Alegre, F. (Félix)

Bilbao, J.I. (José I.)

Diaz-Dorronsoro, L. (Lourdes)

Herrero, J.I. (José Ignacio)

Iñarrairaegui, M. (Mercedes)

Pardo, F. (Fernando)

Quiroga, J. (Jorge)

Dadun, University of Navarra

IMAGES IN LIVER TRANSPLANTATIONHepatic Encephalopathy After LiverTransplantation in a Patient with a NormallyFunctioning Graft: Treatment with Embolizationof Portosystemic CollateralsJ. Ignacio Herrero,1,4 Jose Ignacio Bilbao,2 Maria Lourdes Diaz,2 Felix Alegre,1Mercedes Inarrairaegui,1 Fernando Pardo,3 and Jorge Quiroga1,41Liver Unit, 2Department of Radiology, and 3Department of Surgery, Clı´nica Universitaria de Navarra,Pamplona, Spain; and 4Centro de Investigaciones Biome´dicas en Red de Enfermedades Hepa´ticas yDigestivas, SpainReceived April 5, 2008; accepted May 11, 2008.Portosystemic encephalopathy is one of the most im-portant complications of liver cirrhosis. The restorationof normal hepatic function and the reduction of porto-systemic shunts by means of a liver graft are followedby the resolution of hepatic encephalopathy. We reportthe case of a patient with a normal functioning graftthat developed recurrent encephalopathy after trans-plantation. The patient was successfully treated by em-bolization of a large portosystemic shunt between thesuperior mesenteric vein and both gonadal veins, thiscausing an inversion of the superior mesenteric veinﬂow.CASE REPORTA 58-year-old male with alcoholic liver cirrhosis wasreferred to our center for liver transplantation in April2006. Liver cirrhosis had been diagnosed in October2005, and he had remained abstinent since then. Atdiagnosis, he had jaundice, edema, and ascites. De-spite 6 months of abstinence, his Model for End-StageLiver Disease score at referral for transplantation was20. Three months later, he had his ﬁrst episode ofhepatic encephalopathy, with rapid improvement afterdiuretic withdrawal and treatment with oral lactulose.He had no more episodes of encephalopathy beforetransplantation. In the pretransplant assessment, apatent portal vein, with slow hepatopetal ﬂow, wasfound in a Doppler ultrasound examination. An abdom-inal computed tomography scan showed a cirrhoticliver without hypervascular lesions; the portal vein di-ameter was 12 mm, and important collateral circula-tion was found.He underwent liver transplantation in August 2006with a whole cadaveric graft from a 70-year-old woman.Portal vein ﬂow at the beginning of the surgery was 200mL/minute; it increased to 1000 mL/minute after graftreperfusion. His postoperative course was uneventful,and he was discharged 6 days after transplantation. Hedeveloped posttransplant diabetes mellitus, requiringinsulin therapy. In the following months, he had mod-erate tremor, secondary to tacrolimus, that improvedwhen the tacrolimus dose was reduced. Five monthsafter transplantation, he had a moderate increase inserum aminotransferase values (up to 5 times the up-per limit of normal range). A liver biopsy showed amoderate portal and lobular inﬂammatory inﬁltrateand mild portal ﬁbrosis. Liver function tests spontane-ously improved without changes in immunosuppres-sive therapy (tacrolimus, 4 mg/day, and prednisone,7.5 mg/day).Ten months after transplantation, the patient wasadmitted to the hospital with a 2-day history of disori-entation. On physical examination, the patient was dis-oriented and had inappropriate speech; asterixis wasevident, and no sign suggestive of focal neurologicalThe Centro de Investigaciones Biome´dicas en Red de Enfermedades Hepa´ticas y Digestivas is funded by the Instituto de Salud CarlosIII.Address reprint requests to J. Ignacio Herrero, Liver Unit, Clı´nica Universitaria de Navarra, 36 Avenida Pio XII 36, 310008 Pamplona, Spain.Telephone: 34-948-296637; FAX: 34-948-296500; E-mail: iherrero@unav.esDOI 10.1002/lt.21552Published online in Wiley InterScience (www.interscience.wiley.com).LIVER TRANSPLANTATION 15:111-114, 2009© 2008 American Association for the Study of Liver Diseases.damage was found. Serum urea, creatinine, and liverfunction tests were normal. Serum ammonia levelswere 197 g/dL. A brain magnetic resonance scan didnot reveal changes when compared with a scan per-formed before liver transplantation (T1-weighted hyper-intensity of basal ganglia was present in both examina-tions). Doppler ultrasound revealed patency of both theportal vein (with a ﬂow of 15 cm/second) and the he-patic artery. The patient was treated with oral lactulose,and the clinical picture improved in less than 24 hours.An uncomplicated urinary tract infection was also di-agnosed, and ceftriaxone treatment was indicated. Hewas discharged 3 days after admission; oral lactulosewas prescribed at discharge.Two weeks later, the patient was admitted again withdisorientation and somnolence. On physical examina-tion, asterixis was again evident. Serum ammonia lev-els were 202 g/dL, and liver function tests were nor-mal. An electroencephalogram was consistent withmetabolic encephalopathy (lentiﬁcation and occasionaltriphasic waves). Nuclear magnetic resonance spectros-copy revealed a marked glutamine increase and a de-crease in myo-inositol suggestive of hepatic encepha-lopathy.1 A urine culture was negative, and the patientdid not have any other apparent cause or precipitant ofthis episode of encephalopathy.With the aim of detecting occult portosystemic collat-erals, abdominal angiography was performed. The ve-nous phase of the superior mesenteric arteriogramshowed that the venous return from jejunal, ileal, andcolonic veins was deviated to gross varices draining toinferior vena cava (Fig. 1). The splenic angiographyshowed that a large proportion of venous ﬂow was sto-len from the superior mesenteric vein to the previouslymentioned varices (Fig. 2). A retrospective examinationof the abdominal computed tomography scan per-formed before transplantation showed the presence ofhuge collaterals in the retroperitoneum (Retzius veins)2that connected these varices to both gonadal veins anda large left renal vein (Fig. 3).Embolization of these collateral veins was decidedand then performed; bilateral femoral vein access wasused. After catheterization of the left femoral vein, acatheter was introduced through the left gonadal vein,which received its ﬂow from a large-caliber tortuousretroperitoneal collateral. In parallel with this catheter,a second catheter was advanced, and the ﬂow was sub-Figure 1. Late venous phase of a superior mesenteric arte-riogram. The superior mesenteric vein is not opaciﬁed. Theﬂow is diverted toward large collateral veins (arrows).Figure 2. Late venous phase of a splenic arteriogram. Thereis hepatofugal ﬂow toward the superior mesenteric vein (ar-rowhead). The ﬂow is diverted toward large collateral veins(arrows).Figure 3. Computed tomography performed before livertransplantation. Collaterals in the territory of the left gonadalvein are clearly depicted (arrow). An enlarged right gonadalvein can also be seen (arrowhead).112 HERRERO ET AL.LIVER TRANSPLANTATION.DOI 10.1002/lt. Published on behalf of the American Association for the Study of Liver Diseasessequently stopped. Segments of mobile core guide anddifferent caliber coils were used to completely occludethe left shunt (Fig. 4). Afterwards, the right gonadal veinwas catheterized and completely occluded with severalcoils and two 12-mm occluding Amplatzer devices(Fig. 5).One month later, a new angiogram from the superiormesenteric artery showed that venous mesenteric veinﬂow was patent and hepatopetal and that there was noﬂow to varices or collateral veins (Fig. 6). The venousphase of a splenic angiograph showed the absence ofreverse ﬂow directed toward the superior mesentericartery (Fig. 7). Ten months after the embolization, thepatient remains free of new episodes of encephalopa-thy.DISCUSSIONHepatic encephalopathy is usually a complication ofacute and chronic liver disease, but it has also beenreported in patients with major portosystemic shuntswithout cirrhosis.3 In patients with liver cirrhosis, therestoration of normal liver function after liver trans-plantation is usually followed by the resolution of en-cephalopathy, despite the persistence of portosystemicshunts. In the case reported here, the development ofhepatic encephalopathy was unexpected because graftfunction was normal. High ammonia levels, electroen-cephalogram changes, improvement with lactulose andmagnetic resonance spectroscopy, and the exclusion ofother structural or metabolic causes strongly suggestthat the clinical picture was consistent with hepaticencephalopathy related to the presence of such shunts.Finally, the absence of new episodes of encephalopathyafter their embolization conﬁrmed that suspicion.In liver transplant recipients, large collateral veinsmay steal ﬂow from the portal vein because they mayremain patent even with a very low portosystemic pres-Figure 4. Left gonadal vein phlebography performed after itsembolization with coils and segments of guide wire. An occlu-sion balloon catheter (still inﬂated) is seen (arrow).Figure 5. Right gonadal vein phlebography performed afterits embolization with coils and Amplatzers (arrow).Figure 6. Late venous phase of a superior mesenteric arte-riogram. The superior mesenteric vein is now opaciﬁed andpresents hepatopetal ﬂow.HEPATIC ENCEPHALOPATHY AFTER LIVER TRANSPLANTATION 113LIVER TRANSPLANTATION.DOI 10.1002/lt. Published on behalf of the American Association for the Study of Liver Diseasessure gradient. These collateral veins may reduce portalﬂow through a competitive ﬂow-steal phenomenon,thus precipitating portal vein thrombosis.4 Large spon-taneous portosystemic shunts may also have a detri-mental effect on graft function.5 In patients with cirrho-sis and hepatic encephalopathy, it has been previouslyreported that the occlusion of portosystemic shuntsimproves this condition.6 Thus, in liver transplant can-didates, the occlusion of portosystemic shunts wouldameliorate hepatic encephalopathy and avoid all theseaforementioned risks. Unfortunately, the closure ofthese shunts could lead to esophageal or gastricvariceal bleeding.7 This complication is not expected inliver transplant recipients with a normal grafted liver.Therefore, a potential approach to this problem couldbe the intraoperative ligation or embolization of theseshunts in the immediate postoperative period. In a re-cent article, Aucejo et al.8 suggested that triple-phasecomputed tomography should be used for characteriz-ing these portosystemic shunts. They also recom-mended measuring intraoperative portal vein ﬂow. Ifpostreperfusion portal vein ﬂow is less than 1L/minute, shunt ligation should be indicated to avoidthe risk of postoperative portal vein thrombosis.8Portosystemic shunts, although detected in sectionalstudies (computed tomography or magnetic resonance),should be evaluated by conventional angiography,which allows not only their demonstration but also therecognition of their precise routes of connection. Whenidentiﬁed, they can be embolized, as demonstrated inthis case, with speciﬁc methods such as the use oflarge-caliber occluding devices (Amplatzer or wire seg-ments) or the reduction of their ﬂow with simultaneousoccluding techniques (balloon catheters).9In conclusion, large portosystemic shunts may per-sist after liver transplantation in patients with cirrhosisif they are not ligated during transplant surgery. Theseshunts may allow the development of hepatic enceph-alopathy in the absence of signiﬁcant liver damage.Embolization of these shunts is a potential and effectivetreatment for this condition.REFERENCES1. Zwingmann C. Nuclear magnetic resonance studies of en-ergy metabolism and glutamine shunt in hepatic encepha-lopathy and hyperammonemia. J Neurosci Res 2007;85:3429-3442.2. Ibukuro K, Tsukiyama T, Mori K, Inoue Y. Veins of Retziusat CT during arterial portography: anatomy and clinicalimportance. Radiology 1998;209:793-800.3. Ferenci P, Lockwood A, Mullen K, Tarter R, Weissenborn K,Blei AT, and the Members of the Working Party. Hepaticencephalopathy. Deﬁnition, nomenclature, diagnosis, andquantiﬁcation: ﬁnal report of the working party at the 11thWorld Congress of Gastroenterology, Vienna, 1998. Hepa-tology 2002;35:716-721.4. Bilbao JI, Arias M, Herrero JI, Iglesias A, Martinez-RegueiraF, Alejandre PL, et al. Percutaneous transhepatic treatmentof a posttransplant portal vein thrombosis and a preexist-ing splenorenal shunt. Cardiovasc Intervent Radiol 1995;25:323-326.5. De Carlis, Del Favero E, Rondinara G, Belli LS, SansaloneCV, Zani B, et al. The role of spontaneous portosystemicshunts in the course of orthotopic liver transplantation.Transpl Int 1992;5:9-14.6. Zamora CA, Sugimoto K, Tsurusaki M, Yamaguchi M, IzakiK, Taniguchi T, et al. Portosplenic blood ﬂow separation ina patients with portosystemic encephalopathy and a spon-taneous splenorenal shunt. J Vasc Interv Radiol 2004;15:875-879.7. Shah SR, Pramesh CS, Desmukh HL, Mathur SK. Splenicartery embolization for variceal hemorrhage followingblocked distal splenorenal shunt. Hepatogastroenterology2003;50:1167-1168.8. Aucejo FN, Hashimoto K, Quintini C, Kelly D, Vogt D,Winans C, et al. Triple-phase computed tomography andintraoperative ﬂow measurements improve the manage-ment of portosystemic shunts during liver transplantation.Liver Transpl 2008;14:96-99.9. Bilbao JI, Arias M, Longo JM, Alejandre PL, Betes MT,Elizalde AM. Embolization of nonvariceal portosystemic col-laterals in transjugular intrahepatic portosystemic shunts.Cardiovasc Intervent Radiol 1997;20:149-153.Figure 7. Late venous phase of a splenic arteriogram. Thereis no hepatofugal ﬂow toward the superior mesenteric vein.114 HERRERO ET AL.LIVER TRANSPLANTATION.DOI 10.1002/lt. Published on behalf of the American Association for the Study of Liver Diseases

Hepatic encephalopathy after liver transplantation in a patient with a normally functioning graft: Treatment with embolization of portosystemic collaterals

Universidad de Navarra

Hepatic encephalopathy after liver transplantation in a patient with a normally functioning graft: Treatment with embolization of portosystemic collaterals

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