A new look at selective vagotomies

REVIEW

A New Look at Selective Vagotomies David Johnston, MD, Richard L. Blackett, MD, Leeds, United Kingdom

T his review is mainly about the elective surgical treatment of duodenal ulcer. Gastric ulceration is thought

to be too major and complicated a topic to deal with adequately, although highly selective vagotomy and exci- sion of the ulcer are being used in its treatment at several centers. At the risk of insulting our readers' intelligence, definitions of the three principal types of vagotomy are given in Table I, because the differences between them are still misunderstood, particularly the difference between selective and highly selective vagotomies.

Partial gastrectomy should no longer be used elective- ly for duodenal ulcer. It is too dangerous, may produce troublesome side effects such as dumping and bile reflux, has long-term sequelae such as loss of weight, bone disease and anemia, and increases the chance of eventual death from gastric cancer. Vagotomy is thus the main- stay of surgical treatment for duodenal ulcer in the 1980s [1]; however, should it be truncal (total), selective, or highly selective; combined with antrectomy or with a drainage procedure; or should the pylorus be kept intact? Is a single operative method suitable for all patients, or should the operation be tailored to the patient's individual requirements? If the latter is true, what criteria govern the choice of operation? Is selective vagotomy more likely than total vagotomy to be complicated by recurrent ulceration? What is the place of intraoperative and postoperative tests of completeness of vagotomy? Will gastric seromyotomy supersede section of the vagal trunks or branches outside the wall of the stomach?

The questions are endless and certainly cannot all be answered here, due to lack of space, and in some in- stances, lack of knowledge. The answers are based to some extent upon philosophic considerations, on our knowledge of abnormalities of gastrointestinal function after the various operative procedures, and on document- ed clinical results. In the end, however, after considering all the available evidence, a surgeon who operates on a patient with a duodenal ulcer has to make certain decisions, of which we believe the following are the most important: (1) Should the vagotomy be unselective in nature, that is, truncal or total abdominal vagotomy, or should it be selective? If selective, should it be bilateral selective (complete gastric vagotomy) or highly selective (proximal gastric or parietal cell vagotomy)? (2) Should the pylorus be preserved, destroyed, bypassed? In the remainder of this article, we shall attempt to answer these questions from philosophic, physiologic, and clinical viewpoints.

From the University Department of Surgery, The General Infirmary, Leeds, United Kingdom.

Requests for reprints should be addressed to David Johnston, MD, University Department of Surgery, The General Infirmary, Leeds LS 1 3EX, United Kingdom.

PHILOSOPHIC VIEWPOINT At the risk of derision in this age of superscience,

computers, and measurement, we venture to suggest that, whatever Helmholtz may have said, not all science is measurement, and the wealth of data generated by our machines may conceal poverty of thought: not a null hypothesis, but no hypothesis. The late Harold Burge [4], a pioneer of the selective principle in vagotomy, once informed a patient that he proposed to cure his duodenal ulcer by cutting the nerves to his stomach, but at the same time assured him that he would take great care to preserve the nerves to his liver, gallbladder, pancreas, and intestines, to which the patient replied indignantly, "I should hope so too, doctor!" Yet what was completely obvious to this patient was, at the time, disputed vigorous- ly by many learned professors of surgery, who said, in effect, "You haven't proved that cutting the hepatic and celiac branches of the vagus does the patient any harm, so we'll go on cutting them."

Both Burge and Charles A. Griffith [5], who argued that "cutting these nerves cannot do the patient any good, and could do harm, so we'll preserve them," temporarily lost the argument. Philosophic considerations, the p r i - m u m non nocere principle in medicine, even plain common sense, succumbed to mere data, to the results of experimental studies too imprecise to be capable of show- ing the abnormalities of function of the~gallbladder, pancreas, and intestines that follow trunc'al vagotomy. In fact, it took years for the appropriate tests to be performed, and in the meantime, thousands of patients continued to have their hepatic and celiac vagi needlessly severed. It is strange to think how structures that we sacrificed so thoughtlessly all those years turned out to have functions. Think of the spleen!

So, truly, "there are more things in heaven and earth, Horatio, than are dreamt of in [our] philosophy" [6]. Let us not forget this, as we contemplate the computer print- out, with its means and medians, standard deviations, confidence limits, and Mann-Whitney U values. We have no wish to deride data or the experimental method, but cogitation must come first, along with a continual aware- ness that what we see as we contemplate our data is not all there is.

PHYSIOLOGIC CONSIDERATIONS Functions of the antrum and pylorus: The stomach

is both the hopper and the mill of the alimentary tract. Its principal function is to receive food by receptive relaxa- tion and accommodation to distension in the fundus and body, mix and grind it in the antral mill, and then pass it onwards in a graduated fashion through the pylorus into the small intestine. Milling and grinding in the antrum are affected not merely by propulsive waves of peristalsis,

416 THE AMERICAN JOURNAL OFSURGERY VOLUME 156 NOVEMBER 1988

but also by retropulsion, whereby particulate matter is driven forcibly back into the body of the stomach by terminal antral contraction [7]. These activities of the antrum, pylorus, and duodenum are coordinated by nerves and hormones [8]. Gastric emptying is thus order- ly and controlled, and excessive reflux of potentially harmful duodenal contents (malevolent gall) is prevent- ed. An intact antropyloroduodenal segment is thus necessary for optimal health. Its loss through antrectomy, de- struction by pyloroplasty, or bypass by gastrojejunostomy can lead to unrelated gastric emptying, dumping, diarrhea, bilious vomiting, gastritis, and perhaps, in the long- term, gastric carcinoma.

To return to our two questions, it is obvious that they are interlinked. Vagotomy of the entire stomach, whether truncal or bilateral selective, permanently alters the myoelectrical activity of the antrum so that peristalsis is weakened, and the visa tergo applied to the food may be insufficient to drive it efficiently through the narrow pyloric orifice [9-12]. Hence the performance of truncal or bilateral selective vagotomy creates the need for pyloroplasty, gastrojejunostomy, or antrectomy. Highly selective vagotomy, in contrast, by preserving the nerves of Latarjet, keeps the antral mill grinding normally so that the pylorus can be kept intact [13,14].

Gastrin and the vagus: It was believed formerly that cutting the vagal nerve supply to the gastric antrum, as in truncal or bilateral selective vagotomy, reduced circulating levels of gastrin. It was partly for this reason that surgeons believed that vagotomy of the stomach should be total truncal or bilateral selective vagotomy; they were taught that direct vagal stimulation of the parietal cell mass was thus removed, and vagal release of gastrin abol- ished. Now surgeons are able to measure circulating levels of gastrin by radioimmunoassay and know that vagal release of gastrin is relatively unimportant in man. Vagal stimulation by sham feeding, for example, evoked no acid secretion after highly selective vagotomy in patients, and sham feeding of healthy volunteers elicited a gastric acid response but no increase in the serum gastrin level [17,18]. Atropine increases the gastrin response to feeding in human subjects, which points to cholinergic inhibi- tion of gastrin release [19]. In dogs, increasing degrees of vagotomy, first of the parietal cell mass (highly selective vagotomy), then of the antrum (bilateral selective vagotomy), and finally of the vagal trunks (truncal vagotomy), led to stepwise increases in serum gastrin and acid output [20,21]. In human subjects, gastrin levels are no higher when the gastric antrum is left innervated, as in highly selective vagotomy, than when it is vagally denervated, as in truncal vagotomy [22]. That is the key to modern surgery for peptic ulcer, since when the antrum is left innervated, the stomach empties satisfactorily through an intact pylorus. Hence antrectomy, pyloroplasty, and gas- troenterostomy are all unnecessary, and their side effects are preventable.

Motility of the gastric antrum and vagotomy: Both truncal and bilateral selective vagotomy impair gastric myoelectrical activity, motility, and emptying [9-12]. It is well known that many of Dragstedt's [66] early pa-

TABLE I The Three Types of Vagotomy

Type Description

Truncal vagotomy

Selective vagotomy

Highly selective vagotomy*

Severs the anterior and posterior vagal trunks and all vagal branches below the diaphragm. Denervatas the entire stomach, liver, gallbladder, pancreas, small intestine, and proximal large intestine. Propulsive power of the gastric antral mill is permanently impaired. To prevent stasis, stomach must be drained by means of P, GJ, or A. Loss of antropy- Ioric function leads to unregulated gastric emptying and excessive reflux of bile into the stomach.

Vagally denervates the entire stomach. Same need for gastric drainage by P, GJ, or A and same loss of antropyloric function as in truncal vagotomy. Pre- serves the hepatic branches of anterior vagal trunk to liver and gallbladder, and celiac branch of posterior vagal trunk to pancreas and intestines.

Denervates acid-secreting proximal three- quarters of stomach and the parietal cell mass. Preserves the vagal nerves of Latarjet to the antrum and leaves the alkaline antrum and pylorus innervated and intact. Little change in gastric emptying pattern or in duodenogastric reflux. Hepatic and celiac vagal branches preserved as in selective vagotomy.

* Parietal cell or proximal gastric vagotomy. A = antrectomy; GJ = gastrojejunostomy; P = pyloroplasty.

tients, who underwent truncal vagotomy alone, suffered from foul eructations and vomiting due to gastric stasis. Since then, sporadic attempts have been made to return to the use of total gastric vagotomy without a drainage procedure, but all have foundered on the inherent problem that after truncal or bilateral selective vagotomy without drainage, the propulsive and retropulsive powers of the antral musculature are enfeebled and prove insufficient to expel solid food from the stomach, even when the duodenal ulcer has not produced any pyloroduodenal stenosis.

Although there is much loose talk about the stomach recovering its tone in the long-term after complete gastric vagotomy, and although there is admittedly some im- provement in gastric emptying as time passes, compared with early postoperative stasis, it must be emphasized that both truncal vagotomy and bilateral selective vagotomy impair gastric motility permanently [9,10]. There- fore, closure of gastrojejunostomy stomas and reversal of pyloroplasties in an attempt to remedy side effects after vagotomy with a drainage procedure is a hit-or-miss af- fair, which produces delayed gastric emptying of solids in many patients and yields disappointing results in about 50 percent of cases. If normal antral motility is to be maintained and gastric emptying assured, it is essential that the motor nerve supply to the antral mill via the nerves of Latarjet be preserved by the use of highly selective vagotomy.

THE AMERICAN JOURNAL OF SURGERY VOLUME 156 NOVEMBER 1988 417

JOHNSTON AND BLACKETT

The extragastr ic vagal branches: The hepatic branches of the anterior vagal trunk are visible in the upper part of the lesser omentum. They are preserved in the course of bilateral selective vagotomy and highly selective vagotomy but severed by truncal vagotomy. Their loss leads to dilatation of the gallbladder, which can be demonstrated several years after truncal vagotomy [23,24]. This in turn leads to an increased risk of gallstone formation, which is probably due more to stasis than to altered composition of the bile [25-27]. It is ironic that truncal vagotomy with pyloroplasty, gastrojejunostomy, or antrectomy leads to rapid gastric emptying, rapid intestinal transit, and in susceptible patients, to diarrhea. Diarrhea is characteristically episodic and fair- ly mild in about 15 percent of patients, troublesome in 8 percent, and catastrophic, due to urgency and sometimes incontinence, in 1 to 3 percent of patients. Truncal vagotomy also predisposes to gallstone formation, and when cholecystectomy is added to truncal vagotomy with a drainage procedure, the chances that the patient will suf- fer from severe diarrhea are greatly increased to about a 1 in 3 or 1 in 4 chance [28,29]. Thus, from the patient's point of view, truncal vagotomy needlessly increases the chance of gallstones and leads to a small, but unnecessary, risk that quality of life will be seriously impaired by the development of diarrhea.

The celiac branch of the posterior vagal trunk supplies the pancreas, the small intestine, and the large intestine as far distally as the mid transverse colon. For many years after Dragstedt's reintroduction of truncal vagotomy in 1943, it was believed that the procedure had no significant effect on pancreatic function in man; secretin and pancreozymin (cholecystokinin) were thought to be the principal stimuli to pancreatic exocrine secretion, the vagal component being considered unimportant. In recent years, however, there has been increasing recognition that the vagus plays a major role in stimulation of pancreatic secretion. Not only is there a cephalic phase of pancreatic secretion, which is vagally mediated, but it has been reported by Solomon and Grossman [30] that the vagus in dogs plays a large part in the intestinal phase of pancreatic secretion. Malagelada et al [31] found that enzyme output by the human pancreas in response to duodenal perfusion with amino acids was greatly diminished after truncal vagotomy, and MacGregor et al [32] and Smith et al [33] showed that the pancreatic enzyme response to a meal also decreased by about 50 percent after truncal vagotomy, whereas after highly selective vagotomy it was unaltered [34]. Endocrine function of the pancreas is also altered by truncal vagotomy, but not by highly selective vagotomy, perhaps through disturbance of the enteroin- sulin axis [35].

Fecal fat excretion increases significantly after truncal vagotomy with a drainage procedure, but not after highly selective vagotomy [36]. The increase is probably due to several causes: impaired function of the antral mill after truncal vagotomy; loss of pyloric control of gastric emptying; damage to the normal integration of the functions of the stomach, biliary system, and pancreas; dimin-

ished pancreatic secretion; rapid intestinal transit; and perhaps impaired small bowel function.

In summary, every nerve fiber has a function: if the fiber is severed, the function is lost. Although it is clear that in most patients, severance of the extragastric vagal fibers in the course of truncal vagotomy does not produce any major physiologic upset or serious impairment of health, some patients are more seriously damaged, to the extent that clinical symptoms develop and their quality of life suffers. The absence of symptoms in most patients after extragastric vagotomy can be attributed more to the reserve capacity of the pancreas and other viscera than to the intrinsic merits of the operative procedure. Since severance of the hepatic and celiac vagal branches impairs physiologic function in all patients and leads to clinical symptoms in some, and since such vagotomy of the extragastric viscera is unnecessary and done only for technical convenience, it seems sensible, not to say ethical or legally desirable, to preserve these vagal fibers by selective or highly selective vagotomy.

To this suggestion, the proponents of truncal vagotomy might respond that the greater technical convenience of truncal vagotomy compared with bilateral selective vagotomy or highly selective vagotomy has clinical advantages for the patient: a lower operative mortality rate, fewer incomplete vagotomies, and hence a lower incidence of recurrent ulceration. Such arguments will be addressed in the next section, where it will be seen that they are without foundation.

CLINICAL COMPARISONS Clinicians have always been suspicious, and rightly so

in our view, of attempts to base decisions affecting patients on philosophic considerations or on the evidence afforded by physiologic studies. Too often this "scientific foundation" of surgery has been built on sand: the animal model perhaps irrelevant to man, the doses of drugs phar- macologic rather than physiologic, the method used a bludgeon rather than a rapier thrust to the heart of the matter, the light of inquiry focused on peripheral matters while the central issue remained obscure.

In the end, therefore, the answers to our questions must depend on clinical evidence. Which of the various options is best, overall, for the patient? But what do we mean by best? Best for curing all ulcers would be total gastrectomy or, less absurdly, vagotomy combined with antrectomy; best with respect to absence of side effects would be sham laparotomy or, more realistically, highly selective vagotomy. In short, we can only decide which procedure is best by deciding first what yardsticks to employ, the clinical factors that we regard as important, and what relative value we wish to assign to each of them [37]. The typical surgical paper on peptic ulcer, which expresses the outcome in terms of operative mortality, incidences of recurrent ulceration, and side effects, does not take into consideration several other important factors, and the weight or relative importance of each may not even be discussed. In Table II, we list the factors that we consider to be important. We have suggested previous-


SELECTIVE VAGOTOMIES

ly the relative weight that should be assigned to each, although we realize that every surgeon will have his or her own personal scoring system [37].

Operative mortality: The mean operative mortality in elective cases of highly selective vagotomy is 0.3 percent, of truncal vagotomy with a drainage procedure or bilateral selective vagotomy with a drainage procedure, 0.6 percent, and of vagotomy and antrectomy, 1 percent [2,3,38]. Although very experienced surgeons can, by a combination of good luck and good judgment, perform hundreds of gastric resections (partial gastrectomy or vagotomy and antrectomy) without mortality, review of a vast literature leaves one in little doubt that a patient is twice as likely to die after vagotomy with a drainage procedure as after highly selective vagotomy, and three or four times as likely to die after partial gastrectomy or vagotomy and antrectomy as after highly selective vagotomy. Despite the occasional occurrence of lesser curve necrosis after highly selective vagotomy (approximately 1:500 patients), highly selective vagotomy is still the saf- est procedure, because of the absence of any breach in the continuity of the gastrointestinal tract, of a suture line that might leak or bleed, and of any stoma or blind loop [38].

Postoperative complications are also least after highly selective vagotomy, so much so that patients can be nursed without either a nasogastric tube or an intrave- nous drip, which makes them more comfortable, mobile, and confident and makes it easier to clear the chest.

Bilateral seleetive vagotomy eompared with truneal vagotomy: Both truncal vagotomy and bilateral selective vagotomy are complete gastric vagotomies, and must therefore be complemented either by a drainage procedure (pyloroplasty or gastrojejunostomy) or by antrectomy. The advocates of bilateral selective vagotomy claimed that it was superior to truncal vagotomy in two respects: first, it permitted performance of a more reliable and complete vagotomy, thus lowering the incidence of recurrent ulcer; second, preservation of the hepatic and celiac vagi would lead to fewer side effects, and diarrhea in particular would be less of a problem than after truncal vagotomy [5]. The first of these claims is now known to be incorrect, but the second one is true. There is no good evidence that the incidence of recurrent ulcer is significantly lower after bilateral selective vagotomy than after truncal vagotomy. Admittedly, the pioneers of bilateral selective vagotomy such as Griffith [5] and Sawyers et al [39] in the United States and Burge [4], Grassi [51], Amdrup [14], and other investigators in Europe, were able to point to lo,w incidence both of incomplete vagotomy and of recurrent ulcer after this procedure. However, the apparent superiority of bilateral selective vagotomy compared with truncal vagotomy in some prospective trials was, in retrospect, almost certainly a phenomenon related to the skill of the individual surgeons concerned rather than a reflection of any true or systematic superiority of bilateral selective vagotomy over truncal vagotomy. The evidence now available strongly supports the view that completeness of vagotomy is surgeon-related,

TABLE II Factors In Choosing an Elect ive Operat ion for

Duodenal Ulcer

1. Operative mortality and postoperative morbidity 2. incidence of recurrent ulceration after 5-10 years 3. Side effects of operation (dumping, diarrhea, etc.) 4. Long-term metabolic consequences after 5-30 years

a. Loss of weight b. Anemia

Iron deficiency Megaloblasts

c. Tuberculosis d. Bone disease

Osteomalacia Osteoporosis

5. incidence of gastric carcinoma after 15-30 years 6. Relative ease or difficulty of second salvage operation if the first

operation fails 7. Surgeon performing the operation

rather than related to the particular type of vagotomy employed. Thus, while Kennedy et al [40,41], Sawyers et al [39], and Griffith [5] could quote incidences of incomplete vagotomy of only 2 to 4 percent after bilateral selective vagotomy, and therefore, not surprisingly, very low incidences of recurrent ulcer, Kronborg et al [42] reported an incidence of incomplete vagotomy of 41 percent after bilateral selective vagotomy by Hollander-positive insulin tests soon after operation [52]. Similarly, in a study of 676 patients after truncal vagotomy or bilateral selective vagotomy, we found no significant difference between the incidence of incomplete vagotomy after truncal vagotomy (16 percent) and bilateral selective vagotomy (14 percent). The subsequent incidence of recurrent ulcer was also similar, being approximately 10 percent after both types of vagotomy [2,43]. De Miguel [42], too, found incidences of recurrent ulcer of approximately 10 percent after truncal vagotomy, bilateral selective vagotomy, and highly selective vagotomy, after a minimum follow-up of 5 years. At our institution, we found that some surgeons were more adept at performing truncal vagotomy than bilateral selective vagotomy, and in some the reverse was true: some surgeons had no positive Hol- lander test results 1 week after truncal vagotomy, others had positive results in 50 percent; some had no positive results after bilateral selective vagotomy, others had positive results in 30 percent [43]. We find the same degree of variation in surgeons after highly selective vagotomy. The fault lies not in the vagotomy, but in ourselves: neither selective nor highly selective vagotomy is intrinsically or systematically superior to truncal vagotomy, with respect to completeness of parietal cell denervation.

Does bilateral selective vagotomy then possess other advantages compared with truncal vagotomy, such as a lower incidence of side effects? Studies by Burge and Vane [4], Sawyers et al [39], and Griffith [5], and in particular that by Kennedy et al [40,41], have shown that the incidence of postvagotomy diarrhea is significantly less after bilateral selective vagotomy with a drainage procedure than after truncal vagotomy with a drainage



TABLE Ili Comparison of Highly Selective Vagotomy With

Vagotomy and Antrectomy*

Highly Selective Vagotomy & Vagotomy Antrectomy

Operative mortality 0.3 (0-1) 1 (0-2) Postoperative Less: minimal More: gastric stasis,

morbidity anastomotic leakage

Recurrent ulceration 10 (2-30) 2 (0-4) after 5-10 years

Side effects

Long-term sequelae

Carcinoma of stomach

Options available if first operation fails

Minimal: little problem More troublesome: with dumping, responsible for fair diarrhea or bilious to poor outcome in vomiting 10-30

No weight loss, no Significant weight anemia loss, some anemia

Insufficient foUow-up Increased risk

Many Few

* All values expressed as percentages.

procedure. However, since pyloric function is lost after bilateral selective vagotomy with a drainage procedure just as after truncal vagotomy with a drainage procedure, incidences of dumping and of symptoms associated with duodenogastric reflux are as great after bilateral selective vagotomy as after truncal vagotomy. The clinical advantage of bilateral selective vagotomy with a drainage procedure over truncal vagotomy with a drainage procedure is slight.

Since highly selective vagotomy possesses the major advantage over bilateral selective vagotomy of preserving the antral mill and pylorus, most surgeons who were interested in the selective principle in vagotomy have now abandoned bilateral selective vagotomy with a drainage procedure in favor of highly selective vagotomy. Highly selective vagotomy has been found by most investigators to be as effective as bilateral selective vagotomy with a drainage procedure in curing duodenal ulcers [16], an exception being the trial by Kronborg and Madsen [45], in which the incidences of recurrent ulcer were 28 percent after highly selective vagotomy and 18 percent after bilateral selective vagotomy and pyloroplasty after 6 to 9 years of follow-up. However, the incidence of incomplete vagotomy was very high in that trial, 58 percent of the highly selective vagotomy patients having positive Hol- lander test results 1 week after operation.

Highly selective vagotomy compared with truneal vagotomy with drainage: Two prospective trials of highly selective vagotomy versus truncal vagotomy and pyloroplasty reported in favor of highly selective vagotomy, because incidences of recurrent ulcer were similar, whereas side effects such as dumping, diarrhea, and vomiting were less frequent and less severe after highly selective vagotomy than after truncal vagotomy and pyloroplasty [46,47]. The results of two other such trials in Britain and of a nonrandom comparative study in London were less decisive. In these studies, incidences of recurrent ulcer after highly selective vagotomy were higher (range

13 to 25 percent) than in other trials involving highly selective vagotomy, and although side effects were again found to be less common after highly selective vagotomy than after truncal vagotomy and pyloroplasty, the overall results obtained in the two groups of patients did not differ significantly [47-49].

When all the evidence is considered, the clinical results after highly selective vagotomy seem to be better than those after truncal vagotomy with a drainage procedure. Moreover, these trials could assign little weight to four important factors in peptic ulcer surgery, namely operative mortality, long-term sequelae, risk of gastric carcinoma, and the options open to the surgeon if the first operation fails. Since highly selective vagotomy is probably superior to truncal vagotomy with a drainage procedure with regard to each of these factors, the overall results of the trials are more favorable to highly selective vagotomy than their conclusions might suggest.

No form of quality control, such as a Burge vagometer test, Grassi test, insulin test, or sham feeding test, was used in any of these trials [4,51-54]. Therefore, when the operation was deemed to have failed because of recurrent ulceration, it was impossible to tell whether such failure was due to incomplete vagotomy or to the use of vagotomy without antrectomy.

Finally, it is of great interest that Fraser et al [47] found only 1 case of recurrent ulcer among 69 patients who were followed for a mean of 5 years after highly selective vagotomy (recurrence rate 1.4 percent). After 12 years' follow-up of the same patients, the incidence of recurrence only increased to 5 percent, and the three patients concerned were successfully treated medically [Koruth NM, Matheson NA, et al: in press, 1989]. Since the patients who entered the trial of highly selective vagotomy versus truncal vagotomy and pyloroplasty were consecutive and must presumably have included the usual proportions of patients with hypersecretion and normal secretion, and of patients with G-cell hyperplasia and antral dominance, if any, it follows that a high incidence of recurrent ulcer is not inevitable after highly selective vagotomy, and that highly selective vagotomy can be used in a consecutive series of duodenal ulcer patients, including patients with hypersecretion of acid and those with antral dominance, with excellent results. Jordan's [60,61] brilliant work in Houston led to the same conclusions and Herrington et al [56], former staunch advocates of vagotomy combined with antrectomy, also reported satisfactory results 6 to 13 years after highly selective vagotomy.

Highly selective vagotomy compared with vagotomy and antrectomy: A comparison of highly selective vagotomy with vagotomy and antrectomy is of great interest and importance. Vagotomy and antrectomy is widely acknowledged to be the most effective procedure available for curing ulcers, since both the vagal and the gastrin drive on the parietal cells is removed and the long- term incidence of recurrent ulceration is only 1 to 2 percent [55]. Highly selective vagotomy, in contrast, is much more "physiological," but has a higher recurrence rate, which ranges from 2 percent to over 30 percent. The



question is whether the advantages of highly selective vagotomy are outweighed by the lower incidence of recurrent ulceration after vagotomy and antrectomy.

The answer can be found in the results reported after many thousands of highly selective vagotomy and vagotomy and antrectomy procedures in uncontrolled studies (Table III) and several controlled trials [55-65]. The results of six prospective trials comparing the two procedures have been published, and we have analyzed them in detail elsewhere [64]. The mean incidences of recurrent ulcer were 1 percent after vagotomy and antrectomy and 10 percent after highly selective vagotomy, but operative mortality was slightly higher after vagotomy and antrectomy than after highly selective vagotomy; postoperative complications were more common after vagotomy and antrectomy; and side effects such as dumping, diarrhea, and bilious vomiting were also more frequent after vagotomy and antrectomy [57-64]. The overall clinical results favored highly selective vagotomy in four trials and were roughly equal in two trials.

The operative mortality rate ofvagotomy and antrectomy is approximately three times that of highly selective vagotomy, and its side effects and long-term sequelae are much worse. Nevertheless, the final clinical status of patients after vagotomy and antrectomy might approach or equal the status of patients who have undergone highly selective vagotomy if recurrent ulceration after highly selective vagotomy, the potential Achilles heel of the procedure, were to be attended by significant spontaneous mortality or by a cumulative mortality due to ulcer complications and reoperations. Such fears are groundless, however, for it has been reported by many investigators that recurrent ulcer after highly selective vagotomy usually runs a benign course, with a low risk of dangerous complications, such as hemorrhage or perforation, and a low rate of reoperation. At our institution, we studied 56 patients with recurrent ulcer after highly selective vagotomy and found that only one presented with perforation, eight presented with hemorrhage, and the remainder complained of pain or discomfort. There were no deaths from the ulcer complications or after the 12 reoperations. Most patients were treated successfully by medical mea- sures, including administration of cimetidine or ranitidine. Thus, we conclude that a greater proportion of patients who undergo highly selective vagotomy than who undergo vagotomy and antrectomy have good quality of life.

For these reasons, we believe that highly selective vagotomy is the operation of choice for most patients who require surgical treatment for duodenal ulcer. The addi- tion of antrectomy to vagotomy is merely an insurance policy against incomplete vagotomy, but the premium that has to be paid is too high in terms both of operative risk and of side effects. As Dragstedt [66] said, it does not seem wise to subject all patients to more surgery than they need merely to prevent recurrent ulcer in a few. Patients with recurrent ulcer are still living, and thus can receive further treatment.

Hypersecretion of acid: Most patients with duodenal ulcer have acid outputs within the normal range, but

TABLE IV Peak Acid Output Before and Recurrent Ulcer After

Highly Selective Vagotomy in 322 Patients*

PAO Pg Patients Recurrent Ulceration (rnrnol/h) (n) n %

< 30 39 1 2.6 30-40 79 6 7.6 40-50 82 10 12.2 50-60 67 8 11.9 > 60 55 3 5.5

Total 322 28 8.7

* Mean duration of follow,up, 6 years. PAO = peak acid output; Pg = pentagastrin.

about 30 percent of them have acid hypersecretion. Hence, if we were to tailor the extent of operation to the acid output, we would have to perform vagotomy and antrectomy in 30 to 40 percent of patients and vagotomy alone in the remainder. However, although there is some evidence that recurrence rates are higher in patients with hypersecretion than in those with normal secretion, when truncal vagotomy or bilateral selective vagotomy has been employed [67-70], that is not the case with highly selective vagotomy [15,69-71]. In our own highly selective vagotomy series, the preoperative basal acid output was 7.2 4- 0.7 mmol/hour (mean 4- SEM) in 28 patients who developed recurrent ulcer, and 7.6 4- 0.6 mmol/hour in 100 patients without recurrent ulcer after highly selective vagotomy. The influence of preoperative peak acid output on the chances of recurrent ulcer developing in the patient after highly selective vagotomy is shown in Table IV. The mean incidence of recurrent ulcer in patients with hypersecretion was 8 percent, whereas in patients with normal secretion, the mean incidence was 9.2 percent. Since there was no statistically significant difference between patients with hypersecretion (peak acid output more than 50 mmol/hour) and patients with acid secretion within the normal range, it does not seem wise to add antrectomy to vagotomy in patients with hypersecretion. To do so needlessly increases operative mortality, postoperative complications, and operative side effects.

Gastrin cell hyperplasia and antral dominance: Conditions of G-cell hyperplasia or antral dominance are difficult to define. We suggest that a patient with these conditions is one who has undergone a complete vagotomy as determined by the Hollander, Burge, or Grassi test, but in whom recurrent ulcer nevertheless develops because of excessive release of gastrin from the antrum in the absence of antral stasis or the Zollinger-Ellison syndrome. When we bear in mind all the potential difficulties and errors associated with the study of G cells in preoperative antral biopsies, and the current paucity of informa- tion on the numbers of G cells and serum gastrin levels in males and females of various ages, races, and physical types, we must conclude that, at present, it is virtually impossible to pinpoint before operation, patients with G- cell hyperplasia or antral dominance with any degree of confidence [72]. Since when the vagotomy is good techni-



cally, recurrent ulcer develops in few duodenal ulcer patients, as evidenced by the 1.4 percent incidence of recurrent ulcer 5 years after highly selective vagotomy reported by Fraser et al [47], our personal 2.5 percent incidence at 5 years and 5 percent at 10 years, and several other reports of low incidences of recurrent ulcer in large numbers of patients after highly selective vagotomy [61], it seems likely that antral dominance, as we have defined it, is rare, amounting perhaps to not more than 1 or 2 patients in 100. It would be very difficult and time-con- suming to discover these patients preoperatively, and thus it is probably best not to be concerned with antral dominance until easier ways of defining it become available.

Highlights: (1) As a policy, for the surgical treatment of all patients with duodenal ulcer, vagotomy and antrectomy yields inferior overall results to those of highly selective vagotomy. (2) The use of vagotomy and antrectomy for patients with hypersecretion of acid is also illogical, because the incidence of recurrent ulcer after highly selective vagotomy in these patients is the same as the incidence in patients with normal secretion. (3) G-cell hyperplasia and antral dominance are poorly defined en- tities, relatively rare, and probably best ignored at present in the routine preoperative assessment of patients with duodenal ulcer.

RECURRENT ULCERATION AFTER HIGHLY SELECTIVE VAGOTOMY

Recurrent ulceration is without doubt the potential Achilles heel of highly selective vagotomy. Indeed, were it not for the fact that very high incidences of recurrent ulcer have been reported after highly selective vagotomy by several investigators, it seems likely that highly selective vagotomy would have been more widely adopted and truncal vagotomy with a drainage procedure and vagotomy and antrectomy abandoned [48-50,62,73,74,76]. The question is whether such high recurrence rates are inevitable; are they an intrinsic feature of the operation?

We compared various preoperative factors in 48 patients in whom recurrent ulcer developed after highly selective vagotomy with the same factors in 400 patients in whom recurrent ulcer did not develop postoperatively. We found no difference between the two groups of patients with respect to age, sex, length of ulcer history, previous ulcer complications, and basal or peak acid output. The crucial difference between the two groups was at operation, since we found significant correlations between subsequent recurrent ulcer and (1) the individual surgeon who had performed the operation and (2) the postoperative acid response to insulin 1 week postoperatively. In short, recurrence correlated with incomplete vagotomy and was thus related to operative technique [71,77].

The object of vagotomy is to deprive the parietal cell mass completely of its vagal nerve supply. Incidences of recurrence would thus be expected to be higher when the vagotomy is incomplete than when it is complete. This is indeed what has been found in practice. For example, after truncal vagotomy with a drainage procedure. MacKay [78] reported that recurrent ulcer developed in 4 percent of patients 1 week after vagotomies that were

complete according to the results of the Hollander insulin test, whereas recurrent ulcer developed in 7 percent of patients with a late-positive response to insulin and 21 percent of patients with an early-positive response to insulin. The same was true for bilateral selective vagotomy and highly selective vagotomy. Thus, Muller et al [79], using Burge's intraoperative electrotest as the index of complete vagotomy, found a 5 percent incidence of recurrent ulcer 5 years after highly selective vagotomy when the test result had been negative, whereas when the result was positive, both postoperative acid outputs and the incidence of recurrent ulcer (17 percent) were significantly higher (p <0.01). Our experience at the Leeds Infirma- ry has been similar: of the highly selective vagotomies performed between 1969 and 1975, the incidence of recurrent ulcer was 4 percent when the postoperative insulin test was negative, whereas when the test was positive. the incidence of recurrent ulcer 5 to l 5 years later was 40 percent (p <0.02). Thus, the incidence of recurrent ulcer after complete vagotomy (truncal vagotomy, bilateral selective vagotomy or highly selective vagotomy) is in the range of 2 to 6 percent. More effort should therefore be devoted to achieving complete vagotomy, which is all that is required to provide permanent cure of ulcer in most patients.

Influenee of the individual surgeon: In one study, two surgeons performed more than 30 consecutive truncal vagotomies without a single positive insulin result and with an incidence of recurrent ulcer of 5 percent or less [43]. In the same study, other surgeons were found to be leaving 25 to 50 percent of their patients with an incomplete vagotomy, and the recurrence rates were predicted to range from 10 to 30 percent. Our group and that of Adami et al [76] have found that the same intersurgeon variation exists in the performance of highly selective vagotomy: some surgeons have incidences of recurrent ulcer of 1 to 4 percent 5 years after highly selective vagotomy, whereas others have incidences of recurrent ulcer of 20 or even 30 percent. A further disturbing find- ing is that such variation among surgeons in the ability to achieve a complete vagotomy, and consequently a low incidence of recurrent ulcer, was by no means confined to trainee surgeons. There was also great variation among staff and consulting surgeons.

In another study at this institution, the incidence of recurrent ulcer in 237 patients who were followed for 5 to 12 years (mean 8 years) after elective highly selective vagotomy was 12 percent [2,3,77]. This mean figure con- ceals a wide range of recurrence, from 3 to 30 percent, depending on which surgeon performed the operation. For comparison, the mean incidence of recurrent ulcer 5 to 10 years after truncal vagotomy and pyloroplasty and bilateral selective vagotomy with a drainage procedure was 8 percent and 11 percent, respectively. The incidence of recurrent ulcer approximately doubled between 5 and 10 years after highly selective vagotomy, but there have been few recurrences after 10 years (current maximum period of follow-up, 19 years).

Gastrie stasis: Holle and Bauer [80] have consistently advocated routine drainage of the antrum in conjunction with highly selective vagotomy by means of a small pylor-



oplasty or by antrectomy. They have claimed that leaving the pylorus intact predisposes to antral stasis, excessive release of gastrin, and recurrent ulceration. Prospective trials of highly selective vagotomy alone or with a drainage procedure have failed, however, to show any significant reduction in the incidence of recurrent ulcer in the patients who underwent vagotomy with drainage compared to those who underwent highly selective vagotomy alone [49,81]. Again, several large consecutive series of duodenalulcer patients have been treated by highly selective vagotomy alone, with incidences of recurrent ulcer of 5 percent or less [23,82]. Finally, at our institution we studied gastric emptying of radiolabeled liquid and solid meals in 18 patients with recurrent ulcer after highly selective vagotomy and in 18 closely matched patients without recurrent ulcer after highly selective vagotomy. For liquid meals, gastric emptying took 7.7 4- 4.7 minutes (mean 4- SD) in patients with recurrent ulcer and 9.8 4- 7.2 minutes in patients without recurrent ulcer; for solid meals, 64 4- 32 minutes and 82 4- 52 minutes, respectively. We found no delay in gastric emptying in patients with recurrent ulcer [77].

In summary, there is no evidence that a drainage procedure should be added routinely to highly selective vagotomy. Although stasis of food in the antrum secon- dary to operative trauma to the nerves of Latarjet may contribute to recurrent ulcer in a few patients after highly selective vagotomy, there seems to be little doubt that in most patients, recurrence is a consequence of incomplete vagotomy of the parietal cell mass.

Operative technique" The difficulties involved in the performance of highly selective vagotomy, whether real or imagined, have been discussed widely, while it has been tacitly assumed that truncal vagotomy is relatively easy to perform [83-85]. In fact, all types of vagotomy are technically demanding, if complete vagotomy of the parietal cell mass is to be achieved consistently. There is probably as much variation among surgeons in the achievement of complete truncal vagotomy as there is in the achievement of complete highly selective vagotomy of the parietal cell mass [43].

Thorough mobilization of the esophagus is essential, so that it may be rotated easily between the thumb and fingers, thereby demonstrating all vagal fibers, which can then be severed. About 6 cm of distal esophagus should be cleared of all fibers, as Hallenbeck et al [83] and others have shown with respect to highly selective vagotomy, but it is equally true of truncal vagotomy.

Highly selective vagotomy, unlike truncal vagotomy, may be incomplete (to the parietal cell mass) distally as well as proximally. In patients with duodenal ulcer, the parietal cell mass is extensive and the alkaline pyloric gland area or antrum relatively small. To answer the question of how far distally the highly selective vagotomy dissection should extend, the findings of Bone et al [84] and Johnson and Baxter [85,86] suggest that if the dissection extends to within 5 to 6 cm of the pylorus, the parietal cell vagotomy should be complete in about 98 percent of patients. However, a few patients have an "acid antrum," and a few surgeons are now advocating the use of Congo Red dye to delineate the extent of the

antrum and parietal cell mass. Whether the right gastroe- piploic vessels or their branches to the greater curvature should be cut, as Rosati et al [87] suggested, has been disputed. Our personal belief is that it is not necessary, since excellent results have been reported after highly selective vagotomy without this added maneuver.

The place of intraoperative tests of completeness of vagotomy i s also debated. Certainly, recurrent ulcer has been shown to be more common when the Burge electrotest result remained positive than when it was negative, and Johnson, Grassi, Narbona and others have made a cogent plea for the use of the intraoperative Grassi test. Nevertheless. as we have seen. low incidences of recurrent ulcer may be achieved without the use of these tests. Their most important function may be to focus attention on the importance of taking great pains to achieve a complete vagotomy at the time of operation. Postopera- tive tests such as the Hollander insulin test or the modified sham feeding test also provide good quality control and so exert psychologic pressure on a surgeon who is leaving many patients with an incomplete vagotomy. The individual patient with a positive test result, however, does not benefit, because one would never reoperate merely because of a positive result [52-54]. In this respect, the intraoperative tests are much superior because the surgeon, once alerted to the presence of an incomplete vagotomy, has the opportunity to put matters right.

MODIFIED VAGOTOMIES The concept of preservation of the antrum and pylorus

in duodenal ulcer surgery is now widely accepted. Within these limits, various technical modifications are being tried, with the aim of simplifying the procedure and reducing the operating time. Of these, the simplest and least controversial is the use of metal clips, such as hemo- cliPs or surgiclips, in place of conventional ligatures, to deal with the numerous blood vessels encountered along the lesser curvature and on the esophagus [88]. One of us used to take 90 to 120 minutes on average to perform highly selective vagotomy, but practice and the use of these clips has reduced this time to about 75 minutes (60 to 120 minutes, depending on the patient's build). Much of that time is still spent laboriously clearing the distal 6 cm of esophagus of all vagal fibers, and no way has yet been found to speed up that maneuver. Obesity is not regarded as a contraindication to the use of highly selective vagotomy; the vagal anatomy is the same, but the procedure just takes more time and perserverence.

Another modification is the use of anterior highly selective posterior truncal vagotomy without a drainage procedure. Originally described by Hill and Barker [89], this procedure keeps the antrum and pylorus intact but vagally denervates the pancreas and intestines and also the posterior wall of the antrum to some extent, because the posterior nerve of Latarjet is destroyed. Gastric emptying of liquids and semisolids does not seem to be impaired, however, perhaps because of bilateral innervation of the antrum, and dumping and duodenogastric reflux are virtually eliminated as in highly selective vagotomy. The number of patients undergoing this procedure has been small and we are following them with great interest.



A similar operation is anterior seromyotomy and posterior truncal vagotomy without a drainage procedure. It has been widely used in Edinburgh and Manchester by Taylor [90,92] and other investigators in the past 9 years. The results to date are encouraging, with a low mortality (0.4 percent), good gastric emptying through the intact pylorus in most patients, and a 3 percent recurrence rate after 3 years and 14 percent after 5 years. Compared with highly selective vagotomy, there is a slightly greater incidence of gastric stasis and diarrhea. The advantages claimed for this procedure are that it is easier and quicker to perform than highly selective vagotomy; however, we find that the tedious part of highly selective vagotomy is not the lesser curve dissection, but the esophageal component, which remains unchanged in Taylor's operation. In our opinion, if one decides to be highly selective, one might as well go the whole hog and preserve the posterior nerve of Latarjet and the celiac branch of the vagus. Nevertheless, use of seromyotomy with an intact pylorus seems a better option, from the patient's point of view, than truncal vagotomy with a drainage procedure. Long- er postoperative follow-up is needed to discover if the nerves severed in the gastric wall are capable of reinner- vating the parietal cell mass and producing recurrent ulcer. The possibility of subclinical antral stasis, with a prolonged chemical phase of gastrin release; also war- rants further investigation.

COMMENTS Ordinary selective vagotomy shares many of the dis-

advantages of truncal vagotomy because of the need for a drainage procedure and is now obsolete. We still sometimes use bilateral selective vagotomy in preference to truncal vagotomy in the treatment of the few patients who present with gastrojejunal stomal ulcer after Polya partial gastrectomy. Thus, in practice, the choice of elective operation for duodenal ulcer is highly selective vagotomy, truncal vagotomy with a drainage procedure, or vagotomy and antrectomy.

The use of vagotomy and antrectomy as the primary method of surgical treatment for duodenal ulcer is not recommended, because the results both of uncontrolled studies and of prospective trials show that highly selective vagotomy yields better overall results, despite its higher incidence of recurrent ulceration. Compared with highly selective vagotomy, patients undergoing vagotomy and antrectomy procedures had a higher operative mortality and postoperative morbidity, more and worse side effects, and more long-term sequelae.

Vagotomy combined with antrectomy possesses at least one clear advantage over highly selective vagotomy--its 1 percent incidence of recurrent ulceration--but truncal vagotomy with a drainage procedure has no advantage at all. Compared with truncal vagotomy with drainage, highly selective vagotomy is as likely to cure the ulcer but has a slightly lower operative mortality and morbidity, fewer side effects, and fewer metabolic sequelae. Recurrent ulceration after highly selective vagotomy can usually be treated successfully, either medically or

surgically, whereas for dumping, diarrhea, and symptoms associated with excessive duodenogastric reflux after truncal vagotomy with a drainage procedure or vagotomy and antrectomy, there is no reliable remedy.

A high incidence of recurrent ulceration is not inevitable after highly selective vagotomy. Recurrence is surgeon-related and thus attributable to inadequate operative technique. Some surgeons have reported a 2 percent incidence of recurrent ulceration 5 years after highly selective vagotomy, whereas others have reported 10, 20 and even 30 percent incidence. When some form of quality control has been used, and the test used is negative, indicating that vagotomy is complete, the incidence of recurrence has been 3 to 5 percent after 5 years of follow- up.

Some practical points to consider in the selection of a surgical treatment for duodenal ulcer follow:

How long does highly selective vagotomy take to perform? Should truncal vagotomy with drainage be used in obese patients? Forty to 120 minutes: We do not exclude patients on the grounds of obesity: the requirements are a long incision, good retraction of the rib cage by a substernal retractor, and perseverance.

Should all elective cases of non-stenosing duodenal ulcer be treated by highly selective vagotomy? No. Besides the ideal operative procedure, two other factors must be considered, namely the patient and the surgeon. If the patient is over 70 or at high risk because of impaired cardiac, respiratory or renal function, operative treatment should be avoided if possible, by the use of cimetidine and other forms of medical therapy. If an operation is inevitable, the quickest and simplest procedure may be the best, and truncal vagotomy and pyloroplasty may then still have a place. As for the surgeon, although we think that surgeons in training should be taught highly selective vagotomy as the operation of choice for duodenal ulcer, it is perhaps unrealistic to expect surgeons of long experience, who have used gastric resection for many years and know that in their hands it is safe and yields good results, to abandon a well-tried and trusted procedure for one which, initially at least, might yield worse results for technical reasons. Thus, paradoxi- cally, we think that truncal vagotomy should be abandoned, but that the continued use of partial gastrectomy may be justified in expert hands, provided that the extent of resection is not too radical.

How should recurrent ulcerat ion after highly selective vagotomy be treated? First, establish the cause, by studies of acid output (basal acid output, peak acid output using insulin and pentagastrin), gastrin levels, and if the recurrence is a new gastric ulcer, biopsy. The Zol- linger-Ellison syndrome and multiple endocrine adeno- matosis should be excluded. The ulcer is then treated medically by withdrawing steroids, nonsteroidal anti-in- flammatory drugs, alcohol, cigarettes, and stress, if possible, and administering ranitidine, cimetidine, or one of the newer mucosa-protecting agents. This treatment is usually successful, Only 20 to 30 percent of such patients in our practice have required surgical treatment, which

424 THE AMERICAN JOURNAL OF SURGERY VOLUME 156 NOVEMBER 1988


should consist of hemigastrectomy, with or without reva- gotomy and with or without Roux-Y biliary diversion. We frankly do not know which of these options is best.

Selecting the patient: Selecting the right patient for operation is as important or more important than selecting the right type of vagotomy. Although it is impossible to make hard and fast rules, the following factors are relative contraindications to elective surgical treatment for duodenal ulceration: (1) youth; (2) short ulcer history; (3) atypical pain as the only symptom; (4) absence from work for long periods because of pain; (5) heavy cigarette smoking or drinking; (6) the use of medication for ner- vousness or depression. We ensure that such patients receive both the full benefit of medical treatment and a thorough explanation of the dangers and disadvantages of surgical treatment. This may induce them to give up smoking and drinking, although it seldom does, and medical treatment may succeed eventually. The procrastinat- ing tactics may at least give them time to move to another town or another surgeon!

Compl ica ted ulcers: With the great advances in medical treatment in recent years, patients suffering from perforation, hemorrhage, or pyloric stenosis form an increasing proportion of those who require surgical treatment. N o attempt has been made here to cover this topic. Selection is the key to success: selection of the right operation for the individual patient by a very experienced surgeon. We employed highly selective vagotomy in 252 such patients who were carefully selected because they were younger and fitter than the average; there were 4 operative deaths and an incidence of ulcer recurrence equal to that found in elective cases.

Can vago tomy succeed if e imetidine o r rani t idine have fai led? The H2 receptor antagonists have different modes of action than vagotomy and are less successful than highly selective vagotomy in reducing gastric acid concentration in man over a 24-hour period [92-94]. Incidences of recurrent ulceration 1 year after vagotomy (0 to 3 percent) are much lower than after 1 year of maintenance therapy with H2 receptor antagonists (15 to 30 percent). A prospective trial of highly selective vagotomy versus maintenance treatment with cimetidine for 1 to 4 years showed that highly selective vagotomy was much more potent in curing duodenal ulcer [95]. Recent clinical studies suggest that highly selective vagotomy provides effective therapy for ulcers that have been resistant to H2 receptor antagonists [98,99], but our own and other data suggest that there may be a higher incidence of recurrent ulceration in such patients [74,100]. This important question requires further study.

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A new look at selective vagotomies

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