Further Evaluation of the Sugiura Procedure in the Treatment of Esophageal Varices Mitsuo
Sugiura, MD, Shunji Futagawa,
MD
\s=b\ A total of 276 patients had an esophageal transection with paraesophagogastric devascularization (the Sugiura procedure) for esophageal varices from 1967 to the present; 60 procedures were prophylactic, 164 were elective, and 52 were emergency procedures. The age distribution was from 9 months to 74 years. The origin was cirrhosis in 191 patients, fibrosis in 59, extrahepatic portal vein occlusion in 18, hepatoma in five, schistosomiasis in one, Budd-Chiari syndrome in one, and carcinoma of the pancreas in one patient. The mortality within one month of operation was 5.0% in prophylactic cases, 1.8% in elective cases, and 11.5% in emergency cases (mean, 4.3%). The
actuarial seven-year survival rate was 83%. There was an obvious positive correlation between survival rate and stage of the disease. Ninety-five percent of class A (Child's classification) and 87% of class B are alive, but only 59% of class C patients are alive at the present. Six patients had recurrences of varices for a recurrence rate of 2.3%, of whom four had esophageal bleeding. It may be that recurrence of varices occurred due to incomplete devascularization of the esophagus at the diaphragm because of the necessity of two-stage operations in poor-risk patients. All survivors are free from encephalopathy. The present study reconfirmed that our method is safe and effective in controlling esophageal variceal bleeding without compromising hepatic function.
(Arch Surg 112:1317-1321, 1977)
Earlier, paraesophagogastric
have shown that esophageal transection devascularization (the Su¬ giura procedure) provided better results in controlling bleeding from esophageal varices without compromising hepatic function and causing hepatic encephalopathy.13 Since our report in 1973,' another 191 patients have been treated with the Sugiura procedure at our institution. The analysis of these cases forms the basis for this report. we
with
Accepted for publication July 27, 1977. From the Second Department of Surgery, Faculty of Medicine, University of Tokyo, Tokyo. Read before the 25th scientific meeting of the International Cardiovascular Society, Rochester NY, June 16, 1977. Reprint requests to the Second Department of Surgery, Faculty of Medicine, University of Tokyo, Hongo 7-3-1, Bunkyoku, Tokyo, Japan (Dr Sugiura).
MATERIALS AND METHODS The details of our technique have been described earlier.' In brief, the Sugiura procedure consists of transthoracic esophageal transection and devascularization, and transabdominal esophagogastric devascularization, including splenectomy (Fig 1). With this technique, the esophagus and the stomach are thoroughly stripped of all venous collaterals from the left inferior pulmonary vein to the upper half of the stomach. The thoracic and abdominal procedures can be performed in one or two stages, depending on the patients condition. When the operations are performed in one stage, it is preferable to perform the abdominal procedure transdiaphragmatically from the thoracic cavity. During the period from June 1967 through May 1977, two hundred seventy-six patients have undergone the Sugiura proce¬ dure (199 males and 77 females). The age distribution was from 9 months old to 74 years old and 80.4% of the patients were from 30 to 60 years old. The origin of the portal hypertension includes liver cirrhosis (191 patients), liver fibrosis (59 patients), extrahepatic portal vein occlusion (18 patients), hepatoma (five patients), schistosomiasis (one patient), Budd-Chiari syndrome (one patient), and carcinoma of the pancreas (one patient).
RESULTS
Among 276 patients, 219 were observed for at least one year, the longest period of observation being ten years. The operative mortality within 30 days after surgery was 4.3%. Fifty two patients were treated on an emergency basis for uncontrolled hemorrhage or within 48 hours after hemorrhage. Six of these patients died (operative mortali¬ ty was 11.5%). Elective operations were performed for prevention of recurrent hemorrhage from varices in 164 patients who had previously bled, with a mortality of 1.8%. Sixty patients underwent prophylactic operations for extremely large esophageal varices that had not bled. Their operative mortality was 5.0%. The correlation between operative mortality and underlying disease is summarized in Table 1. It appears that operative mortality for cirrhotic patients was slightly higher than for those with fibrosis, however, the difference is not statistically significant. Five patients with hepa-
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MAY '77 Survival
100 „V 9\%
BfcK
HQ%
57% 54*
50 o-o ·—--·
OP Fig
Fig 1.—Illustration of esophageal transection with paraesophagogastric devascularization (Sugiura procedure). Table
1.—Operative Mortality No. (%) of
Operative
No. of Patients 191 59
Liver cirrhosis
Liver fibrosis
Deaths 9 (4.7) 1
(1.7)
Extrahepatic portal vein occlusion
0(0) 2 (40.0) 0(0) 0(0) 0(0)
Hepatoma Pancreatic carcinoma Schistosomiasis Budd-Chiari syndrome Total
276
Table 2—Causes of
Emergency
Causes
12(4.3)
Operative
Elective
Prophylactic
Total
failure
Hepatoma Renal failure
Intraperitoneal bleeding Empyema Toxicodermia Total
12
toma were treated with our technique in an attempt to control acute esophageal variceal bleeding. Although bleeding control was successful, two of them died of progression of the hepatoma within 30 days after surgery.
One
patient
with
a
hepatoma
whose
esophageal bleeding
therapy underwent emergency Sugiura procedure along with canulation of the hepatic artery for continuous infusion of chemotherapeutic agents. This patient died 11 months postoperatively, secondary to hepatoma. One patient with pancreatic carci¬ noma was treated with the two-stage Sugiura procedure for acute esophageal bleeding. At the time of laparotomy, was
an
not controlled with conservative
2
3
4
"
39%
series
5
7 years
6
it was found that the tumor was encroaching on the portal vein, causing esophageal varices. This patient survived the procedure. The three operative deaths in the prophylactic group were due to hepatic failure. Three deaths among 164 elective patients were caused by hepatic failure, empyema secondary to anastomosis leak, and toxic dermatitis, probably due to drug allergy, respectively. Progressive hepatic failure (two patients), hepatoma (2 patients), renal failure (1 patient), and intraperitoneal bleeding (1 patient) account for six deaths in the emergency cases (Table 2). Nineteen patients displayed upper gastrointestinal bleed¬ ing after the Sugiura procedure. Causes
Hemorrhagic gastritis Recurrent varices Gastric ulcer Gastric cancer Total
Hepatic
1
5^
Sugiura Procedure Portasystemic Shunt
2.—Actuarial survival rate.
Hepatoma
Deaths
°-o-o-o——o
85% 83% 83% 83% 83%
No. (%) of Patients
10 4 1 1 3 19
(3.8) (1.5) (0.4) (0.4) (1.1) (7.2)
The most
common cause of bleeding was hemorrhagic gastritis. Four patients displayed esophageal variceal bleeding. Thus, the recurrence rate of bleeding esophageal
varices was 1.5%. The actuarial survival rate is shown in Fig 2. The overall seven-year survival rate was 83%. A positive correlation between survival rate and stage (Child's classification) of the disease is demonstrated in Tables 3 through 6. Ninety-five percent of group A patients and 87% of group patients survived, but only 59% of group C patients are alive at the time of this study. In the series of 52 emergency cases, the operative mortality for group A and would be 0%, while that for group C would be 24% (Table 6). Ages and survivals are shown in Table 7. The youngest was nine months old and the oldest was 74 years old. There were 32 late deaths. Hepatic failure and hepatoma were the most common causes of late deaths (Table 8). In this series, none of the patients had postoperative hepatic encephalo-
pathy.
All patients were subjected to endoscopie and barium swallow examinations postoperatively. Six patients had
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Table 3.—Results in 276 Patients
No.
No. (%) of No. of Patients 111
Group A
C
Deaths
No. of Late Deaths
(0)
5
Operative 0 11
15
(17.2)
(%)
of Survivors 106 (95)
_101_1 (1.0)_12_88 38 64
Table 4.—Results of 60 Prophylactic Clinical Risk Groups
by Clinical Risk Groups
(%) of Operative
No.
Group
No. of Patients
Deaths
24 20
(87) (59)
No. (%) of No. of Patients
Group
Deaths
Table 6.—Results of 52 Emergency Clinical Risk Groups
by Clinical
No. of Late Deaths
Operative
No. of Late Deaths
0(0) 0(0) 3(19)
16
Table 5.—Results of 164 Elective Operations Risk Groups
No. (%) of Survivors
Operations by
Patients
Group
A_79_OJO)_3_76 (96)
_62_1 (1.6)_9_52 (84) 6 15(65) C 23 2(8.7)
No. (%) of
Late Deaths 1
Deaths
0(0) 0(0) 6(24)
19 25
Operations by No. of
(%) of Operative
No.
No. of
No. (%) of Survivors 23 (96) 20 (100) 9 (56)
Survivors
7(88) 16(84) 14(56)
Table 8—Causes of Late Deaths
Table
7.—Ages and Survivals of Esophageal Transection With Paraesophagogastric Devascularization
Age, yr Q- 9
No. of Patients 6
Late Deaths 0
Operative Deaths 0
No. (%) of Survivors 6 (100)
276
32
12
Prophylactic
Elective
16
failure
Pancreatic carcinoma
Gastric carcinoma Pneumonia Suicide Unknown Total
232(84)
Table 9.—Recurrence of Varices and
32
18
Bleeding
No. of Patients
Operated
Esophageal transection and devascularization Simple esophageal transection
276 40
of the varices (recurrence rate was 2.3%), of whom four had bleeding. Therefore, success in controlling esophageal varices was 97.7% (Table 9). Suture insufficiencies were noted in 19 patients. However, only two patients with severe hepatic failure subsequently had empyema and died. The other 17 patients were successfully treated conservatively with nasogastric tube nutrition for several days. Postoperative suture line stricture of the esophagus was noted in nine patients. However, only two of them required repeated bougienages. All other complications were successfully treated with conservative methods. recurrence
COMMENT
ligation of varices,46 Nonshunting procedures gastric transecupper resection,7" gastroesophageal such
as
Total
Hepatoma Bleeding
10-19_7_o_o_7 goo) 20-29_12_1_0_11 (92) 30-39_53_1_2_50 (94) 40-49_96_2_14_80 (83) 50-59_73_5_12_56 (77) 60_29_3_4_22 (76) Total
Emergency
Causes
Hepatic
Survived 264 39
No. (%) of Hemorrhages
No. (%) of Recurrent Varices
4(1.5) 7(18.0)
6(2.3) 18(46.0)
tion,""' simple esophageal transection,1'1 or coronary vein ligation with splenectomy2"-' did not produce further liver damage but were associated with a high incidence of recurrent hemorrhage and fell into disfavor. In our department, during the period from 1964 to 1968, 40 patients with esophageal varices underwent simple esophageal transection (26 underwent Walker's simple
esophageal transection1'' and 14 underwent Walker's simple esophageal transection with excision of coronary veins). This procedure was also associated with a high incidence of recurrent hemorrhage, in both the immediate and late postoperative periods (Table 9). To obtain better results, it is necessary to combine extensive paraesophagogastric devascularization with simple esophageal transec¬ tion. The
key point
in
our
procedure
is
paraesophagogastric
devascularization; that is, dividing and ligating shunting
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veins between the collateral veins and the esophagus and cardia. This is done very close to the esophagus and cardia so that all venous collaterals can be preserved, which may be very important in preventing further development or recurrence of varices. The main difference between our procedure and other techniques is that extensive paraesophagogastric devascu¬ larization is performed both transthoracically and transab-
dominally. The esophagus is thoroughly stripped of all vessels from the level of the left inferior pulmonary vein to the upper half of the stomach, 6 to 7 cm along the lesser curvature
below the cardia. The upper half of the stomach contains all of the lowest shunting veins from the portal blood system to the gastroesophageal varices. Blood flow from the varices leaves by way of the bronchial veins and the azygos vein. Drainage from varices begins at the level of the left inferior pulmonary vein. These findings were demon¬ strated by direct venograph of varices during thoracic
operations.
unsatisfactory results of in the past, such as reported nonshunting procedures Tanner's operation,---1' Womack's operation,21 gastroeso¬ phageal resection,711 etc25 was that the extensive devas¬ cularization procedure was not performed transthoraci¬ cally. In our series, recurrence of variceal bleeding was noted in only six patients. All of these were poor-risk patients and the procedure was performed in two stages. The main
cause
of the
"27
of recurrence of varices was due to the incom¬ of the esophagus at the diaphragm. devascularization plete To obtain good results on varices, it is preferable to perform our procedure in one stage. If the operation is performed in two stages, it is preferable to perform the transthoracic operation first. When the thoracic operation is performed as the first staged operation, it is very important to perform devascularization from the left inferior pulmonary vein to the esophagogastric junction. Four to six weeks after the thoracic operation performed as the first operation, the second or abdominal operation is done. At this time organized thrombus inside the varices and collateral veins of the abdominal esophagus and cardia have been observed occasionally. This may be another The
cause
why recurrent bleeding of gastroesophageal varices did not occur after the thoracic operation. All of our patients with liver cirrhosis had postnecrotic or posthepatitic cirrhosis. According to the Child hepatic risk criteria, those patients who were in the class C risk group in our series were very poor operative risks. In Japan, the mortality and the incidence of encephalopathy after portasystemic shunting procedure in the postnecrotic or posthepatitic cirrhotic patients is very high. The incidence of encephalopathy in our 109 portasystemic shunting procedures was 36%·. This experience of a high incidence of encephalopathy and hepatic failure led us to select a nonshunting procedure instead of a shunting procedure. The clinical status and the chemical information suggest that esophageal transection with paraesophagogastric devascularization will be indicated for patients in whom severe hepatic failure has not been present (total bilirubin reason
value less than 5.0 mg). The high incidence of ascites, hepatic coma, and jaundice underlined the importance of patient selection in avoiding a high operative mortality. The prognosis for patients with an increased serum total bilirubin level before hemorrhage is poor. CONCLUSION 1. Esophageal transection with paraesophagogastric devascularization and splenectomy was performed in 276 patients, either prophylactically, electively, or in emer¬ gency situations. 2. Varices recurred in six patients (2.3%); one with hepatoma and five with incomplete devascularization of the esophagus at the hiatus. Disappearance of the varices was noted in 97.7% of the cases. 3. The operative mortality was 4.3% and the late mortality was 11.6%. 4. In emergency cases, the operative mortality was 11.5%. 5. Encephalopathy has been notably absent. The present study demonstrates that our technique has proved safe and effective in both stopping and preventing bleeding from varices without compromising hepatic func¬ tion, and the immediate and long-term results are much superior to those of other published methods. Our tech¬ nique is indicated in all cases except severe hepatic failure (comatous status or a total bilirubin value more than 5
mg). This investigation was partially supported by the grant in aid for Special Project Research, Ministry of Education, and a research grant from the Intractable Diseases Division, Public Health Bureau, Ministry of Health and Welfare, Tokyo.
References 1. Sugiura M, Futagawa S: A new technique for treating esophageal varices. J Thorac Cardiovasc Surg 66:677-685, 1973. 2. Sugiura M, Futagawa S, Shima F, et al: Esophageal transection with paraesophagogastric devascularization; surgical treatment of esophageal varices. Jap J Gastroenterol 9:23-28, 1974. 3. Sugiura M, Futagawa S, Ichihara S, et al: Surgical treatment of portal hypertension. Jap Med News 2410:7-11, 1970. 4. Boerema I: Chirurgische Hulp bij Bloedingen vit Varices van de Oesophagus bij Lebercirrhose en bij Het Syndroom van Banti. Ned Tijdschr Geneeskd 93:4174-4182, 1949. 5. Crile CG Jr: Transesophageal ligation of bleeding esophageal varices. Arch Surg 61:654-660, 1950. 6. Britton, RC, Crile GC Jr: Late results of transesophageal suture of bleeding esophageal varices. Surg Gynecol Obstet 117:10-14, 1963. 7. Perry JF Jr, Root HD, Miller FA, et al: Total removal of the intrathoracic esophagus and antethoracic jejunal esophageal replacement for treatment of esophageal varices due to extrahepatic portal block. Ann Surg 158:126-128, 1963. 8. Sheline GE, Clark DE, Adams WE, et al: Partial gastroesophagectomy for esophageal varices. Surg Clin North Am 31:213-227, 1951. 9. Nachlas MM: Treatment of bleeding esophageal varices by resection of the lower esophagus. Arch Surg 72:634-643, 1956. 10. Koop CE, Roddy SR: Colonic replacement of distal esophagus and proximal stomach in the management of bleeding varices in children. Ann Surg 147:17-25, 1958. 11. Phemister DB, Humphreys EM: Gastroesophageal resection and total gastrectomy in the treatment of bleeding varicose veins in Banti's syndrome. Ann Surg 126:397-406, 1947. 12. Schafer PW, Kittle CF: Partial esophagogastrectomy in the treatment of esophagogastric varices. Arch Surg 61:235-243, 1950. 13. Habif DV: Treatment of esophageal varices by partial esophagogastectomy and interposed jejunal segment. Surgery 46:212-235, 1959.
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14. Lynn HB: Colon interposition in pediatric patients with esophageal varices. Ann Surg 173:706-713, 1971. 15. Tanner NC: Discussion: Gastroduodenal hemorrhage as a surgical emergency. Proc R Soc Med 43:147-152, 1950. 16. Mikkelsen WP, Pattison AC: Upper gastric transection (Tanner operation): Its failure to control varical bleeding. Surgery 46:501-506, 1959. 17. Vosschulte K: Dissektionsligatur des Oesophagus bei Varicen der Speiserohre Infolge Pfortaderhypertonie. Chirurg Fie 28:186-189, 1957. 18. Schmitt W, Heinrich P: Zur chirurgischen Behandlung der unstillbaren Oesophagusvaricen-Blutung durch Kardiaumpflanzung. Chirurgie 34:529-537, 1963. 19. Walker RM: Esophageal transection for bleeding varices. Surg Gynecol Obstet 118:323-329, 1964. 20. Boerema I, Klopper PJ, Holscher AA: Transabdominal ligation\x=req-\ resection of the esophagus in cases of bleeding esophageal varices. Surgery 67:409-413, 1970. 21. Burns GP, Schenk WG Jr: Pilot experience with the "Boerema button" in emergency management of bleeding esophageal varices. Am J Surg 121:115-118, 1971. 22. Tanner NC: Direct operations in the treatment of complications of portal hypertension. J Int Coll Surg 36:308-314, 1961. 23. Tanner NC: Direct surgical operations for portal hypertension, in Read AE (ed): The Liver, London, Butterworth & Co, 1967, p 393. 24. Peters RM, Womach NA: Surgery of vascular distortions in cirrhosis of the liver. Ann Surg 154:432-445, 1961. 25. Hassab MA: Gastroesophageal decongestion and splenectomy in the treatment of esophageal varices in bilharzial cirrhosis: Further studies with a report on 355 operations. Surgery 61:169-176, 1967. 26. Hassab MA: Gastroesophageal decongestion and splenectomy: A method of prevention and treatment of bleeding from esophageal varices associated with bilharzial hepatic fibrosis: Preliminary report. J Int Coll Surg 41:232-248, 1964. 27. Hassab MA: Nonshunt operations in portal hypertension without cirrhosis. Surg Gynecol Obstet 131:648-654, 1970.
Discussion George J. Johnson, MD, Chapel Hill, NC: We are very much in¬ debted to Dr Sugiura and his colleagues for this update on their work on the surgical treatment of bleeding esophageal varices presented before the American Association for Thoracic Surgeons in 1973. At the University of North Carolina in Chapel Hill, we have performed an ablative operation that encompasses many of the objectives of the procedures you describe. It does not include esophageal transection, an addition that Dr Womack thought should be included. Over the past 24 years, we have performed this operation on 60 patients with a 35% mortality and a 40% late mortality. The longterm survival is 25%. Fifty percent of those that have survived have rebled. We have therefore been unable to duplicate the results that you report. Although the operative procedure seems to be similar to the one you describe, we have a 30% mortality. If we were able to decrease our two-year mortality, our long-term survival would be similar to yours. We have previously emphasized that whereas the patients continue to die after portacaval shunt, an ablative operation similar to yours is well tolerated after the initial
operative mortality. My question is similar to that I proposed to Dr Yamamoto two years ago. Why is there a difference in your early mortality and ours? As stated, the operations seem similar. Are you better technicians than we are or are these different types of patients? Is the cirrhotic any different in Japan than in the United States? Does Japanese alcohol create a different disease? Or, perhaps, the survivors you report are nonalcoholics? Edwin J. Wylie, MD, San Francisco: I comment with humility since I am sure that those of us who have been exploring techniques for portal decompression as a treatment for this syndrome for the past 25 years are impressed with the dramatic improvement in results that this new approach provides. We have
been conditioned to believe that any operation that has the objective of interrupting the venous channels in the esophageal veins was doomed to eventual failure on the assumption that reformation of collateral channels was inevitable. Our pessimism was reinforced by the numerous failures that followed transeso¬ phageal ligation of varices or the more proximal operation of gastric transection and reanastomosis. The long-term results in Dr Suguira's operation suggest that these operations failed only because they were incomplete. I think Dr Johnson's questions were particularly pertinent. If our surgeons are able to duplicate the results we have heard this morning, there would seem to be little point in pursuing decompression operations to treat bleeding esophageal varices. Worthington G., MD, Buffalo: After 25 years of working with the portacaval shunt problem, we have now come to the conclusion that the portacaval shunt is totally irrational. The problem is not the portal hypertension; it is varix hemorrhage, and most of the time, the patient needs his portal hypertension for survival. Therefore, the Sugiura procedure makes good sense and we must compliment them on their superb results. We have a small experience with another approach and that is the use of the Boerema button, a modification of the old Murphy button. This modification was developed by Prof Boerema of Amsterdam. He developed it for esophagojejunostomy after total gastrectomy, and it makes possible complete interruption of the esophagus with no sutures, performed through a simple gastro-
tomy.
Our mortality is extremely high in the 25 patients in whom we have tried this because the patients whom we have picked have all been the most severe class 3 child classification, already in hapatic failure, with jaundice, ascites, and in and out of coma. They then begin to bleed massively. However, we have had only one patient who has bled after having done the procedure, although most have died of their continuing hepatic failure. We do combine it not with splenectomy but with ligation of the splenic artery, leaving the spleen in place, and devascularization of the proximal stomach. I believe the procedure and the philosophy just expressed to you by Professor Sugiura and his associates is the route of the future. Akio Wakabayashi, MD, Irvine, Calif: Dr Sugiura said you cannot lose blood during the operation, and very often, his patients do not require blood transfusions. This is very important in order to obtain good operative results. He started this operation only for emergency cases, but after they found that none of their patients had encephalopathy, they extended their technique to patients who have large varices, which appear purple-red in color and about to rupture. His final comment was that the most important part of this operation is complete devascularization of the intrathoracic esophagus. As shown by his excellent slides, if you devascularize the lower esophagus the interior pulmonic vein down to the proximal stomach, the recurrence rate is very low. In his series, only two patients had recurrence. Subsequent venography showed one feeding collateral vein, indicating incomplete devasculariza¬ tion. So Dr Sugiura would like to reemphasize the importance of complete devascularization. President Connolly: The interesting thing is that their patients have as high portal pressures as our patients with Laennec's cirrhosis. And also, the other interesting observation that I became aware of in visiting Japan last August is that almost every surgeon in that country has switched away from portal decompression operations to the Sugiura operation.
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Sugiura, MD, Shunji Futagawa,
MD
\s=b\ A total of 276 patients had an esophageal transection with paraesophagogastric devascularization (the Sugiura procedure) for esophageal varices from 1967 to the present; 60 procedures were prophylactic, 164 were elective, and 52 were emergency procedures. The age distribution was from 9 months to 74 years. The origin was cirrhosis in 191 patients, fibrosis in 59, extrahepatic portal vein occlusion in 18, hepatoma in five, schistosomiasis in one, Budd-Chiari syndrome in one, and carcinoma of the pancreas in one patient. The mortality within one month of operation was 5.0% in prophylactic cases, 1.8% in elective cases, and 11.5% in emergency cases (mean, 4.3%). The
actuarial seven-year survival rate was 83%. There was an obvious positive correlation between survival rate and stage of the disease. Ninety-five percent of class A (Child's classification) and 87% of class B are alive, but only 59% of class C patients are alive at the present. Six patients had recurrences of varices for a recurrence rate of 2.3%, of whom four had esophageal bleeding. It may be that recurrence of varices occurred due to incomplete devascularization of the esophagus at the diaphragm because of the necessity of two-stage operations in poor-risk patients. All survivors are free from encephalopathy. The present study reconfirmed that our method is safe and effective in controlling esophageal variceal bleeding without compromising hepatic function.
(Arch Surg 112:1317-1321, 1977)
Earlier, paraesophagogastric
have shown that esophageal transection devascularization (the Su¬ giura procedure) provided better results in controlling bleeding from esophageal varices without compromising hepatic function and causing hepatic encephalopathy.13 Since our report in 1973,' another 191 patients have been treated with the Sugiura procedure at our institution. The analysis of these cases forms the basis for this report. we
with
Accepted for publication July 27, 1977. From the Second Department of Surgery, Faculty of Medicine, University of Tokyo, Tokyo. Read before the 25th scientific meeting of the International Cardiovascular Society, Rochester NY, June 16, 1977. Reprint requests to the Second Department of Surgery, Faculty of Medicine, University of Tokyo, Hongo 7-3-1, Bunkyoku, Tokyo, Japan (Dr Sugiura).
MATERIALS AND METHODS The details of our technique have been described earlier.' In brief, the Sugiura procedure consists of transthoracic esophageal transection and devascularization, and transabdominal esophagogastric devascularization, including splenectomy (Fig 1). With this technique, the esophagus and the stomach are thoroughly stripped of all venous collaterals from the left inferior pulmonary vein to the upper half of the stomach. The thoracic and abdominal procedures can be performed in one or two stages, depending on the patients condition. When the operations are performed in one stage, it is preferable to perform the abdominal procedure transdiaphragmatically from the thoracic cavity. During the period from June 1967 through May 1977, two hundred seventy-six patients have undergone the Sugiura proce¬ dure (199 males and 77 females). The age distribution was from 9 months old to 74 years old and 80.4% of the patients were from 30 to 60 years old. The origin of the portal hypertension includes liver cirrhosis (191 patients), liver fibrosis (59 patients), extrahepatic portal vein occlusion (18 patients), hepatoma (five patients), schistosomiasis (one patient), Budd-Chiari syndrome (one patient), and carcinoma of the pancreas (one patient).
RESULTS
Among 276 patients, 219 were observed for at least one year, the longest period of observation being ten years. The operative mortality within 30 days after surgery was 4.3%. Fifty two patients were treated on an emergency basis for uncontrolled hemorrhage or within 48 hours after hemorrhage. Six of these patients died (operative mortali¬ ty was 11.5%). Elective operations were performed for prevention of recurrent hemorrhage from varices in 164 patients who had previously bled, with a mortality of 1.8%. Sixty patients underwent prophylactic operations for extremely large esophageal varices that had not bled. Their operative mortality was 5.0%. The correlation between operative mortality and underlying disease is summarized in Table 1. It appears that operative mortality for cirrhotic patients was slightly higher than for those with fibrosis, however, the difference is not statistically significant. Five patients with hepa-
Downloaded From: http://archsurg.jamanetwork.com/ by a New York University User on 06/14/2015
MAY '77 Survival
100 „V 9\%
BfcK
HQ%
57% 54*
50 o-o ·—--·
OP Fig
Fig 1.—Illustration of esophageal transection with paraesophagogastric devascularization (Sugiura procedure). Table
1.—Operative Mortality No. (%) of
Operative
No. of Patients 191 59
Liver cirrhosis
Liver fibrosis
Deaths 9 (4.7) 1
(1.7)
Extrahepatic portal vein occlusion
0(0) 2 (40.0) 0(0) 0(0) 0(0)
Hepatoma Pancreatic carcinoma Schistosomiasis Budd-Chiari syndrome Total
276
Table 2—Causes of
Emergency
Causes
12(4.3)
Operative
Elective
Prophylactic
Total
failure
Hepatoma Renal failure
Intraperitoneal bleeding Empyema Toxicodermia Total
12
toma were treated with our technique in an attempt to control acute esophageal variceal bleeding. Although bleeding control was successful, two of them died of progression of the hepatoma within 30 days after surgery.
One
patient
with
a
hepatoma
whose
esophageal bleeding
therapy underwent emergency Sugiura procedure along with canulation of the hepatic artery for continuous infusion of chemotherapeutic agents. This patient died 11 months postoperatively, secondary to hepatoma. One patient with pancreatic carci¬ noma was treated with the two-stage Sugiura procedure for acute esophageal bleeding. At the time of laparotomy, was
an
not controlled with conservative
2
3
4
"
39%
series
5
7 years
6
it was found that the tumor was encroaching on the portal vein, causing esophageal varices. This patient survived the procedure. The three operative deaths in the prophylactic group were due to hepatic failure. Three deaths among 164 elective patients were caused by hepatic failure, empyema secondary to anastomosis leak, and toxic dermatitis, probably due to drug allergy, respectively. Progressive hepatic failure (two patients), hepatoma (2 patients), renal failure (1 patient), and intraperitoneal bleeding (1 patient) account for six deaths in the emergency cases (Table 2). Nineteen patients displayed upper gastrointestinal bleed¬ ing after the Sugiura procedure. Causes
Hemorrhagic gastritis Recurrent varices Gastric ulcer Gastric cancer Total
Hepatic
1
5^
Sugiura Procedure Portasystemic Shunt
2.—Actuarial survival rate.
Hepatoma
Deaths
°-o-o-o——o
85% 83% 83% 83% 83%
No. (%) of Patients
10 4 1 1 3 19
(3.8) (1.5) (0.4) (0.4) (1.1) (7.2)
The most
common cause of bleeding was hemorrhagic gastritis. Four patients displayed esophageal variceal bleeding. Thus, the recurrence rate of bleeding esophageal
varices was 1.5%. The actuarial survival rate is shown in Fig 2. The overall seven-year survival rate was 83%. A positive correlation between survival rate and stage (Child's classification) of the disease is demonstrated in Tables 3 through 6. Ninety-five percent of group A patients and 87% of group patients survived, but only 59% of group C patients are alive at the time of this study. In the series of 52 emergency cases, the operative mortality for group A and would be 0%, while that for group C would be 24% (Table 6). Ages and survivals are shown in Table 7. The youngest was nine months old and the oldest was 74 years old. There were 32 late deaths. Hepatic failure and hepatoma were the most common causes of late deaths (Table 8). In this series, none of the patients had postoperative hepatic encephalo-
pathy.
All patients were subjected to endoscopie and barium swallow examinations postoperatively. Six patients had
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Table 3.—Results in 276 Patients
No.
No. (%) of No. of Patients 111
Group A
C
Deaths
No. of Late Deaths
(0)
5
Operative 0 11
15
(17.2)
(%)
of Survivors 106 (95)
_101_1 (1.0)_12_88 38 64
Table 4.—Results of 60 Prophylactic Clinical Risk Groups
by Clinical Risk Groups
(%) of Operative
No.
Group
No. of Patients
Deaths
24 20
(87) (59)
No. (%) of No. of Patients
Group
Deaths
Table 6.—Results of 52 Emergency Clinical Risk Groups
by Clinical
No. of Late Deaths
Operative
No. of Late Deaths
0(0) 0(0) 3(19)
16
Table 5.—Results of 164 Elective Operations Risk Groups
No. (%) of Survivors
Operations by
Patients
Group
A_79_OJO)_3_76 (96)
_62_1 (1.6)_9_52 (84) 6 15(65) C 23 2(8.7)
No. (%) of
Late Deaths 1
Deaths
0(0) 0(0) 6(24)
19 25
Operations by No. of
(%) of Operative
No.
No. of
No. (%) of Survivors 23 (96) 20 (100) 9 (56)
Survivors
7(88) 16(84) 14(56)
Table 8—Causes of Late Deaths
Table
7.—Ages and Survivals of Esophageal Transection With Paraesophagogastric Devascularization
Age, yr Q- 9
No. of Patients 6
Late Deaths 0
Operative Deaths 0
No. (%) of Survivors 6 (100)
276
32
12
Prophylactic
Elective
16
failure
Pancreatic carcinoma
Gastric carcinoma Pneumonia Suicide Unknown Total
232(84)
Table 9.—Recurrence of Varices and
32
18
Bleeding
No. of Patients
Operated
Esophageal transection and devascularization Simple esophageal transection
276 40
of the varices (recurrence rate was 2.3%), of whom four had bleeding. Therefore, success in controlling esophageal varices was 97.7% (Table 9). Suture insufficiencies were noted in 19 patients. However, only two patients with severe hepatic failure subsequently had empyema and died. The other 17 patients were successfully treated conservatively with nasogastric tube nutrition for several days. Postoperative suture line stricture of the esophagus was noted in nine patients. However, only two of them required repeated bougienages. All other complications were successfully treated with conservative methods. recurrence
COMMENT
ligation of varices,46 Nonshunting procedures gastric transecupper resection,7" gastroesophageal such
as
Total
Hepatoma Bleeding
10-19_7_o_o_7 goo) 20-29_12_1_0_11 (92) 30-39_53_1_2_50 (94) 40-49_96_2_14_80 (83) 50-59_73_5_12_56 (77) 60_29_3_4_22 (76) Total
Emergency
Causes
Hepatic
Survived 264 39
No. (%) of Hemorrhages
No. (%) of Recurrent Varices
4(1.5) 7(18.0)
6(2.3) 18(46.0)
tion,""' simple esophageal transection,1'1 or coronary vein ligation with splenectomy2"-' did not produce further liver damage but were associated with a high incidence of recurrent hemorrhage and fell into disfavor. In our department, during the period from 1964 to 1968, 40 patients with esophageal varices underwent simple esophageal transection (26 underwent Walker's simple
esophageal transection1'' and 14 underwent Walker's simple esophageal transection with excision of coronary veins). This procedure was also associated with a high incidence of recurrent hemorrhage, in both the immediate and late postoperative periods (Table 9). To obtain better results, it is necessary to combine extensive paraesophagogastric devascularization with simple esophageal transec¬ tion. The
key point
in
our
procedure
is
paraesophagogastric
devascularization; that is, dividing and ligating shunting
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veins between the collateral veins and the esophagus and cardia. This is done very close to the esophagus and cardia so that all venous collaterals can be preserved, which may be very important in preventing further development or recurrence of varices. The main difference between our procedure and other techniques is that extensive paraesophagogastric devascu¬ larization is performed both transthoracically and transab-
dominally. The esophagus is thoroughly stripped of all vessels from the level of the left inferior pulmonary vein to the upper half of the stomach, 6 to 7 cm along the lesser curvature
below the cardia. The upper half of the stomach contains all of the lowest shunting veins from the portal blood system to the gastroesophageal varices. Blood flow from the varices leaves by way of the bronchial veins and the azygos vein. Drainage from varices begins at the level of the left inferior pulmonary vein. These findings were demon¬ strated by direct venograph of varices during thoracic
operations.
unsatisfactory results of in the past, such as reported nonshunting procedures Tanner's operation,---1' Womack's operation,21 gastroeso¬ phageal resection,711 etc25 was that the extensive devas¬ cularization procedure was not performed transthoraci¬ cally. In our series, recurrence of variceal bleeding was noted in only six patients. All of these were poor-risk patients and the procedure was performed in two stages. The main
cause
of the
"27
of recurrence of varices was due to the incom¬ of the esophagus at the diaphragm. devascularization plete To obtain good results on varices, it is preferable to perform our procedure in one stage. If the operation is performed in two stages, it is preferable to perform the transthoracic operation first. When the thoracic operation is performed as the first staged operation, it is very important to perform devascularization from the left inferior pulmonary vein to the esophagogastric junction. Four to six weeks after the thoracic operation performed as the first operation, the second or abdominal operation is done. At this time organized thrombus inside the varices and collateral veins of the abdominal esophagus and cardia have been observed occasionally. This may be another The
cause
why recurrent bleeding of gastroesophageal varices did not occur after the thoracic operation. All of our patients with liver cirrhosis had postnecrotic or posthepatitic cirrhosis. According to the Child hepatic risk criteria, those patients who were in the class C risk group in our series were very poor operative risks. In Japan, the mortality and the incidence of encephalopathy after portasystemic shunting procedure in the postnecrotic or posthepatitic cirrhotic patients is very high. The incidence of encephalopathy in our 109 portasystemic shunting procedures was 36%·. This experience of a high incidence of encephalopathy and hepatic failure led us to select a nonshunting procedure instead of a shunting procedure. The clinical status and the chemical information suggest that esophageal transection with paraesophagogastric devascularization will be indicated for patients in whom severe hepatic failure has not been present (total bilirubin reason
value less than 5.0 mg). The high incidence of ascites, hepatic coma, and jaundice underlined the importance of patient selection in avoiding a high operative mortality. The prognosis for patients with an increased serum total bilirubin level before hemorrhage is poor. CONCLUSION 1. Esophageal transection with paraesophagogastric devascularization and splenectomy was performed in 276 patients, either prophylactically, electively, or in emer¬ gency situations. 2. Varices recurred in six patients (2.3%); one with hepatoma and five with incomplete devascularization of the esophagus at the hiatus. Disappearance of the varices was noted in 97.7% of the cases. 3. The operative mortality was 4.3% and the late mortality was 11.6%. 4. In emergency cases, the operative mortality was 11.5%. 5. Encephalopathy has been notably absent. The present study demonstrates that our technique has proved safe and effective in both stopping and preventing bleeding from varices without compromising hepatic func¬ tion, and the immediate and long-term results are much superior to those of other published methods. Our tech¬ nique is indicated in all cases except severe hepatic failure (comatous status or a total bilirubin value more than 5
mg). This investigation was partially supported by the grant in aid for Special Project Research, Ministry of Education, and a research grant from the Intractable Diseases Division, Public Health Bureau, Ministry of Health and Welfare, Tokyo.
References 1. Sugiura M, Futagawa S: A new technique for treating esophageal varices. J Thorac Cardiovasc Surg 66:677-685, 1973. 2. Sugiura M, Futagawa S, Shima F, et al: Esophageal transection with paraesophagogastric devascularization; surgical treatment of esophageal varices. Jap J Gastroenterol 9:23-28, 1974. 3. Sugiura M, Futagawa S, Ichihara S, et al: Surgical treatment of portal hypertension. Jap Med News 2410:7-11, 1970. 4. Boerema I: Chirurgische Hulp bij Bloedingen vit Varices van de Oesophagus bij Lebercirrhose en bij Het Syndroom van Banti. Ned Tijdschr Geneeskd 93:4174-4182, 1949. 5. Crile CG Jr: Transesophageal ligation of bleeding esophageal varices. Arch Surg 61:654-660, 1950. 6. Britton, RC, Crile GC Jr: Late results of transesophageal suture of bleeding esophageal varices. Surg Gynecol Obstet 117:10-14, 1963. 7. Perry JF Jr, Root HD, Miller FA, et al: Total removal of the intrathoracic esophagus and antethoracic jejunal esophageal replacement for treatment of esophageal varices due to extrahepatic portal block. Ann Surg 158:126-128, 1963. 8. Sheline GE, Clark DE, Adams WE, et al: Partial gastroesophagectomy for esophageal varices. Surg Clin North Am 31:213-227, 1951. 9. Nachlas MM: Treatment of bleeding esophageal varices by resection of the lower esophagus. Arch Surg 72:634-643, 1956. 10. Koop CE, Roddy SR: Colonic replacement of distal esophagus and proximal stomach in the management of bleeding varices in children. Ann Surg 147:17-25, 1958. 11. Phemister DB, Humphreys EM: Gastroesophageal resection and total gastrectomy in the treatment of bleeding varicose veins in Banti's syndrome. Ann Surg 126:397-406, 1947. 12. Schafer PW, Kittle CF: Partial esophagogastrectomy in the treatment of esophagogastric varices. Arch Surg 61:235-243, 1950. 13. Habif DV: Treatment of esophageal varices by partial esophagogastectomy and interposed jejunal segment. Surgery 46:212-235, 1959.
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14. Lynn HB: Colon interposition in pediatric patients with esophageal varices. Ann Surg 173:706-713, 1971. 15. Tanner NC: Discussion: Gastroduodenal hemorrhage as a surgical emergency. Proc R Soc Med 43:147-152, 1950. 16. Mikkelsen WP, Pattison AC: Upper gastric transection (Tanner operation): Its failure to control varical bleeding. Surgery 46:501-506, 1959. 17. Vosschulte K: Dissektionsligatur des Oesophagus bei Varicen der Speiserohre Infolge Pfortaderhypertonie. Chirurg Fie 28:186-189, 1957. 18. Schmitt W, Heinrich P: Zur chirurgischen Behandlung der unstillbaren Oesophagusvaricen-Blutung durch Kardiaumpflanzung. Chirurgie 34:529-537, 1963. 19. Walker RM: Esophageal transection for bleeding varices. Surg Gynecol Obstet 118:323-329, 1964. 20. Boerema I, Klopper PJ, Holscher AA: Transabdominal ligation\x=req-\ resection of the esophagus in cases of bleeding esophageal varices. Surgery 67:409-413, 1970. 21. Burns GP, Schenk WG Jr: Pilot experience with the "Boerema button" in emergency management of bleeding esophageal varices. Am J Surg 121:115-118, 1971. 22. Tanner NC: Direct operations in the treatment of complications of portal hypertension. J Int Coll Surg 36:308-314, 1961. 23. Tanner NC: Direct surgical operations for portal hypertension, in Read AE (ed): The Liver, London, Butterworth & Co, 1967, p 393. 24. Peters RM, Womach NA: Surgery of vascular distortions in cirrhosis of the liver. Ann Surg 154:432-445, 1961. 25. Hassab MA: Gastroesophageal decongestion and splenectomy in the treatment of esophageal varices in bilharzial cirrhosis: Further studies with a report on 355 operations. Surgery 61:169-176, 1967. 26. Hassab MA: Gastroesophageal decongestion and splenectomy: A method of prevention and treatment of bleeding from esophageal varices associated with bilharzial hepatic fibrosis: Preliminary report. J Int Coll Surg 41:232-248, 1964. 27. Hassab MA: Nonshunt operations in portal hypertension without cirrhosis. Surg Gynecol Obstet 131:648-654, 1970.
Discussion George J. Johnson, MD, Chapel Hill, NC: We are very much in¬ debted to Dr Sugiura and his colleagues for this update on their work on the surgical treatment of bleeding esophageal varices presented before the American Association for Thoracic Surgeons in 1973. At the University of North Carolina in Chapel Hill, we have performed an ablative operation that encompasses many of the objectives of the procedures you describe. It does not include esophageal transection, an addition that Dr Womack thought should be included. Over the past 24 years, we have performed this operation on 60 patients with a 35% mortality and a 40% late mortality. The longterm survival is 25%. Fifty percent of those that have survived have rebled. We have therefore been unable to duplicate the results that you report. Although the operative procedure seems to be similar to the one you describe, we have a 30% mortality. If we were able to decrease our two-year mortality, our long-term survival would be similar to yours. We have previously emphasized that whereas the patients continue to die after portacaval shunt, an ablative operation similar to yours is well tolerated after the initial
operative mortality. My question is similar to that I proposed to Dr Yamamoto two years ago. Why is there a difference in your early mortality and ours? As stated, the operations seem similar. Are you better technicians than we are or are these different types of patients? Is the cirrhotic any different in Japan than in the United States? Does Japanese alcohol create a different disease? Or, perhaps, the survivors you report are nonalcoholics? Edwin J. Wylie, MD, San Francisco: I comment with humility since I am sure that those of us who have been exploring techniques for portal decompression as a treatment for this syndrome for the past 25 years are impressed with the dramatic improvement in results that this new approach provides. We have
been conditioned to believe that any operation that has the objective of interrupting the venous channels in the esophageal veins was doomed to eventual failure on the assumption that reformation of collateral channels was inevitable. Our pessimism was reinforced by the numerous failures that followed transeso¬ phageal ligation of varices or the more proximal operation of gastric transection and reanastomosis. The long-term results in Dr Suguira's operation suggest that these operations failed only because they were incomplete. I think Dr Johnson's questions were particularly pertinent. If our surgeons are able to duplicate the results we have heard this morning, there would seem to be little point in pursuing decompression operations to treat bleeding esophageal varices. Worthington G., MD, Buffalo: After 25 years of working with the portacaval shunt problem, we have now come to the conclusion that the portacaval shunt is totally irrational. The problem is not the portal hypertension; it is varix hemorrhage, and most of the time, the patient needs his portal hypertension for survival. Therefore, the Sugiura procedure makes good sense and we must compliment them on their superb results. We have a small experience with another approach and that is the use of the Boerema button, a modification of the old Murphy button. This modification was developed by Prof Boerema of Amsterdam. He developed it for esophagojejunostomy after total gastrectomy, and it makes possible complete interruption of the esophagus with no sutures, performed through a simple gastro-
tomy.
Our mortality is extremely high in the 25 patients in whom we have tried this because the patients whom we have picked have all been the most severe class 3 child classification, already in hapatic failure, with jaundice, ascites, and in and out of coma. They then begin to bleed massively. However, we have had only one patient who has bled after having done the procedure, although most have died of their continuing hepatic failure. We do combine it not with splenectomy but with ligation of the splenic artery, leaving the spleen in place, and devascularization of the proximal stomach. I believe the procedure and the philosophy just expressed to you by Professor Sugiura and his associates is the route of the future. Akio Wakabayashi, MD, Irvine, Calif: Dr Sugiura said you cannot lose blood during the operation, and very often, his patients do not require blood transfusions. This is very important in order to obtain good operative results. He started this operation only for emergency cases, but after they found that none of their patients had encephalopathy, they extended their technique to patients who have large varices, which appear purple-red in color and about to rupture. His final comment was that the most important part of this operation is complete devascularization of the intrathoracic esophagus. As shown by his excellent slides, if you devascularize the lower esophagus the interior pulmonic vein down to the proximal stomach, the recurrence rate is very low. In his series, only two patients had recurrence. Subsequent venography showed one feeding collateral vein, indicating incomplete devasculariza¬ tion. So Dr Sugiura would like to reemphasize the importance of complete devascularization. President Connolly: The interesting thing is that their patients have as high portal pressures as our patients with Laennec's cirrhosis. And also, the other interesting observation that I became aware of in visiting Japan last August is that almost every surgeon in that country has switched away from portal decompression operations to the Sugiura operation.
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