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CASE REPORT Endovascular treatment for pseudoaneurysms arising from the hepatic artery after liver transplantation Ashok Thorat, Chen-Fang Lee, Tsung-Han Wu, Kuang-Tse Pan, Sung-Yu Chu, Hong-Shiue Chou, Kun-Ming Chan, Ting-Jung Wu, Wei-Chen Lee* Chang-Gung Transplantation Institute, Department of Liver and Transplantation Surgery, Chang-Gung Memorial Hospital, College of Medicine, Chang-Gung University, Taoyuan, Taiwan Received 20 August 2013; received in revised form 6 July 2014; accepted 14 July 2014 KEYWORDS hepatic artery; liver transplantation; pseudoaneurysm; stent Summary Hepatic artery pseudoaneurysm after liver transplantation is an uncommon but potentially lethal complication. Early diagnosis and treatment are essential to avoid life- threatening hemorrhage in these patients. We herein report the case of three patients who developed hepatic artery pseudoaneurysms after living donor liver transplantation. Two pa- tients presented with massive duodenal bleeding secondary to erosion of the hepatic artery into the bile duct, and one patient presented with intra-abdominal bleeding. These patients were managed by catheter-based minimal invasive endovascular procedures including coil embolization and stent grafting. All the patients were treated successfully with uneventful re- covery. This technique can be considered as an effective treatment option for hepatic artery pseudoaneurysms instead of a difficult surgical intervention. Copyright ª 2014, Asian Surgical Association. Published by Elsevier Taiwan LLC. All rights reserved. 1. Introduction Hepatic artery pseudoaneurysm is a rare complication after orthotopic liver transplantation with a reported incidence of 0.5e2.0%. 1,2 This usually occurs within the first few months following a transplantation and are commonly re- ported to be associated with massive bleeding and localized infection. 3,4 Conflicts of interest: All contributing authors declare no con- flicts of interest. * Corresponding author. Chang-Gung Transplantation Institute, Department of Liver and Transplantation Surgery, Chang-Gung Memorial Hospital, College of Medicine, Chang Gung University, Number 5, Fu-Hsing Street, Kwei-Shan, Taoyuan, Taiwan. E-mail address: [email protected] (W.-C. Lee). + MODEL Please cite this article in press as: Thorat A, et al., Endovascular treatment for pseudoaneurysms arising from the hepatic artery after liver transplantation, Asian Journal of Surgery (2014), http://dx.doi.org/10.1016/j.asjsur.2014.07.001 http://dx.doi.org/10.1016/j.asjsur.2014.07.001 1015-9584/Copyright ª 2014, Asian Surgical Association. Published by Elsevier Taiwan LLC. All rights reserved. Available online at www.sciencedirect.com ScienceDirect journal homepage: www.e-asianjournalsurgery.com Asian Journal of Surgery (2014) xx,1e5

Pseudoaneurysms arising from hepatic artery

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Asian Journal of Surgery (2014) xx, 1e5

Available online at www.sciencedirect.com

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journal homepage: www.e-asianjournalsurgery.com

CASE REPORT

Endovascular treatment forpseudoaneurysms arising from the hepaticartery after liver transplantation

Ashok Thorat, Chen-Fang Lee, Tsung-Han Wu, Kuang-Tse Pan,Sung-Yu Chu, Hong-Shiue Chou, Kun-Ming Chan, Ting-Jung Wu,Wei-Chen Lee*

Chang-Gung Transplantation Institute, Department of Liver and Transplantation Surgery, Chang-GungMemorial Hospital, College of Medicine, Chang-Gung University, Taoyuan, Taiwan

Received 20 August 2013; received in revised form 6 July 2014; accepted 14 July 2014

KEYWORDShepatic artery;liver transplantation;pseudoaneurysm;stent

Conflicts of interest: All contributflicts of interest.* Corresponding author. Chang-Gun

Department of Liver and TransplantMemorial Hospital, College of MedicNumber 5, Fu-Hsing Street, Kwei-Shan

E-mail address: [email protected]

Please cite this article in press as: Tliver transplantation, Asian Journal o

http://dx.doi.org/10.1016/j.asjsur.201015-9584/Copyright ª 2014, Asian Su

Summary Hepatic artery pseudoaneurysm after liver transplantation is an uncommon butpotentially lethal complication. Early diagnosis and treatment are essential to avoid life-threatening hemorrhage in these patients. We herein report the case of three patients whodeveloped hepatic artery pseudoaneurysms after living donor liver transplantation. Two pa-tients presented with massive duodenal bleeding secondary to erosion of the hepatic arteryinto the bile duct, and one patient presented with intra-abdominal bleeding. These patientswere managed by catheter-based minimal invasive endovascular procedures including coilembolization and stent grafting. All the patients were treated successfully with uneventful re-covery. This technique can be considered as an effective treatment option for hepatic arterypseudoaneurysms instead of a difficult surgical intervention.Copyright ª 2014, Asian Surgical Association. Published by Elsevier Taiwan LLC. All rightsreserved.

ing authors declare no con-

g Transplantation Institute,ation Surgery, Chang-Gungine, Chang Gung University,, Taoyuan, Taiwan.g.tw (W.-C. Lee).

horat A, et al., Endovascular treaf Surgery (2014), http://dx.doi.o

14.07.001rgical Association. Published by E

1. Introduction

Hepatic artery pseudoaneurysm is a rare complication afterorthotopic liver transplantation with a reported incidenceof 0.5e2.0%.1,2 This usually occurs within the first fewmonths following a transplantation and are commonly re-ported to be associated with massive bleeding and localizedinfection.3,4

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lsevier Taiwan LLC. All rights reserved.

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Figure 1 Hepatic artery angiography for Case 1. (A) Pseudoaneurysm arose from the anterior branch of the right hepatic artery.(B) Pseudoaneurysm was embolized by coil. The liver parenchyma perfusion was preserved from the posterior branch of the righthepatic artery.

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Pseudoaneurysms of the hepatic artery may be asymp-tomatic and detected during imaging evaluation for otherreasons. They may present with nonspecific symptoms suchas hemobilia, a falling hemoglobin level, unexplained fever,or graft dysfunction or may manifest with gastrointestinal(GI) bleeding or hemoperitoneum, which is often presentedas profound shock.5,6 Early diagnosis requires a high level ofsuspicion and close monitoring. With early diagnosis, anumber of treatment options exist to prevent life-threatening hemorrhage and for graft salvage. Existingtreatment options that allow for preservation of the arte-rial flow into the graft are surgical resection and revascu-larization, and catheter-based minimal invasiveendovascular treatments such as coil embolization andstent grafting.5,7e9

Herein, we report a series of three cases of hepatic ar-tery pseudoaneurysms following orthotopic living donorliver transplantation that were treated successfully by coilembolization and endovascular stent grafting in ourinstitute.

Between January 2007 and December 2011, a total of219 patients underwent living donor liver transplantation atour institute. Three patients (1.37%) developed hepaticartery pseudoaneurysms after the transplantation. All thepatients underwent minimal invasive endovascular treat-ment. The demographic, clinical, and laboratory data werecollected and reviewed.

2. Case Reports

2.1. Case 1

A 51-year-old man underwent living donor liver trans-plantation for hepatitis B-related liver cirrhosis and hepa-tocellular carcinoma in 2007. The postoperative course wasuneventful and the patient recovered well. He was dis-charged after 1 month and regularly received immunosup-pressant drugs, tacrolimus, and mycophenolatemofetil.The follow-up computed tomography (CT) scan at 3 monthspost-transplantation revealed biliary anastomotic stricturewith moderate dilatation of intrahepatic biliary ducts.

Please cite this article in press as: Thorat A, et al., Endovascular trealiver transplantation, Asian Journal of Surgery (2014), http://dx.doi.o

Endoscopic retrograde cholangiopancreatography andbiliary stenting were carried out to treat the condition. Thepatient was treated with antibiotics for biliary tractinfection caused by Escherichia coli and Pseudomonasaeruginosa. Two weeks after biliary stenting, the patienthad an episode of upper GI bleeding. When the patient wassubjected to celiac angiography, inflammatory change overthe duodenum with subacute bleeding from the gastrodu-odenal artery was noted. Superselective catheterizationand coil embolization were performed to control thebleeding. Three weeks later, the patient had anotherepisode of upper GI bleeding due to hemobilia, as evi-denced by endoscopy showing bleeding from the ampullarypapilla in the duodenum. Repeated angiography confirmeda pseudoaneurysm arising from the anterior branch of thehepatic artery. Coil embolization of the anterior branch ofthe right hepatic artery distal and proximal to the neck ofpseudoaneurysm was performed (Fig. 1). Postembolizationangiography showed complete occlusion of the segmentcontaining pseudoaneurysm and good flow in the posteriorbranch. The patient recovered well with no further epi-sodes of bleeding. The patient was discharged 1 monthlater and regularly followed up until now.

2.2. Case 2

A 52-year-old patient underwent living donor liver trans-plantation for alcoholic liver cirrhosis with ChildePugh Cstatus in 2010. This patient had diabetes mellitus, atrialfibrillations, and chronic kidney disease prior to the oper-ation. Postoperative course was uneventful and the patientwas discharged 1 month after the transplantation. Twomonths after the transplantation, the patient had a spike offever and an elevation of liver function test values. Ultra-sonography of the abdomen showed liver abscess. CT-guided pigtail catheter drainage of liver abscess was per-formed. E. coli and Enterococcus faecium growth was notedon pus culture. After 1 week of antibiotic treatment, pusculture data revealed the growth of E. faecium, Steno-trophomonas maltophilia, and yeast-like micropathogen.The patient was continuously treated with antibiotics andfluconazole. After 2 weeks of catheter drainage, the

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Hepatic artery pseudoaneurysm in liver transplantation 3

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patient developed upper GI bleeding and melena. Pan-endoscopy was performed, and the results revealedbleeding from the ampullary papilla. Celiac angiographyshowed A saccular pseudoaneurysm at the distal properhepatic artery with anastomotic narrowing of the proximalhepatic artery and poststenotic dilatation. Subacutebleeding was noted from the pseudoaneurysm. After se-lective cannulation of the right hepatic artery, successfulangioplasty of the hepatic artery with placement of endo-vascular stent graft (Abbott, Jostent, Abbott Vasculat Inc.Santa Clara, CA, USA, 3 mm/26 mm) to cover pseudoa-neurysm was performed (Fig. 2). Postprocedure angiog-raphy showed successful exclusion of a pseudoaneurysmwith a good flow to the graft and marked improvement inthe luminal diameter of the hepatic artery without signifi-cant residual stenosis. The patient was continuouslytreated with antibiotics, recovered well, and was dis-charged 1 month later.

2.3. Case 3

A 65-year-old male had recurrent hepatocellular carcinomaand underwent living donor liver transplantation in 2011.On the 8th postoperative day, the patient underwent re-exploration due to a significant drop in hemoglobin leveldespite blood transfusion. Diffuse oozing was noted aroundthe celiac trunk. Hemostasis materials were applied, andthe bleeding was controlled. The patient had to be re-explored again 7 days later due to persistence of bleedingthat revealed active bleeding from hepatic artery anasto-mosis. The bleeding was sealed off with hemostasis mate-rials. The patient was subjected to celiac angiography dueto persistent drop in hemoglobin level. The angiographicresults revealed pseudoaneurysms in the left gastric arteryand hepatic artery anastomosis. Left gastric artery pseu-doaneurysm was successfully occluded with coil emboliza-tion. An endovascular stent graft (Jostent, Abbott VasculatInc. Santa Clara, CA, USA, 4 mm/16 mm) was placed andhepatic artery pseudoaneurysm was excluded (Fig. 3).Postprocedure angiography showed adequate flow in the

Figure 2 Hepatic artery angiography for Case 2. (A) Pseudoaneuafter placement of stent graft.

Please cite this article in press as: Thorat A, et al., Endovascular trealiver transplantation, Asian Journal of Surgery (2014), http://dx.doi.o

liver graft. Bacterial cultures for blood, sputum, and urinewere performed and only sputum culture showed S. mal-tophilia growth. The patient recovered well and was dis-charged 2 weeks later. The patient is doing well andregularly followed up.

3. Discussion

Pseudoaneurysms of the hepatic artery after liver trans-plantation is rare but a potentially lethal complication.Hepatic artery pseudoaneurysms are classified as intra-hepatic and extrahepatic. Intrahepatic pseudoaneurysmsoccur in 31% of the cases, whereas extrahepatic pseudoa-neurysms occur in 69% of the cases.10 Intrahepatic pseu-doaneurysms are mostly the result of iatrogenic injury,whereas extrahepatic pseudoaneurysms are commonlyassociated with localized infection or are due to technical,anastomotic problems.1 In this series, intrahepatic pseu-doaneurysm in Case 1 might be due to iatrogenic injuryduring stenting biliary stenosis, and extrahepatic pseudoa-neurysms in Cases 2 and 3 were due to abscess erosion tothe artery and technical error while performing the arterialangulation at the anastomotic site, respectively. Pseudoa-neurysms may rupture into the peritoneum or GI tractcausing life-threatening hemorrhage with profoundshock11,12 or rupture into biliary tract causing hemobilia.13

Therefore, the diagnosis and treatment of pseudoaneur-ysms at the earliest are important for graft and patientsurvival. Regular Doppler ultrasonography in the early post-transplant period can be used to detect pseudoaneurysms,especially when the patients have invasive intervention orrepeated infection.

Classic treatment options are surgical resection of thepseudoaneurysms and revascularization of the injuredvessel segment by arterial reconstruction, ligation of thehepatic artery, and retransplantation.2,6,7 However,retransplantation or surgical revascularization is associatedwith poor outcome and direct reconstruction may not befeasible in an infected field. In addition, surgical inter-vention near the hepatic vessels is a major procedure,

rysm at the anastomotic site. (B) Pseudoaneurysm disappeared

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Figure 3 Hepatic artery angiography for Case 3. (A) Pseudoaneurysm at the anastomotic site and the left gastric artery. (B)Pseudoaneurysm disappeared after placement of stent graft. The left gastric artery was embolized by coil.

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which is complicated due to the presence of intra-abdominal adhesions. Coil embolization of the aneurismalsac or exclusion of the pseudoaneurysms by stent graft hasbeen reported as an important and the most effectivetreatment option even in an emergency setting.5,9,14 Se-lective microcatheterization of the aneurysmal sac anddeploying coils to pack the lesions definitively close thepseudoaneurysm with preservation of the arterial flow tothe graft if the neck of pseudoaneurysm is narrow. If theneck of pseudoaneurysm is broad, endovascular stentgrafting to exclude the pseudoaneurysm proves to be themost effective treatment option. This technique may beperformed immediately following the diagnostic angiog-raphy, and has the unique advantage of completelyexcluding the pseudoaneurysm without injecting embolicagents into the aneurysm and concomitantly preserving thearterial blood flow to the graft. Until now, limited evidencesuggests that stenting of the hepatic artery pseudoaneur-ysm during an acute hemorrhage can be successfully per-formed in elective as well as emergency setting. Thisprompted us to use endovascular stent grafting as the pri-mary treatment for hepatic artery pseudoaneurysms.

The mortality of a bleeding hepatic pseudoaneurysmfollowing a liver transplantation is very high owing to acombination of factors such as the poor general conditionof the patient, poor graft function, and medical complica-tions in the postoperative course.2 When the recipients arein an infectious state, an existing hepatic pseudoaneurysmresulting from an infection should be ruled out. An infec-tious pseudoaneurysm easily causes arterial thrombosis andgraft failure after surgical or radiological intervention.8,15

Currently, an endovascular stent is a treatment option foran infectious artery pseudoaneurysm. However, prolongedantibiotic treatment is necessary to achieve freedom frominfection.16e18 As long as the infection is eradicated,patency of the artery can be sustained, increasing thelikelihood of the patients survival.

In conclusion, hepatic artery pseudoaneurysm is a rarevascular complication after liver transplantation. Earlydetection with Doppler ultrasonography, CT scan, orangiogram is crucial to save the lives of these patients. Coilembolization of aneurysmal sac or placement of a stent

Please cite this article in press as: Thorat A, et al., Endovascular trealiver transplantation, Asian Journal of Surgery (2014), http://dx.doi.o

graft is a minimally invasive alternative to surgery anddefinitively excludes a bleeding hepatic artery pseudoa-neurysm. This technique can be considered as an effectivetreatment option for hepatic artery pseudoaneurysminstead of a difficult surgical repair.

References

1. Leelaudomlipi S, Bramhall SR, Gunson BK, et al. Hepatic-arteryaneurysm in adult liver transplantation. Transpl Int. 2003;16:257e261.

2. Marshall MM, Muiesan P, Srinivasan P, et al. Hepatic arterypseudoaneurysms following liver transplantation: incidence,presenting features and management. Clin Radiol. 2001;56:579e587.

3. Patel JV, Weston MJ, Kessel DO, Prasad R, Toogood GJ,Robertson I. Hepatic artery pseudoaneurysm after liver trans-plantation: treatment with percutaneous thrombin injection.Transplantation. 2003;75:1755e1757.

4. Lowell JA, Coopersmith CM, Shenoy S, Howard TK. Unusualpresentations of nonmycotic hepatic artery pseudoaneurysmsafter liver transplantation. Liver Transpl Surg. 1999;5:200e203.

5. Maleux G, Pirenne J, Aerts R, Nevens F. Case report: hepaticartery pseudoaneurysm after liver transplantation: definitivetreatment with a stent-graft after failed coil embolisation. BrJRadiol. 2005;78:453e456.

6. Madariaga J, Tzakis A, Zajko AB, et al. Hepatic artery pseu-doaneurysm ligation after orthotopic liver transplantationdareport of 7 cases. Transplantation. 1992;54:824e828.

7. Bonham CA, Kapur S, Geller D, Fung JJ, Pinna A. Excision andimmediate revascularization for hepatic arterypseudoaneurysmfollowing liver transplantation. Transplant Proc. 1999;31:443.

8. Almogy G, Bloom A, Verstandig A, Eid A. Hepatic artery pseu-doaneurysm after liver transplantation. A result of trans-hepatic biliary drainage for primary sclerosing cholangitis.Transpl Int. 2002;11:53e55.

9. Muraoka N, Uematsu H, Kinoshita K, et al. Covered coronarystent graft in the treatment of hepatic artery pseudoaneurysmafter liver transplantation. J Vasc Interv Radiol. 2005;16:300e302.

10. Saad WE. Management of nonocclusive hepatic artery compli-cations after liver transplantation. Tech Vasc Interv Radiol.2007;10:221e232.

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11. Slater K, Ludkowski M, Mehling J, et al. Hepatic artery pseu-doaneurysmdduodenal fistula after living donor liver trans-plant. Clin Transplant. 2004;18:734e736.

12. Riedmann B, Pernthaler H, Konigsrainer A, Nachbaur K,Vogel W, Margreiter R. Life-threatening gastrointestinalbleeding after liver transplantation due to hepatic arterypseudoaneurysm perforating into the common bile duct. A casereport. Transpl Int. 1995;8:492e495.

13. Leonardi LS, Soares Jr C, Boin IF, Oliveira VC. Hemobilia aftermycotic hepatic artery pseudoaneurysm after liver trans-plantation. Transplant Proc. 2001;33:2580e2582.

14. Elias G, Rastellini C, Nsier H, et al. Successful long-term repairof hepatic artery pseudoaneurysm following liver

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transplantation with primary stent-grafting. Liver Transpl.2007;13:1346e1348.

15. Dharancy S, Bulois P, Sergent G, Pasturel U, Seddick M, Paris JC.Hepatic mycotic aneurysms. J Hepatol. 2003;38:696e697.

16. Jaffers GJ, Bohannon WT, Buckley C. Endovascular repair of apancreatic allograft mycotic aneurysm: two-year follow-up. JEndovasc Ther. 2011;18:607e610.

17. Ferrero E, Ferri M, Carbonatto P, et al. Endovascular treatmentof a symptomatic mycotic aneurysm of the peroneal artery.Ann Vasc Surg. 2011;25:982. e11e14.

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