube that provides safe and rapid passage of a swallowed bolus to the stomach, it is not homogeneous in its structure. The oesophagus comprises of two muscular layers critical to its function, the inner circular and the outer longitudinal layer. The regional anatomical differences within the oesophagus are most conspicuous between the relatively small, proximal striated muscle portion and the larger, distal smooth muscle portion.1 Although there is significant overlap between these regions each may have important functional differences.2–5 Our understanding of oesophageal function is based on earlier observations from barium contrast studies,6 manometric studies7,8 and more recently these modalities combined.9,10 Intraluminal, oesophageal impedance measurements can now be obtained during oesophageal function testing.11 This is a validated technique whereby a drop in impedance to 50% a baseline value correlates precisely with the entrance of a bolus into an intraluminal segment. A rise from a nadir to 50% of the baseline value correlates precisely with the exit of a bolus from a segment of the oesophagus.12,13 The velocity at which the bolus enters and exits the entire oesophagus has been reported in normal subjects14,15 and in subjects with gastro-oesophageal reflux disease16 using intraluminal impedance. In this study, we utilized combined manometry and impedance technology to test the hypotheses that oesophageal bolus transit and motor function vary regionally, with bolus viscosity and with body position.

Abstract We tested the hypotheses that oesophageal bolus transit and motor function vary regionally, with bolus viscosity and with body position. In healthy volunteers, we measured the bolus head advance time, bolus presence time and bolus transit time in the proximal and distal oesophagus using water and viscous materials. We compared concurrent manometric responses. Bolus head advance time, bolus presence time and bolus transit time were longer in the distal oesophagus during water and viscous swallows in the upright and supine positions. The total bolus head advance time and transit time, measured across the entire oesophageal body, were shorter for water than viscous swallows. The amplitudes of peristaltic pressure waves were lower for viscous swallows, and varied as a function of region. These studies demonstrated true functional differences between the proximal and distal oesophagus using multichannel intraluminal impedance and that the viscosity of the bolus is a determinant of oesophageal function. Keywords deglutition, motility, oesophagus, peristalsis, swallowing.

INTRODUCTION The most important function of the oesophagus is to act as a mechanical pump for the transport of ingested food to the stomach. During normal deglutition, the oesophageal body accepts a bolus from the pharynx as it passes the upper oesophageal sphincter. The coordinated contraction of striated and smooth muscle portions of the oesophagus propels the bolus along the body of the oesophagus into the stomach through a relaxed lower oesophageal sphincter (LOS).

MATERIALS AND METHODS Nineteen healthy volunteers (five men and 14 women, age, 40 ± 3 years, 18–55) without complaints of dysphagia, heartburn, acid regurgitation, or chest pain were studied in the oesophageal motility laboratory the morning following an overnight fast. Non-pregnant subjects were included if they were at least 18 years of age, had no history of oesophageal or gastric surgery, or any kind of pacemaker.

Address for correspondence Joseph A. Murray, MD, Department of Gastroenterology and Hepatology Mayo Clinic, 200 First Street SW Rochester, MN 55905, USA. e-mail: [email protected] Received: 12 March 2003 Accepted for publication: 13 June 2003 Ó 2004 Blackwell Publishing Ltd

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Figure 1 Combined impedance–manometry catheter within the oesophagus is depicted on the left side. The impedance segments are located at 20, 15, 10 and 5 cm above lower oesophageal sphincter (LOS) and manometric sensors at 15, 10, 5 cm above LOS. Impedance and manometric data at each segment, superimposed at 15, 10 and 5 cm above LOS is given on the right side. The swallowing sequences with water at left and viscous at right are also given. Note the rapid rise in impedance corresponding to air within the head of the bolus.

The parameters measured included total and regional bolus filling velocity, regional bolus presence time, and the total and regional bolus clearance velocity (Fig. 2). Regional bolus head advance time was measured in the proximal and distal oesophagus as the time, in seconds, from when the bolus entered the oesophagus at a MII segment until it entered the next distal segment (5 cm distal). Therefore, the proximal bolus head advance time was the time, in seconds, from when the bolus entered a MII segment 20 cm from the LOS to the time it entered the next distal segment 15 cm from the LOS. The distal bolus head advance time was measured in the same manner except that measurements were taken from a MII segment 10 cm from the LOS to the next distal segment 5 cm from the LOS. Regional bolus presence time was measured in the proximal and distal oesophagus. The proximal bolus presence time was measured as the time in seconds between when the bolus entered and exited the proximal impedance segment 20 cm from the LOS. The distal bolus presence time was measured from the time the bolus entered at an impedance segment 10 cm from the LOS until the time it left that same segment. Regional bolus transit time was measured in the proximal and distal oesophagus as the time, in seconds, from when the bolus entered the oesophagus at a MII segment until it left from the next distal segment

Subjects underwent stationary oesophageal function testing using combined multichannel intraluminal impedance (MII) and oesophageal manometry (OM) catheter (MII/OM). This catheter was composed of four, solid-state pressure transducers: one located at the LOS and three others 5, 10, and 15 cm above the LOS. The catheter also contained four, impedancesensing segments positioned at 5, 10, 15 and 20 cm above the LOS (Fig. 1). Pressure measurements from the oesophageal body were taken from the three manometric sensors above the LOS and impedance measurements from all four of the impedance segments. After the application of intranasal topical anaesthesia, the combined MII/OM catheter was placed transnasally into the stomach with the subject in the sitting position. Circumferential pressure transducers were used to identify the LOS during a standard station pullthrough technique. After positioning of the most distal circumferential sensor within the LOS, subjects were given a series of 10, 5 cm3 swallows of water followed by a series 10, 5 cm3 swallows of a viscous material of known impedance (viscosity 600 millipoises). Data were obtained in both the supine and upright positions. Recordings were made using Bioview acquisition software (Sandhill Scientific Co., Denver CO, USA). Regional oesophageal bolus handling was assessed for each substance in the upright and supine positions. 32

Ó 2004 Blackwell Publishing Ltd

Volume 16, Number 1, February 2004

Regional oesophageal function

the baseline value. Clearance of the bolus was defined as a rise in impedance to 50% of the previous baseline as previously confirmed in validation studies.11,12 Each swallow was analysed for manometric characteristics. Peak amplitude was measured at a single, proximal, directional sensor located 15 cm from the LOS and a single, distal, circumferential sensor located 5 cm from the LOS. Onset velocity was measured from the onset of the first manometric pressure wave located at 15 cm from the LOS to the distal sensor 5 cm from the LOS. Swallows with no manometric response, a simultaneous or retrograde pattern, or associated with a second, or double swallow, within 5 s of the intended swallow, were excluded. The Mayo Clinic, Rochester Institutional Review Board approved the study, and informed consent was obtained from each subject.

Statistical analysis All data were analysed using the SASÓ software program. Intrasubject means were compared using paired t-tests. Threshold for statistical significance was set at an a of 0.05.

RESULTS Figure 2 Combined impedance–manometry catheter with associated schematic representation of measurements: proximal bolus head advance time (B); distal bolus head advance time (E); proximal bolus presence time (A); distal bolus presence time (D); proximal bolus transit time (C); distal bolus transit time (F).

Differences in regional bolus head advance times, bolus presence times and bolus transit times The head of the bolus advanced rapidly through oesophagus during all swallows. The leading edge of water propagated more rapidly through the proximal oesophagus than the distal oesophagus in the supine position (see Table 1 and Fig. 3). This difference was maintained in the upright position. It took longer for the combined air/viscous bolus to enter the oesophagus but the disparity between shorter advance times into the proximal compared with the

(5 cm distal). Therefore, the proximal bolus transit time was the distance over time, in seconds, from the time the bolus entered a MII sensor 20 cm from the LOS until the time of its clearance from a MII sensor 15 cm from the LOS. The distal bolus transit time was measured in the same manner except that the points of measurement included a MII sensor 10 cm from the LOS to a MII sensor 5 cm from the LOS. The total bolus head advance time and total bolus transit time were measured as the time, in seconds, from the moment the bolus entered a MII segment 20 cm from the LOS until its entrance at or clearance across a MII sensor 5 cm above the LOS, respectively. An abrupt rise in impedance as the bolus entered the segment was interpreted as gas or air within the bolus head. The air within the bolus head was measured as part of the bolus in all measurements. Entry of a purely liquid bolus at an oesophageal impedance segment was determined by a rapid decline in impedance to 50% of Ó 2004 Blackwell Publishing Ltd

Table 1 Proximal compared with distal bolus times, in seconds, in the supine position Proximal (s) Bolus head advance times Water 0.36 ± 0.06 Viscous 0.72 ± 0.09 Bolus presence times Water 3.2 ± 0.3 Viscous 3.1 ± 1.1 Bolus transit times Water 5.41 ± 0.35 Viscous 5.20 ± 0.40

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Distal (s)

0.81 ± .16 (P < 0.005) 1.30 ± 0.14 (P < 0.01) 5.5 ± 0.2 (P < .001) 4.9 ± 0.4 (P < 0.001) 7.00 ± 0.27 (P < 0.001) 6.73 ± 0.42 (P < 0.01)

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Table 2 Upright compared with supine bolus times Upright (s) Proximal bolus head advance times Water 0.30 ± .05 Viscous 0.65 ± 0.07 Proximal bolus presence time Water 2.3 ± 0.2 Viscous 2.4 ± 0.3 Distal bolus presence times Water 4.7 ± 0.2 Proximal bolus transit times Water 4.12 ± 0.29

Supine (s)

0.40 ± 0.08 (P < 0.05) 0.75 ± 0.09 3.3 ± 0.3 3.0 ± 0.3 5.5 ± 0.3 5.10 ± 0.28 (P < 0.05)

Figure 3 Regional bolus head advance times in the supine position: comparing the proximal with the distal oesophagus with water and viscous separately (*P < 0.001, **P < 0.01).

distal oesophagus was maintained The results are presented in Table 1 and Fig. 3. The proximal bolus presence time was significantly shorter than the distal bolus presence time in both supine and upright positions during water and viscous swallows (see Table 1). The proximal bolus transit time was shorter than the distal bolus transit time during water and viscous swallows in both the supine and upright positions (Table 1).

Figure 4 Regional bolus presence time: comparing the upright and supine positions at each oesophageal region using water and viscous separately (*P < 0.05).

The effect of body position on bolus transit The difference between proximal bolus head advance time in the upright position compared with supine did not reach statistical significance for either the water, 0.30 ± 0.05 s vs 0.40 ± 0.08 s (P ¼ 0.194) or viscous bolus 0.65 ± 0.07 vs 0.75 ± 0.09 s (P ¼ 0.196). There was no difference between total or distal bolus filling velocities comparing the upright to the supine position. There were differences in the bolus presence times in both the proximal and distal oesophagus during water swallows in the upright position (see Table 2 and Fig. 4). There was a difference between upright and supine proximal bolus presence times for viscous swallows. However, this did not reach statistical significance (2.4 ± 0.3 vs 3.0 ± 0.3 s). There were no significant differences in the distal bolus presence time, upright vs supine, measured during viscous swallows. The proximal bolus transit time was faster during upright water swallows than in the supine position (see Table 2 and Fig. 4). These differences with body position were not seen during water swallows distally or in either region using viscous material. There was a difference in the total bolus transit time when comparing the upright with the supine positions.

The effect of bolus viscosity on bolus transit In each region of the oesophagus and in each body position, viscous material filled the oesophagus more slowly than water. The same measurements were compared in the upright position. The differences between water and viscous material were maintained in the distal oesophagus (see Table 3 and Fig. 5). There was no difference in the regional bolus presence times or the regional bolus transit times in either the proximal or distal oesophagus comparing water swallows with viscous swallows. The bolus head traversed the full length of the oesophageal body during water swallows with an average bolus head advance time of 1.56 ± 0.22 s. There were significant differences in the total bolus head advance times comparing water swallows with viscous swallows in the upright and supine positions (see Table 4). The entire oesophagus was cleared of water in the supine position with a total bolus transit time of 7.73 ± 0.29 s during water swallows. There were significant differences in the total bolus transit times between water and viscous in the supine position. This 34




101.1 ± 9.1 mmHg in the upright position (P < 0.05). During viscous swallows the mean peak amplitude at the proximal sensor was 64.6 ± 8.2 mmHg compared with a distal average amplitude of 94.6 ± 11.0 mmHg in the supine position (P < 0.01) and 75.9 ± 9.1 mmHg vs 92.3 ± 9.4 mmHg in the upright position (P < 0.05). The average proximal amplitude during viscous swallows was 64.6 ± 8.2 mmHg in the supine position and 75.9 ± 9.1 mmHg distally, in the upright position compared with water 76.5 ± 8.6 and 78.6 ± 9.3 mmHg respectively. The distal amplitudes were 94.6 ± 11.0 and 92.3 ± 9.4 mmHg for viscous supine and upright respectively, compared with water at 106.5 ± 9.1 and 101.1 ± 9.1 mmHg. These differences did not reach statistical significance. There were no differences in proximal or distal oesophageal amplitudes between swallows measured in the upright or supine position respectively. Onset velocity measured from 15 to 5 cm from the LOS was not significantly different when comparing water with viscous swallows or comparing swallows in the upright and supine body positions.

Table 3 Water compared with viscous for regional bolus times Water (s) Supine bolus head advance times Proximal 0.35 ± 0.06 Distal 0.81 ± 0.16 Upright bolus head advance times Proximal 0.35 ± 0.06 Distal 0.76 ± 0.09

Viscous (s)

0.72 ± 0.09 1.30 ± 0.14 (P < 0.05) 0.72 ± 0.09 (P < 0.0001) 1.50 ± 0.17 (P < 0.01)

DISCUSSION This study was undertaken to characterize and quantify regional differences in oesophageal function, particularly bolus behaviour during primary peristalsis. Insights into regionalization of function were derived initially from animal models, particularly the opossum, closest in muscular composition to human. Investigators demonstrated regional gradients in potassium, muscular oscillatory frequency, and the latency of the ‘off-response’ in these models.17–20 More recently investigators have found functional variation by region within the oesophageal body of cats.21 Traditionally, OM and radiographic studies are used to examine oesophageal physiology and define pathophysiological processes. While OM accurately portrays the neuromuscular function of the oesophagus, it provides scant information about bolus transit. Intraluminal impedance accurately represents bolus transit providing segmental measurements of drops in impedance over time.12 It provides reproducible and precisely quantifiable data to examine oesophageal function without the need for radiation or complex analysis. Additionally, OM can be carried out concurrently. This allows the simultaneous evaluation of bolus transit and neuromuscular processes responsible for bolus movement. Using a combined impedance–manometry catheter we tested the hypothesis that oesophageal function differs regionally. These studies demonstrate that there

Figure 5 Regional bolus transit times in the supine position: comparing the proximal with the distal oesophagus with water and viscous separately (*P < 0.001, **P < 0.01).

Table 4 Water compared with viscous for total bolus times Water (s) Total bolus head advance times Upright 1.66 ± 0.17 Supine 1.56 ± 0.22 Total bolus transit times Upright 7.28 ± 0.29 Supine 7.73 ± 0.29

Viscous (s)

3.34 ± 0.18 (P < 0.0001) 3.40 ± 0.19 (P < 0.0001) 8.41 ± 0.54 (P < 0.05) 8.60 ± 0.36 (P < 0.05)

difference was also seen in the upright position (see Table 4).

MANOMETRIC RESULTS There were significant differences between the peak amplitudes of contraction in the proximal versus the distal oesophagus for all swallows. During water swallows the mean peak amplitude at the proximal sensor was 76.5 ± 8.6 mmHg compared with 106.5 ± 9.1 mmHg distally, in the supine position (P < 0.05), and 78.7 ± 9.3 mmHg compared with Ó 2004 Blackwell Publishing Ltd

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different viscosities has long intrigued investigators of oesophageal function.10,27–31 Barium swallow and scintigraphic studies have demonstrated that liquid boluses are cleared from the oesophagus in 8–10 s when the subject is in the supine position.9,23 Solid foods such as unchewed bread or liver cubes31 are cleared more slowly, particularly in the supine position. Using MII, it was shown that viscous materials take longer to traverse the entire oesophagus and also to be cleared from the entire oesophagus.15,16 Our results are similar. Total bolus head advance and total bolus transit times were more prolonged with a more viscous material. The affect gravity has on oesophageal function has also been examined with barium radiography, scintigraphy and manometry.6,32,33 In the upright position a bolus of low viscosity seemed to spread out over the entire oesophagus during rapid filling. In the supine position, the bolus appeared to be more compact and filling was more closely related to peristalsis.29 In our study, water boluses were retained in the proximal oesophagus for a shorter period of time and entered into the length of the oesophagus more rapidly. Gravity may play a part in the differences we observed. It was interesting that we did not observe differences in transit times in the upright compared with the supine positions during water or viscous swallows; suggesting bolus transit is closely correlated to peristalsis. This suggests that the major driving force for bolus entry into the oesophagus is not gravitational pull but probably the ‘pharyngeal pump’. Swallows associated with failed peristalsis were not evaluated in this study: their analysis may have lead to a more striking difference between regional bolus head advance and transit times in the upright and supine positions. The understanding of bolus transit and differences in regional oesophageal function is an important step towards a better understanding and characterization of swallowing complaints. Although there appear to be complimentary roles for both bolus transit characterization and pressure wave assessment in the investigation of oesophageal function,19 there are practical limitations to combining videoflouroscopy and manometry in the same study setting. Combined impedance and manometry may make assessment of this relationship clinically feasible. In addition, bolus transit can be instantly and precisely quantified using impedance technology. Any alterations in these normal physiological relationships seen in patients with swallowing disorders may provide greater insight into the mechanisms of dysfunction and the causes of oesophageal dysphagia.

are regional differences in the time it takes for a bolus to enter and be cleared from an oesophageal segment. They also show that the time bolus remains in an oesophageal segment varies as a function of its location along the length of the oesophagus. These observations depict an organ that does not behave as a uniform tube, but one which has regional, functional differences. The bolus enters and is cleared from the proximal oesophagus over a shorter period of time than in the distal oesophagus. It also remains in the proximal oesophagus for a shorter time. The measurement of the relative slowing of bolus transit in the distal oesophagus has been previously recorded using auscultation22 and directly observed by combined videoflouroscopic and manometric studies10 and ultra fast computed tomography.23 A potential explanation for the more rapid bolus entry into the proximal compared with the distal oesophagus is the ‘pharyngeal pump’. The pharynx can behave as a pump generating positive pressure by the posterior two-thirds of the tongue. Negative pressure created by the opening of the UES causes ‘ejection’ of the bolus through the proximal oesophagus and distal oesophagus.24 As the bolus is ejected through the proximal oesophagus it may slow down by force of friction. This may account for the observed differences in bolus head advance time. Bolus presence time is a function of the rate of entrance of the bolus and the rate of its clearance or transit. The bolus dwells longer in the distal oesophagus. It is possible that the bolus is slowed as it enters the more compliant muscular region. Shortening of a thin-walled tube increases the diameter of its lumen: thus greater shortening of the distal oesophagus may increase its capacity to provide a wider space.25 The idea of an anatomically and physiologically disparate region in the distal, tubular oesophagus known as the ‘phrenic ampulla’ has been of interest for sometime. Investigators have previously reported the effects of peristalsis and hydrostatic forces on filling and emptying of the most distal aspect of the oesophageal body during barium studies. In these careful studies, clearing waves slowed in velocity as they reached the distal oesophagus.26 Using combined videoflouroscopy, investigators reported the slowing of bolus transit in the distal oesophagus and the increase in intrabolus pressure.10 This was postulated to be caused by transmission of positive pressure from the abdominal cavity as bolus transit was further delayed by application of abdominal pressure during swallows. This study documents the effect viscosity has on bolus handling. How the oesophagus handles boluses of 36




ACKNOWLEDGMENTS I would like to acknowledge Patty Kammer, senior technical assistant, for her help performing oesophageal function tests and Louis Kost for technologic assistance and data management. Joseph A. Murray was supported by NIH R01 DK 57982.

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