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Endovascular Stent Placement in Patients With Hepatic Artery Stenoses or Thromboses After Liver Transplant

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doi:10.1016/j.transproceed.2007.12.027 Copyright © 2008 Elsevier Inc. All rights reserved.

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Endovascular Stent Placement in Patients With Hepatic Artery Stenoses or Thromboses After Liver Transplant

F. Boyvata, C. Aytekina, A. Harmana, Ş. Sevmişb, H. Karakayalib and M. Haberalb, , aDepartment of Radiology, Başkent University Medical Faculty, Ankara, TurkeybDepartment of General Surgery, Başkent University Medical Faculty, Ankara, Turkey. Available online 6 February 2008.

Abstract

Hepatic artery stenosis or thrombosis following liver transplant is a potentially life-threatening complication. Successful liver transplant depends on uncompromised hepatic arterial inflow. Early diagnosis and treatment of complications prolong graft survival. Interventional radiologic techniques are frequently used to treat hepatic artery complications. Twenty patients with hepatic artery stenoses (n = 11) or thromboses (n = 9) were included in this study. Eighteen of the 20 patients were successfully treated by stent placement. In 9 patients, early endovascular interventions were performed 1 to 7 days after surgery. Two patients were operated owing to the effects of dissection and bleeding from the hepatic artery. Repeat endovascular interventions were performed 10 times in 6 patients. Follow-up ranged from 5 months to 4.5 years. Nine patients with patent hepatic arteries died during follow-up owing to reasons unrelated to the hepatic artery interventions. In 3 patients, the stents became occluded at 3, 5, and 9 months after surgery but no clinical symptoms were present.

Article Outline

Materials and Methods Results Discussion References

The incidence of hepatic artery thromboses in adults varies from 2.6% to 20%. It is a life-threatening complication.[1] and [2] Patients with hepatic artery thromboses may present with acute graft failure, hepatic necrosis with fulminant septicemia, abscess, biliary leak, or stricture. The presentation of a delayed hepatic artery thrombosis varies.3 Hepatic artery stenoses rates as high as 11% have been reported.4 Early recognition and treatment are important to prevent liver damage and progression to hepatic artery thromboses. Surgical revascularization, in many centers, has been the first choice for treatment of early hepatic artery thromboses but recently, endovascular interventions have achieved good success rates with results comparable to those of surgery. Retransplantation, if required, carries with it a high mortality rate, which also is limited by organ availability.5 Interventional radiology including percutaneous transluminal angioplasty, thrombolysis, and stent placement are frequently used to treat vascular complications after liver transplant. In this study, we present our experiences managing hepatic artery stenoses and thromboses following liver transplant and assess the feasibility of stent placement to treat this potentially life-threatening condition. Materials and Methods

Between March 2000 and February 2007, 20 patients (10 children, 10 adults; 5 female, 15 male; mean age, 27.6 years; age range, 6 months to 62 years) with hepatic artery problems following transplant were treated. Table 1 summarizes the patients’ relevant characteristics. Four patients with hepatic artery problems received a whole liver graft from deceased donors, and the remaining patients received a transplant from a living donor. Eight patients received a right lobe, 1 received a left lobe, and 7 received a lateral segment transplant. The indications for endovascular treatment for these patients were hepatic artery thromboses (n = 9) and hepatic artery stenoses (n = 11). Doppler ultrasound was used initially to diagnose the hepatic artery problems. If necessary, computed tomography angiography or conventional angiography was performed also. Endovascular interventions were performed via right femoral artery access. A 6-French vascular sheath was placed and after selective catheterization of the celiac trunk or the superior mesenteric artery, a microcatheter and a 0.016-inch glidewire (Terumo, Tokyo, Japan) were negotiated through the stenosis or the occlusion. Then, a 0.014-inch guidewire was placed in the hepatic artery. Once the guidewire was placed, a 6-French guiding catheter was advanced to the origin of the celiac trunk or the superior mesenteric artery. If the luminal diameter of the hepatic artery was decreased by more than 50%, a percutaneous transluminal angioplasty was performed (Fig 1). Before percutaneous transluminal angioplasty, heparin (100 units/kg) was injected intravenously. The percutaneous transluminal angioplasty was performed with a monorail balloon. Balloon size was selected according to the diameter of the hepatic artery, distal to the stenosis. If the hepatic artery remained stenotic after balloon dilatation (more than 20% stenosis) or if extravasation of contrast material occurred, then stents were placed (Fig 2). Intra-arterial thrombolysis was performed during the procedure.

Table 1. Summary of Patients

Pt No.

Sex/Age

Preoperative Diagnosis

Graft

Post Op Int Day

Angiographic Findings

1

M/55

HBV-cirrhosis.

Right lobe

129

HAS-90%

2

F/14

’s disease

Left lateral

210

HAS-90%

3

M/10

’s disease

Left lateral

11

HAS-75%

4

M/62

HCV-cirrhosis

Whole

189

HAS-80%

5

M/16

’s disease

Left lobe

18

HAS-90%

6

M/39

HBV-cirrhosis

Right lobe

10

HAT

7

M/44

HBV-cirrhosis

Whole

34

HAS-70%

8

M/49

HBV-cirrhosis

Right lobe

4

HAT

9

M/54

HBV-cirrhosis

Whole

11

HAS-75%, dissection

10

F/13

Tyrosinemia-HCC

Right lobe

1

HAT

11

F/24

Autoimmune hepatitis

Right lobe

2

HAT

12

F/44

HBV-cirrhosis

Right lobe

14

HAS-75%

13

M/9

Tyrosinemia-HCC

Left lateral

1

HAS-90%

14

M/32

HBV-cirrhosis

Right lobe

5

HAT

15

M/8

Biliary atresia

Whole

6 h

HAT

16

M/4

PFIC

Left lateral

5

HAT

17

M/0.6

Biliary atresia

Left lateral

9

HAT

18

M/13

Cryptogenic

Left lobe

5

HAS-90%

19

M/36

HBV-cirrhosis

Right lobe

26

HAS-80%

20

F/0.6

PFIC

Left lateral

7

HAT

Abbreviations: Pt, patient; Op, operative; HCV, hepatitis C virus; HBV, hepatitis B virus; HCC, hepatocellular carcinoma; PFIC, progressive familial intrahepatic cholestasis; Int, intervention.

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Fig 1. A 10-year-old boy underwent a left lateral segment liver transplant, endovascular intervention was performed 11 days after transplant. (A) A celiac arteriogram showing a high grade stenosis of the hepatic artery. (B) Percutaneous transluminal angioplasty and bare stent placement were performed but rupture was occurred. © After placement of the graft-covered stent, contrast extravasation stopped with good flow.

Display Full Size version of this image (464K)

Fig 2. A 13-year-old female, underwent a right lobe liver transplant, endovascular intervention was performed post operative 1 st day. (A) Celiac arteriogram showed occluded hepatic artery. (B) A micro catheter was advanced through the thrombosed hepatic artery showing distal flow. © Thrombolysis and PTA were performed with ineffective flow. (D) Wall-stent was placed across the hepatic artery resulting in improved flow.

In 9 patients, stents (wall-stents [boston Scientific, Natick, Mass], coronary stents [boston Scientific], graft-covered stents [Jo Stents, Abbott vascular devices, Holland B.V. The Netherlands], over-and-under [Medical Ventures Corp, Richmond, Canada]) were placed during the endovascular procedures between 1 and 7 days after surgery; in 7 patients, they were placed between 8 and 28 days after surgery; and in 4 patients, they were placed after 28 days after surgery. Stents were bare (n = 13) or graft-covered (n = 7). The main indications for using graft-covered stents were rupture of the hepatic artery during endovascular intervention and early postoperative intervention. Results

Technical success was achieved in 18 of 20 endovascular procedures. Two patients required an operation, 1 owing to the effects of dissection and the other owing to bleeding from the hepatic artery. Five ruptures were seen during the initial percutaneous transluminal angioplasty of the hepatic artery; however, only 1 required a reoperation. The other patients with hepatic artery ruptures were managed by placing graft-covered stents. For patients with a hepatic artery thrombosis, intra-arterial thrombolysis was performed. Thrombolytic treatment was performed with a 4-French catheter after placement of a 0.014-inch guidewire in the distal hepatic artery. A “Y” connector was attached to the 4-French catheter while the 0.014-inch guidewire was placed, and 1 to 3 mg tPA or 50,000 to 250,000 IU urokinase was injected through the catheter. Mechanical fragmentation of the thrombus was performed with a balloon catheter. Continuous thrombolysis to lyse the thrombus was necessary only in 2 patients. Owing to early occlusion of the hepatic arteries, repeat endovascular interventions were performed 10 times in 6 patients. After stent placement, patients underwent anticoagulation. Anticoagulation in adult patients was accomplished with a combination of aspirin and clopidogrel bisulfate, and pediatric patients were given aspirin and dipyridamole. This was followed by Doppler ultrasonography to monitor vessel patency every day until discharge. Then, control Doppler ultrasonography was performed at 1 week, 1 month, 3 months, and 6 months. Follow-up angiography was scheduled for 1 year after transplant. Follow-up ranged from 5 months to 4.5 years. Nine patients with patent hepatic arteries died during follow-up owing to reasons unrelated to the hepatic artery interventions. At the 1-year follow-up angiography, minimal intimal hyperplasia was observed in 3 stents. In 3 patients, the stents became occluded at 3, 5, and 9 months after surgery, but clinical symptoms were not apparent. Discussion

Hepatic artery stenoses have been reported as occurring in 2% to 13% of patients undergoing liver transplant.6 Hepatic artery stenoses may be due to operative technique, vascular clamp injury, allograft rejection, preservation injury, anastomosis of the small arteries, or procoagulant disorders.7 Stenoses have been found to occur at the anastomotic site in 70% of patients with the disorder.6 Hepatic artery stenoses may be undetectable and cause insidious and persistent ischemic effects on the graft. Initially, the stenosis causes uncomplicated and reversible biliary ischemia; however, it later causes irreversible biliary necrosis, which leads to allograft dysfunction. Therefore, early detection of hepatic artery stenoses and treatment are crucial for good graft survival. Although, a hepatic artery stenosis after liver transplant is treated either by surgical repair or by retransplant, use of interventional radiologic procedures such as percutaneous transluminal angioplasty or application of stents has been reported.[8] and [9] The clinical presentation of a hepatic artery thrombosis varies from a mild elevation of liver enzyme and bilirubin levels to fulminant hepatic necrosis. Acute presentation is usually associated with an early hepatic artery thrombosis.10 Early hepatic artery thromboses have been reported as occurring in 2.6% to 20% of adults (age > 16 years), in 9% to 14.9% of pediatric patients (age, 1–16 years), and in as many as 30% of infants aged younger than 1 year.2 Once a hepatic artery thrombosis has been confirmed, immediate intervention is indicated, be it surgical or endovascular. Recently, successful endovascular interventions for hepatic artery stenoses or hepatic artery thromboses, were reported from several institutions. There is current discussion regarding the best time for the earliest endovascular intervention after liver transplant. To safely perform endovascular interventions, Kodama and associates suggest 7 days; Ueno and associates suggest 3 weeks after liver transplant.[6] and [11] In the current study, we performed endovascular interventions within 7 days after transplant in 9 patients. Although, we encountered extravasation or rupture of the hepatic arteries in 5 of these 9 patients, we used graft-covered stents to solve this problem in all but 1 patient. Our failure in that 1 patient was due to the hepatic artery diameter being larger than the largest of our stent grafts. With the graft-covered stents currently available, there is no time restriction after surgery for performing endovascular interventions. Kodama and associates6 and Wael and associates,12 in their series, found good results for treating hepatic artery thromboses with percutaneous transluminal angioplasty. However, in the current series, we found that the initial percutaneous transluminal angioplasty was not effective, and so stents were placed. Because the percutaneous transluminal angioplasties in 16 of our patients were performed within 28 days after transplant, we suggest that better outcomes might have occurred had we performed earlier postoperative interventions. Ueno and associates accomplished primary stenting of the hepatic arteries in 26 adult patients with a 78% patient survival rate, suggesting that stent placement in the hepatic arteries is well tolerated and effective. Their mean time for intervention after transplant was 203 days (range, 34–784 days); that is far beyond from our mean intervention time of 34.6 days (range, 6 hours-210 days). Hepatic artery occlusion is a real emergency requiring endovascular or surgical intervention. In all of our patients, we used thrombolytic treatment as well as an under-sized balloon for mechanical fragmentation of thrombus; afterward, stents were placed. Although there is a general reluctance to use thrombolytic agents in the 3 weeks following major surgery, we observed extravasation of contrast material through the arterial anastomosis in only 1 patient, and this was treated with a graft-covered stent. Thus, while it is obvious that early postoperative thrombolytic intervention may pose the risk of bleeding, limited dosages of these agents (1 to 3 mg tPA or 50 000 to 250 000 IU urokinase) may be safely given. (In our 2 patients administered infusions of thrombolytic agents, no bleeding complications were encountered.) Early placement of a stent in the graft hepatic artery is technically feasible. In particular, graft-covered stents may be placed safely and effectively in the early postoperative period.

References

1 N.B. Amesur and A.B. Zajko, Interventional radiology in liver transplantation, Liver Transpl 12 (2006), p. 330. View Record in Scopus | Cited By in Scopus (2) 2 C.K. Oh, S.J. Pelletier and R.G. Sawyer et al., Uni- and multi-variate analysis of risk factors for early and late hepatic artery thrombosis after liver transplantation, Transplantation 27 (2001), p. 767. View Record in Scopus | Cited By in Scopus (39) 3 B.J. Stange, M. Glanemann and N.C. Nuessler et al., Hepatic artery thrombosis after adult liver transplantation, Liver Transpl 9 (2003), p. 612. Abstract | View Record in Scopus | Cited By in Scopus (59) 4 C. Vignali, I. Bargellini and R. Cioni et al., Diagnosis and treatment of hepatic artery stenosis after orthotopic liver transplantation, Transplant Proc 36 (2004), p. 2771. Abstract | Full Text + Links | PDF (139 K) | View Record in Scopus | Cited By in Scopus (8) 5 M.G. Tian, W.K. Tso and C.M. Lo et al., Treatment of hepatic artery thrombosis after orthotopic liver transplantation, Asian J Surg 27 (2004), p. 213. View Record in Scopus | Cited By in Scopus (6) 6 Y. Kodama, Y. Sakuhara and D. Abo et al., Percutaneous transluminal angioplasty for hepatic artery stenosis after living donor liver transplantation, Liver Transpl 12 (2006), p. 465. View Record in Scopus | Cited By in Scopus (2) 7 J.B. Karani, D.F. Yu and P.A. Kane, Interventional radiology in liver transplantation, Cardiovasc Intervent Radiol 28 (2005), p. 271. View Record in Scopus | Cited By in Scopus (4) 8 J. Zhou, J. Fan and J.H. Wang et al., Continuous transcatheter arterial thrombolysis for early hepatic artery thrombosis after liver transplantation, Transplant Proc 37 (2005), p. 4426. Abstract | Full Text + Links | PDF (158 K) | View Record in Scopus | Cited By in Scopus (1) 9 U. Settmacher, B. Stange and R. Haase et al., Arterial complications after liver transplantation, Transpl Int 13 (2000), p. 372. View Record in Scopus | Cited By in Scopus (43) 10 M.A. Silva, P.S. Jambulingam and B.K. Gunson et al., Hepatic artery thrombosis following orthotopic liver transplantation: a 10-year experience from a single centre in the United Kingdom, Liver Transpl 12 (2006), p. 146. View Record in Scopus | Cited By in Scopus (15) 11 T. Ueno, G. and A. et al., Clinical outcomes from hepatic artery stenting in liver transplantation, Liver Transpl 12 (2006), p. 422. View Record in Scopus | Cited By in Scopus (8) 12 W.E. Saad, M.G. Davies and N.E. Saad et al., Catheter thrombolysis of thrombosed hepatic arteries in liver transplant recipients: predictors of success and role of thrombolysis, Vasc Endovascular Surg 41 (2007), p. 19. View Record in Scopus | Cited By in Scopus (1)

Address reprint requests to Mehmet Haberal, MD, FACS, FICS (Hon), Başkent University Rektorluk, 1. Cad. No:77 Kat:4, Bahcelievler, 06490, Ankara, Turkey.

Transplantation Proceedings Volume 40, Issue 1, January-February 2008, Pages 22-26

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