Postoperative Bile Duct Strictures

Biliary Tract Surgery

0039-6109/90 $0.00

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Postoperative Bile Duct Strictures

Keith D. Lillemoe, MD, * Henry A. Pitt, MD, t and John L. Cameron, MDt

Benign bile duct strictures represent one of the most difficult challenges that a biliary surgeon may face. Despite numerous technological developments that have facilitated diagnosis and management, bile duct strictures remain a significant clinical problem. If they are unrecognized or are managed improperly, life-threatening complications such as biliary cirrhosis, portal hypertension, and cholangitis may develop. Benign bile duct strictures can have numerous causes. However, most follow primary operations on the gallbladder or biliary tree. Operative injury to the bile ducts also can occur during nonbiliary operations or as a result of external penetrating or blunt abdominal trauma. Inflammatory conditions and fibrosis secondary to chronic pancreatitis, gallstones within the gallbladder or the bile ducts, stenosis of the sphincter of Oddi, biliary tract infections, or duodenal ulcers can all cause benign bile duct strictures. This article will focus only on postoperative biliary strictures and their management.

PATHOGENESIS More than 80% of bile duct strictures occur after injury to the bile ducts during cholecystectomy. 5, 26 Bile ducts also can be injured during exploration of the common bile duct or other upper-abdominal operations, including gastrectomy, portacaval shunt, and hepatic and pancreatic procedures. In all of these cases, the strictures are associated with an iatrogenic injury to the biliary tree. The exact incidence of bile duct injury is unknown, as many cases may go unreported in the literature. However, Scandinavian From the Department of Surgery, The Johns Hopkins University, Baltimore, Maryland

*Assistant Professor tProfessor and Vice-Chairman :f:Professor and Chairman

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data from the years 1975 to 1981 suggest that the current incidence of such injury during cholecystectomy is approximately 1 in 1000. 1, 2 A number of obvious factors have been associated with bile duct injury during cholecystectomy, including inadequate exposure and lighting, inexperience, and failure to identify structures before clamping, ligating, or dividing them. More specific causes of bile duct injury also exist. Bleeding from the cystic artery or hepatic artery may lead to bile duct injury during attempts to gain hemostasis. The generous application of ligaclips to areas not easily visible in the hilum can result in placement of a clip on or across a bile duct, with resultant injury (Fig. 1). Failure to recognize congenital anomalies of the bile ducts such as insertion of the right hepatic duct into the cystic duct or a long common wall of the cystic duct and common bile duct may also lead to injury. Variations from the commonly described anatomic pattern of the extrahepatic biliary tree and adjacent hepatic arteries occur in more than 50% of individuals.:" Many of these involve an unusual termination of the cystic duct with the common hepatic duct. Attempts to ligate the cystic duct flush with the common bile duct in such cases may result in bile duct injury. Excessive traction on the cystic duct may also lead to an avulsion injury or to inclusion of a portion of the common bile duct wall in the cystic duct stump ligature. The "difficult cholecystectomy," as in cases of acute cholecystitis, is often cited as contributing to bile duct injury. Acute inflammation may distort tissue planes, and a tense, distended gallbladder may make exposure in the hilum difficult. Despite these potential technical problems, recent reviews of iatrogenic bile duct injury have demonstrated that inflammation and bleeding playa very small role in the reported injuries. 1, 36 Moreover,

Figure 1. Percutaneous transhepatic cholangiogram in a patient with a bile duct stricture secondary to iatrogenic injury during cholecystectomy. Note the large number of ligaclips in the area of the stricture.

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an anatomic anomaly was recognized only after injury had occurred in 16 of 55 cases in a Scandinavian review." In recent years, the importance of ischemia of the bile duct in the formation of postoperative strictures has been emphasized. 31,41 Unnecessary dissection around the bile duct during cholecystectomy or bile duct anastomosis may divide or injure the major arteries of the bile duct, which run in the 3 o'clock and 9 o'clock positions (Fig. 2). These axial arteries provide the nutrient blood supply of the supraduodenal bile duct, with flow coming from below in about 60% of patients and from above in 38% of patients. In 2% of patients, the common duct is supplied directly from the common hepatic artery in a nonaxial fashion. Thus, the portion of the supraduodenal bile duct proximal to the locus of transection or damage is vulnerable to ischemia, which may contribute to fibrosis and stricture formation during healing. A tremendous local inflammatory response also can develop in the adjacent tissues in association with bile leakage, which occurs with many bile duct injuries. The leakage of bile itself can cause inflammation, which may be intensified in the face of infection and may result in the development of a phlegmon or abscess. This inflammation results in additional fibrosis and scarring in the periductal tissue, contributing to the bile duct stricture. Finally, late presentation of a stricture can be the result of a neuroma forming in the periductular tissues. Bile duct injury also can occur during common duct exploration. Excessive instrumentation or dilation of the distal bile duct during attempts at stone extraction or sphincter manipulation, or the creation of a false passage during instrumentation, can result in injury. Moreover, exploration of and T-tube placement in a small bile duct may lead to a stricture. In this setting, passage of a Fogarty biliary catheter via the cystic duct and transduodenal sphincteroplasty may be safer than supraduodenal duct exploration.

Figure 2. Anterior view of the blood supply of the human bile duct. The blood supply to the ducts in the hilum of the liver (above) and to the retropancreatic bile duct (below) from adjacent arteries is profuse. The supraduodenal bile duct blood supply is axial and tenuous, with 60% from below and 38% from above. The small main axial vessels (3- and 9 o'clock arteries) are easily damaged. RHA = right hepatic artery; RDA = retroduodenal artery. (From Terblanche J, Allison HF, Northover JMA: An ischemic basis for biliary strictures. Surgery 94:52, 1983; with permission.)

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After cholecystectomy and common bile duct exploration, the two most common operations associated with bile duct injury are gastrectomy and hepatic resection. The most common situation resulting in biliary injury during the course of a gastrectomy involves dissection of the pyloric region and the first portion of the duodenum in the face of acute and chronic inflammation of peptic ulcer disease. In general, the injury occurs during mobilization of the duodenum either for creation of a Billroth I gastroduodenostomy or for closure of the duodenal stump. Biliary injury during liver resection is most likely to occur when the tumor or cyst being resected is near the hilum and the biliary tree is damaged during dissection. Management of injury from a partial hepatectomy can be extremely difficult, and there can be significant complications if the remaining lobe atrophies. Intraoperative cholangiography may be helpful in identifying the anatomy and avoiding injury in difficult cases. In addition to iatrogenic bile duct injury during cholecystectomy or other operations, postoperative bile duct strictures can occur at previous biliary anastomoses. Such strictures can occur at a biliary-enteric anastomosis performed for reconstruction after resection for benign or malignant disease of the pancreaticobiliary system, following end-to-end repair of a traumatic injury, or after liver transplantation. Unfortunately, the recurrence of bile duct strictures after an initial attempt at end-to-end repair is not uncommon and may account for a number of anastomotic strictures.P: 36 Many of these same pathophysiologic mechanisms may contribute to the development of anastomotic bile duct strictures. Ischemia secondary to excessive skeletonization of the duct in preparation for the anastomosis is most likely an important factor in many such strictures. Pitt et aP6 looked at a number of factors in patients with a recurrent bile duct stricture, including the length of follow-up, the influence of previous operations, the type of operation performed, the type of sutures used, and the use and duration of postoperative stenting. In this report, previous attempt at repair and a procedure other than choledochojejunostomy or hepaticojejunostomy appeared to be associated with a higher incidence of recurrent stricture. The type of suture material did not influence the outcome. However, when postoperative bile duct stents were used, long-term transhepatic stenting appeared to be most favorable. Pellegrini and colleagues:" confirmed the advantage of a biliary-enteric anastomosis but could not show a correlation with previous attempts at repair or an advantage to postoperative stenting. Both groups of authors stress the importance of long-term follow-up of bile duct anastomoses, because strictures can develop years after the anastomosis.

LOCATION AND CLASSIFICATION The etiology, ease of management, operative technique, and ultimate prognosis of postoperative bile duct strictures can differ considerably. The location of the stricture is of primary importance in dictating the management and predicting the outcome. In recognition of this, Bismuth has developed a classification of benign bile duct strictures based on the

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Figure 3. Classification of bile duct strictures based on the level of the stricture in relation to the confluence of the hepatic ducts. (From Bismuth H: Postoperative strictures of the bile duct. In Blumgart LH (ed): The Biliary Tract. Clinical Surgery International, vol 5. Edinburgh, Churchill Livingstone, 1982, pp 209-218; with permission.)

anatomic pattern of involvement" (Fig. 3). This classification not only defines postoperative strictures in a specific manner but permits comparison of various treatment modalities with respect to the extent of involved bile duct. The distribution of strictures based on this classification is shown in Table 1.

CLINICAL PRESENTATION Most patients with benign postoperative bile duct strictures present soon after their initial operation (Fig. 4). Although only about 10% of cases Table 1. Distribution of Bile Duct Strictures Based on Bismuth Classification TYPE

Type Type Type Type

1 2 3 4

Type 5 CHD

DESCRIPTION

INCIDENCE (%)

Low common hepatic or bile duct (CHD > 2 em) Mid common hepatic duct (CHD < 2 em) Hilar stricture Destruction of hilar confluence (right and left hepatic ducts separated) Involvement of right hepatic branch alone or with common duct

18-26 27-38 20-33 14-16

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3mo 6mo 9mo 1yr 2~r INTERVAL FROM SURGERY UNTIL PRESENTATION

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Figure 4. The cumulative percentage of patients developing symptoms with respect to the time since the procedure at which the injury occurred. (From Pitt HA, Miyamoto T, Parapatis SK, et al: Factors influencing outcome in patients with postoperative biliary strictures. Am J Surg 144:14, 1982; with permission.)

of postoperative strictures are suspected within the first week after cholecystectomy, nearly 70% of patients are identified within the first 6 months and more than 80% within 1 year of surgery. 36 In the remaining patients, presentation may be delayed for many years after the initial operative procedure. Thus, the timing of presentation often dictates the mode of presentation. Those patients found to have postoperative bile duct strictures within days to weeks of initial operation often present in one of two ways. One mode of presentation is progressively abnormal liver function tests, particularly total bilirubin and alkaline phosphatase. These changes often can be seen as early as the second or third postoperative day. In patients who were jaundiced prior to an initial operation, failure of serum bilirubin to return to normal should alert the surgeon to the possibility of bile duct injury. The jaundice mayor may not be associated with biliary sepsis. The second mode of early presentation relates to the leakage of bile from the injured bile duct. Bilious drainage from operatively placed drains or through the wound after cholecystectomy is abnormal and undoubtedly represents some form of bile duct injury. In cases with injury associated with distal bile duct obstruction, the amount of bilious drainage may represent the entire bile production and can be associated with development of fluid and electrolyte abnormalities. In those patients without drains, or in whom the drains have been removed, the bile leak may be either free into the peritoneal cavity or loculate, often as a perihepatic collection. The free accumulation of bile in the peritoneal cavity may result in either biliary ascites or bile peritonitis. The presence of bacteria in bile primarily determines this differentiation. Similarly, a loculated bile collection may result in a sterile biloma or in an infected subhepatic or subdiaphragmatic

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abscess. In the latter case, postoperative sepsis may herald the diagnosis. In all situations suggesting a bile leak, whether controlled via a drain or with free or loculated intra-abdominal bile accumulation, prompt investigation is warranted. Computed tomography is useful to define the presence of both a bile collection and a dilated biliary tree secondary to obstruction. The presentation of patients with postoperative bile duct strictures months to years after the initial operation most frequently is associated with episodes of cholangitis. Fever, chills, abdominal pain, and jaundice can be found in most patients. These episodes of cholangitis are frequently mild and respond to antibiotic therapy. Recurrent episodes usually precede the diagnosis. Less commonly, patients present with painless jaundice and no evidence of sepsis. Finally, in cases with a markedly delayed diagnosis, the patient may present with advanced biliary cirrhosis and portal hypertension.

LABORATORY AND RADIOLOGIC INVESTIGATIONS Liver function tests usually show evidence of cholestasis. The serum bilirubin may fluctuate and may even be normal. When elevated, serum bilirubin usually ranges from 2 to 6 mg/dl unless secondary biliary cirrhosis has developed. Elevations of bilirubin often are associated with cholangitis and may represent obstruction of the narrow lumen by biliary sludge that forms proximal to the stricture. Serum alkaline phosphatase also may fluctuate but is usually elevated even between acute attacks. Serum transaminase levels may be normal or slightly elevated except during episodes of cholangitis. If advanced liver disease exists with impaired hepatic synthetic function, serum albumin and prothrombin time may also become abnormal. Serum electrolytes and hematologic values are normal unless there is associated biliary sepsis. The imaging techniques of abdominal ultrasound and CT may play an initial role in the evaluation of patients with benign postoperative biliary strictures. In those patients presenting in the early postoperative period with evidence of a bile leak or biliary sepsis, these studies are useful to rule out intra-abdominal collections that might require drainage (Fig. 5A). In addition, in patients presenting with jaundice months or years after the operation, both ultrasound and CT can confirm biliary obstruction by demonstrating a dilated biliary tree. Computed tomography is especially useful in localizing the site of obstruction on the basis of the extent of dilatation of the extrahepatic bile duct. In patients whose presentations are remote from the operation, CT can also rule out biliary or pancreatic neoplasms as a cause of jaundice. The gold standard for patients with bile duct strictures is cholangiography. Percutaneous transhepatic cholangiography (PTC) is generally more valuable than endoscopic retrograde cholangiography (ERC). The former study is more useful in that it defines the anatomy of the proximal biliary tree, which is used in the surgical reconstruction. Moreover, during PTC, transhepatic catheters can be placed, which can be useful in providing

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Figure 5. Radiologic studies used in the diagnosis of postoperative bile duct strictures presenting in early postoperative period. A, Computed tomogram demonstrating a large biloma in a patient with a bile duct injury. B, Percutaneous transhepatic cholangiogram and biliary drainage in the same patient, demonstrating a bile duct injury and leakage of contrast into the subhepatic space.

decompression to treat either a bile fistula (Fig. 5B) or cholangitis. These catheters may also play an important technical role in surgical reconstruction 14 or, as will be discussed later, may provide access for balloon dilatation. The endoscopic study is often less useful in that the discontinuity of the common bile duct usually prevents adequate filling of the proximal biliary tree. Often, ERC will demonstrate only a normal-size distal bile duct up to the site of the stricture (Fig. 6). Regardless of which technique is chosen, patients should receive prophylactic antibiotic coverage because of the high incidence of postprocedure cholangitis. The diagnosis of a benign postoperative stricture weeks to months after cholecystectomy often is obvious. In a significant percentage of patients, however, the presentation is so remote from the operation as to raise suspicion of malignant biliary obstruction. Computed tomography is useful to rule out the presence of a pancreatic mass as a cause of biliary obstruction.

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Figure 6. Endoscopic retrograde pancreaticocholangiogram showing filling of a normal pancreatic duct. The common bile duct does not fill beyond the large Liga clip, which appears to have been placed across the duct.

In other cases, the cholangiographic pattern may suggest a malignant obstruction. In cases in which the hepatic duct bifurcation is involved, distinguishing cholangiocarcinoma from a benign stricture may be quite difficult. In recent years, significant experience has been gained in establishing a preoperative diagnosis using either bile cytology or cytologic brushings or biopsies obtained via transhepatic catheters.':' Hepatic arteriography and portal venous-phase studies may also suggest malignancy by showing vessel encasement or occlusion by tumor.!' If a malignancy is suspected, a segment of the bile duct stricture should be resected at the time of repair for histologic study.

PREOPERATIVE MANAGEMENT

The preoperative management of a patient with postoperative bile duct stricture depends primarily on the timing of the presentation. Patients presenting in the early postoperative period frequently are septic with either cholangitis or intra-abdominal bile collections. Sepsis must be controlled first with broad-spectrum parenteral antibiotics, percutaneous biliary drainage, percutaneous or operative drainage of biliary leaks, or some combination thereof. Once sepsis is controlled, there is no hurry in proceeding with surgical reconstruction of the bile duct stricture. Attention should be paid to correcting fluid and electrolyte abnormalities, anemia, and nutritional deficits. The combination of proximal biliary decompression and external drainage will allow most biliary fistulas to be controlled or even to close. 24, 45 The patient often may then be discharged home to allow 2 to 3 months for resolution of the inflammation in the periportal region and recovery of overall health. 16 In patients presenting with a biliary stricture remote from the initial operation, symptoms of cholangitis may necessitate urgent cholangiography and biliary decompression after delineation of the anatomic pathology.

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Biliary drainage usually is best accomplished by the transhepatic method, although endoscopic stent placement can also be successful. Parenteral antibiotics and biliary drainage should be continued until sepsis is controlled. Other patients present with jaundice without cholangitis. In these cases, PTe should be performed to define the anatomy. The use of preoperative biliary stents in these patients is controversial. In patients with benign bile duct strictures, preoperative biliary decompression has not been demonstrated to improve the outcome. 20, 28, 37

SURGICAL MANAGEMENT The goal of operative management of a bile duct stricture is the establishment of bile flow into the proximal gastrointestinal tract in a manner that prevents cholangitis, sludge or stone formation, restricture, and biliary cirrhosis. This goal is best accomplished with a tension-free anastomosis between healthy tissues that are as free as possible of scar tissue. A number of surgical alternatives exist for primary repair of bile duct strictures, including end-to-end repair, Roux-en-Y hepaticojejunostomy or choledochojejunostomy, choledochoduodenostomy, or mucosal grafting. The choice of repair depends on a number of factors, including the extent and location of the stricture, the experience of the surgeon, and the timing of the repair. Intraoperative Bile Duct Injury In many cases, proper management of a bile duct injury recognized at the time of cholecystectomy can avert the development of a bile duct stricture. Unfortunately, the injury is recognized at the original operation in only 12% to 46% of patients. 9, 12,21,25 In almost all cases where an injury occurs and is recognized, repair is best performed at that time. If a bile duct injury is suspected, intraoperative cholangiography should be performed to delineate the existing anatomy. If a segmental or accessory duct less than 3 mm in size has been injured and cholangiography demonstrates segmental or subsegmental drainage of the uninjured ductal system, simple ligation of the injured duct is adequate. However, if the injured duct is 4 mm or more in size, it is likely to drain multiple hepatic segments or the entire right or left lobe, and this injury requires operative repair. Likewise, if the injury involves the common hepatic duct or the common bile duct, repair should be carried out at the time of injury. The aims of any repair should be to maintain ductal length and not sacrifice tissue, as well as to effect a repair that will not result in postoperative bile leakage. In order to accomplish these goals, almost all repairs at the time of initial operation should involve some form of external drainage. Although lateral injuries without significant loss of length are unusual, such injuries must be recognized and repaired to avoid a bile leak. If such a defect is small, as with an avulsion injury of the cystic duct, direct repair over a T-tube can often be accomplished without the development of late stricture. If ,he injured segment of the bile duct is short (generally less than 1 em) and the two ends can be apposed without tension, then an

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end-to-end anastomosis can be performed using interrupted 4-0 or 5-0 sutures and placing a T-tube through a separate choledochotomy either above or below the anastomosis. A generous Kocher maneuver can be useful to help mobilize and approximate the cut ends. An end-to-end repair should be avoided if the ductal injury is high, near the hepatic duct bifurcation. In cases of proximal injuries or if the injured segment of bile duct is greater than 1 ern in length, an end-to-end bile duct anastomosis should be avoided because of the excessive tension in these situations. In these circumstances, the distal bile duct should be oversewn, and the proximal bile duct should be debrided of injured tissue and anastomosed in an endto-side fashion to a Roux-en-Y loop of jejunum. Our preference is to use a transhepatic biliary stent in this situation. The Roux-en-Y loop should be at least 40 em long to avoid the reflux of intestinal contents into the biliary tree. The use of a Roux-en-Y jejunal limb is also preferable to anastomosis to the duodenum, because in the latter case, an anastomotic leak will result in a duodenal fistula. Regardless of the type of anastomosis, the area should be drained externally with a closed suction drain. Only limited data are available on the long-term results of immediate repair of common bile duct injuries. Most injuries occur away from major medical centers, and, thus, even the successes are unlikely to be reported in the literature. In recent reports from Sweden and Chile, the results of immediate repair appear to be poor. 2,15 In the Swedish report," early primary repair with end-to-end anastomosis resulted in good results in only 22% of patients. Anastomotic leak necessitating reoperation occurred in 32% of patients. A late stricture occurred in another 37% of patients. In patients undergoing immediate repair with a biliary-enteric anastomosis, good results were seen in 54% of patients, with restricture occurring in only 12% of patients. Similar late results were noted in the series by Csendes et al,15 in which 29 of 36 patients with primary end-to-end repair developed postoperative strictures within four years. In contrast, Browder and colleagues" in the United States reported excellent results in eight patients with intraoperative repair. In this report, two early bile fistulas developed, but both closed spontaneously. Moreover, although end-to-end anastomosis was performed in seven of the eight patients, none of the patients developed a bile duct stricture during a limited follow-up (3 months to 6 years; mean 2.5 years). Injuries Recognized in the Early Postoperative Period Injuries not recognized at the time of operation usually present early in the postoperative period. As previously discussed, the initial management involves control of any biliary leak and associated sepsis. If a fistula is recognized in the postoperative period, immediate repair usually is not indicated, because the inflammation associated with the bile leak makes exposure of healthy bile duct mucosa extremely difficult. The use of percutaneous biliary drainage combined with the percutaneous drainage of intra-abdominal collections will result in the control of biliary sepsis and fistula output and often is associated with closure of the-bile leak. 24, 45 After

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closure of the leak, adequate time is allowed for inflammation to resolve prior to repair. Elective Repair Several important principles are associated with successful repair of a biliary stricture: (1) exposure of healthy proximal bile ducts that provide drainage of the entire liver; (2) preparation of a suitable segment of intestine that can be brought to the area of the stricture without tension, most frequently a Roux-en- Y jejunal loop; and (3) creation of a direct biliaryenteric mucosa-to-mucosa anastomosis. Simple excision of a bile duct stricture and end-to-end bile duct anastomosis or repair of the damaged duct can rarely be accomplished because of the invariable loss of length as a result of fibrosis associated with the injury. Similarly, anastomosis to the duodenum as a choledochoduodenostomy, which is an ideal operation for strictures associated with chronic pancreatitis, is not suitable for most postcholecystectomy strictures in that adequate length of bile duct for anastomosis to the duodenum often cannot be obtained. In addition, a postoperative biliary leak will result in a duodenal fistula. A number of alternatives exist for elective repair of bile duct strictures. The choice among them is dictated by the location of the stricture, the history of previous attempts at repair, and the surgeon's personal preference. However, experience with end-to-end repairs, choledochojejunostomy or hepaticoduodenostomy, and intrahepatic cholangiojejunostomy has not shown the good long-term results that have been achieved with Rouxen-Y choledochojejunostomy or hepaticojejunostomy." 7, 15,35,36,43 Thus, in almost all cases, a hepaticojejunostomy constructed to a Roux-en-Y loop of jejunum is preferable. The role of biliary stenting of this anastomosis is more controversial. However, we believe that a transanastomotic stent is helpful in almost all cases. In the early postoperative period, a stent is useful to decompress the biliary tree if a leak occurs and to provide access for cholangiography or removal of retained intrahepatic stones. If the injury has involved the common bile duct or the common hepatic duct well distal to the bifurcation where adequate bile duct mucosa could be defined (Bismuth Type I), the use of long-term biliary stents is not necessary. Regardless of whether a transhepatic catheter or T-tube is used, the catheter or tube can be removed 4 to 6 weeks after reconstruction. However, when adequate proximal bile duct is not available for a good mucosa-to-mucosa anastomosis, we favor long-term stenting of the biliary-enteric anastomosis with a Silastic transhepatic stent, usually for at least 12 months. Silastic transhepatic biliary stents can be inserted by a number of methods, including utilization of either preoperatively placed percutaneous transhepatic catheters, Randall stone forceps, or a long Bakes dilator. 10 The simplest approach, and the one we prefer, involves the preoperative percutaneous placement of transhepatic catheters. In injuries recognized to involve the hepatic duct bifurcation, two catheters should be placed preoperatively for each of the hepatic lobes. After mobilization and division of the bile duct, the biliary catheters protrude through the proximal end.

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A radiologic guidewire is passed through these catheters. A 14-Fr conde catheter, with its small-diameter end oriented toward the hepatic hilum, is then passed over the guidewire and sutured to the Ring catheter (Fig. 7A). The long arteriography guidewire is recommended, as the sutures occasionally break, resulting in the loss of the established tract. The coude catheter is pulled upward through the existing catheter tract into the hepatic parenchyma by withdrawing the preoperatively placed Ring catheter upward through the liver. A Silastic biliary stent is passed over the guidewire and sutured into the wider end of the coude catheter. The Silastic stent is then positioned with the previously formed transhepatic tract as the coude catheter is pulled forward through the liver. If a transhepatic biliary catheter has not been placed preoperatively, Randall stone forceps or a long Bakes dilator can be introduced into either the right or the left hepatic duct and used to assist the placement of the Silastic transhepatic stents (Fig. 7B). After the instrument has been advanced as far as possible, generally to within 1 to 2 em of the surface of the liver, Glisson's capsule is incised with the cautery, and the instrument is advanced out the superior aspect of the liver. The Silastic catheter is then secured to the instrument and pulled into position as the instrument is withdrawn downward out of the hepatic hilum. Alternatively, a heavy suture can be passed and sutured to a coude catheter and, subsequently, to the Silastic stent as described above. The Silastic stents are 70 em in length and come in 12-Fr to 22-Fr sizes. Multiple side holes are present along 40% of the length. These holes are positioned within the intrahepatic biliary tree and the portion of the Roux-en-Y jejunal loop used for the biliary anastomosis. The end of the stent without the side holes exits through the hepatic parenchyma and is brought directly through a stab wound in the upper anterior abdomen. The stent is fixed to the skin with wire sutures and is attached initially to a bile bag for dependent gravity drainage. After stent placement, a Roux-en-Y jejunal loop is prepared for the biliary-enteric anastomosis. The use of the defunctionalized Roux-en-Y loop minimizes the risk associated with anastomotic leak and prevents reflux of intestinal contents into the biliary tree. The loop should be at least 40 to 60 em long with its closed end brought up to the hepatic hilum in a tensionfree retrocolic position. The anastomosis is then performed as an end-toside hepaticojejunostomy (Fig. 7C). After completion of the anastomosis, Huorocholangiography can be performed to check the position of the transhepatic stents. If an acceptable proximal biliary segment is available with an adequate circumferential ring of healthy bile duct mucosa (Bismuth type 1), a mucosato-mucosa biliary-enteric anastomosis can be created over a preoperatively placed transhepatic catheter or an operatively placed T-tube. This anastomosis may be done in one or two layers, usually with 4-0 or 5-0 sutures. In this situation, the use of a larger Silastic transhepatic stent for long-term stenting is not necessary. However, particularly in cases with prior attempts at stricture repair, adequate healthy bile duct mucosa may be absent, and in these cases, long-term Silastic transhepatic stents are recommended. The side of the Roux-en-Y jejunal loop is sutured circumferentially with

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Figure 7. Operative repair of bile duct stricture using transhepatic biliary stents. A, A coude catheter is sutured to the preoperatively placed transhepatic catheter, which protrudes through the transected hepatic duct. The catheter, and subsequently the Silastic stent, can then be pulled through the catheter tract in the hepatic parenchyma. B, Alternatively, stone forceps can be passed into the hepatic duct, advanced through the intrahepatic biliary tree, and forced out through the parenchyma on the anterior surface of the liver. A Silastic biliary stent is then sutured to the end of the forceps so that it can be drawn back into the intrahepatic biliary tree and out the hepatic duct.

interrupted 4-0 or 5-0 sutures to the ductal tissue at the exit site of the stent from the hepatic hilum. For strictures of the common hepatic duct just distal to the hepatic duct bifurcation (Bismuth type 2), only one transhepatic stent usually is needed. However, for higher strictures involving the hepatic duct bifurcation (Bismuth type 3 or 4), both the right and the left main hepatic ducts should have stents placed preoperatively. In these latter cases, after dissection and resection of the stricture, including the bifurcation, the individual right and left hepatic ducts are defined, and Silastic transhepatic stents are positioned as previously described. Bilateral hepaticojejunostomies are then performed separately to the Roux-en-Y loop. After completion of the biliary-enteric anastomoses, the Roux-en-Y jejunal loop is tacked to

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Figure 7 (Continued). C, A Roux-en-Y jejunal loop is then anastomosed to the hepatic duct, liver capsule, and other structures at the egress site of the stent in the hilum of the liver. That portion of the stent that passes through the liver and into the jejunum contains multiple side holes. D, The completed biliary-enteric anastomosis over bilateral Silastic biliary stents is tacked to the undersurface of the liver. (From Cameron JL, Gayler BW, Zuidema GD: The use of Silastic transhepatic stents in benign and malignant biliary strictures. Ann Surg 188:552, 1978; with permission.)

the undersurface of the liver to avoid tension on the anastomosis (Fig. 7D). The defect in the transverse mesocolon, through which the retrocolic Rouxen- Y limb was placed, is closed to prevent small bowel herniation. Closed suction drains are placed near the biliary-enteric anastomosis. The sites where the Silastic stents exit the liver are also drained.

POSTOPERATIVE BILIARY STENTING The role of biliary stenting and the length of time the stent is employed remain controversial. As stated previously, when a large bile duct with circumferential mucosa is available, we employ only short-term stenting,

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usually 4 to 6 weeks with either a T-tube or a transhepatic stent. However, a number of authors do not believe that stenting is required even in the early postoperative period. 3, 7, 23 We have employed transhepatic Silastic stents for at least a year postoperatively in cases in which the anastomosis is performed at the area of the hilum and when the bile ducts are small and only a one-layer anastomosis is possible. 38 We prefer the use of transhepatic Silastic stents with one end left in the jejunum (a J-tube). However, other authors have described the use of transhepatic V-tubes. 34, 40 V-tubes, like the Silastic J-stents, exit through the anterior surface of the liver and the anterior abdominal wall on one end, but the other end is also brought through the Roux-en-Y limb as a Witzel enterostomy and then subsequently brought through the anterior abdominal wall. Those authors suggest that U-tubes are more easily changed. However, when bilateral stents are necessary, V-tubes require four tube exit sites versus two with the J-tubes. Moreover, the jejunal exit sites are more prone to bile leakage. The duration of stenting is also controversial, with recommendations ranging from long-term stenting for at least 6 months to 2 years" 10, 38, 40 to those authors who do not do stent at all or leave tubes in place for only 2 to 3 months. 3, 6, 7, 19, 23 Data concerning this controversy have been generated by Pitt et al,36 who found significantly better results in patients whose stents were in place for more than 1 month than in patients in whom the stent was removed in less than 1 month. Moreover, in patients stented for more than 9 months, results were significantly better if Silastic changeable stents were employed.

POSTOPERATIVE MANAGEMENT Postoperatively, the transhepatic catheter or Silastic biliary stent is placed to dependent gravity drainage for 5 to 7 days. At this time, cholangiography is performed to document anastomotic integrity and the absence of a biliary leak (Fig. 8). If no evidence of a leak is apparent, external biliary drainage can be discontinued, and the operatively placed drains can be removed. We believe that the duration of stenting is important to a good longterm result. Long-term stenting permits healing and scar contracture and thus assures a stable biliary anastomosis. Because the side holes of the transhepatic stents may become occluded by biliary sludge and secretions, we recommend daily saline flushes as well as routine changing of Silastic stents fluoroscopically over guidewires every 3 to 4 months. This procedure usually can be performed on an outpatient basis, although prophylactic antibiotics are recommended to prevent cholangitis.

RESULTS Morbidity and Mortality Repair of a bile duct stricture is associated with significant morbidity and mortality rates. A 1982 review of 38 series published since 1900

POSTOPERATIVE BILE DUCT STRICTURES

1371

Figure 8. Postoperative cholangiogram performed through Silastic biliary stents showing no evidence of anastomotic leak.

encompassing more than 7643 procedures in 5586 patients found an overall operative mortality rate of 8.3%.43 In the last decade, however, most series have reported mortality rates of less than 5%. 7, 19, 23, 34, 36, 38 Factors frequently associated with operative death are advanced age, coexistent disease, and a history of serious infection. The extent of underlying liver disease is the most important, however. In patients with advanced biliary cirrhosis and portal hypertension, operative mortality rates, with death from liver failure, can approach 30%.7 Proximal location of a bile duct stricture is usually associated with increased technical difficulty and thus with a slight higher risk. Postoperative morbidity rates also are significant, usually approaching 20% to 30%. Complications include the common postoperative problems such as hemorrhage, cardiopulmonary problems, urinary tract infection, and wound infection. Complications specific to the repair of bile duct strictures include anastomotic leaks, cholangitis, and hepatic insufficiency from prior biliary cirrhosis. Most anastomotic leaks documented by postoperative cholangiography or by bilious drainage from intraoperatively placed drains can be managed nonoperatively. Transhepatic stenting diverts biliary secretions externally in the face of a leak, which is one of the advantages of this technique. In most of these cases, anastomotic leaks heal in short order with no long-term consequences. Long-Term Results Excellent long-term results can be achieved in 70% to 90% of patients undergoing repair of bile duct strictures. 19, 23, 33, 35, 36, 38 The definition of satisfactory results in most series includes patients being asymptomatic with the absence of jaundice or episodes of cholangitis (Table 2). The length of follow-up is important in analyzing final results, because restenosis can occur as much as 20 years after the initial procedure'": 36 (Fig. 9). In general, however, approximately two thirds of restrictures will be evident within 2

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Table 2. Results of Surgical Management of Bile Duct Strictures MEAN FOLLOW-UP YEAR

INSTITUTION 36

UCLA UCSF35 Cleveland Clinic" Ohio State" St. Ceorge's'" Johns Hopkins"

1982 1984 1986 1988 1988 1989

NO. OF PATIENTS

SUCCESS (%)

66

86 78 82 95 72 88

60 105 22 163 25

(MOS.)

60 102

60 72 133

57

years and 90% within 7 years.:" The percentage of patients with good results may be inversely related to the number of previous repairs. Other factors that favor a good outcome are young age at the time of stricture repair, use of a Roux-en-Y biliary-enteric anastomosis, absence of infection and hepatic fibrosis, and the use of transhepatic stents. We recently reported our experience in the management of 25 consecutive patients with benign postoperative strictures using long-term transhepatic stents.:" Thirty-five per cent of these patients were classified as having Bismuth II strictures and 40% Bismuth III or IV. Stenting was employed for a mean of 13.8 months postoperatively. Follow-up for these patients was for a mean of 57 months. Three failures occurred (88% success), with two of these patients also having had multiple unsuccessful previous attempts at surgical repair. None of the patients died, and the operative morbidity rate was 20%. The chance of late recurrent strictures requires that patients be w

.-o~100 90 .-en~ .-z 80

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60

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i

2 3 4 5 6 12 INTERVAL UNTIL RECURRENCE (years)

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19

Figure 9. The cumulative percentage of recurrent strictures is shown with respect to the time interval from the initial repair until the next repair. (From Pitt HA, Miyamoto T, Pampatis SK, et al: Factors influencing outcome in patients with postoperative biliary stricture. Am J Surg 144:14, 1982; with permission.)

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POSTOPERATIVE BILE DUCT STRICTURES

followed indefinitely. Serum bilirubin, liver transaminases, and alkaline phosphatase are used. Radionuclide (IDA) scanning provides good physiologic information concerning bile flow and can be very useful in follow-up. Ultrasound or CT scanning to look for biliary dilatation and intrahepatic stones also can be helpful.

NONOPERATIVE MANAGEMENT Operative management of bile duct strictures is technically difficult and continues to be associated with significant postoperative morbidity. Moreover, in all series, recurrent strictures develop in some percentage of patients. These factors, in addition to the technical developments in the fields of therapeutic radiology and endoscopy, have led to the nonoperative management of bile duct strictures. Percutaneous Balloon Dilatation The largest nonoperative experience in the management of benign bile duct strictures is via the percutaneous transhepatic route. With this technique, access to the proximal biliary tree is gained, and the stricture is traversed with a guidewire under fluoroscopic guidance. Dilatation of the stricture is performed using angioplasty balloon catheters chosen on the basis of the location of the stricture and the diameter of the normal duct (Fig. 10). After the procedure, transhepatic stents are left in place for access to the biliary tree, for follow-up cholangiography, for repeat dilatation, and for maintenance of a lumen during healing. In most series, several dilatations are required. The procedure in many cases can be performed with a combination of local anesthesia and intravenous sedation. However, many patients find the procedure quite painful, and general or regional anesthesia has been necessary in a significant percentage. The early results in a number of series have been encouraging (Table 3). In a multicenter review by Mueller and colleagues;" 3-year follow-up showed a 76% patency rate for iatrogenic primary bile duct strictures and a 67% patency rate for anastomotic strictures, for an overall 70% success rate. Patency was based on the absence of symptoms and normal bilirubin and alkaline phosphatase. Williams and colleagues from the Mayo Clinic" achieved successful dilatation in 88% of patients with primary ductal strictures and 73% of patients with biliary-enteric anastomotic strictures, for an overall success rate of 78%. In this series, success was defined as absence of symptoms after stent removal with a mean follow-up of 28 Table 3. Results of Transhepatic Balloon Dilatation of Bile Duct Strictures YEAR

1985 1986 1987 1987 1989

INSTITUTION

Univ. Florida42 Multiple inst.:" Mayo Clinic"

Duke'" Johns Hopkins"

NO. OF PATIENTS

SUCCESS (%)

MEAN FOLLOW-UP (MOS.)

13 61 64 18 20

85 70 78 83 55

24 36 28 33 59

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Figure 10. See legend on opposite page

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POSTOPERATIVE BILE DUCT STRICTURES

1375

months (range 1-50 months). Similar results have also been reported in smaller series. 29, 42 In contrast, in the recent report from the Johns Hopkins Hospital, with one of the longest follow-ups available-59 months-the success rate was only 55%.38 Complications of balloon dilatation are frequent. In a report by Williams et al, 44 29% of patients lost 2 gm or more of hemoglobin after the procedure, and 7 of 65 patients (11%) undergoing transhepatic procedures required blood transfusion. Arteriobiliary fistulas were present in six of eight patients who did not stop bleeding spontaneously. Treatment by embolization in one case resulted in a left hepatic-lobe infarction and abscess that required surgical drainage. Sepsis with positive blood cultures occurred in 24% of patients despite antibiotic prophylaxis. Pancreatitis occurred in two patients, and a catheter-related duodenal perforation that necessitated surgery occurred in one patient. No sepsis or significant bleeding occurred in patients dilated via a T-tube tract, suggesting that much of the morbidity is attributable to traversing the hepatic parenchyma by large catheters. In the Johns Hopkins series, significant he mobilia was seen in 20% of patients, 38 but in the multicenter review by Mueller et al,30 the morbidity rate was less: septicemia with fever and hypothermia developed in less than 5% of patients, with no bleeding and no deaths. Endoscopic Dilatation The experience with endoscopic balloon dilatation is somewhat more limited, as this technique is technically possible only in patients with primary bile duct strictures or strictures at a choledochoduodenal anastomosis. Moreover, if long-term stenting with a prosthesis is indicated, repeat endoscopy will be necessary to change occluded stents. This technique begins with an ERC and endoscopic sphincterotomy. Re-evaluation with cholangiography and possible redilatation is performed every 3 to 6 months. In most reports, an endoprosthesis is left in place for at least 6 months. The largest experience with this technique has been reported by Huibregtse and colleagues" from The Netherlands (Table 4). Successful dilatation was achieved in 27 of 29 patients (93%) with benign postoperative bile duct strictures. A total of 70 procedures was performed in the 29 patients. Clinical follow-up of at least 6 months was available, with 19 patients having satisfactory results. The stricture was at the level of the cystic duct or proximal to it in 26 of 29 patients. No morbidity or death was associated with the procedure, although one death occurred in a patient who had failed dilatation; this death was the result of sepsis after a percutaneous transhepatic cholangiogram.

Figure 10. Stricture dilatation technique. A, Transhepatic cholangiogram demonstrating stricture at a previous choledochojejunostomy. B, Progressive dilatation of the strictured anastomosis with an angioplasty balloon catheter. C, Postdilatation stenting of the anastomotic stricture for long period. D, Subsequent cholangiography demonstrating resolution of the stricture. (From Pitt HA, Kaufman SL, Coleman J, et al: Benign postoperative biliary strictures: Operate or dilate? Ann Surg 210:417, 1989; with permission.)

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Table 4. Results of Endoscopic Balloon Dilatation of Bile Duct Strictures MEAN FOLLOW-UP YEAR

INSTITUTION

NO. OF PATIENTS

SUCCESS (%)

(MOS.)

1985 1986 1989

Cleveland Clinic" Amsterdam'" Milwaukee"

9 21 25

55 83 88

6 17 48

A similar experience has been reported by Geenen and colleagues at the Medical College of Wisconsin. 18 In this series, 18 of 25 strictures were postoperative in nature. Strictures were located at the cystic duct junction in 17 patients and in the distal bile duct in the remaining 8 patients. Twenty-two patients (88%) obtained significant clinical benefit. Only two complications occurred: one case each of mild pancreatitis and cholangitis. This series provides some of the longest follow-up available for this technique, ranging from 6 months to 7 years (mean 4.0 ± 0.3 years). Of the 25 patients, 8 had been asymptomatic for longer than 2 years since the last dilatation at the time of the report, and 8 patients had been asymptomatic for longer than 5 years. It should be acknowledged that a great deal of expertise is necessary to achieve such results. In a report by Foutsch and Sivac.!? success was obtained in only five patients with two serious complications among nine patients, including a common bile duct perforation and respiratory arrest. Moreover, two of the patients in whom the procedure failed died within 1 month as a result of complications of liver disease.

COMPARATIVE DATA Comparison of results of balloon dilatation with those of surgery has been difficult. Not only do few centers have a significant experience with both operative and nonoperative management, but the definition of a successful procedure and complications, as well as the length of follow-up, has not been consistent in the literature. To compare the results of balloon dilatation and surgery at one institution over the same period of time with similar management techniques, a retrospective review of results at The Johns Hopkins Hospital between 1979 and 1987 was complctcd.:" In this report, 42 patients had 45 procedures for benign postoperative biliary strictures. Three patients were managed with both surgery and balloon dilatation. Twenty-five patients underwent surgical repair with Roux-en-Y choledochojejunostomy or hepaticojejunostomy with postoperative transhepatic stenting for a mean of 13.0 ± 1.3 months. Twenty patients had balloon dilatation a mean of 3.9 times and were stented transhepatically for a mean of 13.3 ± 2 months. The two groups were similar with respect to multiple features that might have influenced the outcome, including age, sex, level of stricture, secondary biliary cirrhosis, and intrahepatic stones. Of the surgical patients, 56%

1377

POSTOPERATIVE BILE DUCT STRICTURES

SURGERY

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O-+-------~---------------------t I I I 12 60 72 o 48 Figure 11. Actuarial success rates over 72 months for surgery (89%) and balloon dilatation (52%). The difference is statistically significant (P < 0.01). (From Pitt HA, Kaufman SL, Coleman J, et al: Benign postoperative biliary strictures: Operate or dilate? Ann Surg 210:417, 1989; with permission.)

had undergone one or more previous surgical attempts at stricture repair as had 65% of the balloon dilatation patients. In the balloon dilatation group, all previous repairs had been a biliary-enteric anastomosis. In the surgical group, nine patients had undergone a previous biliary-enteric anastomosis, whereas five had had a previous end-to-end surgical reconstruction. The mean length of follow-up was 57 ± 7 and 59 ± 6 months for surgery and balloon dilatation, respectively. For both groups, a successful outcome was defined as no evidence of cholangitis or jaundice necessitating another procedure as judged more than 12 months from the onset of treatment. A failed treatment was defined as the need for operation or dilatation, hospital death after a procedure, or late death from liver failure, biliary sepsis, or portal hypertension. No patient died after any of the procedures. Procedure-related morbidity occurred in 20% of surgical patients and 35% of the patients undergoing balloon dilatation. Although the overall complication rate was not significantly different, the incidence of significant hemobilia after surgery and balloon dilatation was 4% and 20%, respectively (P <0.02). A successful repair was achieved in 88% of the surgical patients and in only 55% of those having balloon dilatation (P <0.02) (Fig. 11). The overall late mortality rate in this series was 10%. One late death occurred in the surgical group, whereas three late deaths followed balloon dilatation (4% versus 15%; P <0.02). However, none of the deaths was attributed to liver failure, biliary sepsis, or portal hypertension associated with the bile duct stricture. The factors influencing outcome are shown in Table 5. In order to define further the relative benefit of the two procedures, total hospital stay and total procedural costs were determined. As expected,

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Table 5. Factors Influencing Outcome of the Management of Postoperative Bile Duct Strictures SUCCESSFUL OUTCOME (%)

FACTOR

Type of Stricture Primary Anastomotic

86* 61

Level of Stricture (Bismuth) Type 1 Type 2 Type 3 Type 4 Type 5

100:j: 59

87 71 33

"P < 0.05 versus anastomotic strictures. :j:P < 0.05 versus Types 2-5.

the initial hospitalization was longer for surgery than for balloon dilatation. However, when rehospitalization for further dilatations, complications, or recurrences was considered, the total hospital stay did not differ significantly between the two groups: the mean stay for surgery was 26.4 ± 2.5 days, and that for balloon dilatation was 21.4 ± 1.7 days. Moreover, since 1984, the mean total hospital stay for surgery was down to 17.9 ± 1.5 days compared with 21.2 ± 1.7 days for balloon dilatation. Cost data paralleled hospitalization data and did not differ significantly between groups. The estimated total cost for surgery was $20,988 ± $1376 and that for balloon dilatation was $17,728 ± $1688. We concluded from this study that until properly designed, randomized, prospective controlled trials can be performed that prove otherwise, surgical repair for benign postoperative strictures is associated with fewer problems that necessitate further therapy. Nevertheless, nonoperative management may be reasonable in high-risk patients and in those who are unwilling to undergo further surgery.

SUMMARY Bile duct strictures are an uncommon but serious complication of primary operations on the gallbladder or biliary tree. Most strictures occur as a result of injury to the bile duct during cholecystectomy. In addition, strictures can occur at the site of previous biliary anastomoses for reconstruction of the biliary tree. Most patients with benign bile duct strictures present soon after their initial operation; however, in some cases, presentation is delayed for years. Cholangiography is essential for defining the anatomy of the biliary tree prior to management. In many cases, nonoperative biliary drainage is useful to treat sepsis and biliary fistulas. A number of alternatives exist for elective repair of bile duct strictures. Experience would suggest, however, that a choledochojejunostomy or hepaticojejunostomy performed through a Roux-en-Y limb of jejunum is the preferable management in most cases. Postoperative biliary stenting may be valuable in optimizing the results. Nonoperative management by

POSTOPERATIVE BILE DUCT STRICTURES

1379

percutaneous transhepatic or endoscopic balloon dilatation has been reported to be successful in a number of small series. Long-term results are limited, however. Comparative data suggest that surgical repair for benign postoperative strictures is associated with fewer long-term problems and with similar overall morbidity and costs.

REFERENCES 1. Andren-Sandberg A, Alinder G, Bengmark S: Accidental lesions of the common bile duct at cholecystectomy: Pre- and perioperative factors of importance. Ann Surg 201:328332, 1985 2. Andren-Sandberg A, Johansson S, Bengmark S: Accidental lesions of the common bile duct at cholecystectomy II: Results of treatment. Ann Surg 201:452-455, 1985 3. Aust JB, Root HD, Urdaneta L, et al: Biliary stricture. Surgery 42:601-608, 1967 4. Bismuth H: Postoperative strictures of the bile duct. In Blumgart LH (ed): The Biliary Tract. Edinburgh, Churchill Livingstone, 1982, pp 209-218 5. Bismuth H, Lazorthes, F: Les Traumatismes Operatoires de la Voie Biliare Principale, vol 1. Paris, Masson, 1981 6. Bismuth H, Franco D, Corlete MB, et al: Long-term results of Roux-en- Y hepaticojejunostomy. Surg Gynecol Obstet 146:161-167, 1978 7. Blumgart LH, Kelley CJ, Benjamin IS: Benign bile duct stricture following cholecystomy: Critical factors in management. Br J Surg 71:836-843, 1984 8. Braasch JW: Current considerations in the repair of bile duct strictures. Surg Clin North Am 53:423-433, 1973 9. Browder IW, Dowling JB, Koontz KK, et al: Early management of operative injuries of the extrahepatic biliary tract. Ann Surg 205:649-656, 1987 10. Cameron JL, Gayler BW, Zuidema GD: The use of Silastic transhepatic stents in benign and malignant biliary strictures. Ann Surg 188:552-561, 1978 11. Cameron JL, Pitt HA, Zinner MJ, et al: Management of proximal cholangiocarcinomas by surgical resection and radiotherapy. Am J Surg 159:91-98, 1990 12. Castrini G, Pappalardo G: Iatrogenic strictures of the bile ducts: Our experience with 66 cases. World J Surg 5:753-758, 1981 13. Cobb CJ, Floyd WN: Usefulness of bile cytology in the diagnostic management of patients with biliary obstruction. Acta Cytol 29:93-100, 1985 14. Crist DW, Kadir S, Cameron JL: The value of preoperatively placed percutaneous biliary catheters in reconstruction of the proximal part of the biliary tract. Surg Gynecol Obstet 165:421-424, 1987 15. Csendes A, Diaz JC, Burdiles P, et al: Late results of immediate primary end to end repair in accidental section of the common bile duct. Surg Gynecol Obstet 168:125130, 1989 16. Czerniak A, Thompson IN, Soreide 0, et al: The management of fistulas of the biliary tract after injury to the bile duct during cholecystectomy. Surg Gynecol Obstet 167:3338, 1988 17. Foutsch PG, Sivak MV Jr: Therapeutic endoscopic balloon dilatation of the extrahepatic biliary ducts. Am J Gastroenterol 80:575-580, 1985 18. Geenen DJ, Geenen JE, Hogan WJ, et al: Endoscopic therapy for benign bile duct strictures. Gastrointest Endosc 35:367-371, 1989 19. Genest JF, Nanon E, Grundfest-Broniatowski S, et al: Benign biliary strictures: An analytic review (1970 to 1984). Surgery 99:409-413, 1986 20. Hatfield ARW, Tobas R, Terblanche J, et al: Preoperative external biliary drainage in obstructive jaundice: a prospective controlled clinical trial. Lancet 2:896-899, 1982 21. Hillis TM, Westbrook KC, Caldwell FT, et al: Surgical injury of the common bile duct. Am J Surg 134:712-716, 1977 22. Huibregtse RM, Katon RM, Tytgat GNJ: Endoscopic treatment of postoperative biliary strictures. Endoscopy 18:133-137, 1986 23. Innes JT, Ferrara JJ, Carey LC: Biliary reconstruction without transanastomotic stent. Am Surg 54:27-30, 1988

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24. Kaufman SL, Kadir S, Mitchell SE, et al: Percutaneous trans hepatic biliary drainage for bile leaks and fistulas. AJR 144:1055-1058, 1985 25. Kune G: Bile duct injury during cholecystectomy: Causes, prevention and surgical repair in 1979. Aust NZ J Surg 49:35-40, 1979 26. Lindenauer SM: Surgical treatment of bile duct strictures. Surgery 73:875-880, 1973 27. Maroney TP, Ring EJ: Percutaneous transjejunal catheterization of Roux-en-Y biliaryjejunal anastomoses. Radiology 164:151-153, 1987 28. McPherson GAD, Benjamin IS, Hodgson HJF, et al: Preoperative percutaneous transhepatic biliary drainage: The results of a controlled trial. Br J Surg 71:371-375, 1984 29. Moore AV Jr, Illescas FF, Mills SR, et al: Percutaneous dilatation of benign biliary strictures. Radiology 163:625-628, 1987 30. Mueller PR, vanSonnenberg E, Ferrucci JT, et al: Biliary stricture dilatation: Multicenter review of clinical management in 73 patients. Radiology 160:17-22, 1986 31. Northover JMA, Terblanche J: A new look at the arterial supply of the bile duct in man and its surgical implications. Br J Surg 66:379-384, 1979 32. Northover JMA, Terblanche J: Applied surgical anatomy of the biliary tree. Clin Surg Int 5:1-16, 1982 33. Pain JA, Knight M, Smith RS: Long-term results of the mucosal graft operation for benign bile duct strictures. Netherland J Surg: Abstracts of Second World Congress of HepatoPancreatic-Biliary Surgery, 1988, p 170 34. Parker GA, Halloran LG: Reconstruction of the bile duct with transanastomotic U tubes. Surg Gynecol Obstet 162:433-436, 1986 35. Pelligrini CA, Thomas MJ, Way LW: Recurrent biliary stricture: Patterns of recurrence and outcome of surgical therapy. Am J Surg 147:175-180, 1984 36. Pitt HA, Miyamoto T, Parapatis SK, et al: Factors influencing outcome in patients with postoperative biliary strictures. Am J Surg 144:14-21, 1982 37. Pitt HA, Gomes AS, Juan LF, et al: Does preoperative percutaneous biliary drainage reduce operative risk or increase hospital cost? Ann Surg 201:545-553, 1985 38. Pitt HA, Kaufman SL, Coleman J, et al: Benign postoperative biliary strictures: Operate or dilate? Ann Surg 210:417-427, 1989 39. Russell E, Yrizarry JM, Huber JS, et al: Percutaneous transjejunal biliary dilatation: Alternate management for benign strictures. Radiology 159:209-214, 1986 40. Saypol GM, Kurian GA: A technique of repair stricture of the bile duct. Surg Gynecol Obstet 128:1071-1076, 1969 41. Terblanche J, Allison HF, Northover JMA: An ischemic basis for biliary strictures. Surgery 94:52-57, 1983 42. Vogel SB, Howard RJ, Caridi J: Evaluation of percutaneous transhepatic balloon dilatation of benign biliary strictures in high-risk patients. Am J Surg 149:73-79, 1985 43. Warren KW, Christophi C, Armendari ZR: The evolution and current perspectives of the treatment of benign bile duct strictures: A review. Surg GastroenteroI1:141-154, 1982 44. Williams HJ, Bender CE, May GR: Benign postoperative biliary strictures: Dilatation with fluoroscopic guidance. Radiology 163:629-634, 1987 45. Zuidema GO, Cameron JL, Sitzmann JV, et al: Percutaneous transhepatic management of complex biliary problems. Ann Surg 197:584-593, 1983

Address reprint requests to Keith D. Lillemoe, MD Blalock 656 Department of Surgery The Johns Hopkins Hospital 600 North Wolfe Street Baltimore, Maryland 21205