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Benign Biliary Strictures: Diagnostic Evaluation and Approaches to Percutaneous Treatment
Benign Biliary Strictures: Diagnostic Evaluation and Approaches to Percutaneous Treatment Nicholas Fidelman, MD Interventional radiologists are often consulted to help identify and treat biliary strictures that can result from a variety of benign etiologies. Mainstays of noninvasive imaging for benign biliary strictures include ultrasound, contrast-enhanced computed tomography and magnetic resonance imaging, magnetic resonance cholangiopancreatography, and computed tomography cholangiography. Endoscopic retrograde cholangiography is the invasive diagnostic procedure of choice, allowing both localization of a stricture and treatment. Percutaneous biliary interventions are reserved for patients who are not candidates for endoscopic retrograde cholangiography (eg, history of distal gastrectomy and biliary-enteric anastomosis to a jejunal roux limb). This review discusses the roles of percutaneous transhepatic cholangiography and biliary drainage in the diagnosis of benign biliary strictures. The methodology for crossing benign biliary strictures, approaches to balloon dilation, management of recalcitrant strictures (ie, large-bore biliary catheters and retrievable covered stents), and the expected outcomes and complications of percutaneous treatment of benign biliary strictures are also addressed. Tech Vasc Interventional Rad 18:210-217 C 2015 Elsevier Inc. All rights reserved. KEYWORDS benign biliary stricture, drainage, balloon dilation, cholangioplasty
Introduction Patients presenting with clinical signs and symptoms of obstructive jaundice require a multidisciplinary approach for effective clinical management. Cross-sectional imaging using ultrasonography (US), computed tomography (CT), and magnetic resonance (MR) imaging allows detection of biliary ductal dilatation and may point to its cause. Further evaluation with endoscopic retrograde cholangiography (ERC) affords an opportunity to help establish the etiology of a stricture (detection of stones and brush biopsy) and intervene on a stricture by performing balloon dilation and by inserting stents. However, endoscopic access to the bile ducts is not always possible for patients with surgical alteration of gastrointestinal anatomy (ie, patients who previously underwent distal gastrectomy or Roux-en-Y hepaticojejunostomy), narrowing of the bowel lumen preventing endoscope passage, or stenosis at the level of ampulla of Vater precluding bile duct cannulation.
Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, CA. Address reprint requests to Nicholas Fidelman, MD, Department of Radiology and Biomedical Imaging, University of California San Francisco, 505 Parnassus Ave, Room M-361, San Francisco, CA 94143. E-mail: [email protected]
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Interventional radiologists play an important role in the diagnosis and treatment of patients with bile duct strictures who cannot be treated by the endoscopic approach by precisely defining bile duct anatomy via percutaneous transhepatic cholangiography, providing access into the biliary system by performing percutaneous transhepatic drainage, and offering a number of therapeutic options including percutaneous treatment of bile duct strictures using catheters, balloons, and stents. The purpose of this review was to summarize the contemporary approach to diagnosis and treatment of patients with benign bile duct strictures with a focus on percutaneous techniques.
Clinical and Laboratory Evaluation Taking a careful clinical history may help to elucidate the etiology of a biliary stricture. Typical causes of benign strictures are listed in Table 1. Malignant etiology should be suspected if a patient does not have one of the more common reasons to develop a benign biliary stricture, such as history of biliary surgery, liver transplantation, cholelithiasis, pancreatitis, or cholangitis.1,2 Patients with a biliary stricture may be asymptomatic or may present with
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Table 1 Etiologies for Benign Biliary Strictures Categories
Examples
Typically unifocal Iatrogenic Liver transplantation Partial hepatectomy Bile duct injury with or without subsequent operative repair Stone disease Mirizzi syndrome Pancreatitis Acute or chronic pancreatitis of any etiology Trauma Radiation therapy Portal biliopathy Idiopathic Papillary stenosis Typically diffuse Sclerosing Primary or secondary cholangitis Ischemia Hepatic artery occlusion after liver transplantation Cholangitis Recurrent pyogenic cholangitis Other infections (tuberculosis, HIV, and parasitic) Autoimmune IgG4-related cholangiopathy
abdominal pain, nausea, vomiting, anorexia, fatigue, jaundice, and fever (if ongoing infection is present). Blood tests in patients with biliary strictures should include liver function tests (total and direct bilirubin, aspartate and alanine aminotransferase, alkaline phosphatase, and γ-glutamyl transferase levels), complete blood count (especially if ongoing infection is suspected), serum albumin level, and coagulation profile (to test synthetic liver function and to prepare for possible invasive testing).
also point to its cause, such as choledocholithiasis or a mass. Alternatively, a CT scan with administration of an intravenous contrast agent could be obtained as a first-line imaging test. It is noteworthy that these imaging modalities may show normal-caliber bile ducts for patients with sclerosing cholangitis or a posttransplant biliary stricture. Additional noninvasive imaging workup could include abdominal MR imaging with an MR cholangiopancreatography sequence. MR cholangiopancreatography can be used for definitive diagnosis of conditions that do not require intervention, such as primary sclerosing cholangitis (Fig. 2), or as an intermediate diagnostic step toward invasive imaging evaluation (Fig. 3). Alternatively, CT cholangiogram using Cholografin (Bracco Diagnostics, Monroe Township, NJ) may be used for patients with serum bilirubin levels less than 3 mg/mL (Fig. 4).
Invasive Imaging Evaluation Endoscopic Retrograde Cholangiography Patients with suspected biliary obstruction that is occult on cross-sectional imaging and patients requiring biliary decompression usually proceed to invasive testing. For most patients, ERC with or without endoscopic US is used for detection of biliary stricture(s) and determination of their etiology (cholangiographic appearance and brush or endoscopic US–guided biopsy); this technique also provides an opportunity for decompression (balloon dilation and stenting). An endoscopic approach may not be possible for patients with a history of a distal gastrectomy (Billroth II and Whipple procedures), patients with a biliary-enteric anastomosis to a jejunal roux limb (repair of iatrogenic bile duct injury and liver transplantation), or those with duodenal or papillary obstruction that prevents passage of the endoscope or the duct cannula. Such patients are usually referred for percutaneous transhepatic cholangiography (PTC).
Noninvasive Imaging Evaluation US evaluation of the right upper quadrant (Fig. 1) is a reasonable and inexpensive first-line imaging test for patients with suspected biliary obstruction; this test may not only demonstrate biliary ductal dilation, but it could
A
Percutaneous Transhepatic Cholangiography Typical indications and contraindications for PTC and percutaneous transhepatic biliary drainage (PTBD) are
B
Figure 1 Images from a 68-year-old female recipient of a living donor left lobe liver transplant that was performed 2 years ago who developed an elevated alkaline phosphatase level. US with Doppler image (A) demonstrates intrahepatic biliary ductal dilatation. Percutaneous cholangiogram (B) demonstrates intrahepatic biliary ductal dilatation and narrowing at the site of the biliary-enteric anastomosis (arrow). (Color version of figure is available online.)
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prove technically challenging and time consuming. Alternatively, a patient may present with cholangitis (fever and biliary obstruction) or may develop signs of bleeding or infection during the procedure. In such instances, it would be reasonable to insert an external biliary drainage catheter for biliary diversion and not attempt to cross the stricture right away. Patients can be brought back several days later for an attempt to cross the stricture. On the contrary, if symptoms of cholangitis are absent and catheterization of the intrahepatic bile ducts is straightforward, then attempts to cross the biliary stricture can be undertaken immediately after bile duct catheterization.
Basic Technique
Figure 2 Image from a 32-year-old woman with primary sclerosing cholangitis. An MRCP maximum-intensity projection image demonstrates multifocal alternating narrowing and dilatation of the intrahepatic ducts.
summarized in Table 2.3 PTC and PTBD techniques are well known.4,5 In the setting of focal biliary obstruction due to a benign cause (Fig. 4), insertion of a biliary drain for biliary decompression and access for balloon angioplasty is usually indicated. Conversely, insertion of a biliary drain should be avoided in patients with multifocal strictures (ie, primary or secondary sclerosing cholangitis and diffuse biliary ischemia) who do not have a clear dominant stricture that could be relieved by decompression (Fig. 5).
Traversing Benign Strictures When to Try to Get Across? The decision regarding whether to attempt to cross a bile duct obstruction immediately after percutaneous catheterization of the intrahepatic bile ducts depends on whether technical challenges or significant complications were encountered during bile duct catheterization. If ducts are nondilated or minimally dilated, their catheterization may
A
A sheath with a side arm should be placed within the intrahepatic bile duct. The purpose of the sheath is to allow intermittent bile duct opacification with contrast agent as well as bile duct decompression during biliary instrumentation. The sheath should have a radiopaque marker (such as BRITE TIP Sheath Introducer, Cordis Corporation, Fremont, CA) at the distal end to help with visualization of the tip. It may be helpful to use a longer sheath (23 cm rather than 11 cm in length) to provide additional support for the angiographic catheter and a guidewire in the process of crossing a stricture. If the operator decides to place a “safety” guidewire within an intrahepatic duct, a sheath measuring at least 7 F in diameter should be used to accommodate a 5-F angiographic catheter. Uniformly stiff 0.035-in guidewires, such as Lunderquist-Ring Torque (Cook Medical, Indianapolis, IN) or Rosen (Cook Medical) guidewires, serve well as safety guidewires because they provide adequate support for catheter insertion all the way to their distal tip. If a safety guidewire is not used, a smaller-caliber sheath (6 F) is adequate. On insertion of a sheath and a safety guidewire, a cholangiogram should be performed. Right anterior oblique projection helps to splay open the confluence of the right and the left ducts. Ideally, the entire stricture length and the duct or bowel distal to the narrowing can be opacified with contrast agent administration, which provides a road map for the subsequent catheterization. The tip of the sheath should be placed peripheral to the site of
B
Figure 3 Images from a 13-year-old male recipient of a left lobe living donor transplant that was performed 5 years ago. A T2-weighted MR image (A) demonstrates intrahepatic biliary ductal dilatation and choledocholithiasis (arrowheads). Subsequent PTC (B) revealed a tight anastomotic stenosis (arrow) and redemonstrated intraductal stones (arrowheads).
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B
Figure 4 Images from a 53-year-old male recipient of a liver transplant that was performed 3 years ago who had an elevated alkaline phosphatase level. A volume-rendered CT cholangiogram image (A) demonstrates a “cut-off” of an intrahepatic duct. Subsequent PTC (B) revealed a right hepatic duct stricture (arrow).
the stricture, allowing enough space for the angiographic catheter tip to assume its shape. An angled-tip 5-F braided angiographic catheter (such as a 40-cm KMP, Cook Medical) should be used for guidewire guidance. If the basic angled-tip catheter does not provide an adequate shape for cannulation of the narrowed duct segment, other 5-F angiographic catheters, such as Cobra 2 (Cordis Corporation) or Sos (Cordis Corporation), may prove to be helpful. Glide catheters may not be stiff enough and, therefore, may not provide enough support for the guidewire. The sheath should be advanced over the 5-F catheter to prevent buckling of the catheter within the duct. A 0.035-in glidewire (such as the one produced by Terumo Medical Corporation, Somerset, NJ) is a good starting guidewire. Other guidewires that may be helpful for crossing difficult strictures include stiff glidewires and the Lunderquist-Ring Torque guidewire. The LunderquistRing Torque guidewire was specifically designed for biliary interventions. This guidewire is very stiff all the way to the distal tip and is torqueable. For optimal use, the distal 7-8 mm should be bent into a “hockey-stick” shape, whereas the proximal end should be looped several times to make a “handle” (Fig. 6). Rotation of the handle results in 1:1 rotation of the wire tip.
For strictures that are difficult to cross, an angiographic microcatheter and a microwire can be inserted through the 5-F catheter; this technique may be used to get past a very tight stricture that is too narrow to accommodate a 5-F catheter. Once a microcatheter is across the stricture, a stiff 0.018-in guidewire can be used as a platform for balloon dilation and passage of the angiographic catheter distal to the narrowed bile duct segment. Cholangiographic identification of the strictured duct is not always possible. If the stricture site is not apparent, the duct can be “probed” with a combination of an angled-tip 5-F catheter and a glidewire. If this catheter-guidewire combination is not effective, then a combination of an angled-tip catheter and a Lunderquist-Ring Torque guidewire may help. If the instrumentation causes a tear in the bile duct and a false passage is created, the procedure should be stopped, an external biliary drain with a distal locking mechanism (Cope loop or Malecot type) should be placed, and the patient should be asked to return for another attempt in 1 or 2 weeks. Additional attempts at crossing the stricture after creating a false passage would most likely result in the catheter exiting the biliary system via the tear. If a stricture is chronic, intrahepatic ducts may be massively dilated, and the site of the stricture may not be
Table 2 Indications and Contraindications for PTC and PTBD PTC: Indications
PTBD: Indications
PTC-PTBD: Contraindications
Define level(s) of obstruction Evaluate for presence of bile duct stones Determine etiology of cholangitis Evaluate suspected bile duct inflammatory disorders Demonstrate site(s) of bile duct leak Decompress obstructed biliary tree Dilate biliary strictures Remove bile duct stones Divert bile from and stent bile duct defect Unfavorable anatomy (ascites, colon interposition, and liver masses) Uncorrectable severe coagulopathy or thrombocytopenia or both
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Balloon Dilation Strategies When to Dilate?
Figure 5 Image from a 56-year-old male recipient of a liver transplant that was performed 5 years ago for primary sclerosing cholangitis who presented with mild hyperbilirubinemia and elevated alkaline phosphatase level. PTC demonstrates multiple long- and short-segment intrahepatic and extrahepatic biliary strictures consistent in appearance with recurrent PSC. Because of the diffuse nature of structuring and spontaneous contrast agent flow to the Roux limb, a biliary drain was not placed.
apparent on cholangiography. In this instance, it is helpful to leave an external biliary drain for a period of 1-2 weeks to allow the bile ducts to become decompressed. Repeat sheath cholangiography may identify the stricture site on the second (or later) attempt to cross a stricture.
Once a stricture has been crossed with a guidewire and a catheter, a decision regarding whether to attempt balloon dilation should be made. Balloon dilation is an accepted percutaneous treatment strategy for benign biliary strictures. However, if one is treating a postoperative biliaryenteric anastomotic narrowing and the anastomosis was created less than 1 month ago, the narrowing may be related to postsurgical edema or a kink. Neither of these entities is likely to respond to balloon dilation. Furthermore, balloon dilation may disrupt a fresh surgical anastomosis and result in a leak. In these cases, it is reasonable to leave an internal-external PTBD across the stricture for approximately 2 weeks and then perform another cholangiogram. Edema should resolve over time, which could allow for the biliary drain to be removed.
What to Dilate? Short-segment benign strictures involving a major bile duct (lobar or common hepatic or bile duct) tend to respond to balloon dilation with short-term duct patency rates of 50%-90%.6-9 Longer-term patency rates are lower (approximately 56%-74%).7,10,11 Long-segment strictures or multifocal strictures tend to not respond to dilation. That said, it is reasonable to attempt balloon dilation in most patients with a benign stricture (barring patients with a recent biliary-enteric anastomosis or ongoing infection).
Tips and Tricks Do not perform extensive biliary manipulation in a febrile patient. Place an external drain and attempt to cross the stricture at a later date after the infection resolves. If ducts are massively dilated and contrast agent is not flowing across the narrowed biliary segment, place an external drain and wait 1-2 weeks before trying to cross again. If a certain guidewire-catheter combination is not working, try another catheter or another guidewire. Use a glidewire first. If unable to cross with a glidewire, try the Lunderquist-Ring Torque guidewire next.
What Balloon Size to Use? The diameter of the balloon should be at least as large as the diameter of the bile duct proximal and distal to the obstruction and can be oversized by 25%-30%.9 Strictures in the common hepatic and common bile ducts can generally be safely dilated to 10-14 mm in an adult. A smaller balloon (4-8 mm) may need to be used for lobar ducts and for treatment of biliary strictures in children. The balloon should be kept inflated for at least 1 minute (inflation duration up to 20 minutes is used at some centers9), and the dilation should be repeated at the stricture site several times. Because balloon dilation often results in mucosal tears, bleeding, and edema, it is common practice to leave a PTBD across the narrowed biliary segment with side holes above and below the site of obstruction.
Dilation Schedule
Figure 6 A Lunderquist-Ring Torque guidewire with a “hockey stick” formed at the distal end and a “handle” formed on the proximal end to allow torqueing.
A typical approach at our institution is to perform a sheath cholangiogram approximately 1 month after each balloon dilation session. Periods between balloon dilation sessions depend on local experience and vary from every 1-2 weeks7,9 to every 3 months.6 If the stricture persists, it can be dilated again with a larger diameter or a highpressure balloon. A Cutting balloon (Boston Scientific,
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Natick, MA), which has 4 long blades attached to the balloon material and is available in diameters of up to 8 mm, can also be used in these cases.12 The diameter of the Cutting balloon should be 1-2 mm less than the required diameter of a conventional balloon (eg, use a 6-mm Cutting balloon and 8-mm conventional balloon for a bile duct with a diameter of 8 mm). Cutting balloons require switching to a 0.018-in guidewire platform. Usually, it is straightforward to switch between 0.018and 0.035-in guidewires using a 5-F angiographic catheter.
Assessment of Outcome If successful, biliary stricture dilation should result in the resolution of intrahepatic biliary ductal dilation, spontaneous passage of contrast agent through the previously narrowed biliary segment, and near-complete or complete resolution of bile duct narrowing (less than 20%-30% residual stenosis has been considered acceptable in many series). To document bile duct patency (Fig. 7), an over-thewire sheath cholangiogram can be performed in the right anterior oblique obliquity with a filming rate of 1 per second. Alternatively, a fluoroscopic cine clip demonstrating contrast agent passage across the previously narrowed biliary segment may be saved. Contrast agent should be instilled slowly to prevent pressure buildup in the intrahepatic ducts, which may lead to biliary sepsis. After documentation of bile duct patency, an external
A
biliary drain should be inserted and left capped for a period of 1-2 weeks (longer if a patient is at an increased risk for stricture recurrence). The external biliary drain may be removed at the end of the capping trial if the patient has not experienced recurrence of biliary obstruction symptoms (pain, jaundice, fever, and leakage of bile around the drainage catheter), there has been a complete or near-complete normalization of liver function test abnormalities, and tube injection cholangiogram demonstrates no significant residual narrowing and brisk flow of contrast agent across the previously narrowed biliary segment.
Percutaneous Treatment of Recalcitrant Strictures Recalcitrant biliary strictures may be amenable to surgical revision. However, surgical revision is often not an option (eg, difficult operative approach because of intrahepatic location of a stricture, adhesions, and patients who are poor surgical candidates). Patients with recalcitrant strictures may require a biliary drain for their lifetime, which leads to considerable morbidity and decline in the quality of life. Biliary drains may become clogged and require routine exchanges every 4-8 weeks for maintenance of patency. Patients with long-term indwelling PTBD may also develop intraductal debris and stones, which may ultimately lead to secondary biliary cirrhosis. Several percutaneous
B
D
C
E
Figure 7 Images from a 36-year-old woman who had undergone surgical repair (hepaticojejunostomy) of a cholecystectomy-related bile duct injury 4 years ago who presented with a markedly elevated alkaline phosphatase level and mild hyperbilirubinemia. PTC (A) demonstrates severe narrowing (arrows) at the biliary-enteric anastomosis. During balloon dilation of the stricture (B), a “waist” was demonstrated (arrow), which resolved after balloon inflation to 12 atmospheres (C). A cholangiogram performed 1 month later (D) showed a widely patent biliary-enteric anastomosis (arrows) that remained patent 2 weeks later at the time of cholangiography through the external biliary drain (E, arrows).
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Large-bore Biliary Drain One approach, first reported by Ring et al,13 involves placement of a large-bore PTBD measuring 16-18 F, which is left across the narrowed duct segment for a period of several months (typically 6-12 months). Silastic or silicone catheters are favored for this procedure because they are softer and may be easier to tolerate than the stiffer polyurethane tubes are. According to recently published series,14,15 75%-85% of patients who underwent a biliary drainage procedure for a benign stricture eventually received a large-bore drain. Patency at the stricture site allowing drain removal was achieved in 82%-87% of the remaining patients who completed the treatment period of 6-12 months. After drain removal, stricture patency rate was 84% at 1 year, 74% at 5 years, and 67% at 10 years.15
Double-Barrel Technique A promising alternative to large-bore drain placement has been proposed by Gwon et al.16 This technique involves insertion of a 14-F internal-external biliary drain (Cook Medical) through which a second 8.5-F PTBD (Cook Medical) is threaded so that the smaller drain exits from the larger drain peripheral to the site of the stricture. At the level of the stricture, the drains run parallel, yielding a total diameter of 22.5 F. Successful restoration of stricture patency and removal of the biliary catheters were reported in 78 of 79 patients (99%) after 5.5-14.2 months (mean ¼ 6.5 months) with both drainage catheters in place. Catheters were exchanged approximately once every 2 months. Strictures recurred in 7 patients (9%) at 6.1-26.2 months after catheter removal.
Stenting Use of permanent metal stents for patients with benign biliary strictures is not recommended because of a high rate of stent obstruction.17 However, there have been reports on the use of retrievable covered stents.18-21 In these studies, 75%-80% of the stents could be removed after a dwell time of 6-12 months. Strictures recurred in 15%-37% of patients, and the prevalence of stricture recurrence increased over time. It is noteworthy that these studies also reported a 10%-20% rate of stent migration.
Complications Common complications of bile duct instrumentation include pericatheter leakage, catheter dislodgement, bleeding (usually minor and self-limited), fever, and bile duct tears that may result in a biliary leak. Major complications are uncommon and may include arterial bleeding or pseudoaneurysm formation,7 abscess, and biliary sepsis.15 Even if infectious symptoms are absent, patients should receive at least 1 dose of broad-spectrum antibiotics with
both gram-positive and gram-negative coverage. Placing a biliary drainage catheter across the instrumented narrowed biliary segment and leaving the PTBD to gravity drainage overnight allows for decompression of the intrahepatic ducts (with clearance of potentially infected bile and blood) and may prevent life-threatening cholangitis. If an internal-external PTBD is left in place, it usually can be capped 1 day after the biliary instrumentation as long as there is adequate external drainage overnight and the intraductal bleeding has resolved. Patients do not require an overnight hospital admission after biliary instrumentation except for PTC and PTBD insertion. However, observation for at least 1 hour after biliary instrumentation is advisable to monitor for signs of significant bleeding or biliary sepsis.
Conclusion Interventional radiologists play a key role in diagnosis and treatment of patients with benign biliary strictures who cannot be managed by the endoscopic approach. Mainstays of the percutaneous technique involve precise localization of the stricture location by PTC followed by insertion of internal-external PTBD for the purpose of reestablishing biliary drainage into the bowel. Biliary drainage catheters often need to remain in place for weeks to months to allow patients to undergo periodic balloon dilation procedures. Patients with biliary strictures resistant to the conventional balloon dilation technique may benefit from Cutting balloons, large-bore PTBD, or placement of retrievable covered metal stents.
References 1. Singh A, Gelrud A, Agarwal B: Biliary strictures: Diagnostic considerations and approach. Gastroenterol Rep 3:22-31, 2015 2. Tummala P, Munigala S, Eloubeidi MA, et al: Patients with obstructive jaundice and biliary stricture ⫾ mass lesion on imaging: Prevalence of malignancy and potential role of EUS-FNA. J Clin Gastroenterol 47:532-537, 2013 3. Burke DR, Lewis CA, Cardella JF, et al: Society of Interventional Radiology Standards of Practice Committee: Quality improvement guidelines for percutaneous transhepatic cholangiography and biliary drainage. J Vasc Interv Radiol 14:S243-S246, 2003 4. Covey AM, Brown KT: Percutaneous transhepatic biliary drainage. Tech Vasc Interv Radiol 11:14-20, 2008 5. Kim HS, Lund GB, Venbrux AC: Advanced percutaneous transhepatic biliary access. Tech Vasc Interv Radiol 4:153-171, 2001 6. Kocher M, Cerna M, Havlik R, et al: Percutaneous treatment of benign bile duct strictures. Eur J Radiol 62:170-174, 2007 7. Cantwell CP, Pena CS, Gervais DA, et al: Thirty years’ experience with balloon dilation of benign postoperative biliary strictures: Longterm outcomes. Radiology 249:1050-1057, 2008 8. Janssen JJ, van Delden OM, van Lienden KP, et al: Percutaneous balloon dilatation and long-term drainage as treatment of anastomotic and nonanastomotic benign biliary strictures. Cardiovasc Intervent Radiol 37:1559-1567, 2014 9. Zajko AB, Sheng R, Zetti GM, et al: Transhepatic balloon dilation of biliary strictures in liver transplant patients: A 10-year experience. J Vasc Interv Radiol 6:79-83, 1995 10. Weber A, Rosca B, Neu B, et al: Long-term follow-up of percutaneous transhepatic biliary drainage (PTBD) in patients with benign bilioenterostomy stricture. Endoscopy 41:323-328, 2009
Benign biliary strictures 11. Ramos-De la Medina A, Misra S, Leroy AJ, et al: Management of benign biliary strictures by percutaneous interventional radiologic techniques (PIRT). HPB (Oxford) 10:428-432, 2008 12. Saad WE, Davies MG, Saad NE, et al: Transhepatic dilation of anastomotic biliary strictures in liver transplant recipients with use of a combined cutting and conventional balloon protocol: Technical safety and efficacy. J Vasc Interv Radiol 17:837-843, 2006 13. Ring EJ, Husted JW, Oleaga JA, et al: A multihole catheter for maintaining longterm percutaneous antegrade biliary drainage. Radiology 132:752-754, 1979 14. Glas L, Courbiere M, Ficarelli S, et al: Long-term outcome of percutaneous transhepatic therapy for benign bilioenteric anastomotic strictures. J Vasc Interv Radiol 19:1336-1343, 2008 15. DePietro DM, Shlansky-Goldberg RD, Soulen MC, et al: Long-term outcomes of a benign biliary stricture protocol. J Vasc Interv Radiol 26:1032-1039, 2015 16. 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
217 17. Venbrux AC, Osterman FA Jr: Percutaneous management of benign biliary strictures. Tech Vasc Interv Radiol 4:141-146, 2001 18. Gwon DI, Ko GY, Ko HK, et al: Percutaneous transhepatic treatment using retrievable covered stents in patients with benign biliary strictures: Mid-term outcomes in 68 patients. Dig Dis Sci 58: 3270-3279, 2013 19. Walter D, Laleman W, Jansen JM, et al: A fully covered selfexpandable metal stent with antimigration features for benign biliary strictures: A prospective, multicenter cohort study. Gastrointest Endosc 81:1197-1203, 2015 20. Deviere J, Nageshwar Reddy D, Puspok A, et al: Benign Biliary Stenoses Working Group: Successful management of benign biliary strictures with fully covered self-expanding metal stents. Gastroenterology 147:385-395, 2014 21. Saxena P, Diehl DL, Kumbhari V, et al: A US multicenter study of safety and efficacy of fully covered self-expandable metallic stents in benign extrahepatic biliary strictures. Dig Dis Sci 2015 [Epub ahead of print]
Introduction Patients presenting with clinical signs and symptoms of obstructive jaundice require a multidisciplinary approach for effective clinical management. Cross-sectional imaging using ultrasonography (US), computed tomography (CT), and magnetic resonance (MR) imaging allows detection of biliary ductal dilatation and may point to its cause. Further evaluation with endoscopic retrograde cholangiography (ERC) affords an opportunity to help establish the etiology of a stricture (detection of stones and brush biopsy) and intervene on a stricture by performing balloon dilation and by inserting stents. However, endoscopic access to the bile ducts is not always possible for patients with surgical alteration of gastrointestinal anatomy (ie, patients who previously underwent distal gastrectomy or Roux-en-Y hepaticojejunostomy), narrowing of the bowel lumen preventing endoscope passage, or stenosis at the level of ampulla of Vater precluding bile duct cannulation.
Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, CA. Address reprint requests to Nicholas Fidelman, MD, Department of Radiology and Biomedical Imaging, University of California San Francisco, 505 Parnassus Ave, Room M-361, San Francisco, CA 94143. E-mail: [email protected]
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Interventional radiologists play an important role in the diagnosis and treatment of patients with bile duct strictures who cannot be treated by the endoscopic approach by precisely defining bile duct anatomy via percutaneous transhepatic cholangiography, providing access into the biliary system by performing percutaneous transhepatic drainage, and offering a number of therapeutic options including percutaneous treatment of bile duct strictures using catheters, balloons, and stents. The purpose of this review was to summarize the contemporary approach to diagnosis and treatment of patients with benign bile duct strictures with a focus on percutaneous techniques.
Clinical and Laboratory Evaluation Taking a careful clinical history may help to elucidate the etiology of a biliary stricture. Typical causes of benign strictures are listed in Table 1. Malignant etiology should be suspected if a patient does not have one of the more common reasons to develop a benign biliary stricture, such as history of biliary surgery, liver transplantation, cholelithiasis, pancreatitis, or cholangitis.1,2 Patients with a biliary stricture may be asymptomatic or may present with
1089-2516/15/$ - see front matter & 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.tvir.2015.07.004
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Table 1 Etiologies for Benign Biliary Strictures Categories
Examples
Typically unifocal Iatrogenic Liver transplantation Partial hepatectomy Bile duct injury with or without subsequent operative repair Stone disease Mirizzi syndrome Pancreatitis Acute or chronic pancreatitis of any etiology Trauma Radiation therapy Portal biliopathy Idiopathic Papillary stenosis Typically diffuse Sclerosing Primary or secondary cholangitis Ischemia Hepatic artery occlusion after liver transplantation Cholangitis Recurrent pyogenic cholangitis Other infections (tuberculosis, HIV, and parasitic) Autoimmune IgG4-related cholangiopathy
abdominal pain, nausea, vomiting, anorexia, fatigue, jaundice, and fever (if ongoing infection is present). Blood tests in patients with biliary strictures should include liver function tests (total and direct bilirubin, aspartate and alanine aminotransferase, alkaline phosphatase, and γ-glutamyl transferase levels), complete blood count (especially if ongoing infection is suspected), serum albumin level, and coagulation profile (to test synthetic liver function and to prepare for possible invasive testing).
also point to its cause, such as choledocholithiasis or a mass. Alternatively, a CT scan with administration of an intravenous contrast agent could be obtained as a first-line imaging test. It is noteworthy that these imaging modalities may show normal-caliber bile ducts for patients with sclerosing cholangitis or a posttransplant biliary stricture. Additional noninvasive imaging workup could include abdominal MR imaging with an MR cholangiopancreatography sequence. MR cholangiopancreatography can be used for definitive diagnosis of conditions that do not require intervention, such as primary sclerosing cholangitis (Fig. 2), or as an intermediate diagnostic step toward invasive imaging evaluation (Fig. 3). Alternatively, CT cholangiogram using Cholografin (Bracco Diagnostics, Monroe Township, NJ) may be used for patients with serum bilirubin levels less than 3 mg/mL (Fig. 4).
Invasive Imaging Evaluation Endoscopic Retrograde Cholangiography Patients with suspected biliary obstruction that is occult on cross-sectional imaging and patients requiring biliary decompression usually proceed to invasive testing. For most patients, ERC with or without endoscopic US is used for detection of biliary stricture(s) and determination of their etiology (cholangiographic appearance and brush or endoscopic US–guided biopsy); this technique also provides an opportunity for decompression (balloon dilation and stenting). An endoscopic approach may not be possible for patients with a history of a distal gastrectomy (Billroth II and Whipple procedures), patients with a biliary-enteric anastomosis to a jejunal roux limb (repair of iatrogenic bile duct injury and liver transplantation), or those with duodenal or papillary obstruction that prevents passage of the endoscope or the duct cannula. Such patients are usually referred for percutaneous transhepatic cholangiography (PTC).
Noninvasive Imaging Evaluation US evaluation of the right upper quadrant (Fig. 1) is a reasonable and inexpensive first-line imaging test for patients with suspected biliary obstruction; this test may not only demonstrate biliary ductal dilation, but it could
A
Percutaneous Transhepatic Cholangiography Typical indications and contraindications for PTC and percutaneous transhepatic biliary drainage (PTBD) are
B
Figure 1 Images from a 68-year-old female recipient of a living donor left lobe liver transplant that was performed 2 years ago who developed an elevated alkaline phosphatase level. US with Doppler image (A) demonstrates intrahepatic biliary ductal dilatation. Percutaneous cholangiogram (B) demonstrates intrahepatic biliary ductal dilatation and narrowing at the site of the biliary-enteric anastomosis (arrow). (Color version of figure is available online.)
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prove technically challenging and time consuming. Alternatively, a patient may present with cholangitis (fever and biliary obstruction) or may develop signs of bleeding or infection during the procedure. In such instances, it would be reasonable to insert an external biliary drainage catheter for biliary diversion and not attempt to cross the stricture right away. Patients can be brought back several days later for an attempt to cross the stricture. On the contrary, if symptoms of cholangitis are absent and catheterization of the intrahepatic bile ducts is straightforward, then attempts to cross the biliary stricture can be undertaken immediately after bile duct catheterization.
Basic Technique
Figure 2 Image from a 32-year-old woman with primary sclerosing cholangitis. An MRCP maximum-intensity projection image demonstrates multifocal alternating narrowing and dilatation of the intrahepatic ducts.
summarized in Table 2.3 PTC and PTBD techniques are well known.4,5 In the setting of focal biliary obstruction due to a benign cause (Fig. 4), insertion of a biliary drain for biliary decompression and access for balloon angioplasty is usually indicated. Conversely, insertion of a biliary drain should be avoided in patients with multifocal strictures (ie, primary or secondary sclerosing cholangitis and diffuse biliary ischemia) who do not have a clear dominant stricture that could be relieved by decompression (Fig. 5).
Traversing Benign Strictures When to Try to Get Across? The decision regarding whether to attempt to cross a bile duct obstruction immediately after percutaneous catheterization of the intrahepatic bile ducts depends on whether technical challenges or significant complications were encountered during bile duct catheterization. If ducts are nondilated or minimally dilated, their catheterization may
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A sheath with a side arm should be placed within the intrahepatic bile duct. The purpose of the sheath is to allow intermittent bile duct opacification with contrast agent as well as bile duct decompression during biliary instrumentation. The sheath should have a radiopaque marker (such as BRITE TIP Sheath Introducer, Cordis Corporation, Fremont, CA) at the distal end to help with visualization of the tip. It may be helpful to use a longer sheath (23 cm rather than 11 cm in length) to provide additional support for the angiographic catheter and a guidewire in the process of crossing a stricture. If the operator decides to place a “safety” guidewire within an intrahepatic duct, a sheath measuring at least 7 F in diameter should be used to accommodate a 5-F angiographic catheter. Uniformly stiff 0.035-in guidewires, such as Lunderquist-Ring Torque (Cook Medical, Indianapolis, IN) or Rosen (Cook Medical) guidewires, serve well as safety guidewires because they provide adequate support for catheter insertion all the way to their distal tip. If a safety guidewire is not used, a smaller-caliber sheath (6 F) is adequate. On insertion of a sheath and a safety guidewire, a cholangiogram should be performed. Right anterior oblique projection helps to splay open the confluence of the right and the left ducts. Ideally, the entire stricture length and the duct or bowel distal to the narrowing can be opacified with contrast agent administration, which provides a road map for the subsequent catheterization. The tip of the sheath should be placed peripheral to the site of
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Figure 3 Images from a 13-year-old male recipient of a left lobe living donor transplant that was performed 5 years ago. A T2-weighted MR image (A) demonstrates intrahepatic biliary ductal dilatation and choledocholithiasis (arrowheads). Subsequent PTC (B) revealed a tight anastomotic stenosis (arrow) and redemonstrated intraductal stones (arrowheads).
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Figure 4 Images from a 53-year-old male recipient of a liver transplant that was performed 3 years ago who had an elevated alkaline phosphatase level. A volume-rendered CT cholangiogram image (A) demonstrates a “cut-off” of an intrahepatic duct. Subsequent PTC (B) revealed a right hepatic duct stricture (arrow).
the stricture, allowing enough space for the angiographic catheter tip to assume its shape. An angled-tip 5-F braided angiographic catheter (such as a 40-cm KMP, Cook Medical) should be used for guidewire guidance. If the basic angled-tip catheter does not provide an adequate shape for cannulation of the narrowed duct segment, other 5-F angiographic catheters, such as Cobra 2 (Cordis Corporation) or Sos (Cordis Corporation), may prove to be helpful. Glide catheters may not be stiff enough and, therefore, may not provide enough support for the guidewire. The sheath should be advanced over the 5-F catheter to prevent buckling of the catheter within the duct. A 0.035-in glidewire (such as the one produced by Terumo Medical Corporation, Somerset, NJ) is a good starting guidewire. Other guidewires that may be helpful for crossing difficult strictures include stiff glidewires and the Lunderquist-Ring Torque guidewire. The LunderquistRing Torque guidewire was specifically designed for biliary interventions. This guidewire is very stiff all the way to the distal tip and is torqueable. For optimal use, the distal 7-8 mm should be bent into a “hockey-stick” shape, whereas the proximal end should be looped several times to make a “handle” (Fig. 6). Rotation of the handle results in 1:1 rotation of the wire tip.
For strictures that are difficult to cross, an angiographic microcatheter and a microwire can be inserted through the 5-F catheter; this technique may be used to get past a very tight stricture that is too narrow to accommodate a 5-F catheter. Once a microcatheter is across the stricture, a stiff 0.018-in guidewire can be used as a platform for balloon dilation and passage of the angiographic catheter distal to the narrowed bile duct segment. Cholangiographic identification of the strictured duct is not always possible. If the stricture site is not apparent, the duct can be “probed” with a combination of an angled-tip 5-F catheter and a glidewire. If this catheter-guidewire combination is not effective, then a combination of an angled-tip catheter and a Lunderquist-Ring Torque guidewire may help. If the instrumentation causes a tear in the bile duct and a false passage is created, the procedure should be stopped, an external biliary drain with a distal locking mechanism (Cope loop or Malecot type) should be placed, and the patient should be asked to return for another attempt in 1 or 2 weeks. Additional attempts at crossing the stricture after creating a false passage would most likely result in the catheter exiting the biliary system via the tear. If a stricture is chronic, intrahepatic ducts may be massively dilated, and the site of the stricture may not be
Table 2 Indications and Contraindications for PTC and PTBD PTC: Indications
PTBD: Indications
PTC-PTBD: Contraindications
Define level(s) of obstruction Evaluate for presence of bile duct stones Determine etiology of cholangitis Evaluate suspected bile duct inflammatory disorders Demonstrate site(s) of bile duct leak Decompress obstructed biliary tree Dilate biliary strictures Remove bile duct stones Divert bile from and stent bile duct defect Unfavorable anatomy (ascites, colon interposition, and liver masses) Uncorrectable severe coagulopathy or thrombocytopenia or both
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Balloon Dilation Strategies When to Dilate?
Figure 5 Image from a 56-year-old male recipient of a liver transplant that was performed 5 years ago for primary sclerosing cholangitis who presented with mild hyperbilirubinemia and elevated alkaline phosphatase level. PTC demonstrates multiple long- and short-segment intrahepatic and extrahepatic biliary strictures consistent in appearance with recurrent PSC. Because of the diffuse nature of structuring and spontaneous contrast agent flow to the Roux limb, a biliary drain was not placed.
apparent on cholangiography. In this instance, it is helpful to leave an external biliary drain for a period of 1-2 weeks to allow the bile ducts to become decompressed. Repeat sheath cholangiography may identify the stricture site on the second (or later) attempt to cross a stricture.
Once a stricture has been crossed with a guidewire and a catheter, a decision regarding whether to attempt balloon dilation should be made. Balloon dilation is an accepted percutaneous treatment strategy for benign biliary strictures. However, if one is treating a postoperative biliaryenteric anastomotic narrowing and the anastomosis was created less than 1 month ago, the narrowing may be related to postsurgical edema or a kink. Neither of these entities is likely to respond to balloon dilation. Furthermore, balloon dilation may disrupt a fresh surgical anastomosis and result in a leak. In these cases, it is reasonable to leave an internal-external PTBD across the stricture for approximately 2 weeks and then perform another cholangiogram. Edema should resolve over time, which could allow for the biliary drain to be removed.
What to Dilate? Short-segment benign strictures involving a major bile duct (lobar or common hepatic or bile duct) tend to respond to balloon dilation with short-term duct patency rates of 50%-90%.6-9 Longer-term patency rates are lower (approximately 56%-74%).7,10,11 Long-segment strictures or multifocal strictures tend to not respond to dilation. That said, it is reasonable to attempt balloon dilation in most patients with a benign stricture (barring patients with a recent biliary-enteric anastomosis or ongoing infection).
Tips and Tricks Do not perform extensive biliary manipulation in a febrile patient. Place an external drain and attempt to cross the stricture at a later date after the infection resolves. If ducts are massively dilated and contrast agent is not flowing across the narrowed biliary segment, place an external drain and wait 1-2 weeks before trying to cross again. If a certain guidewire-catheter combination is not working, try another catheter or another guidewire. Use a glidewire first. If unable to cross with a glidewire, try the Lunderquist-Ring Torque guidewire next.
What Balloon Size to Use? The diameter of the balloon should be at least as large as the diameter of the bile duct proximal and distal to the obstruction and can be oversized by 25%-30%.9 Strictures in the common hepatic and common bile ducts can generally be safely dilated to 10-14 mm in an adult. A smaller balloon (4-8 mm) may need to be used for lobar ducts and for treatment of biliary strictures in children. The balloon should be kept inflated for at least 1 minute (inflation duration up to 20 minutes is used at some centers9), and the dilation should be repeated at the stricture site several times. Because balloon dilation often results in mucosal tears, bleeding, and edema, it is common practice to leave a PTBD across the narrowed biliary segment with side holes above and below the site of obstruction.
Dilation Schedule
Figure 6 A Lunderquist-Ring Torque guidewire with a “hockey stick” formed at the distal end and a “handle” formed on the proximal end to allow torqueing.
A typical approach at our institution is to perform a sheath cholangiogram approximately 1 month after each balloon dilation session. Periods between balloon dilation sessions depend on local experience and vary from every 1-2 weeks7,9 to every 3 months.6 If the stricture persists, it can be dilated again with a larger diameter or a highpressure balloon. A Cutting balloon (Boston Scientific,
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Natick, MA), which has 4 long blades attached to the balloon material and is available in diameters of up to 8 mm, can also be used in these cases.12 The diameter of the Cutting balloon should be 1-2 mm less than the required diameter of a conventional balloon (eg, use a 6-mm Cutting balloon and 8-mm conventional balloon for a bile duct with a diameter of 8 mm). Cutting balloons require switching to a 0.018-in guidewire platform. Usually, it is straightforward to switch between 0.018and 0.035-in guidewires using a 5-F angiographic catheter.
Assessment of Outcome If successful, biliary stricture dilation should result in the resolution of intrahepatic biliary ductal dilation, spontaneous passage of contrast agent through the previously narrowed biliary segment, and near-complete or complete resolution of bile duct narrowing (less than 20%-30% residual stenosis has been considered acceptable in many series). To document bile duct patency (Fig. 7), an over-thewire sheath cholangiogram can be performed in the right anterior oblique obliquity with a filming rate of 1 per second. Alternatively, a fluoroscopic cine clip demonstrating contrast agent passage across the previously narrowed biliary segment may be saved. Contrast agent should be instilled slowly to prevent pressure buildup in the intrahepatic ducts, which may lead to biliary sepsis. After documentation of bile duct patency, an external
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biliary drain should be inserted and left capped for a period of 1-2 weeks (longer if a patient is at an increased risk for stricture recurrence). The external biliary drain may be removed at the end of the capping trial if the patient has not experienced recurrence of biliary obstruction symptoms (pain, jaundice, fever, and leakage of bile around the drainage catheter), there has been a complete or near-complete normalization of liver function test abnormalities, and tube injection cholangiogram demonstrates no significant residual narrowing and brisk flow of contrast agent across the previously narrowed biliary segment.
Percutaneous Treatment of Recalcitrant Strictures Recalcitrant biliary strictures may be amenable to surgical revision. However, surgical revision is often not an option (eg, difficult operative approach because of intrahepatic location of a stricture, adhesions, and patients who are poor surgical candidates). Patients with recalcitrant strictures may require a biliary drain for their lifetime, which leads to considerable morbidity and decline in the quality of life. Biliary drains may become clogged and require routine exchanges every 4-8 weeks for maintenance of patency. Patients with long-term indwelling PTBD may also develop intraductal debris and stones, which may ultimately lead to secondary biliary cirrhosis. Several percutaneous
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Figure 7 Images from a 36-year-old woman who had undergone surgical repair (hepaticojejunostomy) of a cholecystectomy-related bile duct injury 4 years ago who presented with a markedly elevated alkaline phosphatase level and mild hyperbilirubinemia. PTC (A) demonstrates severe narrowing (arrows) at the biliary-enteric anastomosis. During balloon dilation of the stricture (B), a “waist” was demonstrated (arrow), which resolved after balloon inflation to 12 atmospheres (C). A cholangiogram performed 1 month later (D) showed a widely patent biliary-enteric anastomosis (arrows) that remained patent 2 weeks later at the time of cholangiography through the external biliary drain (E, arrows).
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Large-bore Biliary Drain One approach, first reported by Ring et al,13 involves placement of a large-bore PTBD measuring 16-18 F, which is left across the narrowed duct segment for a period of several months (typically 6-12 months). Silastic or silicone catheters are favored for this procedure because they are softer and may be easier to tolerate than the stiffer polyurethane tubes are. According to recently published series,14,15 75%-85% of patients who underwent a biliary drainage procedure for a benign stricture eventually received a large-bore drain. Patency at the stricture site allowing drain removal was achieved in 82%-87% of the remaining patients who completed the treatment period of 6-12 months. After drain removal, stricture patency rate was 84% at 1 year, 74% at 5 years, and 67% at 10 years.15
Double-Barrel Technique A promising alternative to large-bore drain placement has been proposed by Gwon et al.16 This technique involves insertion of a 14-F internal-external biliary drain (Cook Medical) through which a second 8.5-F PTBD (Cook Medical) is threaded so that the smaller drain exits from the larger drain peripheral to the site of the stricture. At the level of the stricture, the drains run parallel, yielding a total diameter of 22.5 F. Successful restoration of stricture patency and removal of the biliary catheters were reported in 78 of 79 patients (99%) after 5.5-14.2 months (mean ¼ 6.5 months) with both drainage catheters in place. Catheters were exchanged approximately once every 2 months. Strictures recurred in 7 patients (9%) at 6.1-26.2 months after catheter removal.
Stenting Use of permanent metal stents for patients with benign biliary strictures is not recommended because of a high rate of stent obstruction.17 However, there have been reports on the use of retrievable covered stents.18-21 In these studies, 75%-80% of the stents could be removed after a dwell time of 6-12 months. Strictures recurred in 15%-37% of patients, and the prevalence of stricture recurrence increased over time. It is noteworthy that these studies also reported a 10%-20% rate of stent migration.
Complications Common complications of bile duct instrumentation include pericatheter leakage, catheter dislodgement, bleeding (usually minor and self-limited), fever, and bile duct tears that may result in a biliary leak. Major complications are uncommon and may include arterial bleeding or pseudoaneurysm formation,7 abscess, and biliary sepsis.15 Even if infectious symptoms are absent, patients should receive at least 1 dose of broad-spectrum antibiotics with
both gram-positive and gram-negative coverage. Placing a biliary drainage catheter across the instrumented narrowed biliary segment and leaving the PTBD to gravity drainage overnight allows for decompression of the intrahepatic ducts (with clearance of potentially infected bile and blood) and may prevent life-threatening cholangitis. If an internal-external PTBD is left in place, it usually can be capped 1 day after the biliary instrumentation as long as there is adequate external drainage overnight and the intraductal bleeding has resolved. Patients do not require an overnight hospital admission after biliary instrumentation except for PTC and PTBD insertion. However, observation for at least 1 hour after biliary instrumentation is advisable to monitor for signs of significant bleeding or biliary sepsis.
Conclusion Interventional radiologists play a key role in diagnosis and treatment of patients with benign biliary strictures who cannot be managed by the endoscopic approach. Mainstays of the percutaneous technique involve precise localization of the stricture location by PTC followed by insertion of internal-external PTBD for the purpose of reestablishing biliary drainage into the bowel. Biliary drainage catheters often need to remain in place for weeks to months to allow patients to undergo periodic balloon dilation procedures. Patients with biliary strictures resistant to the conventional balloon dilation technique may benefit from Cutting balloons, large-bore PTBD, or placement of retrievable covered metal stents.
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Benign biliary strictures 11. Ramos-De la Medina A, Misra S, Leroy AJ, et al: Management of benign biliary strictures by percutaneous interventional radiologic techniques (PIRT). HPB (Oxford) 10:428-432, 2008 12. Saad WE, Davies MG, Saad NE, et al: Transhepatic dilation of anastomotic biliary strictures in liver transplant recipients with use of a combined cutting and conventional balloon protocol: Technical safety and efficacy. J Vasc Interv Radiol 17:837-843, 2006 13. Ring EJ, Husted JW, Oleaga JA, et al: A multihole catheter for maintaining longterm percutaneous antegrade biliary drainage. Radiology 132:752-754, 1979 14. Glas L, Courbiere M, Ficarelli S, et al: Long-term outcome of percutaneous transhepatic therapy for benign bilioenteric anastomotic strictures. J Vasc Interv Radiol 19:1336-1343, 2008 15. DePietro DM, Shlansky-Goldberg RD, Soulen MC, et al: Long-term outcomes of a benign biliary stricture protocol. J Vasc Interv Radiol 26:1032-1039, 2015 16. 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
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