Successful Treatment of Hepatic Venocclusive Disease in a Bone Marrow Transplant Patient With Side-to-Side Portacaval Shunt
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1 GASTROENTEROLOGY 1987;92: Successful Treatment of Hepatic Venocclusive Disease in a Bone Marrow Transplant Patient With Side-to-Side Portacaval Shunt JEFFREY A. MURRAY, DOUGLAS R. LABRECQUE, ROGER D. GINGRICH, KEVIN C. PRINGLE, and FRANK A. MITROS Departments of Internal Medicine, Surgery, and Pathology, University of Iowa Hospitals and Clinics Iowa City, Iowa Hepatic venocclusive disease developed in a 14-yrold white girl after allogenic bone marrow trans~ plantation from an HLA-identical sibling donor. Clinical diagnosis of venocclusive disease was based on the development of ascites, hepatomegaly, and jaundice 3 wk after transplantation. Current treatment of hepatic venocclusive disease is ineffective. The pathophysiology of the hepatic lesion suggests that construction of a side-to-side portacaval shunt should be beneficial in relieving the ascites and preventing further hepatic damage. Because the ascites was refractory to medical therapy and she was clinically deteriorating, a side-to-side portacaval shunt was performed. Histologic examination of a liver biopsy specimen obtained at surgery documented the presence of venocclusive disease. Postoperatively, the patient diuresed and returned to her baseline weight. One year after surgery the patient was doing well, her weight was stable, and she was being maintained on salt restriction alone. While the resolution of ascites and improvement of hepatic function in our patient after side-to-side portacaval shunt does not guarantee that such an approach will be uniformly successful, it should serve to encourage others to consider such therapy for this frequently devastating complication of chemoradiation therapy. Venocclusive disease of the liver, a fibrous obliteration of the small hepatic venules, is a common Received July 7, Accepted September 25, Address requests for reprints to: Douglas R. LaBrecque, M.D., Associate Professor, Department of Internal Medicine, Division of Gastroenterology-Hepatology, University of Iowa Hospitals and Clinics, Iowa City, Iowa by the American Gastroenterological Association /87/$3.50 complication of the chemoradiation therapy used to prepare patients for bone marrow transplantation (1). To date, no effective therapy has been described for this condition and the mortality from venocclusive disease has been noted to be as high as 32% (2). The following case report describes the occurrence of severe venocclusive disease in a bone marrow transplant recipient who was treated successfully with a side-to-side portacaval shunt. Case Report A 14-yr-old white girl was determined to have acute myelomonocytic leukemia on November 21, She received induction therapy of intravenous cytosine arabinoside and doxorubicin in two cycles plus intrathecal cytosine arabinoside. Maintenance chemotherapy consisting of three cycles of intravenous doxorubicin and cytosine arabinoside plus oral 6-thioguanine was completed in March In July and August 1984, she received sequence two of the remission maintenance protocol consisting of cytosine arabinoside, adriamycin, and 5-azacytidine. Her course was complicated by neutropenic fevers as well as acute aspergillus rhinitis. Her leukemia recurred in June At that time, mild liver abnormalities were noted with an aspartate aminotransferase (AST) of 51 lull (normal, ), alanine aminotransferase of 45 lull (normal, )' alkaline phosphatase of 120 lull (normal, ), and total bilirubin of 0.5 mg/dl (normal, ). A second remission was induced with intravenous VP-16 (etoposide), doxorubicin, and cytosine arabinoside in June and July On August 19, 1985 she was admitted for allogenic bone marrow transplantation from an HLA-identical sibling donor. Conditioning chemoradiation therapy consisted of cytosine arabinoside, 3 g/m2 every 12 h for the 4 days just before transplantation; cyclophosphamide, 90 mg/kg on day 6 before transplantation; and total body irradiation of 200 cgy/fraction given as six fractions over the 3 days just before transplantation.
2 1074 MURRAY ET AL. GASTROENTEROLOGY Vol. 92, No.4 Table 1. Laboratory Values Days from transplant AST AP B ALB AST, aspartate aminotransferase, normal lull; AP, alkaline phosphatase, normal lull; B, total bilirubin, normal mg/dl; ALB, albumin, normal gldl. 0 Date of side-to-side portacaval shunt. Prophylaxis for graft-versus-host disease consisted of methotrexate, 15 mg/m 2 on day 1 and 10 mg/m 2 on days 3, 6, and 11 after transplantation. Daily methylprednisolone, 0.4 mg/kg, was started on day 8 after transplantation. Admission laboratory values obtained before conditioning chemoradiation therapy included an AST of 189 lull, a total bilirubin of 0.7 mg/dl, and an alkaline phosphatase of 151 lull. Pretransplant evaluation of her hepatitis revealed negative serologies for hepatitis B surface antigen, hepatitis B e antigen, hepatitis B e antibody, hepatitis A virus antibody-immunoglobulin M, and cytomegalovirus (acute and convalescent). Antibodies to hepatitis B surface antigen were present. Physical examination on admission revealed a weight of 40.0 kg, a blood pressure of 110/58, and a pulse of 95 beats per minute. No stigmata of chronic liver disease were noted. The abdomen was soft, the spleen was not palpable, and the liver was 9 cm in span. No ascites or extremity edema were noted. On August 29, 1985 she underwent allogeneic bone marrow transplantation from an HLA-identical sibling donor. Her posttransplant course was complicated by Escherichia coli bacteremia and neutropenic fevers, which were treated with various antibiotics including tobramycin, carbenicillin, vancomycin, and ceftazidime. By day 21 after transplant she had evidence of marrow engraftment but had also gained 10 kg with concurrent ascites and pleural effusions. Thoracentesis and paracentesis revealed serosanguineous fluid. The ascites had a total protein of 3.3 g/dl and lactate dehydrogenase of 309 lull. Cultures for' aerobic and anaerobic bacteria, mycobacteria, and fungi were negative. Because of intense abdominal pain and recurrent fevers, she had three subsequent therapeutic paracenteses with similar findings. Repeated cultures were negative. An hepatic ultrasound on day 25 revealed massive ascites and normal, nondilated portal and splenic veins and inferior vena cava. Colloid liver-spleen imaging on day 32 revealed hepatomegaly with decreased radiotracer uptake in a uniform distribution. By day 35, the patient had developed tense ascites and severe, diffuse abdominal pain. Abdominal computed tomography scan 50 days after transplantation revealed only massive ascites. No focal lesions were noted within the hepatic parenchyma. Laboratory data including AST, alkaline phosphatase, total bilirubin, and body weight are illustrated in Table 1. Of note, she was not azotemic during this period and continued to maintain normal serum values for blood urea nitrogen and creati- nine throughout her hospital course. Despite intense medical management, including a 500-mg oral sodium restriction, spironolactone up to 300 mg/day, intermittent furosemide, and constant bedrest, she showed no evidence of effective diuresis. Urine sodium to potassium ratios were never >1 and urine Na+ was generally <10 meq/l. Because of refractory ascites and continued clinical deterioration, it was elected to perform a side-to-side portacaval shunt on day 50. This had to be postponed because of Staphylococcus epidermidis bacteremia that resolved after Hickman catheter replacement. On day 62, tense ascites remained, she weighted 50 kg, and serum albumin was 2.4 g/dl. At surgery, 7 L of brown ascitic fluid as well as a thick fibrin peel on the anterior peritoneal wall were noted. Before portacaval shunt, the inferior mesenteric vein had a pressure of 18 cmhzo and the inferior vena cava had a pressure of 3 cmh 2 0. Histologic examination of a liver biopsy specimen obtained at surgery revealed moderate centrilobular sinusoidal congestion as well as focal central vein intimal changes with luminal compromise typical of hepatic venocclusive disease (Figure 1). Surrounding the involved veins, moderate hepatocellular necrosis was present. No evidence of cytomegalovirus was seen on histologic stains. Immunohistologic stains to rule out other viral hepatitis infections were not performed because of the patient's negative serologic status with regard to hepatitis B, hepatitis A, and cytomegalovirus. After the operation, the patient diuresed with significant weight loss (Figure 2) on sodium restriction and spironolactone (400 mg/day tapered to 100 mg/day). The patient was discharged on day 74 with no clinical evidence of graftversus-host disease and a stable weight of 37 kg. She was seen in follow-up on days 110 and 143. Her weight was 36 kg and she was doing very well. Ascites and abdominal pain had resolved completely. On a recent clinical follow-up, 238 days after surgery and 300 days after transplantation, she had continued to do well without any sodium restriction or diuretic therapy. She had no clinical evidence of ascites or edema and had achieved a weight of 38.8 kg. Laboratory evaluation at that time revealed the following; AST, 59 IU/L; total bilirubin, 0.7 mg/dl; alkaline phosphatase, 158 IU/L; and albumin, 3.8 g/dl. Discussion Hepatic venocclusive disease was originally described in patients ingesting herbal or bush teas that contained pyrolizidine alkaloids (3). More recently, venocclusive disease has been associated with preparative chemoradiation therapy for bone marrow transplantation. Specifically, venocclusive disease has been described as a complication of chemotherapy with 5-thioguanine (4), cytosine arabinoside (1), azathioprine (5), urethane (5), dacarbazine (7), carmustine (8), mitomycin C (9), and dimethylbusulfan (10). Shulman et al. (10) suggested that high-dose regimens may be more strongly associated with the presence of venocclusive disease than low- or moderate-dose regimens. These same authors have theorized that chemoradiation therapy
3 April 1987 PORTACAVAL SHUNT FOR VENOCCLUSIVE DISEASE 1075 Figure 1. Typical involved central vein. The dark-staining material (arrow) is the native collagen associated with the central vein, and is normal. A subintimal fibrous proliferation largely occludes the central lumen, which contains three red cells and a lymphocyte. There is hepatocellular necrosis (upper left). About 50%-60% of the central veins showed similar changes. Trichrome, X250. causes damage to both centrilobular hepatocytes and venules. A previous review demonstrated hepatocyte damage without venule damage when antineoplastic agents were used alone (11). However, other reports in the literature have demonstrated that in early venocclusive disease there is severe damage to terminal venules but not pericentral hepatocytes (10). The incidence of hepatic venocclusive disease among patients undergoing bone marrow transplantation has recently been reported to be 21% (2). Jaundice, fluid accumulation, and right upper quadrant pain were the three most common clinical features. In our patient, a clinical diagnosis of venocclusive disease was based on the presence of ascites, hepatomegaly, and jaundice that developed 3 wk after bone marrow transplantation. The diagnosis was confirmed by liver biopsy at the time of surgery. Using multivariate analysis, it has been shown (12) that the relative risk of developing venocclusive disease is 3.4 times higher if the AST was elevated before transplantation. Our patient's AST was more than fourfold increased before her pretransplant chemoradiation. As previously alluded to, morbidity and mortality from hepatic venocclusive disease can be significant. In the series by McDonald et al. (2), venocclusive - 60 ~ 50 * x * transplant x shunt 30 _L1~0~0--~170~2~0~~30~~4~0--5~0~~60~~7~0~8~0~~9ftO-"10~0~ 10 Days from Transplant Figure 2. Rapid accumulation in weight (in kilograms) after bone marrow transplantation (*) as well as rapid loss of weight after portacaval shunt (x).
4 1076 MURRAY ET AL. GASTROENTEROLOGY VoL 92, No.4 disease contributed to the deaths of 17 of 52 patients (32%) and persisted as a major medical problem in another 7 (13%) who later died of causes other than liver disease. As demonstrated in our patient, medical management is often not successful in relieving the tense ascites and hepatomegaly. In the study by McDonald et al. (2) only 53% of patients improved spontaneously or with medical therapy. Of those who did not improve in the first 4-6 wk, the morbidity and mortality of the disease did not appear to be improved by intensive medical management of the ascites. Because current medical treatment of venocclusive disease is unsatisfactory, other approaches must be sought. The pathophysiology of the hepatic damage produced by obstruction to hepatic venous outflow is primarily related to pressure necrosis caused by greatly increased sinusoidal pressure. The necrosis is augmented by local hypoxia due to decreased hepatic arterial flow. In our patient, Figure 2 demonstrates that the patient started to gain weight in the first week after transplantation, and had gained ~3 kg by day 10. It is worth noting that bilirubin, AST, albumin, and alkaline phosphatase were relatively normal at this time, suggesting that intrasinusoidal hypertension and not zone 3 necrosis was the initial major lesion. The Leveen shunt is often recommended for treatment of ascites that is intractable to medical therapy. This approach, however, requires the placement of a catheter between the abdomen and the superior vena cava with the attendant risks of infection in an immunocomprorhised patient. The Leveen shunt also fails to do anything to reduce the continued liver damage. Given the lack of acceptable therapies, it seems reasonable to consider construction of a side-to-side portosystemit shunt in patients with venocclusive disease of the liver who have intractable a~cites. This therapeutic approach will eliminate the ascites and should prevent further liver damage by.relieving the hepatic congestion. Resolution of the ascites should also improve nutritic;m as well as fluid and electrolyte balance. Surgical construction of a side-to-side porto systemic shunt has begun to playa major role in the treatment of the Budd-Chiari syndrome (obstruction of the major hepatic veins) (13). Because of the similar pathophysiology of the liver damage in hepatic venocclusive disease, it was decided to construct a side-to-side portacaval shunt in our patient. After operation, our patient had dramatic weight loss with resolution of ascites. A brief review of the literature documents at least three previous instances in which a portosystemic shunt was performed in patients with hepatic venocclusive disease. In 2 patients with suspected herbal tea poisoning, a side-to-side shunt was per- formed with resultant complete resolution of ascites (11). In these 2 patients, no mention is made of follow-up liver function tests. The third patient had received azathioprine after renal transplantation and was subsequently treated with an end-to-side shunt. The patient's course was complicated by transient hyperbilirubinemia and encephalopathy (15) and we would not recommend an end-to-side portacaval shunt. The shunt is intended to prevent further hepatic damage by reducing hepatic pressure via the creation of a low-pressure outflow tract for the congested liver. An end-to-side shunt, which completely eliminates the only available outflow tract from the liver, would not be expected to be beneficial and might well be detrimental. Such end-to-side shunts have been uniformly unsuccessful in treating the Budd-Chiari syndrome (16). It is important to note that our patient's AST and alkaline phosphatase levels have remained mildly elevated despite dramatic resolution of the ascites after porto systemic shunt. This may indicate lowgrade graft-versus-host disease, although she has no other manifestations of such. She also had evidence of hepatitis before the transplant and chronic hepatitis may account for her elevated AST. Thus, although the shunt appears to have been successful in alleviating her ascites and preventing further hepatic damage from pericentral congestion, she may yet develop additional liver difficulties. More patients will need to be shunted and further prospective observations recorded to determine whether side-to-side portacaval shunts will have a long-term beneficial effect on the natural history of venocclusive disease. The encouraging results in our patient should serve to stimulate further efforts to treat this frequently devastating side effect of bone marrow transplantation. Note added in proof. The patient was seen 497 days after transplantatioh (435 days postshuntj. There was no ascites present and all liver studies were within the normal range, including an AST of 17 lull, an alkaline phosphatase of 98 lull, and a total bilirubin of 0.4 mg/dl. References 1. Berk PD, Popper H, Krueger GRF, et al Veno-occlusive disease of the liver after allogeneic bone marrow transplantation. Ann Intern Med 1979;90: McDonald GB, Sharma P, Matthews DE, et al The clinical course of 53 patients with venocclusive disease of the liver after bone marrow transplantation. Transplantation 1985; 39: Bras G. Aspects of hepatic vascular diseases. In: Gall EA, Mostofi FK, eds. The liver. Baltimore: Williams & Wilkins, 1973: Gill RA, Onstad GR, Cardamone JM, et al Hepatic venocclusive disease caused by 6-thioguanine. Ann Intern Med 1982;96:58-60.
5 April 1987 PORT ACAV AL SHUNT FOR VENOCCLUSIVE DISEASE Marubbio AT, Danielson B. Hepatic veno-occlusive disease in a renal transplant patient receiving azathioprine. Gastroenterology 1975:69: Meachem GC, Tillotson FW, Heinle RW. Liver damage after prolonged urethane therapy. Am J Clin PathoI1952;22: Asbury RF, Rpsenthal SAS, Descalzi ME, et al. Hepatic venocclusive disease due to DTIC. Cancer 1980;45: Mcintyre RE, Magidson JG, Austin GE, et al. Fatalvenoocclusive qisease of the liver following high dose 1,3-bis (2 chloroethyl)-l-nitrosourea (BCNU) and autologous bone marrow transplantation. Am J Clin Pathol 1981;75: Gottfried MR, Sudilovsky O. Hepatic veno-occlusive disease after high dose mitomycin-c and autologous bone marrow transplantation. Hum Pat/lol 1982;13: Shulman HM, McDonald GB, Matthews D, et al. An analysis of hepatic venocclusive disease and centrilobular hepatic degeneration following bone marrow transplantation. Gastroenterology 1980;79: Menard DB, Gisselbrecht C, Marty M, et al. Antineoplastic agents and the liver. Gastroenterology 1980;78: McDonald GB, Sharma P, Matthews DE, et al. Venocclusive disease of the liver after bone marrow transplantation: diagnosis, incidence and predisposing factors. Hepatology 1984; 4: Mitchell MC, Boitnott JK, Kaufman S, et al. Budd-Chiari syndrome: etiology, diagnosis and management. Medicine 1982;61: McDermott WV, Stone MD, Bothe A, et al. Budd-Chiari syndrome. Am J Surg 1984;147: Eisenhauer T, Hartmann H, Rumpf KW, et al. Favorable outcome of hepatic venc10cciusive disease in a renal transplant patient receiving azathioprine, treated by portocaval shunt. Digestion 19ij4;30: Langer B, Stone RM, Colapinto RF, et al. Clinical spectrum of the Budd-Chiari syndrome and its surgical management. Am J Surg 1975;129:
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