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Myths of the esophagus
Volume 98,
Number 1
July 1989
THORACIC AND CARDIOVASCULAR SURGERY The Journal
J THORAC
CARDIOVASC SCRG
of
1989;98:1-IO
Presidential Address
Myths of the esophagus Lucius D. Hill, MD, Seattle, Wash.
he
earliest recorded research on the function of the esophagus was conducted by Hippocrates, who gave colored beverages to pigs and simultaneously slit their throats. After these experiments, he concluded that "when liquid is swallowed a portion goes to the lungs. From there it is filtered into the pericardiaI sac where it lubricates and cools the feverish heart. The rest of the liquid is exhaled as a vapor." This myth persisted for a thousand years until Albinus in 1747 proved that liquids, when swallowed, enter the gastrointestinal tract, not the respiratory tract. Advances in knowledge of the esophagus proceed slowly. Even today, many myths concerning the esophagus prevail. For example, even in this modern age of advanced technology, the way in which the gastroesophageal junction is depicted is misleading. Fig. 1 depicts the manner in which the esophagus is invariably illustrated. I would defy anyone to find an illustration, whether in an anatomy, physiology, surgery, or medical textbook, that differs from this drawing. You may ask, "What is
From the Health Resources Building, Seattle. Wash. Read at the Fourteenth Annual Meeting of The Western Thoracic Surgical Association in Hawaii. June 22-25, 1988. Address for reprints: Lucius D. Hill, MD. Health Resources Building, 909 University St., Suite 163, Seattle. WA 98101.
A
Normal
Fig. 1. The gastroesophageal junction is invariably depicted as an open conduit with no valve and no barrier to reflux. In reality, the gastroesophageal junction remains closed except during swallowing, belching, and vomiting. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
The Journal of
2
Hill
Thoracic and Cardiovascular Surgery
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Fig. 2. The stomach can be filled to pressure levels of 15 cm of water before reflux occurs. In the cadaver. there is no sphincter action. The gradient. therefore. is due solely to the gastroesophageal valve. (From Hill LD. McCallum R. Kozarek R. Mercer D. eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders. 1988.)
wrong with this illustration?" I would ask, "How would you feel if your gastroesophageal junction were like this at this moment?" Your gastroesophageal junction would be wide open. Gastric contents, including whatever you have eaten, would have ready access to your esophagus. It is this kind of loose thinking that allows myths to prevail. Anyone with a cursory knowledge of the esophagus knows that the gastroesophageal junction stays closed at all times except during swallowing, vomiting, or belching. The lower esophageal barrier maintains a resting pressure that is greater than the pressure in the stomach. For the past 30 years, the myth has prevailed that the barrier to reflux consists solely of the lower esophageal sphincter. Over 20 years ago an equation -.lS
~>
-.lG -.lS
I = No reflux
~
-.lG
Reflux
was developed which states that the sphincter pressure must always be greater than the intragastric pressure. Otherwise, reflux occurs. This concept prevailed, despite the fact that it was known that the lower esophageal sphincter is a weak sphincter exerting a resting pressure of only 15 to 18 mm Hg. In fact, even with maneuvers, it
may develop pressures of only 100 mm Hg. Yet anyone with a normal gastroesophageal junction can stand on his or her head and reflux will not occur. In addition, anyone who has a normal gastroesophageal barrier can lie down and have someone stand on his abdomen and still reflux will not occur. Hundreds of pounds of pressure can be applied, yet the lower esophageal sphincter is a weak sphincter. Football players bury their helmets in the abdomen of the ball carrier, yet reflux does not occur with these massive pressures. It becomes apparent that the sphincter alone cannot do the job. It was these observations that stimulated my colleagues and me to return to cadaver dissections to study the gastroesophageal barrier. The first thing one notes during these dissections is that, in a subject with a normal gastroesophageal junction, the stomach may be grossly distended, yet there is nothing in the esophagus. We conducted a series of simple experiments consisting of placing a catheter in the stomach to measure pressures and another catheter to fill the stomach. The pylorus was tied off, an additional catheter was placed in the esophagus, and the esophagus was tied off. The gastroesophageal junction was left in situ (Fig. 2). These experiments showed that the stomach can be filled to levels up to 15 ern of water or more before reflux occurs. In the cadaver, obviously, there is no sphincter activity; therefore, the gradient between the esophagus and
Volume 98 Number 1 July 1989
Myths of esophagus
3
Fig. 3. The gastroesophageal valve visualized through a gastrostomy can be seento be a 180-degree flat valve that closes against the lesser curvature and is about 3 em long. (From Hill LD. McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.) stomach is produced by the gastroesophageal valve. This valve was described over 100 years ago by Braune] and later by Gubaroff.: It was recognized by Barrett' and others. When the technology became available to measure lower esophageal sphincter pressure, the valve was forgotten. The myth prevailed that the primary barrier to reflux was the lower esophageal sphincter. This pressure was something that physicians could measure and show patients and present at meetings. Despite the fact that these measurements showed that the sphincter is relatively weak, the role of the valve was overlooked. Thevalve is a one-way flutter valve that, in the human, is a flat I80-degree valve. It closes against the lesser curve. When visualized through a gastrostomy, it can be seen to be about 3 em long (Fig. 3) and, as Barrett' stated, "it closes so effectively against the lesser curve that it may be difficult to find" (Fig. 4). With the gastroesophageal junction carefully left intact with the posterior attachments not disturbed, we found a consistent significant gradient between the esophagus and stomach measuring anywhere from 5 to 15 cm of water. This gradient can be eliminated by simply pressing down on the cardia, eliminating the angle of His, and thereby eliminating the valve and converting the gastroesophageal junction to a funnel, whereupon free reflux occurs. The lowering of the cardia matches what happens during vomiting. This same phenomenon occurs in most patients with hiatal hernia, in whom the gastroesophageal junction slides into the posterior mediastinum and thereby eliminates the angle of His and the valve.
We carried these experiments a step further and performed a valvuloplasty, lengthening and stabilizing the valve, which raised the gradient a statistically significant amount. With a Dent sleeve in the lumen of the esophagus, we made certain we were not producing a constrictive effect that increased the gradient. Lengthening the valve to increase the gradient further substantiated the observation that the valve can prevent reflux. The valve offers no resistance to the flow of food and fluid aborally into the stomach but considerable resistance to retrograde flow. The gastroesophageal junction should no longer be depicted as a wide open conduit. The appropriate illustration is one that brings together the lower esophageal sphincter in the closed position with the gastroesophageal valve and the collar sling musculature anchored posteriorly. Together these structures make up the antireflux barrier (Fig. 5). What evidence is there in the living human being that the valve really works? In doing myotomies for achalasia, we measure the sphincter pressure before myotomy and then divide the musculature to reduce the length of the sphincter to less than 1 ern, We thereby reduce the obstruction to the flow of food and fluid into the abdomen but leave enough sphincter to prevent reflux. This is a delicate undertaking, and even with intraoperative pressure measurements the surgeon may divide too much of the sphincter. Therefore, we began the practice of completing the myotomy and then, through a gastrostomy, suturing and stapling the valve both anteriorly
The Journal of Thoracic and Cardiovascular Surgery
4 Hill
Fig. 4. The gastroesophageal valve visualized through a gastrostomy closes so effectively that it may be difficult to find. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
and posteriorly, to fix and lengthen the valve after the myotomy. There was concern that carrying the myotomy through the collar sling musculature would not only eliminate the sphincter but also impair the muscular contraction of the collar sling, which could eliminate or weaken the valve. In a small group of patients, we have been able to show the effectiveness of the valvuloplasty wherein the entire sphincter was divided and postoperatively the sphincter pressure was zero, yet the patient did not have reflux, even with forcible maneuvers of drawing the knees up and straining. We therefore have clear evidence in the living human being that the valve working alone with a zero sphincter pressure can indeed maintain competence of the gastroesophageal junction. From a practical standpoint, any surgical procedure that is going to prevent reflux should aim to create a 180-degree valve as near to the normal valve as possible. This method eliminates the need for an antireflux procedure in achalasia or other motility disorders. An anti reflux procedure in the presence of impaired motility can be a disaster, inasmuch as the esophagus does not have enough motility to overcome the obstruction created by an antireflux procedure. The equation that has prevailed over the past 25 years should therefore read .lS
+V
~>1 =
No reflux
since It IS obvious that the sphincter alone cannot prevent reflux with the enormous pressures to which it is subjected. What is actually being measured during
manometry is not the lower esophageal sphincter alone but the lower esophageal sphincter and the gastroesophageal valve, which together form the antirejlux barrier. Having eliminated the myth of the barrier by rewriting the equation, one must ask, "How can this be applied to antireflux surgery?" The following should be the aims of a good anti reflux operation: 1. Reconstruct the gastroesophageal junction by reducing the hernia and anchoring the gastroesophageal junction posteriorly. 2. Calibrate the cardia so that the sphincter pressure is in a normal range. This can be best accomplished with intraoperative manometries. 3. Restore the gastroesophageal 180-degree valve by placing tension on the collar sling musculature and recreating the angle of His. The valve can be palpated through the stomach wall. These three objectives can be accomplished by reducing the hernia, dividing the gastrophrenic ligament on the greater curvature side, and rotating the esophagus around to visualize both the anterior and posterior phrenoesophageal bundles and both vagus nerves. The preaortic fascia and median arcuate ligament are dissected out and an instrument is placed beneath the ligament to protect the underlying aorta and the celiac artery. A simpler and safer method to accomplish this consists of placing a finger into the esophageal hiatus, behind the preaortic fascia, lifting it up off of the aorta, and then placing the sutures through it without dissect-
Volume 98 Number 1 July 1989
Myths of esophagus
5
Jo Ann C'Ji1'&n:l 1981 .
Fig. 5. The appropriate view of gastroesophageal junction brings together the lower esophageal sphincter in the closed position with the gastroesophageal valve and the collar sling musculature anchored posteriorly. Together, these structures make up the antireflux barrier. (From Hill LD, McCallum R, Kozarek R, Mercer D, cds, The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1989.)
ing out the celiac artery. The hiatus is closed loosely about the esophagus, and then sutures are taken in the anterior and posterior phrenoesophageal bundles and carried down through the preaortic fascia (Fig. 6). Usually, five such sutures are taken, avoiding the vagus nerves. These sutures are reinforced with Teflon pledgets so that they will not pull out over the long term. As these sutures are tied, a single throw is placed in the knot and the nasogastric tube is used, which is in place and has been modified to allow for pressure measurements. This tube is simply passed up and down through the sphincter to measure the barrier pressure. The sump tube is attached to a manometer that gives a digital readout and a tracing that the surgeon can see in the operating room. The kind of tracing we obtain means out at about 45 mm Hg over 4 em, The completed procedure fulfills the aforementioned objectives (Fig. 7): There is an intraabdominal segment of the esophagus; the gastroesophageal junction is secured permanently to the preaortic fascia; the angle of His has automatically
Fig. 6. The hiatus has been closed and five sutures are taken including the anterior and posterior phrenoesophageal bundles avoiding the vagus nerves and the esophagus. These are carried through the preaortic fascia and median arcuate ligament. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 19S9.)
been re-created by tension on the collar sling musculature; and the gastroesophageal valve can be palpated through the stomach wall. The operation should restore the normal anatomy with the gastroesophageal junction anchored posteriorly, which is where the gastroesophageal junction, along with the entire gastrointestinal tract, both the solid and hollow viscera, is anchored by the dorsal mesentery to the posterior body wall. We tested the thesis of whether intraoperative manometry is worth the time and effort by analyzing two sets of cases totaling 1000 patients (those with strictures and reoperations were eliminated) that were matched as closely as possible. It was obvious from this study that the prevalence of persistent reflux was far less in the postmanometry period (1.5%) than in the premanometry period (4.8%). In those patients with achalasia and with scleroderma or in patients who have had
The Journal of
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Hill
Fig. 7. The final appearance of the repair. The phrenoesophageal bundles are anchored securely to the preaortic fascia and the median arcuate ligament. The gastroesophageal valve has been accentuated with tension on the collar sling musculature, and the lower esophageal sphincter has been calibrated. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
several repeat operations, we fortify the valve through a gastrostomy with sutures anteriorly and posteriorly, and we measure the pressure and make certain that we are not narrowing the lumen of the esophagus. This approach is ideal for patients with achalasia and scleroderma in that it offers no resistance to flow into the stomach but considerable resistance to retrograde flow. We have now monitored patients with the valvuloplasty for more than 2'/2 years, and in most of these patients the valve is holding up nicely. Having pointed out these features of our procedure many times, we believed that we were getting the word across about the fundamentals of the operation as we saw it-the procedure being an effort to simply restore the gastroesophageal junction to its normal anatomy and function. We were surprised therefore by a report by the group from the University of Ireland in Hennes-
Thoracic and Cardiovascular Surgery
Fig. 8. Severe peptic stricture with tortuosity and deep penetrating ulcer termed "undilatable stricture with short esophagus." (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
sey's book purporting to show our operation. The authors depict our operation as a procedure that consists of sutures placed in the esophagus, anchoring the esophagus to the preaortic fascia and bunching up the esophagus in an effort to curtail reflux. This violates all of the criteria that we have emphasized. We obviously have more work to do. This illustrates how myths begin. There is no area in surgery that has created more myths and more controversies than peptic esophageal strictures. Although Lam and Gahagan" wrote a report entitled "The Myth of the Short Esophagus," most workers in this area previously thought that patients with severe peptic strictures with tortuosity and deep penetrating ulcers (Fig. 8) had an undilatable stricture with a short esophagus. This myth was derived from an
Volume 98
Number 1
Myths of esophagus 7
July 1989
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Fig. 9. Postoperative radiograph of patient shown in Fig. 6. Four weeks after the operation, the stricture has opened and reflux has been corrected. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.) unfortunate statement by Barrett,' who stated that "any portion of the gullet lined with columnar epithelium must be stomach." Allison and Johnstone" published a report shortly afterward stating that the portion of the gullet lined by columnar epithelium represented columnar-lined esophagus rather than stomach. Barrett' later changed his mind, but the term "short esophagus" persisted and many patients were subjected to resections with a mortality rate of from 10% to 15%. We investigated these strictures, particularly at operation, and believed that the portion of the gullet from the stricture down indeed was not stomach but was rather gastric-lined esophagus. We developed a technique of simply doing an antireflux procedure and at the same time straightening the esophagus and dilating it at operation. The patient shown in Fig. 8 had been told she had an undilatable stricture and a short esophagus and
needed a resection. At operation we were able to do a simple antireflux procedure and dilate the esophagus. Within 3 weeks this patient was swallowing solid food for the first time in 2 years. The upper gastrointestinal tract radiograph showed that the stricture had opened (Fig. 9). She has remained well since 1970 and swallows all solid food. We have expanded this series to over 170 patients, and even with tight strictures above the aortic arch in patients who could swallow only thin liquids, we have been able to dilate the stricture, do an antireflux procedure, and within 3 to 6 weeks the stricture opens. An important example of this is a young boy who had had a stricture almost since birth and had been living on liquids for over a year. A simple antireflux procedure was done but the barrier pressure was raised to only 9 mm Hg, which is insufficient, and the stricture per-
The Journal of
8 Hill
Fig. 10. A gastrobronchial fistula resulting from a gastric ulcer occurring after a transabdominal Nissen repair that slipped. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
sisted. At a second operation, the sphincter pressure was raised to 25 nun Hg and the previous stricture healed rapidly. This patient vividly illustrates the fact that an antireflux procedure must curtail reflux. Otherwise, the stricture will persist. It is this failure of a simplified antireflux procedure that leads many surgeons, even today, to state that a simple antireflux procedure will not work in these patients and resection is necessary. Our concept of peptic strictures is that there is a small hiatal hernia with reflux that denudes the squamous epithelium, which is replaced with columnar epithelium by a process of creeping substitution. This process may extend all the way up to the aortic arch. In operations on these patients, intraoperative pressure measurements are important. A study of 170 cases showed that early operation gave the best result by far. Patients who had a previous operation had only fair results, but the group who had multiple dilatations had the worst outcome. We concluded that a conservative antireflux operation plus dilatation is a viable method of dealing with these patients. We believe that the myth of the short esophagus has been laid to rest.
Thoracic and Cardiovascular Surgery
An important aspect of peptic strictures is the presence of Barrett's epithelium, which has engendered many myths. There are those who have stated that all patients with Barrett's epithelium should have a resection. This would include all patients with a columnarlined esophagus. Others have said that intermittent surveillance is all that is required. It is only recently, through careful studies, that we have been able to determine which patients require resection and which patients can be watched The group at the University of Washington? has done the most meticulous study to be reported. They have studied 215 patients with esophagitis and 154 with Barrett's esophagus and have performed deep biopsies on 154 patients, 30 to 40 per patient. These specimens have been studied with a light microscope and with flow cytometry. The group of Reid, Haggitt, and Rubin' have been able to correlate the histologic characteristics with flow cytometry and have shown that patients can be grouped into those having simple metaplasia and dysplasia. The patients with dysplasia may be further grouped according to mild, moderate, and severe dysplasia. It is only the patients with severe dysplasia who appear to have a premalignant condition. In patients with severe dysplasia, the spectrum ranges from advanced changes in histologic characteristics to carcinoma in situ. In patients with high-grade dysplasia or Barrett's specialized epithelium, most surgeons are now recommending resection. Several studies, including that done at the University of Washington,' have shown that cancer of the esophagus arises in areas of high-grade dysplasia and, when high-grade dysplasia is seen, concomitant carcinoma in situ or invasive carcinoma is often present but undetected. All of the carcinomas in the group studied at the University of Washington? were in areas of high-grade dysplasia. It is interesting that in all of the careful studies published to date, patients with Barrett's epithelium had gastroesophageal reflux. The finding of severe dysplasia is important beyond carcinoma of the esophagus and, in fact, has been shown to be the precursor of other cancers, particularly cancer of the cervix. The question of whether it would be useful to detect cancer at this stage of carcinoma in situ or microinvasive carcinoma was answered forcibly by the group in China," where massive surveys have been done with long-term follow-up. In a large survey reported from China, 100 patients with severe dysplasia, carcinoma in situ, and microinvasive cancer were treated by resection, and 99 of the 100 patients were alive at 5 years. This result leaves no doubt that the cure rate of cancer of the esophagus would be high if carcinoma
Volume 98 Number 1 July 1989
could be detected at this stage. Cytologic brushings and biopsies were used in the China study. Several reports, particularly the study at the University of Washington,' show that flow cytometry correlates well with severe dysplasia. If results of flow cytometry are grossly abnormal, the patient is at risk for carcinoma of the esophagus. Efforts to develop a reliable, inexpensive screening test to detect microinvasive cancer are underway. It is studies such as these that will dispel the myths surrounding Barrett's esophagus, indicate which patients will benefit from surgery, and at the same time lead to improved results. The worth of any operation is best estimated by the long-term follow-up and the number of operations that fail and must be redone. We 9 recently reported 305 reoperations for failed antireflux procedures, of which 114 were failed Nissen repairs. The number of failed Nissen operations continues to increase and now numbers.over 145 reoperations. Those patients who require reoperation are simply the tip of the iceberg. There are many more who have gas bloat syndrome, dysphagia, inability to maintain weight, and constant epigastric pain or reflux. We realize that the number of patients having failed repairs requiring reoperation comes from a large population having had the Nissen repair. The Nissen operation consists of wrapping the lower esophagus with the cardia containing the parietal cell mass of the stomach, which is the most potent acidproducing segment of the entire gastrointestinal tract. This wrap depends on sutures in the esophagus for its integrity, yet the esophagus has no serosa and sutures must be taken carefully in the muscularis and submucosa; otherwise, through-and-through sutures may cause fistulas. When these sutures disrupt, the entire wrap may slip, and the kinds of failures of the Nissen repair that we encounter show that slippage is the most common cause of failure. The patulous repair, the obstructed repair, and various disruptions, along with a series of fistulas, constitute the remainder of these failures. The patulous repair is one of the most common causes of failure of all antireflux procedures. It is this kind of failure that can be prevented by the use of intraoperative pressure measurements. If one is measuring the pressure in a gastroesophageal junction that will allow the passage of three fingers, the machine will indicate that the pressure is zero and the surgeon has more work to do. When the repair slips, the wrap usually ends up at the junction of the upper and middle thirds of the stomach and partially obstructs the parietal cell mass. The partially obstructed parietal cell mass with food
Myths of esophagus 9
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Fig. 11. The hemostat demonstrates a huge gastric ulcer that perforated the stomach, the diaphragm, and the pericardium. The base of the ulcer was the myocardium. This patient with "true heartburn" is the only survivor of a gastropericardial fistula of whom we are aware. (From Hill LD, McCallum R, Kozarek R, Mercer D. eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
retention, increased acid output, poor drainage, and ischemia represents an excellent ulcerogenic preparation, as good as any that could be constructed in the experimental laboratory. This is borne out clinically by the fact that many of these individuals have gastric ulcers in the pouch. Two patients seen by us with a gastric ulcer had a perforation that produced a gastrocutaneous fistula. These patients were in the intensive care unit for several weeks before being sent for a repeat operation. The slipped Nissen may precipitate gastric ulcers that penetrate the stomach, the diaphragm, and the lung. One patient with a failed Nissen had a right gastrobronchial fistula (Fig. 10). Another patient had a transthoracic Nissen repair, which most workers now believe produces a paraesophageal hernia with all of its serious complications. This gastric ulcer penetrated through the stomach and into the left lung and produced a gastrobronchial fistula. Another patient had a posterior pene-
The Journal of
10
Thoracic and Cardiovascular
Hill
trating ulcer after a slipped Nissen in a transabdominal repair. This posterior gastric ulcer perforated the aorta. A very alert surgeon, Dr. Edwin James, was able to get a clamp on the aorta, remove a huge clot, close both the aortic and gastric openings, and salvage the patient. This is the only survivor of a gastroaortic fistula of whom we are aware. An even more challenging problem occurred when a patient was admitted to the coronary care unit with a diagnosis of myocardial infarction. The electrocardiogram showed diaphragmatic pericarditis. The patient had no other cardiac abnormalities. An alert surgeon recognized that this patient had had a Nissen repair. There was air in the pericardium and, on barium swallow, barium entered the pericardial sac. It became apparent that there was a gastropericardial fistula. At operation (Fig. II), a huge gastric ulcer was noted to have penetrated through the stomach, the diaphragm, and the pericardium. The base of the ulcer was the myocardium. This patient represents a case of true "heartburn," "heartburn" being the worst myth connected with the esophagus, since "heartburn" actually has nothing to do with the heart except in rare cases such as this. The gastric ulcer was taken down and closed, as was the diaphragm. The gastroesophageal junction was anchored to the preaortic fascias, but the patient was in such poor condition that a formal takedown of the wrap and repair could not be done. The patient survived this procedure, the only survivor of a gastropericardial fistula of whom we are aware. Since the wrap was stilI in place, however, another gastric ulcer rapidly developed and penetrated along the left gastric pedicle into the liver. At reoperation, it was necessary to divide the left gastric pedicle to close the ulcer. The patient had had a floppy Nissen, which included division of all of the short gastric vessels all the way to the antrum. The blood supply to the greater curvature had been ligated previously, and on ligation of the left gastric pedicle the entire stomach turned black, necessitating a total gastric resection. This patient has survived with an esophagojejunostomy, but these complications indicate the seriousness of the slipped Nissen type of repair. As long as an obstructed parietal cell mass is present, the patient is at risk for penetrating gastric ulcers. In most patients with a failed Nissen requiring reoperation, we were able to do an anti reflux procedure; however, in the last patient a resection was required. The fistulas were dealt with on an individual basis, and the results were better than we had anticipated, with 86% of patients reporting a good outcome. This is gratifying, because some of these patients had been operated on as
Surgery
many as five times. These patients have led us to believe that the Nissen procedure, even when properly performed, carries life-threatening risks. Surgeons using this technique should be aware of these risks. Because of the failures seen by internists, there are concerns about the durability of antireflux operations. Dr. Low and our group'? are reporting a follow-up of 167 patients having the Hill repair that starts at 15 years with a mean follow-up of 17.8 years. The 15- to 20-year follow-up is compared with the follow-up at 10 and 5 years. This landmark report shows that properly performed antireflux operations give lasting good results. Eighty-eight percent of patients had good to excellent results at 15 to 20 years. There are many more myths connected with the esophagus. I am sure that these myths will be laid to rest and myths connected with the whole of thoracic surgery (cardiac, pulmonary, as well the esophagus) will be dispelled and the truth developed. On the cutting edge of research, dispelling these myths, will be the members of this great association, the Western Thoracic. REFERENCES I. Braune W. Topographisch-anatomischer Atlas nach Durchschnitten an getrorene Cadarem. Leipzig: Kleine Ausgahe, 1878: 113-4. 2. Von Gubaroff A. Uber den Verschluss der menschlichen Magens an der Cardia. Arch Anat Physiol 1886:395. 3. Barrett NR. Hiatus hernia: a review of some controversial points. Br J Surg 1954:42:231-44. 4. Lam CR. Gahagan TH. Special comment: the myth of the short esophagus. In: :\yhus LM. Harkins HN. eds. Hernia. Philadelphia. J B Lippincott. 1964:450. 5. Barrett N. Quoted in: Hill LD. McCallum R. Kozarek R. Mercer D. OOs. The esophagus: medical and surgical management. Philadelphia: WB Saunders. 1988: 139. 6. Allison PRo Johnstone AS. The esophagus lined with gastric mucous membrane. Thorax 1953:8:87. 7. Reid BJ. Haggitt RC, Rubin CEo Barrett's esophagus and esophageal adenocarcinoma. In: Hill LD. McCallum R. Kozarek R. Mercer D. cds. The esophagus: medical and surgical management. Philadelphia: WB Saunders. 1988:157-66. 8. Tumor Prevention. Treatment and Research Group. Chengchow, Honan: Esophageal Cancer Research Group. Chinese Academy of Medical Sciences. Peking: and Linhsien County People's Hospital. Honan. Pathology of early esophageal squamous cell carcinoma. Chin Moo J 1977;3: 180-92. 9. Low DE. Mercer CD. Turner EC, Hill LD. Post Nissan syndrome. Surg Gynecol Obstet 1988:167:1-5. 10. Low DE. Anderson RP. lives R. Riccardelli E. Hill LD. Fifteen- to twenty-year results after the Hill antireftux operation. J THORAC CARDIO\ASC SLRG [In press].
Number 1
July 1989
THORACIC AND CARDIOVASCULAR SURGERY The Journal
J THORAC
CARDIOVASC SCRG
of
1989;98:1-IO
Presidential Address
Myths of the esophagus Lucius D. Hill, MD, Seattle, Wash.
he
earliest recorded research on the function of the esophagus was conducted by Hippocrates, who gave colored beverages to pigs and simultaneously slit their throats. After these experiments, he concluded that "when liquid is swallowed a portion goes to the lungs. From there it is filtered into the pericardiaI sac where it lubricates and cools the feverish heart. The rest of the liquid is exhaled as a vapor." This myth persisted for a thousand years until Albinus in 1747 proved that liquids, when swallowed, enter the gastrointestinal tract, not the respiratory tract. Advances in knowledge of the esophagus proceed slowly. Even today, many myths concerning the esophagus prevail. For example, even in this modern age of advanced technology, the way in which the gastroesophageal junction is depicted is misleading. Fig. 1 depicts the manner in which the esophagus is invariably illustrated. I would defy anyone to find an illustration, whether in an anatomy, physiology, surgery, or medical textbook, that differs from this drawing. You may ask, "What is
From the Health Resources Building, Seattle. Wash. Read at the Fourteenth Annual Meeting of The Western Thoracic Surgical Association in Hawaii. June 22-25, 1988. Address for reprints: Lucius D. Hill, MD. Health Resources Building, 909 University St., Suite 163, Seattle. WA 98101.
A
Normal
Fig. 1. The gastroesophageal junction is invariably depicted as an open conduit with no valve and no barrier to reflux. In reality, the gastroesophageal junction remains closed except during swallowing, belching, and vomiting. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
The Journal of
2
Hill
Thoracic and Cardiovascular Surgery
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Esophageal manometric catheter 2 leads to recorder
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Fig. 2. The stomach can be filled to pressure levels of 15 cm of water before reflux occurs. In the cadaver. there is no sphincter action. The gradient. therefore. is due solely to the gastroesophageal valve. (From Hill LD. McCallum R. Kozarek R. Mercer D. eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders. 1988.)
wrong with this illustration?" I would ask, "How would you feel if your gastroesophageal junction were like this at this moment?" Your gastroesophageal junction would be wide open. Gastric contents, including whatever you have eaten, would have ready access to your esophagus. It is this kind of loose thinking that allows myths to prevail. Anyone with a cursory knowledge of the esophagus knows that the gastroesophageal junction stays closed at all times except during swallowing, vomiting, or belching. The lower esophageal barrier maintains a resting pressure that is greater than the pressure in the stomach. For the past 30 years, the myth has prevailed that the barrier to reflux consists solely of the lower esophageal sphincter. Over 20 years ago an equation -.lS
~>
-.lG -.lS
I = No reflux
~
-.lG
Reflux
was developed which states that the sphincter pressure must always be greater than the intragastric pressure. Otherwise, reflux occurs. This concept prevailed, despite the fact that it was known that the lower esophageal sphincter is a weak sphincter exerting a resting pressure of only 15 to 18 mm Hg. In fact, even with maneuvers, it
may develop pressures of only 100 mm Hg. Yet anyone with a normal gastroesophageal junction can stand on his or her head and reflux will not occur. In addition, anyone who has a normal gastroesophageal barrier can lie down and have someone stand on his abdomen and still reflux will not occur. Hundreds of pounds of pressure can be applied, yet the lower esophageal sphincter is a weak sphincter. Football players bury their helmets in the abdomen of the ball carrier, yet reflux does not occur with these massive pressures. It becomes apparent that the sphincter alone cannot do the job. It was these observations that stimulated my colleagues and me to return to cadaver dissections to study the gastroesophageal barrier. The first thing one notes during these dissections is that, in a subject with a normal gastroesophageal junction, the stomach may be grossly distended, yet there is nothing in the esophagus. We conducted a series of simple experiments consisting of placing a catheter in the stomach to measure pressures and another catheter to fill the stomach. The pylorus was tied off, an additional catheter was placed in the esophagus, and the esophagus was tied off. The gastroesophageal junction was left in situ (Fig. 2). These experiments showed that the stomach can be filled to levels up to 15 ern of water or more before reflux occurs. In the cadaver, obviously, there is no sphincter activity; therefore, the gradient between the esophagus and
Volume 98 Number 1 July 1989
Myths of esophagus
3
Fig. 3. The gastroesophageal valve visualized through a gastrostomy can be seento be a 180-degree flat valve that closes against the lesser curvature and is about 3 em long. (From Hill LD. McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.) stomach is produced by the gastroesophageal valve. This valve was described over 100 years ago by Braune] and later by Gubaroff.: It was recognized by Barrett' and others. When the technology became available to measure lower esophageal sphincter pressure, the valve was forgotten. The myth prevailed that the primary barrier to reflux was the lower esophageal sphincter. This pressure was something that physicians could measure and show patients and present at meetings. Despite the fact that these measurements showed that the sphincter is relatively weak, the role of the valve was overlooked. Thevalve is a one-way flutter valve that, in the human, is a flat I80-degree valve. It closes against the lesser curve. When visualized through a gastrostomy, it can be seen to be about 3 em long (Fig. 3) and, as Barrett' stated, "it closes so effectively against the lesser curve that it may be difficult to find" (Fig. 4). With the gastroesophageal junction carefully left intact with the posterior attachments not disturbed, we found a consistent significant gradient between the esophagus and stomach measuring anywhere from 5 to 15 cm of water. This gradient can be eliminated by simply pressing down on the cardia, eliminating the angle of His, and thereby eliminating the valve and converting the gastroesophageal junction to a funnel, whereupon free reflux occurs. The lowering of the cardia matches what happens during vomiting. This same phenomenon occurs in most patients with hiatal hernia, in whom the gastroesophageal junction slides into the posterior mediastinum and thereby eliminates the angle of His and the valve.
We carried these experiments a step further and performed a valvuloplasty, lengthening and stabilizing the valve, which raised the gradient a statistically significant amount. With a Dent sleeve in the lumen of the esophagus, we made certain we were not producing a constrictive effect that increased the gradient. Lengthening the valve to increase the gradient further substantiated the observation that the valve can prevent reflux. The valve offers no resistance to the flow of food and fluid aborally into the stomach but considerable resistance to retrograde flow. The gastroesophageal junction should no longer be depicted as a wide open conduit. The appropriate illustration is one that brings together the lower esophageal sphincter in the closed position with the gastroesophageal valve and the collar sling musculature anchored posteriorly. Together these structures make up the antireflux barrier (Fig. 5). What evidence is there in the living human being that the valve really works? In doing myotomies for achalasia, we measure the sphincter pressure before myotomy and then divide the musculature to reduce the length of the sphincter to less than 1 ern, We thereby reduce the obstruction to the flow of food and fluid into the abdomen but leave enough sphincter to prevent reflux. This is a delicate undertaking, and even with intraoperative pressure measurements the surgeon may divide too much of the sphincter. Therefore, we began the practice of completing the myotomy and then, through a gastrostomy, suturing and stapling the valve both anteriorly
The Journal of Thoracic and Cardiovascular Surgery
4 Hill
Fig. 4. The gastroesophageal valve visualized through a gastrostomy closes so effectively that it may be difficult to find. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
and posteriorly, to fix and lengthen the valve after the myotomy. There was concern that carrying the myotomy through the collar sling musculature would not only eliminate the sphincter but also impair the muscular contraction of the collar sling, which could eliminate or weaken the valve. In a small group of patients, we have been able to show the effectiveness of the valvuloplasty wherein the entire sphincter was divided and postoperatively the sphincter pressure was zero, yet the patient did not have reflux, even with forcible maneuvers of drawing the knees up and straining. We therefore have clear evidence in the living human being that the valve working alone with a zero sphincter pressure can indeed maintain competence of the gastroesophageal junction. From a practical standpoint, any surgical procedure that is going to prevent reflux should aim to create a 180-degree valve as near to the normal valve as possible. This method eliminates the need for an antireflux procedure in achalasia or other motility disorders. An anti reflux procedure in the presence of impaired motility can be a disaster, inasmuch as the esophagus does not have enough motility to overcome the obstruction created by an antireflux procedure. The equation that has prevailed over the past 25 years should therefore read .lS
+V
~>1 =
No reflux
since It IS obvious that the sphincter alone cannot prevent reflux with the enormous pressures to which it is subjected. What is actually being measured during
manometry is not the lower esophageal sphincter alone but the lower esophageal sphincter and the gastroesophageal valve, which together form the antirejlux barrier. Having eliminated the myth of the barrier by rewriting the equation, one must ask, "How can this be applied to antireflux surgery?" The following should be the aims of a good anti reflux operation: 1. Reconstruct the gastroesophageal junction by reducing the hernia and anchoring the gastroesophageal junction posteriorly. 2. Calibrate the cardia so that the sphincter pressure is in a normal range. This can be best accomplished with intraoperative manometries. 3. Restore the gastroesophageal 180-degree valve by placing tension on the collar sling musculature and recreating the angle of His. The valve can be palpated through the stomach wall. These three objectives can be accomplished by reducing the hernia, dividing the gastrophrenic ligament on the greater curvature side, and rotating the esophagus around to visualize both the anterior and posterior phrenoesophageal bundles and both vagus nerves. The preaortic fascia and median arcuate ligament are dissected out and an instrument is placed beneath the ligament to protect the underlying aorta and the celiac artery. A simpler and safer method to accomplish this consists of placing a finger into the esophageal hiatus, behind the preaortic fascia, lifting it up off of the aorta, and then placing the sutures through it without dissect-
Volume 98 Number 1 July 1989
Myths of esophagus
5
Jo Ann C'Ji1'&n:l 1981 .
Fig. 5. The appropriate view of gastroesophageal junction brings together the lower esophageal sphincter in the closed position with the gastroesophageal valve and the collar sling musculature anchored posteriorly. Together, these structures make up the antireflux barrier. (From Hill LD, McCallum R, Kozarek R, Mercer D, cds, The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1989.)
ing out the celiac artery. The hiatus is closed loosely about the esophagus, and then sutures are taken in the anterior and posterior phrenoesophageal bundles and carried down through the preaortic fascia (Fig. 6). Usually, five such sutures are taken, avoiding the vagus nerves. These sutures are reinforced with Teflon pledgets so that they will not pull out over the long term. As these sutures are tied, a single throw is placed in the knot and the nasogastric tube is used, which is in place and has been modified to allow for pressure measurements. This tube is simply passed up and down through the sphincter to measure the barrier pressure. The sump tube is attached to a manometer that gives a digital readout and a tracing that the surgeon can see in the operating room. The kind of tracing we obtain means out at about 45 mm Hg over 4 em, The completed procedure fulfills the aforementioned objectives (Fig. 7): There is an intraabdominal segment of the esophagus; the gastroesophageal junction is secured permanently to the preaortic fascia; the angle of His has automatically
Fig. 6. The hiatus has been closed and five sutures are taken including the anterior and posterior phrenoesophageal bundles avoiding the vagus nerves and the esophagus. These are carried through the preaortic fascia and median arcuate ligament. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 19S9.)
been re-created by tension on the collar sling musculature; and the gastroesophageal valve can be palpated through the stomach wall. The operation should restore the normal anatomy with the gastroesophageal junction anchored posteriorly, which is where the gastroesophageal junction, along with the entire gastrointestinal tract, both the solid and hollow viscera, is anchored by the dorsal mesentery to the posterior body wall. We tested the thesis of whether intraoperative manometry is worth the time and effort by analyzing two sets of cases totaling 1000 patients (those with strictures and reoperations were eliminated) that were matched as closely as possible. It was obvious from this study that the prevalence of persistent reflux was far less in the postmanometry period (1.5%) than in the premanometry period (4.8%). In those patients with achalasia and with scleroderma or in patients who have had
The Journal of
6
Hill
Fig. 7. The final appearance of the repair. The phrenoesophageal bundles are anchored securely to the preaortic fascia and the median arcuate ligament. The gastroesophageal valve has been accentuated with tension on the collar sling musculature, and the lower esophageal sphincter has been calibrated. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
several repeat operations, we fortify the valve through a gastrostomy with sutures anteriorly and posteriorly, and we measure the pressure and make certain that we are not narrowing the lumen of the esophagus. This approach is ideal for patients with achalasia and scleroderma in that it offers no resistance to flow into the stomach but considerable resistance to retrograde flow. We have now monitored patients with the valvuloplasty for more than 2'/2 years, and in most of these patients the valve is holding up nicely. Having pointed out these features of our procedure many times, we believed that we were getting the word across about the fundamentals of the operation as we saw it-the procedure being an effort to simply restore the gastroesophageal junction to its normal anatomy and function. We were surprised therefore by a report by the group from the University of Ireland in Hennes-
Thoracic and Cardiovascular Surgery
Fig. 8. Severe peptic stricture with tortuosity and deep penetrating ulcer termed "undilatable stricture with short esophagus." (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
sey's book purporting to show our operation. The authors depict our operation as a procedure that consists of sutures placed in the esophagus, anchoring the esophagus to the preaortic fascia and bunching up the esophagus in an effort to curtail reflux. This violates all of the criteria that we have emphasized. We obviously have more work to do. This illustrates how myths begin. There is no area in surgery that has created more myths and more controversies than peptic esophageal strictures. Although Lam and Gahagan" wrote a report entitled "The Myth of the Short Esophagus," most workers in this area previously thought that patients with severe peptic strictures with tortuosity and deep penetrating ulcers (Fig. 8) had an undilatable stricture with a short esophagus. This myth was derived from an
Volume 98
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Myths of esophagus 7
July 1989
•.
.~ ~~;~ "
..
... :''"-,;.~'
._
ij
~~~--~---._--,
\1
Fig. 9. Postoperative radiograph of patient shown in Fig. 6. Four weeks after the operation, the stricture has opened and reflux has been corrected. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.) unfortunate statement by Barrett,' who stated that "any portion of the gullet lined with columnar epithelium must be stomach." Allison and Johnstone" published a report shortly afterward stating that the portion of the gullet lined by columnar epithelium represented columnar-lined esophagus rather than stomach. Barrett' later changed his mind, but the term "short esophagus" persisted and many patients were subjected to resections with a mortality rate of from 10% to 15%. We investigated these strictures, particularly at operation, and believed that the portion of the gullet from the stricture down indeed was not stomach but was rather gastric-lined esophagus. We developed a technique of simply doing an antireflux procedure and at the same time straightening the esophagus and dilating it at operation. The patient shown in Fig. 8 had been told she had an undilatable stricture and a short esophagus and
needed a resection. At operation we were able to do a simple antireflux procedure and dilate the esophagus. Within 3 weeks this patient was swallowing solid food for the first time in 2 years. The upper gastrointestinal tract radiograph showed that the stricture had opened (Fig. 9). She has remained well since 1970 and swallows all solid food. We have expanded this series to over 170 patients, and even with tight strictures above the aortic arch in patients who could swallow only thin liquids, we have been able to dilate the stricture, do an antireflux procedure, and within 3 to 6 weeks the stricture opens. An important example of this is a young boy who had had a stricture almost since birth and had been living on liquids for over a year. A simple antireflux procedure was done but the barrier pressure was raised to only 9 mm Hg, which is insufficient, and the stricture per-
The Journal of
8 Hill
Fig. 10. A gastrobronchial fistula resulting from a gastric ulcer occurring after a transabdominal Nissen repair that slipped. (From Hill LD, McCallum R, Kozarek R, Mercer D, eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
sisted. At a second operation, the sphincter pressure was raised to 25 nun Hg and the previous stricture healed rapidly. This patient vividly illustrates the fact that an antireflux procedure must curtail reflux. Otherwise, the stricture will persist. It is this failure of a simplified antireflux procedure that leads many surgeons, even today, to state that a simple antireflux procedure will not work in these patients and resection is necessary. Our concept of peptic strictures is that there is a small hiatal hernia with reflux that denudes the squamous epithelium, which is replaced with columnar epithelium by a process of creeping substitution. This process may extend all the way up to the aortic arch. In operations on these patients, intraoperative pressure measurements are important. A study of 170 cases showed that early operation gave the best result by far. Patients who had a previous operation had only fair results, but the group who had multiple dilatations had the worst outcome. We concluded that a conservative antireflux operation plus dilatation is a viable method of dealing with these patients. We believe that the myth of the short esophagus has been laid to rest.
Thoracic and Cardiovascular Surgery
An important aspect of peptic strictures is the presence of Barrett's epithelium, which has engendered many myths. There are those who have stated that all patients with Barrett's epithelium should have a resection. This would include all patients with a columnarlined esophagus. Others have said that intermittent surveillance is all that is required. It is only recently, through careful studies, that we have been able to determine which patients require resection and which patients can be watched The group at the University of Washington? has done the most meticulous study to be reported. They have studied 215 patients with esophagitis and 154 with Barrett's esophagus and have performed deep biopsies on 154 patients, 30 to 40 per patient. These specimens have been studied with a light microscope and with flow cytometry. The group of Reid, Haggitt, and Rubin' have been able to correlate the histologic characteristics with flow cytometry and have shown that patients can be grouped into those having simple metaplasia and dysplasia. The patients with dysplasia may be further grouped according to mild, moderate, and severe dysplasia. It is only the patients with severe dysplasia who appear to have a premalignant condition. In patients with severe dysplasia, the spectrum ranges from advanced changes in histologic characteristics to carcinoma in situ. In patients with high-grade dysplasia or Barrett's specialized epithelium, most surgeons are now recommending resection. Several studies, including that done at the University of Washington,' have shown that cancer of the esophagus arises in areas of high-grade dysplasia and, when high-grade dysplasia is seen, concomitant carcinoma in situ or invasive carcinoma is often present but undetected. All of the carcinomas in the group studied at the University of Washington? were in areas of high-grade dysplasia. It is interesting that in all of the careful studies published to date, patients with Barrett's epithelium had gastroesophageal reflux. The finding of severe dysplasia is important beyond carcinoma of the esophagus and, in fact, has been shown to be the precursor of other cancers, particularly cancer of the cervix. The question of whether it would be useful to detect cancer at this stage of carcinoma in situ or microinvasive carcinoma was answered forcibly by the group in China," where massive surveys have been done with long-term follow-up. In a large survey reported from China, 100 patients with severe dysplasia, carcinoma in situ, and microinvasive cancer were treated by resection, and 99 of the 100 patients were alive at 5 years. This result leaves no doubt that the cure rate of cancer of the esophagus would be high if carcinoma
Volume 98 Number 1 July 1989
could be detected at this stage. Cytologic brushings and biopsies were used in the China study. Several reports, particularly the study at the University of Washington,' show that flow cytometry correlates well with severe dysplasia. If results of flow cytometry are grossly abnormal, the patient is at risk for carcinoma of the esophagus. Efforts to develop a reliable, inexpensive screening test to detect microinvasive cancer are underway. It is studies such as these that will dispel the myths surrounding Barrett's esophagus, indicate which patients will benefit from surgery, and at the same time lead to improved results. The worth of any operation is best estimated by the long-term follow-up and the number of operations that fail and must be redone. We 9 recently reported 305 reoperations for failed antireflux procedures, of which 114 were failed Nissen repairs. The number of failed Nissen operations continues to increase and now numbers.over 145 reoperations. Those patients who require reoperation are simply the tip of the iceberg. There are many more who have gas bloat syndrome, dysphagia, inability to maintain weight, and constant epigastric pain or reflux. We realize that the number of patients having failed repairs requiring reoperation comes from a large population having had the Nissen repair. The Nissen operation consists of wrapping the lower esophagus with the cardia containing the parietal cell mass of the stomach, which is the most potent acidproducing segment of the entire gastrointestinal tract. This wrap depends on sutures in the esophagus for its integrity, yet the esophagus has no serosa and sutures must be taken carefully in the muscularis and submucosa; otherwise, through-and-through sutures may cause fistulas. When these sutures disrupt, the entire wrap may slip, and the kinds of failures of the Nissen repair that we encounter show that slippage is the most common cause of failure. The patulous repair, the obstructed repair, and various disruptions, along with a series of fistulas, constitute the remainder of these failures. The patulous repair is one of the most common causes of failure of all antireflux procedures. It is this kind of failure that can be prevented by the use of intraoperative pressure measurements. If one is measuring the pressure in a gastroesophageal junction that will allow the passage of three fingers, the machine will indicate that the pressure is zero and the surgeon has more work to do. When the repair slips, the wrap usually ends up at the junction of the upper and middle thirds of the stomach and partially obstructs the parietal cell mass. The partially obstructed parietal cell mass with food
Myths of esophagus 9
.-~~~ p; ",~,t" ..
Fig. 11. The hemostat demonstrates a huge gastric ulcer that perforated the stomach, the diaphragm, and the pericardium. The base of the ulcer was the myocardium. This patient with "true heartburn" is the only survivor of a gastropericardial fistula of whom we are aware. (From Hill LD, McCallum R, Kozarek R, Mercer D. eds. The esophagus: medical and surgical management. Philadelphia: WB Saunders, 1988.)
retention, increased acid output, poor drainage, and ischemia represents an excellent ulcerogenic preparation, as good as any that could be constructed in the experimental laboratory. This is borne out clinically by the fact that many of these individuals have gastric ulcers in the pouch. Two patients seen by us with a gastric ulcer had a perforation that produced a gastrocutaneous fistula. These patients were in the intensive care unit for several weeks before being sent for a repeat operation. The slipped Nissen may precipitate gastric ulcers that penetrate the stomach, the diaphragm, and the lung. One patient with a failed Nissen had a right gastrobronchial fistula (Fig. 10). Another patient had a transthoracic Nissen repair, which most workers now believe produces a paraesophageal hernia with all of its serious complications. This gastric ulcer penetrated through the stomach and into the left lung and produced a gastrobronchial fistula. Another patient had a posterior pene-
The Journal of
10
Thoracic and Cardiovascular
Hill
trating ulcer after a slipped Nissen in a transabdominal repair. This posterior gastric ulcer perforated the aorta. A very alert surgeon, Dr. Edwin James, was able to get a clamp on the aorta, remove a huge clot, close both the aortic and gastric openings, and salvage the patient. This is the only survivor of a gastroaortic fistula of whom we are aware. An even more challenging problem occurred when a patient was admitted to the coronary care unit with a diagnosis of myocardial infarction. The electrocardiogram showed diaphragmatic pericarditis. The patient had no other cardiac abnormalities. An alert surgeon recognized that this patient had had a Nissen repair. There was air in the pericardium and, on barium swallow, barium entered the pericardial sac. It became apparent that there was a gastropericardial fistula. At operation (Fig. II), a huge gastric ulcer was noted to have penetrated through the stomach, the diaphragm, and the pericardium. The base of the ulcer was the myocardium. This patient represents a case of true "heartburn," "heartburn" being the worst myth connected with the esophagus, since "heartburn" actually has nothing to do with the heart except in rare cases such as this. The gastric ulcer was taken down and closed, as was the diaphragm. The gastroesophageal junction was anchored to the preaortic fascias, but the patient was in such poor condition that a formal takedown of the wrap and repair could not be done. The patient survived this procedure, the only survivor of a gastropericardial fistula of whom we are aware. Since the wrap was stilI in place, however, another gastric ulcer rapidly developed and penetrated along the left gastric pedicle into the liver. At reoperation, it was necessary to divide the left gastric pedicle to close the ulcer. The patient had had a floppy Nissen, which included division of all of the short gastric vessels all the way to the antrum. The blood supply to the greater curvature had been ligated previously, and on ligation of the left gastric pedicle the entire stomach turned black, necessitating a total gastric resection. This patient has survived with an esophagojejunostomy, but these complications indicate the seriousness of the slipped Nissen type of repair. As long as an obstructed parietal cell mass is present, the patient is at risk for penetrating gastric ulcers. In most patients with a failed Nissen requiring reoperation, we were able to do an anti reflux procedure; however, in the last patient a resection was required. The fistulas were dealt with on an individual basis, and the results were better than we had anticipated, with 86% of patients reporting a good outcome. This is gratifying, because some of these patients had been operated on as
Surgery
many as five times. These patients have led us to believe that the Nissen procedure, even when properly performed, carries life-threatening risks. Surgeons using this technique should be aware of these risks. Because of the failures seen by internists, there are concerns about the durability of antireflux operations. Dr. Low and our group'? are reporting a follow-up of 167 patients having the Hill repair that starts at 15 years with a mean follow-up of 17.8 years. The 15- to 20-year follow-up is compared with the follow-up at 10 and 5 years. This landmark report shows that properly performed antireflux operations give lasting good results. Eighty-eight percent of patients had good to excellent results at 15 to 20 years. There are many more myths connected with the esophagus. I am sure that these myths will be laid to rest and myths connected with the whole of thoracic surgery (cardiac, pulmonary, as well the esophagus) will be dispelled and the truth developed. On the cutting edge of research, dispelling these myths, will be the members of this great association, the Western Thoracic. REFERENCES I. Braune W. Topographisch-anatomischer Atlas nach Durchschnitten an getrorene Cadarem. Leipzig: Kleine Ausgahe, 1878: 113-4. 2. Von Gubaroff A. Uber den Verschluss der menschlichen Magens an der Cardia. Arch Anat Physiol 1886:395. 3. Barrett NR. Hiatus hernia: a review of some controversial points. Br J Surg 1954:42:231-44. 4. Lam CR. Gahagan TH. Special comment: the myth of the short esophagus. In: :\yhus LM. Harkins HN. eds. Hernia. Philadelphia. J B Lippincott. 1964:450. 5. Barrett N. Quoted in: Hill LD. McCallum R. Kozarek R. Mercer D. OOs. The esophagus: medical and surgical management. Philadelphia: WB Saunders. 1988: 139. 6. Allison PRo Johnstone AS. The esophagus lined with gastric mucous membrane. Thorax 1953:8:87. 7. Reid BJ. Haggitt RC, Rubin CEo Barrett's esophagus and esophageal adenocarcinoma. In: Hill LD. McCallum R. Kozarek R. Mercer D. cds. The esophagus: medical and surgical management. Philadelphia: WB Saunders. 1988:157-66. 8. Tumor Prevention. Treatment and Research Group. Chengchow, Honan: Esophageal Cancer Research Group. Chinese Academy of Medical Sciences. Peking: and Linhsien County People's Hospital. Honan. Pathology of early esophageal squamous cell carcinoma. Chin Moo J 1977;3: 180-92. 9. Low DE. Mercer CD. Turner EC, Hill LD. Post Nissan syndrome. Surg Gynecol Obstet 1988:167:1-5. 10. Low DE. Anderson RP. lives R. Riccardelli E. Hill LD. Fifteen- to twenty-year results after the Hill antireftux operation. J THORAC CARDIO\ASC SLRG [In press].