IJGII Inernational Journal of Gastrointestinal Intervention

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Review Article

Gastrointestinal Intervention 2018; 7(2): 57-66

Published online July 31, 2018 https://doi.org/10.18528/gii180012

Copyright © International Journal of Gastrointestinal Intervention.

Anastomotic stricture after liver transplantation: It is not Achilles’ heel anymore!

Sung Ill Jang, and Dong Ki Lee*

Department of Internal Medicine, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, Korea

Correspondence to:*Department of Internal Medicine, Gangnam Severance Hospital, Yonsei University College of Medicine, 211 Eonju-ro, Gangnam-gu, Seoul 06273, Korea. E-mail address: dklee@yuhs.ac (D.K. Lee). ORCID: https://orcid.org/0000-0002-0048-9112

Received: April 19, 2018; Accepted: July 13, 2018

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

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Biliary-tract complications, such as biliary strictures, anastomotic leaks, choledocholithiasis, and biliary casts, can occur after liver transplantation (LT). Of these complications, biliary strictures are regarded as an Achilles’ heel. Recently, treatment of anastomotic biliary stricture (ABS) has transitioned from conventional surgical revision to a nonsurgical treatment modality. Endoscopic serial balloon dilatation and/or multiple plastic stent replacements are highly effective and are now regarded as the first-line treatments. However, if the patient has undergone anastomosis by means of a hepaticojejunostomy, percutaneous treatment is performed. With recent technological advances and the rendezvous method, the clinical success rates of endoscopic and percutaneous ABS treatments have increased, but these methods fail in some patients who have total obstruction of anastomotic stricture. For these patients, magnetic compression anastomosis (MCA) has been suggested as an alternative method. Animal and human studies have demonstrated the safety and efficacy of MCA, and advancements in these nonsurgical methods have increased the clinical success rate of ABS. This review focuses on ABSs that develop after LT and discusses the clinical results of various nonsurgical methods and future directions.

Keywords: Anastomosis, Bile duct obstruction, Complication, Liver transplantation, Stricture

Introduction

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Although the incidence of complications after liver transplantation (LT) has decreased because of advancements in surgical techniques, organ preservation, and immunosuppressive management, biliary complications remain common. Of these, biliary stricture and leakage occur most frequently and are affected by various factors, including the type of graft, reconstruction technique, use of biliary stents, and other characteristics of the recipient and donor. Anastomotic biliary stricture (ABS) occurs because of ischemia at the end of the bile duct, causing a fibro-proliferative response and small bile leaks that induce perianastomotic fibro-inflammatory responses. The incidence of post-LT ABS is 5% to 10% in deceased-donor LT (DDLT) and 15% to 30% in living-donor LT (LDLT).1–3 Post-LT ABS is regarded as an Achilles’ heel, because often it is not resolved even by use of multiple treatment modalities.4 Treatment methods for ABS include both surgical and nonsurgical approaches, such as endoscopic or percutaneous procedures; nonsurgical management has recently become more popular. The use of magnetic compression anastomosis (MCA) for complete biliary obstruction or severe biliary benign strictures that cannot be treated by conventional nonsurgical methods has also been discussed, and its feasibility for post-LT ABS has been suggested. This review identifies effective treatment strategies for ABS by comparing the outcomes of the various methods.

Endoscopic Management

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Endoscopic retrograde cholangiopancreatography (ERCP) has been attempted as the first-line treatment modality for post-LT biliary complications, particularly in patients undergoing LT with end-to-end anastomosis. Endoscopic treatment avoids liver puncture and enables access through a nondilated intrahepatic duct, making the procedure safe for patients with cirrhosis, ascites, or coagulopathy. Although endoscopic treatment for ABS can be successful in LT patients who receive Roux-en-Y choledochojejunostomy,5,6 it remains challenging, because of the anastomosis site must be approached using a balloon enteroscope or colonoscope. Therefore, percutaneous therapy based on interventional radiology is usually performed for ABS that develops following LT in patients undergoing Roux-en-Y choledochojejunostomy. ABS treatment by ERCP involves balloon dilatation (BD), the placement of single or multiple plastic stents (MPS), and insertion of a retrievable self-expandable metal stent (SEMS).7–9 Standard endoscopic treatment can be summarized as the use of ERCP after sphincterotomy with various combinations of progressive pneumatic BD (from 4 to 10 mm) and/or plastic- or metal-stent insertion with periodic stent replacement.

BD and/or plastic-stent insertion in patients with ABS after LT

Although the optimal treatment strategy for ABS is unclear, multiple sessions of BD followed by endoscopic placement of multiple side-by-side plastic stents (BD with MPS) is the most common approach. These treatments have success rates of 70% to 100% in DDLT patients,10–12 and 60% to 75% in LDLT patients.13–17 The incidence of recurrence is 0% to 20% and is usually managed by repeated endoscopic stent placement.3,7,18–25Tables 13,18,21–23,26–41 and 210,13–16,42–47 summarize the results of BD with MPS in DDLT and LDLT patients.

The majority of patients with ABS undergo BD and long-term stenting by ERCP at three-month intervals for 12 to 24 months to prevent clogging, cholangitis, and stone formation. This method involves passing a guidewire across the stricture, after which 8.0- to 11.5-Fr plastic stents are inserted following BD to 6 to 8 diameters. If possible, the stent diameter or the number of stents is increased at each session. Although this technique usually requires sphincterotomy of the papilla, similar ABS success rates can be achieved without sphincterotomy by placing the stent above the sphincter of Oddi.46 The clinical success rate of BD alone is < 50%, whereas that of BD with MPS is 75%.20,26,27 Dual or multiple stents yield better results than a single stent by ensuring greater dilatation of the stricture.3,23,27,32,48 Zoepf et al20 reported that BD with maximal plastic-stent insertion is more effective and has a lower recurrence rate than does BD alone.

In endoscopic treatment, differences in causes and treatment outcomes can be seen based on when stricture occurs. Generally, post-LT ABS is caused by an improper surgical technique, including excessive use of electrocoagulation, tension at the level of the anastomosis, and inappropriate bile duct dissection, as well as by small-caliber bile ducts, localized ischemia, infections, or fibrotic healing,2,49–51 with most cases occurring within 12 months after LT.36 ABS that occurs one or two months after LT may result from transient narrowing caused by postoperative edema and inflammation.49 This type of early ABS has a good response to BD with temporary stent placement.50 However, in contrast to early narrowing, treatment is more difficult in late strictures, which occur in most patients, because the strictures are more fibrotic and inherently more difficult to dilate than are early strictures because of fibrotic scarring from ischemia in the donor or recipient bile duct near the anastomosis. Therefore, late ABS is managed more aggressively, with ongoing ERCP sessions every two or three months, longer stent durations, and/or a greater number of stents in situ for 12 to 24 months.11 The recurrence rate of ABS following BD with MPS is 18%, and the mean time for recurrence is 110 days. Because there is a negligible difference between BD alone and BD with MPS in early ABSs that develop within two months after LT, even BD alone can be effective.52 However, BD with MPS would likely be more effective than BD alone for late ABS.

The procedure-related complication rate in BD with MPS is 0% to 24%, and the complications tend to be minor to moderate, e.g., leakage cholangitis, pancreatitis, and bleeding related to sphincteroplasty. The success rate is based on the time of onset of the stricture, the complexity of the deformity at the anastomosis, and the number of stents placed during the initial procedure.52 In DDLT patients, a longer stent duration and greater maximal diameter versus a greater total number of stents per patient in MPS are associated with a greater likelihood of a successful outcome.11,21 The stricture resolution rate was 97% and 78% for MPS durations of < 12 and ≥ 12 months, respectively. More stents at initial ERCP and more total stents per patient are predictive of stricture resolution.21

The outcomes of endoscopic treatment differ with the type of graft in which the stricture occurred. ABS is more common in LDLT patients than in DDLT patients, and treatment rates range from 60% to 75%, because the response to BD with MPS treatment is diminished.13–15,19 In most post-LDLT ABSs, the stricture resolution rate is lower than that for post-DDLT ABSs, because BD alone or BD followed by insertion of a single PS was performed.43,45 That is, in LDLT, the donor bile duct and strictures are smaller and anatomically more challenging, with generally more strictures in LDLT patients than in DDLT patients. Moreover, the risks of cholangitis and stent occlusion are higher in LDLT patients than in DDLT patients.11

In one study, no differences in the clinical success, failure, complication, or recurrence rates were observed in patients with post-DDLT ABSs treated with BD alone and those treated with BD with endoprosthesis.53 However, that study lacked a well-designed randomized and controlled evaluation of BD alone and BD with MPS for post-DDLT ABS; so definitive conclusions could not be drawn,7,20 because of the small number of enrolled patients. However, such studies emphasize the need for further investigation of the utility of several sessions of BD with MPS.

SEMS insertion in patients with ABS after LT

A major disadvantage of endoscopic BD with MPS treatment is the need for multiple procedures over an extended period and the risk of cholangitis resulting from stent occlusion. Although endoscopic BD with MPS management is less invasive and has a high success rate, its disadvantage is that ERCP must be repeated every three or four months for up to two years.12 Early ABS (< six months post-LT) usually has a good response to a single endoscopic therapy session, but late ABS requires longer treatment, because it is associated with ischemic injury in bile-duct anastomosis.54 Consequently, frequent replacement and an increasing number of plastic stents are needed because of the development of occlusions within three to six months; thus, BD and plastic stent placement must be performed four or five times at three-month intervals.

There have been attempts to overcome the limitations of periodic plastic-stent replacement by placing temporary single-session SEMSs. Post-LDLT ABS has the following characteristics: (1) ABS at a high level, (2) an acute-angulated bile duct, and (3) a narrow lumen of the intrahepatic duct above the ABS.

Because of these characteristics of post-LDLT ABS, MPS insertions can be technically difficult within the limited space in the intrahepatic duct and because of the high rate at which plastic stents migrate when the proximal rather than the central portion of the plastic stent is placed at the stricture. SEMS has shown promise in post-LT patients.9,55–58 In benign biliary diseases, uncovered SEMSs are susceptible to reactive hyperplasia and consequent secondary stone formation above the stent, as well as difficult removal six to nine months after placement. Because of these limitations, a partially covered or fully-covered SEMS (FCSEMS) is used for benign biliary stenosis. Recently, FCSEMS has been used in ABS after DDLT in place of an aggressive approach (MPS insertions with several sessions of ERCP).39,41

FCSEMSs have better durability and patency than do plastic stents, which reduces the number of replacement sessions.59 In a small randomized prospective study of the efficacy of FCSEMSs and plastic stents in post-LT ABS, FCSEMS reduced the number of ERCP sessions needed to resolve ABS, with similar recurrence rates and lower complication rates compared to plastic stents.59 This modified FCSEMS (KAFFESTM; Taewoong Medical, Seoul, Korea) has a central waist to prevent its migration and a long string to facilitate removal using standard endoscopic biopsy forceps. The structural benefits of the modified FCSEMS can be expected to improve the clinical resolution of post-LDLT ABS. Moreover, FCSEMS can be an effective salvage treatment for patients with a failed plastic-stenting treatment (Fig. 1).9,56 If the strictness of the stricture is technically severe, it is advantageous to perform the BD in advance and enter the introducer of the FCSEMS.

In many cases, stenting is placed at an acute angle, which hampers stent release. In such cases, stent deployment can be accomplished by pushing the stent far enough inside the stricture, or by lowering the stent down into the stricture, deploying the stent a little, reinserting it into the introducer, and placing the stent in the middle portion of the stricture. The disadvantage of this stent is occasional detachment of the silk thread (string) used for removal. In this case, the stent can be removed from the common bile duct (CBD) by using grasping forceps (Fig. 2). The more common problem of this FCSEMS is sludge or stone formation in the inner lumen of the stent cavity. This problem is more frequent in LT patients than in those with other benign biliary strictures (BBSs), presumably because of epithelial dysfunction of the donor liver. This limits the stent indwelling duration to three or four months. If stricture resolution is incomplete after placement of the first SEMS, insertion of a second SEMS is advantageous. To overcome this problem, one should try to reduce sludge formation by hydrophilic or hydrophobic coating of the inner lumen of the SEMS-covering membrane.

Although SEMSs are reportedly effective in patients who are refractory to plastic-stent treatment, there are arguments for its use as the initial method. Unfortunately, a comparative study on BD with MPS and SEMS lacked a large randomized and controlled trial directly comparing the two, and there are limitations in drawing conclusions from other existing studies because of the heterogeneity of the SEMSs used. In previous studies, SEMSs had a stricture-resolution rate very similar to that for MPS. However, because SEMSs have higher migration rates and differing results,11 their efficacy in patients with ABS compared to that of maximal plastic-stent therapy is unclear. The ABS resolution rate is 80% to 95% when SEMS patency is ≥ 3 months and 94% to 100% when dilatation and plastic-stent treatments last for 12 months.11 Although the clinical success rate of biliary stricture treatment using SEMS is 86.4% to 100%, the rates of migration rate (4%–37%) and complications (0%–41%) are high.9 The main concern in using covered SEMSs is migration and the risk of occluding secondary branch ducts or the pancreatic duct, which could cause cholangitis and pancreatitis.60 SEMSs have a high rate of migration, and mucosal hyperplasia-induced stricture can occur at the proximal uncovered end of partially covered SEMSs.61 Moreover, SEMS removal is labor-intensive and can occasionally cause mucosal ulceration and bleeding because of the use of traumatic anti-migration systems (e.g., anchor fins).62 Therefore, a FCSEMS without a traumatic anti-migration system is recommended for treating BBSs,9 and new types of SEMSs are needed. For thetreatment of post-LT ABS, although the efficacy of SEMS and MPS has been evaluated,39,41 a large randomized and controlled trial and more data are needed to reach definitive conclusions about SEMSs as compared to BD with MPS in terms of deciding on the optimal stenting protocol, duration, indications, and cost-effectiveness, and whether they should be the primary or secondary treatment modality after MPS replacement.

Percutaneous Treatment

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Endoscopic methods are generally accepted as the first-line treatment for post-LT biliary complications, although these treatments are virtually impossible in patients receiving LT with hepaticojejunostomy (HJ).63,64 Although endoscopic access to the HJ site has become possible with advances in small-bowel endoscopy and balloon endoscopy, its use is limited to hospitals because of the long case times, considerable operator expertise, consistent caseloads required, limited availability of balloon enteroscopes, smaller channel size, and fewer endoscopic accessories; furthermore, its efficacy has not yet been firmly established.65 In duct-to-duct anastomosis, recanalization using ERCP can fail if the anastomosis is pouch-shaped.66 Moreover, because the success rate of percutaneous treatment is 40% to 80%, like that of endoscopic treatment, it is considered an important treatment method for biliary complications.67,68 A meta-analysis of ABS in DDLT patients revealed no significant differences in the successful intervention rate (60% vs 59.3%; P = 1.00), time to recurrence after successful intervention (44.8 ± 7.4 months vs 41.9 ± 3.4 months; P = 0.47), or complication rate (24% vs 23%) between endoscopic treatment and percutaneous treatment. However, the number of intervention sessions was higher for percutaneous treatment (7.2 ± 0.6) than for endoscopic treatment (2.9 ± 0.6) (P < 0.01).53 A retrospective study of 498 patients who underwent percutaneous treatment for post-LDLT ABS reported a success rate of 98%, clinical success rate of 88.4%, and recurrence rates of 5% to 17.1%.64 The success rate of percutaneous treatment has increased because of advances in cannulation techniques, such as the conventional 0.035-inch guidewire, microcatheter, and rendezvous techniques.69–72 However, although percutaneous treatment yielded a success rate of 40% to 85%,72–77 the procedure is invasive and associated with complications, including hemorrhage, bile leakage, and significant morbidity. Cannulation is difficult if the intrahepatic ducts are not dilated sufficiently, and it involves a 2.2% risk of hepatic-artery injury. Furthermore, prolonged use of percutaneous drainage catheters can cause discomfort in patients; hence, percutaneous treatment can be considered a second-line option for post-LT ABS.64,78 For this reason, it is important to increase the treatment rate of ABS by performing percutaneous treatment in ABS patients who failed endoscopic treatment.10,66,79 The rendezvous technique, which combines percutaneous transhepatic biliary drainage and ERCP, involves support from an external drainage catheter. Its success rate is very high, and it is especially useful in angulated and twisted strictures.80 In a study using the rendezvous technique to treat ABS by means of an ordinary guidewire, such as the Kumpe® access catheter (Cook Medical, Bloomington, IN, USA), the procedural time was reduced. Therefore, in cases with technically difficult biliary access via an endoscopic approach, a percutaneous approach can be useful as an endoscopic and percutaneous/surgical method.69,70,81,82

Other Approaches

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In post-LT ABS patients, the use of paclitaxel-eluting ballooning shows promise. In a prospective study of 13 ABS patients, paclitaxel-eluting balloon treatment yielded a sustained clinical success rate of 92%; indeed, the clinical success rate was high after a single intervention.83 In a prospective pilot study, these treatments had a 92.3% clinical success rate during a two-year follow-up.84 Because paclitaxel-eluting ballooning can decrease the overall duration of endoscopic treatment by reducing the number of interventions required, a large randomized and controlled trial is warranted.

New intraductal endoscopy techniques, such as the incorporation of the SpyGlass direct-visualization system (Boston Scientific, Natick, MA, USA), can facilitate the passage of guidewires through tight strictures by enabling direct observation of the inner wall of the biliary duct.85–87 The development and modification of balloons and stents is ongoing. The development of new balloons, such as cutting balloons, can increase the success rate of stent insertion by enabling recanalization of tight strictures.88

Use of bioabsorbable materials in covered SEMSs obviates the need for additive procedures for stent removal, and benefits from impregnated antimicrobial and antineoplastic agents are anticipated. However, the efficacies of these methods are unclear at present,89,90 and further studies are needed to compare the clinical success rates and cost-effectiveness of endoscopic and percutaneous methods.

MCA in Patients with Totally Occluded ABS

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Endoscopic and percutaneous procedures have high success rates in post-LT ABS. However, recanalization is impossible with conventional endoscopic and percutaneous methods in cases of a severe stricture or complete obstruction that prevents passage of the guidewire. In such cases, surgical revision must be performed, or external drainage catheters must be maintained. Surgical revision of BBSs has morbidity and mortality rates of 9.1% to 28% and 0% to 2.6%, respectively. Moreover, the rate of recurrent strictures requiring further interventions following surgical revision is 10% to 30%. Catheter-related complications can arise when percutaneous external drainage catheters are maintained, and the patient’s quality of life can be compromised. MCA was developed as a nonsurgical alternative for patients with BBSs in whom conventional endoscopic or percutaneous methods failed.91–100 The attractive force from the two magnets on both sides of the ABS creates compression, which induces ischemia in the ABS tissue. As the two magnets approach each other, complete necrosis of ABS tissues occurs, and a new fistula is formed to complete the recanalization (Fig. 3). An animal study of anastomoses formed by MCA and surgical hand-suturing revealed no differences in gross appearance, histology, functionality, or mechanical integrity.101 Histologically, MCA-formed anastomoses exhibited continuity of the serosal, submucosal, and mucosal layers, but neither ischemia nor necrosis.102,103 Thus, MCA is safe and equivalent or superior to anastomoses created by traditional suturing or stapling techniques. Overall, 22 MCA procedures for bilio-biliary anastomosis and eight MCA procedures for bilio-enteric anastomosis have been performed in patients with BBSs.91–100 One study observed a stricture resolution rate of 83.3% without complications after MCA performed in patients with post-LT ABS that was refractory to conventional methods, demonstrating the safety and feasibility of MCA.91 Restenosis occurred in only one of the patients who underwent MCA, but recanalization was achieved by conventional endoscopic methods.91 Since fistulas formed by MCA were formed from necrosis of ABS fibrotic tissue, the restenosis rate is expected to be low because of elastic recoiling of fibrotic tissue. However, although mid-term follow-up reports show a low recurrence rate,104 there are still limitations in the usefulness of MCA for post-LT ABS, in that there have not been any case reports or case series about it, and long-term follow-up data are lacking.91,93–100 Another limitation is the lack of a noninvasive modality to evaluate the probability of success of MCA. Even if the length of the stricture is measured before MCA by computed tomography, magnetic resonance cholangiopancreatography, and ERCP, MCA can fail if the distance is too great or the axes of the magnet are in parallel.91 The greater the distance between the magnets, the weaker the attractive power, and magnetic approximation may not occur. In one case, two magnets on the intrahepatic side were used to increase the attractive power, which resulted in successful MCA (Fig. 4). In MCA, various endoscopic and percutaneous methods, along with a surgically made fistula, are used to deliver the magnets.92 Endoscopic and percutaneous tracts are used primarily in post-LT ABS, but in other types of ABS, the delivery route appropriate for each case was used, indicating that no magnet-delivery system has been firmly established. Therefore, development of a pre-MCA assessment method for predicting outcomes, smaller and more powerful magnets, and an effective magnet-delivery system are needed, as are long-term follow-up data obtained from large-scale studies.

Conclusion

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The proposed treatment modality for post-LT ABS is as follows (Fig. 5). The initial treatment modality is endoscopic for duct-to-duct anastomosis or percutaneous for HJ anastomosis. If endoscopic treatment fails for duct-to-duct anastomosis, one could try to convert to percutaneous treatment. If percutaneous treatment fails for HJ anastomosis, recanalization by an endoscopic procedure and/or the rendezvous method is a possibility, as they are for duct-to-duct anastomosis. In cases of failed endoscopic and percutaneous therapy for ABS, MCA is an alternative method. Application of these various modalities is expected to increase the success rate of ABS treatment.

For ABS occurring after LT, the clinical success rates of endoscopic and percutaneous methods have been increased by novel ERCP techniques, advances in endoscopy, better guidewire techniques, and improvements in stent design. Moreover, use of the organic rendezvous technique, which encompasses these two methods, can increase the success rate in patients in whom one of the methods has failed. Furthermore, because MCA has been proposed as an effective and safe alternative for cases that cannot be treated by endoscopic and percutaneous methods, the treatment rate of ABS is expected to increase, whereas reliance on surgical modalities is expected to decrease. In conclusion, ABS after LT is no longer an Achilles’ heel, and adverse events are effectively manageable.

Acknowledgments

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Authors’ contributions: Jang SI reviewed the literature, collected data, and wrote the first draft of this manuscript; Lee DK designed, reviewed the literature, revised the paper, and performed significant editing.

Figures

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Fig. 1. Cholangiogram showing the use of a retrievable, fully covered, self-expandable metal stent (FCSEMS) with a long removal string to treat a biliobiliary stricture that developed after living-donor liver transplantation (LDLT). (A) Multiple sessions of balloon dilatation with multiple plastic stenting failed to resolve the anastomotic biliary stricture (ABS) after LDLT. (B) Two guidewires were passed though ABSs to the superior and inferior intrahepatic ducts in the right hepatic lobe. (C) Two FCSEMSs were inserted for two months. (D) The FCSEMSs were removed because the ABSs had resolved.
Fig. 2. Cholangiogram showing the removal of a retrievable, fully covered, self-expandable metal stent (FCSEMS) with a detached string. (A) An anastomotic biliary stricture (ABS) developed after living-donor liver transplantation, which was not resolved by multiple endoscopic sessions of balloon dilatation with multiple plastic stenting. (B) FCSEMS and plastic stent were inserted in the ABS. (C) After two months, the plastic stent and FCSEMS were planned to be removed. (D) The removal string detached from the FCSEMS. (E) The FCSEMS was easily removed without complications using biopsy forceps. (F) The ABS had resolved.
Fig. 3. Cholangiogram showing the use of magnetic compression anastomosis to treat a biliobiliary stricture that developed after living-donor liver transplantation. (A) Endoscopy could not be used to pass a guidewire because of a severe stricture at the site of the anastomosis. After injection of contrast medium through a percutaneous transhepatic tract, the medium did not drain to the common bile duct (CBD) because the obstruction was complete. (B) After insertion of a percutaneous transhepatic biliary drainage (PTBD) catheter, the tract was dilated to 18 F, and a covered self-expandable metal stent was inserted into the CBD. (C) A magnet attached to a polypectomy snare was delivered via an endoscopic retrograde cholangiopancreatography (ERCP) scope through the CBD. (D) A second magnet was fixed to alligator forceps and moved toward the anastomosis site through the PTBD tract. The magnets were approximated, and the PTBD catheter inserted. (E) After removal of the approximated magnets, a retrievable, fully covered, self-expandable metal stent (FCSEMS) was inserted for six months. (F) The FCSEMS was removed, and a new fistula had formed.
Fig. 4. Cholangiogram showing the performance of magnetic compression anastomosis using three magnets. (A) After living-donor liver transplantation, a completely obstructed anastomotic stricture occurred, and a percutaneous transhepatic biliary drain (PTBD) was inserted. (B) One magnet (diameter × length: 4 mm × 8 mm) was moved through the PTBD tract and a second magnet (2 mm × 6 mm) was moved to the common bile duct (CBD), but the approximation failed. (C) One magnet (4 mm × 8 mm) was moved through the PTBD tract and the other magnet (4 mm × 8 mm) was moved to the CBD, but the approximation again failed. (D) Two magnets (4 mm × 8 mm) were moved to the PTBD tract and the other magnet (2 mm × 6 mm) was moved to the CBD; the approximation was successful. (E) The approximated magnets were removed, and a new fistula had formed. (F) A fully-covered self-expandable metal stent and plastic stent were inserted into the newly formed fistula.
Fig. 5. Proposed treatment algorithm for anastomotic biliary stricture (ABS) after liver transplantation (LT).

Tables

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Outcomes of Endoscopic Treatment of ABS in Deceased-Donor LT

Author (year) No. of patients Type of report Interval of ABS after LT Technique No. of procedures per patient (mean) Technical success rate (%) Interval of stenting Ratio of stent insertion (%) Stent-free follow-up (mo) Clinical success rate (%) Recurrence rate (%) Complication (%) Recurrence treatment
Mahajani et al26 (2000) 30 R 6.9 wk BD ± stent 2 100 14 wk - 17.9 100 10 6.4 T-tube, PTBD
Schwartz et al27 (2000) 15 R 19.9 wk BD 1.87 73.3 - - 25.2 80 27.7 17.4 Surgery, ERCP
Chahin et al28 (2001) 22 R - BD + stent - 100 3–4 mo - 12 68.8 9 13.6 -
Morelli et al23 (2003) 25 R 7.8 wk BD + stent 3.1 88 13 wk - 54 80 0 3.7 None
Graziadei et al3 (2006) 65 P - BD ± stent 4.1 89.2 4 mo 71 42.2 76.9 - 1.2 -
Akay et al22 (2006) 20 R - BD ± stent 1.65 75 3 mo 73.3 22 53.3 10 20 Surgery, ERCP
Holt et al29 (2007) 53 P - BD + stent 3 92 - 100 18 69 3 20.7 Surgery
Pasha et al30 (2007) 25 R 2 mo BD + stent 3.5 88 2–3 mo 100 21.5 91 18.1 5 Surgery, ERCP
Elmi and Silverman18 (2007) 15 R 29 days Stent ± BD 3.5 100 - 73.4 17.5 87 6.7 33.3 -
Barriga et al31 (2008) 22 R 53 mo BD + stent 3.6 95.5 2–4 mo 100 24 67 13.6 4.2 Surgery
Morelli et al32 (2008) 38 P 88.9 days BD + stent 3.45 100 2 wk 100 11.8 87 13.1 5.2 Surgery, ERCP
Tabibian et al21 (2010) 83 R 20 mo BD + stent 3 83.1 3 mo 100 11 94 3 5.7 ERCP
Sanna et al33 (2011) 34 R - BD ± stent - 90.7 - - - 64.7 17.6 - Surgery
Cai et al34 (2012) 38 R 6.73 mo BD + stent 4.86 83.9 3 mo 100 10 83..9 27.7 16.1 -
Poley et al35 (2013) 31 R - BD + stent 5 100 3 mo 100 28 80.6 19.3 67.7 Surgery, FCSEMS
Albert et al36 (2013) 47 R 16.25 mo BD ± stent 4.2 100 - 57.4 37.5 95.7 34 16 ERCP
Faleschini et al37 (2015) 79 R - BD + stent 3 100 2–3 mo 100 - 68 - 4 -
Tringali et al38 (2016) 51 R 6.8 mo Additive stenting 4 100 4 mo 100 5.8 yr 98 6 5.4 -
Tal et al39 (2017) 58 RCT 5.4 mo FCSEMS 2 100 4–6 mo 100 13.8 100 20.8 4.1 -
7.4 mo MPS 4 95.8 6–12 wk 100 17.1 95.8 20.8 4.1 -
Barakat et al40 (2018) 32 P - Additive stenting 4.1 100 2.5–3 mo 100 6 96.9 1.1 3.1 -
45 - Stent exchange 6.2 100 2.5–3 mo 100 6 95.6 1.4 4.4 -
Martins et al41 (2018) 32 RCT 7.7 mo FCSEMS 2 100 6 mo 100 36.4 83.3 23.3 32 -
32 9.3 mo MPS 4.9 100 12 mo 100 32.9 96.5 6.4 0 -

ABS, anastomotic biliary stricture; LT, liver transplantation; R, retrospective; P, prospective; RCT, randomized controlled trial; BD, balloon dilatation; FCSEMS, fully-covered self-expandable metal stent; MPS, multiple plastic stents; PTBD, percutaneous transhepatic biliary drainage; ERCP, endoscopic retrograde cholangiopancreatography.

Outcomes of Endoscopic Treatment of ABS in Living-Donor LT

Author (year) No. of patients Type of report Interval of ABS after LT Technique No. of procedures per patient (mean) Technical success rate (%) Interval of stenting Ratio of stent insertion (%) Stent-free follow-up (mo) Clinical success rate (%) Recurrence rate (%) Complication (%) Recurrence treatment
Hisatsune et al42 (2003) 14 R - BD + stent* 1 77.8 - 100 19.2 92.8 0 7.1 Surgery
Tsujino et al43 (2006) 17 R - BD ± stent 4.3 71 3 mo 33.3 10.1 56 33.3 8.3 ERCP
Yazumi et al44 (2006) 75 R 186 days BD ± stent 2.7 64 6 mo 73.3 8.8 70.7 5.5 7.3 ERCP
Seo et al13 (2009) 26 R 8.6 mo BD + stent 1.1 57.6 - 100 31 64.5 30 - ERCP, PTBD
Kato et al14 (2009) 41 R - BD + stent 5.4 85 - 100 21.5 51 25 19 ERCP
Chang et al16 (2010) 101 R 6 mo BD + stent 3.2 52 - 100 22 45 - 18.8 -
Lee et al45 (2011) 137 R 6.6 mo BD + stent 4.8 46.7 - 100 - - - - -
Kim et al15 (2011) 147 R 22.4 wk BD + stent 6.3 55.8 Several months 100 21.5 36.9 11.5 7.2 ERCP
Kurita et al46 (2013) 94 R 6.4 mo BD + stent 1.4 79.7 7.1 mo 100 53 90.1 9.9 22.3 ERCP, PTBD, re-LT
Hsieh et al47 (2013) 41 R 2.1 mo BD + stent 4.0 84.2 2–3 mo 100 70 100 21 17.1 ERCP
Chok et al10 (2014) 56 R - BD ± stent 3 - 6 wk - 66.6 73.2 - 40 -

ABS, anastomotic biliary stricture; LT, liver transplantation; R, retrospective; BD, balloon dilatation; ERCP, endoscopic retrograde cholangiopancreatography; PTBD, percutaneous transhepatic biliary drainage.

Inside stent was placed within the choledochus above the sphincter of Oddi without performing endoscopic sphincterotomy.

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