Ann Thorac Surg 1998;65:1711-1714
© 1998 The Society of Thoracic Surgeons
Original articles: general thoracic
Improvement in Esophageal Varices and Liver Histology Postoperatively in Budd-Chiari Syndrome
Yukio Kuniyoshi, MDa,
Kageharu Koja, MDa,
Mituru Akasaki, MDa,
Kazufumi Miyagi, MDa,
Mituyoshi Shimoji, MDa,
Manabu Kudaka, MDa,
Tooru Uezu, MDa
a Second Department of Surgery, Faculty of Medicine, University of the Ryukyus, Okinawa, Japan
Accepted for publication March 3, 1998.
Address reprint requests to Dr Kuniyoshi, Second Department of Surgery, Faculty of Medicine, University of the Ryukyus, 207 Uehara Nishihara-Cho, Okinawa 903-01, Japan
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Abstract
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Background. In the past 17 years, 32 patients with Budd-Chiari syndrome were treated by reconstruction of the occluded inferior vena cava and reopening of the hepatic veins under femoro-femoral normothermic extracorporeal partial bypass. The mean follow-up was 8 years (range, 1.5 to 17 years).
Methods. To evaluate the benefits of our operative procedure, we compared the preoperative, early postoperative, and late postoperative endoscopic appearance of the esophageal varices and the histologic findings of the liver tissue obtained intraoperatively and at a later date.
Results. The esophageal varices found preoperatively in 29 patients (90.6%) had disappeared in 7 patients by the time of discharge, and in 2 patients they disappeared 4 to 7 years after surgery. In the remaining 20 patients, the grade of the esophageal varices was reduced markedly. Histologic examination of the liver showed cirrhosis in 22 patients, fibrosis in 9 patients, and severe congestion in 1 patient. Inspection of the liver in the late postoperative period (in 10 patients) showed improvement in centrilobular congestion and no increase in interlobular fibrosis.
Conclusions. Gradual and steady improvement of esophageal varices and hepatic fibrosis can be achieved after our operative procedure.
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Introduction
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There are several operative procedures currently used in the treatment of Budd-Chiari syndrome [1–8]. The conventional procedure has been the shunt operation [7–9]. However, most of these procedures do not reopen the occluded hepatic veins, nor do they reconstruct the occluded inferior vena cava (IVC). A reduction in portal hypertension depends on the patency of the shunt. In our operative procedure, the occluded hepatic veins were reopened and the IVC was reconstructed [1]. A radical correction of the abnormalities was achieved. Because of the poor long-term prognosis for patients with Budd-Chiari syndrome and the relative safety of our operative procedure (no procedure-related deaths were experienced), 100% of patients presenting with Budd-Chiari syndrome at our hospital are treated. This study includes 32 patients who underwent reconstruction using our method since 1979. To evaluate the benefits of our operative procedure, we studied the long-term postoperative changes in the esophageal varices (EV) and the histologic changes in the liver.
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Patients and methods
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Of the 32 patients, 10 were female and 22 were male. The ages of the patients ranged from 24 to 73 years, with an average of 47 years. Ascites was found in all patients, and EV were noted in 29 patients (90.6%). All but 1 patient suffered from chronic Budd-Chiari syndrome. The hepatic IVC was occluded in association with the obstruction of the hepatic veins. One patient was reoperated on because of occlusion of a shunt performed in another hospital. The duration of the illness ranged from 1 year to 41 years. Four patients had histories of hepatic encephalopathy, and 6 had gastroduodenal ulcers. Laboratory data revealed slight to moderate hepatic dysfunction (Table 1). Inferior cavography and right atriography were performed, and the pressure of the inferior vena cava was measured. Of the 32 patients, 28 had complete obstruction of the hepatic inferior vena cava, and 4 patients had severe stenosis of the hepatic inferior vena cava. The mean venous pressure of the infrahepatic vena cava in these patients was 25.1 cm H2O.
Through a right thoracoabdominal incision, the occluded hepatic inferior vena cava was exposed directly while we rotated the liver medially (Fig 1). The femorofemoral bypass circuit was established (Fig 2). The pericardium was excised as an autologous patch graft [11]. Before a caval venotomy, one half of the autopericardium was sutured parallel to the caval venotomy line (Fig 3b). Under femorofemoral normothermic partial bypass, a longitudinal incision was made on the occluded vena cava, and open endvenectomy was performed (Fig 3c-1). To widen the luminal space of the vena cava and to reopen the ostia of the hepatic veins, the thickened caval wall involving the hepatic tissue was partially resected. We reopened as many of the obstructed hepatic veins as possible (Fig 3c-2). Blood through the hepatic veins and the reopened hepatic veins was returned to the extracorporeal circulation circuit by suckers. The other half of the pericardial patch was then sutured (Fig 3d). During this procedure, no vascular clamps were applied to the hepatic artery or portal vein, to prevent liver ischemia. Preoperatively, 23 of the patients had only a single patent right hepatic vein. The average number of preoperative patent hepatic veins was 1.1. All three hepatic veins were reopened in 23 patients (Table 2). The average pressure in the IVC was 25.1 cm H2O preoperatively and 11.8 cm H2O at the time of discharge. The patency of the reconstructed vena cava was confirmed by cavography in all patients at discharge. Liver tissue for microscopic examination was obtained from all patients intraoperatively. There was no serious postoperative hepatic failure, and all of the patients were discharged in good condition.
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Fig 1. The standard incision consists of a thoracoabdominal incision (1) to directly visualize the occluded hapatic inferior vena cava and a right femoral incision (2) for femorofemoral partial bypass.
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Fig 2. The extracorporeal circulation circuit. During the procedure for reconstruction of the occluded inferior vena cava (IVC) or hepatic veins, blood is returned to extracorporeal circulation circuit by suckers.
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Fig 3. The occluded hepatic inferior vena cava is exposed directly (a). One side of the autopericardium is sutured before extracorporeal circulation is started (c). The end-venectomy (c-1) and excision of liver tissue (c-2) are performed to reopen the occluded hepatic veins. Finally, the other side of the autopericardium is sutured (d).
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To evaluate the benefits of our procedure in the postoperative stage, we compared the changes in the EV and the histologic findings. The endoscopic appearance of the EV was compared in the preoperative, early postoperative (at 1 to 2 months after the operation), and late postoperative periods. The histologic characteristics of the liver tissue obtained intraoperatively were compared with those of tissue obtained 1.8 to 9.1 years later (mean, 5.2) at autopsy (n = 1), by liver biopsy (n = 2), or at a subsequent operation (n = 7; hepatoma resection in 5 patients, other operations in 2). The probability of survival was calculated by the Kaplan-Meier method. Statistical analysis was done by the paired Student’s t test. A p value less than 0.05 was considered statistically significant. Data are presented as mean ± standard deviation of the mean.
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Results
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There were no operative deaths. All patients were discharged in good condition. At discharge, the patency of the reconstructed IVC and reopened hepatic veins was confirmed by venography. Postoperative follow-up ranged from 1.5 to 17 years (average, 8 years). During this period, occlusion of the IVC occurred (2 and 6 years after the procedure) in 2 patients who were successfully treated by percutaneous transluminal angioplasty or reoperation. The long-term patency of the reconstructed hepatic IVC and the reopened hepatic veins was examined and confirmed by ultrasonography and computed tomography. In the late postoperative period, 4 patients died of unrelated causes (suicide, recurrence of hepatoma, pneumonia, and intestinal perforation). In 7 patients, a hepatoma was identified; it was resected by a concomitant operation in 2 patients or a staged operation in 6 patients. The cumulative survival rates at 3, 5, 10, and 17 years after the procedure were 93.6%, 93.6%, 81.0%, and 81.0%, respectively (Fig 4). Esophagoscopy was performed from 9 months to 13.7 years after the operation (average, 4.7 years). Esophageal varices found in 29 of 32 patients (90.6%) preoperatively had disappeared in 7 patients by the time of discharge, and in a further 2 patients they disappeared 4 to 7 years after the operation.
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Fig 4. Actuarial survival of the 32 patients with Budd-Chiari syndrome who were treated using our method. The patients were followed up for a maximum of 17 years after the operation.
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Blue varices were present in 23 of 26 patients (88.4%) preoperatively, in 12 of 18 patients (66.7%) at the time of discharge, and in 7 of 14 patients (50.0%) in the late postoperative period. The red color was present in 9 of the patients (34.6%) preoperatively, and disappeared postoperatively. Extension of the EV to the upper esophagus was seen in 13 of 26 (50.0%) patients preoperatively, in 8 of 18 patients (44.5%) at the time of discharge, and in 3 of 14 patients (21.4%) in the late postoperative period. Microscopic examination of the liver tissue obtained intraoperatively showed cirrhosis in 22 patients, fibrosis in 9 patients, and congestion in 1 patient. The mean age of the patients with live congestion and fibrosis was 37.7 ± 11.5 years, and the mean age of the patients with cirrhosis was 51.0 ± 8.8 years. There was a significant correlation between the severity of fibrosis and age (p < 0.01). In the late postoperative period, liver specimens were obtained in 10 patients (at laparotomy, autopsy, or liver biopsy). Liver cirrhosis in 6 patients and liver fibrosis in 4 patients persisted but there was no progression of interlobular fibrosis. All liver specimens showed an improvement in liver architecture. There was a marked reduction in the congestion in the perisinusoidal areas and around the central veins. There was no evidence of hemosiderosis, and we also found a reduction in the number of lymphocytes.
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Comment
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Various patterns of vascular occlusion can be seen in Budd-Chiari syndrome. The type most often seen in the Orient is obstruction of the hepatic IVC in association with occlusion of the hepatic veins [1, 9–12]. The occluded hepatic veins and IVC cause liver congestion and continuous injury to the hepatic sinusoidal structures, resulting in fibrosis and cirrhosis. Parker [13] reported that cirrhosis developed within a few months after venous outflow obstruction. When clinical signs such as ascites, edema of the lower extremities, and venous dilation of the abdominal wall appear, the liver has already become severely fibrotic. The purposes of any operation are the reduction of portal hypertension and the preservation of liver function. Various operations have been devised and performed, the most popular of which is the shunt procedure [7, 8]. The long-term success of a shunt operation depends on the patency of the graft, which requires anticoagulation therapy [7, 8]. We developed an operative procedure in which we reconstruct the occluded IVC and reopen the occluded hepatic veins to achieve radical correction of the abnormalities. The overall postoperative patency rate of the reconstructed IVC and the hepatic veins was 93.7% without any anticoagulation therapy.
With the progression of hepatic fibrosis, EV develop as a part of the collateral circulation. It is important to follow up the status of the EV, because rupture of EV is a fatal complication of Budd-Chiari syndrome and one of the major factors affecting its prognosis. There are few reports on the course of EV after operation. In the patient who undergoes reoperation for occlusion of the reconstructed IVC, the first sign of restenosis is worsening of the EV. In our patients, the EV disappeared early in 7 patients and late in 2 patients. In the remaining patients, the degree of the EV was reduced markedly in the early postoperative period, and continued to improve, implying a continuous reduction in the portal pressure. The degree to which the portal pressure is reduced and the degree of improvement in the EV depends on the severity of fibrosis of the liver.
Accordingly, the EV disappeared in 6 of 9 patients (66.7%) with fibrosis, and in only 3 of 22 patients (13.6%) with cirrhosis in our series. A significant correlation exists between liver histology and age. With aging, hepatic fibrosis progresses in severity to liver cirrhosis. However, specimens obtained in the long-term follow-up period showed marked improvement of congestion and hindrance of progression of hepatic fibrosis although there is no method to quantify the degree of fibrosis. Henderson and colleagues [5] and Orloff and associates [8] reported that congestion of the liver was markedly improved and complete resolution of the liver tissue was achieved when the Budd-Chiari syndrome was treated in the acute stage, but liver fibrosis or liver cirrhosis persisted when treated in the chronic stage. Henderson and colleagues [5] reported that Budd-Chiari syndrome in the chronic stage requires liver transplantation. This study demonstrates that gradual and steady improvement of EV and hepatic fibrosis can be achieved after our operative procedure. We encountered 7 patients (21.9%) with hepatocellular carcinoma associated with Budd-Chiari syndrome. As cirrhosis is a factor that predisposes to hepatocellular carcinoma [14], our operative procedure, by preventing the progression of hepatic fibrosis to cirrhosis, should prolong the survival of patients with Budd-Chiari syndrome. Moreover, patients with Budd-Chiari syndrome should undergo the procedure before liver cirrhosis develops.
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References
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Abstract
Introduction
