Technical aspects of biliary reconstruction in adult living donor liver transplantation

Hangzhou, China

Technical aspects of biliary reconstruction in adult living donor liver transplantation

Xiao-Ning Feng, Chao-Feng Ding, Mei-Yuan Xing, Min-Xia Cai and Shu-Sen Zheng

Hangzhou, China

BACKGROUND: The last decade has witnessed great progress in living donor liver transplantation worldwide. However, biliary complications are more common in partial liver transplantation than in whole liver transplantation. This is due to an impaired blood supply of the hilar bile duct during organ procurement and recipient surgery, commonly encountered anatomical variations, a relatively small graft duct, and complicated surgical techniques used in biliary reconstruction.

DATA SOURCES: MEDLINE and PubMed were searched for articles on "living donor liver transplantation", "biliary complication", "anatomical variation", "biliary reconstruction", "stenting" and related topics.

RESULT: In this review, biliary complications were analyzed with respect to anatomical variation, surgical techniques in biliary reconstruction, and protection of the arterial plexus of the hilar bile duct.

CONCLUSION: Transecting the donor bile duct at the right place to secure a larger bile duct stump, anastomosing techniques, and stenting methods as well as preserving the blood supply to the bile duct are all important in reducing biliary complications.

(Hepatobiliary Pancreat Dis Int 2011; 10: 136-142)

living donor; liver transplantation; biliary complications; biliary reconstruction; biliary drainage; biliary anatomy

Introduction

With various refinements in organ procurement, surgical techniques, postoperative management, and immunosuppression, the outcome of liver transplantation has been greatly improved. However, biliary complications (BCs) remain a major cause of mortality and morbidity after living donor liver transplantation (LDLT), with a reported incidence of 10%-60%.[1-3]In the last decade, the technical aspects of biliary reconstruction have been discussed and debated for their impact on BCs in LDLT. On one hand, common biliary variations have been recognized by radiological studies, and hence several types of biliary reconstruction have been developed. On the other hand, techniques have been described to avoid devascularizing the bile duct and therefore to reduce the chance of non-anastomotic stricture.[4-7]Moreover, the technical considerations on whether duct-to-duct choledochocholedochostomy (D-D) is better than Roux-en-Y hepatico-jejunostomy (RYHJ) or whether T-tube drainage should be abandoned or not have always been topics of debate.[8]This review aims to provide updated information on these topics.

Hilar anatomy as applied to biliary reconstruction

By receiving a partial graft with less volume in LDLT, the recipient has to face increased surgical complications associated with complicated hilar anatomical variation that requires multiple biliary reconstructions, as compared to a whole liver transplant. It is essential to perform a detailed preoperative evaluation of the graft biliary system followed by an intraoperative cholangiogram through the cystic duct.

Fig. 1. Huang's classification of the hilar biliary anatomy according to Kapoor.[10]Type A1: normal right and left hepatic duct junction; type A2: common junction of the RAHD, RHPD and LHD; type A3: aberrant drainage of the RPHD to the left main duct; type A4: aberrant drainage of the RPHD to the main hepatic duct; type A5: aberrant drainage of the RPHD to the cystic duct or its periphery.

Fig. 2. Several choices for biliary reconstruction in right-lobe LDLT. A: right liver graft with a single duct opening. B: right liver graft with two adjacent duct openings for which ductoplasty could be performed. C: right liver graft with two distant duct openings; a: single D-D anastomosis; b: single RYHJ; c: double D-D anastomosis with cystic duct and common bile duct; d: double D-D anastomosis with two recipient hepatic ducts; e: combination of D-D anastomosis and RYHJ; f: double RYHJ.

At present, Huang's classification[9]is frequently used in the evaluation of donor bile duct anatomy (Fig. 1). According to this classification from ERCP findings among the Chinese population, the confluence patterns of the biliary system are defined as type A1 (the normal right and left hepatic duct junction), type A2 (common junction of the right anterior hepatic duct (RAHD), right posterior hepatic duct (RPHD) and left hepatic duct (LHD)), type A3 (aberrant drainage of the RPHD to the left main duct), type A4 (aberrant drainage of the RPHD to the main hepatic duct) and type A5 (aberrant drainage of RPHD to the cystic duct or its periphery) based on the correlation of the RPHD with either the RAHD or LHD.[9]Several new classifications have subsequently described a more detailed bile duct anatomy. These classifications were based on either the correlation of the RAHD and portal vein or the correlation of hepatic segmental ducts and the cystic duct, or the presence of any accessory duct, and supplemented several rare anatomical variations to Huang's classification.[11-14]

Type A1 is present in 63% of potential donors among the Chinese population, and is also predominant among other geographical and racial populations such as Japanese, North Americans, Anatolian Caucasians, North Indians, and Koreans, but not Germans.[15]This type is anatomically simplest to deal with in hepatobiliary surgery and is ideal for harvesting a partial liver graft in LDLT. Either type A2 or type A3 is the most common anatomical variation in most races, followed by type A4 which is present in 1%-11% of normal livers. Type A5, as defined by cystic duct drainage of the RPHD, is uncommon with an incidence of 2%-5% in reported series.[9-20]

The ramification pattern of the hilar bile duct may affect hepatic biliary flow and is associated with the incidence of biliary static diseases such as hepatolithiasis and pyogenic cholangitis.[21]The high incidence of hepatolithiasis in the left liver may well support this theory.[22]Likewise, the acute angle between the RPHD and LHD in type A3 anatomy is also responsible for a higher incidence of hepatolithiasis.[11]In this sense, a detailed preoperative evaluation of hilar anatomy is crucial in LDLT, not only to avoid ligation or resection of accessory graft ducts, but also to reconstruct the graft duct with the recipient's common hepatic duct in a more appropriate way. For grafts with normal anatomy (type A1) (Fig. 2A), a single anastomosis is made between the graft duct and the recipient hepatic duct or jejunal loop (Fig. 2 a, b). In donors with biliary variations of trifurcation, the LHD and RPHD draining to the left hepatic duct or common hepatic duct, grafts are always harvested with double ducts. When the two openings are adjacent, the reconstruction can be achieved with a unification ductoplasty (Fig. 2B). This technique was reported to favor outcome when grafts with multiple openings are encountered.[23]However, when the two openings are distant, double D-D anastomosis or double RYHJ anastomosis is a preferable choice (Fig. 2C, d, f).[12, 20, 25]

Sometimes, the recipient cystic duct is used as one of the double D-D anastomoses (Fig 2C, c).[25-28]As the bile flow can pass through the cystic duct in both directions, reconstruction with a cystic duct does not cause functional obstruction.[27,29]The diameter of the cystic duct usually matches the graft duct well, and its length and blood supply are sufficient for anastomosis to be performed under most conditions. Cystic duct anastomosis is therefore becoming a feasible and safe option in right lobe LDLT.[30-32]Rarely, a combination of D-D and RYHJ depends on the situation (Fig. 2C, e).

Anatomical variations of biliary structures in rightlobe grafts are common. However, with a preoperative imaging study with either conventional MRCP, or enhanced excretory MRCP, or CT cholangiography and a detailed intraoperative cholangiography, most of these variations can be managed safely with technical modifications.

Table. Clinical outcomes of LDLT using different anastomotic techniques

Arterial supply to the bile duct

Another point that requires attention in LDLT is the arterial supply to the bile duct. The peribiliary vascular plexus is nourished by three arterial branches. One branch arising from the posterior superior pancreaticoduodenal artery nourishes the middle segment of the bile duct. One branch from the right hepatic artery nourishes the parallel common bile duct. Another branch from either the right or left hepatic artery supplies the hilar bile duct via the hilar plexus dorsally.[33-36]

While injury to this vascular plexus may cause severe bile duct ischemia and result in post-transplant BCs, surgeons are requested to avoid devascularizing the hilar bile duct when harvesting a partial liver graft.[4,37,38]

A variety of techniques have been described to avoid injury to the duct blood supply in LDLT. For example, Lo et al[5]suggested that the right hepatic artery should be divided to the right of the common bile duct in recipient surgery to preserve the dorsal arterial supply of the pericholedochal vascular plexus. Some centers have applied an intrahepatic Glissonian approach in recipient hepatectomy which is characterized by high hilar dissection to obtain a longer and better-nourished bile duct for anastomosis.[6]And recently, Soejima et al[7]described a technique ofen blocdissection of the bile duct and hepatic artery without dissecting the connective tissue between them. These methods could be of choice in recipient hepatectomy when necessary to achieve a bile duct with sufficient arterial supply and long enough for anastomosis.

Techniques of biliary reconstruction

The optimal technique for biliary anastomosis in LDLT is still controversial. Either D-D or RYHJ is the most common method of choice. In the early years, RYHJ was the standard biliary reconstructive technique of partial liver transplantation because of a more reliable blood perfusion, and the results in pediatric cases or recipients with primary sclerosing cholangitis were quite satisfactory.[23]

With growing experience of post-transplant management, certain disadvantages of RYHJ, such as potential contamination from the opened loop of jejunum, delayed return of gastrointestinal function, longer operation time, and extended stay in the ICU have been found. Moreover, the reestablished bilioenteric connection in RYHJ is not physiological, and it hinders the postoperative management of BCs by ERCP.[30,40]

Since the late 1990s, D-D anastomosis has been increasingly reported in LDLT and split liver transplants. Although the incidence of anastomotic stricture was higher in the initial series, more and more centers have recently reported the safety and feasibility of D-D anastomosis in LDLT in large case series, as a result of technical improvements.[37,41,42]Advantages over RYHJ include preservation of function of the sphincter of Oddi to maintain defense against enteric reflux and ascending infection, abrogation of the need for intestinal manipulation and therefore reducing the risk of intra-abdominal contamination, and early recovery of oral intake after transplantation. In case of major BCs, anastomosis can be converted to RYHJ.[40]

According to the Kyoto group's experience, the incidence of anastomotic leakage was significantly lower in the D-D group (4.7% in D-D, 12% in RYHJ), while that of anastomotic stricture was higher (26.6% in D-D, 8.3% in RYHJ).[43]However, the Seoul group reporteda much higher BC incidence for D-D anastomosis with regard to both anastomotic leakage and stricture.[44]In Shah's research from the Toronto group, strictures developed more frequently after RYHJ (14/64; 22%) than D-D (8/64; 12%), but the difference did not reach statistical significance (P=0.16).[23]Conversely, another case series from Osaka reported no statistically significant difference between RYHJ and D-D as to the incidence of bile leak and stricture.[8]While in Kobayashi et al's left lobe graft series, D-D over a T-tube achieved a much lower incidence of bile leakage.[45]

The results of these studies seemed quite controversial. However, LDLT consists of complicated surgical procedures with many confounding factors which could hardly be balanced in those retrospective studies. It is also impossible to randomize the anastomosis technique even in well-designed prospective studies. Comparison between D-D and RYHJ anastomosis is suggested to take into account factors like primary liver disease, hilar anatomy, duct size, previous history of surgery, design of anastomosis, and learning curve.

Preferentially, D-D was performed on single and snout graft ducts, while RYHJ was electively performed on recipients with congenital bile duct diseases, prior biliary surgery, re-transplantation, significant duct size discrepancy, and the presence of multiple or small bile ducts which need complicated anastomosis.[46]It is suggested that surgeons should be accustomed to both procedures and follow the principle of tension-free and viable anastomosis.[4]Moreover, a routine microsurgical reconstruction would reduce the incidence of anastomotic complications and optimize the long-term outcomes, expecially in those grafts with small ducts.[47]

Biliary drainage

Stenting of the anastomosis is another controversy in LDLT. In early cases, a stent at the anastomotic site was used to prevent accidental catching of the posterior wall and post-transplant anastomotic stricture in grafts with small ducts.[31,46,48]The rationale of the T-tube includes the maintenance of biliary flow, easy access to the biliary tree, monitoring the quality of output bile, allowing the cholangiographic assessment of biliary anatomy, and protecting the anastomosis from leakage by lowering the biliary pressure. A number of transplant centers still prefer to use T-tubes, based on their own experiences. For example, Weiss et al[49]reported a significantly increased complication rate in the group without T-tube insertion, and advocated the safety of T-tube usage in biliary anastomoses.

However, in the recent decade, biliary drainage by a T-tube has been reported to cause increased BCs. These complications include narrowing of the bile duct lumen by the stent or the stay sutures, spontaneous dislodgment of the stent from the biliary system, and accidental early removal of the stent. And because fibrogenesis was impaired under immunosuppression, bile leaks developed frequently following T-tube removal.[50-56]

As a result, T-tube stenting has largely been abandoned in deceased donor liver transplantation. A recent systematic review showed that most of the retrospective studies from larger transplant centers have tended to avoid routine use of T-tubes in OLT since 1996.[57]However, the size of the graft duct is a significant difference between partial grafting and fullsize liver transplantation. The average diameter of a partial graft duct is about 4 mm, whereas the common hepatic or bile duct is usually twice that diameter. Due to the size discrepancy between graft and recipient, the LDLT recipient is more liable to develop post-transplant BCs. Therefore, it is sensible to place a T-tube in the duct-to-duct procedure in LDLT.

Kim et al[58]reported that the incidence of BCs in those with an external stent was 0% compared to 30.8% in those without a stent, and complications related to stent removal were not observed in his series. The Kyoto group reported a 17.6% BC incidence using a biliary stent for right lobe LDLT.[59]Another Japanese center achieved a 21% BC incidence in their group of D-D anastomosis with a T-tube in left lobe LDLT.[45]In Hong Kong, T-tube was not used in D-D reconstruction for right lobe LDLT, and the overall incidence of BC was 24%, which was slightly higher than that in the Kyoto Group, but it was also satisfactory.

Techniques of suturing

The type of suturing methods as well as materials are significantly associated with the incidence of BCs. Kim et al[58]reported a higher incidence of biliary stricture (43.1%) using 6-0 prolene with either interrupted suture or posterior continuous and anterior interrupted suture. When using continuous suture with 7-0 prolene, the incidence of biliary stricture significantly decreased to 4.7%, but the incidence of bile leakage rose to 23.1%. The reason for bile leakage was concluded to be partial tearing of the sutured graft duct, and could be successfully prevented with a 4- or 5-Fr external biliary stent. Yan et al[60]described their microsurgical techniques in biliary reconstruction with 6-0 prolene for D-D anastomosis and 8-0 prolene for RY anastomosis. The result was satisfactory with only 2 episodes of BC.Recently, Kim and coworkers[61]have reported their tailored telescopic reconstruction using the inner layer of the bile duct epithelium in D-D anastomosis. The biliary complication rate was significantly decreased compared to the conventional method with the whole layer (9.1% vs. 43.5%).

These precise manipulations, like using a smaller needle, a microscope, or doing D-D anastomosis in a more delicate way, favor the outcomes of biliary reconstruction, especially in grafts with small ducts and multiple openings. However, these issues should be subjected to prospective studies.

Conclusion

The development of BCs after LDLT is correlated with biliary anatomy, and has been significantly influenced by such technical aspects as the design of reconstruction and type of anastomosis. A detailed anatomical appraisal and a reasonable reconstruction design accordingly is always helpful, while the idea to maximally preserve the biliary arterial supply should always be kept in mind. The type of anastomosis as well as the use of T-tube drainage should be decided flexibly according to the etiology and bile duct condition of both graft and recipient. Future studies are expected to be prospectively designed, with expanded samples and extended views on the choice of suture material, the comparison between continuous and interrupted suture, as well as the topics discussed in this paper.

Funding: This study was supported by grants from the National Key Technology R&D Program in the Eleventh Five-Year Plan of China (2008BAI60B01 and 2008BAI60B02).

Ethical approval: Not needed.

Contributors: FXN wrote the main body of the article under the supervision of ZSS. DCF, XMY and CMX provided advice on medical aspects. All authors contributed to the design and interpretation of the study and to further drafts. ZSS is the guarantor.

Competing interest: No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

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Received October 10, 2010

Accepted after revision February 22, 2011

Author Affiliations: Division of Hepatobiliary and Pancreatic Surgery, First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou 310003, China (Feng XN, Ding CF, Xing MY, Cai MX and Zheng SS)

Shu-Sen Zheng, MD, PhD, FACS, Division of Hepatobiliary and Pancreatic Surgery, First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou 310003, China (Tel: 86-571-87236601; Fax: 86-571-87236601; Email: shusenzheng@zju.edu.cn)

? 2011, Hepatobiliary Pancreat Dis Int. All rights reserved.