Abstract: Biliary tract complications are often referred to as the "Achilles' heel" of liver transplantation and various tech- niques have been developed to ...
Surgery Today Jpn. J. Surg. (1992) 22:493-500
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SURGERYTODAY
© Springer-Verlag 1992
Review Article
Biliary Tract Reconstruction in Liver Transplantation KATSUHIKOYANAGAand KEIzo SUGIMACHI The Second Department of Surgery, Facultyof Medicine, KyushuUniversity, Higashi-ku, Fukuoka, 812 Japan
Abstract: Biliary tract complications are often referred to as the "Achilles' heel" of liver transplantation and various techniques have been developed to overcome them. The two major methods of bile duct reconstruction currently in use consist of either (1) choledochocholedochostomy over a T-tube or, when duct-to-duct approximation is not feasible, choledochojejunostomy over an internal stent, or (2) interposition of the donor gallbladder as a conduit between the donor bile duct and either the recipient bile duct or a jejunal loop. Although these standardizations of biliary tract reconstruction have resulted in a reduction of biliary complications after liver transplantation, further advancement in the elucidation of ampullary obstruction and viability of the donor bile duct is needed. Key Words: liver transplantation, biliary tract reconstruction, complication
Introduction
During the developmental phase of liver transplantation (LT), biliary tract complications were extremely common.t'2 In fact, the complications of biliary tract reconstruction (BTR) in LT were often fatal until the mid-1970s, mainly due to an ill-advised increase in immunosuppression on the assumption of graft rejection or, conversely, an acute rejection triggered by a reduction in immunosuppression for intraperitoneal sepsis caused by a bile leak. 1"3-5 Thus, BTR has repeatedly been described as the "Achilles' heel" of LT. 2"6'7 However, the techniques of BTR have now been standardized2-4 and improved early and late resuits are being reported. 3's'9 In this article, we describe the evolution and current concepts of surgical technique as well as the results of BTR in LT. Reprint requests to: K. Yanaga (Received for publication on July 31, 1991; accepted on July 6, 1992)
Animal E x p e r i m e n t s and the Inaugural Period
In the first report of an experimental LT model in 1955,1° BTR of a canine heterotopic allograft was achieved by cholecystoduodenostomy. For orthotopic transplantation, two independent reports in 1960 described canine LT in which cholecystoduodenostomy11 or loop cholecystojejunostomywith side-to-side jejunojejunostomy12 was employed. In humans, the first LT was performed orthotopically on March 1, 1963 in Denver, on a 3 year old boy with congenital biliary atresia. 13 The moribund state of the patient at the time of BTR permitted only a simple drainage procedure with loop cholecystojejunostomy and ligation of the common bile duct. For the next six patients in the Denver series, choledochocholedochostomy over a T-tube was performed in five, one of whom died of bile peritonitis due to a bile leak from the anastomosis. 13-16 In Boston, four LTs were performed, one in September, 1963, and the other three in 1968. Two of these transplants were orthotopic employing choledochocholedochostomy over a T-tube or cholecystoduodenostomy, while the other two were heterotopic transplants using cholecystostomy.17,18In January, 1964, another orthotopic LT was performed in Paris 19 with choledochocholedochostomy over a T-tube. Iv_ Cambridge, five LTs, the first being heterotopic and the other four orthotopic, were reported in 1967 and 1968, respectively, e° In these transplants, BTR was performed by Roux-en-Y Cholecystojejunostomy in three patients and end-to-end cholecystocholedochostomy and choledochocholedochostomy over a T-tube in one patient each, respectively. In this report, a postoperative hemorrhage from a cholecystojejunostorey was documented. During this inaugural period, the significance of biliary tract complications was concealed by intraoperative death or short survival after transplant, which was mostly attributable to ischemic allografts, changes in
494
K. Yanaga and K, Sugimachi: Biliary Complications in Liver Transplantation
Table 1. Early results of biliary tract reconstruction in orthotopic liver transplantation according to Williams et al. 5 in 1973
and Starzl et al. 6 in 1974 Method of biliary tract reconstruction Cholecystoduodenostomy Cholecystojejunostomy (Roux-en-Y) Cholecysto-loop jejunostomy Cholecystocholedochostomy Choledochocholedochostomy Choledochoduodenostomy Total
Total 0 0 5 6 6 0 17 b
Cambridge series5 (1973) Obstruction Leak ---2a (33%) 1a (17%) -3 (18%)
---
4 (80%) 2a (33%) 3a (50%)
Total 59 8
2 0 9
--
4
9 (53%)
82
Denver series6 (1974) Obstruction Leak 15 (25%) 2 (25%)
0
2 (3%) 0
0 --
-5 (56%)
17 (21%)
8(10%)
0 0
1 (25%)
a One patient had a bile leak associated with obstruction due to biliary sludge bNine patients with early mortality were excluded
intra- and immediate postoperative coagulation profiles, and postoperative immunosuppression therapy. 21
The Developmental
Period
In Denver, prolonged survival was achieved in a patient in 1967, 22 by performing B T R with a cholecystoduodenostomy. The improved outcome was attributed to more discriminating donor selection and improvement in the liver preservation and immunosuppression regimen. 22
Recognition of Biliary Tract Complications Until the mid-1970s, technical complications related to B T R were frequent and often l e t h a l ) Table 1 lists the biliary tract complications reported from Cambridge/ L o n d o n in 19735 and from Denver in 1974. 6 The Cambridge/London group in an analysis of their first 26 orthotopic LTs documented that complications related to B T R were directly responsible for death in 10 out of 17 patients (58.8%) who survived the immediate postoperative period, and were described as the most serious complications of LT. 5 They speculated that biliary complications may be attributable to pre-existing biliary tract infection, rejection, tenuous blood supply of the bile duct and changes in biliary secretion. In the report from Denver 6 on the initial 82 orthotopic liver transplants, biliary obstructions were documented in 17 patients (20.7%) while bile leak was described after eight transplants (9.8%). Of the 25 patients with posttransplant biliary complications, biliary reoperations were attempted in 13, 9 of which (69.2%) failed. Of the various methods of B T R performed, choledochocholedochostomy and choledochoduodenostomy were associated with a high risk of bile leak, while cholecystoduodenostomy had a tendency to cause biliary obstruction.
Refinements in Surgical Techniques With regard to the chronological changes in the techniques of B T R in Denver, choledochocholedochostomy had been replaced by cholecystoduodenostomy by 1967 because of the high incidence of bile leakage in the former.22 However, cholecystoduodenostomy, although simple to perform, was complicated by functional biliary obstruction at the narrowed donor cystic duct or by a bile leak in 30% of their initial 93 patients, which almost always proved fatal. 23 Furthermore, the conversion of cholecystoduodenostomy to choledochoduodenostomy was often followed by duodenal fistula and sepsis. 1'24 In 1973, cholecystojejunostomy using a jejunal Roux limb of at least 18 inches became the first choice of BTR, since this technique had a lower incidence of biliary complications and, in cases of bile leak, peritoneal contamination from the gastrointestinal contents could be minimized. Choledochocholedochostorey ovei' a T-tube or Roux-en-Y choledochojejunostomy was considered when the donor cystic duct joining the common hepatic duct was too low to allow the donor gallbladder to function as a conduit.l'6 In these cases, however, one-third of the cholecystoj ejunostomy later required conversion to choledochojejunostomy, due to obstruction at the donor cystic duct level. 24 Thus by 1979, end-to-end choledochocholedochostomy over a T-tube had become the first choice due to improved results related to the easy access to bile and the biliary tract for cholangiograms. 24 Cholecystojejunostomy had been abandoned in Pittsburgh by 1982, mainly due to the high incidence of biliary obstruction. 3 The first choice of bile duct reconstruction in Pittsburgh now is end-to-end choledochocholedochostomy over a T-tube which is brought through a choledochotomy in the suprapancreatic recipient duct. 9 This technique reduces the operative time, preserves the sphincter of Oddi, and allows easy access to bile and the biliary tree for postoperative investigations. 9 When
K. Yanaga and K. Sugimachi: Biliary Complications in Liver Transplantation choledochocholedochostomy is contraindicated or not feasible, choledochojejunostomy over an internal stent is performed. 9 The indications for choledochojejunostomy consist mainly of involvement of the extrahepatic bile duct such as in primary sclerosing cholangitis or malignancy, or in cases of major duct size discrepancy between the donor and recipient. The reason for the superiority of choledochocholedochostomy over choledochojejunostomy includes the capability to monitor bile through easy access to the biliary tree postoperatively and the absence of such serious technical complications related to Roux-en-Y jejunojejunostomy as hemorrhage and leakage of the intestinal contents. In Cambridge, a completely different technique of B T R evolved. Due to the dissatisfaction with the high incidence of biliary tract complications preferentially by choledochocholedochostomy over a T-tube, together with a recognition of the importance of sphincter mechanism for the prevention of cholangitis, they adopted a technique used in biliary surgery, 25 the interposition of the gallbladder between the donor and recipient common bile ducts. ~'26 This technique gives all the benefits of choledochocholedochostomy, while allowing wide anastomosis without tension. If the recipient common bile duct is not available, the donor gallbladder conduit is anastomosed to a Roux loop of the jejunum. Since 1976, the Cambridge group has been using this technique almost exclusively, except in cases of a good size match of the donor and recipient common duct with good alignment, when endto-end choledochocholedochostomy over a T-tube is performed, s'27 In the Denver/Pittsburgh series, ten gallbladder conduit BTRs have been performed to date (0.5%), among which four out of eight survivors of LT (50%) later required conversion to choledochojejunostorey for anastomotic stricture and the formation of biliary sludge or stones. 28 They recommend limiting the gallbladder conduit technique only to patients with extensive adhesions of the intestine or to those with a short gut due to construction of multiple Roux limbs or intestinal resection. Currently, most smaller programs seem to have adopted an approach similar to that of the Pittsburgh group. 29-4° Variations from this strategy include cholecystojejunostomy for children in Minnesota 38 and external cholecystostomy without a T-tube in London, Canada and in Chicago. 4°'4~ Some other programs adopt a slightly different approach. In Villejuif, France, hepaticojejunostomy is performed routinely, 42 while side-to-side choledochocholedochostomy over a T-tube is being performed in Hannover. 43-46 The side-to-side choledochocholedochostomy allows the creation of a wide anastomosis without tension, although bile leakage from the blind end of the bile duct has been described. 44
495
A group in Birmingham, England 4v uses the WaddellCalne technique. 2 Regarding the suture materials used, most institutions use absorbable sutures, such as braided polyglactin (Vicryl, Ethicon, Peterborough, Canada) or monofilament polyglyconate (Maxon, Davies & Geck, Gosport, UK),~,41,48 although the use of non-absorbable monofilament polypropylene (Prolene, Ethicon, Somerville, NJ, USA) has also been reported. ~2 In a randomized comparison of suture materials for B T R between braided polyglactin and monofilament polyglyconate, the latter was associated with better results. 48 That study advocated the use of a synthetic and monofilament suture material for B T R in LT because of reduced tissue reaction by synthetic materials as well as bacterial adherence. 48 With regard to the size of the bile duct, children do not seem to be at particularly risk of biliary tract complications. ~
Blood Supply of the Common Bile Duct In 1948, a peculiar feature of the arterial blood supply to the common bile duct was reported by Shapiro and Robillard, 49 being that the common bile duct is supplied in an axial fashion, primarily by the posterosuperior pancreaticoduodenal artery from below, and by the cystic artery or right hepatic artery from above, while the proper hepatic artery rarely contributes to its blood supply. In the same year, Douglass and Cutter described an abundant epicholedochal plexus in 42 of 50 postmortem specimens (84%). 5° Parke et al. 51 in 1963 detailed an analysis of the blood supply to the common bile duct, demonstrating the presence of two intraluminal plexuses, subadventitial and submucosal, with an origin of blood supply from perforating branches of the epicholedochal plexus. The poor results of B T R in biliary surgery 52 and LT necessitated a better comprehension of the blood supply to the common bile duct. With the use of a new polyester resin cast technique, Northover and Terblanche 53'~4 in 1978 and 1979 advocated the retroportal artery as an important source of blood supply to the posterior wall of the supraduodenal common bile duct, and reemphasized the significance of the axial blood supply of the human common bile duct. The relative proportions of the total arterial blood supply of the supraduodenal bile duct were 60% from below, 38% from above and only 2% from the proper hepatic artery. 53 For successful biliary anastomosis, they advocated the importance of the division of the donor bile duct at a high level where adequate perfusion is maintained. In the absence of any attachments in recipients of a transplant liver other than four vascular and one biliary
496
K. Yanaga and K. Sugimachi:Biliary Complicationsin Liver Transplantation
anastomoses, the blood supply to the donor common bile duct is derived solely from the hepatic artery after LT. ~ Thrombosis of the hepatic artery can therefore cause a delayed bile leak from the biliary anastomosis in the absence of technical failure due to necrosis of the donor bile duct. e5 For the recognition of hepatic artery thrombosis, Doppler ultrasonography is the first choice and, if an arterial Doppler pulse cannot be detected, emergency arteriography needs to be performed to confirm patency of the hepatic artery. If detected early, urgent exploration and reconstruction could result in successful revascularization and the avoidance of biliary anastomotic break down. 56
Healing of the Bile Duct Anastomosis In a porcine model, healing of the bile duct anastomosis was evaluated after simple transverse choledochotomy or end-to-end choledochocholedochostomyin auto- and allo-transplantation of the liver. ~7 Although the tensile strength of the biliary anastomosis after simple transverse choledochotomy returned to normal within 15 days, that after both types of transplantation never returned to normal, even by postoperative day 50. This study seems to demonstrate a significant adverse effect of organ preservation and transplantation on healing of : the bile duct, even when the preservation time is short, or in the absence of immunosuppression or rejection.
Bile Production and Bile Cast Syndrome Bile production immediately following revascularization is a good indicator of graft viability in experimental and human LT. 58-6° Postoperatively, the production of scant, pale, or watery bile is indicative of poor allograft function,6a while thinning of the bile in the early postoperative period may indicate acute rejection. 37 A recent bile study after LT demonstrated a correlation between acute cellular rejection and a rise in biliary ~2-microglobulin, a low molecular weight protein associated with HLA class I antigens, as well as an elevated bile/serum ratio of 1~2-microglobulin.62 In 1972, the Denver group first described a syndrome of bile cast formation in the biliary tract associated with delayed obstruction in 4 out of 40 patients (10%) following LT with cholecystoduodenostomy.63 All 4 died of fulminant cholangitis, and the autopsies on all 4 revealed a chalk-like, crumbly debris which formed casts in the dilated intrahepatic bile ducts. In !973, the London/Cambridge group also identified similar findings in patients after LT. 5 In the Denver series, biliary cast syndrome was always associated with mechanically defective BTR, whereas in Cambridge, mechanical obstruction was documented in only one out of four patients with bile cast formation. TM The cause
of this marked discrepancy between the two groups was elucidated later when the significance of bile duct damage from bile during cold preservation was clarified, s,65 A group from New York 66 in 1971 reported a patient who had undergone a cholecystoduodenostomy in whom an increase in bile salt synthesis and a reduction in the bilirubin to bile salt ratio suggestive of a disturbance in the excretory capacity of conjugated bilirubin was seen, as well as an interruption in the enterohepatic circulation of bilirubin due to the diversion of bile though a T-tube. The Cambridge group, in their reports of 1975 and 197864,67 revealed a supersaturation of bile with cholesterol immediately after transplantation, which was attributed primarily to reduced levels of bile acids following interruption of the enterohepatic circulation and the depletion of the bile acid pool. Clamping of the T-tube caused the prompt unsaturation of bile with cholesterol and increased the bile acid levels. They also noted that the cast was always confined to the donor bile duct. Chemical analysis and histological studies revealed that a major constituent of the bile sludge was necrotic collagen from the donor bile duct walls, while ischemic damage of the bile duct epithelium during cold preservation was regarded as a cause of early bile cast formation, which occurs in the absence of biliary obstruction, s'64'65'68 The absence of this early bile cast syndrome in the Denver series was attributed to their routine in situ flushing of the gallbladder and bile duct. 8'69 This deleterious effect of bile on the bile duct mucosa during cold preservation was later confirmed by animal studies in Cambridge,65'68 and the early bile cast syndrome has not been observed since the adoption of the techniques used in Pittsburgh. s
Postoperative Investigation of the Biliary Tract Prior to the recognition of biliary tract complications after LT, liver dysfunction was generally attributed to rejection, for which immunosuppression was increased unnecessarily.64'7° However, with the increasing awareness of biliary complications being a major cause of liver dysfunction, investigation of the biliary tree has been identified as an extremely important adjunct to the overall postoperative management of LT recipients. 7°,71 The placement of a T-tube at the time of choledochocholedochostomy or the Waddell-Calne technique in LT allows easy access to the biliary tree for postoperative cholangiography.2'9 A group in London, Canada leaves a cholecystostomy tube in place, while a team from Villejuif, France places a small-caliber catheter through the cystic duct remnant for the same purpose. 4°'42 In Pittsburgh, a T-tube cholangiogram is taken one week after the transplant, and if it is normal,
K. Yanaga and K. Sugimachi: Biliary Complications in Liver Transplantation the T-tube is usually clamped once the serum total bilirubin reaches below 2.5 mg/dl or when the absorption of oral cyclosporin is inadequate. When completely internal biliary drainage, mainly in the form of choledochojejunostomy, is performed, or after the T-tube has been removed, radiographic assessment of the bile duct is achieved by percutaneous transhepatic cholangiography (PTC) or endoscopic retrograde cholangiography. 71"72 In Pittsburgh, PTC is performed preferentially for the assessment of the biliary tree with minimal morbidity. 71
Treatment of Bile Leakage or Biliary Obstruction Bile leakage following LT is a serious complication which usually occurs within 2 weeks of LT, and is usually found at the anastomosis or T-tube insertion site (9). For anastomotic leaks from choledochocholedochostomy, the treatment consists of an emergency laparotomy and conversion to choledochojejunostomy using the Roux-en-Y technique. The simple addition of a suture across the anastomosis is rarely satisfactory. In the case of bile leakage from a choledochojejunostomy, revision of the anastomosis is performed. However, when contamination of the subhepatic space and edema of the jejunum are extensive or when the donor bile duct is necrotic, the bile is drained externally. 9 If the bile leak originates from the T-tube insertion site, a simple suture-ligature of the T-tube site usually controls the problem. 9 Biliary obstruction after choledochocholedochostomy is usually due to anastomotic stricture or ampullary obstruction. 48"73 For obstruction of the ampulla of Vater, ampullary dysfunction presumably due to denervation is suspected. 73 A mucocele of the donor cystic duct is a rare cause of obstruction. 74 Regardless of the etiology, obstruction is treated by conversion to a Roux-en-Y choledochojejunostomy. 9 Biliary obstruction after choledochojejunostomy, on the other hand, is usually due to anastomotic stricture or a retained stent across the anastomosis with luminal obstruction. 71 For anastomotic strictures, percutaneous transhepatic balloon dilatation is usually tried, whereas refractory or recurrent strictures are most often treated by revision of the choledochojejunostomy, and retained stents are almost always removed by the percutaneous transhepatic technique. 7°
Postoperative Removal of a Biliary Catheter T-tubes placed across the anastomosis of choledochocholedochostomy or Waddell-Calne's gallbladder conduit are removed approximately 3 months after the transplant, following confirmation of the absence of abnormal findings on cholangiography. 7"8 However, removal of a T-tube or biliary catheter 4° can
497
cause a biliary leak from the insertion site, which seems to be a demerit of partial external biliary drainage, 9"29-31'33'34"4°'47 although in Cambridge, no bile leak has occurred after the routine removal of a T-tube 3 months post-transplant, s
Recent Results
Table 2 lists the results of BTR in orthotopic LT at various centers. The incidence of biliary complications varies from 3% to 24%, consisting mainly of bile leaks ( 0 % - 1 4 % ) and obstruction ( 1 % - 6 % ) .
Comments
The ideal method of BTR in LT should provide simplicity, reliability, easy access for postoperative biliary investigation, and avoid cholangitis. It seems obvious that choledochojejunostomy does not qualify as the first choie of BTR, because of the added intestinal procedures, the absence of sphincteric protection, and the difficulty in managing a bile leak. Among the methods of BTR which preserve the sphincteric function and avoid intestinal procedures, end-to-end choledochocholedochostomy seems superior to the Waddell-Calne technique 2 and side-to-side choledochocholedochostomy, due to the absence of bile stagnation in the biliary tree which could cause the inspissation and infection of bile. In that regard, we recommend BTR in LT as employed by the Pittsburgh team, namely, end-to-end choledochocholedochostomy over a T-tube whenever feasible, or choledochojejunostomy otherwise. Reduced mortality and morbidity following BTR is undoubtedly one of the major factors contributing to the improved outcome of orthotopic LT. 3 However, despite earlier recognition and more appropriate management of biliary tract complications after LT, no marked reduction in the incidence of such complications has occurred. The dilemma with BTR in LT includes the inability to assess the blood supply to the donor bile duct, the unknown etiology of ampullary dysfunction after choledochocholedochostomy,73 the oversaturation of bile produced by the transplant liver, and the lack of a specific laboratory technique to discriminate liver dysfunction caused by biliary complications from others. Further research on BTR encompassing these aspects should therefore be conducted.
Acknowledgment. We would like to thank Drs. Thomas E. Starzl and Shunzaburo Iwatsuki of the University of Pittsburgh for comments on the manuscript.
498
K. Yanaga and K. Sugimachi: Biliary Complications in Liver Transplantation
Table 2. Recent results on the incidence of biliary complications following orthotopic liver transplantation No. of biliary complications Location
Year
Denver/ Pittsburgh 9
1980-1984
Boston 37
1983-1986
leak obst. J-J leak leak obst.
Omaha 35
1985-1989 leak obst. J-J leak
Los Angeles33
1984-1986 leak obst. J-J leak J-J bleed
Dallas 31
1984-1987 leak obst.
London, Canada 4°
1982-1987
Villejuif, France 42
1984-1986
Birmingham
1982-1986
leak obst. others leak obst. leak obst.
U K 47
Gronigen, Netherland 29
1979-1984 leak obst. necrosis GB
Overall
C-C over T-tube
C-J (Roux-en-Y)
Others
52/393 (13%) 27 (7%) 20 (5%) 6 (2%) 5/150 (3%) 4 (3%) 1 (1%) 50/264 (19%) 14 (5%) 23 (9%) 9 (3%) 24/100 (24%) 14 (14%) 6 (6%) 2 (2%) 1 (1%) 12/91 (13%) 8 (9%) 4 (4%) 11/92 (12%) 4 (4%) 5 (5%) 2 (2%) 3/58 (5%) 0 3 (5%) 6/46 (13%) 4 (9%) 2 (4%) 6/31 (19%) 4 (13%) 1 (3%) 1 (3%)
(n = 159; 40%) 15 (9%) 5 (3%)
(n = 175; 45%) 3 (2%) 4 (2%) 6 (3%) NA
(n = 59; 15%) a 9 (15%) 11 (19%)
NA
(n = 118; 45%) 7 (6%) 16 (14%)
NA
(n = 144; 55%) 7 (5%) 7 (5%) 9 (6%) (n = 33; 33%) 3 (9%) 2 (6%) 2 (6%) 1 (3%) NA
(n = 80; 87%) 4 (5%) 5 (6%)
(n = 10; 11%) 0 0
--
(n = 58; 100%) c 0 3 (5%) --
(n = 67; 67%) 11 (16%) 4 (6%)
(n = 1; 2%) 0 0 (n = 29; 94%) 4 (14%) 1 (3%)
(n : 1; 3%) 0 0
NA
NA
(n = 2; 2%) b 0 0 2 (100%) --
(n = 45; 98%) a 4 (9%) 2 (4%)
(n = 1; 3%) 1 (100%)
a Choledochocholedochostomy with internal stent in 32, Waddell-Calne in 6, cholecystoenterostomy in 7 and external drainage in 5 patients b Cholecystojejunostomy (Roux-en-Y) in both patients cHepaticojejunostomy in all patients d Waddell-Calne in 40 and gallbladder conduit with cholecystojejunostomy in 5 patients C-C, choledochocholedochostomy; C-J, choledochojejunostomy; J-J, jejunojejunostomy; NA, not available; GB, gallbladder
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