Biliary Stricture Secondary to Donor B-Cell Lymphoma After Orthotopic Liver Transplantation
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1 Biliary Stricture Secondary to Donor B-Cell Lymphoma After Orthotopic Liver Transplantation Pedro W. Baron, * Michael A. Heneghan, * Paul V. Suhocki, J. Dean Nuckols, J. Elizabeth Tuttle-Newhall, * David N. Howell, and Pierre-Alain Clavien * Biliary complications after orthotopic liver transplantation (OLT) lead to considerable morbidity and occasional mortality after surgery. Bile duct strictures secondary to localized lymphoproliferative disorder of the porta hepatis is rare, with only 12 cases reported in the English literature. Posttransplant lymphoproliferative disorder develops in up to 9% of liver allograft recipients. We describe 2 adult patients who developed Epstein-Barr virus associated localized B-cell lymphoma of donor-tissue origin confined to the porta hepatis 3 and 5 months after OLT. Both patients were administered cyclosporine (CyA) and prednisone as primary immunosuppression. One patient was administered basiliximab as induction therapy. Neither patient had CyA trough levels greater than 250 ng/ml. Both patients were treated with a hepatojejunostomy, 75% reduction in immunosuppression therapy, and acyclovir. One patient had complete involution of the tumor, and the second patient had an 80% reduction of the tumor at the 2-year follow-up visit. This report illustrates the need to consider localized lymphoma post-olt as a cause of obstructive jaundice even within the first 6 months after surgery. Aggressive reduction of immunosuppression in conjunction with acyclovir remains a highly effective therapy. (Liver Transpl 2001;7: ) From the Departments of *Surgery, Radiology, and Pathology, Section of Hepatobiliary Surgery and Transplantation, Duke University Medical Center, Durham, NC. Address reprint requests to Pierre-Alain Clavien, MD, PhD, FACS, Department of Visceral and Transplantation Surgery, Zurich University Medical Center, Raemistrasse 100, Zurich 8091, Switzerland. Telephone: ; FAX: ; clavien@chir.unizh.ch Copyright 2001 by the American Association for the Study of Liver Diseases /01/ $3.00/0 doi: /jlts Biliary complications after orthotopic liver transplantation (OLT) are reported in 11% to 40% of the cases. 1-5 Biliary strictures are classified as anastomotic or nonanastomotic and are usually secondary to preservation injury, hepatic artery thrombosis and/or stenosis, chronic rejection, cytomegalovirus (CMV) infection, blood group type incompatibility, and recurrence of the underlying biliary disease, such as primary sclerosing cholangitis. 1-8 The development of posttransplant lymphoproliferative disorder (PTLD) after solid-organ transplantation constitutes a challenging diagnostic and therapeutic problem. Penn et al 9 first reported this entity in 1969 in a patient who had undergone living related kidney transplantation. A 1.7% to 9% incidence of PTLD after OLT has been reported Causes include greater levels of immunosuppression, use of OKT3, antilymphoblast globulin (ALG), antithymocyte globulin (ATG), and Epstein-Barr virus (EBV) infection In this report, we describe 2 adult patients seen within a 6-month period who developed EBV-associated PTLD (B-cell lymphoma) from donor tissue. Both tumors were confined to the porta hepatis and presented as nonspecific bile duct strictures 3 and 5 months after OLT. Case Reports Case 1 A 41-year-old white man underwent OLT secondary to hepatitis C cirrhosis. An end-to-end choledochocholedochostomy was fashioned over an 8 F T-tube. The donor was a 15-year-old boy who died of closed head injury after a motor vehicle accident. Donor CMV antibody screen was negative at the time of procurement. Donor EBV antibody status was unknown, whereas the recipient was CMV and EBV antibody positive at the time of OLT. He was administered CMV prophylaxis with intravenous ganciclovir, 5 mg/kg, every 12 hours for 2 weeks, followed by acyclovir, 800 mg, orally 3 times daily for 12 weeks. The patient had an uneventful postoperative course and was discharged postoperative day 8. Immunosuppression therapy consisted of cyclosporine (CyA; Neoral; Novartis Pharmaceuticals Corp, East Hanover, NJ) and prednisone. He was also enrolled onto a double-blind randomized trial comparing rapamycin with placebo (protocol no. RADB 158; Novartis Pharma AG, Basel, Switzerland) in conjunction with CyA. He experienced 1 episode of biopsy-proven rejection 14 days after OLT that was successfully treated with methylprednisolone (500 mg/d intravenously for 3 days). The patient withdrew from the randomized trial day 17 post-olt because of abdominal discomfort. Azathioprine was initiated at a dose of 100 mg/d. Three months after OLT, the patient developed jaundice, pruritus, acholia, anorexia, and low-grade fever. T-tube cholangiography showed no opacification of the bile duct superior to the entrance site of the T-tube into the intrahepatic ducts. The bile duct was patent from the T-tube entrance site to the small bowel. A percutaneous transhepatic 62 Liver Transplantation, Vol 7, No 1 ( January), 2001: pp 62-67
2 Lymphoma as Biliary Stricture 63 cholangiogram was performed. This showed complete occlusion of the common hepatic duct with proximal dilatation and a stricture (3 cm long) that did not opacify with contrast above the T-tube (Fig. 1). Computed tomography (CT) of the abdomen and pelvis showed mild intrahepatic bile duct and severe proximal hepatic ductal dilatation. No porta hepatis, intrahepatic, or retroperitoneal masses were seen. An 8 F percutaneous biliary drain (PBD) was placed. The patient underwent laparotomy after normalization of liver function test results. The common bile duct, hepatic duct, hepatic artery, and portal vein were encased in a dense mass. The presence of the T-tube enabled identification of the bile duct. The hepatic duct was opened up to 1 cm below the bifurcation. A mucosa-to-mucosa hepaticojejunostomy Roux-en-Y was performed. Three days postoperatively, the patient developed right upper quadrant tenderness without fever or elevated liver function test results. Cholangiography performed through the PBD showed a fistula between the hepaticojejunostomy and the recipient transected common bile duct. The PBD was left open, and the patient was discharged home in good condition postoperative day 8. Histological sections of the surrounding dense tissue showed a polymorphic infiltrate of mononuclear cells with Figure 1. A 41-year-old man with PTLD involving the donor common hepatic duct. The percutaneous biliary drainage catheter (white arrows) lies in the donor common hepatic duct, just above the site of occlusion by tumor. The T-tube lies within the recipient common bile duct (black arrows). focally atypical features. Immunohistochemical stains were positive for CD20 (B-cell marker) and negative for CD3 (T-cell marker). Immunoperoxide stains were strongly positive for EBV nuclear antigen-2 and latent protein membrane-1. The diagnosis of an EBV-associated B-cell polymorphic PTLD was made. The donor origin of the PTLD was determined by short tandem repeat analysis of paraffinembedded material with the polymerase chain reaction based Geneprint short tandem repeat multiplex system (Promega, Madison, WI). 17 In each case, porta hepatis tissue involved with PTLD was compared with tissue from the donor (donor liver biopsy specimen obtained at the time of OLT or subsequent biopsy of transplant liver tissue uninvolved with PTLD) and recipient (native hepatectomy tissue). Studies to show clonality of the tumor were attempted but were unsuccessful because of the lack of tumor tissue. CyA and prednisone doses were reduced by 75% (from 8 to 2 mg/kg/d and 0.2 to 0.05 mg/kg/d, respectively) to maintain CyA trough levels at less than 50 ng/ml. Azathioprine was discontinued. Oral acyclovir, 800 mg, 4 times daily was initiated. Postoperative metastatic lymphoma workup was negative. Moderately severe, acute cellular rejection developed 30 days after surgery and was treated with methylprednisolone (500 mg/d intravenously for 3 days). Low-dose tacrolimus therapy (2 mg twice daily to achieve target levels of 5 to 7 ng/ml) was instituted with cessation of CyA therapy. The PBD was removed 6 weeks after surgery. Follow-up CT of the abdomen and pelvis showed no evidence of residual mass 12 months after the diagnosis of PTLD. The patient continues to do well. No other recipient of the donor s organs has developed PTLD. Case 2 A 59-year-old white woman underwent OLT for end-stage liver disease secondary to cryptogenic cirrhosis. The donor was a 23-year-old man who died after severe head trauma. An end-to-end choledochocholedochostomy was fashioned over a 10 F T-tube. Donor CMV antibody was negative, and EBV antibody status was unknown at the time of procurement. The patient was CMV antibody and EBV antibody positive. She was administered basiliximab as part of a multicenter Simulect (Novartis Pharmaceuticals Corp) versus placebo, randomized, controlled trial. Primary immunosuppression consisted of CyA and prednisone. She was administered CMV prophylaxis with intravenous ganciclovir, 5 mg/kg, twice daily for 2 weeks, followed by acyclovir, 800 mg, orally 3 times daily for 12 weeks. Her postoperative course was uncomplicated, and she was discharged from the hospital postoperative day 7. The T-tube was removed 5 months post-olt. Ten days later, she developed fever, vomiting, and jaundice. Liver biopsy showed no evidence of acute rejection. Endoscopic retrograde cholangiopancreatography showed a long stricture involving the entire donor bile duct (Fig. 2). The stricture was step dilated, and a 10 F stent was inserted from the papilla to the bifurcation of the hepatic ducts. The patient developed
3 64 Baron et al Immunohistochemical stains were positive for CD20 and negative for CD3. EBV stains were strongly positive for EBV nuclear antigen-2 and focally positive for latent protein membrane-1. The diagnosis of EBV-associated B-cell polymorphic PTLD was made. Lack of tumor tissue precluded definition of clonality. Polymerase chain reaction (discussed previously) showed the tumor DNA to be of donor origin. The patient had an uncomplicated postoperative course and was discharged postoperative day 5. Postoperative metastatic lymphoma workup was negative. The PBD was removed 1 month after surgery after normal cholangiography results. To maintain CyA trough levels at less than 50 ng/ml, CyA and prednisone dosages were reduced from 4 to 1.5 mg/kg/d and 0.3 to 0.07 mg/kg/d, respectively. The patient was administered oral acyclovir, 800 mg, 4 times daily. She developed acute cholangitis 3 months post PBD removal (7 months post biliary-enteric bypass) secondary to recurrent bile duct strictures at the site of the hepaticojejunostomy. This was successfully balloon dilated, and the patient remains asymptomatic. Two years after the diagnosis of PTLD, CT of the abdomen and pelvis showed involution of the porta hepatis mass by 80% without evidence of other intrahepatic or retroperitoneal masses. The patient remains well. No other recipient of the donor s organs has developed PTLD. Figure 2. A 59-year-old woman with PTLD involving the donor common hepatic duct. The percutaneous biliary drainage catheter (arrows) passes through the obstructed donor common hepatic duct and into the duodenum. The nasobiliary drainage catheter (arrowhead) passes through the duodenum and into the intrahepatic bile ducts. cholangitis 48 hours later and was treated with intravenous antibiotics. The biliary stent was removed endoscopically, and a PBD was placed to improve biliary drainage, as well as to facilitate identification of the proximal biliary system. Five days later, a laparotomy was performed. The common bile duct, hepatic ducts, hepatic artery, and portal vein were encased in a dense mass similar to the previous case. The hepatic duct could be identified by following the percutaneous biliary stent. The duct was opened up to 1 cm of the bifurcation of the right and left hepatic ducts. No further dissection was performed for fear of injury to the hepatic artery. At this level, the posterior wall of the hepatic duct appeared fibrotic without an apparent mucosal layer. A hepaticojejunostomy Roux-en-Y was performed without mucosa-to-mucosa apposition in the posterior part of the anastomosis. Histological sections of the mass showed a polymorphic infiltrate of mononuclear cells with focally atypical features. Discussion Between 11% and 40% of liver allograft recipients develop biliary strictures and leaks after OLT. 1-5 Typically, patients with biliary strictures present with symptoms of obstructive jaundice within 6 months of OLT, 1,2 with the majority of strictures being focal, benign, and anastomotic in nature. 1-6 Nonanastomotic bile duct strictures are usually multiple and associated with bile lakes within the hepatic parenchyma. Strictures of this type are believed to be related to preservation injury, vascular complications, CMV infection, and blood group type incompatibility. We report 2 cases of PTLD presenting as bile duct strictures after OLT. These strictures were caused by external compression and direct invasion of the bile duct wall by B-cell lymphoma of donor origin. PTLD presenting as a localized tumor at the porta hepatis causing biliary stricture is exceedingly rare PTLD is most commonly described in pediatric populations in association with recent EBV infection, whereas in adults, the use of induction therapy and high doses of immunosuppressive therapy are recognized risk factors PTLD may be a localized or generalized disease. It affects only extranodal tissues in approximately 70% of the cases. We identified 12 patients in the literature with biliary strictures associated with invasive PTLD after OLT (Table 1) In 7 of these patients, the lymphoma originated from the hepatic
4 Lymphoma as Biliary Stricture 65 Table 1. Reported Cases of B-Cell Lymphoma After OLT Localized in the Porta Hepatis and Causing Extrahepatic Biliary Stricture Reference (yr) No. of Patients Age (yr) Induction Therapy Maintenance Immunosuppression Therapy CyA (ng/ml) Time Between OLT and PTLD (mo) Origin of PTLD EBV Ab No. of AR Therapy Outcome/ Follow-Up (mo) Moody et al 18 (1992) 1? ALG 14 d (all patients) Cherqui et al 19 (1993) 1 55 ATG 7d (100 mg/d) CyA, prednisone (all patients)? 4?? Re-OLT? 1?? 6??? Re-OLT? 1?? 9?? Re-OLT? Spiro et al 20 (1993) 1 54? CyA (12 mg/kg), prednisone, azathioprine CyA, prednisone, azathioprine? 8 Donor 0 Bilio-enteric bypass?? 4.5 Donor? 1* D/C azathioprine, radiotherapy Armes et al 21 (1994) 1 39? CyA (10 mg/kg), prednisone? 7 Donor 2 s Immunosuppression Alive ? Azathioprine? 7 Acyclovir, chemotherapy Alive 3 Ribas et al 22 (1995) 1 51 ATG 7d (2 mg/kg) Strazzabosco et al 23 (1997) CyA, prednisone, azathioprine? 2 Donor 2 s Immunosuppression, re-olt, acyclovir 1 48? CyA, prednisone Donor 1 s Immunosuppression 1 54? Azathioprine Laparotomy, T-tube in bile duct Navarro et al 24 (1998) 1 56 No CyA, prednisone *? Dead No Azathioprine 430 3? 0 D/C CyA, Alive 18 chemotherapy Current study 1 41 No CyA, prednisone, rapamycin? Donor 1 CyA to FK506 Alive Basiliximab CyA, prednisone s Immunosuppression Alive 24? Dead 9 Alive 17 Abbreviations:?, unknown; AR, acute rejection; Re-OLT, retransplantation; Ab, antibody; D/C, discontinue. * Steroid-resistant rejection treated with OKT3.
5 66 Baron et al hilar lymph node basin, as in the 2 patients described here. In many of the reported patients, chromosomal analysis of tumor cells differentiated donor from recipient tissue and allowed the origin of the PTLD to be identified In our 2 patients, chromosomal analysis showed that the lymphoma tissue was of donor origin. Both were related to EBV infection and both were B-cell lymphomas. Five of the 12 patients were administered induction therapy with either ALG or ATG (Table 1). Use of induction therapy was unknown in 5 patients. Eight patients were administered azathioprine as part of their immunosuppression regimen. Moreover, all patients described with hilar PTLD were administered CyAbased primary immunosuppression; 3 patients were administered high doses of CyA, and 2 other patients had documented high CyA trough levels. 20,21,24 Consistent with the observation that the use of induction agents or excess immunosuppression predisposes to PTLD development, 1 of our patients (patient 2) was administered basiliximab as a part of a multicenter Simulect versus placebo, randomized, controlled trial, whereas the second patient was enrolled onto a randomized clinical trial comparing rapamycin with placebo. Although trough levels of CyA were never greater than 250 ng/ml in the early postoperative phase, to date, we are uncertain whether patient 1 was administered rapamycin or placebo. Although patient 1 was treated for acute cellular rejection 2 weeks post-olt with 3 doses of methylprednisolone, a satisfactory clinical response was obtained, and it is unlikely that steroids contributed to development of the lymphoma. The 2 patients described here have the shortest interval between OLT and the development of strictures related to PTLD. Moreover, patient survival post diagnosis of extrahepatic biliary stricturing type PTLD is the longest described to date. Both patients were treated with reduction of CyA and prednisone by 75% in addition to oral acyclovir. Both patients underwent a biliary-enteric bypass. In conclusion, we report 2 cases of PTLD of donor origin localized to the porta hepatis that caused obstructive jaundice. T-tube cholangiography performed immediately post-olt showed normal results in both patients. This report illustrates the need to consider localized biliary PTLD as a cause of obstructive jaundice, even within the first 3 to 6 months after OLT, and reiterates the need for judicious immunosuppression. References 1. Greif F, Bronsther O, Van Thiel D, Casavilla A, Iwatsuki S, Tzakis A, et al. The incidence, timing and management of biliary tract complications after orthotopic liver transplantation. Ann Surg 1994;219: Vallera R, Cotton P, Clavien P. Biliary reconstruction for liver transplantation and management of biliary complications: Overview and survey of current practices in the United States. Liver Transpl Surg 1995;2: Stratta RJ, Wood RP, Langnas AN, Hollins RR, Bruder KJ, Donovan JP, et al. Diagnosis and treatment of biliary tract complications after orthotopic liver transplantation. Surgery 1989; 106: O Connor TP, Lewis WD, Jenkins RL. Biliary tract complications after liver transplantation. Arch Surg 1995;130: Williams R, Smith M, Shilkin KB, Herbertson B, Joysey V, Calne RY. Liver transplantation in man: The frequency of rejection, biliary tract complications, and recurrence of malignancy based on an analysis of 26 cases. Gastroenterology 1973;64: Miller WJ, Campbell WL, Zajko AB, Pinna A, Zetti G, Stieber AC, et al. Obstructive dilatation of extrahepatic recipient and donor bile ducts complicating orthotopic liver transplantation: Imaging and laboratory findings. AJR Am J Roentgenol 1991; 157: Sanchez-Urdazpal L, Gores GJ, Ward EM, Maus TP, Buckel EG, Steers JL, et al. Diagnostic features and clinical outcome of ischemic-type biliary complications after liver transplantation. Hepatology 1993;17: Colonna JO II, Shaked A, Gomes AS, Colquhoun SD, Jurim O, McDiarmid SV, et al. Biliary strictures complicating liver transplantation: Incidence, pathogenesis, management, and outcome. Ann Surg 1992;216: Penn I, Hammond W, Brettschneider L, Starzl TE. Malignant lymphomas in transplantation patients. Transplant Proc 1969; 1: Jain A, Reyes J, Kashyap R, Rohal S, Cacclarelli T, McMichael J, et al. Liver transplantation under tacrolimus in infants, children, adults, and seniors: Long-term results, survival, and adverse events in 1000 consecutive patients. Transplant Proc 1998;30: Levy M, Backman L, Husberg B, Goldstein R, McMillan R, Gibbs J, et al. De novo malignancy following liver transplantation: A single-center study. Transplant Proc 1993;25: Nalesnik MA, Jaffe R, Starzl TE, Demetris AJ, Porter K, Burnham JA, et al. The pathology of posttransplant lymphoproliferative disorders occurring in the setting of cyclosporine A-prednisone immunosuppression. Am J Pathol 1988;133: Stieber AO, Boillot O, Scotti-Foglieni C, Nalesnik MA, Gordon RD, Marino I, et al. The surgical implications of the posttransplant lymphoproliferative disorders. Transplant Proc 1991;23: Malatack JF, Gartner JC Jr, Urbach AH, Zitelli BJ. Orthotopic liver transplantation, Epstein-Barr virus, cyclosporine, and lymphoproliferative disease: A growing concern. J Pediatr 1991;118: Renard TH, Andrews WS, Foster ME. Relationship between OKT3 administration, EBV seroconversion, and the lymphoproliferative syndrome in pediatric liver transplant recipients. Transplant Proc 1991;23: Cox KL, Lawrence-Miyasaki LS, Garcia-Kennedy R, Lennette ET, Martinez OM, Krams SM, et al. An increased incidence of Epstein-Barr virus infection and lymphoproliferative disorder in
6 Lymphoma as Biliary Stricture 67 young children on FK506 after liver transplantation. Transplantation 1995;59: Nuckols JD, Baron PW, Stenzel TT, Olatidoye B, Tuttle-Newhall JE, Clavien P-A, Howell DN. The pathology of liver-localized post-transplant lymphoproliferative disease: A report of three cases and a review of the literature. Am J Surg Pathol 2000;24: Moody AR, Wilson SR, Greig PD. Non-Hodgkin lymphoma in the porta hepatis after orthotopic liver transplantation: Sonographic findings. Radiology 1992;182: Cherqui D, Duvoux C, Plassa F, Gaulard P, Julien M, Fagniez PL, et al. Lymphoproliferative disorder of donor origin in a liver transplant recipient: Complete remission after drastic reduction of immunosuppression without graft loss. Transplantation 1993;56: Spiro IJ, Yandell DW, Li C, Saini S, Ferry J, Powelson J, et al. Brief report: Lymphoma of donor origin occurring in the porta hepatis of a transplanted liver. N Engl J Med 1993;329: Armes JE, Angus P, Southey MC, Battaglia SE, Ross BC, Jones RM, et al. Lymphoproliferative disease of donor origin arising in patients after orthotopic liver transplantation. Cancer 1994;74: Ribas Y, Rafecas A, Figueras J, Benasco C, Fabregat J, Torras J, et al. Post-transplant lymphoma in a liver allograft. Transplant Int 1995;8: Strazzabosco M, Corneo B, Iemmolo RM, Menin C, Gerunda G, Bonaldi L, et al. Epstein-Barr virus-associated post-transplant lymphoproliferative disease of donor origin in liver transplant recipients. J Hepatol 1997;26: Navarro F, Pyda P, Pageaux GP, Perrigault PF, Ramos J, Taourel P, et al. Lymphoproliferative disease after liver transplantation: Primary biliary localization. Transplant Proc 1998;30: McDiarmid SV, Jordan S, Lee GS, Toyoda M, Goss JA, Vargas JH, et al. Prevention and preemptive therapy of posttransplant lymphoproliferative disease in pediatric liver recipients. Transplantation 1998;66: Penn I. Immunosuppression A contributory factor in lymphoma formation. Clin Transplant 1992;6: Starzl TE, Nalesnik MA, Porter KA, Ho M, Iwatsuki S, Griffith BP, et al. Reversibility of lymphomas and lymphoproliferative lesions developing under cyclosporin-steroid therapy. Lancet 1984;1: Reyes J, Tzakis A, Green M, Nour B, Nalesnik M, Van Thiel D, et al. Posttransplant lymphoproliferative disorders occurring under primary FK506 immunosuppression. Transplant Proc 1991; 23: Penn I. De novo cancers in organ allograft recipients. Curr Opin Organ Transplant 1998;3: Penn I. The role of immunosuppression in lymphoma formation. Springer Semin Immunopathol 1998;20:
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