Postoperative Biliary Strictures and Leaks


Introduction

Accidental injuries of the bile ducts leading to biliary leaks and strictures may occur during any surgical procedure involving the biliary tract. However, the main causes of injury of the bile ducts at the present time are laparoscopic cholecystectomy (LC) and after liver transplantation (LT). Although LC has proved to be superior to open cholecystectomy in terms of shorter hospitalization, lower overall morbidity, faster recovery, and better cosmetic outcome, the risk of bile duct injury during LC is two to six times greater compared with open cholecystectomy. Bergman et al (1996) described four types of postoperative bile duct injuries, as follows:

  • Type A: Cystic duct leaks or leakage from aberrant or peripheral hepatic radicles (minor lesions)

  • Type B: Major bile duct leaks with or without concomitant biliary strictures (major lesions)

  • Type C: Bile duct strictures without bile leakage (major lesions)

  • Type D: Complete transection of the duct with or without excision of some portion of the biliary tree (major lesions)

Biliary strictures in patients with LT are classified as anastomotic strictures (ASs) and nonanastomotic strictures (NASs). AS are by far the most common. In most centers, a biliary duct-to-duct anastomosis is preferred over a Roux-en-Y choledochojejunostomy as it offers the advantage of easy endoscopic access to the biliary system and preservation of the sphincter of Oddi. The type of LT and biliary reconstruction has some implications in the development of biliary strictures. Due to the small diameter of the anastomotic bile duct, biliary strictures are known to be more common in living-donor LT (LDLT) than in deceased-donor LT (DDLT). The type of biliary reconstruction (duct-to-duct choledocho-choledochostomy vs. Roux-en-Y choledochojejunostomy) in DDLT has been suggested as a risk factor for biliary complications; however, it is now generally agreed upon that the rate of complications is similar with the Roux-en-Y choledochojejunostomy.

Epidemiology

LC was first performed by Mouret in France in 1987. The technique was standardized by two other French surgeons, Dubois in Paris and Perissat in Bordeaux. This new technique spread very rapidly around the world; in the United States, the percentage of cholecystectomies done laparoscopically grew from zero in 1987 to over 90% in 2010. The advent of LC also induced an estimated increase of at least 25% in the overall number of cholecystectomies performed, so that the likely number of cholecystectomies performed at the present time in the United States is 800,000 per year. The number of iatrogenic injuries to the bile duct has increased accordingly.

There are many reasons that may explain the increased incidence of biliary complications at the beginning of the laparoscopic era, most related to the new technical skills required to perform laparoscopically what had previously been done by open surgery: bidimensional vision, loss of tactile sensations, different visual approach of the hepatic pedicle, difficult hemostatic maneuvers, abuse of electrocoagulation, and lack of confidence with the new instrumentation. The rate of injuries seemed to be related to the surgeon's learning curve and his or her personal experience. An inversely proportional relationship between the number of cholecystectomies performed and the rate of injuries was suggested by earlier reported series. In a review of 77,604 LCs performed in the United States, the incidence of biliary injuries decreased from 0.6% to 0.4% ( p < 0.001) for surgical teams having an experience of more than 100 LCs. A Belgian survey suggested the number of 50 LCs as the threshold of a completed learning curve; however, the same authors emphasized that one-third of the biliary injuries in their country had occurred with surgeons with an experience of more than 100 LCs. When reviewing several multicenter series published before 1995, totaling 198,267 LCs, the incidence of biliary injuries was 0.55% in 13 European series and 0.49% in 17 series outside Europe.

In the mid-1990s, the incidence of biliary injury seemed to be three times higher for LC than for open cholecystectomy. However, these figures most likely underestimated reality because there was a tendency not to declare all the lesions, as revealed by the low rate of reply to most surveys and by the increasing number of reported lesions in direct proportion with the collected replies. At the present time, the incidence of biliary injuries has not substantially changed, even if a trend toward reduction has been reported by some authors. The estimated overall incidence is 0.25% to 0.74% for major biliary lesions ( Table 54.1 ) and 0.1% to 1.7% for minor biliary lesions ( Table 54.2 ). These figures are only partially explained by the still increasing number of LCs performed around the world and by the activity of young surgeons at the beginning of their learning curve. However, at least one-third of biliary injuries may be ascribed to technical mistakes during surgery. The learning curve is not the only risk factor for LC.

TABLE 54.1
Incidence of Major Biliary Lesions (Bergman's Type B, C, and D) During Laparoscopic Cholecystectomy (LC) (Multicenter Surveys)
Author Country Year No. LC Major Biliary Lesions (%)
MacFayden et al United States 1998 114,005 0.5
Nuzzo Italy 2002 56,591 0.31
Russell et al United States 1996 15,221 0.25
Z'graggen et al Switzerland 1998 10,174 0.31
Gigot et al Belgium 1997 9959 0.5
Wherry et al United States 1996 9130 0.41
Adamsen et al Denmark 1997 7654 0.74
Richardson et al Scotland 1996 5913 0.33

TABLE 54.2
Incidence of Minor Biliary Lesions (Bergman's Type A) During Laparoscopic Cholecystectomy (LC) (Multicenter Surveys)
Author Country Year No. LC Minor Biliary Lesions (%)
MacFayden et al United States 1998 114,005 0.38
Nuzzo Italy 2002 56,591 0.1
Z'graggen et al Switzerland 1998 10,174 0.93
Wherry et al United States 1996 9130 0.53
Adamsen et al Denmark 1997 7654 1.7
Richardson et al Scotland 1996 5913 0.28

Bile duct strictures after LT account for approximately 40% to 50% of all biliary complications after LT. The incidence of AS in various reports ranges between 10% and 15%. Strictures that occur early after LT are mainly due to technical problems, whereas late strictures are mainly due to vascular insufficiency, ischemia, and problems with healing and fibrosis. Patients with Roux-en-Y choledochojejunostomy may also develop strictures at the anastomosis with the bowel, and in most cases percutaneous therapy by interventional radiology is performed in these individuals. In some centers with experienced endoscopists, endoscopic retrograde cholangiopancreatography (ERCP) can be successfully performed in patients with a Roux-en-Y choledochojejunostomy with small bowel enteroscopy.

Pathogenesis

An unintentional lesion of the bile duct also may occur during an “easy” cholecystectomy performed by an experienced surgeon. Intuitively, the likelihood of injuring the bile duct should increase when the cholecystectomy is difficult and the surgeon is inexpert. Any cholecystectomy may become unexpectedly difficult during surgery; however, clinical and morphologic criteria exist that may be useful in predicting a cholecystectomy at higher risk of bile duct injury. Clinical criteria are obesity; previous abdominal surgery; cirrhosis; portal hypertension; age of the patient; and previous cholecystitis, cholangitis, or pancreatitis. Morphologic criteria revealed by preoperative abdominal ultrasound (US) are related to the gallbladder status (scleroatrophic gallbladder, thickening of the gallbladder wall, gallbladder distention resulting from a stone in the infundibulum) and to the liver (hepatomegaly, atrophy or hypertrophy of the liver lobes). The presence of several criteria raises the chances of being confronted with a difficult cholecystectomy and the risk of concomitant common bile duct (CBD) stones.

In patients who have undergone LT, a number of factors play a role in the development of ASs and NASs. In most instances, the major underlying risk factor is ischemic due to problems with the hepatic artery, mainly stenosis or thrombosis (HAT). As the biliary system receives blood supply mainly via the hepatic artery, low flow of the hepatic artery can lead to complex ASs and hilar strictures. Hepatic artery stenosis can also lead to both ASs and NASs, particularly when associated with long, cold ischemia time. T-tube placement in LT is controversial. Originally T-tubes were routinely placed as a prophylactic measure for AS development. However, the results of several comparative studies, systematic reviews, and meta-analysis suggest no major differences in the incidence of biliary complications, and the current trend has favored the abandonment of the use of T-tubes after LT in most centers. Other factors include concomitant bile leak, technical factors during surgery (tight anastomosis, excessive dissection and electrocautery during the reconstruction, redundant bile duct), mismatched size between donor and recipient bile ducts, ischemia/reperfusion injury, presence of cytomegalovirus infection, donation after cardiac death, ABO blood group mismatch, older age of donor, graft, steatosis, prolonged cold and warm ischemia times, and primary sclerosing cholangitis.

Unrecognized CBD stones are one of the major risk factors of cystic duct leakage after LC. The mechanism and the cause of a biliary injury remain unexplainable in at least one-third of cases. In more than 50% of cases, the injury occurs during the dissection of the cystic duct or during separation of the gallbladder neck from the CBD. Misinterpretation of the cystic duct and the CBD is the most common cause of injury. Excessive traction on the gallbladder neck, especially if the tissues are not inflamed, may facilitate the injury of the CBD. Conversely, when the area is acutely or chronically inflamed or when a stone is trapped in the gallbladder infundibulum, the risk of CBD injury is higher during the dissection of the gallbladder neck from the hepatic pedicle. Other common reasons for bile duct injury are related to incorrect hemostatic maneuvers in the case of bleeding from the cystic artery; inappropriate use of electrocautery; and other specific maneuvers, such as intraoperative cholangiography, which is used in cases of suspected CBD stones or difficult anatomy, cystic duct dilation, and transcystic CBD instrumental exploration.

An anatomic anomaly is often reported by the surgeon as having caused a biliary injury. Variations of the biliary anatomy, especially at the level of the main hepatic confluence, are present in 50% of patients (see the later section on interpretation of intrahepatic cholangiography ). Surgeons must be aware of such variations and must keep in mind the danger of injuring aberrant ducts originating in the right liver during dissection of the gallbladder pedicle. Aberrant ducts must not be interpreted as accessory ducts because the biliary distribution within the liver parenchyma is of a terminal type; this implies that there are no intrahepatic anastomoses between the ducts and that every injury of an aberrant duct would determine functional exclusion of the corresponding liver area. Injury to a small aberrant duct may still be considered a minor lesion; however, it would cause a bile leak into the peritoneal space with all the related consequences. Another cause of injury is clipping or ligation of an aberrant duct. This injury does not involve a bile leak but entails the functional exclusion of the corresponding liver area leading to its progressive atrophy and hypertrophy of the remaining liver parenchyma. This possible event may be clinically totally asymptomatic and noted only by an increase in biochemical parameters of cholestasis and cytolysis ( Fig. 54.1 ). Although there is no indication of treatment in asymptomatic cases, if the obstructed ducts become infected, recurrent cholangitis is the typical clinical manifestation often requiring operative reestablishment of an adequate bile flow.

FIG 54.1, This patient presented 2 years after laparoscopic cholecystectomy (LC) with only occasional minor right upper quadrant pain and slightly elevated liver function tests. A, Magnetic resonance cholangiography shows complete obstruction and dilation of the right biliary ductal system with normal common bile duct (CBD) and left biliary ductal system. B, Abdominal magnetic resonance imaging shows hypotrophy of the right liver and compensatory hypertrophy of the left liver.

Clincial Features

Schematically, three main clinical pictures are characteristic of a bile duct injury: (A) external biliary fistula, (B) choleperitoneum, and (C) cholestasis with or without the features of acute cholangitis. Various combinations of these clinical pictures may also be present. Most important, although some of the clinical manifestations, such as mild jaundice or well-drained external bile leakage, do not require any emergency treatment, the presence of infection must be regarded as an important criterion that requires intensive care and rapid decisions to treat sepsis. Septic complications are the main reason for mortality in these patients in the postoperative period. External biliary fistula and choleperitoneum are both typical features of the immediate postoperative period, whereas obstructive jaundice may occur either immediately after surgery or later, within days to several years. When symptoms arise late after surgery because of a slow progression from injury to stricture, overt jaundice may be absent, and the clinical picture is typically that of anicteric cholestasis, with or without itching, and recurrent bouts of acute cholangitis.

The suspicion of bile duct injury after LC injury is not always straightforward. When subtle symptoms such as dull abdominal pain, abdominal distention, low-grade fever, and nausea arise in the first days after LC, one should always suspect a possible complication. Intraperitoneal bile collections may initially produce very little or no specific symptoms, but they should be quickly suspected and eventually confirmed to identify the cause and to plan the best treatment for the individual patient. Hemobilia is a rare but alarming clinical presentation of a bile duct injury. The mechanism by which a biliary injury may be associated with hemobilia is often the perforation of a pseudoaneurysm of the right hepatic artery or one of its branches into the bile ducts. These pseudoaneurysms are the result of an inadvertent intraoperative injury of the artery produced by hemostatic maneuvers during a difficult cholecystectomy and cause hemoperitoneum. In patients with an external biliary drainage or fistula, the bleeding may become suddenly and massively apparent through the drain and may occasionally require emergency treatment.

In individuals who undergo LT, the clinical presentation is variable according to the type of lesion. In many cases, patients will have nonspecific symptoms such as malaise and anorexia. Others may present with pruritus, jaundice, or associated bile ascites and abdominal pain. In most instances, a biliary stricture is usually first suspected in asymptomatic LT recipients who have elevations of serum bilirubin, alkaline phosphatase and/or gamma-glutamyl transferase levels. Although strictures usually present as asymptomatic cholestasis, some patients can present with cholangitis, especially if the patient has concomitant bile duct stones.

Diagnostic Approach and Differential Diagnosis

In all cases of a suspect biliary stricture, the initial evaluation should include an abdominal US. In those with LT, a Doppler evaluation of the hepatic vessels to rule out hepatic artery thrombosis or stenosis and/or portal or hepatic vein occlusion must also be performed. Unfortunately, abdominal US may not be sufficiently sensitive (sensitivity 40% to 66%) to detect biliary obstruction in many patients. Thus, the absence of bile duct dilation on US should not preclude further evaluation with more sensitive tests if there is clinical suspicion of a biliary stricture. In such cases, a magnetic resonance cholangiopancreatography (MRCP) is considered an optimal noninvasive diagnostic tool for the assessment of the biliary strictures. Although ERCP or percutaneous transhepatic cholangiography are the gold standard, MRCP has gained acceptance as the most reliable noninvasive study for the evaluation of the bile ducts, particularly in patients after LT (sensitivity 96%, specificity 94%). The preferred approach is to perform an MRCP first; however, proceeding with a diagnostic invasive procedure such as ERCP without an MRCP can be an acceptable clinical strategy in some patients because of the high likelihood that a therapeutic intervention will be required. An algorithm depicting the diagnostic approach for patients with suspected AS is shown in Fig. 54.2 .

FIG 54.2, An algorithm depicting the diagnostic approach for patients with suspected biliary anastomotic strictures.

Strictures occurring long after surgery may need to be distinguished from malignant strictures and other benign conditions such as primary sclerosing cholangitis, autoimmune cholangitis, or sclerosing cholangitis in critically ill patients among others. The clinical history may be helpful only in cases in which the biliary injury had been recognized and eventually treated at the time of surgery. In this setting, the stricture is usually the result of progressive scarring at the site of surgical repair. In all other circumstances, the relationship with cholecystectomy or LT should be questioned. However, clinical presentation may be helpful in discriminating postoperative and malignant stenoses; painless jaundice is in favor of a malignant disease, whereas development of overt jaundice in benign strictures is often heralded by a long period of anicteric cholestasis and relapsing attacks of mild to severe acute cholangitis. Stricture morphology may be very helpful in discriminating scars from neoplastic involvement of the bile duct. Postoperative strictures are usually short, with sharp, often asymmetric edges, close to the cystic duct stump, and clips may be seen lying over the bile duct or located medially to it. ASs after LT are defined as a dominant short narrowing at the anastomotic site without free or effective passage of contrast material as demonstrated by cholangiography ( Fig. 54.3 ).

FIG 54.3, Biliary anastomotic stricture after liver transplantation. The structure is quite short and in the area of the anastomosis. These strictures are amenable to endoscopic therapy with biliary dilation and subsequent plastic stent placement across the stricture.

Treatment

In recent years, ERCP has acquired a pivotal role in the management of postsurgical biliary complications. Both the major typical clinical presentations occurring in this setting may be addressed by ERCP: (A) biliary leak into the peritoneal cavity or external leak and (B) obstructive syndrome with cholestasis, cholangitis, or jaundice. ERCP confirms the clinical suspicion of biliary injury and provides detailed morphologic information of the lesion. ERCP is currently considered a first-line therapeutic tool in complications that are amendable to endoscopic treatment.

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