High incidence of recurrence andhematologic events following livertransplantation for Budd–Chiari syndrome

Budd–Chiari syndrome (BCS) is characterized byhepatic venous outflow obstruction involving thehepatic vein, inferior vena cava (IVC) or both. Thepresentation of BCS may be acute or chronic,typically associated with signs and symptoms ofportal hypertension (1). Hepatic congestion result-ing from outflow obstruction leads to hepaticnecrosis and ischemic injury, with progressivecentrilobular fibrosis and eventual cirrhosis (1).Most cases of BCS in the Western hemisphere areassociated with underlying myeloproliferative dis-ease (MPD) or other hematologic disorders with

inherent thrombogenic propensity (1–5). Treatmentof BCS consists of medical and surgical interven-tions (1–3). Medical management includes treatingthe underlying hematologic disorder, anticoagula-tion and the use of diuretics for control of ascites(1, 5, 6). Percutaneous balloon angioplasty, stentingand thrombolytic therapy may be beneficial inselected cases with acute presentation (1, 7, 8).Porto-systemic shunting converts the portal veininto an outflow tract for the liver, thus relievinghepatic congestion and necrosis (2, 9). Recently,transjugular intrahepatic portosystemic shunt

Cruz E, Ascher NL, Roberts JP, Bass NM, Yao FY. High incidence ofrecurrence and hematologic events following liver transplantation forBudd–Chiari syndrome.Clin Transplant 2005: 19: 501–506. ª Blackwell Munksgaard, 2005

Abstract: Background: Most cases of Budd–Chiari syndrome (BCS) inWestern countries are related to underlying hematologic diseases withinherent thrombogenic propensity. We evaluated the long-term outcome,risks for recurrent disease, and other hematologic complications followingorthotopic liver transplantation (OLT) for BCS.Methods: Clinical data from 11 consecutive patients with BCS whounderwent OLT were retrospectively reviewed. Four patients had a priortransjugular intrahepatic portosystemic shunt and one had a surgical shuntprocedure. All patients were started on intravenous heparin within the first24 h following OLT. All except one patient who had protein C deficiencywere maintained on long-term oral anticoagulation.Results: The Kaplan–Meier survival rates at 1, 5 and 10 yr were 81, 65and 65%, respectively. Three patients developed BCS recurrence, inclu-ding two who died as a consequence of rapid graft failure within daysafter OLT. Three patients developed other thrombotic events, includingsplenic vein thrombosis associated with gastric variceal hemorrhagerequiring splenectomy, portal vein thrombosis and pulmonary embolism.Four patients experienced severe bleeding complications within 7 d afterOLT requiring exploratory laparotomy. One patient died after transfor-mation of polycythemia vera to acute myelogenous leukemia at 2.1 yrafter OLT.Conclusion: We observed a high incidence of recurrent BCS and compli-cations related to the underlying hematologic disorder or anticoagulationafter OLT for BCS. The present series also included the first two cases ofrapid recurrence of BCS and graft failure within days after OLT.

Elizabeth Cruza, Nancy L Ascherb,John P Robertsb, Nathan M Bassa

and Francis Y Yaoa,b

a Division of Gastroenterology, Department of

Medicine, and b Division of Transplantation,

Department of Surgery, University of California,

San Francisco, CA, USA

Key words: bleeding complications –

Budd–Chiari syndrome – orthotopic liver

transplantation – recurrence – thrombosis

Corresponding author: Francis Y. Yao, M.D.,

Division of Gastroenterology, Department of

Medicine, University of California, San Francisco,

Box 0538, 513 Parnassus Avenue, Room S-357,

San Francisco, CA 94143-0538, USA.

Tel.: +1 415 514 0332; fax: +1 415 476 0659;

e-mail: yaofyk@itsa.ucsf.edu

Accepted for publication 17 March 2005

Clin Transplant 2005: 19: 501–506 DOI: 10.1111/j.1399-0012.2005.00374.xCopyright ª Blackwell Munksgaard 2005

501

(TIPS) has also been shown to be an effectivealternative therapy among patients with BCSrefractory to medical therapy (10, 11).BCS accounts for about 1% of all indications for

orthotopic liver transplantation (OLT) in theUnited States (12) and in Europe (13). The usualcriteria for OLT for patients with BCS includefulminant disease presentation, advanced fibrosisor cirrhosis by liver biopsy and deterioration ofliver function despite medical or surgical interven-tions (1–3). While satisfactory patient survivalfollowing OLT for BCS has been reported (13–21), information on the risks for recurrent BCS andother hematologic complications after OLT is stilllimited.In the present study, we reviewed the results of

OLT in 11 consecutive patients with BCS andcompared the outcome with other published data.We focussed on hematologic complications follow-ing OLT, including recurrent BCS, otherthrombotic events, bleeding associated with anti-coagulation and hematologic malignancies.

Patients and methods

Among 1162 adult patients over the age of 18 yrwho underwent OLT at the University of Califor-nia San Francisco between January 1988 andJanuary 2002, 11 patients (1%) had BCS as theprimary indication for OLT. Clinical data of these

patients were collected retrospectively from acomputerized database and by review of theirmedical charts.

The individual baseline clinical characteristicsare presented in Table 1. To summarize, there werenine females and two males with a median age of48 yr (range 27–62 yr). Polycythemia vera (PCV)was the most common underlying hematologicdisorder, found in six patients (55%). One patienthad protein C deficiency. The type of MPD couldnot be specified in two patients. The remaining twopatients had no known underlying hematologicdiagnosis. Three of the patients with PCV also hada history of oral contraceptive use.

The interval from the diagnosis of BCS to theday of OLT ranged from 1 month to 18 yr. Sixpatients were on chronic oral anticoagulation for3–156 months prior to OLT. Anticoagulation wasdiscontinued after 14 yr for patient no. 5 followingan episode of upper gastrointestinal bleeding at1 yr prior to OLT. Four other patients were not onoral anticoagulation prior to OLT because of acutepresentation of BCS within 4 weeks before OLT intwo patients and for unknown reasons in the othertwo patients.

All 11 patients had ascites requiring diuretictherapy at the time of OLT. Five patients had ahistory of hepatic encephalopathy treated withneomycin or lactulose or both. Pertinent laborat-ory data within 24 h prior to OLT were recorded.

Table 1. Baseline characteristics for the 11 patients in the present cohort who underwent liver transplantation

PatientGender(M/F)

Age(years)

Hematologicdiagnosis

Duration ofBCS diagnosisbefore OLT(months)

Anticoagulationbefore OLT(time before OLT)

Other treatments(time before OLT) HE

Bilirubin(mg/dL) INR

Creatinine(mg/dL)

1 F 27 PCV 24 Warfarin (15 months) SSPCS (26 months),hydroxyurea, phlebotomy

Yes 1.5 1.4 1.4

2 F 54 Protein Cdeficiency

48 Warfarin (39 months) TIPS (11 months) No 2.3 1.3 1.3

3 F 52 PCV 2 Warfarin (2 months) TIPS (9 d) No 15.9 1.9 0.64 F 56 PCV 1 Intraveneous heparin No 8.1 2.6 2.55 F 47 PCV 216 Warfarin for 14 yr

before stopped1 yr before OLT

Phlebotomy (7 yr) No 1.8 1.5 1.1

6 F 58 PCV 18 Warfarin(18 months)

Hydroxyurea (5 yr) No 7.0 3.6 1.5

7 M 29 MPDa 8 TIPS Yes 3.6 1.3 1.98 F 55 MPDa 1 Intraveneous

heparin (1 month)Peritoneovenous shunt Yes 1.7 1.1 3.9

9 M 62 Unknown 6 Failed TIPS attempt No 1.2 1.7 1.710 F 54 PCV 2 TIPS (2 months),

hydroxyurea (9 yr)Yes 4.9 1.5 0.9

11 F 50 Unknown 48 Warfarin (4 yr) Yes 1.2 1.2 0.8

BCS, Budd–Chiari syndrome; OLT, orthotopic liver transplantation; HE, hepatic encephalopathy; INR, international normalized ratio for prothrombin time; PCV, polycyt-hemia vera; SSPCS, side-to-side portal caval shunt; TIPS, transjugular intrahepatic portosystemic shunt; MPD, myeloproliferative disorder.a The type of myeloproliferative disorder could not be further specified in two patients (patient nos 7 and 8).

Cruz et al.

502

The bilirubin level ranged from 1.5 to 8.1 mg/dLwith a median of 2.3 mg/dL. The serum creatinineranged from 0.9 to 2.5 mg/dL with a median of1.4 mg/dL. The last set of values for the interna-tional normalized ratio for prothrombin time(INR) before OLT was presented in Table 1.

Four patients underwent TIPS between 9 d and11 months prior to OLT. This procedure wascomplicated by severe intra-abdominal bleedingwith rapid deterioration of liver function in patientno. 3, resulting in OLT 9 d after the procedure.Patient no. 9 had attempted TIPS that failed fortechnical reasons. Patient no. 1 had a side-to-sideportocaval shunt performed at 26 months prior toOLT. Patient no. 8 had a peritoneovenous shuntplaced for control of ascites (Table 1).

Results

The outcome of the individual patient is summar-ized in Table 2. All 11 patients were started onintravenous heparin within the first 24 h afterOLT. The single patient with protein C deficiencywas not maintained on long-term anticoagulationas OLT would cure this disorder. The other eightpatients who survived the initial hospitalization forOLT were maintained on chronic warfarin

therapy. Six patients were also placed on hydroxy-urea and aspirin after OLT.

Patient and graft survival

The Kaplan–Meier survival rates at 1, 5 and 10 yrwere 81, 65 and 65%, respectively. The respectivegraft survival rates were identical to patient survi-val. The median follow-up was 4.7 yr amongsurvivors with a range of 0.3–11 yr. Nine of 11patients survived the initial hospitalization forOLT. The two early deaths were both because ofrecurrent BCS. The first patient (patient no. 3,Table 2) was found to have extensive thrombosisinvolving the hepatic veins, portal vein and IVC onDoppler ultrasound examination performed withinthe first 24 h after OLT. She experienced severegraft failure and died 2 d after OLT. Patient no. 4developed early recurrent BCS and underwent liverre-transplantation 4 d after primary OLT. Pathol-ogy of the first liver graft revealed extensive intra-hepatic thrombi consistent with rapid recurrence ofBCS. This patient developed multi-organ failureand died 16 d after the second OLT. At autopsy, alarge organizing thrombus was found in the IVC,associated with extensive central venous necrosis inthe liver. Patient no. 5 died at 27 months after OLT

Table 2. Summary of outcome after liver transplantation for the 11 patients in the present cohort

PatientThrombotic event(time after OLT)

Treatment forthrombotic eventin addition toanticoagulation

Bleeding event(time after OLT)

Treatment forbleeding event(time after OLT) Outcome

1 Splenic vein thrombosiswith gastric varicealbleeding at 7 and 9 d

Splenectomy at 11 d Splenic vein thrombosiswith gastric varicealbleeding at 7 and 9 d

Alive at 23 months

2 Intra-abdominalbleeding on day 3

Exploratorylaparotomy

Alive at 94 months

3 Recurrent BCS(within 1 d)

Died 3 d after OLTfrom graft failure

4 Recurrent BCS(within 2 d)

Re-OLT at 4 d after OLT Died 16 d afterre-OLT from multi-organ failure andrecurrent BCS of thesecond graft

5 Pulmonary embolism(intraoperative)

Intra-abdominal bleedingon day 6 from hepaticartery anastomosis

Exploratorylaparotomy

AML at 24 monthsDied at 27 months

6 Portal vein thrombosis(2 months)

Thrombolytic therapywith urokinase

Intra-abdominalbleeding on day 2

Exploratorylaparotomy

Alive at 3 months

7 Intra-abdominalbleeding on day 3

Exploratorylaparotomy

Alive at 9 months

8 Alive at 132 months9 Alive at 100 months

10 Alive at 100 months11 Recurrent BCS

(26 months)Placement of TIPS Alive at 29 months

OLT, orthotopic liver transplantation; BCS, Budd–Chiari syndrome; re-OLT, liver re-transplantation; TIPS, transjugular intrahepatic portosystemic shunt.

Liver transplant for Budd–Chiari syndrome

503

following transformation of PCV to acute myelo-genous leukemia at 24 months after OLT.

Thrombotic complications

In addition to the two early deaths because ofrecurrent BCS, four other patients had thromboticevents following OLT (Table 2). Patient no. 1 wasfound to have splenic vein thrombosis presentingwith gastric variceal bleeding at 7 and 9 d respect-ively, after OLT, requiring splenectomy at 11 dafter OLT. Patient no. 5 experienced pulmonaryembolism intra-operatively but recovered withoutsequelae. Patient no. 6 developed portal veinthrombosis two months after OLT despite beingon oral anticoagulation with therapeutic INRlevels. This patient was given thrombolytic therapywith urokinase and was subsequently maintainedon low molecular weight heparin subcutaneously.Patient no. 11 developed recurrent BCS at26 months after OLT associated with sub-thera-peutic INR levels and non-compliance. Thispatient did well after a TIPS procedure.

Bleeding complications associated with anticoagulation

Not including patient no. 1 who had splenic veinthrombosis presenting with gastric variceal bleed-ing, four other patients had major intra-abdominalhemorrhage within the first 7 d after OLT requi-ring exploratory laparotomy for control of bleed-ing (Table 2). All patients had uneventful recoveryfrom these bleeding episodes and were subse-quently maintained on anticoagulation therapy.

Discussion

We presented our single-center experience withOLT for BCS in 11 patients and reviewed the datafrom eight series published since 1990 (14–21),which are summarized in Table 3. The 65%actuarial patient survival rates at 5 and 10 yr afterOLT in the present study were similar to thatreported in most other published series, althoughSrinivasan et. al. (20) reported an exceptional 5 yrsurvival rate of 95% (Table 3). For patients withBCS because of antithrombin III, protein S orprotein C deficiency, OLT also cures the inbornerror of metabolism and eliminates the associatedthrombogenic propensity. Other patients with BCSand MPD such as PCV continue to be at risk forthrombosis after OLT and require long-term anti-coagulation. The incidence of recurrent BCSfollowing OLT ranged from 0% to about 10% inthese studies (14–21). Including information fromisolated case reports (22, 23), recurrence of BCS

was diagnosed between 5 months and 7 yr afterOLT and was most often because of sub-therapeu-tic anticoagulation (14, 18, 21). Jamieson et al. (15)reported a patient who received no anticoagulationafter OLT and developed recurrent BCS at 28 dafter OLT. In addition to recurrent BCS, somepostoperative thrombotic events, including pul-monary embolism, portal vein thrombosis andhepatic artery thrombosis, have culminated indeath or graft loss (14, 15, 18–21) (Table 3). Earlyadministration of anticoagulation therapy toreduce the risk for thrombosis in these patientsneeds to be carefully balanced against bleedingcomplications associated with anticoagulationespecially in the early postoperative period. Melearet al. (21) reported a low incidence of thromboticevents with no major bleeding complications afterOLT for BCS using anti-platelet agents includinghydroxyurea and aspirin without warfarin in themajority of their patients with MPD.

Compared to prior studies, there are severalunusual aspects of our findings. First, early recur-rence of BCS within hours to days after OLTleading to rapid graft failure was observed in twopatients and confirmed by histopathology of theliver graft. One of the two patients died withoutre-OLT, whereas the other patient suffered fromrecurrent BCS again in the second liver graft anddied eventually of multi-organ failure. To ourknowledge, these are the first two reported casesthat clearly demonstrated rapid recurrence of BCSwithin days after OLT and led to rapid graft losseven when anticoagulation was initiated within24 h after OLT. Some investigators recommendedanticoagulation to be commenced within 6 h afterOLT (21), despite substantial bleeding risk duringthe early postoperative period. Second, the overallincidence of all types of thrombotic events in ourseries (55%) appears to be significantly higher thanother reports (Table 3), although the small samplesize may be a source of bias. We also observed ahigh incidence of serious postoperative bleedingrequiring surgical intervention. Only three of 11patients in our series were completely free ofhematologic complications after OLT. However,these complications were not the focus of some ofthe published series. Consequently, their trueincidence could have been underestimated in thesestudies.

One patient in our series died after transforma-tion from PCV to acute myelogenous leukemia at2 yr after OLT. This patient was diagnosed withPCV at 7 yr and BCS at 18 yr, prior to OLT.Srinivasan et al. (20) also described a patient withPCV who developed acute leukemia 8 yr afterOLT. It has been suggested that patients with PCV

Cruz et al.

504

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Liver transplant for Budd–Chiari syndrome

505

have a near-normal life expectancy in the first 10 yrsince the initial diagnosis. However, the risk formyelofibrosis and acute leukemia increases there-after, estimated to be 10% at 15 yr and 25% at25 yr (3). Consequently, the duration of PCV maybe an important factor in considering OLT forthese patients (1–3).In conclusion, we observed a high incidence of

disease recurrence as well as other associatedhematologic complications in patients with BCSwho underwent OLT. Our series also included thefirst two cases of rapid recurrence of BCS leadingto graft failure within days after OLT, despiteanticoagulation initiated within 24 h after OLT.Correcting the thrombogenic propensity of theunderlying hematologic disorder remains the keyto the management of these patients, althoughanticoagulation carries a substantial bleeding riskin the early postoperative period.

Acknowledgements

The work was supported in part by a grant from theNational Institute of Health to the University of California,San Francisco Liver Center (P30DK26743).

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