Prevention and Management of Bile Duct Injury


Bile duct injuries most commonly occur after primary operations on the gallbladder or biliary tree. Biliary injuries themselves are also among the most difficult challenges that a surgeon will face. Although numerous technologic developments have facilitated diagnosis and management, bile duct injuries remain a significant clinical problem. If they go unrecognized or are managed improperly, life-threatening early complications such as sepsis and multisystem organ failure or late complications of biliary cirrhosis, portal hypertension, and cholangitis can develop. To avoid these complications, virtually every patient with a bile duct stricture should undergo evaluation and treatment with the goal of relieving the obstruction to bile flow and its associated hepatic injury. Finally, the occurrence of a major bile duct injury during an elective cholecystectomy remains one of the most common indications of medical malpractice claims within the United States.

Epidemiology of Bile Duct Injuries

Most benign bile duct strictures result from operations in or near the right upper quadrant. More than 80% of strictures occur after injury to the bile ducts during cholecystectomy ( Fig. 113.1 ). The exact incidence of bile duct injury is unknown because many cases go unreported in the literature. Data suggest that the incidence of bile duct injury during the “open cholecystectomy era” was 1 in 500 to 1000 cases. The incidence of bile duct injury during laparoscopic cholecystectomy is clearly higher. Although a wide range in the incidence of injury can be found in reported series, the most accurate data are derived from surveys encompassing thousands of patients. These reports reflect the results from a large number of surgeons in both community and teaching hospitals. These series suggest an incidence of bile duct injury during laparoscopic cholecystectomy ranging from 0.3% to 0.7%. Fortunately, now over 25 years after its introduction in the United States, the incidence of bile duct injury associated with laparoscopic cholecystectomy may be starting to trend downward in recent reports. The increase in incidence of biliary injuries when compared with the open technique is likely inherent within the laparoscopic approach and certainly no longer the function of a learning curve. Furthermore, the introduction of new techniques such as single-port laparoscopic cholecystectomy and robotic cholecystectomy do raise some concerns that injuries could become more common. Finally, as experience in open cholecystectomy in surgical training programs has decreased, there are also concerns for a potential increase in the incidence (and severity) of injuries during difficult laparoscopic cases that are converted to open procedures.

FIGURE 113.1, Strasberg bile duct injury classification scheme.

General Prevention of Bile Duct Injuries

A number of factors are associated with bile duct injury during either open or laparoscopic cholecystectomy, including acute or chronic inflammation, inadequate exposure, patient obesity, and failure to identify structures before clamping, ligating, or dividing them. Bleeding from the cystic or hepatic arteries can lead to bile duct injury during attempts to achieve hemostasis. The generous application of Ligaclips at either open or laparoscopic cholecystectomy to hilar areas not well visualized can result in placing a clip on or across a bile duct, with resultant injury. Failure to recognize congenital anatomic anomalies of the bile ducts, such as the low insertion of the right hepatic duct or even into the cystic duct, or a long common wall between the cystic duct and the common bile duct, can also lead to injury. There have been many discussions concerning the risks of bile duct injury during cases of severe acute cholecystitis, as well as how these risks are affected by timing of cholecystectomy. Although 30-day postoperative morbidity and mortality rates may remain independent of timing, it is clear that patients who undergo laparoscopic cholecystectomy beyond 24 hours are more likely to require an open procedure and sustain significantly longer postoperative and overall lengths of hospital admission (and therefore cost).

Numerous technical factors that are associated with laparoscopic cholecystectomy can also increase the risk of bile duct injury compared with the open procedure. These factors include the use of an end-viewing laparoscope, which alters the surgeon's perspective of the operative field. The issue of visual alignment and perspective has become even more topical with the proliferation of single-incision laparoscopic cholecystectomy that is known to be associated with a higher rate of common bile duct injury than the traditional four-incision laparoscopic technique using an angled scope. Excessive cephalad retraction of the gallbladder fundus can cause the cystic duct and common bile duct to become aligned in the same plane. This distortion often results in the classic laparoscopic injury, in which the common bile duct is mistaken for the cystic duct and clipped and divided.

The role of intraoperative cholangiography (IOC) in preventing bile duct injury during laparoscopic cholecystectomy remains controversial. Individual series have failed to demonstrate that either performing routine or selective IOC affects the incidence of bile duct injury. Although an initial retrospective nationwide cohort analysis of Medicare patients undergoing laparoscopic cholecystectomy between 1992 and 1999 demonstrated that common bile duct injuries occurred in 0.39% of patients in which IOC was performed versus 0.58% in patients not undergoing IOC (unadjusted relative risk, 1.49; 95% confidence interval, 1.42 to 1.57), a more recent Medicare-based study (2000–2009), analyzing over 92,000 patients undergoing cholecystectomy identified no statistically significant association between IOC and common bile duct injury. The authors therefore concluded that IOC is not effective as a preventive strategy against common duct injury during cholecystectomy. Despite this controversy, the proper interpretation of IOC can minimize the extent of injury. Nevertheless, only 27% of surgeons in the United States perform IOC routinely (see Fig. 113.1 ). Finally, ample evidence exists to support the conclusion that the experience of the surgeon in performing laparoscopic cholecystectomy can be correlated with the risk of bile duct injury.

Cognitive Factors Related to the Prevention of Bile Duct Injuries

In recent years, there has been a growing understanding of surgeon cognitive factors associated with bile duct injury during laparoscopic cholecystectomy. An analysis examining 252 biliary injuries during laparoscopic cholecystectomy using human error factor and cognitive science techniques found that 97% of injuries were caused by visual-perceptual illusion or inadequate visualization. Further work from the same group has determined a major explanation for the surgeon's frequent inability to recognize bile duct injury. These bile duct injuries appear to be associated with confirmation bias, which is a propensity to seek cues to confirm a belief and to discount cues that might discount the belief. Although cognitive factors are important for the understanding of the psychological issues associated with bile duct injuries, surgeons must continue to have the appropriate corrective mechanisms in place to minimize the chance of these injuries, including knowledge of anatomy, typical mechanisms of injury, and a true sense of suspicion and logic. An example of such a corrective mechanism occurs within the operative technique of laparoscopic cholecystectomy, which defines the “critical view of safety,” and therefore helps prevent misidentification and injury of the major bile ducts ( Fig. 113.2 ). This concept mandates that the fundus of the gallbladder be retracted superiorly while the infundibulum is retracted laterally. This exposure generally allows the surgeon to carefully dissect out the triangle of Calot, leaving only two structures connected to the lower end of the gallbladder: the cystic artery and cystic duct. The critical view of safety has also been enhanced to now describe both anterior and posterior views.

FIGURE 113.2, The critical view needed to avoid bile duct injury. Here, the triangle of Calot has been dissected free of all tissue except the cystic duct and cystic artery. A laparoscopic instrument is shown dorsal to the cystic duct and artery.

While this maneuver is the single most effective means of preventing a bile duct injury, the reality is substantially more complex. In scenarios of a short or nonexistent cystic duct, or a small common bile duct (common in acute cholecystitis), these structures can be confused for each other. Furthermore, inappropriate or overzealous traction then makes these associations even more challenging. Similarly, inflammation closes the space between the gallbladder and the bile duct. In extreme cases, they may even be fused and move as a single unit (Mirrizi type A). This not uncommon reality makes identification of associated regional anatomy even more important for the surgeon in an attempt to orient the critical structures of interest and proceed with a safe procedure. These spatial-regional issues can be further challenged by a loss of perspective given the tendency of many camera operators to move ever closer to the operative dissection itself.

In all laparoscopic cholecystectomies for acute cholecystitis, the surgeon should perform a “bile duct time out” to evaluate their understanding of targeted anatomy based on regional structures ( Box 113.1 ). After a wide laparoscopic view of the subhepatic space is obtained, the surgeon should lift the liver off the porta hepatis and identify a checklist of landmarks around the gallbladder, including duodenum, sulcus of Rouvier, umbilical fissure, pulsations of the common hepatic artery, and the bile duct itself. Once these landmarks are identified, a careful dissection of the triangle of Calot can be accomplished with minimal cautery. A specific search for a sectoral duct should also be completed. Then with a cleared triangle and the true gallbladder cystic duct angle identified, the correct “cognitive map” of the biliary tree can be superimposed on the patient's specific anatomy in the correct location. In cases of severe acute cholecystitis, it may be unclear if the operator can safely even obtain this anatomic viewpoint (and therefore the ability to safely proceed with a laparoscopic technique). In most scenarios, however, if the surgeon can still obtain a clear dissection of the junction between the cystic duct and the gallbladder on the lateral edge, then it is safe to continue. Initial dissection in the lateral tissues for cases of a severely inflamed field is also safest from a bile duct injury point of view. If it is unsafe to proceed with further dissection medial to the gallbladder, however, a subtotal cholecystectomy may represent the best option. The gallbladder should be opened, all stones and debris extracted, and then closed using the surgeon's preferred minimally invasive modality (Endoloops, suturing, thick stapler) as low as is safe given the regional inflammation.

Box 113.1
Bile Duct “Time Out” (B.E. S.A.F.E.)

  • B—Bile duct

  • E—Enteric (duodenum) position

  • S—Sulcus of Rouvier

  • A—Artery (hepatic artery)

  • F—Fissure (umbilical fissure)

  • E—Environment (back the camera out for improved perspective)

During the entire operation, a surgeon must maintain a vigilant attitude, and when ambiguity arises, must slow down and back out the camera to widen the view of all landmarks (complete another “bile duct time out”). The surgeon must avoid both physical and mental “tunnel vision.” Inability to accurately place the cognitive map is a stop signal. If this cannot be resolved, conversion to open surgery with top down dissection will improve safety. For patients with inflammatory obliteration of the triangle of Calot, near-total cholecystectomy or cholecystostomy can prevent injury. Furthermore, any dissection on the left side of the bile duct should be considered a “near miss.” Surgeons must also have several “cognitive maps” in their minds—normal, caudal sectoral duct, and short cystic duct. The maps must be somewhat “plastic” as size and distances vary with each patient.

Vasculobiliary Injuries

The importance of ischemia of the bile duct in the formation of postoperative strictures is significant. Injury to the hepatic artery at the time of biliary injury during laparoscopic cholecystectomy has been recognized at an increased incidence, as high as 50%, when investigated at the time of presentation. The true impact of an arterial injury, however, remains debated. It is clear that the most common site of vasculobiliary injury is the right hepatic artery ( Fig. 113.3 ). Damage to this vessel may lead to a higher injury level on the bile duct than the initial grossly observed mechanical trauma. As a result, concurrent injury to the right hepatic artery may prompt the surgeon to delay biliary reconstruction for a later date to allow the level of the final injury to become more apparent upon exploration. Similarly, trauma to the right hepatic artery is also a significantly larger problem in the context of higher biliary injuries. More specifically, disruption of the crossing arterial plexus at the hilar bifurcation remains a more challenging reconstruction issue worthy of thoughtful consideration. Vasculobiliary injuries may also have specific effects on the arteries (pseudoaneurysm with delayed hemorrhage), bile ducts (necrosis, stenosis, cholangitis), and/or liver (necrosis, atrophy) over variable lengths of time. Concurrent hepatic artery and portal vein injuries can have catastrophic effects on the liver, including rapid necrosis, potentially requiring urgent liver transplant. Finally, a clinically important and a more common cause of bile duct ischemia is excessive dissection around the bile duct during bile duct anastomosis for repair of an injury, which can divide or injure the major arteries of the bile duct that run in the 3-o'clock and 9-o'clock positions.

FIGURE 113.3, Hannover bile duct injury classification scheme. (A) Type A, peripheral bile leak. (B) Type B, bile duct obstruction. (C) Type C, tangential bile duct injury. (D) Type D, transected bile duct. (E) Type E, late bile duct stenosis. Vascular injury modifiers include right hepatic artery (d), left hepatic artery (s), proper hepatic artery (p), common hepatic artery (com), cystic artery (c), and portal vein (pv).

Another important factor contributing to the formation of biliary strictures is the intense connective tissue response with fibrosis and scarring that can occur after bile duct injury. Experimental studies of bile duct ligation in a canine model have demonstrated immediate and sustained elevation of bile duct pressure and progressive increase in bile duct diameter. Histologic changes at 1 month after ligation have shown that the bile duct wall is thickened, with a reduction of mucosal folds and loss of surface microvilli, associated with a well-defined epithelial degeneration. Biochemical analysis of connective tissue response to ligation showed that collagen synthesis and proline hydroxylase activity are increased within 2 weeks in the obstructed bile duct and are sustained throughout the period of observation. Finally, a marked local inflammatory response can develop in the adjacent tissue in association with bile leakage, which occurs with many bile duct injuries. This inflammation can be further intensified in the face of infection. This inflammation results in fibrosis and scarring in the periductal tissue, further contributing to stricture formation. These factors can be of major importance in bile duct injuries during laparoscopic cholecystectomy, which are frequently associated with bile leaks.

After cholecystectomy and common bile duct exploration, the two most common operations associated with bile duct injury are gastrectomy and hepatic resection. The typical situation resulting in bile duct injury during gastrectomy involves dissection of the pyloric region and the first portion of the duodenum. 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 during dissection of the hepatic hilum.

Unfortunately, the recurrence of bile duct strictures after an initial attempt at repair is not uncommon and can also account for a number of anastomotic strictures. A number of factors have been evaluated in patients who have a recurrent bile duct stricture, including the location of the stricture, 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. Previous attempts at repair, performance of a procedure other than choledochojejunostomy or hepaticojejunostomy, and stricture location higher in the biliary tree appear to be associated with a higher incidence of recurrent stricture. Finally, long-term follow-up of a bile duct anastomosis is important because strictures can develop years after the original anastomosis.

Clinical Presentation of Patients With Bile Duct Injuries

Most patients with biliary injuries present early after their initial operation. After open cholecystectomy, only approximately 10% of postoperative strictures are actually suspected within the first week, but nearly 70% are diagnosed within the first 6 months, and more than 80% are diagnosed within 1 year of surgery. In series reporting bile duct injuries during laparoscopic cholecystectomy, the injury is usually recognized either during the procedure (25% to 30%) or, more commonly, in the early postoperative period.

Patients suspected of having a postoperative bile duct injury within days to weeks of initial operation usually present in one of two ways. One presentation is the progressive elevation of liver function test results, particularly total bilirubin and alkaline phosphatase levels. These changes can often be seen as early as the second or third postoperative day. The second mode of early presentation is with leakage of bile from the injured bile duct. This presentation appears to occur most often in patients presenting with bile duct injuries after laparoscopic cholecystectomy. Bilious drainage from operatively placed drains or through the wound after cholecystectomy is abnormal and represents some form of biliary injury. In patients without drains (including patients in whom the drains have been removed), the bile can leak freely into the peritoneal cavity or it can loculate as a collection. Free accumulation of bile into the peritoneal cavity results in either biliary ascites or bile peritonitis. Similarly, a loculated bile collection can result in sterile biloma or in an infected subhepatic or subdiaphragmatic abscess.

Patients with postoperative bile duct strictures who present months to years after the initial operation frequently have evidence of cholangitis. The episodes of cholangitis are often mild and respond to antibiotic therapy. Repetitive episodes usually occur before the definitive diagnosis. Less commonly, patients may present with painless jaundice and no evidence of sepsis. Finally, patients with markedly delayed diagnoses may present with advanced biliary cirrhosis and its complications.

Diagnostic Recognition and Evaluation—Laboratory Tests

Liver function tests usually show evidence of cholestasis. In patients with bile leakage, the bilirubin can be normal or minimally elevated because of absorption from the peritoneal cavity. When elevated, serum bilirubin usually ranges from 2 to 6 mg/dL, although it can rise higher in the context of delayed recognition. Serum alkaline phosphatase is also usually elevated. Serum aminotransferase levels can be normal or minimally elevated except during episodes of cholangitis. If advanced liver disease exists, hepatic synthetic function can be impaired, with lowered serum albumin and a prolongation of prothrombin time. Serum electrolytes and complete blood count are typically normal unless there is associated biliary sepsis.

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