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The Role of Interventional Radiology in the Multidisciplinary Management of Biliary Complications After Liver Transplantation
The Role of Interventional Radiology in the Multidisciplinary Management of Biliary Complications After Liver Transplantation Jonathan M. Lorenz, MD, FSIR Interventional radiology is a key component of the multidisciplinary team, which is required for a successful liver transplant program, as it provides safe, effective, and minimally invasive management of transplant-related complications. Biliary complications remain highly prevalent among transplant recipients, and radiologic techniques can improve graft and patient survival in this population. Such techniques can serve as definitive, first-line therapies in some cases and as adjuncts to multidisciplinary approaches in others. This article reviews vascular and nonvascular radiologic techniques for managing transplant-related biliary complications. Tech Vasc Interventional Rad ]:]]]-]]] C 2015 Elsevier Inc. All rights reserved. KEYWORDS biliary complications, liver transplant, interventional radiology
Introduction Biliary complications remain a significant contributor to premature graft loss and can occur in up to one-third of patients who undergo liver transplantation.1-4 Markedly lower rates of such complications are seen after orthotopic transplants than after reduced-size liver transplants and after adult liver transplants when compared with pediatric liver transplants. The prognosis and choice of treatment depend on the type and timing of the complication after transplant. Minimally invasive methods are standard firstline options to manage most biliary complications, not only as definitive treatments but also as stepping stones to or components of strategies that combine interventional radiology (IR) techniques, endoscopic techniques, and open surgical techniques. The morbidity and mortality associated with surgical options varies with clinical condition, type of complication, and number of previous abdominal surgical procedures, but for appropriate candidates and indications, such options may be preferred to minimize treatment time and maximize success rates. However, careful application of IR and endoscopic
Section of Interventional Radiology, The University of Chicago, Chicago, IL. Address reprint requests to Jonathan M. Lorenz, MD, FSIR, Section of Interventional Radiology, The University of Chicago, 5841 S. Maryland Ave, MD2026, Chicago, IL 60637. E-mail: jlorenz@radiology. bsd.uchicago.edu 1089-2516/14/$ - see front matter & 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.tvir.2015.07.010
techniques and the addition of technological advances such as covered stents may continue to reduce the need for open surgical treatment.
Diagnosis and Treatment Modalities Detection and surveillance of biliary complications have evolved toward noninvasive modalities such as Doppler ultrasound (US), computed tomography (CT), and magnetic resonance cholangiopancreatography. For transplant recipients, endoscopic retrograde cholangiopancreatography (ERCP) is typically performed with the intent to both diagnose and treat strictures and leaks.5 ERCP is usually successful for choledochocholedochostomy biliary reconstructions, but for many transplant recipients, a Roux-en-Y hepaticojejunostomy (RYHJ) proves too tortuous or lengthy for the endoscopic approach. Percutaneous transhepatic cholangiography (PTC) and percutaneous transhepatic biliary drainage (PTBD) are second-line options for most indications and are reserved for cases in which ERCP fails or is infeasible for clinical or anatomical reasons. That said, imaging detection of biliary obstruction in liver transplant recipients could be difficult because of the reduced compliance of the liver parenchyma associated with chronic graft-versus-host disease, which may prevent biliary dilatation in the setting of obstruction. In such patients, as well as in patients with biliary leakage, the 1
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2 absence of biliary dilatation can necessitate PTC and PTBD for the initial diagnosis as well as for treatment.
Vascular-Related Biliary Complications Collateral circulation is compromised during liver transplantation, and consequently, the biliary system relies heavily on hepatic arterial supply for sustained viability.6 Consequently, the donor bile ducts are at an increased risk of biliary ischemia. This risk is higher for split-liver than for whole-liver grafts.7 Ischemic complications may result from hepatic artery thrombosis (HAT) or stenosis (HAS) but can also occur in the presence of a grossly intact hepatic artery (HA).8 Sequelae include biliary strictures, occlusions, leaks, fistulas, and hepatic abscesses. Although ischemic strictures can affect the entire biliary system, the intrahepatic blood supply relies exclusively on the patency of the HA and is particularly susceptible to HAT or HAS. When diffuse intrahepatic biliary strictures result from ischemia, options for minimally invasive duct decompression may be limited or nonexistent, as, in some cases, placement of drainage catheters may obstruct diseased biliary radicles and worsen the clinical picture. HA compromise occurs in 2%-8% of liver transplant recipients9-11 and is commonly managed surgically. Consequently, HA percutaneous transarterial angioplasty (PTA) and HA thrombolysis after liver transplantation are described in only short series and case reports. However, published cases describing the clinical success of endovascular revascularization suggest that this strategy may be underutilized.
HA Stenosis HAS often presents with a more insidious onset than HAT does, usually resulting in ischemic biliary strictures without frank necrosis. Patients often present with constitutional symptoms and laboratory evidence of ductal compromise and obstruction such as elevations of serum levels of gamma-glutamyl transferase, alkaline phosphatase, and bilirubin; a relative absence of alternative explanations for those elevations; and ultimately, imaging evidence of HAS. Not all cases of HAS require endovascular reconstruction. Appropriate clinical indications and risks should be considered alongside imaging findings. Detailed noninvasive vascular imaging with US, CT angiography, and MR angiography is critical to verify the location and nature of the arterial obstruction and to plan appropriate therapy. For the main HA and arterial anastomosis, US offers real-time interrogation of the HA during respiratory variation to distinguish cases of kinking or torsion from cases involving stenoses intrinsic to the vessel wall, such as surgical strictures at the anastomosis and clamp-related injury. CT angiography and MR angiography offer the advantage of 3-dimensional images and the detection of more distal, branch-point stenoses. All members of the multidisciplinary transplant team should be involved in planning and coordination before
HA PTA is performed, and expectations should be communicated to the patient or appropriate representative, particularly regarding the potential need for delayed or emergent surgical reconstruction or even retransplantation in case of failed or complicated PTA. Techniques required for HA PTA vary based on the imaging findings described earlier and may include concurrent thrombolysis in cases of partial thrombosis or thrombotic complications; double-balloon technique in cases of branch-point stenosis; microwires and microballoons in cases of small vessel stenosis (Fig. 1); and stents in cases of kinks, torsions, and refractory stenoses. During the procedure, heparinization before wire traversal of the stenosis is standard. In our experience and in the published literature,11,12 stenoses involving the arterial anastomosis, the extrahepatic HA, and the right and left intrahepatic HAs are all amenable to PTA, with excellent angiographic and clinical results. HAS of the main HA and anastomosis are particularly amenable to stent placement. Rostambeigi et al12 performed a metaanalysis of 263 liver transplants with HAS in 257 patients. PTA was performed in 147 patients, and stent placement was performed in 116. Follow-up was 1 month to 4.5 years. For PTA and stent placement, technical success rates were 89% and 98%, complication rates were 16% and 19%, arterial patency rates were 76% and 68%, reintervention rates were 22% and 25%, and retransplantation rates were 20% and 24%, respectively. Similarly, Hamby et al11 reviewed 35 HA interventions in 23 patients and observed a technical success rate of 97%. Respective primary patency rates at 1, 3, and 6 months for 10 patients undergoing PTA were 70%, 60%, and 50%, respectively, as compared with 92%, 85%, and 69%, respectively, for 13 stented patients. After PTA, patients should be observed and treated with anticoagulation overnight under the care of a dedicated transplant hepatology team, and serial hepatology panels should be performed to monitor progress and to assess for evidence of acute arterial compromise.
HA Thrombosis Clinical implications of HAT can range from acute graft failure to compromise of long-term graft survival. Interestingly, some studies have reported graft survival rates of up to 50% in patients with untreated cases of HAT that present late (after 1 month).10,13 In cases of early (o30 days after transplantation) HAT, graft loss is virtually guaranteed without early intervention. Revascularization within 1 week has been shown to preserve graft survival and prevent the associated extensive, life-threatening biliary complications associated with HAT that include biliary necrosis, bilomas, biliary casts, abscesses, leaks, and fistulas. For early HAT, Scarinci et al10 reviewed the significance of the timing of surgical reconstruction and reported rates of graft survival of 81%, 62%, and 0% when reconstruction was performed within 1, 2, and 4 weeks, respectively. Until recently, surgery has been considered the optimal treatment for HAT in the early postoperative period. Patients were considered poor candidates for
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Figure 1 (A) A 62-year-old woman with hepatic artery stenosis involving the junction of the proper hepatic artery and the right and left hepatic arteries (arrow). (B) Angioplasty of the proper and right hepatic arteries using 0.014in microwires and a low-profile balloon. Wires were placed in both the right and the left hepatic arteries to maintain a contralateral safety wire during balloon inflation. (C) Angioplasty of the proper left and proximal right hepatic arteries. (D) Marked angiographic improvement in all 3 arteries after angioplasty. Wires were maintained in both the left and right hepatic arteries during the angiogram to allow for treatment of any complications.
thrombolysis, success rates of thrombolysis were unknown, and rapid HA revascularization was considered critical to graft survival. However, recent reports suggest that, despite the known risks of thrombolysis in patients who have undergone major abdominal surgery, endovascular revascularization may be a viable first-line consideration when compared with the morbidity and outcomes associated with surgical reconstruction. Abdelaziz et al14 reviewed the cases of 11 adults who underwent thrombolysis for early HAT after living donor liver transplantation. Technical success was achieved in 82.8% of these patients, long-term patency was observed in 66.7%, and hemorrhage was observed in 18.2%. Similarly, Zhou et al15
reviewed the cases of 8 patients who underwent thrombolysis for HAT; technical success and long-term patency were observed in the 6 surviving patients, and no major complications related to thrombolysis were observed. Before HA thrombolysis is performed, the same coordination and management planning described for HA PTA must take place, particularly because precedents in the published literature are minimal and recent major abdominal surgery was previously considered a contraindication for thrombolysis. Published cases should be discussed with the patient or representative, with the caveat that true complication rates are unknown. Technically, standard caliber, multiple side hole infusion catheters may be
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Figure 2 (A) A 13-year-old boy with hepatic artery thrombosis 2 weeks after whole-liver transplantation. Thrombolysis was initiated with the tip of a microcatheter (arrow) placed just beyond the hepatic artery anastomosis. (B) After overnight infusion of tissue plasminogen activator at a rate of 0.25 mg/h, complete thrombolysis of the hepatic artery was achieved.
sufficient in cases with limited tortuosity and adequate caliber of the HA. However, we have found that these cases often require infusion of the thrombolytic agent using endhole microcatheters, as larger-bore catheters may restrict flow through an underlying stenosis or a diffusely narrow donor HA. The most common location of obstruction in posttransplant patients is the arterial anastomosis. In such cases, the microcatheter tip can be placed just distal to the anastomosis (Fig. 2). The pulsed spray technique is worth attempting, as reestablishment of flow in a single setting avoids risky overnight infusion and facilitates same-day PTA at the anastomosis to improve the chances for sustained flow. Such PTA of a fresh anastomosis should be performed carefully with a conservative balloon diameter and a standby transplant surgeon. Again, close overnight observation and anticoagulation by a dedicated hepatology team are critical, and follow-up serial hepatology and hematology panels are standard.
Bile Duct Necrosis and Ischemic Strictures When biliary compromise occurs after HAT, IR techniques are usually the first-line options and often serve to bridge the gap to retransplantation, particularly in acute cases. Necrosis of the biliary system may lead to biloma and abscess formation, biliary sludge and cast formation, biliary to portal fistulas, and ischemic strictures that tend to involve both the intrahepatic and extrahepatic bile ducts. PTBD is more useful for extrahepatic strictures and less so for the typically diffuse intrahepatic involvement. For infected bilomas and frank abscesses resulting from early HAT, percutaneous catheter drainage (PCD) offers the best option for treatment and, in some cases, can be combined with radiologic or endoscopic biliary drainage to divert bile and encourage closure of the causative abscess-to-biliary fistula. Diversion can be accomplished with a PTBD or via ERCP with either a nasobiliary tube or internal plastic stent. Treatment includes broad-spectrum antibiotics or antifungal medications or both as indicated.
Despite these efforts, many patients live with external drainage catheters until retransplantation can be performed. Anecdotally, we have found that progressive reduction of output and eventual catheter removal are more common in patients with biliary abscesses resulting from delayed and chronic HAT (Fig. 3). In general, liver abscess is an uncommon complication of liver transplantation, occurring in approximately 1% of patients in a review of 560 orthotopic liver transplantations.16 Although HAT is a common predisposing factor, other risk factors may include diabetes mellitus and opportunistic and pyogenic enteric pathogens that take advantage of the combination of immune suppression and the absence of a bilioenteric sphincter in patients with a RYHJ. When biliary compromise leads to fistulization to the vascular system—typically the portal vein—the clinical presentation is sometimes fulminant and treatment may be urgent. Presenting signs are related to biliary obstruction from hemobilia or gastrointestinal bleeding or both. IR options include covered stent placement within either the affected venous branch or the biliary tree (Fig. 4). Such a choice is case specific and depends on factors such as fistula location and reconstruction or retransplantation options. Compromise of major venous or biliary branches and consumption of portal vein length by stent placement should be discussed with the transplant team.
Nonvascular Biliary Complications Overview Nonvascular biliary complications can be further divided into those attributable to surgical technique, the most common category, and those related to medical conditions that tend to affect liver transplant recipients.17 As is the case with diffuse ischemic strictures, such medical conditions may affect multiple intrahepatic biliary radicles, and options for minimally invasive duct decompression
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Figure 3 (A) A 30-year-old man with chronic hepatic artery thrombosis presented with fever and leukocytosis; CT evaluation demonstrated a liver abscess (arrow). (B) Percutaneous catheter drainage was performed. Abscessogram was delayed for 3 days to avoid the risk of sepsis. (C) After 1 week, high output was noted from the drainage catheter, and an abscessogram demonstrated fistulization to the biliary tree (arrows). (D) Despite communication with the biliary tree and hepatic artery thrombosis, output gradually declined over 4 weeks and the catheter was removed. The abscess was thought to be the result of an infected biloma caused by hepatic artery thrombosis. Concurrent percutaneous biliary drainage was considered to divert bile from the healing abscess, but this strategy proved to be unnecessary in this case. In some patients, this complication can lead to protracted drainage or the need for surgical management resulting from the underlying etiology of biliary ischemia.
may be limited or nonexistent. Nonvascular etiologies for biliary obstruction include graft-versus-host disease, recurrent primary sclerosing cholangitis (Fig. 5), infections, drugs, and toxins, all of which can lead to diffuse ductopenia, or vanishing duct syndrome.18 Biliary stones and cast formation can result from both vascular and nonvascular etiologies. Conditions related to surgical technique include anastomotic complications such as strictures; obstruction and leaks; isolated, leaking ducts; and excluded, obstructed ducts that do not communicate with the anastomosed biliary system.
Strictures and Obstruction of the Biliary Anastomosis Strictures or obstruction can be caused by infection, ischemia, choledochoceles, stones, and sludge, but the most common etiology is an overzealous or scarred choledochocholedochostomy or RYHJ. Other causes for obstruction such as kinking, torsion, or extrinsic compression are much less common. Anastomotic strictures or frank obstruction represents the most common
complication of liver transplantation. In the setting of early or late obstruction, determination of surgical candidacy should be a first priority, as minimally invasive therapies tend to commit the patient to protracted external drainage or repeat procedures in either the IR or the gastroenterology suite. Indeed, the need for sustained drainage and repeat procedures causes these patients to be highly prevalent in IR practices that manage transplant patients. Surgical repair seems to result in similar rates of success compared when with those of minimally invasive therapies, but at the risk of higher morbidity. Reichman et al19 reviewed the cases of 12 patients who underwent surgical repair of anastomotic strictures after live donor liver transplantation. Surgical morbidity was high (58%), but clinical success was 67% at a mean of 43.7 months. In all cases of anastomotic obstruction, endoscopic management, when feasible, is a common alternative to surgical revision. Regardless of the etiology, the endoscopic approach allows for decompression via placement of an internal plastic stent. For tightly sewn or scarred anastomoses occurring after 2-3 weeks, balloon dilatation from the percutaneous or
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Figure 4 (A) A 55-year-old man with chronic hepatic artery thrombosis 10 weeks after liver transplantation. Complete occlusion of the proper hepatic duct and biliary-enteric anastomosis (arrow) was thought to be of ischemic origin. (B) Dilation using a 7-mm angioplasty balloon. (C) Placement of an internal-external drainage catheter. Follow-up cholangiogram was scheduled for 3 months to assess response to balloon dilation. (D) The patient presented to IR with jaundice and was found to be anemic with acutely increasing serum transaminases. Initial cholangiogram through the existing biliary drainage catheter demonstrated filling defects in the biliary system. The drain was removed over a wire, and a repeat cholangiogram was performed through a side arm sheath. Fistulization from the proper hepatic duct to the right portal vein (arrow) was observed. (E) Stent graft placement (arrow) from the right intrahepatic duct to the proper hepatic duct was performed to exclude the fistula. Consideration was given to stent placement from the portal venous side of the fistula, but after consultation with the transplant surgeon, biliary stent placement was performed to preserve the portal system for planned retransplantation. (F) After 1 week, serum bilirubin levels remained high, and a left-sided biliary drain (arrow) was placed. This catheter was internalized alongside the stent graft, and no recurrence of hemobilia was noted and bilirubin level returned to normal.
Figure 5 MRCP demonstrates beaded segmental bile ducts (arrows) indicating recurrence of primary sclerosing cholangitis after liver transplantation. MRCP, magnetic resonance cholangiopancreatography.
endoscopic approach is a standard treatment followed by a period of catheter placement to establish patency during the subsequent healing process. The advantage of the percutaneous over the endoscopic approach is the ability to place large-bore catheters (Fig. 6) or dual catheters across the anastomosis either from both the right and left lobes or from a single percutaneous tract, a strategy that has been associated with higher success rates in the recent published literature. Gwon et al20 performed balloon dilatation of anastomotic strictures in 79 patients followed by serial exchanges of drains sized up to 14 Fr at 1-month intervals. Dual-drainage catheters through the single tract were then exchanged up to 3 times at 2-month intervals. During a mean follow-up period of 34.5 months in 78 patients, symptom recurrence was noted in 9% of patients at a mean of 15.4 months after catheter removal, and complications were noted in 17.8%. Retrievable stent grafts have also been applied to the problem of anastomotic strictures with some success. Kim et al21 evaluated patients with strictures after living donor liver transplantation. The technique of balloon dilatation followed by 14French biliary catheter placement in 39 patients was compared with percutaneous covered retrievable stent
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Figure 6 (A) A 4-year-old boy with a biliary-enteric stricture (arrow) 2 months after liver transplantation. (B) Balloon dilatation was performed to a diameter of 6 mm. (C) Follow-up cholangiogram showed immediate resolution of the stricture. (D) An internal-external biliary drainage catheter was placed. This catheter was removed at 1 month after cholangiographic demonstration of persistent patency.
placement (29 stents in 20 patients). The stent migration rate was 24%, and clinical success was higher for the catheter group (95%) than for the stent group (70%). On the contrary, the treatment period was shorter for the stent group than for the catheter group (197 vs 278 days). For excluded ductal systems or for complete anastomotic obstruction (Fig. 7), sharp recanalization as a minimally invasive method to create a RYHJ has been described in case reports. This can be performed with assistance from endoscopy, cholangioscopy, and fluoroscopy. Once sharp passage is achieved from the biliary system to the Roux limb, a large-bore biliary drainage catheter can be left in place to allow a patent anastomosis to develop.22 Rates of success and complications have not been established, but for poor surgical candidates, sharp recanalization may be an option.
duct leaks, leaks from small biliary radicles, minor duct injury, or small anastomotic leaks, antegrade (PTBD) or retrograde (internal plastic stent or nasobiliary drain) biliary drainage often diverts sufficient bile from the leak point to allow for spontaneous resolution, typically within a few weeks. For isolated ducts and complete anastomotic
Bile Leaks Surgical technique accounts for a large percentage of bile leaks after liver transplantation. Leaks may occur from the donor’s or the recipient’s cystic duct remnant, a partially incompetent biliary anastomosis resulting from surgical technique or ischemia; frank anastomotic breakdown; ductal injury; or isolated, leaking ducts. For many patients with early large bile leaks from isolated ducts, open surgical repair or reconstruction should be considered, although after such operations, further complications are commonly encountered.23 For smaller leaks such as cystic
Figure 7 Cholangiogram performed after persistent elevations of serum bilirubin levels 1 week after right lobe liver transplantation shows complete obstruction of the biliary-enteric anastomosis (arrow). Communication with the Roux-en-Y could not be established, and surgical reconstruction was performed. In some cases of complete obstruction, particularly for poor surgical candidates, sharp puncture from a biliary sheath to the Roux limb can be performed to reestablish communication.
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8 breakdown, biloma drainage combined with either PTC or ERCP may temporize the presenting symptoms and facilitate surgical reconstruction. Interventional radiologists should avoid the common and disproven misconception that PTC and PTBD performed for conditions associated with nondilated ducts (such as bile leaks) are associated with low success and high complication rates. When PTC is routinely performed in large transplant centers, complication and success rates are similar for dilated and nondilated ducts.24,25 Isolated, leaking ducts are intrahepatic ducts draining directly into the abdomen from the cut edge of a reducedsize graft. Smaller leaking ducts may resolve spontaneously. Large segmental ducts typically require surgical anastomosis to a Roux-en-Y. In such cases, IR treatment can facilitate successful creation of a RYHJ. Initially, our treatment strategy involves PCD of the biloma followed by PTBD with the biliary drainage catheter left coiled in the perihepatic biloma, either immediately before surgical revision or electively (Fig. 8). Subsequent open surgical RYHJ is performed by cutting the pigtail portion of the drain from the abdominal side, leaving a straight drain (with additional side holes as needed); then, using the protruding straight drain as a guide, the Roux limb is sewn to the duct around the catheter. After the surgical
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Stones and Sludge Choledocholithiasis or cholangiolithiasis in transplant recipients usually consists of soft pigment debris that presents on imaging studies as well-defined stones or
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reconstruction, the straight biliary drain can be exchanged through IR techniques for a new, internal-external biliary drain with an intact pigtail, preferably over a standard rather than a stiff guidewire to avoid inadvertent disruption of the fresh anastomosis. When managing anastomotic breakdown in the setting of a patent HA, we routinely use a similar strategy of PCD of the biloma, PTBD, and then elective, open surgical reconstruction. In most cases of extensive bile leakage, the biloma drainage catheter is left as a surgical drain to reduce the risk of infection and serve as a surgical drain after revision. For smaller leaks occurring from an otherwise intact extrahepatic biliary system, percutaneous and endoscopic biliary drainage are first-line options. A period of percutaneous drainage with an internal-external drain crossing the leak is usually sufficient as a definitive therapy and otherwise bridges the gap to surgical reconstruction.
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Figure 8 (A) Multidisciplinary management strategy to treat a missed duct. A percutaneous drainage catheter (arrow) has been placed within a large fluid collection adjacent to a left lateral segment graft 3 days after transplantation. (B) After persistent elevations of serum bilirubin levels, an internal-external biliary drainage catheter was placed from the segment 3 bile duct (small arrow). Injection of the pigtail catheter demonstrated reflux from a biloma (arrowhead) into the segment 2 bile duct (large arrow). (C) Dual-stick technique was used to access the decompressed segment 2 bile duct. First, a 21-G needle (arrow) was advanced into a small branch using a combination of US and fluoroscopic guidance. (D) Although the first needle was injected and during rapid loss of contrast agent to the biloma, the segment 2 duct was transiently opacified while undergoing puncture with a second 21-G needle (arrow) under fluoroscopic guidance. (E) A wire was passed from the segment 2 duct across the cut edge of the liver and into the biloma. (F) An internal-external biliary drainage catheter was placed, extending from the duct into the biloma (arrow). (G) Surgical reconstruction was then performed by cutting the newly placed pigtail from the abdominal side and performing a new anastomosis to the Roux-en-Y using the protruding straight portion (arrow) as a guide. The separate segment 3 internal-external drain (arrowhead) is again shown.
The role of interventional radiology in the multidisciplinary management of biliary complications sludge, making these conditions quite amenable to endoscopic or percutaneous balloon maceration and removal. However, cholesterol stones may occur in some cases. Contributing factors include infection, obstruction, and external drainage (cholesterol supersaturation and loss of bile acids). For patients with an intact sphincter of Oddi and favorable anatomy, the endoscopic approach allows for stone removal and concurrent sphincterotomy, which can release distal strictures, facilitate hard stone removal, and reduce the chance for recurrence. Percutaneous removal is typically reserved for patients in whom endoscopic removal has failed or is infeasible (Fig. 9), as well as for patients with extensive intrahepatic stones.
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When percutaneous removal is indicated, our approach is to perform a PTC and then place an 8-French side arm vascular sheath, with the expectation that stone retrieval through the sheath is typically not necessary and an 8French biliary drain would conclude the case. We reserve the option for a larger sheath if necessary to extract large, hard stones. Regardless of stone location and extent, percutaneous treatment can be attempted.26 After wire access is obtained in the affected duct, an appropriately sized angiographic balloon is used to attempt to macerate soft pigment stones and sludge and push them into the small bowel. Multiloop snares and baskets are useful for capturing and breaking up hard stones.
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Figure 9 (A) A 69-year-old man with elevated serum bilirubin levels 6 months after orthotopic liver transplant despite placement of a right-sided internal-external biliary drainage catheter. Cholangiogram from a right side arm sheath shows large stones (arrow) obstructing the left main intrahepatic bile duct. (B) Access to the left bile duct was achieved from the right, and a balloon catheter was used to macerate the stones. Stones occurring after transplantation tend to be soft pigment stones. (C) Partial resolution with a residual small stone (arrow) in the left duct. This stone was pulled from the left to the main duct and then pushed into the bowel using a balloon. (D) Complete resolution of choledocholithiasis and replacement of an internal-external biliary drain. This drain was left in place to allow for an interval cholangiogram at 1 week to remove any residual stones. (E) Follow-up MRCP at 6 months demonstrates no further strictures or stones. MRCP, magnetic resonance cholangiopancreatography.
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Conclusion IR and endoscopic options have become first-line and definitive therapies for managing a variety of biliary complications after liver transplantation and avoiding the morbidity associated with open surgery. IR offers minimally invasive options for both vascular- and nonvascularrelated complications, but for some patients, endoscopic and surgical options may be advantageous. Multidisciplinary cooperation is critical to individualize the treatment plan and optimize the long-term results.
References 1. Egawa H, Inomata Y, Uemoto S, et al: Biliary anastomotic complications in 400 living related liver transplantations. World J Surg 25:1300-1307, 2001 2. Brown RS Jr, Russo MW, Lai M, et al: A survey of liver transplantation from living adult donors in the United States. N Engl J Med 348:818-825, 2003 3. Nemec P, Ondrasek J, Studenik P, et al: Biliary complications in liver transplantation. Ann Transplant 6:24-28, 2001 4. Patkowski W, Nyckowski P, Zieniewicz K, et al: Biliary tract complications following liver transplantation. Transplant Proc 35:2316-2317, 2003 5. Rerknimitr R, Sherman S, Fogel EL, et al: Biliary tract complications after orthotopic liver transplantation with choledochocholedochostomy anastomosis: Endoscopic findings and results of therapy. Gastrointest Endosc 55:224-231, 2002 6. Zajko AB, Campbell WL, Logsdon GA, et al: Cholangiographic findings in hepatic artery occlusion after liver transplantation. Am J Roentgenol 149:485-489, 1987 7. Vellar ID: The blood supply of the biliary ductal system and its relevance to vasculobiliary injuries following cholecystectomy. Aust N Z J Surg 69:816-820, 1999 8. Schlitt HJ, Meier PN, Nashan B, et al: Reconstructive surgery for ischemic-type lesions at the bile duct bifurcation after liver transplantation. Ann Surg 229:137-145, 1999 9. Stange BJ, Glanemann M, Nuessler NC, et al: Hepatic artery thrombosis after adult liver transplantation. Liver Transpl 9:612-620, 2003 10. Scarinci A, Sainz-Barriga M, Berrevoet F, et al: Early arterial revascularization after hepatic artery thrombosis may avoid graft loss and improve outcomes in adult liver transplantation. Transpl Proc 42:4403-4408, 2010 11. Hamby BA, Ramirez DE, Loss GE, et al: Endovascular treatment of hepatic artery stenosis after liver transplantation. J Vasc Surg 57: 1067-1072, 2013
J.M. Lorenz 12. Rostambeigi N, Hunter D, Duval S, et al: Stent placement versus angioplasty for hepatic artery stenosis after liver transplant: A metaanalysis of case series. Eur Radiol 23:1323-1334, 2013 13. Warnaar N, Polak WG, de Jong KP, et al: Long-term results of urgent revascularization for hepatic artery thrombosis after pediatric liver transplantation. Liver Transpl 16:847-855, 2010 14. Abdelaziz O, Hosny K, Amin A, et al: Endovascular management of early hepatic artery thrombosis after living donor liver transplantation. Transpl Int 25:847-856, 2012 15. Zhou J, Fan J, Wang JH, et al: Continuous transcatheter arterial thrombolysis for early hepatic artery thrombosis after liver transplantation. Transpl Proc 37:4426-4429, 2005 16. Nikeghbalian S, Salahi R, Salahi H, et al: Hepatic abscesses after liver transplant: 1997-2008. Exp Clin Transplant 7:256-260, 2009 17. Campbell WL, Shen R, Zajko AB, et al: Intrahepatic biliary strictures after liver transplantation. Radiology 191:735-740, 1994 18. van Hoek B, Wiesner RH, Krom RA, et al: Severe ductopenic rejection following liver transplantation: Incidence, time of onset, risk factors, treatment, and outcome. Semin Liver Dis 12:41-50, 1992 19. Reichman TW, Sandroussi C, Grant DR, et al: Surgical revision of biliary strictures following adult live donor liver transplantation: Patient selection, morbidity, and outcomes. Transpl Int 25:69-77, 2012 20. Gwon DI, Sung KB, Ko GY, et al: Dual catheter placement technique for treatment of biliary anastomotic strictures after liver transplantation. Liver Transpl 17:159-166, 2011 21. Kim J, Ko GY, Sung KB, et al: Percutaneously placed covered retrievable stents for the treatment of biliary anastomotic strictures following living donor liver transplantation. Liver Transpl 16:1410-1420, 2010 22. Rhee K, Jang SI, Lee D: Recanalization of completely obstructed bilioenteric anastomoses using a needle knife puncture. Gastrointest Interv 2:68-71, 2013 23. Melcher ML, Freise CE, Ascher NL, et al: Outcomes of surgical repair of bile leaks and strictures after adult-to-adult living donor liver transplant. Clin Transplant 24:E230-E235, 2010 24. Funaki B, Zaleski GX, Straus CA, et al: Percutaneous biliary drainage in patients with nondilated intrahepatic bile ducts. Am J Roentgenol 173:1541-1544, 1999 25. de Jong EA, Moelker A, Leertouwer T, et al: Percutaneous transhepatic biliary drainage in patients with postsurgical bile leakage and nondilated intrahepatic bile ducts. Dig Surg 30:444-450, 2013 26. Zhou CG, Wei BJ, Gao K, et al: Successful treatment of complex cholangiolithiasis following orthotopic liver transplantation with interventional radiology. World J Gastroenterol 21:2000-2004, 2015
Introduction Biliary complications remain a significant contributor to premature graft loss and can occur in up to one-third of patients who undergo liver transplantation.1-4 Markedly lower rates of such complications are seen after orthotopic transplants than after reduced-size liver transplants and after adult liver transplants when compared with pediatric liver transplants. The prognosis and choice of treatment depend on the type and timing of the complication after transplant. Minimally invasive methods are standard firstline options to manage most biliary complications, not only as definitive treatments but also as stepping stones to or components of strategies that combine interventional radiology (IR) techniques, endoscopic techniques, and open surgical techniques. The morbidity and mortality associated with surgical options varies with clinical condition, type of complication, and number of previous abdominal surgical procedures, but for appropriate candidates and indications, such options may be preferred to minimize treatment time and maximize success rates. However, careful application of IR and endoscopic
Section of Interventional Radiology, The University of Chicago, Chicago, IL. Address reprint requests to Jonathan M. Lorenz, MD, FSIR, Section of Interventional Radiology, The University of Chicago, 5841 S. Maryland Ave, MD2026, Chicago, IL 60637. E-mail: jlorenz@radiology. bsd.uchicago.edu 1089-2516/14/$ - see front matter & 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.tvir.2015.07.010
techniques and the addition of technological advances such as covered stents may continue to reduce the need for open surgical treatment.
Diagnosis and Treatment Modalities Detection and surveillance of biliary complications have evolved toward noninvasive modalities such as Doppler ultrasound (US), computed tomography (CT), and magnetic resonance cholangiopancreatography. For transplant recipients, endoscopic retrograde cholangiopancreatography (ERCP) is typically performed with the intent to both diagnose and treat strictures and leaks.5 ERCP is usually successful for choledochocholedochostomy biliary reconstructions, but for many transplant recipients, a Roux-en-Y hepaticojejunostomy (RYHJ) proves too tortuous or lengthy for the endoscopic approach. Percutaneous transhepatic cholangiography (PTC) and percutaneous transhepatic biliary drainage (PTBD) are second-line options for most indications and are reserved for cases in which ERCP fails or is infeasible for clinical or anatomical reasons. That said, imaging detection of biliary obstruction in liver transplant recipients could be difficult because of the reduced compliance of the liver parenchyma associated with chronic graft-versus-host disease, which may prevent biliary dilatation in the setting of obstruction. In such patients, as well as in patients with biliary leakage, the 1
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2 absence of biliary dilatation can necessitate PTC and PTBD for the initial diagnosis as well as for treatment.
Vascular-Related Biliary Complications Collateral circulation is compromised during liver transplantation, and consequently, the biliary system relies heavily on hepatic arterial supply for sustained viability.6 Consequently, the donor bile ducts are at an increased risk of biliary ischemia. This risk is higher for split-liver than for whole-liver grafts.7 Ischemic complications may result from hepatic artery thrombosis (HAT) or stenosis (HAS) but can also occur in the presence of a grossly intact hepatic artery (HA).8 Sequelae include biliary strictures, occlusions, leaks, fistulas, and hepatic abscesses. Although ischemic strictures can affect the entire biliary system, the intrahepatic blood supply relies exclusively on the patency of the HA and is particularly susceptible to HAT or HAS. When diffuse intrahepatic biliary strictures result from ischemia, options for minimally invasive duct decompression may be limited or nonexistent, as, in some cases, placement of drainage catheters may obstruct diseased biliary radicles and worsen the clinical picture. HA compromise occurs in 2%-8% of liver transplant recipients9-11 and is commonly managed surgically. Consequently, HA percutaneous transarterial angioplasty (PTA) and HA thrombolysis after liver transplantation are described in only short series and case reports. However, published cases describing the clinical success of endovascular revascularization suggest that this strategy may be underutilized.
HA Stenosis HAS often presents with a more insidious onset than HAT does, usually resulting in ischemic biliary strictures without frank necrosis. Patients often present with constitutional symptoms and laboratory evidence of ductal compromise and obstruction such as elevations of serum levels of gamma-glutamyl transferase, alkaline phosphatase, and bilirubin; a relative absence of alternative explanations for those elevations; and ultimately, imaging evidence of HAS. Not all cases of HAS require endovascular reconstruction. Appropriate clinical indications and risks should be considered alongside imaging findings. Detailed noninvasive vascular imaging with US, CT angiography, and MR angiography is critical to verify the location and nature of the arterial obstruction and to plan appropriate therapy. For the main HA and arterial anastomosis, US offers real-time interrogation of the HA during respiratory variation to distinguish cases of kinking or torsion from cases involving stenoses intrinsic to the vessel wall, such as surgical strictures at the anastomosis and clamp-related injury. CT angiography and MR angiography offer the advantage of 3-dimensional images and the detection of more distal, branch-point stenoses. All members of the multidisciplinary transplant team should be involved in planning and coordination before
HA PTA is performed, and expectations should be communicated to the patient or appropriate representative, particularly regarding the potential need for delayed or emergent surgical reconstruction or even retransplantation in case of failed or complicated PTA. Techniques required for HA PTA vary based on the imaging findings described earlier and may include concurrent thrombolysis in cases of partial thrombosis or thrombotic complications; double-balloon technique in cases of branch-point stenosis; microwires and microballoons in cases of small vessel stenosis (Fig. 1); and stents in cases of kinks, torsions, and refractory stenoses. During the procedure, heparinization before wire traversal of the stenosis is standard. In our experience and in the published literature,11,12 stenoses involving the arterial anastomosis, the extrahepatic HA, and the right and left intrahepatic HAs are all amenable to PTA, with excellent angiographic and clinical results. HAS of the main HA and anastomosis are particularly amenable to stent placement. Rostambeigi et al12 performed a metaanalysis of 263 liver transplants with HAS in 257 patients. PTA was performed in 147 patients, and stent placement was performed in 116. Follow-up was 1 month to 4.5 years. For PTA and stent placement, technical success rates were 89% and 98%, complication rates were 16% and 19%, arterial patency rates were 76% and 68%, reintervention rates were 22% and 25%, and retransplantation rates were 20% and 24%, respectively. Similarly, Hamby et al11 reviewed 35 HA interventions in 23 patients and observed a technical success rate of 97%. Respective primary patency rates at 1, 3, and 6 months for 10 patients undergoing PTA were 70%, 60%, and 50%, respectively, as compared with 92%, 85%, and 69%, respectively, for 13 stented patients. After PTA, patients should be observed and treated with anticoagulation overnight under the care of a dedicated transplant hepatology team, and serial hepatology panels should be performed to monitor progress and to assess for evidence of acute arterial compromise.
HA Thrombosis Clinical implications of HAT can range from acute graft failure to compromise of long-term graft survival. Interestingly, some studies have reported graft survival rates of up to 50% in patients with untreated cases of HAT that present late (after 1 month).10,13 In cases of early (o30 days after transplantation) HAT, graft loss is virtually guaranteed without early intervention. Revascularization within 1 week has been shown to preserve graft survival and prevent the associated extensive, life-threatening biliary complications associated with HAT that include biliary necrosis, bilomas, biliary casts, abscesses, leaks, and fistulas. For early HAT, Scarinci et al10 reviewed the significance of the timing of surgical reconstruction and reported rates of graft survival of 81%, 62%, and 0% when reconstruction was performed within 1, 2, and 4 weeks, respectively. Until recently, surgery has been considered the optimal treatment for HAT in the early postoperative period. Patients were considered poor candidates for
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Figure 1 (A) A 62-year-old woman with hepatic artery stenosis involving the junction of the proper hepatic artery and the right and left hepatic arteries (arrow). (B) Angioplasty of the proper and right hepatic arteries using 0.014in microwires and a low-profile balloon. Wires were placed in both the right and the left hepatic arteries to maintain a contralateral safety wire during balloon inflation. (C) Angioplasty of the proper left and proximal right hepatic arteries. (D) Marked angiographic improvement in all 3 arteries after angioplasty. Wires were maintained in both the left and right hepatic arteries during the angiogram to allow for treatment of any complications.
thrombolysis, success rates of thrombolysis were unknown, and rapid HA revascularization was considered critical to graft survival. However, recent reports suggest that, despite the known risks of thrombolysis in patients who have undergone major abdominal surgery, endovascular revascularization may be a viable first-line consideration when compared with the morbidity and outcomes associated with surgical reconstruction. Abdelaziz et al14 reviewed the cases of 11 adults who underwent thrombolysis for early HAT after living donor liver transplantation. Technical success was achieved in 82.8% of these patients, long-term patency was observed in 66.7%, and hemorrhage was observed in 18.2%. Similarly, Zhou et al15
reviewed the cases of 8 patients who underwent thrombolysis for HAT; technical success and long-term patency were observed in the 6 surviving patients, and no major complications related to thrombolysis were observed. Before HA thrombolysis is performed, the same coordination and management planning described for HA PTA must take place, particularly because precedents in the published literature are minimal and recent major abdominal surgery was previously considered a contraindication for thrombolysis. Published cases should be discussed with the patient or representative, with the caveat that true complication rates are unknown. Technically, standard caliber, multiple side hole infusion catheters may be
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Figure 2 (A) A 13-year-old boy with hepatic artery thrombosis 2 weeks after whole-liver transplantation. Thrombolysis was initiated with the tip of a microcatheter (arrow) placed just beyond the hepatic artery anastomosis. (B) After overnight infusion of tissue plasminogen activator at a rate of 0.25 mg/h, complete thrombolysis of the hepatic artery was achieved.
sufficient in cases with limited tortuosity and adequate caliber of the HA. However, we have found that these cases often require infusion of the thrombolytic agent using endhole microcatheters, as larger-bore catheters may restrict flow through an underlying stenosis or a diffusely narrow donor HA. The most common location of obstruction in posttransplant patients is the arterial anastomosis. In such cases, the microcatheter tip can be placed just distal to the anastomosis (Fig. 2). The pulsed spray technique is worth attempting, as reestablishment of flow in a single setting avoids risky overnight infusion and facilitates same-day PTA at the anastomosis to improve the chances for sustained flow. Such PTA of a fresh anastomosis should be performed carefully with a conservative balloon diameter and a standby transplant surgeon. Again, close overnight observation and anticoagulation by a dedicated hepatology team are critical, and follow-up serial hepatology and hematology panels are standard.
Bile Duct Necrosis and Ischemic Strictures When biliary compromise occurs after HAT, IR techniques are usually the first-line options and often serve to bridge the gap to retransplantation, particularly in acute cases. Necrosis of the biliary system may lead to biloma and abscess formation, biliary sludge and cast formation, biliary to portal fistulas, and ischemic strictures that tend to involve both the intrahepatic and extrahepatic bile ducts. PTBD is more useful for extrahepatic strictures and less so for the typically diffuse intrahepatic involvement. For infected bilomas and frank abscesses resulting from early HAT, percutaneous catheter drainage (PCD) offers the best option for treatment and, in some cases, can be combined with radiologic or endoscopic biliary drainage to divert bile and encourage closure of the causative abscess-to-biliary fistula. Diversion can be accomplished with a PTBD or via ERCP with either a nasobiliary tube or internal plastic stent. Treatment includes broad-spectrum antibiotics or antifungal medications or both as indicated.
Despite these efforts, many patients live with external drainage catheters until retransplantation can be performed. Anecdotally, we have found that progressive reduction of output and eventual catheter removal are more common in patients with biliary abscesses resulting from delayed and chronic HAT (Fig. 3). In general, liver abscess is an uncommon complication of liver transplantation, occurring in approximately 1% of patients in a review of 560 orthotopic liver transplantations.16 Although HAT is a common predisposing factor, other risk factors may include diabetes mellitus and opportunistic and pyogenic enteric pathogens that take advantage of the combination of immune suppression and the absence of a bilioenteric sphincter in patients with a RYHJ. When biliary compromise leads to fistulization to the vascular system—typically the portal vein—the clinical presentation is sometimes fulminant and treatment may be urgent. Presenting signs are related to biliary obstruction from hemobilia or gastrointestinal bleeding or both. IR options include covered stent placement within either the affected venous branch or the biliary tree (Fig. 4). Such a choice is case specific and depends on factors such as fistula location and reconstruction or retransplantation options. Compromise of major venous or biliary branches and consumption of portal vein length by stent placement should be discussed with the transplant team.
Nonvascular Biliary Complications Overview Nonvascular biliary complications can be further divided into those attributable to surgical technique, the most common category, and those related to medical conditions that tend to affect liver transplant recipients.17 As is the case with diffuse ischemic strictures, such medical conditions may affect multiple intrahepatic biliary radicles, and options for minimally invasive duct decompression
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Figure 3 (A) A 30-year-old man with chronic hepatic artery thrombosis presented with fever and leukocytosis; CT evaluation demonstrated a liver abscess (arrow). (B) Percutaneous catheter drainage was performed. Abscessogram was delayed for 3 days to avoid the risk of sepsis. (C) After 1 week, high output was noted from the drainage catheter, and an abscessogram demonstrated fistulization to the biliary tree (arrows). (D) Despite communication with the biliary tree and hepatic artery thrombosis, output gradually declined over 4 weeks and the catheter was removed. The abscess was thought to be the result of an infected biloma caused by hepatic artery thrombosis. Concurrent percutaneous biliary drainage was considered to divert bile from the healing abscess, but this strategy proved to be unnecessary in this case. In some patients, this complication can lead to protracted drainage or the need for surgical management resulting from the underlying etiology of biliary ischemia.
may be limited or nonexistent. Nonvascular etiologies for biliary obstruction include graft-versus-host disease, recurrent primary sclerosing cholangitis (Fig. 5), infections, drugs, and toxins, all of which can lead to diffuse ductopenia, or vanishing duct syndrome.18 Biliary stones and cast formation can result from both vascular and nonvascular etiologies. Conditions related to surgical technique include anastomotic complications such as strictures; obstruction and leaks; isolated, leaking ducts; and excluded, obstructed ducts that do not communicate with the anastomosed biliary system.
Strictures and Obstruction of the Biliary Anastomosis Strictures or obstruction can be caused by infection, ischemia, choledochoceles, stones, and sludge, but the most common etiology is an overzealous or scarred choledochocholedochostomy or RYHJ. Other causes for obstruction such as kinking, torsion, or extrinsic compression are much less common. Anastomotic strictures or frank obstruction represents the most common
complication of liver transplantation. In the setting of early or late obstruction, determination of surgical candidacy should be a first priority, as minimally invasive therapies tend to commit the patient to protracted external drainage or repeat procedures in either the IR or the gastroenterology suite. Indeed, the need for sustained drainage and repeat procedures causes these patients to be highly prevalent in IR practices that manage transplant patients. Surgical repair seems to result in similar rates of success compared when with those of minimally invasive therapies, but at the risk of higher morbidity. Reichman et al19 reviewed the cases of 12 patients who underwent surgical repair of anastomotic strictures after live donor liver transplantation. Surgical morbidity was high (58%), but clinical success was 67% at a mean of 43.7 months. In all cases of anastomotic obstruction, endoscopic management, when feasible, is a common alternative to surgical revision. Regardless of the etiology, the endoscopic approach allows for decompression via placement of an internal plastic stent. For tightly sewn or scarred anastomoses occurring after 2-3 weeks, balloon dilatation from the percutaneous or
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Figure 4 (A) A 55-year-old man with chronic hepatic artery thrombosis 10 weeks after liver transplantation. Complete occlusion of the proper hepatic duct and biliary-enteric anastomosis (arrow) was thought to be of ischemic origin. (B) Dilation using a 7-mm angioplasty balloon. (C) Placement of an internal-external drainage catheter. Follow-up cholangiogram was scheduled for 3 months to assess response to balloon dilation. (D) The patient presented to IR with jaundice and was found to be anemic with acutely increasing serum transaminases. Initial cholangiogram through the existing biliary drainage catheter demonstrated filling defects in the biliary system. The drain was removed over a wire, and a repeat cholangiogram was performed through a side arm sheath. Fistulization from the proper hepatic duct to the right portal vein (arrow) was observed. (E) Stent graft placement (arrow) from the right intrahepatic duct to the proper hepatic duct was performed to exclude the fistula. Consideration was given to stent placement from the portal venous side of the fistula, but after consultation with the transplant surgeon, biliary stent placement was performed to preserve the portal system for planned retransplantation. (F) After 1 week, serum bilirubin levels remained high, and a left-sided biliary drain (arrow) was placed. This catheter was internalized alongside the stent graft, and no recurrence of hemobilia was noted and bilirubin level returned to normal.
Figure 5 MRCP demonstrates beaded segmental bile ducts (arrows) indicating recurrence of primary sclerosing cholangitis after liver transplantation. MRCP, magnetic resonance cholangiopancreatography.
endoscopic approach is a standard treatment followed by a period of catheter placement to establish patency during the subsequent healing process. The advantage of the percutaneous over the endoscopic approach is the ability to place large-bore catheters (Fig. 6) or dual catheters across the anastomosis either from both the right and left lobes or from a single percutaneous tract, a strategy that has been associated with higher success rates in the recent published literature. Gwon et al20 performed balloon dilatation of anastomotic strictures in 79 patients followed by serial exchanges of drains sized up to 14 Fr at 1-month intervals. Dual-drainage catheters through the single tract were then exchanged up to 3 times at 2-month intervals. During a mean follow-up period of 34.5 months in 78 patients, symptom recurrence was noted in 9% of patients at a mean of 15.4 months after catheter removal, and complications were noted in 17.8%. Retrievable stent grafts have also been applied to the problem of anastomotic strictures with some success. Kim et al21 evaluated patients with strictures after living donor liver transplantation. The technique of balloon dilatation followed by 14French biliary catheter placement in 39 patients was compared with percutaneous covered retrievable stent
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Figure 6 (A) A 4-year-old boy with a biliary-enteric stricture (arrow) 2 months after liver transplantation. (B) Balloon dilatation was performed to a diameter of 6 mm. (C) Follow-up cholangiogram showed immediate resolution of the stricture. (D) An internal-external biliary drainage catheter was placed. This catheter was removed at 1 month after cholangiographic demonstration of persistent patency.
placement (29 stents in 20 patients). The stent migration rate was 24%, and clinical success was higher for the catheter group (95%) than for the stent group (70%). On the contrary, the treatment period was shorter for the stent group than for the catheter group (197 vs 278 days). For excluded ductal systems or for complete anastomotic obstruction (Fig. 7), sharp recanalization as a minimally invasive method to create a RYHJ has been described in case reports. This can be performed with assistance from endoscopy, cholangioscopy, and fluoroscopy. Once sharp passage is achieved from the biliary system to the Roux limb, a large-bore biliary drainage catheter can be left in place to allow a patent anastomosis to develop.22 Rates of success and complications have not been established, but for poor surgical candidates, sharp recanalization may be an option.
duct leaks, leaks from small biliary radicles, minor duct injury, or small anastomotic leaks, antegrade (PTBD) or retrograde (internal plastic stent or nasobiliary drain) biliary drainage often diverts sufficient bile from the leak point to allow for spontaneous resolution, typically within a few weeks. For isolated ducts and complete anastomotic
Bile Leaks Surgical technique accounts for a large percentage of bile leaks after liver transplantation. Leaks may occur from the donor’s or the recipient’s cystic duct remnant, a partially incompetent biliary anastomosis resulting from surgical technique or ischemia; frank anastomotic breakdown; ductal injury; or isolated, leaking ducts. For many patients with early large bile leaks from isolated ducts, open surgical repair or reconstruction should be considered, although after such operations, further complications are commonly encountered.23 For smaller leaks such as cystic
Figure 7 Cholangiogram performed after persistent elevations of serum bilirubin levels 1 week after right lobe liver transplantation shows complete obstruction of the biliary-enteric anastomosis (arrow). Communication with the Roux-en-Y could not be established, and surgical reconstruction was performed. In some cases of complete obstruction, particularly for poor surgical candidates, sharp puncture from a biliary sheath to the Roux limb can be performed to reestablish communication.
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8 breakdown, biloma drainage combined with either PTC or ERCP may temporize the presenting symptoms and facilitate surgical reconstruction. Interventional radiologists should avoid the common and disproven misconception that PTC and PTBD performed for conditions associated with nondilated ducts (such as bile leaks) are associated with low success and high complication rates. When PTC is routinely performed in large transplant centers, complication and success rates are similar for dilated and nondilated ducts.24,25 Isolated, leaking ducts are intrahepatic ducts draining directly into the abdomen from the cut edge of a reducedsize graft. Smaller leaking ducts may resolve spontaneously. Large segmental ducts typically require surgical anastomosis to a Roux-en-Y. In such cases, IR treatment can facilitate successful creation of a RYHJ. Initially, our treatment strategy involves PCD of the biloma followed by PTBD with the biliary drainage catheter left coiled in the perihepatic biloma, either immediately before surgical revision or electively (Fig. 8). Subsequent open surgical RYHJ is performed by cutting the pigtail portion of the drain from the abdominal side, leaving a straight drain (with additional side holes as needed); then, using the protruding straight drain as a guide, the Roux limb is sewn to the duct around the catheter. After the surgical
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Stones and Sludge Choledocholithiasis or cholangiolithiasis in transplant recipients usually consists of soft pigment debris that presents on imaging studies as well-defined stones or
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reconstruction, the straight biliary drain can be exchanged through IR techniques for a new, internal-external biliary drain with an intact pigtail, preferably over a standard rather than a stiff guidewire to avoid inadvertent disruption of the fresh anastomosis. When managing anastomotic breakdown in the setting of a patent HA, we routinely use a similar strategy of PCD of the biloma, PTBD, and then elective, open surgical reconstruction. In most cases of extensive bile leakage, the biloma drainage catheter is left as a surgical drain to reduce the risk of infection and serve as a surgical drain after revision. For smaller leaks occurring from an otherwise intact extrahepatic biliary system, percutaneous and endoscopic biliary drainage are first-line options. A period of percutaneous drainage with an internal-external drain crossing the leak is usually sufficient as a definitive therapy and otherwise bridges the gap to surgical reconstruction.
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Figure 8 (A) Multidisciplinary management strategy to treat a missed duct. A percutaneous drainage catheter (arrow) has been placed within a large fluid collection adjacent to a left lateral segment graft 3 days after transplantation. (B) After persistent elevations of serum bilirubin levels, an internal-external biliary drainage catheter was placed from the segment 3 bile duct (small arrow). Injection of the pigtail catheter demonstrated reflux from a biloma (arrowhead) into the segment 2 bile duct (large arrow). (C) Dual-stick technique was used to access the decompressed segment 2 bile duct. First, a 21-G needle (arrow) was advanced into a small branch using a combination of US and fluoroscopic guidance. (D) Although the first needle was injected and during rapid loss of contrast agent to the biloma, the segment 2 duct was transiently opacified while undergoing puncture with a second 21-G needle (arrow) under fluoroscopic guidance. (E) A wire was passed from the segment 2 duct across the cut edge of the liver and into the biloma. (F) An internal-external biliary drainage catheter was placed, extending from the duct into the biloma (arrow). (G) Surgical reconstruction was then performed by cutting the newly placed pigtail from the abdominal side and performing a new anastomosis to the Roux-en-Y using the protruding straight portion (arrow) as a guide. The separate segment 3 internal-external drain (arrowhead) is again shown.
The role of interventional radiology in the multidisciplinary management of biliary complications sludge, making these conditions quite amenable to endoscopic or percutaneous balloon maceration and removal. However, cholesterol stones may occur in some cases. Contributing factors include infection, obstruction, and external drainage (cholesterol supersaturation and loss of bile acids). For patients with an intact sphincter of Oddi and favorable anatomy, the endoscopic approach allows for stone removal and concurrent sphincterotomy, which can release distal strictures, facilitate hard stone removal, and reduce the chance for recurrence. Percutaneous removal is typically reserved for patients in whom endoscopic removal has failed or is infeasible (Fig. 9), as well as for patients with extensive intrahepatic stones.
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When percutaneous removal is indicated, our approach is to perform a PTC and then place an 8-French side arm vascular sheath, with the expectation that stone retrieval through the sheath is typically not necessary and an 8French biliary drain would conclude the case. We reserve the option for a larger sheath if necessary to extract large, hard stones. Regardless of stone location and extent, percutaneous treatment can be attempted.26 After wire access is obtained in the affected duct, an appropriately sized angiographic balloon is used to attempt to macerate soft pigment stones and sludge and push them into the small bowel. Multiloop snares and baskets are useful for capturing and breaking up hard stones.
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Figure 9 (A) A 69-year-old man with elevated serum bilirubin levels 6 months after orthotopic liver transplant despite placement of a right-sided internal-external biliary drainage catheter. Cholangiogram from a right side arm sheath shows large stones (arrow) obstructing the left main intrahepatic bile duct. (B) Access to the left bile duct was achieved from the right, and a balloon catheter was used to macerate the stones. Stones occurring after transplantation tend to be soft pigment stones. (C) Partial resolution with a residual small stone (arrow) in the left duct. This stone was pulled from the left to the main duct and then pushed into the bowel using a balloon. (D) Complete resolution of choledocholithiasis and replacement of an internal-external biliary drain. This drain was left in place to allow for an interval cholangiogram at 1 week to remove any residual stones. (E) Follow-up MRCP at 6 months demonstrates no further strictures or stones. MRCP, magnetic resonance cholangiopancreatography.
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Conclusion IR and endoscopic options have become first-line and definitive therapies for managing a variety of biliary complications after liver transplantation and avoiding the morbidity associated with open surgery. IR offers minimally invasive options for both vascular- and nonvascularrelated complications, but for some patients, endoscopic and surgical options may be advantageous. Multidisciplinary cooperation is critical to individualize the treatment plan and optimize the long-term results.
References 1. Egawa H, Inomata Y, Uemoto S, et al: Biliary anastomotic complications in 400 living related liver transplantations. World J Surg 25:1300-1307, 2001 2. Brown RS Jr, Russo MW, Lai M, et al: A survey of liver transplantation from living adult donors in the United States. N Engl J Med 348:818-825, 2003 3. Nemec P, Ondrasek J, Studenik P, et al: Biliary complications in liver transplantation. Ann Transplant 6:24-28, 2001 4. Patkowski W, Nyckowski P, Zieniewicz K, et al: Biliary tract complications following liver transplantation. Transplant Proc 35:2316-2317, 2003 5. Rerknimitr R, Sherman S, Fogel EL, et al: Biliary tract complications after orthotopic liver transplantation with choledochocholedochostomy anastomosis: Endoscopic findings and results of therapy. Gastrointest Endosc 55:224-231, 2002 6. Zajko AB, Campbell WL, Logsdon GA, et al: Cholangiographic findings in hepatic artery occlusion after liver transplantation. Am J Roentgenol 149:485-489, 1987 7. Vellar ID: The blood supply of the biliary ductal system and its relevance to vasculobiliary injuries following cholecystectomy. Aust N Z J Surg 69:816-820, 1999 8. Schlitt HJ, Meier PN, Nashan B, et al: Reconstructive surgery for ischemic-type lesions at the bile duct bifurcation after liver transplantation. Ann Surg 229:137-145, 1999 9. Stange BJ, Glanemann M, Nuessler NC, et al: Hepatic artery thrombosis after adult liver transplantation. Liver Transpl 9:612-620, 2003 10. Scarinci A, Sainz-Barriga M, Berrevoet F, et al: Early arterial revascularization after hepatic artery thrombosis may avoid graft loss and improve outcomes in adult liver transplantation. Transpl Proc 42:4403-4408, 2010 11. Hamby BA, Ramirez DE, Loss GE, et al: Endovascular treatment of hepatic artery stenosis after liver transplantation. J Vasc Surg 57: 1067-1072, 2013
J.M. Lorenz 12. Rostambeigi N, Hunter D, Duval S, et al: Stent placement versus angioplasty for hepatic artery stenosis after liver transplant: A metaanalysis of case series. Eur Radiol 23:1323-1334, 2013 13. Warnaar N, Polak WG, de Jong KP, et al: Long-term results of urgent revascularization for hepatic artery thrombosis after pediatric liver transplantation. Liver Transpl 16:847-855, 2010 14. Abdelaziz O, Hosny K, Amin A, et al: Endovascular management of early hepatic artery thrombosis after living donor liver transplantation. Transpl Int 25:847-856, 2012 15. Zhou J, Fan J, Wang JH, et al: Continuous transcatheter arterial thrombolysis for early hepatic artery thrombosis after liver transplantation. Transpl Proc 37:4426-4429, 2005 16. Nikeghbalian S, Salahi R, Salahi H, et al: Hepatic abscesses after liver transplant: 1997-2008. Exp Clin Transplant 7:256-260, 2009 17. Campbell WL, Shen R, Zajko AB, et al: Intrahepatic biliary strictures after liver transplantation. Radiology 191:735-740, 1994 18. van Hoek B, Wiesner RH, Krom RA, et al: Severe ductopenic rejection following liver transplantation: Incidence, time of onset, risk factors, treatment, and outcome. Semin Liver Dis 12:41-50, 1992 19. Reichman TW, Sandroussi C, Grant DR, et al: Surgical revision of biliary strictures following adult live donor liver transplantation: Patient selection, morbidity, and outcomes. Transpl Int 25:69-77, 2012 20. Gwon DI, Sung KB, Ko GY, et al: Dual catheter placement technique for treatment of biliary anastomotic strictures after liver transplantation. Liver Transpl 17:159-166, 2011 21. Kim J, Ko GY, Sung KB, et al: Percutaneously placed covered retrievable stents for the treatment of biliary anastomotic strictures following living donor liver transplantation. Liver Transpl 16:1410-1420, 2010 22. Rhee K, Jang SI, Lee D: Recanalization of completely obstructed bilioenteric anastomoses using a needle knife puncture. Gastrointest Interv 2:68-71, 2013 23. Melcher ML, Freise CE, Ascher NL, et al: Outcomes of surgical repair of bile leaks and strictures after adult-to-adult living donor liver transplant. Clin Transplant 24:E230-E235, 2010 24. Funaki B, Zaleski GX, Straus CA, et al: Percutaneous biliary drainage in patients with nondilated intrahepatic bile ducts. Am J Roentgenol 173:1541-1544, 1999 25. de Jong EA, Moelker A, Leertouwer T, et al: Percutaneous transhepatic biliary drainage in patients with postsurgical bile leakage and nondilated intrahepatic bile ducts. Dig Surg 30:444-450, 2013 26. Zhou CG, Wei BJ, Gao K, et al: Successful treatment of complex cholangiolithiasis following orthotopic liver transplantation with interventional radiology. World J Gastroenterol 21:2000-2004, 2015