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Surgical treatment of Budd-Chiari syndrome
REVIEW
Surgical Treatment of Budd-Chiari Syndrome Andrew S. Klein and Ernesto P. Molmenti Shunting and transplantation are satisfactory methods of treating Budd-Chiari syndrome (BCS). Selection of treatment is based on the degree of hepatic injury (clinical settings), liver biopsy results, potential for parenchymal recovery, and pressure measurements. Shunting is recommended in cases of preserved hepatic function and architecture. In the presence of fulminant forms of BCS, in cases of established cirrhosis or frank fibrosis, or for patients with defined hepatic metabolic defects (e.g., protein C or protein S deficiency), liver transplantation is the treatment of choice. Nonsurgical alternatives, although encouraging, have limited long-term outcome results at the present time. In most cases of BCS, a thrombophilic disorder can be identified. However, it is important to note that postoperative vascular thrombosis has been identified in patients with BCS who do not have a definable hypercoagulable predisposition. It therefore is our practice to recommend early (<24 hours postoperatively) initiation of intravenous heparin therapy in all patients with BCS, who then undergo life-long anticoagulation with coumadin. (Liver Transpl 2003;9:891-896.)
B
udd-Chiari syndrome (BCS) has multiple causes.1 It first was reported in the literature in 1845 to 1846 by the London physician George Budd (1808 to 1882).2-4 Commonly, the term Budd-Chiari syndrome is used to refer to a spectrum of diseases with various pathological, epidemiological, and clinical characteristics of hepatic venous outflow obstruction.5 It can present in fulminant, acute, and chronic forms. The clinical syndrome encompasses structural and functional abnormalities3 in which hepatic venous outlet obstruction is associated with hepatic dysfunction, ascites, abdominal pain, and hepatosplenomegaly. In the absence of surgical therapy, median survival is less than 2 years.6,7 Ascites is the most frequent complication, whereas bleeding is the most frequent cause of death.8 A multidisciplinary approach is recommended for BCS. The primary goal of treatment is to eliminate the morbidity and mortality associated with hepatic congestion. The secondary goal is to prevent its recurrence. The diagnosis of BCS is suspected on clinical grounds, based on the presence of ascites and hepatic congestion. The initial diagnostic imaging modality often is a duplex ultrasound examination of the hepatic vasculature. Hepatic outlet occlusion then is classically confirmed by hepatic venography or mesenteric angiography with delayed portal views. Although venography
has been considered the diagnostic gold standard, the improved resolution of other imaging modalities, including computed tomography and magnetic resonance vascular imaging, has prompted some clinicians to forego hepatic venography.1,9,10 It should be recognized that partial or total inferior vena cava (IVC) occlusion secondary to compensatory caudate lobe hypertrophy is common in BCS. Therefore, imaging of the IVC and measurement of infrahepatic and suprahepatic caval pressures is essential in planning appropriate therapy. Knowledge of such pressures will determine the anatomy of the shunt to be constructed and available options.1 Hepatic venous obstruction may be located anywhere along the venous course from the liver to the heart. Very rarely is obstruction of a single hepatic vein clinically evident.8,11 Obstruction of hepatic veins often is asynchronous, leading to the coexistence of areas with various degrees of liver injury.12,13 The anatomic configuration of the major hepatic veins shows variations in approximately 10% to 15% of individuals.6,14-17 When two or more major hepatic veins become occluded, there is an associated increased pressure and reduced flow in the hepatic sinusoids. The former leads to liver enlargement, pain, and ascites. The latter is thought to produce fibrosis.8,11,18-28 The caudate lobe, which has direct venous drainage into the IVC, often undergoes compensatory hypertrophy.12,13,29 Obstruction of the portal vein is present in 10% to 20% of patients with BCS.30 Large regenerative nodules frequently seen in BCS are benign liver lesions that should be differentiated from multifocal hepatocellular carcinomas.31 It has been suggested that hepatic vein thrombosis occurs when a combination of several thrombogenic conditions exist in the context of a precipitating factor.32-39 In the Western hemisphere, most cases of BCS are associated with an underlying hematologic From the Department of Surgery, Division of Transplantation, The Johns Hopkins University School of Medicine, Baltimore, MD. Address reprint requests to Andrew S. Klein, MD, 600 N Wolfe St, Harvey 611, Baltimore, MD 21287-8611. Telephone: 410-955-5662; FAX: 410-614-2079; E-mail: [email protected] Copyright © 2003 by the American Association for the Study of Liver Diseases 1527-6465/03/0909-0001$30.00/0 doi:10.1053/jlts.2003.50156
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pathological state, part of Virchow’s triad.1,6,40-44 Primary myeloproliferative disorders are the main cause of hepatic vein thrombosis, with polycythemia rubra vera as the most frequently diagnosed entity. Necropsy studies showed a 6% incidence of hepatic vein thrombosis in individuals with polycythemia vera or agnogenic myeloid metaplasia. Hepatic vein thrombosis is seen in up to 12% of patients with paroxysmal nocturnal hemoglobinuria. Deficiency of protein C and protein S, both produced in the liver, may be difficult to diagnose in cases of liver dysfunction. Factor V Leiden leads to resistance to activated protein C. It is present in most cases associated with oral contraceptive use and pregnancy.8,33,34,45-48 BCS is associated with heterozygosity for both factor V Leiden and the G20210A mutation of the prothrombin gene.49 Antiphospholipids constitute a very diverse group of autoantibodies implicated in thrombotic events and are found in patients with liver disease (alcoholic, hepatitis C, and cirrhosis).50 Hyperhomocysteinemia also is a risk factor for BCS.51 Other factors associated with BCS include venous outflow obstruction after piggyback liver transplantation, stenoses of the proximal IVC anastomosis after classic liver transplantation, torsion of the hepatic remnant in right-lobe living related donor liver transplantation, torsion of the hepatic remnant after right hepatic lobectomies, and hormone replacement therapy in women. After the diagnosis of BCS is established, a crucial step in therapeutic planning is performing a liver biopsy. We recommend a bilobar biopsy because, as mentioned, the major hepatic veins may not be involved in similar fashion and the hepatic parenchyma may be affected unevenly. Exclusion of cirrhosis or severe fibrosis will determine the feasibility of shunting without the need for liver transplantation. The characteristic histological appearance of acute BCS is centrilobular congestion, cell loss, and centrilobular fibrosis. In untreated cases, congestion progresses to cirrhosis. The underlying cause of BCS should be confirmed and adequately addressed to allow for long-term success. Treatment is based on the degree of liver injury and its potential for recovery. Associated nonhematologic pathological states at the time of presentation also should be considered when determining the best treatment for BCS. These include, but are not limited to, the presence of cirrhosis, previous decompressive attempts, hepatocellular carcinomas, overall physiological status, and coexistent viral hepatic infection. In most cases of BCS, a thrombophilic disorder can be identified. However, it is important to note that postoperative vascular thrombosis has been identified in patients with BCS
who do not have a definable hypercoagulable predisposition. It therefore is our practice to recommend early (⬍24 hours postoperatively) initiation of intravenous heparin therapy in all patients with BCS, who then undergo life-long anticoagulation with coumadin.1,8 Early initial reports showed a mortality rate of nearly 90% within 3.5 years of the onset of symptoms in patients with BCS.13 Improved prognosis was found in younger individuals with low Child-Pugh scores, absent or easily controlled ascites, and low serum creatinine levels. Patients with portal vein thrombosis had a poor prognosis.8,30,52 Survival was associated with prothrombin time and Child-Pugh score by univariate analysis. Multivariate analysis showed an association between survival and Child-Pugh score, serum alanine aminotransferase level, and treatment with portosystemic shunting as independent prognostic factors.53 Although there are reports of successful treatment of BCS with medical management,54 most investigators consider medical treatment for the infrequent cases in which the diagnosis is made within days of the onset of hepatic vein occlusion or patients with partial venous occlusion. Such patients may benefit from an initial trial of thrombolytic therapy and long-term anticoagulation.1,55,56 Also candidates for primary medical therapy are individuals with major comorbidities and limited life expectancy who refuse invasive therapy. Two patients with BCS and paroxysmal nocturnal hemoglobinuria were treated successfully with anticoagulation alone.57 Reports can be found in the literature describing the use of thrombolytic therapy with or without associated angioplasty.33,58,59 Hepatic vein stenoses have been treated successfully on a short-term basis with percutaneous dilatation. The concomitant use of stents has provided for extended patency rates, sometimes as high as 80% to 90%.8,58,60-62 In a recent series of cases of BCS associated with IVC obstruction, the investigators performed percutaneous balloon angioplasty of the vena cava in 42 patients. Membranous occlusion of the IVC was noted in 29 of these patients, whereas segmental obstruction was seen in the remaining 13 patients. Successful dilatation was achieved in 97.6% of patients (n ⫽ 41). A single patient required stent placement. During a follow-up period of 32 ⫾ 12 months, restenosis was seen in only 1 patient (2.4%) and was addressed successfully with redilatation. Based on their observations, the investigators recommended percutaneous balloon angioplasty as the initial treatment for BCS caused by IVC occlusion.63 In cases of extensive thrombosis in which dilatation is unlikely to be effective, radiological management has
Surgical Treatment of Budd-Chiari Syndrome
been geared toward transjugular intrahepatic portosystemic shunt (TIPS) placement.64 The development of TIPS placed with the aid of radiological imaging has allowed for treatment of even those patients with obliterated hepatic veins. Some found that TIPS is highly effective and has excellent associated long-term survival in patients with BCS uncontrolled by medical therapy.65 A recent series found that a group of patients with TIPSs that were maintained patent had prolonged transplantation-free survival.66 TIPS is of use either as a primary or secondary method to relieve venous obstruction in BCS.1,67-69 It provides immediate symptomatic relief, and its long-term patency can be maintained by means of repeated revisions, if necessary. In cases of complete occlusion of the three hepatic veins, the standard TIPS technique can be laborious. In a recent report, two cases of BCS (one acute and the other hyperacute in onset) were managed using a direct transcaval approach.64 In this approach, a shunt was placed directly between the intrahepatic IVC and the portal vein. One of the patients underwent transplantation 15 months after placement of the shunt, whereas the other patient retained good hepatic function with a patent stent after 24 months. Others also have reported similar approaches.70 Disadvantages of TIPS include that it may impose technical complications at the time of transplantation. Although thrombosis is uncommon with anticoagulation treatment, revisions are required in approximately 70% of cases. The efficacy of this therapeutic modality will be defined further after results of controlled studies are available.8,71-74 In our own experience,1 we have observed that both shunting and liver transplantation are effective therapies associated with 5-year survival rates of 75% or greater. Selection of treatment is based on the degree of hepatic injury (clinical settings), liver biopsy results, potential for parenchymal recovery, and pressure measurements. Shunting is recommended in cases of preserved hepatic function and architecture. After successful decompression of the splachnic circulation, hepatic recovery has been documented even in the presence of fibrosis.75 Historically, two types of mesenteric-systemic shunts have been used: mesocaval and mesoatrial shunts. Both have good results.1,8,40,41,76-78 Mesocaval shunts are used routinely, except in cases in which there is stenosis or obstruction of the IVC. Functional IVC obstruction is defined as a luminal area compromise greater than 75% or a pressure gradient between the infrahepatic vena cava and right atrium greater than 15 mm Hg. Others have suggested gradient pressures of 20 mm Hg or more should be used to define obstruction.
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In such instances, stent insertion in the IVC before mesocaval shunting is one management option. In such cases, care should be taken to ensure that the stent lies within the intrahepatic segment of the IVC to facilitate an eventual liver transplantation. Mesoatrial shunts, although effective, have an increased risk for thrombosis compared with mesocaval shunts and have been placed very infrequently in recent years. Instead, such cases are treated more frequently with transplantation. Surgical or invasive radiological reintervention has been found to allow for satisfactory secondary patency rates. Surgical shunt revision, angioplasty, and stenting are available alternatives to maintain long-term patency.1,8,35,40,44,52,55,62,75,77-82 A recent series showed that a side-to-side portocaval shunt, when placed early in cases of hepatic vein occlusion alone causing BCS, led to reversal of liver damage, prolonged survival, correction of hemodynamic abnormalities, and good quality of life.83 Although highly effective, in our opinion, this type of shunting can impose technical difficulties in cases that eventually require liver transplantation. Moreover, most surgeons with experience in the management of BCS believe that caudate lobe hypertrophy presents a technical contraindication to a direct portal vein–-IVC anastomosis. Cavoatrial shunting in combination with a side-to-side portocaval shunt in cases of BCS with IVC occlusion had similar salutary results. These investigators did not achieve satisfactory results with mesoatrial shunts.83 In another series of 49 patients who underwent surgery for BCS, the investigators observed that the treatment of choice was combined endovascular intervention and shunting.84 Series with large numbers of patients during the past two decades have confirmed that surgical shunting is effective in both prolonging survival and relieving symptoms.44,75-77,85-89 In our experience, both mesocaval (performed remote from the porta hepatis) and mesoatrial shunt placement have been effective treatments and have not imposed unnecessary technical demands or increased morbidity or mortality at the time of subsequent transplantation.1 In the presence of fulminant forms of BCS (⬃5% of cases) or in cases of established cirrhosis or frank fibrosis, liver transplantation clearly is the treatment of choice.1,90 The basis of this recommendation is that shunting usually leads to further hepatic decompensation in these instances.1,41,91,92 Transplantation also is the treatment of choice in cases of BCS associated with an inborn error of metabolism that can be cured with hepatic replacement, such as antithrombin III, protein S, or protein C deficiencies.1,91 Liver transplantation for BCS is associated with acceptable morbidity. Long-
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term survival after transplantation, although good, often is dependent on factors not directly related to transplantation itself, such as progression of the underlying hematologic disease.3 Liver transplantation in selected cases of BCS has a reported 10-year survival rate of approximately 75%. A recent series of 19 patients reported a survival rate after transplantation of more than 80% with a median follow-up of 89 months. Others have reported survival rates between 54% and 87%.1,3,8,41,55,77,78,90-96 Although recurrence of hepatic vein thrombosis occurs infrequently after transplantation, recent series have reported incidences of 0% to 10%. There are no data that suggest a potential immunosuppression-associated exacerbation of underlying malignant or premalignant conditions.3,8,41,55,93,95,96 Even in cases in which liver transplantation is the treatment of choice, many times, decompression of the established portal hypertension is required because of prolonged waiting times for suitable cadaveric livers or acute bleeding episodes. In such cases, when choosing a decompressive procedure, the surgeon should consider which one would cause the least degree of technical difficulty at the time of a subsequent transplantation.1,97 In conclusion, shunting and transplantation are satisfactory methods of treating BCS. Anatomic, physiological, and clinical conditions dictate which one of the two procedures should be performed. Nonsurgical alternatives, such as TIPS placement, have shown encouraging short-term results. Their long-term efficacy is still being evaluated. Most patients, irrespective of the primary treatment, will require anticoagulation therapy for life.
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tion in patients with Budd-Chiari syndrome. J Vasc Interv Radiol 2002;13:193-199. Ochs A, Sellinger M, Haag K, Noldge G, Herbst EW, Walter E, et al. Transjugular intrahepatic porto-systemic stent-shunt (TIPS) in the treatment of Budd-Chiari syndrome. J Hepatol 1993;18:217-225. Rogoupolos A, Gavelli A, Sakai H, NcNamara M, Huguet C. Transjugular intrahepatic portosystemic shunt for Budd-Chiari syndrome after failure of surgical shunting. Arch Surg 1995;130: 227-228. Wittie AM, Koll LJ, Veenendaal R, Lamers CB, van Hoek B. Hepatic vein stenting for Budd-Chiari syndrome. Am J Gastroenterol 1997;92:498-501. Seki S, Sakaguchi H, Kobayashi S, Kitada T, Nakamura K, Yamada R. Transjugular intrahepatic portosystemic shunt in combination with oral anticoagulant for Budd-Chiari syndrome. Hepatogastroenterology 2001;48:1447-1449. Cobo F, Cervantes F, Garcia-Pagan JC. [Budd-Chiari syndrome associated with chronic myeloproliferative syndromes: Analysis of 6 cases]. Med Clin (Barcelona) 1996;107:660-663. Blum U, Rossle M, Haag K. Budd-Chiari syndrome: Technical, hemodynamic, and clinical results of treatment with transjugular intrahepatic portosystemic shunt. Radiology 1995;197:805-811. Ganger DR, Klapman JB, McDonald V. Transjugular intrahepatic portosystemic shunt (TIPS) for Budd-Chiari syndrome or portal vein thrombosis: Review of indications and problems. Am J Gastroenterol 1999;94:603-608. Watanabe H, Shinzawa H, Saito T. Successful emergency treatment with a transjugular intrahepatic portosystemic shunt for life-threatening Budd-Chiari syndrome with portal thrombotic obstruction. Hepatogastroenterology 2000;47:839-841. Klein A, Cameron J. Diagnosis and management of the BuddChiari syndrome. Am J Surg 1990;160:128-133. Ahn S, Yellin A, Sheng F, Colonna JO, Goldstein LI, Busuttil RW. Selective surgical therapy of the Budd-Chiari syndrome provides superior survivor rates than conservative medical management. J Vasc Surg 1987;5:28-37. Bismuth H, Sherlock DJ. Portasystemic shunting versus liver transplantation for the Budd-Chiari syndrome. Ann Surg 1991; 214:581-589. Shaked A, Goldstein R, Klintmalm G, Drazan K, Husberg B, Busuttil RW. Portosystemic shunt versus orthotopic liver transplantation for the Budd-Chiari syndrome. Surg Gynecol Obstetr 1992;174:453-459. Vembrux AC, Mitchell SA, Savader SJ, Lund GA, Trerotola SO, Newman JS, Klein AS, et al. Long-term results with the use of metallic stents in the inferior vena cava for treatment of BuddChiari syndrome. J Vasc Intervent Radiol 1994;5:411-416. Kohli V, Pande GK, Dev V. Management of hepatic venous outflow obstruction. Lancet 1993;342:718-722.
81. Orloff MJ, Johansen KH. Treatment of Budd-Chiari syndrome by side-to-side portacaval shunt: Experimental and clinical results. Ann Surg 1978;188:494-512. 82. Vons C, Smadja C, Bourstyn E. Results of portal systemic shunts in Budd-Chiari syndrome. Ann Surg 1986;203:366-370. 83. Orloff MJ, Daily PO, Orloff SL, Girard B, Orloff MS. A 27-year experience with surgical treatment of Budd-Chiari syndrome. Ann Surg 2000;232:340-352. 84. Xu B, Zhou Y, Jing Z, Cao G, Zhong J. Endovascular intervention versus traditional bypass for treatment of Budd-Chiari syndrome [in Chinese]. Zhonghua Wai Ke Za Zhi 2002;40:423426. 85. Cameron J, Herlong F, Sanfey H, Boitnott J, Kaufman SL, Gott VL, Maddrey WC. The Budd-Chiari syndrome: Treatment by mesenteric-systemic venous shunts. Ann Surg 1983;198:335-346. 86. Orloff M, Orloff M, Daily P. Long-term results of treatment of Budd-Chiari syndrome with portal decompression. Arch Surg 1992;127:1182-1188. 87. Tilanus HV. Budd-Chiari syndrome. Br J Surg 1995;82:10231030. 88. Kugelmas M. Budd-Chiari syndrome. Treatment options and the value of liver transplantation. Hepatogastroenterology 1998; 45:1381-1386. 89. Emre A, Kalayci G, Ozden I, Bilge O, Acarli K, Kaymakoglu S, et al. Mesoatrial shunt in Budd-Chiari syndrome. Am J Surg 2000;179:304-308. 90. Putnam CW, Porter KA, Wile R, Reid HA, Starzl TE. Liver transplantation for Budd-Chiari syndrome. JAMA 1976;236: 1142-1143. 91. Lang H, Oldhafer K, Kupsch E, Ringe B, Pichlmayr R. Liver transplantation for Budd-Chiari syndrome: Palliation or cure? Transplant Int 1994;7:115-119. 92. Knoop M, Lemmens H-P, Lengrehr J, Bechstein WO, Blumhardt G, Schattenfroh N, et al. Liver transplantation for BuddChiari syndrome. Transplant Proc 1994;26:3577-3578. 93. Halff G, Todo S, Tzakis A, Gordon RD, Starzl TE. Liver transplantation for the Budd-Chiari syndrome. Ann Surg 1990;211: 43-49. 94. Scharsschmidt BF. Human liver transplantation: Analysis of data in 540 patients from 4 centers. Hepatology 1984;4:955-1015. 95. Campbell DA, Rolles K, Jamieson N. Hepatic transplantation with perioperative and long term anticoagulation as treatment for BuddChiari syndrome. Surg Gynecol Obstet 1988;166:511-518. 96. Hemming AW, Langer B, Greig P. Treatment of Budd-Chiari syndrome with portosystemic shunt or liver transplantation. Am J Surg 1996;171:176-181. 97. Ryu RK, Durham JD, Krysl J, Shrestha R, Everson GT, et al. Role of TIPS as a bridge to hepatic transplantation in BuddChiari syndrome. J Vasc Intervent Radiol 1999;10:799-805.
Surgical Treatment of Budd-Chiari Syndrome Andrew S. Klein and Ernesto P. Molmenti Shunting and transplantation are satisfactory methods of treating Budd-Chiari syndrome (BCS). Selection of treatment is based on the degree of hepatic injury (clinical settings), liver biopsy results, potential for parenchymal recovery, and pressure measurements. Shunting is recommended in cases of preserved hepatic function and architecture. In the presence of fulminant forms of BCS, in cases of established cirrhosis or frank fibrosis, or for patients with defined hepatic metabolic defects (e.g., protein C or protein S deficiency), liver transplantation is the treatment of choice. Nonsurgical alternatives, although encouraging, have limited long-term outcome results at the present time. In most cases of BCS, a thrombophilic disorder can be identified. However, it is important to note that postoperative vascular thrombosis has been identified in patients with BCS who do not have a definable hypercoagulable predisposition. It therefore is our practice to recommend early (<24 hours postoperatively) initiation of intravenous heparin therapy in all patients with BCS, who then undergo life-long anticoagulation with coumadin. (Liver Transpl 2003;9:891-896.)
B
udd-Chiari syndrome (BCS) has multiple causes.1 It first was reported in the literature in 1845 to 1846 by the London physician George Budd (1808 to 1882).2-4 Commonly, the term Budd-Chiari syndrome is used to refer to a spectrum of diseases with various pathological, epidemiological, and clinical characteristics of hepatic venous outflow obstruction.5 It can present in fulminant, acute, and chronic forms. The clinical syndrome encompasses structural and functional abnormalities3 in which hepatic venous outlet obstruction is associated with hepatic dysfunction, ascites, abdominal pain, and hepatosplenomegaly. In the absence of surgical therapy, median survival is less than 2 years.6,7 Ascites is the most frequent complication, whereas bleeding is the most frequent cause of death.8 A multidisciplinary approach is recommended for BCS. The primary goal of treatment is to eliminate the morbidity and mortality associated with hepatic congestion. The secondary goal is to prevent its recurrence. The diagnosis of BCS is suspected on clinical grounds, based on the presence of ascites and hepatic congestion. The initial diagnostic imaging modality often is a duplex ultrasound examination of the hepatic vasculature. Hepatic outlet occlusion then is classically confirmed by hepatic venography or mesenteric angiography with delayed portal views. Although venography
has been considered the diagnostic gold standard, the improved resolution of other imaging modalities, including computed tomography and magnetic resonance vascular imaging, has prompted some clinicians to forego hepatic venography.1,9,10 It should be recognized that partial or total inferior vena cava (IVC) occlusion secondary to compensatory caudate lobe hypertrophy is common in BCS. Therefore, imaging of the IVC and measurement of infrahepatic and suprahepatic caval pressures is essential in planning appropriate therapy. Knowledge of such pressures will determine the anatomy of the shunt to be constructed and available options.1 Hepatic venous obstruction may be located anywhere along the venous course from the liver to the heart. Very rarely is obstruction of a single hepatic vein clinically evident.8,11 Obstruction of hepatic veins often is asynchronous, leading to the coexistence of areas with various degrees of liver injury.12,13 The anatomic configuration of the major hepatic veins shows variations in approximately 10% to 15% of individuals.6,14-17 When two or more major hepatic veins become occluded, there is an associated increased pressure and reduced flow in the hepatic sinusoids. The former leads to liver enlargement, pain, and ascites. The latter is thought to produce fibrosis.8,11,18-28 The caudate lobe, which has direct venous drainage into the IVC, often undergoes compensatory hypertrophy.12,13,29 Obstruction of the portal vein is present in 10% to 20% of patients with BCS.30 Large regenerative nodules frequently seen in BCS are benign liver lesions that should be differentiated from multifocal hepatocellular carcinomas.31 It has been suggested that hepatic vein thrombosis occurs when a combination of several thrombogenic conditions exist in the context of a precipitating factor.32-39 In the Western hemisphere, most cases of BCS are associated with an underlying hematologic From the Department of Surgery, Division of Transplantation, The Johns Hopkins University School of Medicine, Baltimore, MD. Address reprint requests to Andrew S. Klein, MD, 600 N Wolfe St, Harvey 611, Baltimore, MD 21287-8611. Telephone: 410-955-5662; FAX: 410-614-2079; E-mail: [email protected] Copyright © 2003 by the American Association for the Study of Liver Diseases 1527-6465/03/0909-0001$30.00/0 doi:10.1053/jlts.2003.50156
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pathological state, part of Virchow’s triad.1,6,40-44 Primary myeloproliferative disorders are the main cause of hepatic vein thrombosis, with polycythemia rubra vera as the most frequently diagnosed entity. Necropsy studies showed a 6% incidence of hepatic vein thrombosis in individuals with polycythemia vera or agnogenic myeloid metaplasia. Hepatic vein thrombosis is seen in up to 12% of patients with paroxysmal nocturnal hemoglobinuria. Deficiency of protein C and protein S, both produced in the liver, may be difficult to diagnose in cases of liver dysfunction. Factor V Leiden leads to resistance to activated protein C. It is present in most cases associated with oral contraceptive use and pregnancy.8,33,34,45-48 BCS is associated with heterozygosity for both factor V Leiden and the G20210A mutation of the prothrombin gene.49 Antiphospholipids constitute a very diverse group of autoantibodies implicated in thrombotic events and are found in patients with liver disease (alcoholic, hepatitis C, and cirrhosis).50 Hyperhomocysteinemia also is a risk factor for BCS.51 Other factors associated with BCS include venous outflow obstruction after piggyback liver transplantation, stenoses of the proximal IVC anastomosis after classic liver transplantation, torsion of the hepatic remnant in right-lobe living related donor liver transplantation, torsion of the hepatic remnant after right hepatic lobectomies, and hormone replacement therapy in women. After the diagnosis of BCS is established, a crucial step in therapeutic planning is performing a liver biopsy. We recommend a bilobar biopsy because, as mentioned, the major hepatic veins may not be involved in similar fashion and the hepatic parenchyma may be affected unevenly. Exclusion of cirrhosis or severe fibrosis will determine the feasibility of shunting without the need for liver transplantation. The characteristic histological appearance of acute BCS is centrilobular congestion, cell loss, and centrilobular fibrosis. In untreated cases, congestion progresses to cirrhosis. The underlying cause of BCS should be confirmed and adequately addressed to allow for long-term success. Treatment is based on the degree of liver injury and its potential for recovery. Associated nonhematologic pathological states at the time of presentation also should be considered when determining the best treatment for BCS. These include, but are not limited to, the presence of cirrhosis, previous decompressive attempts, hepatocellular carcinomas, overall physiological status, and coexistent viral hepatic infection. In most cases of BCS, a thrombophilic disorder can be identified. However, it is important to note that postoperative vascular thrombosis has been identified in patients with BCS
who do not have a definable hypercoagulable predisposition. It therefore is our practice to recommend early (⬍24 hours postoperatively) initiation of intravenous heparin therapy in all patients with BCS, who then undergo life-long anticoagulation with coumadin.1,8 Early initial reports showed a mortality rate of nearly 90% within 3.5 years of the onset of symptoms in patients with BCS.13 Improved prognosis was found in younger individuals with low Child-Pugh scores, absent or easily controlled ascites, and low serum creatinine levels. Patients with portal vein thrombosis had a poor prognosis.8,30,52 Survival was associated with prothrombin time and Child-Pugh score by univariate analysis. Multivariate analysis showed an association between survival and Child-Pugh score, serum alanine aminotransferase level, and treatment with portosystemic shunting as independent prognostic factors.53 Although there are reports of successful treatment of BCS with medical management,54 most investigators consider medical treatment for the infrequent cases in which the diagnosis is made within days of the onset of hepatic vein occlusion or patients with partial venous occlusion. Such patients may benefit from an initial trial of thrombolytic therapy and long-term anticoagulation.1,55,56 Also candidates for primary medical therapy are individuals with major comorbidities and limited life expectancy who refuse invasive therapy. Two patients with BCS and paroxysmal nocturnal hemoglobinuria were treated successfully with anticoagulation alone.57 Reports can be found in the literature describing the use of thrombolytic therapy with or without associated angioplasty.33,58,59 Hepatic vein stenoses have been treated successfully on a short-term basis with percutaneous dilatation. The concomitant use of stents has provided for extended patency rates, sometimes as high as 80% to 90%.8,58,60-62 In a recent series of cases of BCS associated with IVC obstruction, the investigators performed percutaneous balloon angioplasty of the vena cava in 42 patients. Membranous occlusion of the IVC was noted in 29 of these patients, whereas segmental obstruction was seen in the remaining 13 patients. Successful dilatation was achieved in 97.6% of patients (n ⫽ 41). A single patient required stent placement. During a follow-up period of 32 ⫾ 12 months, restenosis was seen in only 1 patient (2.4%) and was addressed successfully with redilatation. Based on their observations, the investigators recommended percutaneous balloon angioplasty as the initial treatment for BCS caused by IVC occlusion.63 In cases of extensive thrombosis in which dilatation is unlikely to be effective, radiological management has
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been geared toward transjugular intrahepatic portosystemic shunt (TIPS) placement.64 The development of TIPS placed with the aid of radiological imaging has allowed for treatment of even those patients with obliterated hepatic veins. Some found that TIPS is highly effective and has excellent associated long-term survival in patients with BCS uncontrolled by medical therapy.65 A recent series found that a group of patients with TIPSs that were maintained patent had prolonged transplantation-free survival.66 TIPS is of use either as a primary or secondary method to relieve venous obstruction in BCS.1,67-69 It provides immediate symptomatic relief, and its long-term patency can be maintained by means of repeated revisions, if necessary. In cases of complete occlusion of the three hepatic veins, the standard TIPS technique can be laborious. In a recent report, two cases of BCS (one acute and the other hyperacute in onset) were managed using a direct transcaval approach.64 In this approach, a shunt was placed directly between the intrahepatic IVC and the portal vein. One of the patients underwent transplantation 15 months after placement of the shunt, whereas the other patient retained good hepatic function with a patent stent after 24 months. Others also have reported similar approaches.70 Disadvantages of TIPS include that it may impose technical complications at the time of transplantation. Although thrombosis is uncommon with anticoagulation treatment, revisions are required in approximately 70% of cases. The efficacy of this therapeutic modality will be defined further after results of controlled studies are available.8,71-74 In our own experience,1 we have observed that both shunting and liver transplantation are effective therapies associated with 5-year survival rates of 75% or greater. Selection of treatment is based on the degree of hepatic injury (clinical settings), liver biopsy results, potential for parenchymal recovery, and pressure measurements. Shunting is recommended in cases of preserved hepatic function and architecture. After successful decompression of the splachnic circulation, hepatic recovery has been documented even in the presence of fibrosis.75 Historically, two types of mesenteric-systemic shunts have been used: mesocaval and mesoatrial shunts. Both have good results.1,8,40,41,76-78 Mesocaval shunts are used routinely, except in cases in which there is stenosis or obstruction of the IVC. Functional IVC obstruction is defined as a luminal area compromise greater than 75% or a pressure gradient between the infrahepatic vena cava and right atrium greater than 15 mm Hg. Others have suggested gradient pressures of 20 mm Hg or more should be used to define obstruction.
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In such instances, stent insertion in the IVC before mesocaval shunting is one management option. In such cases, care should be taken to ensure that the stent lies within the intrahepatic segment of the IVC to facilitate an eventual liver transplantation. Mesoatrial shunts, although effective, have an increased risk for thrombosis compared with mesocaval shunts and have been placed very infrequently in recent years. Instead, such cases are treated more frequently with transplantation. Surgical or invasive radiological reintervention has been found to allow for satisfactory secondary patency rates. Surgical shunt revision, angioplasty, and stenting are available alternatives to maintain long-term patency.1,8,35,40,44,52,55,62,75,77-82 A recent series showed that a side-to-side portocaval shunt, when placed early in cases of hepatic vein occlusion alone causing BCS, led to reversal of liver damage, prolonged survival, correction of hemodynamic abnormalities, and good quality of life.83 Although highly effective, in our opinion, this type of shunting can impose technical difficulties in cases that eventually require liver transplantation. Moreover, most surgeons with experience in the management of BCS believe that caudate lobe hypertrophy presents a technical contraindication to a direct portal vein–-IVC anastomosis. Cavoatrial shunting in combination with a side-to-side portocaval shunt in cases of BCS with IVC occlusion had similar salutary results. These investigators did not achieve satisfactory results with mesoatrial shunts.83 In another series of 49 patients who underwent surgery for BCS, the investigators observed that the treatment of choice was combined endovascular intervention and shunting.84 Series with large numbers of patients during the past two decades have confirmed that surgical shunting is effective in both prolonging survival and relieving symptoms.44,75-77,85-89 In our experience, both mesocaval (performed remote from the porta hepatis) and mesoatrial shunt placement have been effective treatments and have not imposed unnecessary technical demands or increased morbidity or mortality at the time of subsequent transplantation.1 In the presence of fulminant forms of BCS (⬃5% of cases) or in cases of established cirrhosis or frank fibrosis, liver transplantation clearly is the treatment of choice.1,90 The basis of this recommendation is that shunting usually leads to further hepatic decompensation in these instances.1,41,91,92 Transplantation also is the treatment of choice in cases of BCS associated with an inborn error of metabolism that can be cured with hepatic replacement, such as antithrombin III, protein S, or protein C deficiencies.1,91 Liver transplantation for BCS is associated with acceptable morbidity. Long-
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term survival after transplantation, although good, often is dependent on factors not directly related to transplantation itself, such as progression of the underlying hematologic disease.3 Liver transplantation in selected cases of BCS has a reported 10-year survival rate of approximately 75%. A recent series of 19 patients reported a survival rate after transplantation of more than 80% with a median follow-up of 89 months. Others have reported survival rates between 54% and 87%.1,3,8,41,55,77,78,90-96 Although recurrence of hepatic vein thrombosis occurs infrequently after transplantation, recent series have reported incidences of 0% to 10%. There are no data that suggest a potential immunosuppression-associated exacerbation of underlying malignant or premalignant conditions.3,8,41,55,93,95,96 Even in cases in which liver transplantation is the treatment of choice, many times, decompression of the established portal hypertension is required because of prolonged waiting times for suitable cadaveric livers or acute bleeding episodes. In such cases, when choosing a decompressive procedure, the surgeon should consider which one would cause the least degree of technical difficulty at the time of a subsequent transplantation.1,97 In conclusion, shunting and transplantation are satisfactory methods of treating BCS. Anatomic, physiological, and clinical conditions dictate which one of the two procedures should be performed. Nonsurgical alternatives, such as TIPS placement, have shown encouraging short-term results. Their long-term efficacy is still being evaluated. Most patients, irrespective of the primary treatment, will require anticoagulation therapy for life.
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