Recent Developments in Transplantation Medicine
	Liver Transplantation

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The Role of Vascular and Interventional Radiology in the Liver Transplant Patient

Norman G. Diamond

Introduction

The interventional radiologist plays a critical role in the multi-disciplinary approach to the liver transplant patient. Pretransplant, the interventionalist uses diagnostic angiographic procedures to define the anatomy for the surgeon. Increasingly, successful interventional radiologic procedures such as transjugular intrahepatic portosystemic shunt (TIPS) and biliary stricture dilation allow transplantation to be delayed. In the posttransplant patient, interventional radiologic manipulation is more effective than surgery in the management of many postoperative complications.

Interventional radiology as a subspecialty of radiology arose following the introduction of diagnostic catheter angiography in the 1950s, as initially described by Seldinger.¹ Technical advances in angiography led to so-called interventional applications. One of the earliest was the use of diagnostic catheters for the treatment of gastrointestinal hemorrhage by infusion of vasoconstrictive drugs.² The development of the modern balloon dilatation catheter for transluminal angioplasty by Gruntzig et al³ in the mid-1970s was an important step in converting this predominantly diagnostic modality into a therapeutic one. More recent innovations include a variety of percutaneous drainage procedures and the use of vascular and biliary stents.

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Pretransplantation

Diagnostic Arteriography

The pretransplant evaluation is usually performed without angiography. Noninvasive modalities such as ultrasound, computed tomography, and magnetic resonance imaging have largely replaced angiography for diagnostic evaluation in the liver transplant population. However, on occasion angiography is necessary. Arteriography can easily define the arterial anatomy of the native liver if a significant abnormality or variation is suspected on noninvasive imaging. If the celiac trunk is narrowed by atherosclerosis or compression by the median arcuate ligament, then aortography not only confirms this prior to transplantation, but also gives precise anatomic detail.

Occasionally, a patient is referred for transplant with known or suspected thrombosis of the portal vein. The surgeon, before contemplating transplant, must be able to find a superior mesenteric vein or vein branch large enough to support the anastomosis to the donor portal vein. Cut-film superior mesenteric arteriography with tolazoline hydrochloride enhancement and prolonged venous filming can delineate this anatomy.

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Percutaneous Transhepatic Cholangiography, Biliary Drainage, and Stricture Dilation

Chronic biliary obstruction with subsequent hepatic failure is a common indication for liver transplantation. Primary sclerosing cholangitis, congenital obstructions, and surgical bile duct injuries account for many such candidates. In the course of evaluating these patients for transplantation, it is not unusual to find central ductal strictures that have not been completely treated. If so, liver function can be stabilized or even improved by repair of the underlying abnormality, and transplantation can be deferred. In some instances, this delay is critical in allowing other medical conditions to stabilize.

Our approach to these patients entails careful review of previous radiologic studies, particularly cholangiograms. We proceed with percutaneous transhepatic cholangiography (PTC) if the underlying

biliary anatomy is not well visualized or if incompletely treated underlying strictures are evident. The techniques for percutaneous access and drainage of the biliary tree have been well described.^4-8 Percutaneous transhepatic cholangiography is performed via a midaxillary puncture just above the inferolateral edge of the liver. If, after diagnostic study, obstruction is encountered, then internal-external biliary drainage is accomplished with an 8 or 10 French catheter. After 24-48 hours of external drainage, symptomatic strictures can be dilated with appropriately sized balloon dilatation catheters (see Figures 1a-c.). Drainage catheters are left across the lesions as stents for several weeks, as these strictures are notoriously elastic and can recur. Repeat dilatations, which can be performed on an outpatient basis, are frequently required. If strictures recur after three dilatations, then consideration must be given to placing metallic stents.⁹

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Transjugular Intrahepatic Portosystemic Shunt (TIPS)

Creating a portosystemic shunt within the liver was first accomplished over 10 years ago.¹⁰ An angioplasty catheter was used to dilate a tract within the liver between portal and hepatic veins. These early shunts almost always failed because of gradual closure of the shunt. Since the introduction of metallic stents to keep the shunts open, TIPS has become an increasingly important treatment for portal hypertension.^11,12

During the past three and one-half years, we have performed more than 250 TIPS procedures in an effort to treat acute or chronic variceal hemorrhage. Many of these patients were also under consideration for transplantation because of associated chronic liver failure. Portocaval and splenorenal shunting, the traditional surgical approaches, involve significant operative risk. These operations also induce scarring and adhesions which complicate subsequent surgical dissection during transplantation. For these reasons, at our institution TIPS is the preferred method of portal decompression prior to transplantation. A number of our patients, in whom bleeding was the major symptom, have been removed from the transplantation lists because of their successful course after TIPS.

Figure 1a.Biliary drainage in a 24-year-old male with a history of surgical repair of choledochal cyst as an infant, who presented with chronic cholangitis and multiple strictures. Three internal-external biliary drainage catheters were placed. Filling defects represented stones and debris.

Figures 1b, 1c.Repeat cholangiogram six weeks later just prior to removing access catheters revealed dramatic improvement in the appearance of the biliary tree. In the interim, four procedures were performed, in which stones were removed and strictures dilated to 10 mm. The patient is asymptomatic 18 months later.

We reserve surgical portosystemic shunting for the occasional patient in whom TIPS cannot be successfully performed.

TIPS is accomplished via a right internal jugular venous puncture. Through a long sheath placed in the right hepatic vein, a long needle is advanced through the back wall of a hepatic vein, through the liver substance, into a portal vein branch. Once this tract is established, it is dilated with a balloon dilatation catheter, and then permanently kept open by the deployment of a metallic stent, usually a Wallstent (see Figures 2a and 2b). The lower end of the stent is positioned near the confluence of the portal veins, leaving the main portal vein free of stent to facilitate subsequent portal venous anastomosis if transplantation becomes necessary. The upper end of the stent is placed in the hepatic vein. On occasion the upper end of the stent comes close to or even protrudes into the lumen of the inferior vena cava. This has not posed a serious problem at the time of transplant as long as the surgeon was aware of the shunt's anatomy. Nineteen of our patients have gone on to transplantation after TIPS.

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Venous Obstruction — Budd-Chiari Syndrome

Budd-Chiari syndrome due to focal hepatic vein stenoses is a rare cause of hepatic failure. Reports of successful angioplasty of these stenoses have appeared in the literature.^13,14 We have performed a TIPS procedure on one patient who had cirrhosis and hepatic vein stenosis. The stent extended from the portal vein to the proximal hepatic vein and thus dilated the hepatic vein stenosis.

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Posttransplant Interventions

Arterial Abnormalities

Diagnostic Arteriography of Hepatic Arterial Thromboses/Stenoses; Role of PTA:As many as 10% of hepatic grafts fail due to hepatic artery thrombosis or stenosis.¹⁵ Graft dysfunction, infarction, abscess, biloma, and bile duct stricture may occur as complications of hepatic artery thrombosis.¹⁶ Diagnosis of thrombosis/stenosis is now usually accomplished with color Doppler sonography,¹⁷ but arteriography is required for confirmation and precise anatomic detail. In some patients who are technically difficult to image with sonography, arteriography is the primary diagnostic procedure.

Figure 2a.TIPS procedure in a 40-year-old alcoholic with severe acute variceal hemorrhage. Initial transjugular entry into the portal vein was obtained with portal venogram, which revealed an enlarged coronary vein.
Figure 2b.Repeat portal venography after creation of TIPS shunt. A 12 mm Wallstent was deployed between the main portal vein and the right hepatic vein. The porto-atrial gradient was reduced from 27 mm pre-shunt to 8 mm Hg. The coronary vein was embolized with coils.

Transfemoral arteriogaphy is performed shortly after the diagnosis is suspected on Doppler studies. Aortography may be done initially if there is concern that the celiac trunk is narrowed or if there is an aorto-hepatic graft. Selective arteriography is then performed with a 4 or 5 French catheter. Because of tortuosity, multiple projections are often necessary to define the anatomy of an hepatic artery stenosis. Thrombosis of the artery is usually evident from one injection sequence.

Thrombolytic therapy has not been advocated for hepatic artery thrombosis.¹⁶ Many thromboses occur in the immediate postoperative period, when thrombolysis would be contraindicated due to bleeding complications. Also, most liver transplant surgeons believe that hepatic damage is irreversible once the artery is thrombosed.

Hepatic artery stenosis usually occurs at the anastomotic or peri-anastomotic site.¹⁶ In the former location, technical factors in performing the anastomosis are usually implicated; in the latter location, surgical clamp injury or intimal dissection is suspected.

The treatment of hepatic arterial anastomotic stenoses has traditionally been surgical, but percutaneous transluminal angioplasty (PTA) has assumed a greater role in the past several years.^18-20 In the first four to six weeks following the transplant, we are concerned that percutaneous transluminal angioplasty might result in rupture of the recently constructed anastomosis. Nevertheless, a recent report has described successful PTA as early as two weeks after transplantation.¹⁸ We consider many factors in deciding whether or not to dilate a hepatic artery stenosis. The tortuosity of the hepatic arterial bed, the proximity of the stricture to branch vessels, the caliber of the artery, and the ability of the patient to withstand operative repair are all important factors.

Ten years ago, most PTAs in moderate-sized vessels were performed with 7 French catheter systems, which were difficult to maneuver in tortuous vascular beds without risking intimal injury.

Currently, angioplasty balloons are available on catheters ranging from 3 to 5 French. These are much less traumatic. The guidewires are 0.014 to 0.018 inches and are essentially atraumatic. Because of these technical refinements, PTA is certainly a more viable option now (see Figures 3a and 3b). There are as yet, however, no convincing reports about the longevity of PTA in hepatic artery stenosis. Periodic Doppler ultrasound examination of post PTA stenoses is warranted. Redilation is still an option if recurrence is present.

Vascular stents, used routinely today for iliac, renal, and coronary stenoses, are usually not considered for the liver transplant population because of the tortuosity of the hepatic arterial bed, which makes delivery of metallic stents cumbersome. Also, the longevity of stent patency in medium-sized vessels is unproven. However, as delivery systems are miniaturized, stents will undoubtedly be used for cases in which PTA has failed or resulted in a complication. We have placed a stent across a long graft stenosis leading from an iliac artery to the donor hepatic artery (see Figures 4a-c). The vascular graft in this patient was straight and large in caliber, which facilitated stent placement.

Embolization of Post-Biopsy Pseudoaneurysms and Arteriovenous Fistulas: Liver biopsy after liver transplantation is a frequent routine procedure, rarely followed by significant intrahepatic hemorrhage or hemobilia. However, this potentially catastrophic complication of biopsy must be diagnosed and treated promptly.²¹ Hepatic arteriography accurately determines the presence of arterial injury. If an AV fistula or pseudoaneurysm is identified, it is embolized, usually with coils, as peripherally as possible, in order not to occlude non-traumatized vessels proximal to the site of injury. On occasion we have identified asymptomatic peripheral hepatic-artery-to-portal-venule fistulas during arteriography for unrelated reasons. These tiny fistulas also probably result from biopsy. No therapy is required.

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Venous Intervention

Portal Vein Recanalization; PTA of Portal Vein Stenoses: Portal vein thrombosis and stenosis are unusual complications of transplantation, occurring in less than 2% of all allografts.¹⁶ The classic symptom is variceal bleeding related to portal hypertension, but there may be no symptoms and very little alteration of liver function.²² Several reports indicate that transhepatic portal vein angioplasty is an effective treatment for portal vein stenosis.^16,22,23 Access to the portal vein is obtained via a percutaneous transhepatic approach. Care must be taken not to overdilate the vein. Once the procedure is accomplished, the transhepatic tract is embolized with Gelfoam (Pharmacia & Upjohn, Inc.).

Figure 3a.Hepatic arteriogram in a 60-year-old male two years after transplant with asymptomatic hepatic artery stenosis, initially suspected on Doppler ultrasound. Note the severe stenosis at and just distal to the anastomosis.
Figure 3b.Repeat arteriogram immediately after PTA to 5 mm demonstrated widely patent lumen. A follow-up Doppler study performed at six months was normal.
Figure 4a.Long segment stenosis in a composite right iliac artery to donor hepatic artery graft.
Figure 4b.The distal end of the graft was patent, with a mild stenosis that is difficult to visualize, but it was not hemodynamically significant.
Figure 4c.Two overlapping Palmaz stents were placed across the stenosis and dilated to 6 mm with no residual narrowing.

Portal vein thrombosis is more difficult to treat. Olcott et al²² treated several patients with angioplasty, but associated morbidities led to death in three of four. We have treated one patient whose portal vein thrombosis had been lysed with systemic streptokinase revealing an underlying anastomotic portal vein stenosis. The stenosis was successfully dilated via a transhepatic approach (see Figures 5a and 5b).

Inferior Vena Caval Stenoses: Inferior vena caval stenoses are even rarer than portal vein complications.²⁴ Stenosis or occlusion may occur at either the suprahepatic or infrahepatic anastomosis, but it is usually associated with the former. Clinical presentation of upper caval stenoses includes hepatomegaly, hepatic dysfunction, lower leg edema, and ascites.^16,24 Initial diagnosis is usually made by Doppler ultrasound. PTA has been reported by several authors,^20,21,25 but recurrence requiring repeat PTA has also been noted. We have treated only a few caval stenoses. In one patient a recurrent stenosis was treated successfully with a large metallic stent.

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Biliary Interventions

Biliary Strictures: Anastomotic and Intrahepatic; Balloon Dilation versus Metallic Stents: Biliary strictures after transplantation may be anastomotic or intrahepatic. Anastomotic strictures are usually related to surgical technique; ischemia also has been implicated.²⁶ Most anastomotic strictures at our hospital are treated with surgical repair, although in the past we have dilated a number of them with mixed results. Several reports have described favorable results with percutaneous balloon dilation of anastomotic strictures.^27,28

Figure 5a.Transhepatic portal venogram in a 24-year-old male revealed focal anastomotic portal vein stenosis. On admission the portal vein had been thrombosed, then recanalized with systemic thrombolysis.
Figure 5b.After PTA to 18 mm, the lumen caliber was now about the same as the adjacent portal vein. A 5 mm pressure gradient across the stenosis was eliminated.

Intrahepatic strictures have a variety of etiologies, although ischemia is the most common cause.²⁹ Biliary ductal tissue is supplied only by arterial branches. In the face of hepatic artery thrombosis or stenosis, the ducts are vulnerable to stricture. Other etiologies implicated in intrahepatic stricture are chronic rejection, preservation injury, cytomegalovirus infection, recurrent sclerosing cholangitis, and ascending cholangitis.^28,30

There is considerable debate about the treatment of intrahepatic biliary strictures occurring posttransplantation. Strictures may involve one or more of the major hepatic ducts, and, when widespread involvement is present, can also involve the anastomosis. Several investigators have claimed that balloon dilation of strictures via a transhepatic approach is the treatment of choice.^27,28,30,31 We have encountered almost universally dismal results with balloon dilation alone. We have treated 11 patients with balloon dilation; in all cases follow-up cholangiograms revealed at least one significant recurrence.

Since 1989, we have treated intrahepatic strictures with metallic stents placed via a transhepatic approach.³² Of 24 patients, 14 are available for long-term follow-up. Eleven of these 14 have remained patent, with the longest follow-up four and one-half years. Five of the 11 have maintained patency with no additional procedures. Six have required secondary procedures to reestablish patency after stent obstruction occurred, often as a result of new strictures. These procedures usually consisted of percutaneous drainage to remove sludge that accumulated within stents, and stenting of new strictures (see Figures 6a-e). These results, despite the necessity of secondary procedures, are encouraging, particularly when compared with our previous experience with balloon dilation alone.

Drainage of Abscesses and Fluid Collections: Percutaneous drainage is generally preferred over surgical techniques in the treatment of postoperative abscesses and fluid collections. Drainage can usually be accomplished very effectively with a minimum of risk.

The transplant patient is susceptible to a variety of fluid collections ranging from intrahepatic and extrahepatic abscesses, hematomas, bilomas, seromas, lymphoceles, and localized areas of ascites.²¹ The presence of an intrahepatic biloma always raises the question of necrotic parenchymal injury, most commonly related to hepatic artery thrombosis. Traditionally, this complication was believed to be incompatible with survival, but treatment of intrahepatic bilomas, even if infected, with drainage catheters, has proved effective.^33,34 Up to 40% of retransplantations can be avoided or forestalled.

Figures 6a, 6b.Figures illustrate metallic stents in biliary strictures. Cholangiogram via the T-tube tract three months after transplantation revealed extensive stricture formation in the right and left biliary tree as well as the common hepatic duct. The underlying etiology of the strictures was hepatic artery thrombosis.
Figure 6c.Metallic biliary stents have been inserted via the T-tube tract, resulting in patent normal caliber right and left hepatic ducts. The common hepatic duct was dilated, but not stented.
Figure 6d.Cholangiogram obtained five months after placement of right and left biliary drainage catheters. The biliary tree was filled with sludge and debris. An underlying stricture of the common hepatic duct was present.
Figure 6e.Repeat cholangiogram after placement of additional stents in the common hepatic and common bile ducts. The sludge seen in the biliary tree cleared significantly. Since this procedure, the patient has been asymptomatic and is now 45 months post initial stent placement.

Diagnosis of intra- and extrahepatic fluid collections is routinely performed with CT or sonography. These modalities are also utilized in guiding the actual drainage procedure. We prefer ultrasound, because it is readily available in the form of a portable unit in the interventional suite. The transducer can be covered with sterile protection, enabling the interventionalist to see the puncture needle entering the collection in real time. This minimizes the risk of needle transgression of bowel or other adjacent organs.

If the fluid is grossly noninfected, a specimen is obtained for culture. We generally remove as much fluid as possible; sometimes this requires placement of a small 5 or 6 French catheter, which is removed after the benign-appearing fluid is aspirated. In situations in which there is overt infection, a drainage catheter large enough to adequately drain the fluid and debris is placed. In very necrotic abscesses large catheters, 16 French or larger, may be required. In superficial extrahepatic abscesses, this large catheter can be placed at the time of initial drainage. For intrahepatic abscesses, however, one risks parenchymal bleeding by placing a very large drainage catheter through the liver on the first day. It is generally safer to place a small catheter the first day and replace it over a guidewire with a larger catheter 24-48 hours later.

Abscess catheters are generally left in place until daily drainage is less than 5-10 cc. While in position they are irrigated by the nursing staff two to four times per day with small aliquots of sterile saline. Follow-up abscessograms or imaging studies are performed depending on clinical response.

Bile Leaks: Extrahepatic bile duct leaks typically occur at the point where the T-tube enters the bile duct or at the bile duct anastomosis.²¹ Minor leaks can occasionally be managed with percutaneous drainage of the biloma and concomitant drainage of the biliary tree, either by indwelling surgical T-tube, endoscopically placed nasobiliary tube, or percutaneous transhepatic biliary catheter. In the same manner as abscess drainage, progress is gauged by diminution in the daily output from the catheter in the area of leakage. Large or nonloculated leaks must be repaired surgically.

Retained Biliary Stents: Biliary anastomoses are performed over small catheters that are designed to pass into the small bowel once their attaching sutures have dissolved.²¹ Occasionally these catheters fail to pass. If the stent is inaccessible to the endoscopist, then the patient is referred to our service. Percutaneous entry into the biliary tree is performed, and the stent is engaged with one of several available snare devices or even a stone basket. The stent is usually removed through the percutaneous tract, since this is often technically easier than pushing it through to the intestine.

Biliary Stone Extraction: In the series reported by Zajko et al,²⁷ stones were found in 4 of 56 percutaneous transhepatic cholangiograms postoperatively. They were all treated surgically. We feel that stones in the intra- and extrahepatic biliary tree can be removed transhepatically, as in the native biliary tree. After standard entry to the bile ducts is achieved, stone baskets are used to engage the stones (see Figures 7a-d). If the stones are small, they can occasionally be removed intact through the transhepatic tract. Usually, however, stones are pushed into the intestine or crushed with the basket, and the fragments then pushed into the bowel. Often an underlying biliary-enteric anastomotic stenosis must be dilated to enable passage of the stone fragments. This technique may also be helpful in clearing biliary casts resulting from mucosal sloughs that precede or coincide with some biliary strictures.³⁰

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Summary

During the past 30 years, hepatic transplantation has grown from an experimental operation to an almost commonplace procedure in many large hospitals. Interventional radiology has changed dramatically during this period, from a strictly diagnostic modality to a highly sophisticated therapeutic specialty. Some procedures, particularly biliary stricture dilation and TIPS, can allow transplantation to be avoided or at least delayed. Many postoperative complications are amenable to the ever-enlarging scope of interventional radiology as well. Every surgical anastomosis — arterial, portal venous, IVC, and biliary — is accessible to some degree to interventional therapy. Abnormalities of the biliary tree and fluid collections are also well suited to percutaneous approaches. These procedures, all performed percutaneously with local anesthesia and intravenous sedation, offer a safer, less invasive alternative to traditional open surgery.

Figure 7a.Biliary stone removal in a 46-year-old female who presented with cholangitis 21 months after transplantation. A cholangiogram obtained after placement of internal-external biliary drainage catheter revealed several large stones in the common bile duct. The catheter traversed a choledochojejunostomy anastomotic stricture.
Figures 7b, 7c.Stone basket is shown pushing stones into the jejunum. The anastomosis was then dilated to 10 mm.
Figure 7d.A cholangiogram several weeks later demonstrated that the biliary tree was free of stones. The anastomosis was widely patent. Immediately after this x-ray study, the biliary catheter was removed.

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References

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18. Mondragon RS, Karani JB, Heaton ND, Thomas S, Wong PYN, O'Grady JG, et al. The use of percutaneous transluminal angioplasty in hepatic artery stenosis after transplantation. Transplantation 1994;57:228-231.
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23. Olliff SP, Pain JA, Karani JB, Mowatt AP, Williams R. Percutaneous transhepatic dilatation of late portal vein stenosis following orthotopic liver transplantation. J Intervent Radiol 1991;6:29-31.
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25. Rose BS, Van-Aman ME, Simon DC, Sommer BG, Ferguson RM, Henry ML. Transluminal balloon angioplasty of infrahepatic caval anastomotic stenosis following liver transplantation: case report. Cardiovasc Intervent Radiol 1988;11:79-81.
26. Terblanche J, Allison JF, Northover JMA. An ischemic basis for biliary strictures. Surgery 1983;94:52-57.
27. Zajko AB, Bron KM, Campbell WL, Behal R, Van Thiel DH, Starzl TE. Percutaneous transhepatic cholangiography and biliary drainage after liver transplantation: a five-year experience. Gastrointest Radiol 1987;12:137-143.
28. McDonald V, Matalon TAS, Patel SK, Brunner MC, Sankary H, Foster P, et al. Biliary strictures in hepatic transplantation. JVIR 1991;2:533-538.
29. Zajko AB, Campbell WL, Logsdon GA, Bron KM, Tzakis A, Esquivel CO, et al. Cholangiographic findings in hepatic artery occlusion after liver transplantation. AJR 1987;149:485-489.
30. Ward EM, Kiely JJ, Maus TP, Wiesner RH, Krom RAF. Hilar biliary strictures after liver transplantation: cholangiography and percutaneous treatment. Radiology 1990;177: 259-263.
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32. Gibbs JF, Holman MJ, Diamond NG, Goldstein RM, Husberg BS, Klintmalm GB. The evolving management of complicated biliary strictures. Transplant Sci 1993;2:7-11.
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34. Kaplan SB, Zajko AB, Koneru B. Hepatic bilomas due to hepatic artery thrombosis in liver transplant recipients: percutaneous drainage and clinical outcome. Radiology 1990;174:1031-1035.

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