ANNALS OF SURGERY

Vol. 184

December 1976

No.

6

Surgical Progress

Current Status of Parietal Cell Vagotomy PAUL H. JORDAN, JR., M.D.

In surgery. as in all the arts, progress is usually to be measured by the gradual transition from complex and intricate procedures to those of a simpler kind" Berkeley Moynihan, 1908.9:3 "

T MIGHT BE ARGUED that surgical treatment for benign I gastric and duodenal ulcers has reached such a high degree of perfection that there is little room for improvement. The results obtained with current operations are, indeed, good to excellent in 80 to 90%o of patients; but, in the remaining patients, gastric complaints occur that vary in severity from being tolerable to totally disabling. Therefore, surgeons continue their efforts to devise an operation that will prevent the poor results without sacrificing the good results already obtainable in the majority of patients.

Development of Vagotomy Although a procedure similar to selective vagotomy combined with gastroenterostomy was performed by Latarjet,77 the modern era of vagotomy for the treatment of duodenal ulcer began when Dragstedt and Owens19 introduced transthoracic vagotomy. Within a short time the problem of gastric stasis led to their adoption of transabdominal, truncal vagotomy combined with a drainage procedure.20 Subsequently, Jackson46 and Submitted for publication February 16, 1976. All correspondence: Paul H. Jordan, Jr., M.D., 1200 Moursund Avenue, Houston, Texas 77030. Abbreviations used: PCV-Parietal cell vagotomy without drainage; TV-D-Truncal vagotomy and drainage; SV-D-Selective vagotomy and drainage; SV-GE-Selective vagotomy and gastroenterostomy; SV-A-Selective vagotomy and antrectomy; SV-P-Selective vagotomy and pyloroplasty; BAO-Basal acid output; MAO-Maximal acid output.

From the Surgical Services of the Cora and Webb Mading Department of Surgery, Baylor College of Medicine and the Veterans Administration Hospital, Houston, Texas

Frankson28 thought that denervation of viscera other than the stomach was neither necessary nor desirable and independently re-introduced selective gastric vagotomy. In spite of theoretical advantages, selective vagotomy was not widely accepted because it was difficult to document its superiority. A few surgeons,92 however, preferred selective vagotomy because the meticulous dissection required to perform the procedure led to a higher incidence of complete denervation of the stomach. Griffith and Harkins32 understood that many of the complaints after gastric operations resulted from the loss, bypass, or mutilation of the pyloroantral pump that regulates gastric emptying. In order to preserve the integrity of this important mechanism when treating duodenal ulcer, they conceived the idea that the fundic gland area of the stomach could be denervated without destroying the innervation of the antrum, thus making it unnecessary to add a drainage procedure to prevent gastric stasis. Holle and Hart39 first performed vagotomy confined to the acid secreting portion of the stomach (Selektive Proximal Vagotomie) on man but their addition of a drainage procedure appeared to negate the advantage of the more conservative vagotomy. In their opinion, an inhibitory effect of the antral nerves on acid secretion was the major contribution of this type of vagotomy.37 Vagal denervation of the acid secreting portion of the stomach while preserving the antral nerves and the integrity of

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660

Ann. Surg.

9

December 1976

The potential disadvantages of the operation that have led to its cautious evaluation include: 1) The possibility that gastric stasis might occur and cause gastric ulcers. 2) Preservation of an innervated antrum might lead to excessive gastrin release and increased acid secretion. 3) Denervation of too much or too little of the stomach might result in gastric stasis or inadequate reduction of acid secretion. 4) The possibility that the recurrent ulcer rate might be unacceptable.

{V C

PAR IETAL CELL

1976

Bal4or Colege d Msd.e

FIG. 1. Diagrammatic representation of the three types of vagotomy: 1) Truncal or total intra-abdominal vagotomy; 2) Selective or total gastric vagotomy; and 3) Parietal cell vagotomy or vagotomy of the acid secreting portion of the stomach.

the pylorus was ultimately utilized in man by Johnston and Wilkinson51 and Amdrup and Jensen.2 Thus there are currently three types of vagotomy: Truncal vagotomy is a total intra-abdominal vagotomy; selective vagotomy is a total gastric vagotomy; and a vagotomy confined to the acid secreting portion or the fundic gland area of the stomach is referred to in this review as a parietal cell vagotomy (PCV) (Fig. 1). Potential Advantages and Disadvantages of PCV The potential advantages of PCV which have been considered include: 1) An innervated pylorus and antrum might provide near normal gastric emptying. 2) The extragastric and antral nerves might preserve inhibitory effects on acid secretion. 3) A functioning pylorus might reduce reflux into the stomach and thus protect the gastric mucosa from the damaging effects of duodenal contents. 4) Preservation of the duodenal innervation might permit normal release of duodenal hormones.

Method While the technique of PCV is one of individual preference, the end result should be essentially the same as that presented in the detailed description by Goligher.29 We divide the diaphragmatic attachment to the left lobe of the liver so that it may be retracted to the right. The anterior and posterior vagus trunks are identified and narrow tapes placed around them for traction. Beginning near the esophagogastric junction and with minimal traction on the anterior vagus nerve, the anterior leaf of the lesser omentum is serially sectioned, staying close to the stomach and avoiding injury to the hepatic branches and to the anterior nerve of Latarjet. When this dissection is well started, an opening is made in the gastro-colic omentum and the adhesions between the pancreas and the posterior wall of the stomach are removed. Traction is applied to the greater curvature of the stomach and section of the anterior leaf of the lesser omentum is begun in the vicinity of the angularis incisura and continued along the lesser curvature of the stomach until the proximal dissection is reached. Returning to the angularis incisura the posterior layer of the lesser omentum is similarly sectioned close to the stomach wall. As the esophagus is approached, traction is placed on the posterior vagus nerve and the dissection continued proximally. All branches to the terminal 4 cm of the esophagus, measured from the Angle of His, are sectioned and any nerve fiber on the anterior or posterior wall of the esophagus is cut. Particular effort is made to section any nerve fiber supplying the stomach that may possibly be lying to the left of the esophagus. In order to ensure section of all nerve fibers in the esophagus going to the stomach, Hedenstedt recommended circumferential section of the longitudinal esophageal muscle. The distal extent of dissection on the lesser curvature formerly depended on identification of the antral-fundal junction by the use of an intraluminal pH probe. Currently, the extent of denervation is dependent on an anatomical landmark which is that point where the last branch of the nerve of Lataret passes obliquely onto the lesser gastric curvature. This is approximately 6 cm from the pylorus. The lesser gastric curvature is reperitonealized by imbricating the anterior and posterior walls of the

Vol. 184 . No. 6

661 more extensively the antrum was denervated, the higher was the secretory response and the longer the serum gastrin concentration remained elevated following a meal. From these data, it would seem preferable to keep all of the antrum innervated when performing PCV. On the

PARIETAL CELL VAGOTOMY

stomach. This maneuver is performed to establish good hemostasis, to discourage vagal reinnervation'3 if this occurs and to protect against fistula formation that might result from necrosis due to inadvertent injury of the gastric wall or from possible devascularization. Finally, the phrenoesophageal ligament at the esophagogastric junction is sutured to the diaphragm at the esophageal hiatus. No gastric drainage procedure is required ifthe operator can approximate his thumb and forefinger through the pylorus. If there is a question regarding the size of the pylorus, we recommend that a drainage procedure be performed if the pylorus cannot accept a 38F (1.26 cm) Hurst-Maloney dilator passed from above by the anesthetist.

other hand, in man, the mean length ofthe lesser curvature left innervated was 7 cm by Goligher,29 9 cm by Amdrup5 and 6 cm by Jordan,64 yet the acid secretory responses in the three groups of patients were nearly the same and gastric emptying was not a problem in any of the groups. From these results, it appeared that the line between denervated and innervated gastric mucosa need not be drawn precisely at the junction of the antrum and fundus as in dog, but could vary as much as 3 cm without increasing the possibility of stasis or an unsatisfactory Technical Complications of PCV reduction in acid secretion. This conclusion was supThe safest operation for the treatment of duodenal ported by Jensen's48 demonstration in man that denervaulcer disease must be PCV. In a collected series of tion of the upper 2 to 5 cm of the antrum did not lead to 4,557 patients the mortality was 0.26%.59 In our ex- stasis. perience, splenic injury requiring splenectomy was the Is Preservation of Antral Innervation a Liability for most common technical complication and occurred in 8 of the Duodenal Ulcer Patient? 147 patients. We did not encounter perforation of the stomach, perforation of the esophagus or hemorrhage Based on experiments in dogs, vagal denervation of the from the neurovascular bundle which have been re- antrum has been considered an essential step in the operaported.66 Necrosis of the lesser curvature is the most tive treatment of duodenal ulcer because it was thought to serious complication following PCV that has been re- reduce gastrin release.86 It had been difficult to document ported. This complication was fatal in 4 of 5 patients in vagal release of gastrin from the innervated antrum bathed which it occurred.34'66'84 In Johnston's59 collected series of with acid9' but the vagal release of gastrin from an antrum 4,557 patients it was a fatal complication in 3 of 7 patients. out of continuity with the acid stream was easily demonThe pathogenesis of this complication was attributed to a strable.12 Subsequently, it was shown that acid secretion relative poverty of the submucosal blood supply to the in response to vagal stimulation (sham feeding) in dogs lesser curve. I submit, however, that this complication was dependent on vagal release of gastrin. 85 Quantities might result from inadvertent and unrecognized injury of exogenous gastrin too small to induce acid secretion caused by the need for application of clamps close to the were, in cooperation with vagal excitation resulting from gastric wall. Reperitonealization by imbrication of the sham feeding,89 capable of stimulating parietal cells to lesser curvature may prevent a catastrophy that might secrete optimally. Gastrin released from the innervated otherwise result from necrosis of the gastric wall. antrum was significantly greater after feeding than after Stasis after PCV may result from pyloric stenosis that sham feeding, but the acid secretory response was not existed at the time of operation or it may result from greater than that observed with sham feeding and diverstenosis due to scarring as ulcer healing occurs. Stasis sion of acid from the antrum.85 This was consistent requiring reoperation occurred in 1% of patients in one with other observations that gastrin potentiation of acid large study4 and in two of our own patients. The degree secretion stimulated by sham feeding was optimal at subof stenosis required to produce stasis after PCV may be maximal doses of gastrin.88 Although denervation of the inversely proportional to the degree of antral denervation. antrum reduced gastrin released in response to acetylThe margin of error that exists for localizing the choline2599 and glycine,25 the gastrin released by local boundary between innervated and denervated gastric stimulation of the antrum may be adequate to potentiate mucosa without causing excessive denervation of the acid secretion of vagally stimulated parietal cells whether antrum or inadequate denervation of the acid secreting the antrum is innervated or not.62 portion of the stomach has been considered. In dogs subIn man, vagal release of antral gastrin participated in jected to PCV, one-half of the antrum needed to be de- the acid response to vagal activation but only in producing nervated before gastric emptying was significantly de- an additive secretory effect.70 Any vagally released gastrin layed.10 On the other hand, denervation of the proximal did not potentiate the direct cholinergic activation of acid 2 cm of the antrum was sufficient to cause a significant secreting glands.69 The vagal phase of gastric acid secreincrease in the acid secretory response to feeding. The tion in duodenal ulcer patients was mainly caused by

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JORDAN

cholinergic activation of the parietal cells. Knutson and Olbe69 concluded that, in contrast to the results in dogs, vagal release of gastrin from the antrum and duodenal bulb participated only in a minor role in gastric acid secretion in duodenal ulcer patients. Thus the essentiality of antral denervation for the control of acid secretion in the treatment of duodenal ulcer in man based on data collected from dogs was challenged. The basal gastrin concentrations of most duodenal ulcer patients rose approximately the same after PCV and SV-D,47'52,96 and in other reports the serum gastrin levels rose after PCV but not to the same extent as after TV-D. 13'36'95 These data suggest that the gastrin elevation after PCV was not dependent on the presence of antral innervation. The higher mean serum gastrin level after TV-D than after SV-D, suggested to Stadil and Rehfeld95 that some action of the extragastric vagi suppressed gastrin release. Serum gastrin increased in response to food after TV and SV. The decreased acid secretion that resulted from these operations was therefore not related to a decrease in vagally released gastrin. Serum gastrin levels in response to a meal were essentially the same after SV-P and PCV47,52 and both were lower than after TV-P, further indicating that the gastrin elevation was not significantly related to the presence of antral innervation. 36,52,96

Vagal stimulation by insulin hypoglycemia may be an unrewarding method to study vagal release of gastrin in man since serum gastrin responses after insulin were only modestly affected by PCV, SV or TV. Stadil and Rehfeld95 and other investigators found that the release of gastrin by insulin hypoglycemia did not depend entirely on the vagus nerve, while Hanskey et al.35 reported that the response was dependent solely on intact vagal fibers. These conclusions are questionable because there is no criterion which is independent of insulin hypoglycemia for determining the completeness of vagotomy. The significance of the relation between gastrin production and acid secretion after insulin hypoglycemia was obscure. Serum gastrin and acid secretory responses to hypoglycemia were positively related before operation but after either PCV or SV-P the acid secretory response fell while the serum gastrin response remained unchanged.75 These results suggested that in the treatment of duodenal ulcer, vagal denervation of the parietal cells was more important than vagal denervation of the antrum. Acid and pepsin secretion in the basal state as well as that following stimulation by pentagastrin, histalog, insulin and meat extract were reduced equally effectively by PCV as by TV-P and SV-P.14,50,52,56,64,73,74 There was no evidence that the vagally innervated gastric antrum after PCV prevented adequate reduction of the acid secretory parameters. A more recent report by Greenall et al.31 showed that the MAO and BAO were inhibited 80 and 50o

Ann. Surg. o December 1976

respectively, 5 years after PCV and concluded that this represented the permanent reduction to be expected. Inhibition of the preoperative secretory response to insulin hypoglycemia was 88% 6 months after PCV and was the same two years after operations.64 Although the actual increase in acid secretion was small,57'64 the number of patients with a positive insulin test increased with time until approximately 50%o had a positive test at two years. The possible explanations for this finding included: Elevation of serum gastrin in response to epinephrine released by insulin hypoglycemia; regeneration of the vagal nerves supplying the fundic gland area of the stomach; or vagal release of gastrin. Similar responses

to insulin also occurred after TV-P63 and SV-P3 in the absence of antral innervation. The small difference in the gastrin response to insulin, whether the antrum was innervated or denervated, suggested that vagally released gastrin was of limited importance for the acid secretory response to insulin hypoglycemia after PCV.95 In summary, vagal stimulation of acid secretion in dogs is dependent on vagal release of antral gastrin. There is little evidence that innervation of the antrum plays such a dominant role in the vagal stimulation of acid secretion in man. From the available data, preservation of antral innervation after vagotomy of the acid secreting portion of the stomach does not constitute a liability from the standpoint of increasing serum gastrin or acid secretion in response to stimulation.

Do the Extragastric and Antral Vagal Nerves Exert a Protective Effect? Debas et al. 16 demonstrated that distension of a denervated antrum was associated with a decreased increment of serum gastrin but an increased acid response to any given increment of gastrin. It was postulated that the increased acid secretion resulted from the absence of an inhibitor factor normally released by distension of an innervated antrum. These studies supported the claim of Hart37 that preservation of antral branches of the vagi contributed to inhibition of acid secretion after PCV. In dogs, TV enhanced fasting gastrin levels and gastrin released in response to feeding.17'18 In man, TV also resulted in elevated fasting serum gastrin36'47'52 and gastrin in response to a protein meal47 while atropine enhanced the gastrin responses to insulin hypoglycemia when the gastric pH was held constant26 and to a protein meal.101 The interpretation of these findings suggested by Debas et al.18 was that the vagi of dogs, at least, contained inhibitory as well as stimulatory fibers for gastrin release. The increase in gastrin release following TV or by atropine might be due to the withdrawal of an inhibitory vagal influence on a local cholinergic mechanism that operated to release gastrin in response to food. The findings of

Vol. 184 . No. 6

PARIETAL CELL VAGOTOMY

gastrin enhancement by vagotomy contradicted early studies from the same laboratory showing that vagotomy in dogs had no effect on fasting gastrin concentration and lowered, rather than enhanced, the response to a meal. 101 The studies by Nilsson et al.85 demonstrating that atropine in dogs markedly inhibited the gastrin response to sham feeding also appeared to contradict the hypothesis that vagal pathways can inhibit gastrin release. Stadil and Rehfeld95'96 and others47'52 showed in man that the basal gastrin levels were not significantly different after PCV and SV. It could not be concluded, therefore, that the vagal branches of the antrum had a stimulatory or inhibitory effect on gastrin release. There were physiological experiments in dog45'97 and man27 suggesting that preservation of the innervated antrum protected against the development of ulcers. Nevertheless, it is easy to appreciate that the evidence as to whether the vagal nerve supply of the antrum exerts an inhibitory effect on gastrin release and what the significance of this effect might be contradictory at the present time. The importance of increased serum gastrin after vagotomy on acid secretion in patients who have had an adequate vagotomy on the fundic gland area is also unknown. Irrespective of the gastrin responses following vagotomy or atropinization, the importance of the antrum, and presumably of the gastrin released by the antrum after vagotomy, in the treatment of duodenal ulcer is suggested by the observation in man that antrectomy after TV or SV will significantly reduce acid secretion and will ensure the lowest recurrent ulcer rate. Before we can evaluate the merit of retained antral innervation we must determine the recurrent duodenal ulcer rate after PCV. If it equals that of TV and the recurrences can be handled effectively by antrectomy one would conclude that the antral vagal fibers have little protective effect. In addition to the mechanism just discussed, inhibition of acid secretion in dogs has been attributed to the extragastric vagi preserved by SV and PCV. Increased acid secretion from a Heidenhain pouch after TV was attributed by Dragstedt2' to gastric stasis leading to antral hyperfunction. Later, it was demonstrated that the increased acid secretion from a Heidenhain pouch in response to eating did not occur after total gastric vagotomy until the extragastric vagi were cut.98 After extragastric vagotomy, Walsh et al.'02 noted that the serum gastrin levels fell and the Heidenhain pouch secretion increased. They concluded that acid secretion from the Heidenhein pouch increased because the denervated parietal cells were more sensitive to gastrin after the removal of a non-competitive inhibitor of gastrin mediated by the extragastric vagi. Stadil and Rehfeld95 found in man that serum gastrin levels were higher after TV than after SV. This suggested to them that by some mechanism the extragastric vagal branches suppressed gastrin release. On the

663 other hand, it was the opinion of Korman et al.7' that the higher gastrin levels after truncal vagotomy in patients with duodenal ulcer might be due to the release of gastrin derived from extragastric sources. The evidence that the extragastric vagi exerted an important role on the reduction of acid secretion from denervated gastric mucosa in dogs was excellent. In man, however, such evidence was not available. The innervated antrum, well drained and in continuity with the acid secreting portion of the stomach, has not been shown to be a greater liability than a denervated antrum from the standpoint of increased acid secretion. On the contrary, under these circumstances the vagal nerve fibers to the antrum and the preserved extragastric vagi may exert a beneficial, modulating effect on gastrin release and acid secretion. Whether this is the case, requires further investigation. Preservation of Near Normal Gastric Emptying by the Innervated Antrum While it was uncertain whether preservation of antral innervation was an asset in terms of the control of acid secretion, its beneficial effects on motility of the antrum and pylorus were evident. Many gastric symptoms that occurred after operative procedures for duodenal ulcer resulted from abnormal gastric emptying due to by-pass, resection or destruction of the pyloro-antral pump. It was expected, therefore, that a pylorus preserving operation that did not produce antral stasis would contribute to improved clinical results. The motility of the pylorus and antrum are highly integrated to permit trituration of food, the rythmical discharge of small aliquots of properly prepared food into the duodenum,79 and, the prevention of reflux of duodenal contents into the stomach. Section of the vagus nerves, either TV or SV, interfered with gastric motility by totally disrupting the antral-duodenal relationship'00 and led to gastric stasis unless a drainage procedure was added. Then gastric emptying proceeded too rapidly producing the well known side effects of dumping and diarrhea. That the drainage procedure rather than the vagotomy was responsible for the majority of symptoms was demonstrated by the occurrence of symptoms after pyloroplasty alone.23 This was further suggested by Wastell et al.'04 who observed symptoms after PCV-P that were significantly greater than after PCV alone. Originally, Dragstedt19 did not perform a drainage procedure in combination with truncal vagotomy. Some of those patients developed stasis but those who did not were among his best results.22 Burge" also indicated that many patients emptied satisfactorily after SV without a drainage procedure. Nevertheless, the number of patients who developed stasis was sufficiently great that Clark and

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Alexander-Williams 15 recommend the practice be abandoned. The possibility that stasis might complicate PCV caused observers to carefully evaluate this aspect of the results. Holle et al.40 continued to perform a drainage procedure with PCV to avoid stasis; although most authors were of the opinion that the addition of a drainage procedure negated the major advantage that resulted from leaving the antrum innervated.'04 The observation by many investigators1' 107 has been that retardation of gastric emptying did not occur when antral innervation was preserved. In fact, gastric emptying was a little faster after PCV.2 It has been demonstrated that epigastric fullness76 and rapidity of gastric emptying after PCV53'54 were inversely related to the magnitude of gastric secretion following insulin stimulation. 82 Epigastric fullness and the shortened gastric emptying time were attributed to the loss of receptive relaxation and increased intragastric pressure which in turn were related to the completeness of vagotomy.72'94 It was also likely that the loss of receptive relaxation contributed to the frequent occurrence of early satiety postoperatively. In studies using a liquid meal of 10%o glucose in man'5 and a similar study in dogs33 the initial gastric emptying time after PCV was shortened compared with the time required preoperatively but the final emptying time was unaltered. The addition of pyloroplasty to either PCV or SV resulted in a more rapid, initial, gastric emptying time and a significant increase in the frequency of dumping. A study yielding similar results was reported by Madsen et al.80 The gastric emptying time of a solid meal in man after PCV was in the normal range and was not prolonged as occurred following TV-P.42 Wilbur and Kelly106 showed that PCV in dogs did not slow gastric emptying of solids and attributed this to the preservation of terminal antral contractions whereas they attributed the decreased gastric emptying time for liquids to increased intragastric pressure that follows vagal denervation of the proximal stomach. In summary, the objective evidence indicates that preservation of antral innervation after PCV was an asset in terms of gastric motility. Gastric stasis did not occur after PCV even though a drainage procedure was not performed. Gastric emptying of solids, regulated by the terminal contractions of the innervated antrum, remained normal although early gastric emptying of liquids was abnormally rapid because of increased gastric pressure that resulted from denervation of the proximal stomach and loss of receptive relaxation. Thus PCV without drainage constituted an operation which reduced the incidence of dumping by permitting more normal gastric emptying than occurred with any previous operative procedure for the treatment of duodenal ulcer.

Ann. Surg. * December 1976

Clinical Results of

Elective

of Diuodenal Ulcer

Holle and Hart39 first performed PCV in man and after an extensive experience with the procedure combined with pyloroplasty, they encountered a recurrence rate of 0.6% and excellent or good clinical result in 90%o of patients.40 This was evidence that an innervated antrum could be retained after proximal gastric vagotomy and pyloroplasty with a low incidence of recurrent ulcer. It was presumed that the results after PCV without pyloroplasty would be associated with an equally low recurrence rate, however, the evidence to support this hypothesis is not yet available. Since PCV without a drainage procedure was first performed2'5' 7 years ago, it has been used by an increasing number of surgeons, particularly in Europe and England. In the combined report on 271 patients operated on in Leeds and Copenhagen, 108 patients were followed 2 to 4 years. This was the largest group of patients followed for the longest period of time that was available for study.5 Although this study was not a randomized trial, the patients were thoroughly evaluated and provided valuable data. All patients were operated on electively for duodenal ulcer. There was no mortality. Two patients required reoperation for gastric stasis. Diarrhea occurred in 5% of patients but was never a serious problem. Dumping occurred in 6% of patients and could be provoked in 47% by oral administration of glucose. Dumping was not disabling in any patient. Other complaints including bilious vomiting and flatulence were encountered less frequently after PCV than after TV-D and SV-P performed by the same surgeons. Three patients were reoperated for suspected but unconfirmed duodenal ulcers. Two patients developed gastric ulcers but only one was reported. (Subsequent to this report, three patients from Copenhagen were operated for proven duodenal ulcers.49) Results from the two institutions were similar and were excellent or good in 88% of patients and failures in 5%. The failures were patients who developed stasis, recurrent or suspected recurrent ulcers. The recurrent ulcer rate in a prospective study begun in 1972 and involving three surgical departments in Copenhagen, including the department submitting the data in the Leeds-Copenhagen study, is currently 10go.49 PCV in Patients with Acid Hypersecretion

Johnston et al.60 studied the adequacy of PCV for patients who were hypersecretors of acid (Peak Acid Output greater than 50 mmol/hr) to determine if antrectomy was not desirable in these patients. Forty high

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PARIETAL CELL VAGOTOMY

665 and secretors 60 normal secretors were treated with PCV. Kronborg and Madsen76 study. In their opinion, the There were no differences between the two groups of pa- high recurrence rate after PCV was not related to the high tients with respect to the clinical results, the per cent proportion of positive insulin tests (58%) because this reduction of acid secretion or the number of patients with was not different from the 51% positive insulin tests positive insulin tests. There were no proven recurrent Amdrup et al.5 reported at the end of one year. Nevertheulcers and 4 of the 6 patients seriously suspected of hav- less, this did represent a significant difference because ing a recurrent ulcer were normal secretors. It was con- the number of patients with a positive insulin test is lowest cluded that patients who were hypersecretors fared as immediately postoperatively and increases with time after well with PCV as do normal secretors and that antrec- all types of vagotomy. Therefore, Kronborg and Madsen's tomy was unnecessary if the PCV was complete. results were in keeping with a positive correlation between insulin positivity soon after vagotomy and subsequent rate of recurrent ulceration.67 The differences in the Prospective Studies insulin tests and the recurrent ulcer rate obtained by There are currently numerous studies in progress in Kronborg and Madsen76 and Amdrup et al.5 suggested which the results of PCV are being compared in a prospec- that there was a basic difference in the operation pertive, randomized manner with different operations. formed by the two groups. Kronborg, in a subsequent Four such studies have been reported and confirmed the personal communication, stated that since changing from clinical results presented by Amdrup et al.5 the operative technique of Amdrup to that of Goligher his Kennedy and co-workers68 compared the results ob- recurrent ulcer rate fell to 8%. This experience emphatained with PCV and SV-GE performed on 50 patients in sized that the technical variations possible in the pereach group. There was no mortality and the average formance of PCV will make it more difficult to evaluate followup was two years. Four patients (8%) had mild the results obtained by different individuals who predumping after PCV while 14 patients had mild dumping sumably perform the same operation. Unless efforts are and 4 had severe dumping after SV-GE, for an incidence of made to avoid such discrepancies, the variability in the 37%. Two patients had mild diarrhea after PCV and 5 had results achieved is likely to lessen the credibility of a mild and one had severe diarrhea after SV-GE. Nausea potentially useful procedure. and bilious vomiting were more frequent after SV-GE than In a study by Wastell'03 the recurrent ulcer rate reported after PCV while heartburn and flatulence were the same initially was also less favorable than in a subsequent in both groups. The decreased incidence of dumping after report. 105 Thirty-six patients were assigned randomly and PCV was attributed to the elimination of a drainage prospectively to PCV with pyloroplasty and PCV without procedure. This was supported by the occurrence of pyloroplasty. During the first 3 to 12 months of the study, dumping in 7 of 24 patients who were treated prospec- two recurrent and one suspected recurrent ulcers octively by PCV-GE. There was one recurrent duodenal curred in the 16 patients without pyloroplasty. Later ulcer after PCV, and one jejunal ulcer and one suspected Wastell105 reported two recurrent ulcers in 48 patients duodenal ulcer after SV-GE. The results after PCV were with PCV and a drainage procedure and in two of 50 excellent or good in 48 of 50 patients, fair in one and patients with PCV without a drainage procedure. The poor (recurrent ulcer) in one. The results after SV-GE latter patients were the same patients reported earlier were excellent or good in 37 of 50 patients, fair in 9 and which suggested that the ulcers occurred during the poor in 3 patients. period that the operative technique was being perfected. In a prospective, randomized study, Kronborg and An important point to emerge from this study was that Madsen76 studied 50 patients who had PCV and 50 dumping occurred in 34% of patients after PCV with who had SV-P. There was no mortality. One year after drainage and in only 10% of patients with PCV alone. operation, the number of patients with dumping or This was good evidence that dumping resulted from the diarrhea was significantly less after PCV than after SV-P. drainage procedure rather than vagal denervation and There were 11 patients with recurrent ulcers after PCV was therefore contraindicated when antral innervation and 4 patients with recurrences after SV-P. The reduced was retained. number of gastric complaints after PCV attributed to In a randomized study by Jordan,64 45 patients with preservation of the pylorus counter-balanced the ad- PCV without drainage were compared with 47 patients verse effects of an ihcreased number of recurrent ulcers with SV-A. He confirmed other reports that dumping, so that the overall clinical rating after PCV and SV-P were diarrhea and other adverse effects associated with gastric similar. operations occurred infrequently after PCV and when Insulin tests performed 10 days after operation were they did occur they were easily controlled. In the impositive in 58% of patients in both groups of the mediate postoperative period gastric stasis was less evi-

Ann. Surg.

JORDAN

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o

December 1976

TABLE 1. Additional Studies of Parietal Cell Vagotomy for Treatment of Duodenal Ulcer

Author

Length of Followup (mon)

Bombeck et al.9 12

Operation

Number of Patients

Dumping

PCV TV-A SV-A

34

0 0 I

Clark et al.'4"5 *

PCV

sv Grassi et al.3"

Imperati et al.44

Per cent Acid Inhibition

Diarrhea

Recurrent Ulcer

BAO

MAO

Emptying

0 0 0

1 0 0

20 86 97

25 86 94

Unchanged Unchanged Rapid- I

3 0

{7

{10 e P ~10 ;P

4

{80

10 c Pt 10 s P

74

Increased

198

Unchanged

194

Increased

I

24

PCV

78

0

6

PCV

21 c Dt 62 s D

1 0

-

At 10 days 69 81

Liavag and Roland79

Unchanged Visick I & II 97%

80-85

1

0

Unchanged

Visick I 85%

Unchanged

Visic I & II 100%

': Rapid

Visick I & II 91%

At 2-3 mon 61 81

12-24

PCV

245

0

0

0 At 1-2 yr 71 56

Moberg and Hedenstedt83

PCV PCV-P

{63

5

0

3

At I yr§ 80

65

36

PCV

14

3

0

0

At3 yr§

50 Perez and Duthie9'

Clinical Results

6-30

TV-P PCV

81 44

5 5

33 7

6 2

50

50

Visick I & II 78% 77%

* Information unavailable. t P= Pyloroplasty.

t D= Drainage. § Percentages were estimated.

dent after PCV than after SV-A. Following SV-A all secretory parameters were inhibited in excess of 85% of the preoperative values for as long as two years. After PCV, the BAO and MAO rose steadily so that after two years they were approximately 50%o of the preoperative values. One patient in the study developed a recurrent ulcer one year after PCV. On withdrawal of alcohol his ulcer healed and remained healed. The overall results were good or excellent in 96% of patients receiving PCV and in 85% of those undergoing SV-A. Besides the randomized studies, there have been numerous other studies performed to evaluate PCV and some of the results are tabulated in Table I. This includes the study of Grassi et al.30 who described the use of an intragastric pH probe to test the completeness of vagotomy. It also includes studies by Moberg and Hedenstedt who contributed significantly to PCV by calling attention to the meticulous dissection required in

the area of the distal esophagus and cardia to obtain adequate gastric denervation. In summary, PCV without drainage for the elective treatment of duodenal ulcer was a safe procedure. All studies were in agreement that there were fewer gastric complaints following this procedure than after any other type of operative treatment. The diarrhea and dumping which did occur was mild and easily controlled. Most ulcers recurred within the first two years. The documentation by several authors of a recurrent ulcer rate of 2 to 8% in patients followed as long as two years suggested that PCV was an effective operation. Considerably more followup time is required before this highly rational operation for duodenal ulcer can be considered the successful procedure that the present evidence suggests. The operation is relatively easy to perform but it does require operative finesse and training which is best acquired in an operating room working with a surgeon who has demon-

Vol. 184 * No. 6

PARIETAL CELL VAGOTOMY

strated good results with PCV. This will spare those doing their initial cases the disappointment of an unnecessary high failure rate.

Metabolic Effects of PCV Edwards et al.24 demonstrated that fecal fat content was significantly greater after TV-P and SV-P than after PCV. The reason suggested for this was unregulated gastric emptying that followed total gastric vagotomy and a drainage procedure. The decreased steatorrhea associated with PCV may be indicative that absorption of other important organic and inorganic nutrients was improved also. This would exert a beneficial effect on a range of metabolic defects including malnutrition, anemia, and osteoporosis that are manifested years after conventional gastric surgery. Experience is unavailable that permits prediction as to whether prevention of these complications by the use of PCV will ultimately contribute to its adoption. Humphrey et al.43 demonstrated that the release of insulin following oral ingestion of glucose was significantly reduced after TV compared with SV or PCV. The insulin released in response to intravenously administered glucose was similar after each of the three types of vagotomy. It was shown also that the pancreatic enzyme response in man following duodenal perfusion with amino acids was reduced following TV whereas the response of the pancreas to exogenous hormones was unchanged.8' These studies supported the conclusion that TV-P led to a delayed or decreased release of endogenous intestinal hormones that exerted an effect on the exocrine and endocrine function of the pancreas. Documentation of this hypothesis would partially explain the good nutritional state in patients who have undergone PCV. The nutritional advantages that were expected of SV on the basis that innervated intra-abdominal organs functioned more normally than denervated ones eluded documentation. Therefore, in addition to retained innervation of intra-abdominal organs, the good nutritional state of patients after PCV must, in some measure, be due to the preservation of a functioning pylorus and antrum that permits the intermittent presentation of small aliquots of properly prepared food to the duodenum. The sensitivity of the exocrine bicarbonate secretory mechanism of the pancreas in patients with duodenal ulcer was considerably less than in non-ulcer patients. Berstad et al.8 demonstrated that the sensitivity of the pancreas to secrete bicarbonate in response to secretin was significantly increased in man after PCV. There was apparently a similar increase in sensitivity of the pancreas to the stimuli for enzyme secretion. This may be an adaptive phenomenon to maintain adequate pancreatic secretion in response to the reduced stimulus for secretin

667 release that followed reduction of acid secretion. Whether this benefit was restricted to PCV was not studied. Additional Applications of PCV Perforated duodenal ulcers are treated with increasing frequency by some type of definitive operative procedure if the patient is a good operative candidate. This approach is appealing since a majority of the patients eventually require a definitive procedure because of persistent pain or recurrent complications. However, the risk of untoward symptoms developing after conventional gastric operations in an individual who might not have required such an operation is a deterrent to their use at the time of perforation. The mild and infrequent sequelae associated with PCV and the protection provided by the operation suggested that this was an ideal procedure to perform at the time of simple closure of a perforated duodenal ulcer. The procedure was used without technical difficulties by several investigators55'65 with this as the indication. The results were gratifying and, in our opinion, the operation was an ideal compromise between simple closure of a perforation with an omental patch and the use of one of the current standard surgical procedures. Bleeding Ulcers: Johnston et al.55 treated 10 patients with bleeding ulcers, 5 gastric and 5 duodenal, by ligation of the bleeding ulcer followed by PCV. The bleeding ulcer was approached via a gastrotomy or duodenotomy in order to preserve the pylorus if possible. We use this approach to good advantage in young people in whom it is necessary to operate for acutely bleeding duodenal ulcers. Patients who require operation for bleeding are frequently older and are subject to a higher mortality rate. For this reason, we prefer TV-P and oversewing of the bleeding ulcer because it can be performed more quickly. As experience increases our attitude regarding bleeding as an indication for PCV may

change. Stenotic Duodenal Ulcers were treated with PCV in 15 patients by Johnston et al.55 Through a small gastrotomy it was possible to finger dilate the pylorus. In four of the 15 patients the scar tissue was ruptured causing perforation of the anterior pyloric wall which was then closed transversely. In one patient, transient postoperative gastric stasis occurred. The remaining patients did well and the possibility of re-stenosis of the pylorus did not materialize. We dilated an obstructed pylorus in two patients by having the anesthesiologist pass a 38 French (1.26 cm) tapered, mercury weighted bougie. The bougie was grasped through the wall of the stomach and guided into the pylorus. This procedure successfully dilated the pylorus in one patient and in the other it was necessary to close transversely a rent in the anterior pyloric wall. Gastric Ulcers have been treated by PCV with4' and

668

JORDAN

without an accompanying drainage procedure.6'23'38'5 Johnston et al.3'54 treated 20 patients with gastric ulcer alone and 10 patients with combined gastric and duodenal ulcers. Adequate, frozen, section biopsies of all gastric lesions were essential. In a later report58 38 patients were studied as long as 4.5 years after operation with a mean followup period of two years. No patient developed stasis or recurrent ulcer and the results were classified as excellent or good in 80%o of patients, with no failures. Hedenstedt38 used PCV with and without pyloroplasty in 32 gastric ulcer patients without complications. Gastric emptying was not prolonged by the operation and healing occurred in all cases. One might expect that the inflammatory involvement of the lesser curvature in response to the ulcer might make it technically difficult to preserve the nerves of Latarjet. Since the antrum of the stomach has been shown to extend cephalad from the pylorus to the proximal margin of the gastric ulcer87 a PCV beginning above the ulcer may suffice to denervate the entire acid-secreting portion of the stomach. In addition to reduction of acid secretion, PCV may promote healing of gastric ulcers by the prevention of reflux of duodenal contents without producing gastric stasis since both factors are possible contributors to this disease. We have utilized PCV in one patient with an ulcer very high on the lesser curvature. The ulcer was removed for biopsy and a PCV performed. In this patient PCV was preferable to a high subtotal gastric resection and may have been superior to TV-P which is advocated particularly in patients with an ulcer near the esophagogastric junction. The evaluation of PCV for the treatment of gastric ulcers is complicated by the variability in pathogenesis of gastric ulcers, the small number of patients who have been treated and the brief period that they have been observed. Fundoplication procedures for the treatment of gastroesophageal reflux and esophagitis were combined with PCV by Bahadorzadeh and Jordan.7 The exposure provided by PCV facilitated the accuracy and precision with which fundoplication and posterior gastropexy were performed. At the same time, reduction in acid secretion which may exert a beneficial effect, was achieved without risking the development of disabling symptoms of dumping or diarrhea which have contraindicated the use of TV with anti reflux operations. Conclusions Parietal Cell Vagotomy without drainage is associated with the lowest mortality of any operation currently being widely used for the elective treatment of duodenal ulcer. There are fewer gastrointestinal complaints of the type observed after more orthodox gastric operations. Diarrhea and dumping may occur after PCV in approxi-

Ann. Surg. * Dec:ember 1976

mately 5% of patients and when these complaints do they are milder and more easily controlled than

occur

after other types of operation. This improvement is attributed to retention of the peristaltic action of the antrum and an intact pyloric sphincter, which together, permit gastric emptying that is more normal than that which occurs with any other gastric procedure. There is insufficient evidence to indicate that retention of antral innervation exerts an inhibitory or a stimulatory effect on acid secretion which would be either beneficial or detrimental to the duodenal ulcer patient. In addition to using PCV for the elective treatment of duodenal ulcer it has been used in the treatment of gastric ulcers and duodenal ulcers complicated by obstruction, perforation and hemorrhage. The experience with PCV for the treatment of these conditions is so fragmentary compared with that already gained in its use for elective treatment of duodenal ulcer that predictions as to its ultimate efficacy for these conditions cannot be made at this time.

The acid secretory rates are reduced effectively by PCV and equal the reductions that follow TV-D. Acid secretory rates increase during the first postoperative year and then remain rather constant with time. This observation in addition to the reports by several observers that the rate of recurrent ulcers after 2 to 4 years followup is 2 to 4%, suggests that PCV is a highly effective procedure which may be equally good or better than truncal vagotomy and pyloroplasty in terms of recurrent ulcer and superior to all operations in terms of postoperative gastric sequelae. On the other hand, the recurrent ulcer rate of 22% reported by one group indicates that the operation is not equally effective in the hands of all surgeons. The discrepancy in the recurrence rates reported by different authors probably relates to the variation in the operative procedure as it is performed by different surgeons. The ultimate recurrence rate will remain unknown until the operation has been studied by more surgeons and sufficient time for observation and followup has elapsed. Continued long term evaluation of PCV by a widening circle of surgeons dedicated to clinical investigation is essential. It is important that this painfully slow but careful acquisition of data be performed even if the general application of the operation is delayed. The alternative is that the operation may be discredited because of poor results obtained by the infrequent user before its maximal potential for the treatment of duodenal ulcer is known. Selected References Griffith, C. A. and Harkins, H. N.: Partial Gastric Vagotomy: An Experimental Study. Gastroenterology, 32:96, 1957. These authors were cognizant of the undesirable side effects that accompanied vagotomy for the treatment of duodenal ulcer.

PARIETAL CELIL VAGOTOMY

Vol. 184 * No. 6

They proposed in this paper the concept of parietal cell vagotomy without drainage. The paper was submitted and turned down by every major surgical journal in America before being accepted by Gastroenterology. Now that the operation is becoming popular, it is important that surgeons do not become as myopic with regard to its acceptance as editors were with regard to its rejection. Amdrup, B. M. and Griffith, C. A.: Selective Vagotomy of the Parietal Cell Mass. Part I. With Preservation of the Innervated Antrum and Pylorus. Ann. Surg., 170:207, 1969. This paper and the one that followed in the same journal referred to experimental work on dogs performed to restudy the possibility that parietal cell vagotomy without a drainage procedure might be acceptable

treatment for duodenal ulcer. Acid secretion from Heidenhain pouches increased 47% following PCV suggesting that the operation would not be satisfactory for clinical use even though it was associated with normal gastric emptying. Further reevaluation and the re-interpretation of the data persuaded Amdrup that the procedure could reasonably be tried in man. Stenning, G. F. and Grossman, M. I.: Gastric Acid Response to Pentagastrin and Histamine after Extra-gastric Vagotomy in Dogs. Gastroenterology, 59:364, 1970. This paper is delightful for its simplicity and elegance. It clearly demonstrated in dogs that the extragastric vagi were responsible for inhibiting the acid secretory response of denervated gastric mucosa to endogenous and exogenous gastrin. Since a similar effect has not been observed in man this paper is an excellent example of a major difference in the acid secretory responses of dog and man. One must therefore view with caution the application to man of data obtained from another species. Wilbur, B. G. and Kelly, K. A.: Effect of Proximal Gastric, Complete Gastric and Truncal Vagotomy on Canine Gastric Electric Activity, Motility and Emptying. Ann. Surg., 178:295, 1973. One of the main concerns regarding the use of proximal gastric vagotomy was whether it would result in gastric stasis. The authors of this paper demonstrated in dogs that proximal gastric vagotomy disturbed gastric emptying less than did either of the other two types of vagotomy. It identified the importance of the innervation of the proximal stomach in regulating gastric emptying of liquids by controlling gastric transmural pressure and of the innervated antrum in regulating gastric emptying of solids by controlling the terminal antral contractions. In contrast to the comments on the paper above, these findings were applicable to man. Johnston, D., Pickford, I. R., Walker, B. E. and Goligher, J. C.: Highly Selective Vagotomy for Duodenal Ulcer: Do Hypersecretors Need Antrectomy? Br. Med. J., 1:716, 1975. These authors have contributed enormously to the literature concerning highly selective vagotomy and it is difficult to single out any one of their contributions. This one is of particular interest, however, because it has been speculated for some time that one might tailor the operation to the individual depending on the rate of acid secretion. This paper does not support this concept for the results after highly selective vagotomy were essentially the same for the high and low acid secretors. Stadil, F., Rehfeld, J. F., Christiansen, P. M. and Kronborg, O.: Gastrin Response to Food in Duodenal Ulcer Patients before and after Selective of Highly Selective Vagotomy. Br. J. Surg., 61:884, 1974. One of the main criticisms of highly selective vagotomy has been that retention of an innervated antrum would lead to excessive gastrin release. The results of this paper showed that the serum gastrin level following stimulation by food was no greater after highly selective vagotomy than after selective vagotomy. A good omen for highly selective vagotomy.

References 1.

B. M. and Griffith, C. A.: Selective Vagotomy of the Parietal Cell Mass. Part I. With Preservation of the Innervated Antrum and Pylorus. Ann. Surg., 170:207, 1969.

Amdrup,

669

2. Amdrup, E. and Jensen, H-E.: Selective Vagotomy of the Parietal Cell Mass Preserving Innervation of the Undrained Antrum. Gastroenterology, 59:522, 1970. 3. Amdrup, E., Kragelund, E., Humphrey, C. S., et al.: Evidence for Partial Vagal Reinnervation of the Stomach after Highly Selective Vagotomy without a Drainage Procedure (H.S.V.) for Duodenal Ulcer in Man. Gut, 12:866, 1971. 4. Amdrup, E.: Parietal Cell Vagotomy-Advantages and Possible Disadvantages. Bull. Soc. Internat. Chir., 33:396, 1974. 5. Amdrup, E., Jensen, H-E., Johnston, D., et al.: Clinical Results of Parietal Cell Vagotomy (Highly Selective Vagotomy) Two to Four Years after Operation. Ann. Surg., 180:279, 1974. 6. Amery, A. H., Cox, P. and Burge, H.: Vagotomy for Benign Lesser Curve Gastric Ulcer 1962-1972. Chir. Gastroenterol., 8:11, 1974. 7. Bahadorzadeh, K. and Jordan, P. H., Jr.: Evaluation of the Nissen Fundoplication for Treatment of Hiatal Hernia. Use of Parietal Cell Vagotomy without Drainage as an Adjunctive Procedure. Ann. Surg., 181:402, 1975. 8. Berstad, A., Roland, M., Petersen, H. and Liavag, I.: The Pancreatic Exocrine Secretion in Duodenal Ulcer Patients before and after Selective Proximal Vagotomy of the Stomach. Scand. J. Gastroenterol., 9:431, 1974. 9. Bombeck, C. T., Condon, R. E., Miller, B. and Nyhus, L. M.: Vagotomy: A Prospective, Randomized Study. Surg. Forum, 25:327, 1974. 10. Bone, J., Brandsborg, O., Brandsborg, M., et al.: Determination of the "Borderline of Stasis" in Parietal Cell Vagotomy. Preliminary Experimental Studies. (1). Bull. Soc. Internat. Chir., 33:405, 1974. 11. Burge, H., MacLean, C., Stedeford, R., et al.: Selective Vagotomy without Drainage. An Interim Report. Br. Med. J., 3:690, 1969. 12. Burstall, P. A. and Schofield, B.: Secretory Effects of Psychic Stimulation and Insulin Hypoglycemia on Heidenhain Gastric Pouches in Dogs. J. Physiol. (Lond.), 120:383, 1953. 13. Clark, C. G., Lewin, M. R., Stagg, B. H. and Wyllie, J. H.: Effect of Proximal Gastric Vagotomy on Gastric Acid Secretion and Plasma Gastrin. Gut, 14:293, 1973. 14. Clark, R. J., Allan, R. N. and Alexander-Williams, J.: The Effect of Retaining Antral Innervation on the Reductions of Gastric Acid and Pepsin Secretion after Vagotomy. Gut, 13:894, 1972. 15. Clarke, R. J. and Alexander-Williams, J.: The Effect of Preserving Antral Innervation and of a Pyloroplasty on Gastric Emptying after Vagotomy in Man. Gut, 14:300, 1973. 16. Debas, H. T., Konturek, S. J., Walsh, J. H. and Grossman, M. I.: Proof of a Pyloro-oxyntic reflex for Stimulation of Acid Secretion. Gastroenterology, 66:526, 1974. 17. Debas, H. T., Walsh, J. H. and Grossman, M. I.: Mechanisms of Release of Antral Gastrin. Symposium on Gastrointestinal Hormones, Galveston, Texas, J. C. Thompson, Editor. University of Texas Press, Austin, Texas, 1975; pp. 425. 18. Debas, H. T., Walsh, J. H. and Grossman, M. I.: After Vagotomy Atropine Suppresses Gastrin Release by Food. Gastroenterology, 70:1082, 1976. 19. Dragstedt, L. R. and Owens, F. M., Jr.: Supra-diaphragmatic Section of the Vagus Nerves in the Treatment of Duodenal Ulcer. Proc. Soc. Exp. Biol. Med., 53:152, 1943. 20. Dragstedt, L. R. and Schafer, P. W.: Removal of the Vagus Innervation of the Stomach in Gastroduodenal Ulcer. Surgery, 17:742, 1945. 21. Dragstedt, L. R., Oberhalman, H. A., Evans, S. 0. and Rigler, S. P.: Antrum Hyperfunction and Gastric Ulcer. Ann. Surg., 140: 396, 1954. 22. Dragstedt, L. R.: Discussion of Sawyers, J. L. and Scott, H. W., Jr.: Selective Gastric Vagotomy with Antrectomy or Pyloro plasty. Ann. Surg., 174:541, 1971. 23. Duthie, H. L.: Vagotomy for Peptic Ulcer. Rendic. Gastroenterol., 7:86, 1975. 24. Edwards, J. P., Lyndon, P. J., Smith, R. B. and Johnston, D.: Faecal Fat Excretin after Truncal, Selective and Highly Selective Vagotomy for Duodenal Ulcer. Gut, 15:521, 1974.

670 25.

26.

27.

JORDAN Emas, S., Vagne, M. and Grossman, M. I.: Heidenhain Pouch Response to Antral Stimulation before and after Antral Denervation in Dogs. Proc. Soc. Exp. Biol. Med., 132:1162, 1969. Farooq, 0. and Walsh, J. H.: Atropine Enhances Serum Gastrin Response to Insulin in Man. Gastroenterology, 68:662, 1975. Ferguson, D. J., Billings, H., Swenson, D. and Hoover, G.: Segmental Gastrectomy with Innervated Antrum for Duodenal Ulcer: Results at One to Five Years. Surgery, 47:548, 1960.

28.

Franksson, C.: Selective Abdominal Scand., 96:409, 1948.

29.

Goligher,

Technique

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61:337, 1974. 30. Grassi, G., Orecchia, C., Sbuelz, B. and Grassi, G. B., Jr.: Early Results of the Treatment of Duodenal Ulcer by Ultraselective

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Greenall,

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33.

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J. C. and

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Vagotomy on Basal and Maximal Acid Output in Man. Gastroenterology, 68:1421, 1975. Griffith, C. A. and Harkins, H. N.: Partial Gastric Vagotomy: An Experimental Study. Gastroenterology, 32:96, 1957. Hallenbeck, G. A. and Gleysteen, J.: Proximal Gastric Vagotomy without "Drainage," An Experimental Study. Ann. Surg., 179: Long

Highly

Term Effect of

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Halvorsen, J. F., Heimann, P., Localized

Solhaug, J.

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Jacobsen, K. B.: Curve of Stomach Br. Med. J., 2:590,

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Hansky, J., Soveny, in

Insulin-mediated

C. and Korman, M. G.: Role of the Vagus Gastrin Release. Gastroenterology, 63:

387, 1972. 36.

Hansky,

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Korman, M. G.:

Immunoassay

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Hart,

W.: Neue Erkenntnisse zur

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39.

40.

41.

42.

des

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und

Chirurgis-

Magenantrums. Langenbecks, Arch. Klin.

Chir., 322:703, 1968. Hedenstedt, S. and Moberg, S.: Gastric Ulcer Treated with Selective Proximal Vagotomy (SPV). Acta. Chir. Scand., 140:309, 1974. Holle, F. and Hart, W.: Neue Wege der Chirurgie des Gastroduodenalulkus. Med. Klin., 62:441, 1967. Holle, F., Bauer, H., Holle, G., et al.: Zur Theorie und Praxis der Selectiven Proximalen Vagotomie (SPV) und Pyloroplastik. Bull. Soc. Int. Chir., 31:90, 1972. Holle, G., Fellner, K. and Schauer, A.: On the Effect of Selective Proximal Vagotomy on the Parietal Cells in Gastric Ulcers. Chir.

Gastroenterol., 7:35, 1973. Howlett, P. J., Ward, A. S. and

Duthie, H. L.: Gastric Emptying Vagotomy. Proc. R. Soc. Med., 67:836, 1974. Humphrey, C. S., Dykes, J. R. W. and Johnston, D.: Effects after

43.

of

Truncal,

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and

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on Secretion in Patients with DuoUlcer. Br. Med. J., 2:112, 1975.

Glucose Tolerance and Insulin denal 44.

45.

Imperati, L., Natale, C. and Marinaccio, F.: Acid Fundic Selective Vagotomy of the Stomach without Drainage in the Treatment of Duodenal Ulcer: Technique and Results. Br. J. Surg., 59: 602, 1972. Interone, C. V., Del Finado, J. E.,

Miller, B., et al.: Parietal

Studies of Gastric Emptying and Observations of Protection from Histamine-Induced Ulcer. Arch. 102: Cell

Vagotomy:

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43, 1971. 46.

Jackson,

R.

G.:

Anatomic

Study

of the

Vagus Nerves: With

Technique of Transabdominal Selective Gastric Vagus Resection. Arch. Surg., 57:333, 1948. Jaffee, B. M., Clendinnen, B. G., Clarke, R. J. and AlexanderWilliams, J.: Effect of Selective and Proximal Gastric Vagotomy a

47.

on Serum Gastrin.

48.

Jensen,

H-E.:

Gastroenterol. 8: 49.

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Extended

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H-E.: Personal

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50. Jepson, K., Lari, J., Humphrey, C. S., et al.: A Comparison of the Effects of Truncal, Selective and Highly Selective Vagotomy on Maximal Acid Output in Response to Pentagastrin. Ann. Surg., 178:769, 1973. 51. Johnston, D. and Wilkinson, A. R.: Highly Selective Vagotomy without a Drainage Procedure in the Treatment of Duodenal Ulcer. Br. J. Surg., 57:289, 1970. 52. Johnston, D., Humphrey, C. S., Smith, R. B. and Wilkinson, A. R.: Should the Gastric Antrum be Vagally Denervated if it is Well Drained and in the Acid Stream? Br. J. Surg., 58:725, 1971. 53. Johnston, D., Humphrey, C. S., Smith, R. B. and Wilkinson, A. R.: Treatment of Gastric Ulcer by Highly Selective Vagotomy without a Drainage Procedure: An Interim Report. Br. J. Surg., 59:787, 1972. 54. Johnston, D., Lyndon, P. J. and Smith, R. B.: Treatment of Gastric Ulcer by Highly Selective Vagotomy without a Drainage Procedure. Gut, 14:825, 1973. 55. Johnston, D., Lyndon, P. J., Smith, R. B. and Humphrey, C. S.: Highly Selective Vagotomy without a Drainage Procedure in the Treatment of Haemorrhage, Perforation and Pyloric Stenosis Due to Peptic Ulcer. Br. J. Surg., 60:790, 1973. 56. Johnston, D., Wilkinson, A. R., Humphrey, C. S., et al.: Serial Studies of Gastric Secretion in Patients after Highly Selective (Parietal Cell) Vagotomy without a Drainage Procedure for Duodenal Ulcer. 1. Effect of Highly Selective Vagotomy on Basal and Pentagastrin-stimulated Maximal Acid Output. Gastroenterology, 64:1, 1973. 57. Johnston, D., Wilkinson, A. R., Humphrey, C. S., et al.: Serial Studies of Gastric Secretion in Patients after Highly Selective (Parietal Cell) Vagotomy without a Drainage Procedure for Duodenal Ulcer. II. The Insulin Test after Highly Selective Vagotomy. Gastroenterology, 64:12, 1973. 58. Johnston, D.: A New Look at Vagotomy. Surg. Ann., 6:125, 1974. 59. Johnston, D.: Operative Mortality and Postoperative Morbidity of Highly Selective Vagotomy. Br. J. Surg., 62:160, 1975. 60. Johnston, D., Pickford, I. R., Walker, B. E. and Goligher, J. C.: Highly Selective Vagotomy for Duodenal Ulcer: Do Hypersecreto'rs Need Antrectomy? Br. Med. J., 1:716, 1975. 61. Jordan, P. H., Jr. and De la Rosa, C.: Magnitude of the Antrum's Role in the Cephalic Phase of Gastric Secretion. Gastric Secretion Mechanisms and Control, Proceedings of Symposium, University of Alberta, Edmonton, Canada. Oxford and New York, Pergamon Press, 1967; pp. 119. 62. Jordan, P. H., Jr.: Relationship between Stimulating Mechanisms of Gastric Secretion in Dogs. JAMA, 199:399, 1967. 63. Jordan, P. H., Jr. and Condon, R. E.: A Prospective Evaluation of Vagotomy-Pyloroplasty and Vagotomy-Antrectomy for Treatment of Duodenal Ulcer. Ann. Surg., 172:547, 1970. 64. Jordan, P. H., Jr.: A Prospective Study of Parietal Cell Vagotomy and Selective Vagotomy-Antrectomy for Treatment of Duodenal Ulcer. Ann. Surg., 183:619, 1976. 65. Jordan, P. H., Jr. and Korompai, F. L.: Surgical Treatment of Perforated Duodenal Ulcer with Special Reference to Simple Closure Combined with Parietal Cell Vagotomy without Drainage. Surg., Gynecol. Obstet., 142:391, 1976. 66. Kalaja, E., Clemmesen, I., Banke, L., et al.: Accidents and Complications in Selective and Proximal Gastric Vagotomy. Surgery, 77:140, 1975. 67. Kennedy, F., MacKay, C., Bedi, B. S. and Kay, A. W.: Truncal Vagotomy and Drainage for Chronic Duodenal Ulcer Disease: A Controlled Trial. Br. Med. J., 2:71, 1973. 68. Kennedy, T., Johnston, G. W., Macrae, K. D. and Spencer, E. F. A.: Proximal Gastric Vagotomy: Interim Results of a Randomized Controlled Trial. Br. Med. J., 2:301, 1975. 69. Knutson, U. and Olbe, L.: Significance of Antrum in Gastric Acid Response to Sham Feeding in Duodenal Ulcer Patients. Fifth Scandinavian Conference on Gastroenterology, Aalborg, Denmark. Gastrointestinal Hormones and Other Subjects. Edited by Eigil H. Thaysen, Munksgaard, 1971; pp. 25. 70. Knutsson, U. and Olbe, L.: The Gastric Acid Response to Sham Feeding in Duodenal Ulcer Patients after Proximal Selective Vagotomy. Scand. J. Gastroenterol., 8: (Suppl. 20), 16, 1973.

Vol. 184 * No. 6

PARIETAL CELL VAGOTOMY

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