Living Donor Liver Transplantation for Echinococcus Alveolaris: Single-Center Experience
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1 LIVER TRANSPLANTATION 21: , 2015 ORIGINAL ARTICLE Living Donor Liver Transplantation for Echinococcus Alveolaris: Single-Center Experience Fatih Ozdemir, Volkan Ince, Bora Barut, Asim Onur, Cuneyt Kayaalp, and Sezai Yilmaz Liver Transplantation Institute, Department of Surgery, _ In on u University, Malatya, Turkey Echinococcus alveolaris (EA) causes a hepatic zoonotic infection and behaves like a malignant tumor during invasion. Liver transplantation (LT) is the only curative treatment option for this unresectable disease. Here, we share our experience with living donor liver transplantation (LDLT) due to EA from the time between March 2002 and November 2014 at the Liver Transplantation Institute of In on u _ University. Ten patients (mean age, 38.6 years) undergoing LDLT because of unresectable EA were evaluated preoperatively, and the operative and follow-up data were analyzed retrospectively. The mean time interval between diagnosis and LT was 27 months. The mean operation time and mean intraoperative blood requirement were 613 minutes and 4 units of packed red blood cells, respectively. Diaphragmatic resections were performed in 3 patients, and vena cava replacement was performed in 2 patients because of difficulties in removing the extended disease. The local recurrence and distant metastasis rates were 10% and 20%, respectively. The mean survival time was 19.5 months (range, 0-54 months), and the mortality rate was 30%. Unresectable hepatic alveolar echinococcosis is a rare indication for LT and presents some technical difficulties during surgery because diaphragmatic resection, vascular reconstruction, or multiple blood transfusions may be needed. LDLT can be performed successfully in patients with this rare infectious disease, with careful follow-up for potential recurrence and metastasis and administration of low-dose immunosuppressive agents. Liver Transpl 21: , VC 2015 AASLD. Received January 30, 2015; accepted May 5, See Editorial on Page 1013 The larval stage of Echinococcus alveolaris (EA) causes hepatic zoonotic infection and behaves like a malignant tumor during invasion in humans who are accidental intermediate hosts. 1 If patients remain untreated after diagnosis, the mortality rate is approximately 90% within 10 years. 2,3 The disease invades neighboring structures when it is located primarily in the liver, and distant organ metastasis may occur hematogenously. Early diagnosis and treatment are the main goals to prevent complications, such as biliary tract infection, liver abscess, bleeding due to portal hypertension (PHT; related to secondary biliary cirrhosis or parasitic involvement of the portal vein), and chronic Budd-Chiari syndrome, in cases of parasitic involvement of the suprahepatic veins. Curative surgery can be performed in only 35% of patients, 4 and a liver transplantation (LT) is the only curative treatment option for unresectable liver disease 5 (Fig. 1). Here, we share our experience with living donor liver transplantation (LDLT) due to EA from the time between March 2002 and November 2014 at the Liver Transplantation Institute of _In on u University. Abbreviations: EA, Echinococcus alveolaris; ICU, intensive care unit; LDLT, living donor liver transplantation; LT, liver transplantation; MELD, Model for End-Stage Liver Disease; MMF, mycophenolate mofetil; PHT, portal hypertension. Potential conflict of interest: Nothing to report. Financial support: Nothing to report. Address reprint requests to Fatih Ozdemir, M.D., Liver Transplantation Institute, Department of Surgery, _ In on u University, Elazig Road 15th kilometer, Malatya, Turkey Telephone: /3701; fatihup@hotmail.com DOI /lt View this article online at wileyonlinelibrary.com. LIVER TRANSPLANTATION.DOI /lt. Published on behalf of the American Association for the Study of Liver Diseases VC 2015 American Association for the Study of Liver Diseases.
2 1092 OZDEMIR ET AL. LIVER TRANSPLANTATION, August 2015 TABLE 1. Patient Demographic Characteristic Figure 1. PATIENTS AND METHODS In total, 1114 LDLTs were performed at our center between March 2002 and November 2014, and 10 patients (0.9%; 2 females and 8 males; age, mean, 38.6 years; range, years) who underwent LDLT due to EA were analyzed retrospectively. The patient s demographic characteristics are summarized in Table 1. The mean time interval between diagnosis and LT was 27 months (range, months). The symptoms at diagnosis were nonspecific upper abdominal pain, jaundice, and fever. The mean patient Model for End- Stage Liver Disease (MELD) score was 15 (range, 7-23). Four patients received interventional procedures before transplantation, including percutaneous biliary drainage and biliary stenting by endoscopic retrograde cholangiography. Four patients had undergone surgery previously, including segmental liver resection for hepatic EA. Six patients received a round of albendazole therapy before LT but were not treated regularly with the drug. One patient had splenic and pulmonary metastases before LDLT and experienced septic biliary complications and liver failure during the evaluation period; thus, we performed palliative LDLT. Our indications for LDLT were extensive liver disease, hilar involvement, recurrent cholangitis, cholestasis, and recurrent disease after surgical resection (Table 2). Staging according to the World Health Organization classification is shown in Table 2. RESULTS Explanted liver with EA. All surgeries performed were LDLTs. Mean operation time was 613 minutes (range, minutes), and the mean intraoperative blood requirement was 4 units (range, 0-15 units) of packed red blood cells. Two patients required replacement of the vena cava because of difficulties removing the extended disease. One of these patients had a vascular reconstruction with a cadaveric caval graft, and the other had a vascular reconstruction with a cadaveric aortic graft. 6,7 Three patients required diaphragmatic resections Value Age, years, 38.6 (19-61) Sex, female/male 2/8 MELD score, 15 (7-23) Intraoperative blood 4 (0-15) requirement, units of packed red blood cells, Operation time, minutes, 613 ( ) Postoperative ICU stay, 4.7 (1-10) days, Length of hospital stay, 32 (17-94) days, Time interval between 27 (3-108) diagnosis and transplantation, months, Medical therapy before 6 (60) transplantation (albendazole), n (%) Hepatic resection before 4 (40) transplantation, n (%) Interventional procedures 4 (40) before transplantation, n (%) Follow-up, months, median 14.5 (2-54) (range) Local recurrence, n (%) 1 (10) Distant metastasis, n (%) 2 (20) Survival time, months, 19.5 (0-54) Mortality, n (%) 3 (30) because of diaphragmatic invasion. Five patients had hepatic hilar invasion (Table 2). Findings of the explanted grafts are provided in Table 3. Only 2 patients received a hepaticojejunostomy anastomosis, and the remainder received a duct-to-duct anastomosis to reconstruct the biliary tract. The vascular graft anastomoses had no extraordinary features. All living donors were in good physical condition without any complications. Follow-Up Data One patient died on postoperative day 1 because of hepatic arterial thrombosis. Another patient, who was receiving oral anticoagulant therapy for mitral valve prolapse, died 6 months postoperatively because of a pulmonary hemorrhage. One patient died suddenly at home 2 months after LDLT. The remaining 7 patients are alive. Median follow-up was 14.5 months (range, 2-54 months). All patients received the same immunosuppressive protocol, consisting of prednisolone, mycophenolate mofetil (MMF), and tacrolimus, from the time of diagnosis. The steroid was discontinued after 3 months, and MMF was discontinued after 6 months. One of the patients, who received a hepaticojejunostomy anastomosis, developed a biliary leak
3 LIVER TRANSPLANTATION, Vol. 21, No. 8, 2015 OZDEMIR ET AL TABLE 2. Patients Data, Intraoperative Findings, and PNM Classification Patients, Age (years), Sex Cause of LT 58, male Extensive disease PHT, hilum invasion 61, male Extensive disease PHT, hilum invasion 19, male Liver abscess, cholangitis, PHT 33, male Hilum invasion, cholangitis 49, female Chronic cholestasis, PHT 21, male Extensive disease hilum invasion 29, male Extensive disease at the liver, cholestasis 51, male Hilum invasion, cholestasis 37, female Extensive disease at the liver 28, male Extensive disease at the liver, cholestasis Distant Organ Metastasis Diaphragma Invasion Hilum Invasion Vena Cava Invasion PNM Stage Lung and splenic metastasis P3N0M1 IV 1 1 P3N1M0 IIIB 1 1 P4N1M0 IV 1 1 P4N1M0 IV P3N0M0 IIIA P1N0M0 I 1 P1N1M0 IIIB NOTE: 1, present;, absent. TABLE 3. Histopathological Findings of the Explanted Livers Patients, Age (Years), Sex Weight of the Explanted Liver, Grams Largest Tumor Size, cm Largest Tumor Localization Histological Diagnosis 58, male Right lobe Liver parancyme necrosis 61, male Right lobe Cholestatic liver destruction 19, male Right lobe Secondary biliary cirrhosis 33, male Right lobe Cholestatic liver destruction 49, female Right lobe Cholestatic liver destruction 21, male Left lobe Cholestatic liver destruction 29, male Right lobe Cholestatic liver destruction 51, male Right lobe Cholestatic liver destruction 37, female Right lobe Nodular cirrhosis 28, male Right lobe Cholestatic liver destruction
4 1094 OZDEMIR ET AL. LIVER TRANSPLANTATION, August 2015 from the anastomosis. He was treated by percutaneous internal-external biliary drainage catheterization, which was performed by an interventional radiologist in the first month after LDLT. Another patient developed ascites because of hepatic venous stenosis during postoperative month 11. He was treated by hepatic vein stent replacement. Brain metastasis occurred in 1 patient 2 months after LDLT and was treated surgically. This patient had pulmonary and splenic metastases before LDLT. The same patient was diagnosed with liver allograft reinfection 3 years after LDLT. He is still alive and has been receiving albendazole for the past 3 months. Another patient, who developed a brain metastasis 1 year after LDLT, received albendazole after the diagnosis. The local recurrence, distant metastasis, and mortality rates in our series were 10%, 20%, and 30%, respectively. Mean survival time was 19.5 months (range, 0-54 months; Table 1). DISCUSSION Hepatic EA is an infectious disease that grows and spreads like a malignant tumor. If curative surgery is not possible in cases of extended disease or because of hilar involvement, the only treatment option is LT. Removing the liver during LT is a major problem in patients with this disease. The long operation times and multiple blood transfusion requirements are the result of technical difficulties related to the extrahepatic extension of the disease (mostly because of the diaphragm but also because of adjacent structures) during surgery. 5 We treated 3 patients who required a diaphragmatic resection because of invasion. We also had technical difficulties while removing the liver, and we removed the retrohepatic vena cava with the liver and replaced the vena cava in 2 patients. 6,7 A prior surgery can make the operation more complicated. Thus, it is important for future transplant candidates to avoid unnecessary abdominal surgery and to undergo endoscopic or percutaneous radiological interventions for unresectable EA. 8 Most of our patients with hepatic EA had advanced disease when diagnosed and had undergone various interventional and surgical procedures before admission to our center. However, their problems persisted. If hepatic EA spreads to the liver hilum, neither an interventional procedure nor medical treatment is adequate to manage the recurrent cholangitis. Patients with extensive disease and recurrent cholangitis require LT. Our series contained only 1 patient with early stage EA, who underwent LT because of concomitant liver failure caused by hepatitis B infection. Bresson-Hadni et al. 8 showed that extrahepatic dissemination, medical treatment before and after transplantation for EA, and immunosuppressive therapy are the major factors responsible for recurrence and mortality in patients with EA. One of our patients developed splenic and pulmonary metastases during the LT evaluation period. Bresson-Hadni et al. 9 reported that potential recurrence of the disease, particularly in patients with residual or metastatic EA lesions, should not be considered a contraindication to LT because EA is lethal in the short term. Our patient had septic biliary complications and liver failure at the time of LDLT, so we performed palliative LDLT. Brain metastasis occurred in the same patient 2 months after LDLT and was treated surgically. He is now receiving albendazole for reinfection of the liver allograft, which was diagnosed 3 years after LDLT. Extrahepatic dissemination seems to be the main reason for morbidity and mortality. Benzimidazole derivates, such as mebendazole and albendazole, are the drugs used to treat EA. However, they have a parasitostatic rather than a parasitosidal effect with an overall success rate of 55%-97%. 10 Patients must receive long-term benzimidazole therapy to reach these success rates and, occasionally, despite severe side effects and intolerability. 11 In addition, an increase in liver enzyme levels can make follow-up difficult after transplantation. Six patients diagnosed with hepatic EA received short-term albendazole therapy before LT in our series. We do not use benzimidazole derivates after curative resection and successful transplantation for hepatic EA unless recurrent disease develops or distant metastasis occurs. Heavy immunosuppressive treatment after LT is related to the possible recurrence of EA. 5 Our immunosuppression protocol included prednisolone, tacrolimus, and MMF. We stopped the steroid treatment after 3 months and continued the tacrolimus and MMF. We only administered tacrolimus at the beginning of month 6. Our aim with immunosuppression is to use the minimum levels of these drugs at which they are most effective. It seems important to reduce the immunosuppressive treatment as early as possible in this particular indication for LT. 5 Cases of LDLT for EA have only been published as case reports since 1989 (the first LDLT) according to PubMed records. 6,7,12-14 We have performed one of the largest LDLT case series due to EA. In conclusion, unresectable hepatic EA is a rare indication for LT. The surgical procedures for this condition are technically complex, including difficult dissections and vascular reconstruction during surgery, such that multiple blood transfusions may be required. In addition, diaphragmatic resection because of disease invasion may be necessary. Cadaveric or artificial vascular grafts should be available for vascular reconstruction during surgery. LDLT can be performed successfully for this rare infectious disease with careful follow-up for potential recurrence and metastasis and administration of low-dose immunosuppressive agents. REFERENCES 1. Gottstein B. Molecular and immunological diagnosis of echinococcosis. Clin Microbiol Rev 1992;5: Moreno-Gonzalez E, Loinaz Segurola C, Garcıa Ure~na MA, Garcıa Garcıa I, Gomez Sanz R, Jimenez Romero C, et al. Liver transplantation for Echinococcus granulosis hydatid disease. Transplantation 1994;58:
5 LIVER TRANSPLANTATION, Vol. 21, No. 8, 2015 OZDEMIR ET AL Xia D, Yan LN, Li B, Zeng Y, Cheng NS, Wen TF, et al. Orthotopic liver transplantation for incurable alveolar echinococcosis: report of five cases from west China. Transplant Proc 2005;37: Bresson-Hadni S, Vuitton DA, Bartholomot B, Heyd B, Godart D, Meyer JP, et al. A twenty-year history of alveolar echinococcosis: analysis of a series of 117 patients from eastern France. Eur J Gastroenterol Hepatol 2000; 12: Koch S, Bresson-Hadni S, Miguet JP, Crumbach JP, Gillet M, Mantion GA, et al.; for European Collaborating Clinicians. Experience of liver transplantation for incurable alveolar echinococcosis: a 45-case European collaborative report. Transplantation 2003;75: Mamedov R, Novruzov N, Baskiran A, Yetisir F, Unal B, Aydın C, et al. Living donor liver transplantation with replacement of vena cava for Echinococcus alveolaris: A case report. Int J Surg Case Rep 2014;5: Yetişir F, Dogan SM, Mamedov R, Kayaalp C, Yilmaz S. Replacement of vena cava up to the right atrium during living donor liver transplantation for Echinococcus alveolaris. Case Rep Transplant 2014;2014: Bresson-Hadni S, Koch S, Miguet JP, Gillet M, Mantion GA, Heyd B, Vuitton DA; for European group of clinicians. Indications and results of liver transplantation for Echinococcus alveolar infection: an overview. Langenbecks Arch Surg 2003;388: Bresson-Hadni S, Blagosklonov O, Knapp J, Grenouillet F, Sako Y, Delabrousse E, et al. Should possible recurrence of disease contraindicate liver transplantation in patients with end-stage alveolar echinococcosis? A 20-year followup study. Liver Transpl 2011;17: Reuter S, Jensen B, Buttenschoen K, Kratzer W, Kern P. Benzimidazoles in the treatment of alveolar echinococcosis: a comparative study and review of the literature. J Antimicrob Chemother 2000;46: Reuter S, Buck A, Manfras B, Kratzer W, Seitz HM, Darge K, et al. Structured treatment interruption in patients with alveolar Echinococcosis. Hepatology 2004;39: Moray G, Shahbazov R, Sevmis S, Karakayali H, Torgay A, Arslan G, et al. Liver transplantation in management of alveolar echinococcosis: two case reports. Transplant Proc 2009;41: Kantarci M, Pirimoglu B, Aydinli B, Ozturk G. A rare reason for liver transplantation: hepatic alveoloar echinococcosis. Transpl Infect Dis 2014;16: Hatipoglu S, Bulbuloglu B, Piskin T, Kayaalp C, Yilmaz S. Living donor liver transplantation for alveolar echinococcus is a difficult procedure. Transplant Proc 2013;45:
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