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Effect of parietal cell vagotomy on gastric emptying in duodenal ulcer disease
Effect of Parietal Cell Vagotomy on Gastric Emptying In Duodenal Ulcer Disease Jureta W. Horton, PhD, Dallas, Texas Robert N. McClelland, MD, Dallas, Texas Robert V. Weger, MD, Dallas, Texas
The use of truncal vagotomy with a drainage procedure in the surgical treatment of chronic duodenal ulcer disease is associated with numerous side effects. Postvagotomy alterations in gastric motility result in a significant incidence of atonia, diarrhea, vomiting and dumping during the postoperative course [I]. The development of parietal cell vagotomy with preservation of antral innervation and the pylorus is directed at a reduction in postgastric surgery side effects. Theoretical advantages of parietal cell vagotomy include (1) preservation of normal gastric motility and emptying, (2) a 75 to 85 percent reduction in basal acid secretion and a 50 to 70 percent reduction in stimulated acid secretion, and (3) unimpaired duodenal hormone secretion [2,3]. The use of radioisotopic techniques for the noninvasive study of gastric emptying is well documented, and gastric emptying rates in healthy volunteers and in post-truncal vagotomy subjects have been reported [4-8]. The purpose of the present study was to determine the immediate and long-term effects of parietal cell vagotomy on gastric emptying patterns, acid secretion and serum gastrin levels. These variables were measured preoperatively, during the early postoperative period, and more than 1 year after operation. Methods Patient
selection:
Nineteen patients of both sexes with an age range of 21 to 84 years (mean 48) were included in this study. These patients were selected as candidates for surgical treatment of intractable chronic pain due to duodenal ulcer disease that had proved unresponsive to conservative medical therapy. Preoperatively, all patients underwent contrast studies and endoscopy; patients with documented perforation, bleeding or mechanical obstruction were excluded from this study. Gastric emptying: Gastric emptying of a special test meal was studied in all 19 patients during the preoperative period and 7 to 90 days postoperatively. Gastric emptying in three patients who initially showed significant but not clinically symptomatic gastric retention was studied more Fromthe Department of Surgery, Southwestern Medical School, The University Of Texas Health Science Center at Dallas, 5323 Harry Hines Boulevard, Dallas, Texas 75235. HeCfUeStSfor reprints should be addressed to Jureta W. Horton, PhD, Department of Surgery, University of Texas Health Science Center at Dallas, 5323 Harry Hines Boulevard, Dallas, Texas 75235. presented at the 22nd Annual Meeting of The Society for Surgery of the Alimentary Tract, New York, New York, May 19-20. 1981. 86
than 1 year postoperatively.
The test meal consisted of a scrambled egg and a piece of toast. One mCi of technetium-99 diethylenetriamene was mixed with a teaspoon of jelly and spread on the toast. After ingesting the test meal, the subject was seated comfortably in a specially designed gamma chair and reclined at a 70” angle. The collimator of a Searle Model Pho-Gamma 5 gamma camera was approximated against the epigastrium and the stomach viewed from the anterior projection. Upon appearance of radioactivity in the stomach, the gamma camera windows were adjusted to allow imaging of the area of interest. Correct positioning of the gamma camera was assured by visual examination of the camera screen (Figure 1). An initial meal volume was calculated from the total counts in the defined area of interest; sequential images and calculation of total counts in the stomach were recorded at 60 second intervals for 30 minutes. The scintillation camera was interfaced with a minicomputer system; all images were recorded on magnetic discs for computer analysis. Counts corrected for decay and background radiation were used in the generation of time-activity curves of stomach activity using a MDS-Modumed Trinary Minicomputer System (Medical Data Systems). The first 30 minutes of the curve after initial emptying was analyzed by a linear regression method. Gastric emptying rates (ml/100 ml/ min) and the percent gastric retention 30 minutes after ingestion was calculated. Graphic results are expressed as the percent retention at 5 minute intervals of imaging.
Gastric acid secretion and serum gastrin: Basal acid secretion was measured by placing a nasogastric tube in the gastric antrum for aspiration of gastric contents at 60 minute intervals. The concentrations of hydrogen ion and volume of aspirated contents were measured. A venous blood sample was collected and the serum gastrin concentration measured by radioimmunoassay [9]. Surgical procedure: Parietal cell vagotomy was carried out using a technique similar to that described by Jordan [IO] and Hallenbeck et al [II]. The anterior and posterior vagal trunks were identified proximal to the gastroesophageal junction. The trunks were carefully freed up and retracted away from the esophagus to prevent injury. After this, all branches of the anterior and posterior vagi to the proximal stomach and distal esophagus were sectioned by dividing the lesser omentum at its junction with the lesser curvature of the stomach from a point 6 cm proximal to the pylorus up to 5 to 7 cm above the gastroesophageal junction. The dissection of the lesser curvature of the stomach was continued proximally from the gastroesophageal junction until the distal 5 to 7 cm of the esophagus was completely denervated. Statistical analysis: All mean values and standard errors of the mean were calculated. A two-sample t test was The American Journal of Surgery
Gastric Emptying and Parietal Cell Vagotomy
Figure 1. Example ot a gastric scan at intervals after Ingestion of a technetiumggm labeled test meal. 7?tis scan demonstrates a normal fate of gastric emptying.
-_ 20 10
I5
-
I
v
I
i i
f:
:Z$
;gii:.
pjIp{,
n= 19
20
Pre-Op
10
111**.11* pas+_(&
gg
%w
;fjQ y 7 a>i.4 I
pjiki.
Pre-Op .....*.I.post_op 5
lo
30
15
20
25
30
MINUTES
MINUTES Figure 2. Comparlson of gastric emptying rates in 19 patients before and after par/eta/ cell vagotomy.
F&we 3. Delayed pre- and postoperative gastric emptying in nine patlents.
ioo employed to compare differences in the two populations, and p values < 0.05 were considered significant. Results
All patients included in this series were studied pre- and postoperatively. An assessment of gastric emptying before parietal cell vagotomy demonstrated a 49.2 f 4.8 percent retention (-1.45 f 0.25 ml/100 ml/min [mean f standard error of the mean]). Gastric emptying rates before surgery in these 19 patients were significantly slower (p = 0.05) than the gastric emptying rates previously established in 40 healthy adult volunteers (-1.74 f 0.15 ml/100 ml/ min) [4] (Figure 2). The 19 subjects in this study were divided into two groups on the basis of their initial gastric scans. While all patients had no clinical evidence of gastric retention before parietal cell vagotomy, gross delay in gastric emptying was documented by scan preoperatively in nine patients in group A who had a mean gastric retention of 69.0 f 4.1 percent at 30 minutes (-0.91 f 0.14 ml/100 ml/min [p = 0.051) (Figure 3). The 10 patients in group B had a normal mean preoperative gastric emptying rate by scan of 34.8 f 4.01 percent retention at 30 minutes (-1.99 f 0.13 ml/100 ml/min) (Figure 4). Gastric emptying rates were measured by scan in all subjects 7 to 90 days after parietal cell vagotomy. The gastric emptying rate was significantly delayed during the early postoperative period with a mean retention rate of 67.8 f 4.4 percent at 30 minutes (-1.02 Volume
f 0.24 ml/100 143, January
1982
ml/min
[p = 0.051) (Table
I).
90 z
80
c
70
5
60
L IX
50
S
40
5
10
15
20
25
30
MINUTES Figure 4. Normal preoperative and delayed postoperative gastrk emptying in 10 patients.
Evaluation of gastric emptying in the two groups of patients after parietal cell vagotomy demonstrated varying responses in emptying rates. In group A, characterized by delayed gastric emptying in the preoperative period, there was an improvement in gastric emptying in three patients and no change in gastric emptying rates in six patients after parietal cell vagotomy. In group B, characterized by normal gastric emptying preoperatively, there was also a variable response to parietal cell vagotomy. Eight patients in group B had an increase in gastric retention after surgery, whereas no change in emptying was apparent in the remaining two patients in this group. 87
Horton et al
TABLE I
Immediate Postoperative Evaluation of Parietal Cell Vagotomy (mean f standard error of the mean)
Gastric retention Percent ml/ 100 ml/min BAO (mEq/hour) PA0 (mEq/hour) Gastrin (pg/ml)
Preoperative
Postoperative
49.2 f 4.9’ -1.5 f 0.3’ 5.6 f 1.3t 45.6 f 3.5t Normap
67.6 f 5.5’ -1.0 f 0.2‘ 1.2 f 0.9* 16.3 f 4.6t Normals
Nineteen patients; t 15 patients; t 11 patients; 5 12 patients. BAO = basal acid output; PA0 = peak acid output. l
Three of the patients in whom gastric retention was documented by scan postoperatively were restudied more than 1 year after parietal cell vagotomy (mean 25 months). Delayed emptying was observed in these patients; the mean gastric retention rate at 30 minutes was 61.5 f 4.5 percent (-1.14 f 0.28 ml/100 ml/min [p = 0.051) (Table II). Basal and peak acid output were measured in 15 patients within approximately 1 week before parietal cell vagotomy. Acid secretion was again measured in 11 patients approximately 7 weeks postoperatively. Basal acid output ranged from 1.1 to 20.9 mEq/hour preoperatively and decreased after vagotomy in all patients, with a mean decrease of 78.9 percent. Peak acid output ranged from 28.8 to 68.4 mEq/hour preoperatively, and decreased after vagotomy in all patients with a mean decrease of 64.1 percent (Table I). Serum gastrin levels before parietal cell vagotomy were normal in the 15 patients who were studied. Serum gastrin levels were slightly higher after parietal cell vagotomy but still remained within normal limits. However, serum gastrin levels remained with the normal range postoperatively. The use of two different techniques of gastrin measurement at Parkland Memorial Hospital and the Dallas Veterans Administration Hospital with different upper limits of normal precluded calculation of a mean serum gastrin level for these patients. However, serum gastrin levels were consistently in the low range of normal. Comments In this study parietal cell vagotomy decisively affected gastric emptying patterns. First, delayed gastric emptying was documented preoperatively in 9 of the patients, but was within normal limits in the remaining 10. These results differ from those in earlier reports of accelerated gastric emptying [12], but confirm reports of normal emptying patterns in other series of duodenal ulcer patients [9,13]. In addition, we demonstrated a significant delay in gastric emptying (p = 0.05) in 17 of 19 patients during the early period after parietal cell vagotomy (7 to 90 days after surgery). Delayed emptying occurred regardless 88
TABLE II
Late Postoperatlve Evaluation of Parietal Cell Vagotomy (mean f standard error of the mean)
Gastric retention Percent ml/l00 ml/min BAQ (mEq/hour) PACY(mEq/hour) Gastrin (pg/ml)
Preooerative
Postooerative
43.7 f 6.6 -1.8 f 0.3 3.8 f 1.6 39.0 f 5.1 Normal
77.6 f 6.6 -0.7 f 0.2 0.0 f 0.0 5.7 f 1.3 Normal
>l
Year
61.5 f 4.5 -1.1 f 0.3 0.4 f 0.2 9.9 f 3.4 Normal
BAO = basal acid output; PA0 = peak acid output.
of whether the patient had normal or delayed gastric scans preoperatively. Previous studies by other investigators of gastric emptying early after postparietal cell vagotomy have produced varying results including normal emptying patterns [13-151, accelerated emptying [9,16,17] and delayed gastric emptying [12]. Transient gastric retention has also been described after truncal vagotomy with pyloroplasty [5] and after parietal cell vagotomy [6]. All patients included in the present study were asymptomatic with regard to gastric atonia during both the pre- and postoperative periods. Finally, delayed emptying rates were documented in three patients during the late period after parietal cell vagotomy (13 to 37 months after surgery). These patients were selected for long-term study because of a gross delay in gastric emptying soon after vagotomy. Our findings of persistent gastric retention more than 1 year after parietal cell vagotomy differ from previous reports of a spontaneous improvement in gastric emptying 3 to 6 months after parietal cell vagotomy [6,22] and truncal vagotomy [5]. While numerous methods for measuring gastric emptying rates have been described [9,18,19], a radioisotope scanning technique was utilized in this study. The use of a noninvasive radioisotope scan method with external detection eliminated gastric intubation, included ingestion of a normal meal and proved more reproducible than gastric aspiration techniques. Certain limitations of a radioisotopic technique for evaluation of gastric emptying were recognized. Anatomic variation in patients with differences in physical stature as well as position of the stomach are definite variables. However, the use of a specially constructed chair positioned all patients in a semirecumbent position at precisely the same angle beneath the gamma camera and assured a standardized method of assessing emptying patterns. While many isotopic indicators have been used, a technetium-99m diethylenetriamene labeled egg and toast meal has been used exclusively at Parkland Memorial Hospital and the Veterans Administration Hospital in Dallas. Previous work by our laboratory demonstrated a reproducible gastric emptying pattern in 40 healthy volunteers with less than 40 percent of the ingested meal retained in the stomach The American Journal of Surgery
Gastric
after 30 minutes of scanning. A retention rate of more than 40 percent 30 minutes after ingestion has been established in our laboratory as evidence of functional or mechanical gastric atonia [4]. Comparison of gastric emptying rates in duodenal ulcer patients pre- and postoperatively is difficult because of a number of factors, including different methods of assessing gastric emptying, the use of solid, liquid and combination types of meals, and the length of the postoperative interval selected for study. Our study confirmed earlier descriptions of gastric emptying patterns [8,20]. Ingestion of the test meal was followed by an initial phase of rapid emptying (5 to 15 minutes) and a second phase of slower emptying at 15 to 45 minutes. The present study demonstrated delayed gastric emptying up to 37 months after parietal cell vagotomy and differs sharply from previous reports of an absence of gastric stasis throughout the postoperative period. In this study, parietal cell vagotomy without drainage was highly effective in long-term reduction of acid secretion, confirming previous reports of reduced basal and stimulated acid secretion after parietal cell vagotomy [9,10]. The normal serum gastrin levels during the early postoperative period in all patients studied and in three patients studied during the late postoperative period are in contrast to a previous report of increased serum gastrin levels after parietal cell vagotomy [9]. Despite the persistent gastric retention documented by scan in the late postoperative period (13 to 37 months), the gastric acid and serum gastrin levels remained low and there was no evidence of ulcer recurrence. Therefore, these findings strongly suggest that the degree of gastric retention in these patients after parietal cell vagotomy is not sufficient to cause increased acid secretion due to excessive antral stimulation and secretion of gastrin. There were no deaths among the 19 patients followed up to 37 months after parietal cell vagotomy. Also, there were no symptoms of weight loss, dumping or diarrhea in these patients. Summary Gastric emptying was delayed preoperatively in 9 of 19 patients with duodenal ulcer disease, but all 9 patients with evidence of retention by scan were asymptomatic; gastric emptying was normal in the remaining 10 patients. A significant delay in gastric emptying was documented by scan in 17 of 19 patients immediately after parietal cell vagotomy (despite the absence of symptoms of gastric retention). Delayed emptying was demonstrated in three patients who were restudied more than 1 year after parietal cell vagotomy; again these patients had no symptoms of gastric retention at any time. A sustained reduction in basal and stimulated acid secretion in both the early and late postoperative periods was documented in all 19 patients, and serum gastrin levels also remained low. This absence of acid or Volume 143, January 1982
Emptying
and Parietal
Cell Vagotomy
gastrin stimulation is corroborated by the fact that there was no recurrence of ulcers in these patients during a follow-up period of up to 37 months. References 1. Jordan PH Jr, Condon RE. A prospective evaluation of vagotomy-pyloroplasty and vagotomy-antrectomy for treatment of duodenal ulcer. Ann Surg 1970;172:547-55. 2. Jordan PH Jr. An interim report on parietal cell vagotomy versus selective vagotomy and antrectomy for treatment of duodenal ulcer. Ann Surg 1979;189:643-53. 3. Miller B, Bombeck CT, Schumer W, Condon RE, Nyhus LM. Vagotomy limited to the parietal cell mass. Preliminary patient studies. Arch Surg 1971;103:153-7. 4. McClelland RN, Horton JW. Relief of acute, persistent postvagotomy atony by metoclopramide. Ann Surg 1978;188: 9-17. 5. Cowley DJ, Vernon P, Jones T, Glass HI, Cox AG. Gastric emptying of solid meals after truncal vagotomy and pyloroplasty in human subjects, Gut 1972;13:176-81. 6. Kalbasi H, Hudson FR, Herring A, Moss S, Glass HI, Spencer J. Gastric emptying following vagotomy and antrectomy and proximal gastric vagotomy. Gut 1975;16:509-13. 7. Sheiner HJ, Quinlan MF, Thompson IJ. Gastric motility and emptying in normal and post-vagotomy subjects. Gut 1980;21:753-9. 8. Gustavsson S, Hemmingsson A, Jung B, Nilsson F, Wadin K. Gastric emptying in duodenal ulcer patients before and after truncal vagotomy with pyloroplasty and parietal cell vagotomv. Acta Chir Stand 1978:144:379-85. 9. Feldman M, Dickerman RM, McClelland RN, Cooper KA, Walsh JH, Richardson CT. Effect of selective proximal vagotomy on food-stimulated gastric acid secretion and gastrin release in patients with duodenal ulcer. Gastroenterology 1979; 76:926-31. 10. Jordan PH Jr. Current status of parietal cell vagotomy. Ann Surg 1976;184:659-71. 11. Hallenbeck GA, Gleysteen JJ, Aldrete JS, et al. Proximal gastric vagotomy: effects of two operative techniques on clinical and gastric secretory results. Ann Surg 1976;184:43542. 12. Guerts WJC, Winckers EKA, Wittebol P. The effects of highly selective vagotomy on secretion and emptying of the stomach. Surg Gynecol Obstet 1977;145:826-36. 13. Brandsborg 0, Brandsborg M, Levgreen NA, et al. Influence of parietal cell vagotomy and selective gastric vagotomy on gastric emptying rate and serum gastrin concentration. Gastroenterology 1977;72:212-4. 14. Wilkinson AJ, Johnston D. Effect of truncal, selective and highly selective vagotomy on gastric emptying and intestinal transit of a food-barium meal in man. Ann Surg 1973; 178: 190-8. 15. Poppen B, Delin A. Parietal cell vagotomy for duodenal and pyloric ulcers. I. Clinical factors leading to failure of the operation. Am J Surg 1981;141:323-9. 16. Hancock BD, Bowen-Jones E, Dixon R. Testa HT, Dymock IW, Cowley DJ. The effect of posture on gastric emptying of solid meals in normal subjects and patients after vagotomy. Br J Surg 1974;61:326-30. 17. Lavigne ME, Wiley ZD, Martin P, et al. Gastric, pancreatic, and biliary secretion and the rate of gastric emptying after parietal cell vagotomy. Am J Surg 1979;138:644-51. 18. Holt S, McDicken WN, Anderson T, Stewart IC, Heading RC. Dynamic imaging of the stomach by real-time ultrasound-a method for the study of gastric motility. Gut 1980;21: 597-601. 19. Perkel MS, Moore C, Hersh T, Davidson ED. Metoclopramide therapy in patients with delayed gastric emptying. A randomized, double-blind study. Dig Dis Sci 1979;24:662-6. 20. Heading RC, Tothill P, McLaughlin GP, Shearman DJC. Gastric emptying rate measurement in man. A double isotope scanning technique for simultaneous study of liquid and solid components of a meal. Gastroenterology 1976:71:45-56.
89
The use of truncal vagotomy with a drainage procedure in the surgical treatment of chronic duodenal ulcer disease is associated with numerous side effects. Postvagotomy alterations in gastric motility result in a significant incidence of atonia, diarrhea, vomiting and dumping during the postoperative course [I]. The development of parietal cell vagotomy with preservation of antral innervation and the pylorus is directed at a reduction in postgastric surgery side effects. Theoretical advantages of parietal cell vagotomy include (1) preservation of normal gastric motility and emptying, (2) a 75 to 85 percent reduction in basal acid secretion and a 50 to 70 percent reduction in stimulated acid secretion, and (3) unimpaired duodenal hormone secretion [2,3]. The use of radioisotopic techniques for the noninvasive study of gastric emptying is well documented, and gastric emptying rates in healthy volunteers and in post-truncal vagotomy subjects have been reported [4-8]. The purpose of the present study was to determine the immediate and long-term effects of parietal cell vagotomy on gastric emptying patterns, acid secretion and serum gastrin levels. These variables were measured preoperatively, during the early postoperative period, and more than 1 year after operation. Methods Patient
selection:
Nineteen patients of both sexes with an age range of 21 to 84 years (mean 48) were included in this study. These patients were selected as candidates for surgical treatment of intractable chronic pain due to duodenal ulcer disease that had proved unresponsive to conservative medical therapy. Preoperatively, all patients underwent contrast studies and endoscopy; patients with documented perforation, bleeding or mechanical obstruction were excluded from this study. Gastric emptying: Gastric emptying of a special test meal was studied in all 19 patients during the preoperative period and 7 to 90 days postoperatively. Gastric emptying in three patients who initially showed significant but not clinically symptomatic gastric retention was studied more Fromthe Department of Surgery, Southwestern Medical School, The University Of Texas Health Science Center at Dallas, 5323 Harry Hines Boulevard, Dallas, Texas 75235. HeCfUeStSfor reprints should be addressed to Jureta W. Horton, PhD, Department of Surgery, University of Texas Health Science Center at Dallas, 5323 Harry Hines Boulevard, Dallas, Texas 75235. presented at the 22nd Annual Meeting of The Society for Surgery of the Alimentary Tract, New York, New York, May 19-20. 1981. 86
than 1 year postoperatively.
The test meal consisted of a scrambled egg and a piece of toast. One mCi of technetium-99 diethylenetriamene was mixed with a teaspoon of jelly and spread on the toast. After ingesting the test meal, the subject was seated comfortably in a specially designed gamma chair and reclined at a 70” angle. The collimator of a Searle Model Pho-Gamma 5 gamma camera was approximated against the epigastrium and the stomach viewed from the anterior projection. Upon appearance of radioactivity in the stomach, the gamma camera windows were adjusted to allow imaging of the area of interest. Correct positioning of the gamma camera was assured by visual examination of the camera screen (Figure 1). An initial meal volume was calculated from the total counts in the defined area of interest; sequential images and calculation of total counts in the stomach were recorded at 60 second intervals for 30 minutes. The scintillation camera was interfaced with a minicomputer system; all images were recorded on magnetic discs for computer analysis. Counts corrected for decay and background radiation were used in the generation of time-activity curves of stomach activity using a MDS-Modumed Trinary Minicomputer System (Medical Data Systems). The first 30 minutes of the curve after initial emptying was analyzed by a linear regression method. Gastric emptying rates (ml/100 ml/ min) and the percent gastric retention 30 minutes after ingestion was calculated. Graphic results are expressed as the percent retention at 5 minute intervals of imaging.
Gastric acid secretion and serum gastrin: Basal acid secretion was measured by placing a nasogastric tube in the gastric antrum for aspiration of gastric contents at 60 minute intervals. The concentrations of hydrogen ion and volume of aspirated contents were measured. A venous blood sample was collected and the serum gastrin concentration measured by radioimmunoassay [9]. Surgical procedure: Parietal cell vagotomy was carried out using a technique similar to that described by Jordan [IO] and Hallenbeck et al [II]. The anterior and posterior vagal trunks were identified proximal to the gastroesophageal junction. The trunks were carefully freed up and retracted away from the esophagus to prevent injury. After this, all branches of the anterior and posterior vagi to the proximal stomach and distal esophagus were sectioned by dividing the lesser omentum at its junction with the lesser curvature of the stomach from a point 6 cm proximal to the pylorus up to 5 to 7 cm above the gastroesophageal junction. The dissection of the lesser curvature of the stomach was continued proximally from the gastroesophageal junction until the distal 5 to 7 cm of the esophagus was completely denervated. Statistical analysis: All mean values and standard errors of the mean were calculated. A two-sample t test was The American Journal of Surgery
Gastric Emptying and Parietal Cell Vagotomy
Figure 1. Example ot a gastric scan at intervals after Ingestion of a technetiumggm labeled test meal. 7?tis scan demonstrates a normal fate of gastric emptying.
-_ 20 10
I5
-
I
v
I
i i
f:
:Z$
;gii:.
pjIp{,
n= 19
20
Pre-Op
10
111**.11* pas+_(&
gg
%w
;fjQ y 7 a>i.4 I
pjiki.
Pre-Op .....*.I.post_op 5
lo
30
15
20
25
30
MINUTES
MINUTES Figure 2. Comparlson of gastric emptying rates in 19 patients before and after par/eta/ cell vagotomy.
F&we 3. Delayed pre- and postoperative gastric emptying in nine patlents.
ioo employed to compare differences in the two populations, and p values < 0.05 were considered significant. Results
All patients included in this series were studied pre- and postoperatively. An assessment of gastric emptying before parietal cell vagotomy demonstrated a 49.2 f 4.8 percent retention (-1.45 f 0.25 ml/100 ml/min [mean f standard error of the mean]). Gastric emptying rates before surgery in these 19 patients were significantly slower (p = 0.05) than the gastric emptying rates previously established in 40 healthy adult volunteers (-1.74 f 0.15 ml/100 ml/ min) [4] (Figure 2). The 19 subjects in this study were divided into two groups on the basis of their initial gastric scans. While all patients had no clinical evidence of gastric retention before parietal cell vagotomy, gross delay in gastric emptying was documented by scan preoperatively in nine patients in group A who had a mean gastric retention of 69.0 f 4.1 percent at 30 minutes (-0.91 f 0.14 ml/100 ml/min [p = 0.051) (Figure 3). The 10 patients in group B had a normal mean preoperative gastric emptying rate by scan of 34.8 f 4.01 percent retention at 30 minutes (-1.99 f 0.13 ml/100 ml/min) (Figure 4). Gastric emptying rates were measured by scan in all subjects 7 to 90 days after parietal cell vagotomy. The gastric emptying rate was significantly delayed during the early postoperative period with a mean retention rate of 67.8 f 4.4 percent at 30 minutes (-1.02 Volume
f 0.24 ml/100 143, January
1982
ml/min
[p = 0.051) (Table
I).
90 z
80
c
70
5
60
L IX
50
S
40
5
10
15
20
25
30
MINUTES Figure 4. Normal preoperative and delayed postoperative gastrk emptying in 10 patients.
Evaluation of gastric emptying in the two groups of patients after parietal cell vagotomy demonstrated varying responses in emptying rates. In group A, characterized by delayed gastric emptying in the preoperative period, there was an improvement in gastric emptying in three patients and no change in gastric emptying rates in six patients after parietal cell vagotomy. In group B, characterized by normal gastric emptying preoperatively, there was also a variable response to parietal cell vagotomy. Eight patients in group B had an increase in gastric retention after surgery, whereas no change in emptying was apparent in the remaining two patients in this group. 87
Horton et al
TABLE I
Immediate Postoperative Evaluation of Parietal Cell Vagotomy (mean f standard error of the mean)
Gastric retention Percent ml/ 100 ml/min BAO (mEq/hour) PA0 (mEq/hour) Gastrin (pg/ml)
Preoperative
Postoperative
49.2 f 4.9’ -1.5 f 0.3’ 5.6 f 1.3t 45.6 f 3.5t Normap
67.6 f 5.5’ -1.0 f 0.2‘ 1.2 f 0.9* 16.3 f 4.6t Normals
Nineteen patients; t 15 patients; t 11 patients; 5 12 patients. BAO = basal acid output; PA0 = peak acid output. l
Three of the patients in whom gastric retention was documented by scan postoperatively were restudied more than 1 year after parietal cell vagotomy (mean 25 months). Delayed emptying was observed in these patients; the mean gastric retention rate at 30 minutes was 61.5 f 4.5 percent (-1.14 f 0.28 ml/100 ml/min [p = 0.051) (Table II). Basal and peak acid output were measured in 15 patients within approximately 1 week before parietal cell vagotomy. Acid secretion was again measured in 11 patients approximately 7 weeks postoperatively. Basal acid output ranged from 1.1 to 20.9 mEq/hour preoperatively and decreased after vagotomy in all patients, with a mean decrease of 78.9 percent. Peak acid output ranged from 28.8 to 68.4 mEq/hour preoperatively, and decreased after vagotomy in all patients with a mean decrease of 64.1 percent (Table I). Serum gastrin levels before parietal cell vagotomy were normal in the 15 patients who were studied. Serum gastrin levels were slightly higher after parietal cell vagotomy but still remained within normal limits. However, serum gastrin levels remained with the normal range postoperatively. The use of two different techniques of gastrin measurement at Parkland Memorial Hospital and the Dallas Veterans Administration Hospital with different upper limits of normal precluded calculation of a mean serum gastrin level for these patients. However, serum gastrin levels were consistently in the low range of normal. Comments In this study parietal cell vagotomy decisively affected gastric emptying patterns. First, delayed gastric emptying was documented preoperatively in 9 of the patients, but was within normal limits in the remaining 10. These results differ from those in earlier reports of accelerated gastric emptying [12], but confirm reports of normal emptying patterns in other series of duodenal ulcer patients [9,13]. In addition, we demonstrated a significant delay in gastric emptying (p = 0.05) in 17 of 19 patients during the early period after parietal cell vagotomy (7 to 90 days after surgery). Delayed emptying occurred regardless 88
TABLE II
Late Postoperatlve Evaluation of Parietal Cell Vagotomy (mean f standard error of the mean)
Gastric retention Percent ml/l00 ml/min BAQ (mEq/hour) PACY(mEq/hour) Gastrin (pg/ml)
Preooerative
Postooerative
43.7 f 6.6 -1.8 f 0.3 3.8 f 1.6 39.0 f 5.1 Normal
77.6 f 6.6 -0.7 f 0.2 0.0 f 0.0 5.7 f 1.3 Normal
>l
Year
61.5 f 4.5 -1.1 f 0.3 0.4 f 0.2 9.9 f 3.4 Normal
BAO = basal acid output; PA0 = peak acid output.
of whether the patient had normal or delayed gastric scans preoperatively. Previous studies by other investigators of gastric emptying early after postparietal cell vagotomy have produced varying results including normal emptying patterns [13-151, accelerated emptying [9,16,17] and delayed gastric emptying [12]. Transient gastric retention has also been described after truncal vagotomy with pyloroplasty [5] and after parietal cell vagotomy [6]. All patients included in the present study were asymptomatic with regard to gastric atonia during both the pre- and postoperative periods. Finally, delayed emptying rates were documented in three patients during the late period after parietal cell vagotomy (13 to 37 months after surgery). These patients were selected for long-term study because of a gross delay in gastric emptying soon after vagotomy. Our findings of persistent gastric retention more than 1 year after parietal cell vagotomy differ from previous reports of a spontaneous improvement in gastric emptying 3 to 6 months after parietal cell vagotomy [6,22] and truncal vagotomy [5]. While numerous methods for measuring gastric emptying rates have been described [9,18,19], a radioisotope scanning technique was utilized in this study. The use of a noninvasive radioisotope scan method with external detection eliminated gastric intubation, included ingestion of a normal meal and proved more reproducible than gastric aspiration techniques. Certain limitations of a radioisotopic technique for evaluation of gastric emptying were recognized. Anatomic variation in patients with differences in physical stature as well as position of the stomach are definite variables. However, the use of a specially constructed chair positioned all patients in a semirecumbent position at precisely the same angle beneath the gamma camera and assured a standardized method of assessing emptying patterns. While many isotopic indicators have been used, a technetium-99m diethylenetriamene labeled egg and toast meal has been used exclusively at Parkland Memorial Hospital and the Veterans Administration Hospital in Dallas. Previous work by our laboratory demonstrated a reproducible gastric emptying pattern in 40 healthy volunteers with less than 40 percent of the ingested meal retained in the stomach The American Journal of Surgery
Gastric
after 30 minutes of scanning. A retention rate of more than 40 percent 30 minutes after ingestion has been established in our laboratory as evidence of functional or mechanical gastric atonia [4]. Comparison of gastric emptying rates in duodenal ulcer patients pre- and postoperatively is difficult because of a number of factors, including different methods of assessing gastric emptying, the use of solid, liquid and combination types of meals, and the length of the postoperative interval selected for study. Our study confirmed earlier descriptions of gastric emptying patterns [8,20]. Ingestion of the test meal was followed by an initial phase of rapid emptying (5 to 15 minutes) and a second phase of slower emptying at 15 to 45 minutes. The present study demonstrated delayed gastric emptying up to 37 months after parietal cell vagotomy and differs sharply from previous reports of an absence of gastric stasis throughout the postoperative period. In this study, parietal cell vagotomy without drainage was highly effective in long-term reduction of acid secretion, confirming previous reports of reduced basal and stimulated acid secretion after parietal cell vagotomy [9,10]. The normal serum gastrin levels during the early postoperative period in all patients studied and in three patients studied during the late postoperative period are in contrast to a previous report of increased serum gastrin levels after parietal cell vagotomy [9]. Despite the persistent gastric retention documented by scan in the late postoperative period (13 to 37 months), the gastric acid and serum gastrin levels remained low and there was no evidence of ulcer recurrence. Therefore, these findings strongly suggest that the degree of gastric retention in these patients after parietal cell vagotomy is not sufficient to cause increased acid secretion due to excessive antral stimulation and secretion of gastrin. There were no deaths among the 19 patients followed up to 37 months after parietal cell vagotomy. Also, there were no symptoms of weight loss, dumping or diarrhea in these patients. Summary Gastric emptying was delayed preoperatively in 9 of 19 patients with duodenal ulcer disease, but all 9 patients with evidence of retention by scan were asymptomatic; gastric emptying was normal in the remaining 10 patients. A significant delay in gastric emptying was documented by scan in 17 of 19 patients immediately after parietal cell vagotomy (despite the absence of symptoms of gastric retention). Delayed emptying was demonstrated in three patients who were restudied more than 1 year after parietal cell vagotomy; again these patients had no symptoms of gastric retention at any time. A sustained reduction in basal and stimulated acid secretion in both the early and late postoperative periods was documented in all 19 patients, and serum gastrin levels also remained low. This absence of acid or Volume 143, January 1982
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Cell Vagotomy
gastrin stimulation is corroborated by the fact that there was no recurrence of ulcers in these patients during a follow-up period of up to 37 months. References 1. Jordan PH Jr, Condon RE. A prospective evaluation of vagotomy-pyloroplasty and vagotomy-antrectomy for treatment of duodenal ulcer. Ann Surg 1970;172:547-55. 2. Jordan PH Jr. An interim report on parietal cell vagotomy versus selective vagotomy and antrectomy for treatment of duodenal ulcer. Ann Surg 1979;189:643-53. 3. Miller B, Bombeck CT, Schumer W, Condon RE, Nyhus LM. Vagotomy limited to the parietal cell mass. Preliminary patient studies. Arch Surg 1971;103:153-7. 4. McClelland RN, Horton JW. Relief of acute, persistent postvagotomy atony by metoclopramide. Ann Surg 1978;188: 9-17. 5. Cowley DJ, Vernon P, Jones T, Glass HI, Cox AG. Gastric emptying of solid meals after truncal vagotomy and pyloroplasty in human subjects, Gut 1972;13:176-81. 6. Kalbasi H, Hudson FR, Herring A, Moss S, Glass HI, Spencer J. Gastric emptying following vagotomy and antrectomy and proximal gastric vagotomy. Gut 1975;16:509-13. 7. Sheiner HJ, Quinlan MF, Thompson IJ. Gastric motility and emptying in normal and post-vagotomy subjects. Gut 1980;21:753-9. 8. Gustavsson S, Hemmingsson A, Jung B, Nilsson F, Wadin K. Gastric emptying in duodenal ulcer patients before and after truncal vagotomy with pyloroplasty and parietal cell vagotomv. Acta Chir Stand 1978:144:379-85. 9. Feldman M, Dickerman RM, McClelland RN, Cooper KA, Walsh JH, Richardson CT. Effect of selective proximal vagotomy on food-stimulated gastric acid secretion and gastrin release in patients with duodenal ulcer. Gastroenterology 1979; 76:926-31. 10. Jordan PH Jr. Current status of parietal cell vagotomy. Ann Surg 1976;184:659-71. 11. Hallenbeck GA, Gleysteen JJ, Aldrete JS, et al. Proximal gastric vagotomy: effects of two operative techniques on clinical and gastric secretory results. Ann Surg 1976;184:43542. 12. Guerts WJC, Winckers EKA, Wittebol P. The effects of highly selective vagotomy on secretion and emptying of the stomach. Surg Gynecol Obstet 1977;145:826-36. 13. Brandsborg 0, Brandsborg M, Levgreen NA, et al. Influence of parietal cell vagotomy and selective gastric vagotomy on gastric emptying rate and serum gastrin concentration. Gastroenterology 1977;72:212-4. 14. Wilkinson AJ, Johnston D. Effect of truncal, selective and highly selective vagotomy on gastric emptying and intestinal transit of a food-barium meal in man. Ann Surg 1973; 178: 190-8. 15. Poppen B, Delin A. Parietal cell vagotomy for duodenal and pyloric ulcers. I. Clinical factors leading to failure of the operation. Am J Surg 1981;141:323-9. 16. Hancock BD, Bowen-Jones E, Dixon R. Testa HT, Dymock IW, Cowley DJ. The effect of posture on gastric emptying of solid meals in normal subjects and patients after vagotomy. Br J Surg 1974;61:326-30. 17. Lavigne ME, Wiley ZD, Martin P, et al. Gastric, pancreatic, and biliary secretion and the rate of gastric emptying after parietal cell vagotomy. Am J Surg 1979;138:644-51. 18. Holt S, McDicken WN, Anderson T, Stewart IC, Heading RC. Dynamic imaging of the stomach by real-time ultrasound-a method for the study of gastric motility. Gut 1980;21: 597-601. 19. Perkel MS, Moore C, Hersh T, Davidson ED. Metoclopramide therapy in patients with delayed gastric emptying. A randomized, double-blind study. Dig Dis Sci 1979;24:662-6. 20. Heading RC, Tothill P, McLaughlin GP, Shearman DJC. Gastric emptying rate measurement in man. A double isotope scanning technique for simultaneous study of liquid and solid components of a meal. Gastroenterology 1976:71:45-56.
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