Clinical Report
New endoscopic classification system for biliary stricture after liver transplantation
Journal of International Medical Research 2014, Vol. 42(2) 566–571 ! The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0300060513507761 imr.sagepub.com
Zhichu Qin* and En-Qiang Linghu*
Abstract Aim: A new classification system for biliary stricture (BS) after liver transplantation (LT) is proposed, aiming to standardize endoscopic treatment for this condition. Methods: Data were retrospectively collected from patients who had undergone endoscopic retrograde cholangiography after LT, and who provided endoscopy images clear enough to reveal the biliary system. Images were classified separately by two endoscopists, who discussed and resolved any disputed findings. From these images, a new classification system is proposed (Ling classification): type A, normal biliary structure; type B, anastomotic stricture and normal intrahepatic biliary structure; type C, narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast without anastomotic stricture; type D, narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast with anastomotic stricture. Results: Analysis involved 93 patients: 76 men and 17 women, median age 54 years (range, 12–69 years). Type B was the most commonly observed BS after LT, accounting for 44 cases (47.3%). Type A, the least commonly observed type, accounted for nine (9.7%), type C for 22 (23.7%) and type D for 18 (19.3%) cases. Conclusion: A new endoscopic classification system for BS after LT is proposed, to help determine the most appropriate treatment for patients with each type of stricture.
Keywords Liver transplantation, biliary stricture, classification, endoscopic retrograde cholangiography Date received: 8 September 2013; accepted: 14 September 2013
Department of Gastroenterology, People’s Liberation Army General Hospital, Beijing, China *These authors contributed equally to this work.
Corresponding author: Dr En-Qiang Linghu, Department of Gastroenterology, People’s Liberation Army General Hospital, 28 Fuxing Road, Beijing 100853, China. Email: [email protected]
Creative Commons CC-BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 3.0 License (http://www.creativecommons.org/licenses/by-nc/3.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified Downloaded from imr.sagepub.com by guest on November 14, 2015 on the SAGE and Open Access page (http://www.uk.sagepub.com/aboutus/openaccess.htm).
Qin and Linghu
567
Introduction Surgical techniques, methods of graft preservation and immunosuppressive drugs for liver transplantation (LT) have improved steadily over the years, but the rate of biliary stricture (BS) remains at 16.2–35.6% for living donor liver transplants,1–5 due to the nature of the surgery and possible postsurgical complications. Treatment for BS has evolved, with the development of less invasive techniques including endoscopic retrograde cholangiopancreatography and transhepatic percutaneous drainage.6–8 Use of the transhepatic percutaneous approach is inconvenient for patients, requiring them to maintain percutaneous drainage tubes for several months.9 Endoscopic retrograde cholangiography (ERC) is considered diagnostic for BS after LT, with therapeutic endoscopy and radiological techniques replacing surgery in the majority of cases as first line therapy, with high success rates.10–13 Until now there has been no standard endoscopic classification for BS after LT. The purpose of the present study was to develop a classification system for BS on the basis of endoscopic pictures after LT, and to use this system to establish an appropriate management strategy for patients. The proposed classification system is named the Ling classification because Ling is short for Linghu, the family name of the corresponding author.
Patients and methods This retrospective study analysed the endoscopic examinations of patients with jaundice who had undergone cadaveric or living donor liver transplantation at the Department of Gastroenterology, People’s Liberation Army General Hospital, Beijing, China between May 2006 and September 2011. Two endoscopists (E-Q.L. and Z.Q.) independently recorded the characteristics of intrahepatic biliary and anastomotic
stricture, and classified patients into four groups according to their findings: type A, normal biliary structure; type B, anastomotic stricture and normal intrahepatic biliary structure; type C, narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast without anastomotic stricture; type D, narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast with anastomotic stricture.
Results In total, there were 93 patients (76 men and 17 women) for whom clear pictures of ERC were available: 15 (16.1%) had undergone living donor liver transplantation; 78 (83.9%) had received cadaver organs. The median age of patients was 54 years (range, 12–69 years). The proportion of each Ling subtype in the included cases is shown in Table 1; typical images obtained for each subtype are shown in Figures 1–5. Of the nine patients classified as Ling A, two had repeated episodes of jaundice with normal ERC results. Their symptoms were alleviated with endoscopic nosalbiliary drainage. The remaining seven patients were treated medically with ursodeoxycholic acid capsules 250 mg, orally, twice daily for 1 month. The 44 patients classified as Ling B were treated with balloon dilatation, stent drainage, external drainage of the bile duct or transhepatic percutaneous drainage. In 40 patients classified as Ling B, endoscopic treatment was successful. One patient from this group developed a severe infection postoperatively and died of multiple organ failure; a further three patients with repeated severe jaundice were treated either surgically to repair the stricture or with biliary–enteric anastomosis, and these measures relieved the symptoms. There were 22 patients classified as Ling C, all of whom were treated
Downloaded from imr.sagepub.com by guest on November 14, 2015
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Journal of International Medical Research 42(2)
Table 1. New endoscopic classification system (Ling Classification) for biliary stricture after liver transplantation, as seen in a series of 93 patients. Type
Anastomosis
State of intrahepatic biliary system
Patients, n
Proportion, %
A B C
Normal Stricture Normal
9 44 22
9.7 47.3 23.7
D
Stricture
Normal Normal Narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast Narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast
18
19.3
Figure 1. Endoscopic image of a Ling classification Type A (normal biliary structure) following liver transplantation. Outside diameter of the endoscope is 12 mm.
Figure 2. Endoscopic image of Ling classification Type B (anastomotic stricture, shown by the arrow, and normal intrahepatic biliary structure) following liver transplantation. Outside diameter of the endoscope is 12 mm.
with endoscopic retrograde biliary drainage (ERBD) and cleaning with ‘bolt-shaped’ material. Eighteen patients were treated successfully, two patients died of multiple organ failure and two patients required a second liver transplant, after which their symptoms were alleviated. Of the 18 patients classified as Ling D, all were treated
with ERBD and cleaning with ‘boltshaped’ material. This procedure successfully mitigated symptoms in 13 patients; one patient had lung metastases and died of respiratory failure, two patients were treated with biliary–enteric anastomosis and two patients required a second liver transplant.
Downloaded from imr.sagepub.com by guest on November 14, 2015
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Figure 3. Endoscopic image of Ling classification Type C (narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast without anastomotic stricture, shown by arrow) following liver transplantation. Outside diameter of the endoscope is 12 mm.
Figure 4. Endoscopic image of Ling classification Type D (narrow and stiff intrahepatic biliary structure, shown by the top arrow, or beaded intrahepatic biliary structure or intrahepatic biliary cast with anastomotic stricture, shown by the bottom arrow) following liver transplantation. Outside diameter of the endoscope is 12 mm.
Discussion Biliary complications are a frequent cause of morbidity and mortality after LT, occurring in between 5.8 and 39.5% of reported cases.6–8,14–18 The most frequent biliary complications are BS, which affect 16.2– 35.6% of patients,1–5 and are classified as anastomotic or nonanastomotic.8,19 Strictures restricted to the anastomotic site are likely to be related to problems encountered during surgery and the type of biliary reconstruction; they are isolated and short, with a reported incidence of 4–9%.20 Nonanastomotic strictures generally occur in groups, are longer than anastomotic strictures, are located in either the intrahepatic and/or donor duct proximal to the anastomotic site and have an incidence of 5–15%.21 Nonanastomotic strictures result primarily from hepatic artery thrombosis.22
Figure 5. Endoscopic image of a Ling classification Type D intrahepatic biliary cast. Outside diameter of the endoscope is 12 mm. The colour version of this figure is available online at http://imr.sagepub.com.
Downloaded from imr.sagepub.com by guest on November 14, 2015
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Journal of International Medical Research 42(2)
Identified causes include chronic ductopenic rejection, ABO incompatibility, ischaemia/ reperfusion injury or recurrence of primary diseases such as primary sclerosing cholangitis or autoimmune hepatitis.22 Biliary strictures can be treated by one or more interventions, including endoscopic transpapillary cholangiography, transhepatic percutaneous cholangiography or transhepatic percutaneous drainage, and/or surgical approaches.23,24 Endoscopic retrograde cholangiography is generally the firstline therapy for BS after LT and has a success rate of between 36.9 and 68%.10–13 However, treatment varies, depending on the features of the BS, hence the need for a standard and clear classification system, for which the Ling classification is proposed. In our study, type B was the most commonly observed BS after LT, accounting for 44 cases (47.3%), and type A was the least commonly observed, accounting for just nine cases (9.7%) of cases. In our experience, patients with type A BS will have symptomatic remission treated with drainage and medical therapy: their jaundice may be caused by a graft rejection reaction. Conversely, patients with type A BS were almost all treated by endoscopic transpapillary cholangiography or transhepatic percutaneous cholangiography, including balloon dilatation and stent drainage. No patients in the present study displayed a type B stricture and retained normal liver function. For patients with type C or D BS, endoscopy treatment was initially most useful,l but surgical repair and retransplantation were necessary for those who needed further endoscopic treatments or who failed endoscopic treatment. Although type C and D BS underwent the same treatment strategies, they were separated into two classifications because of anatomical differences in their appearance. The authors acknowledge there were a number of limitations to the present study, such as the small sample size and the lack of
long-term follow-up. Thus, further prospective studies are needed, to determine the validity of the proposed Ling classification system for selecting candidates for appropriate treatment. In conclusion, we hope that the Ling classification might help in determining the appropriate treatment strategy for patients with BS after LT. Further prospective studies are needed to determine the usefulness of the Ling classification system.
Declaration of conflicting interest The authors had no conflicts of interest to declare in relation to this article.
Funding This research received no specific grant from any funding agency in the public, commercial or notfor-profit sectors.
References 1. Hisatsune H, Yazumi S, Egawa H, et al. Endoscopic management of biliary strictures after duct-to-duct biliary reconstruction in right-lobe living-donor liver transplantation. Transplantation 2003; 76: 810–815. 2. Kasahara M, Egawa H, Takada Y, et al. Biliary reconstruction in right lobe livingdonor liver transplantation: Comparison of different techniques in 321 recipients. Ann Surg 2006; 243: 559–566. 3. Yamamoto S, Sato Y, Oya H, et al. Risk factors and prevention of biliary anastomotic complications in adult living donor liver transplantation. World J Gastroenterol 2007; 13: 4236–4241. 4. Ohkubo M, Nagino M, Kamiya J, et al. Surgical anatomy of the bile ducts at the hepatic hilum as applied to living donor liver transplantation. Ann Surg 2004; 239: 82–86. 5. Shah SA, Grant DR, McGilvray ID, et al. Biliary strictures in 130 consecutive right lobe living donor liver transplant recipients: results of a Western center. Am J Transplant 2007; 7: 161–167.
Downloaded from imr.sagepub.com by guest on November 14, 2015
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6. Park JS, Kim MH, Lee SK, et al. Efficacy of endoscopic and percutaneous treatments for biliary complications after cadaveric and living donor liver transplantation. Gastrointest Endosc 2003; 57: 78–85. 7. Rerknimitr R, Sherman S, Fogel EL, et al. Biliary tract complications after orthotopic liver transplantation with choledochocholedochostomy anastomosis: endoscopic findings and results of therapy. Gastrointest Endosc 2002; 55: 224–231. 8. Tabibian JH, Asham EH, Goldstein L, et al. Endoscopic treatment with multiple stents for post-liver-transplantation nonanastomotic biliary strictures. Gastrointest Endosc 2009; 69: 1236–1243. 9. Ko GY, Sung KB, Yoon HK, et al. Percutaneous transhepatic treatment of hepaticojejunal anastomotic biliary strictures after living donor liver transplantation. Liver Transpl 2008; 14: 1323–1332. 10. Seo JK, Ryu JK, Lee SH, et al. Endoscopic treatment for biliary stricture after adult living donor liver transplantation. Liver Transpl 2009; 15: 369–380. 11. Kato H, Kawamoto H, Tsutsumi K, et al. Long-term outcomes of endoscopic management for biliary strictures after living donor liver transplantation with duct-toduct reconstruction. Transpl Int 2009; 22: 914–921. 12. Yazumi S, Yoshimoto T, Hisatsune H, et al. Endoscopic treatment of biliary complications after right-lobe living-donor liver transplantation with duct-to-duct biliary anastomosis. J Hepatobiliary Pancreat Surg 2006; 13: 502–510. 13. Kim TH, Lee SK, Han JH, et al. The role of endoscopic retrograde cholangiography for biliary stricture after adult living donor liver transplantation: technical aspect and outcome. Scand J Gastroenterol 2011; 46: 188–196. 14. Salahi H, Razmkon A, Mehdizadeh AR, et al. Biliary tract complications after liver transplantation in a single center. Transplant Proc 2005; 37: 3177–3178. 15. Mata A, Bordas JM, Llach J, et al. ERCP in orthotopic liver transplanted patients.
16.
17.
18.
19.
20.
21.
22.
23.
24.
Hepatogastroenterology 2004; 51: 1801–1804. Amador A, Charco R, Martı´ J, et al. One thousand liver transplants: the hospital clinic experience. Transplant Proc 2005; 37: 3916–3918. Abdullah K, Abdeldayem H, Hali WO, et al. Incidence and management of biliary complications after orthotopic liver transplantation: ten years’ experience at King Fahad National Guard Hospital. Transplant Proc 2005; 37: 3179–3181. Alsharabi A, Zieniewicz K, Patkowski W, et al. Assessment of early biliary complications after orthotopic liver transplantation and their relationship to the technique of biliary reconstruction. Transplant Proc 2006; 38: 244–246. Sossenheimer M, Slivka A and Carr-Locke D. Management of extrahepatic biliary disease after orthotopic liver transplantation: review of the literature and results of a multicenter survey. Endoscopy 1996; 28: 565–571. Thuluvath PJ, Atassi T and Lee J. An endoscopic approach to biliary complications following orthotopic liver transplantation. Liver Int 2003; 23: 156–162. Alazmi WM, Fogel EL, Watkins JL, et al. Recurrence rate of anastomotic biliary strictures in patients who have had previous successful endoscopic therapy for anastomotic narrowing after orthotopic liver transplantation. Endoscopy 2006; 38: 571–574. Lee HW, Suh KS, Shin WY, et al. Classification and prognosis of intrahepatic biliary stricture after liver transplantation. Liver Transpl 2007; 13: 1736–1742. Schwartz DA, Petersen BT, Poterucha JJ, et al. Endoscopic therapy of anastomotic bile duct strictures occurring after liver transplantation. Gastrointest Endosc 2000; 51: 169–174. Mahajani RV, Cotler SJ and Uzer MF. Efficacy of endoscopic management of anastomotic biliary strictures after hepatic transplantation. Endoscopy 2000; 32: 943–949.
Downloaded from imr.sagepub.com by guest on November 14, 2015
New endoscopic classification system for biliary stricture after liver transplantation
Journal of International Medical Research 2014, Vol. 42(2) 566–571 ! The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0300060513507761 imr.sagepub.com
Zhichu Qin* and En-Qiang Linghu*
Abstract Aim: A new classification system for biliary stricture (BS) after liver transplantation (LT) is proposed, aiming to standardize endoscopic treatment for this condition. Methods: Data were retrospectively collected from patients who had undergone endoscopic retrograde cholangiography after LT, and who provided endoscopy images clear enough to reveal the biliary system. Images were classified separately by two endoscopists, who discussed and resolved any disputed findings. From these images, a new classification system is proposed (Ling classification): type A, normal biliary structure; type B, anastomotic stricture and normal intrahepatic biliary structure; type C, narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast without anastomotic stricture; type D, narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast with anastomotic stricture. Results: Analysis involved 93 patients: 76 men and 17 women, median age 54 years (range, 12–69 years). Type B was the most commonly observed BS after LT, accounting for 44 cases (47.3%). Type A, the least commonly observed type, accounted for nine (9.7%), type C for 22 (23.7%) and type D for 18 (19.3%) cases. Conclusion: A new endoscopic classification system for BS after LT is proposed, to help determine the most appropriate treatment for patients with each type of stricture.
Keywords Liver transplantation, biliary stricture, classification, endoscopic retrograde cholangiography Date received: 8 September 2013; accepted: 14 September 2013
Department of Gastroenterology, People’s Liberation Army General Hospital, Beijing, China *These authors contributed equally to this work.
Corresponding author: Dr En-Qiang Linghu, Department of Gastroenterology, People’s Liberation Army General Hospital, 28 Fuxing Road, Beijing 100853, China. Email: [email protected]
Creative Commons CC-BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 3.0 License (http://www.creativecommons.org/licenses/by-nc/3.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified Downloaded from imr.sagepub.com by guest on November 14, 2015 on the SAGE and Open Access page (http://www.uk.sagepub.com/aboutus/openaccess.htm).
Qin and Linghu
567
Introduction Surgical techniques, methods of graft preservation and immunosuppressive drugs for liver transplantation (LT) have improved steadily over the years, but the rate of biliary stricture (BS) remains at 16.2–35.6% for living donor liver transplants,1–5 due to the nature of the surgery and possible postsurgical complications. Treatment for BS has evolved, with the development of less invasive techniques including endoscopic retrograde cholangiopancreatography and transhepatic percutaneous drainage.6–8 Use of the transhepatic percutaneous approach is inconvenient for patients, requiring them to maintain percutaneous drainage tubes for several months.9 Endoscopic retrograde cholangiography (ERC) is considered diagnostic for BS after LT, with therapeutic endoscopy and radiological techniques replacing surgery in the majority of cases as first line therapy, with high success rates.10–13 Until now there has been no standard endoscopic classification for BS after LT. The purpose of the present study was to develop a classification system for BS on the basis of endoscopic pictures after LT, and to use this system to establish an appropriate management strategy for patients. The proposed classification system is named the Ling classification because Ling is short for Linghu, the family name of the corresponding author.
Patients and methods This retrospective study analysed the endoscopic examinations of patients with jaundice who had undergone cadaveric or living donor liver transplantation at the Department of Gastroenterology, People’s Liberation Army General Hospital, Beijing, China between May 2006 and September 2011. Two endoscopists (E-Q.L. and Z.Q.) independently recorded the characteristics of intrahepatic biliary and anastomotic
stricture, and classified patients into four groups according to their findings: type A, normal biliary structure; type B, anastomotic stricture and normal intrahepatic biliary structure; type C, narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast without anastomotic stricture; type D, narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast with anastomotic stricture.
Results In total, there were 93 patients (76 men and 17 women) for whom clear pictures of ERC were available: 15 (16.1%) had undergone living donor liver transplantation; 78 (83.9%) had received cadaver organs. The median age of patients was 54 years (range, 12–69 years). The proportion of each Ling subtype in the included cases is shown in Table 1; typical images obtained for each subtype are shown in Figures 1–5. Of the nine patients classified as Ling A, two had repeated episodes of jaundice with normal ERC results. Their symptoms were alleviated with endoscopic nosalbiliary drainage. The remaining seven patients were treated medically with ursodeoxycholic acid capsules 250 mg, orally, twice daily for 1 month. The 44 patients classified as Ling B were treated with balloon dilatation, stent drainage, external drainage of the bile duct or transhepatic percutaneous drainage. In 40 patients classified as Ling B, endoscopic treatment was successful. One patient from this group developed a severe infection postoperatively and died of multiple organ failure; a further three patients with repeated severe jaundice were treated either surgically to repair the stricture or with biliary–enteric anastomosis, and these measures relieved the symptoms. There were 22 patients classified as Ling C, all of whom were treated
Downloaded from imr.sagepub.com by guest on November 14, 2015
568
Journal of International Medical Research 42(2)
Table 1. New endoscopic classification system (Ling Classification) for biliary stricture after liver transplantation, as seen in a series of 93 patients. Type
Anastomosis
State of intrahepatic biliary system
Patients, n
Proportion, %
A B C
Normal Stricture Normal
9 44 22
9.7 47.3 23.7
D
Stricture
Normal Normal Narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast Narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast
18
19.3
Figure 1. Endoscopic image of a Ling classification Type A (normal biliary structure) following liver transplantation. Outside diameter of the endoscope is 12 mm.
Figure 2. Endoscopic image of Ling classification Type B (anastomotic stricture, shown by the arrow, and normal intrahepatic biliary structure) following liver transplantation. Outside diameter of the endoscope is 12 mm.
with endoscopic retrograde biliary drainage (ERBD) and cleaning with ‘bolt-shaped’ material. Eighteen patients were treated successfully, two patients died of multiple organ failure and two patients required a second liver transplant, after which their symptoms were alleviated. Of the 18 patients classified as Ling D, all were treated
with ERBD and cleaning with ‘boltshaped’ material. This procedure successfully mitigated symptoms in 13 patients; one patient had lung metastases and died of respiratory failure, two patients were treated with biliary–enteric anastomosis and two patients required a second liver transplant.
Downloaded from imr.sagepub.com by guest on November 14, 2015
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Figure 3. Endoscopic image of Ling classification Type C (narrow and stiff intrahepatic biliary structure or beaded intrahepatic biliary structure or intrahepatic biliary cast without anastomotic stricture, shown by arrow) following liver transplantation. Outside diameter of the endoscope is 12 mm.
Figure 4. Endoscopic image of Ling classification Type D (narrow and stiff intrahepatic biliary structure, shown by the top arrow, or beaded intrahepatic biliary structure or intrahepatic biliary cast with anastomotic stricture, shown by the bottom arrow) following liver transplantation. Outside diameter of the endoscope is 12 mm.
Discussion Biliary complications are a frequent cause of morbidity and mortality after LT, occurring in between 5.8 and 39.5% of reported cases.6–8,14–18 The most frequent biliary complications are BS, which affect 16.2– 35.6% of patients,1–5 and are classified as anastomotic or nonanastomotic.8,19 Strictures restricted to the anastomotic site are likely to be related to problems encountered during surgery and the type of biliary reconstruction; they are isolated and short, with a reported incidence of 4–9%.20 Nonanastomotic strictures generally occur in groups, are longer than anastomotic strictures, are located in either the intrahepatic and/or donor duct proximal to the anastomotic site and have an incidence of 5–15%.21 Nonanastomotic strictures result primarily from hepatic artery thrombosis.22
Figure 5. Endoscopic image of a Ling classification Type D intrahepatic biliary cast. Outside diameter of the endoscope is 12 mm. The colour version of this figure is available online at http://imr.sagepub.com.
Downloaded from imr.sagepub.com by guest on November 14, 2015
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Journal of International Medical Research 42(2)
Identified causes include chronic ductopenic rejection, ABO incompatibility, ischaemia/ reperfusion injury or recurrence of primary diseases such as primary sclerosing cholangitis or autoimmune hepatitis.22 Biliary strictures can be treated by one or more interventions, including endoscopic transpapillary cholangiography, transhepatic percutaneous cholangiography or transhepatic percutaneous drainage, and/or surgical approaches.23,24 Endoscopic retrograde cholangiography is generally the firstline therapy for BS after LT and has a success rate of between 36.9 and 68%.10–13 However, treatment varies, depending on the features of the BS, hence the need for a standard and clear classification system, for which the Ling classification is proposed. In our study, type B was the most commonly observed BS after LT, accounting for 44 cases (47.3%), and type A was the least commonly observed, accounting for just nine cases (9.7%) of cases. In our experience, patients with type A BS will have symptomatic remission treated with drainage and medical therapy: their jaundice may be caused by a graft rejection reaction. Conversely, patients with type A BS were almost all treated by endoscopic transpapillary cholangiography or transhepatic percutaneous cholangiography, including balloon dilatation and stent drainage. No patients in the present study displayed a type B stricture and retained normal liver function. For patients with type C or D BS, endoscopy treatment was initially most useful,l but surgical repair and retransplantation were necessary for those who needed further endoscopic treatments or who failed endoscopic treatment. Although type C and D BS underwent the same treatment strategies, they were separated into two classifications because of anatomical differences in their appearance. The authors acknowledge there were a number of limitations to the present study, such as the small sample size and the lack of
long-term follow-up. Thus, further prospective studies are needed, to determine the validity of the proposed Ling classification system for selecting candidates for appropriate treatment. In conclusion, we hope that the Ling classification might help in determining the appropriate treatment strategy for patients with BS after LT. Further prospective studies are needed to determine the usefulness of the Ling classification system.
Declaration of conflicting interest The authors had no conflicts of interest to declare in relation to this article.
Funding This research received no specific grant from any funding agency in the public, commercial or notfor-profit sectors.
References 1. Hisatsune H, Yazumi S, Egawa H, et al. Endoscopic management of biliary strictures after duct-to-duct biliary reconstruction in right-lobe living-donor liver transplantation. Transplantation 2003; 76: 810–815. 2. Kasahara M, Egawa H, Takada Y, et al. Biliary reconstruction in right lobe livingdonor liver transplantation: Comparison of different techniques in 321 recipients. Ann Surg 2006; 243: 559–566. 3. Yamamoto S, Sato Y, Oya H, et al. Risk factors and prevention of biliary anastomotic complications in adult living donor liver transplantation. World J Gastroenterol 2007; 13: 4236–4241. 4. Ohkubo M, Nagino M, Kamiya J, et al. Surgical anatomy of the bile ducts at the hepatic hilum as applied to living donor liver transplantation. Ann Surg 2004; 239: 82–86. 5. Shah SA, Grant DR, McGilvray ID, et al. Biliary strictures in 130 consecutive right lobe living donor liver transplant recipients: results of a Western center. Am J Transplant 2007; 7: 161–167.
Downloaded from imr.sagepub.com by guest on November 14, 2015
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6. Park JS, Kim MH, Lee SK, et al. Efficacy of endoscopic and percutaneous treatments for biliary complications after cadaveric and living donor liver transplantation. Gastrointest Endosc 2003; 57: 78–85. 7. Rerknimitr R, Sherman S, Fogel EL, et al. Biliary tract complications after orthotopic liver transplantation with choledochocholedochostomy anastomosis: endoscopic findings and results of therapy. Gastrointest Endosc 2002; 55: 224–231. 8. Tabibian JH, Asham EH, Goldstein L, et al. Endoscopic treatment with multiple stents for post-liver-transplantation nonanastomotic biliary strictures. Gastrointest Endosc 2009; 69: 1236–1243. 9. Ko GY, Sung KB, Yoon HK, et al. Percutaneous transhepatic treatment of hepaticojejunal anastomotic biliary strictures after living donor liver transplantation. Liver Transpl 2008; 14: 1323–1332. 10. Seo JK, Ryu JK, Lee SH, et al. Endoscopic treatment for biliary stricture after adult living donor liver transplantation. Liver Transpl 2009; 15: 369–380. 11. Kato H, Kawamoto H, Tsutsumi K, et al. Long-term outcomes of endoscopic management for biliary strictures after living donor liver transplantation with duct-toduct reconstruction. Transpl Int 2009; 22: 914–921. 12. Yazumi S, Yoshimoto T, Hisatsune H, et al. Endoscopic treatment of biliary complications after right-lobe living-donor liver transplantation with duct-to-duct biliary anastomosis. J Hepatobiliary Pancreat Surg 2006; 13: 502–510. 13. Kim TH, Lee SK, Han JH, et al. The role of endoscopic retrograde cholangiography for biliary stricture after adult living donor liver transplantation: technical aspect and outcome. Scand J Gastroenterol 2011; 46: 188–196. 14. Salahi H, Razmkon A, Mehdizadeh AR, et al. Biliary tract complications after liver transplantation in a single center. Transplant Proc 2005; 37: 3177–3178. 15. Mata A, Bordas JM, Llach J, et al. ERCP in orthotopic liver transplanted patients.
16.
17.
18.
19.
20.
21.
22.
23.
24.
Hepatogastroenterology 2004; 51: 1801–1804. Amador A, Charco R, Martı´ J, et al. One thousand liver transplants: the hospital clinic experience. Transplant Proc 2005; 37: 3916–3918. Abdullah K, Abdeldayem H, Hali WO, et al. Incidence and management of biliary complications after orthotopic liver transplantation: ten years’ experience at King Fahad National Guard Hospital. Transplant Proc 2005; 37: 3179–3181. Alsharabi A, Zieniewicz K, Patkowski W, et al. Assessment of early biliary complications after orthotopic liver transplantation and their relationship to the technique of biliary reconstruction. Transplant Proc 2006; 38: 244–246. Sossenheimer M, Slivka A and Carr-Locke D. Management of extrahepatic biliary disease after orthotopic liver transplantation: review of the literature and results of a multicenter survey. Endoscopy 1996; 28: 565–571. Thuluvath PJ, Atassi T and Lee J. An endoscopic approach to biliary complications following orthotopic liver transplantation. Liver Int 2003; 23: 156–162. Alazmi WM, Fogel EL, Watkins JL, et al. Recurrence rate of anastomotic biliary strictures in patients who have had previous successful endoscopic therapy for anastomotic narrowing after orthotopic liver transplantation. Endoscopy 2006; 38: 571–574. Lee HW, Suh KS, Shin WY, et al. Classification and prognosis of intrahepatic biliary stricture after liver transplantation. Liver Transpl 2007; 13: 1736–1742. Schwartz DA, Petersen BT, Poterucha JJ, et al. Endoscopic therapy of anastomotic bile duct strictures occurring after liver transplantation. Gastrointest Endosc 2000; 51: 169–174. Mahajani RV, Cotler SJ and Uzer MF. Efficacy of endoscopic management of anastomotic biliary strictures after hepatic transplantation. Endoscopy 2000; 32: 943–949.
Downloaded from imr.sagepub.com by guest on November 14, 2015
