Ann Thorac Surg 2001;71:1786-1791
© 2001 The Society of Thoracic Surgeons
Original article: general thoracic
Bile exposure of the denervated stomach as an esophageal substitute
Christian A. Gutschow, MDa,
Jean-Marie Collard, MDa,
Renato Romagnoli, MDa,
Jean-Marie Michel, MDa,
Mauro Salizzoni, MDa,
Arnulf H. Hölscher, MDb
a Department of Surgery, University of Louvain, Brussels, Belgium
b Department of Surgery, University of Cologne, Cologne, Germany
Accepted for publication February 7, 2001.
Address reprint requests to Dr Collard, Upper GI Surgery Unit, St-Luc Academic Hospital, Hippocrate Ave 10, B-1200, Brussels, Belgium
e-mail: collard{at}chir.ucl.ac.be
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Abstract
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Background. Both the supine position and the existence of a gastric drainage procedure are suspected to promote reflux of duodenal juice into the denervated intrathoracic stomach. Erythromycin has been shown to weaken pyloric resistance to gastric outflow and to enhance antral motility, gastric emptying, and gallbladder contractility.
Methods. The presence of bile in the gastric transplant of 79 patients was monitored over a 24-hour period with use of the Bilitec 2000 optoelectronic device 3 to 195 months after subtotal esophagectomy. Ten patients were reinvestigated after a 3-year period. Five groups were studied: group I: n = 12, no gastric drainage, never given erythromycin, group 2: n = 40, gastric drainage, never given erythromycin, group 3: n = 7, no gastric drainage, given erythromycin, group 4: n = 13, gastric drainage, given erythromycin, and group 5: n = 7, no longer given erythromycin (with or without gastric drainage). The percentage of time gastric bile absorbance was more than 0.25 was calculated for the total, supine, and upright periods of recording in reference to data from 25 healthy volunteers.
Results. The Bilitec test was pathologic in 9 of the 12 patients of group 1 whereas it was normal in three. Gastric exposure to bile was longer in group I patients than in controls for the total (p = 0.012) and supine (0.036) periods, but the difference did not reach statistical significance for the upright period (p = 0.080). Bile exposure in group 4 did not significantly differ from controls (total: p = 0.701; supine: p = 0.124; upright: p = 0.712). Bile exposure for the total period did not significantly differ whether patients were taking erythromycin or the drug had been discontinued at the time of the study (p = 0.234); and it tended to decrease with time in patients investigated twice (p = 0.046).
Conclusions. Gastric exposure to bile after truncal vagotomy and transposition of the stomach up to the neck is pathologic in three quarters of patients. It is more marked in the supine than in the upright position and tends to decrease with time. The addition of a gastric drainage procedure in combination with erythromycin therapy tends to normalize gastric exposure to bile. The effects of erythromycin may persist after discontinuation of the drug.
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Introduction
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Pathologic exposure of the gastric mucosa to duodenal juice results from an alteration of the physiologic balance between propulsive activity of the antrum, pyloroduodenal resistance to gastric in– and outflows of biliopancreatic secretion, and delivery of the latter into the duodenal lumen [1, 2]. Bilateral truncal vagotomy that necessarily accompanies esophagectomy for cancer disturbs all these processes [3–5], and placement of the gastric pouch in a negative-pressure environment for its elevation up to the neck creates a duodenogastric reflux (DGR) –promoting pressure gradient between the intraabdominal duodenum and the intrathoracic stomach [6].
To date, objective assessment of DGR after denervation of the stomach and its transposition up to the neck [7] was based on the presence of radioactivity in the stomach at O-diisopropyl iminodiacetic acid (DISIDA) scintigraphy scanning [8, 9], the detection of bile acids in gastric aspirates over a 24-hour period [10, 11], or the existence of an alkaline pH-profile at 24-hour gastric pH-monitoring [12]. On the basis of these classic detection methods of duodenal juice in the gastric lumen, it has been suggested that DGR into the denervated gastric transplant is favored by both the supine position [10, 11] and the presence of a gastric drainage procedure such as a pyloroplasty [8]. Actually, although pyloroplasty has been shown to accelerate vagotomy-delayed gastric emptying [13–15], there is no consensus on the ability of the pylorus itself [16], its denervation [11], and its enlargement after vagotomy [8, 17] to regulate DGR.
In this setting, it was very challenging to study bile exposure of the intrathoracic denervated stomach with use of the Bilitec 2000 device, an optoelectronic instrument which allows the monitoring of bile in the gastric lumen over a 24-hour period [18].
The current study aims to assess the respective role of truncal vagotomy, posture, gastric drainage (i.e. pyloroplasty or pyloromyotomy), early administration of a motilin-receptor agonist such as erythromycin [19–21], and time elapsed since the operation in the regulation of bile exposure of the stomach as esophageal replacement.
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Material and methods
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Study population
The 79 patients studied consisted of 58 males and 21 females, aged 33 to 84 years, who had undergone subtotal esophagectomy and gastric transposition up to the neck for either cancer [22] (n = 73) or benign disease (n = 6) of the thoracic esophagus. The gastric transplant [7] had been placed in the posterior mediastinum and consisted of the whole stomach and a greater curvature tube in 65 and 14 patients, respectively. A gastric drainage procedure was performed in 58 patients whereas it was not in 21 patients. The gastric drainage procedure consisted of a 2-cm Heineke-Mikulicz pyloroplasty and a 2-cm extramucosal pyloromyotomy in 40 and 18 patients, respectively. Twenty patients were under erythromycin therapy [20] (erythromycin ethylsuccinate, 750 mg daily) at the time of the study, the medication had been taken for a period ranging from 3 to 40 months (median: 5.5 months). Seven patients who had taken erythromycin for a minimum period of 6 months after the operation (range: 6 to 18 months; median: 12 months) were investigated after erythromycin therapy had been discontinued for a period ranging from 1 to 35 months (median: 14 months). Ten whole stomach patients accepted to undergo gastric bile monitoring twice, the interval of time between the two examinations ranging from 34 to 42 months (median: 36.5 months). Two among these 10 patients were under erythromycin therapy at the time of the first examination but both were no longer taking the drug at the time of the second examination, and 5 patients had a gastric drainage procedure whereas 5 had not. In all, the presence of bile in the gastric lumen was monitored 89 times in 79 patients. The 89 examinations were performed after a follow-up period ranging from 3 to 195 months (mean: 53 months; median: 39 months). Five distinct groups were compared with each other: group I (12 patients): no gastric drainage, never given erythromycin; group 2 (40 patients): gastric drainage, never given erythromycin; group 3 (7 patients): no gastric drainage, being given erythromycin; group 4 (13 patients): gastric drainage, being given erythromycin; group 5 (7 patients): previously given erythromycin with (n = 5) or without (n = 2) a gastric drainage procedure.
24-hour gastric bile monitoring
The Bilitec 2000 device [18] (Medtronic, Skovlunde, Denmark) is an optoelectronic instrument including a miniaturized fiberoptic probe and a portable recording unit, capable of monitoring the presence of biliary pigments in the foregut lumen over a 24-hour period. The distal tip of the probe contains a 2-mm space through which fluids and small solid particles can flow. The portable unit contains two light-emitting diodes, one having a wavelength of 470 nm (ie, close to the absorbance peak of bilirubin at 453 nm) and the other of 565 nm (reference signal). Optical signals reflected back by the probe are converted into electrical impulses by a photodiode, and a microcomputer calculates the difference between the absorbance at 470 nm and that at 565 nm. This difference is commonly called "absorbance." Absorbance values range from 0 (plain water) to 1 (total screen), but the working range of the instrument has been shown to extend from 0.14 to 0.60 only [18].
From a practical standpoint, the bile probe was passed transnasally under local anesthesia and positioned in the gastric lumen under fluoroscopic control, so that its distal tip lay in the gastric body, about 15 cm distal to the cervical esophagogastrostomy, which corresponds to a point located about 5 cm below the gastroesophageal (G-E) junction of the intraabdominal stomach. Patients were given three standardized meals which were composed of nutrients that could not significantly interfere with bile detection (in vitro absorbance < 0.25). Food consisted of soft cheese, potatoes, chicken breast, white bread, one banana, one apple, milk or plain water, and white sugar. The time spent in the erect and supine position as well as the time during which meals were taken were carefully noted on a standardized sheet. Data were stored in the Bilitec 2000, serial number 001 and transfered to a personal computer that was equipped with the Eso-pH-ogram software (Gastrosoft, Irving, TX). The percentage of time gastric bile absorbance was more than 0.25 for the total, upright, and supine periods of recording was calculated in reference to values from 25 own healthy volunteers [23] (% time absorbance > 0.25: 95th percentile of the total period: 22.9%, supine period: 31.8%, upright period: 18.2%). The distal tip of the probe in healthy volunteers had been positioned 5 cm below the G-E junction. The Bilitec test was defined as pathologic [23] when gastric exposure to bile exceeded the 95th percentile of healthy controls in 1 of the 3 study periods at 1 of the following thresholds: 0.25, 0.30, 0.40, 0.50, and 0.60. Bilitec data obtained from controls and the 5 study groups were expressed as the median [interquartile range]. Data interpretation was based on the concept that the presence of bile in the gastric cavity depends on both the reflux of duodenal juice into the stomach and its reexpulsion into the duodenum on the action of the gastric musculature.
Statistics
2, Mann-Whitney and Kruskal-Wallis rank sum, and Wilcoxon matched pair tests were used appropriately. A p-value less than 0.05 was considered significant.
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Results
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Detection of bile
Bile was detected in the gastric transplant lumen in 62 patients (78.5%) whereas there was no bile detected over the 24-hour period of recording in 17 patients (21.5%). Bile exposure in patients in whom it was detected was pathologic in 43 patients (54.4%) whereas it remained within the normal range in 19 patients (24.1%). Moreover, there was a great variability in gastric bile exposure within each of the 5 groups studied. Indeed, considering the 89 examinations as a whole, the percentage of time bile absorbance more than 0.25 varied from 0% to 90% for the total period, from 0% to 99.3% for the supine period, and from 0% to 89.7% for the upright period of recording. The prevalence of a pathologic gastric exposure to bile did not significantly differ (p = 0.943) between whole stomach patients (55.4%) and those having a greater curvature tube (50%) as esophageal replacement.
Effect of vagotomy
Gastric bile exposure in group 1 (no gastric drainage, never given erythromycin; 12 patients) was pathologic in one or more of the 3 periods of recording in 9 patients (75%), it remained within the normal range in 1 patient (8.3%), and no bile was detected in the gastric transplant lumen in 2 patients (16.7%). Gastric bile exposure during the total period of recording expressed as the median [interquartile range] was significantly longer (p = 0.012) after gastric denervation and pull-up (group 1) than in controls (22.8% [4.5 to 48.2] vs 2% [0.9 to 8.3]) (Fig 1).
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Fig 1. Gastric exposure to bile for the total (left), supine (center), and upright (right) periods of recording in controls (black boxes) and group I patients (blank boxes). Box plot shows medians, interquartile ranges, and absolute ranges.
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Effect of posture
The prevalence of a pathologic Bilitec test in group 1 patients (no gastric drainage, never given erythromycin) was 66.6% during the supine period versus 50% during the upright period (p = 0.679). However, gastric bile exposure was significantly longer (p = 0.036) in group 1 patients than in controls for the supine period (44.6% [1.3 to 68.4] vs 3.6% [0.9 to 13.4]) whereas difference did not reach statistical significance (p = 0.080) for the upright period (7.6% [0 to 27.7] vs 0.3% [0 to 4.5]) (Fig 1). Similarly to controls, gastric exposure to bile in group 1 was significantly longer (p = 0.022) in the supine than in the upright position (44.6% [1.3 to 68.4] vs 7.6% [0 to 27.7]).
Effect of gastric drainage
The Bilitec test was pathologic in 57.5% of patients who were not given erythromycin but in whom a gastric drainage procedure had been added (group 2), which was similar (p = 0.450) to group 1 patients (75%). The prevalence of a pathologic Bilitec test did not significantly differ (p = 0.853) whether patients had a pyloroplasty (60%) or a pyloromyotomy (50%). Supine gastric exposure to bile in group 2 was similar (p = 0.444) to that in group 1 (25.9% [0.3 to 66.9] vs 44.6% [1.3 to 68.4]), and it remained significantly longer (p = 0.018) than in controls (Fig 2). Likewise, there was no difference (p = 0.572) in terms of upright gastric exposure to bile between group 2 patients and those of group 1 (5.5% [0.2 to 13.1] vs 7.6% [0 to 27.7]) (Fig 3).
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Fig 2. Supine gastric exposure to bile in controls and groups 1 to 4. Box plot shows medians, interquartile ranges, and absolute ranges (* technical failure in 1 patient).
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Fig 3. Upright gastric exposure to bile in controls and groups 1 to 4. Box plot shows medians, interquartile ranges, and absolute ranges.
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Effect of erythromycin therapy
The prevalence of a pathologic Bilitec test in group 3 patients (no gastric drainage procedure but being given erythromycin) was 57.1% versus 75% in those of group 1 (no gastric drainage, never given erythromycin) (p = 0.767). As shown in Figures 2 and 3, gastric exposure to bile for both the supine and the upright periods of recording in group 3 patients was not significantly different from that in group 1 patients (supine: 22.1% [0 to 80.3] vs 44.6% [1.3 to 68.4]; p = 0.422; upright: 3.5% [0.1 to 7] vs 7.6% [0 to 27.7]; p = 0.642).
Effect of gastric drainage plus erythromycin therapy
Gastric exposure to bile for the supine period was significantly shorter (p = 0.026) in group 4 patients than in those of group 1 (0% [0 to 4.3] vs 44.6% [1.3 to 68.4]), so that bile exposure in group 4 patients was similar to that in controls (0% [0 to 4.3] vs 3.6% [0.9 to 13.4]; p = 0.124) (Fig 2). As for the upright period (Fig 3), no difference was found between group 4 patients and those of group 1 on the one hand (0.1% [0 to 13.8] vs 7.6% [0 to 27.7]; p = 0.384) and between group 4 patients and controls on the other (0.1% [0 to 13.8] vs 0.3% [0 to 4.5]; p = 0.712).
Effect of erythromycin discontinuation
Figure 4 shows that as compared to the situation in patients who had never been given erythromycin (combined groups 1 and 2), exposure of the gastric mucosa to bile during the total period of recording was significantly reduced in both those patients who had previously been given the drug (group 5) (19% [2.8 to 36.8] vs 0% [0 to 17.8]; p = 0.023) and those who were under erythromycin therapy at the time of the study (groups 3 and 4) (19% [2.8 to 36.8] vs 5% [0.1 to 18.6]; p = 0.042). In contrast, gastric bile exposure in the two latter categories of patients was not significantly different from that in controls (p = 0.194 and p = 0.873, respectively). Moreover, there was no statistically significant difference (p = 0.234) between patients in whom erythromycin therapy had been discontinued (group 5) and those who were taking the drug (combined groups 3 and 4) (0% [0 to 17.8] vs 4.9% [0.1 to 18.6]).
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Fig 4. Total gastric exposure to bile in controls (left), patients who had never been given erythromycin (center left), patients who were taking the drug at the time of the study (center right), and patients who were no longer taking the drug (right). Box plot shows medians, interquartile ranges, and absolute ranges.
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Effect of time elapsed since the operation
Considering the 10 patients who underwent a second examination after a follow-up period ranging from 34 to 42 months (Fig 5), total gastric bile exposure on the second examination was shorter than on the first examination in 8 patients whereas it was longer in 2. None of these 2 patients had ever been given erythromycin. Overall, total bile exposure dropped from 37.7% [11.5 to 51.8] on the first examination to 9% [0 to 34.0] on the second examination (p = 0.046).
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Fig 5. Total gastric exposure to bile in patients investigated twice (thick lines = 8 patients with a decrease in bile exposure with time; dashed lines = 2 patients with an increase in bile exposure with time).
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Comment
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Truncal vagotomy impairs antral propulsive activity [3, 5], does not allow vagal input from the central nervous system to decrease pyloric resistance to gastric outflow [24], makes gastric emptying posture-dependent [25], and alters gallbladder contractility [4], processes that are thought to increase gastric exposure to bile. In addition, placement of the gastric pouch in a negative-pressure environment such as the chest cavity creates a duodenogastric reflux- promoting pressure gradient [6]. Despite all these changes, the current study indicates that within the limits of reliability of the Bilitec 2000 device [18], combined truncal vagotomy and transthoracic elevation of the stomach do not affect gastric bile exposure in every patient. Indeed, one quarter of patients without any gastric drainage procedure and never given erythromycin had a normal Bilitec test. This is to be paralleled to our recent observation that truncal vagotomy fails to alkalinize gastric contents of 33% of patients just after gastric transposition for esophageal replacement [26]. Likewise, although the wide range in terms of magnitude of gastric bile exposure we observed in the current study may just reflect preoperative differences in gastric bile exposure from one subject to another, it may also express individual variations in the modulatory effects of the central nervous system on the enteric nervous system within the gut wall.
Although a substantial number of patients had a positive Bilitec test in both the upright and supine positions, the increase in gastric bile exposure was more marked in the latter position than in the former, indicating that transpyloric flow is more posture-dependent after than before vagotomy [10, 25]. In fact, similarly to the situation in the normally innervated intraabdominal stomach [23], bile exposure of the denervated stomach as an esophageal substitute is longer when the patient assumes the supine position during the night than when he is in the erect position during the day. However, unlike the supine position, the upright position allows gravity [10] to compensate, in part at least, for the decrease in antral propulsive activity [3, 5] and the lack of pyloric relaxation on vagal stimulation [24].
Contrary to the general opinion that performance of a gastric drainage procedure predisposes to the presence of duodenal juice in the lumen of the vagotomized stomach [8], the current study shows that neither enlargement of the pylorus nor postoperative administration of a prokinetics such as erythromycin are able to modify gastric exposure to bile significantly when these measures are taken in an isolated fashion. In contrast, combination of these two measures tends to normalize gastric bile exposure. Indeed, the percentage of supine time bile was present in the gastric cavity in patients both having a gastric drainage procedure and being given erythromycin was similar to that in healthy subjects.
Actually, the reduction in pyloric resistance to gastric outflow that follows pyloroplasty or pyloromyotomy [27] seems to be insufficient to fully compensate for postvagotomy antral [3, 5] and gallbladder [4] hypocontractility and related gastric stasis [3] and duodenogastric reflux [8, 9, 12]. Likewise, although erythromycin increases antral contractility [20], accelerates vagotomy-delayed gastric emptying [21], and improves delivery of bile into the duodenum [28], the sole administration of the drug fails to normalize bile exposure of the denervated stomach, probably because its relaxing action on the pylorus requires an intact vagal supply. We know, indeed, from animal experiments [29] that unlike the stimulating action of the drug on antral contractility, erythromycin-induced decrease in pyloric resistance to gastric outflow is abolished by acute vagal cooling, so that in the latter condition, pyloric resistance is able to overcome the increase in antral propulsive activity. In contrast, the current study indicates that anatomic destruction of the pyloric resistor by means of a pyloroplasty or pyloromyotomy allows erythromycin –enhanced antral contractility [5] to compensate for the mechanisms that increase gastric bile exposure after vagotomy.
Bile exposure in the current study was similar in patients who were taking erythromycin and those who were no longer under prokinetic therapy at the time of the Bilitec test. This observation could theoretically be related to either spontaneous recovery of antral motility over the years that follow truncal vagotomy [5] or the fact that the effects of erythromycin on bile reflux [6, 21] may persist after discontinuation of the drug. The latter explanation is supported by our previous observation [20] that in some patients, erythromycin–enhanced antral contractility early after gastric pull-up persists after the prokinetic therapy has been discontinued for a 4-week period. All this suggests that early postoperative administration of a motilin-receptor agonist [19] such as erythromycin can maintain the gastric machinery in motion, acting as a battery charger that revives the gastric myenteric plexus that has been disconnected from the central nervous system. In contrast, the trend for a spontaneous reduction in gastric bile exposure with time we have noted in the current study probably reflects the spontaneous antral motor recovery process that takes place over the years following extrinsic denervation of the stomach [5], in relation to progressive self-reorganization of the myenteric plexus within the gastric wall [30].
In conclusion, the study strongly suggests that, as far as gastric bile exposure is concerned, a gastric drainage procedure such as a pyloroplasty or a pyloromyotomy should be added to truncal vagotomy and gastric pull-up to the neck and that patients should be given erythromycin during a few-month period after the operation. In this way, the enlarged pylorus cannot oppose resistance to enhanced antral contractility, which facilitates prompt reexpulsion of duodenal refluxate into the duodenal lumen.
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Acknowledgments
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We thank Mrs Nadine Thiebaut and Ms Anja Kalwa for their kind assistance, and UCB-Pharma, Braines, Belgium for its financial support to Doctor Christian Gutschow.
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Abstract
Introduction
