7 Procedures for Benign and Malignant Biliary Tract Disease

Susan Logan, MD, MPP, and David Linehan, MD, FACS

Over the past several decades, advances in imaging technology have been made that allow more accurate diagnosis of biliary tract diseases and better planning of surgical procedures and other interventions aimed at managing these conditions. Operative techniques have also improved as a result of a better understanding of biliary and hepatic anatomy and physiology. The role of endoscopists and interventional radiologists in the management of benign conditions, as well as palliation of malignant disease, is also expanding. Accordingly, biliary tract surgery, like many other areas of modern surgery, is constantly changing.

In this chapter, we describe common operations performed to treat diseases of the biliary tract, emphasizing details of operative planning and intraoperative technique and suggesting specific strategies for preventing common problems. Complex biliary tract procedures should be performed only in specialized centers where experienced multidisciplinary teams, including hepatobiliary surgeons, endoscopists, interventional radiologists, and intensivists, collaborate to manage the special problems and requirements of patients undergoing such procedures.

Preoperative Evaluation

anatomy

Before embarking on any operation on the biliary tract, the surgeon must accurately define the relevant anatomy and extent of disease. Familiarity with the numerous variations of ductal anatomy is crucial [see Figure 1a]. In the prevailing pattern, the segment 6 and 7 ducts coalesce to form the right posterior sectional bile duct, and the segment 5 and 8 ducts join to form the right anterior sectional duct. The right anterior duct is usually oriented vertically, whereas the right posterior duct tends to follow a more horizontal course. The right anterior and posterior sectional ducts unite to form the right hepatic duct. Note that the posterior sectional duct crosses in front of the right anterior portal vein before joining the right anterior bile duct (Hjortsjo crook) [see Figure 1b]. Division of the right anterior portal pedicle too close to its origin may result in injury to the right posterior bile duct. The right hepatic duct runs a short extrahepatic course before joining the left hepatic duct at the hepatic confluence, forming the common hepatic duct. Similarly, in the prevailing pattern, the ducts draining segments 2 and 3 join to form the left lateral sectional duct. This duct then crosses behind the ascending portion of the left portal vein and joins the duct from segment 4 (also called the medial sectional bile duct) to form the left hepatic duct. The left hepatic duct runs a longer, usually horizontal, extrahepatic course at the base of segment 4b.

The above description is of the prevailing pattern of biliary anatomy, but the surgeon must be aware of several common variations, particularly those involving the right-sided ducts [see Figure 1c]. Not infrequently, one of the right sectional ducts crosses the midplane of the liver to drain directly into the left hepatic duct. If this variation is present and the surgeon performs a standard left hepatectomy, the right-sided duct(s) may be injured. The segment 8 duct may also drain into the posterior sectional duct. Other important variations include a low insertion of the right hepatic duct or an anomalous low insertion of a right sectional, segmental, or subsegmental duct directly into the common hepatic duct, the common bile duct, or even the cystic duct. Variations to the left ductal system most frequently involve variable numbers and sites of insertion of the segment 4 duct(s). Rarely, the segment 4 duct(s) may drain directly into the common hepatic duct or confluence.1,2

Finally, familiarity with the plate-sheath system is essential to performing safe dissection at the hepatic hilum [see Figure 1d]. This system is composed of four thick, fibrous plates— hilar, umbilical, cystic, and arantian—of which the hilar plate is most important to the liver surgeon. The hilar plate lies mainly in the coronal plane, at the base of segment 4 and posterior to the vasculobiliary structures in the porta. Superiorly, however, the hilar plate curves anteriorly, along the posterior aspect of the quadrate lobe, and here it is superior to all structures in the porta hepatis, including the right and left bile ducts. As the three vasculobiliary structures pass through the hilar plate, they are “sheathed” within the same fibrous tissue and become a single unit above the plate. Identification of these structures as a single unit above the hilar plate is much simpler and safer than individually isolating each structure lower in the porta hepatis. To gain access to these sheathed pedicles above the hilar plate, the surgeon must dissect the upper border of the hilar plate away from the liver, a technique referred to as “lowering the hilar plate.”3

imaging studies

High-quality ultrasonography is useful for confirming the presence of biliary dilatation, and duplex ultrasonography is excellent for assessing vascular involvement. However, ultrasonography is very user dependent and, even in experienced hands, is less helpful for determining resectability or the level or cause of obstruction. Multidetector computed tomography (MDCT) is noninvasive and provides excellent information regarding mass lesions, the presence or absence of ductal dilatation, the extent and level of duct obstruction, and the extent of vessel involvement. Multiphase computed tomography (CT) generates precise and reliable images of the relevant arterial, portal, and venous anatomy. Therefore, conventional


Figure 1. Common Pattern of Bile Duct Anatomy
angiography is no longer used to determine resectability. Magnetic resonance imaging (MRI) and magnetic resonance cholangiopancreatography (MRCP) can provide detailed images of biliary anatomy and have reported accuracy rates of 100% and 95%, respectively, for determining the location and cause of biliary obstruction. Direct cholangiography— percutaneous transhepatic cholangiography (PTC) and endoscopic retrograde cholangiopancreatography (ERCP)—may supply additional information about ductal anatomy, is useful for providing tissue (e.g., brush cytology) for diagnosis, and allows drainage of the biliary tree prior to operation. When major liver resection is anticipated, liver volumetric analysis using three-dimensional reconstruction of axial CT images should also be performed to confirm adequate size of the future remnant liver.4

In the case of malignant diseases of the biliary tract, evidence of distant organ metastases remains a contraindication to operation. The resectability of locally advanced hilar cholangiocarcinoma depends on the extent of vasculobiliary involvement, the presence or absence of contralateral lobar atrophy, and the predicted size of the future remnant liver.5 Repair of biliary injuries should be deferred in the setting of cholangitis, intra-abdominal infection, and sepsis [see Repair of Biliary Injuries, below].

management of biliary obstruction

Jaundice by itself does not increase operative risk, and we do not routinely perform preoperative biliary drainage in all
patients with jaundice.6 However, long-standing biliary obstruction has secondary effects that may increase perioperative morbidity and mortality. In the presence of these secondary effects, we recommend elective preoperative biliary decompression.

Infection

Patients with cholangitis, whether spontaneous or induced by duct instrumentation (via PTC or ERCP), should be treated with biliary drainage and appropriate antibiotics until they are infection free. We recommend antibiotic treatment and postponement of operation for at least 3 to 4 weeks. Rarely, antibiotics and endoscopic or transhepatic drainage are not immediately effective, and patients with biliary tract infection (e.g., associated with choledocholithiasis) may require urgent surgical decompression. Broad-spectrum antibiotics, including coverage of anaerobic organisms, should be administered preoperatively.

Renal Dysfunction

The pathogenesis of renal failure in the setting of obstructive jaundice is multifactorial. Extracellular water depletion, increased plasma renin and aldosterone activity, a paradoxical increase in atrial natriuretic peptide, and myocardial dysfunction are all thought to contribute to renal insufficiency in jaundiced patients.7 Because the combination of a high bilirubin level and hypovolemia is a significant risk factor for acute renal failure, patients with biliary obstruction should be well hydrated before receiving intravenous contrast agents or
undergoing operative procedures. In patients with acute renal dysfunction secondary to biliary obstruction, decompression of the bile duct until renal function returns to normal is advisable before any major elective procedure for malignant disease.

Impaired Immunologic Function and Malnutrition

In patients with long-standing biliary obstruction, absence of bile salts in the gut lumen may lead to severe malnutrition and contribute to impaired immune function.8 Decompression of the bile duct until immune function and nutritional status are restored to normal is indicated before any major elective procedure is undertaken. This may take as long as 4 to 6 weeks.

Coagulation Dysfunction

Prolonged bile duct obstruction may lead to significant deficits in vitamin K–dependent clotting factors. These deficits should be corrected with fresh frozen plasma and vitamin K before an operative procedure is begun. Even if there is no measurable coagulation dysfunction, vitamin K should be given to all patients with obstructive jaundice at least 24 hours before operation to replenish their depleted vitamin K stores.

Projected Major Liver Resection

If resection of an obstructing bile duct tumor is likely to necessitate major liver resection (e.g., a right trisectionectomy), we recommend unilateral decompression of the liver segments that are to be retained. Unilateral drainage is usually sufficient to normalize serum bilirubin and allows atrophy of the undrained segments to occur, along with concomitant hypertrophy of the future liver remnant.

Operative Planning

general technical considerations

Place the patient in the supine position on an operating table that can be rotated, tilted, and elevated. Equipment for fluoroscopy, intraoperative ultrasonography and choledochoscopy should be available during major resections. Access to a pathology department that can perform cytologic or frozen-section examination of tissue is essential in operations for malignant disease.

A right subcostal incision with vertical midline extension provides excellent exposure for most open procedures on the liver and biliary tract. For more extensive resections or reconstructions, the right subcostal incision can be extended laterally below the costal margin and across the midline to the left as a chevron incision. A vertical midline incision may give sufficient exposure in very thin persons. In any case, the incision must be long enough to allow sufficient visualization and as much mobilization of the liver as is necessary for safe performance of the procedure.

Adequate exposure and lighting are essential. The best retractors are those that can be fixed to the table while remaining flexible in terms of placement and angles of retraction. Retractor blades should be positioned to lift the ribcage anteriorly and cephalad and to pull the right abdominal wall laterally.

Locating the hepatoduodenal ligament and dissecting the structures in the porta hepatis are straightforward in patients who have never had an abdominal operation. However, in patients who have undergone previous operations, there may be considerable obliteration of planes. The following are suggestions for gaining access to the subhepatic space in patients who have had previous abdominal procedures:

  1. Use the falciform ligament as a landmark. In reoperative surgery, the key to opening up the upper abdomen is the falciform ligament. This structure should be found immediately after the opening of the abdominal wall and retracted superiorly. The omentum, the colon, and the stomach are then dissected inferiorly, and a plane that leads to the hepatoduodenal ligament and the porta hepatis is thereby opened.

  2. Take the right posterolateral approach. [see video 1] When the colon and the duodenum are densely adhesed to the undersurface of the right liver, separation may be difficult. In most patients, an open space remains that can be approached by sliding the left hand posteriorly to the right of these adhesions and into the (usually open) subhepatic space in front of the kidney and behind the adhesions. Anterior retraction allows identification of the adherent structures by palpation and permits dissection of the adhesions in a lateral-to-medial direction. The undersurface of the liver is thus cleared, and the hepatoduodenal ligament can be approached.

  3. Take the lesser sac approach. Ordinarily, the foramen of Winslow is open, and the left index finger can be passed through it from the right subhepatic space. When the foramen of Winslow is obliterated, however, one should approach it from the left, dividing the lesser omentum and passing an index finger from the lesser sac behind the hepatoduodenal ligament to reopen the foramen of Winslow by blunt dissection.

For a discussion of techniques to aid in the safe exposure of the porta hepatis in patients who have sustained a bile duct injury or have had previous biliary operations, refer to the section below on repair of biliary injuries: exposure of the porta hepatis.

General Guidelines for Biliary Anastomoses

As a rule, biliary anastomoses, whether of duct to bowel or of duct to duct, heal very well provided that the surgeon adheres to the following principles: (1) preservation of adequate blood supply, (2) avoidance of tension, (3) accurate placement of sutures with mucosa-to-mucosa apposition, and (4) construction of anastomoses of adequate caliber. In preparing the bile duct for anastomosis, it is essential to define adequate margins while avoiding excessive dissection that might compromise the blood supply to the duct. In repairs that follow acute injuries, it is important to resect crushed or devascularized tissue; however, in late repairs, it is not necessary to resect all scar tissue as long as an adequate opening can be made in the proximal obstructed duct through normal healthy tissue and as long as mucosa, rather than granulation tissue, is present at the duct margin. The length of the corresponding opening in the jejunal loop should be significantly smaller than the bile duct opening because the bowel opening tends to enlarge during the procedure.

Certain principles of suture placement apply to all biliary anastomoses. Mucosa-to-mucosa apposition is essential for good healing and the prevention of late stricture.9 Sutures should be of an absorbable, synthetic monofilament material and should be as fine as is practical (e.g., 5-0 for a normal duct and 4-0 for a thickened duct). Because the bile duct wall has only one layer, biliary anastomoses should all be single layer. Sutures should pass through all layers of the bowel, taking sizable bites of the seromuscular layer and much smaller bites of the mucosa, and should take moderate-sized (1 to 3 mm, depending on duct diameter) bites in the bile duct. Interrupted sutures are used when access is difficult or the duct is small; continuous sutures are used when access is easy and the duct is larger. Sutures should be securely placed but should not be so tight as to injure the tissues. Magnification with loupes is useful when anastomosing small ducts. With the exception of repair of high, complex bile duct injuries, we do not routinely place stents for biliary anastomoses. Some studies suggest that placement of drains is not necessary after biliary operations.10,11 Nevertheless, it is currently our practice to place a drain at the time of the operation and to remove the drain within 2 to 3 days if the output does not show evidence of a bile leak.

When the bile duct opening has a vertical configuration (as in side-to-side choledochoduodenostomy or choledochojejunostomy), we place stay sutures inferiorly and superiorly in the duct and at corresponding points in the intestine. Traction is placed on these sutures to line up the adjacent walls. One side of the anastomosis is done first; the bowel is then rotated 180°, and the other side is completed [see Figure 2]. This maneuver may be facilitated by retracting the first interrupted posterior stitch to the opposite side to serve as a pivotal stitch. We recommend sewing about two thirds of the first wall and two thirds of the second, leaving the anterior third of the circumference (the easiest part) to be closed last. For end-to-side choledochojejunostomy, or when the bile duct opening lies transversely, as in bifurcation reconstruction, lateral stay sutures are placed first, and the posterior wall stitches are placed from inside the lumen. If interrupted sutures are used, they are all placed individually before any of them are tied, with the untied tails carefully clamped and arranged in order. When the posterior wall sutures have been tied, the anterior wall can then be sutured with either continuous or interrupted sutures [see Figure 3].

When the intended anastomosis will be to a very smallcaliber or intrahepatic duct, and access is particularly difficult because of some combination of an unfavorable position, a previous scar, or a stiff liver that is difficult to retract, another technique may be useful. Beginning left to right, place all of the anterior wall stitches (inside to outside) into the duct. Clamp each suture and place them in order on a single retracting forceps with the needles left attached. Retract the sutures superiorly to expose the posterior wall of the duct [see Figure 3c]. Again, working left to right, place the posterior stitches inside to outside through the bowel wall and outside to inside into the duct. Remove the needles at the completion of each stitch, clamp each suture, and keep them in order as described for the anterior row. When all of the posterior stitches have been placed, carefully appose the bowel wall to the bile duct, tie all but the two corner stitches in order, and
cut the sutures. Leaving the corner stitches (at 3 and 9 o’clock) loose facilitates accurate placement of the lateral and medial stitches of the anterior wall. Finally, place the anterior wall stitches inside to outside on the bowel, sequentially clamp the stitches until the last stitch is placed, and then tie the stitches in order and cut the sutures.9

When the duct is very small, three additional techniques may be useful for increasing the size of the lumen:

  1. An anterior longitudinal incision can be made in a small common bile duct (CBD) and the sharp corners trimmed to enlarge the opening [see Figure 4a].

  2. If the cystic duct is present alongside a divided CBD, an incision can be made in the shared wall to create a single larger lumen [see Figure 4b].

  3. If the bifurcation has been resected, two small ducts can be brought together and sutures placed into their adjoining walls to form a single larger lumen as long as the space between the ducts is small and the ducts can be brought together without tension [see Figure 4c]. If the ducts cannot be brought together without tension, more than one anastomosis must be created.

Construction of a Roux Loop

When the jejunum is used for long-term biliary drainage, we prefer a 60 cm Roux loop to prevent reflux of small bowel contents into the biliary system. In the creation of the loop, it is important to select a segment of jejunum with a welldefined vascular arcade that will be long enough to support a tension-free anastomosis. If access to the biliary system will be required in the future (e.g., in an operation for recurrent intrahepatic stones), the loop should be long enough to allow one to place a tube jejunostomy, fixing the loop to the abdominal wall with nonabsorbable sutures. The site of attachment should be marked with metallic clips to facilitate future percutaneous puncture, cannulation, and removal of recurrent or persistent stones. The tube can be removed after postoperative imaging studies confirm that the biliary tree is free of stones.

Choledochoduodenostomy

Choledochoduodenostomy is a relatively straightforward end-to-side (or sometimes side-to-side) biliary-enteric bypass procedure that is useful in certain restricted circumstances. It is most commonly used in patients with multiple bile duct stones when there is concern about leaving residual stones at the time of CBD exploration, as well as in patients with recurrent bile duct stones when endoscopic papillotomy either cannot be done or has been unsuccessful. Choledochoduodenostomy has the advantage of being simpler and safer than transduodenal sphincteroplasty. It is also used in patients with benign distal biliary obstruction (e.g., from chronic pancreatitis or a very low bile duct injury) and occasionally in patients with malignant distal CBD obstruction whose life expectancy is limited. Choledochoduodenostomy works best if the CBD is at least 1 cm in diameter.

contraindications

Choledochoduodenostomy should not be used in patients with actual or potential duodenal obstruction.


Figure 2. Side-To-Side Choledochojejunostomy

operative technique

Mobilize the duodenum to allow approximation to the CBD without tension. Ordinarily, the first part of the duodenum can easily be rolled up against the CBD; however, in patients who have chronic pancreatitis or have previously undergone an abdominal procedure, extensive kocherization may be required. If satisfactory approximation is not achieved with this maneuver, a choledochojejunostomy should be performed instead.

Expose the CBD as described elsewhere. Make longitudinal incisions in both the duodenum and the duct [see Figure 2] and create the anastomosis as described previously [see Operative Planning, General Technical Considerations, General Guidelines for Biliary Anastomoses, above].

complications

Late closure or stricture of the anastomosis may occur if the CBD is small, has inadequate blood supply, or malignant
disease is present. Consider alternative methods of biliary decompression in these situations.

Cholangitis related to the presence of food in the CBD distal to the anastomosis (so-called sump syndrome) is an uncommon occurrence. The larger the anastomosis, the smaller is the likelihood that this complication will occur.

Cholecystojejunostomy

Cholecystojejunostomy may be performed to treat malignant biliary obstruction in selected patients whose lesions are found to be unresectable at operation and whose life expectancy is short.

contraindications

Absolute contraindications to this drainage procedure include obstruction above the cystic duct entry point, evidence of cholecystitis, and benign causes of biliary

Figure 3. End-To-Side Choledochojejunostomy
obstruction (i.e., patients with normal life expectancy). This operation is not the preferred procedure for long-term decompression.

operative technique

Step 1: Verification of Feasibility of Procedure

The cystic duct must be patent. Its junction with the CBD must be at least 1 cm above the tumor obstruction [see Figure 5].
The suitability of the anatomy for cholecystojejunostomy should have been verified by preoperative cholangiography; if not, intraoperative cholangiography via the gallbladder or the CBD is mandatory. If one still cannot be certain that the operation is feasible, the CBD should be opened and a choledochoenterostomy performed. The finding of a bile-filled gallbladder is not sufficient evidence that the patient is a suitable candidate for a cholecystojejunostomy. The gallbladder must be normal: there should be no evidence of cholecystitis or stones. Verify normal status by inspection, palpation, and, if necessary, needle cholecystography.

Step 2:Preparation for Anastomosis

Select a site near the fundus for the anastomosis and anchor an appropriate, tension-free segment of proximal jejunum to the gallbladder with two fine stay sutures. Between the two stay sutures, make a 2 cm transverse opening in the gallbladder and a corresponding longitudinal incision in the antimesenteric border of the bowel.

Step 3: Anastomosis

Create a single-layer anastomosis using a continuous monofilament absorbable suture or a stapler.

complications

Bile leakage may occur if there is excessive tension on the anastomosis. In addition, jaundice may persist if there is unrecognized cystic duct obstruction resulting from inflammation or an unnoticed stone in the cystic duct or the gallbladder. Recurrent jaundice is usually the result of extension from an obstructing tumor that has involved the cystic duct–CBD junction.

Choledochojejunostomy

Choledochojejunostomy, one of the most commonly performed biliary tract procedures, is done to provide biliary drainage after CBD resection, repair of ductal injury, or relief of obstruction caused by a benign or malignant stricture. To reduce the likelihood of reflux of intestinal contents into the biliary tract, we prefer to use a 60 cm Roux-en-Y jejunal limb for the anastomosis [seeOperative Planning, General Technical Considerations, Construction of a Roux Loop, above].

When the operation is performed after CBD resection, an end-to-side choledochojejunostomy using the proximal transected duct is preferred as long as adequate vascularization of the transected bile duct is confirmed. When the operation is performed for bile duct obstruction resulting from tumor or stricture and no resection has been performed, a side-to-side anastomosis [see video 3] is constructed.

operative technique

Step 1: Preparation for Anastomosis

Preparation for an end-to-side anastomosis includes resection of any crushed or devitalized bile duct tissue. The CBD should be trimmed back to healthy, viable, bleeding duct wall.

If a side-to-side anastomosis is being performed for stricture or tumor, the proximal duct is almost always dilated and

Figure 4. Three Methods of Enlarging a Small Duct
has thicker walls, facilitating a vertical incision on the anterior surface. When the procedure is being done for malignant disease, the incision should be made as high as possible above the malignancy to delay the eventual obstruction of the anastomosis by tumor growth.

Step 2: Anastomosis

When the duct is large, a secure, tension-free anastomosis is easily constructed by means of the techniques previously illustrated. When the duct is small, extra effort must be made to place sutures carefully to prevent narrowing of the lumen.

troubleshooting

Injured ducts must be adequately débrided, even if this means extending the resection of the duct to the bifurcation. However, preservation of the blood supply to the CBD is essential. Avoid extensive mobilization of the duct from the surrounding tissues to prevent injury to the ductal blood supply. [see video 2] Finally, longitudinal incisions should not be made in the medial or lateral (3 and 9 o’clock) portions of the CBD, where the major longitudinal blood supply is located.

Meticulous surgical technique is critical for ensuring good healing and preventing stricture. Use the finest suture material that will do the job and employ magnifying devices to facilitate accurate placement of sutures. Routine postoperative stenting is unnecessary, but stents may be helpful in those very rare cases in which mucosal apposition cannot be accomplished. In these situations, sutures may have to be placed in surrounding liver or scar tissue in much the same way as in a Kasai procedure.12 In difficult cases of proximal
stricture, the surgeon may be forced to incise and lower the liver plate and seek out viable intrahepatic ducts for anastomosis [see Repair of Biliary Injuries, below].

complications

The main complications of a choledochojejunostomy are bile leakage, late stricture, and recurrent jaundice as a result of tumor extension [see CholecystojejunostomyandCholedochoduodenostomy, above].

Choledochal Cyst Resection

Choledochal cysts are generally categorized according to the Todani classification [see Figure 6]. More than 80% are type I cysts that involve the CBD in its accessible portion. The following discussion addresses the resection of type I cysts and those type IV cysts that include the proximal right or left hepatic ducts.

Most choledochal cysts are associated with an abnormal junction of the pancreatic duct and the distal CBD. Preoperative cholangiography to clarify the anatomy is important for preventing injury to the pancreatic duct, especially when an intrapancreatic resection is required. Occasionally, intraoperative cholangiography is needed to clarify abnormal anatomy. Patients may be symptomatic as a result of stones within the cyst, infection, or malignancy, any of which is an indication for operation. The increased risk of bile duct malignancy associated with choledochal cysts, and the high mortality associated with cholangiocarcinoma, is justification for prophylactic cyst resection even in asymptomatic patients.


Figure 5. Cholecystojejunostomy

The objectives of treatment are (1) to remove the cyst completely, along with the gallbladder and any stones that remain in the bile ducts proximal to the cyst, and (2) to restore biliary-enteric drainage. Resection of a choledochal cyst may be made more difficult by several factors, such as previous operations, recurrent bouts of infection and inflammation in the cyst, and portal hypertension, which may develop as a result of long-standing cholangitis or portal vein thrombosis.13

operative technique

Resection of a choledochal cyst may be difficult, especially if inflammation is present. In addition, dissection of a choledochal cyst in its intrapancreatic portion is hazardous because of the vascularity of this region and the difficulty identifying anatomic structures.

Step 1: Clarification of Anatomy

The proximal and distal extent of the cyst and the presence or absence of stones or tumor may be determined preoperatively, as noted, but in many cases, intraoperative verification of the findings is necessary. Intraoperative cholangiography can be carried out by inserting a catheter through the gallbladder, by directly needling the cyst, or both. If cholangiography does not yield an accurate definition of the anatomy of the cyst, the cyst may then be opened anteriorly and digital exploration and choledochoscopy used to clarify the proximal and distal extent of the cyst.

Step 2: Mobilization of the gallbladder

If the gallbladder is still in place, dissect it free of the liver, leaving it attached to the cyst via the cystic duct, and retract the gallbladder to the right.

Step 3: Distal Dissection

Early distal division of the cyst facilitates the posterior dissection and allows mobilization of the duct to better define the proximal extent of the cyst. Dissect distally along the wall of the cyst until the junction of the cyst with the normal portion of the CBD is reached. If the intrapancreatic portion of the CBD is involved, the cyst must be separated from pancreatic tissue. A number of small vessels must be individually identified and ligated to minimize the risk of early or delayed bleeding. If the cyst is close to the pancreatic duct junction, one must exercise considerable care not to injure the pancreatic duct. Transect the distal bile duct. Place a clamp on the proximal cut end of the duct to assist with retraction and oversew the distal cut end using fine monofilament absorbable suture, being careful not to injure the pancreatic duct.

Step 4: Mobilization of Cyst

Vascularity in the region and the presence of inflammation may render dissection difficult. Rather than cleaning off the hepatic artery and the portal vein and dissecting them off the cyst, find a plane immediately adjacent to the wall of the

Figure 6. Choledochal Cyst Resection: Todani Classification
cyst and remain close to it [see Figure 7]. This approach differs significantly from the corresponding approach in resection of a bile duct malignancy [see Resection of Middle-Third and Proximal Bile Duct Tumors, Operative Technique, below]. If necessary, open the cyst with a vertical anterior cystotomy and continue the dissection with direct visualization of the inside of the cyst to yield a more accurate definition of its boundaries. Clear the cyst circumferentially, separating the cyst from the hepatic artery, the portal vein, and any remaining soft tissue in the hepatoduodenal ligament.

Step 5: Proximal Dissection

If the proximal common hepatic duct is normal (as in a type I cyst), transect the duct above the cyst. If the cystic dilatation includes the bifurcation (as in a type IVa cyst), a small button of proximal cyst is usually left attached to the intrahepatic ducts [see Figure 8].

Step 6: Reconstruction

Reconstruction is accomplished via an end-to-side anastomosis to a Roux jejunal loop to minimize the likelihood of reflux of enteric contents into the biliary tract. Stenting is not required, but we recommend draining the area with closed suction drains, especially if an intrapancreatic resection has been done.


Figure 7. Choledochal Cyst Resection: Plane of Dissection

Figure 8. Choledochal Cyst Resection: Past the Bifurcation

troubleshooting

If dissection of the cyst is carried distally into the pancreas, care must be taken to keep from injuring the pancreatic duct. Transect the cyst as distally as possible and carefully oversew the end with absorbable sutures. Intraoperative cholangiography and/or preoperative MRCP are useful to confirm the relationship of the cyst and the CBD to the pancreatic duct.

If the cystic process extends to include the bifurcation (type IVa), the hepatic ducts should be identified from within the cyst and their orifices preserved by leaving a small button of cyst wall in situ; this is preferable to performing an intrahepatic dissection to remove the entire cyst. The presence of this button simplifies and facilitates the anastomosis to the Roux loop. Note that liver resection for choledochal cyst is rarely justified unless there is evidence of a solid mass or papillary excrescence emanating from the cyst mucosa.

complications

Bleeding and pancreatitis are the main early complications of cystectomy. These can be largely prevented by meticulous dissection and ligation of all fine bleeding vessels as well as tissue adjacent to an intrapancreatic cyst. Late stricture of the anastomosis is an uncommon complication but may occur, especially if a small button of proximal cyst is left in place for the anastomosis; this particular complication is considered an acceptable hazard in a difficult situation.

outcome evaluation

The immediate expected outcome is the relief of pain, jaundice, and cholangitis and the return of liver function to normal. The long-term expected outcome is the absence of
any recurrence of symptoms of stone disease, cholangitis, or malignancy. Because of the rarity of this condition, no good data on the recurrence rate of problems are available, but in our experience, the need for reintervention is rare.

Resection of Middle-Third and Proximal Bile Duct Tumors

The most common bile duct tumor is adenocarcinoma. Because this tumor responds poorly to irradiation and chemotherapy, surgical resection offers the best opportunity for cure. Unfortunately, many patients present with unresectable local disease and distant metastasis, and only palliative interventions are warranted. The appropriate operative approach depends on the location and extent of the tumor [see Figure 9]. Tumors in the distal third of the CBD (the pancreatic portion) are treated by means of a pancreaticoduodenectomy that includes bile duct and periductal tissues right up to the bifurcation. Those in the middle third or the proximal third are treated by means of bile duct resection, often with concurrent liver resection.

Certain basic principles underlying bile duct resection for tumor must be followed. First, the proximal extent of the tumor must be identified so that the correct procedure can be planned. Preoperative PTC is usually not required for staging if high-quality MRI and MRCP are available. With the exception of the clinical circumstances outlined previously [see Management of Biliary Obstruction, above], we do not routinely place preoperative biliary drainage tubes.

Second, given that bile duct tumors spread by local extension to lymphatics, along perineural spaces, and along the biliary radicles directly into the liver, wide local excision beyond the visible edges of the tumor is required in the performance of curative resections. In proximal tumors, such excision necessitates resection of the adjacent segments of the liver. The principles of en bloc resection beyond tumor margins must be closely adhered to: dissection into or even close to the tumor must be avoided.14

Third, intraoperative biopsy of the tumor is unreliable because of the difficulty of making a firm pathologic diagnosis on the basis of frozen-section examination.


Figure 9. Resection of Middle-Third and Proximal Bile Duct Tumors: Location

Finally, given that liver resection is required in most cases, one must be careful to preserve enough healthy liver tissue to allow regeneration of the remnant.15 If there has been long-standing obstruction, biliary drainage on the side to be preserved is important for recovery of function in that portion of the liver. Some surgeons advocate preoperative portal vein embolization on the contralateral side to stimulate hepatic regeneration in the segments to be preserved, especially if the future remnant is marginal in size. Often this is unnecessary, however, because of lobar atrophy attributable to ipsilateral portal vein involvement and compensatory contralateral hypertrophy.

On the whole, we are aggressive in treating proximal tumors for two main reasons: (1) the accompanying liver resection can now be done with low morbidity, and (2) this more radical approach has been shown to yield improved long-term results.5 For middle-third or type I proximal tumors, we favor resection of the bifurcation in conjunction with intrahepatic cholangiojejunostomy. For types II, III, and IV, we recommend additional liver resection: a right trisectionectomy (resection of segments 4, 5, 6, 7, and 8, along with the caudate lobe) for types II, IIIa, and IV and a formal left hepatectomy (resection of segments 1, 2, 3, and 4) for type IIIb. There is some controversy as to whether patients with these complex proximal biliary tumors have a better chance of long-term survival with liver transplantation than with radical resection because of the high incidence of positive microscopic margins. This controversy has yet to be resolved, but we prefer radical resection when feasible. Transplantation for hilar cholangiocarcinoma should be performed only in the context of an approved clinical trial.

operative technique

Step 1: Assessment of Resectability

Assessment of resectability begins with an evaluation of the patient’s fitness and exclusion of underlying liver disease (i.e., cirrhosis and portal hypertension). The next step is to confirm the radiographic appearance of resectability. Radiographic evidence of metastatic disease is an absolute contraindication to resection. In the absence of metastatic disease, the resectability of hilar cholangiocarcinoma is predicted by the extent of vasculobiliary involvement and the presence or absence of contralateral lobar atrophy. In general, if the tumor involves only the ipsilateral portal vein and/or bile ducts, it may be resectable; if the tumor involves the contralateral portal vein and/or contralateral secondary bile ducts, it is generally not resectable.5 Finally, if curative resection requires major hepatectomy, the future remnant liver must be of adequate size to prevent postoperative liver failure.

Before any dissection of the tumor or the CBD is done, conduct a careful search for peritoneal metastases. Evaluate spread within the liver by palpation. Palpate for suspicious lymph nodes in the immediate and secondary drainage areas. Biopsy any suspicious areas outside the planned resection margins and send this for frozen-section analysis. If the frozen section confirms that tumor is present outside the planned resection area, palliative stenting or a bypass procedure is indicated.

During dissection, determination of resectability is often difficult, especially with respect to assessment of tumor extension into the liver and the degree of vessel involvement. Therefore, the surgeon should defer any firm commitment to resection (e.g., dividing the blood supply) until resectability is confirmed.

Dissect the gallbladder off the gallbladder fossa, taking care to leave the cystic plate on the liver. The gallbladder can be left attached to the CBD and used as a retractor. Follow the cystic plate down to the hilar plate and lower the hilar plate by dividing its attachment to segment 4B all the way to the umbilical fissure. This allows palpation and inspection of the hilum to determine the extent of tumor involvement into the left and right hepatic ducts.

Dissection is then begun from below. Identify the common hepatic artery and the portal vein just above the neck of the pancreas and circumferentially clear these of all tissue. Continue the dissection proximally, retracting the hepatic artery to the left and the portal vein to the right. Adjacent areolar tissue, nerve trunks, and lymph nodes should be left in place around the CBD and the tumor [see Figure 10]. As noted, this approach differs from that used in resection of choledochal cysts [see Choledochal Cyst Resection, Operative Technique, above].

Step 2: Division of CBD

Once resectability is confirmed, divide the CBD at the level of the pancreas. Place a clamp on the end of the divided duct and use this as a retractor to facilitate the most proximal dissection of the CBD and the tumor away from the hepatic artery and the portal vein [see Figure 11].

Step 3: Proximal Dissection

With middle-third tumors or Bismuth type I proximal tumors, it is usually possible to palpate the proximal tumor margin and identify uninvolved right and left hepatic ducts. If this is not the case, the surgeon should consider the possibility of a type II or III tumor and be prepared to completely excise the bifurcation, with or without part of the liver.

Dissect the hepatic artery by retracting the vessel anteriorly and to the left, dividing and ligating the cystic artery where it originates from the right hepatic artery, and clearing all tissue off the right and left branches at least 1 cm proximal to the proximal margin of the tumor. Involvement of the right or left hepatic artery by tumor is a sign of extensive spread on the corresponding side and an indication for resection of that half of the liver.

Dissect the portal vein by retracting the bile duct and the tumor anteriorly and the hepatic artery to the left. All tissue should be cleanly dissected away from the portal vein to expose the bifurcation and the region proximal to it [see Figure 11]. At this point, the duct may be tethered down to the caudate lobe. Bile ducts from the caudate lobe may drain into the right or left duct and tumor may extend along these caudate ducts. Therefore, whether or not there is gross tumor in this area, the caudate lobe should be included in the resection.16

The level at which the proximal bile ducts are transected depends on the proximal extent of the tumor. For all middlethird or proximal tumors that are at least 1 cm beyond the bifurcation, proximal resection should be above the level of the bifurcation. For type I or type II proximal tumors, proximal resection should always include all of the bifurcation along with the proximal right and left bile ducts out as far as

Figure 10. Resection of Middle-Third and Proximal Bile Duct Tumors: Plane of Dissection
the first major branch [see Figure 12]. With type III or IV proximal tumors, the proximal extent of the tumor cannot be determined in both right and left ducts unless the main pedicles are dissected out of the liver. Because these tumors tend to infiltrate locally, such dissection is not advisable. Instead, concurrent hepatectomy should be performed to optimize the likelihood of curative resection. Intraoperative ultrasonography may help verify the extent of tumor at this point in the operation. Any major liver resection for type III

Figure 11. Resection of Middle-Third and Proximal Bile Duct Tumors: Resectability Confirmed
or IV bile duct cancer should include the caudate lobe [see Figure 13].

Before committing to a major hepatectomy (i.e., before dividing the blood supply), the tumor must be dissected away from the hepatic artery and portal vein branch supplying the segments of the liver to be preserved. Once this has been accomplished, the hepatic artery and the portal vein branch to the side to be resected can be divided. This allows the tumor to be retracted further and provides better exposure of the duct to the side to be preserved [see Figure 14 and Figure 15]. In selected cases, resection of an involved portal vein bifurcation may be carried out at this point [see Figure 16]; an end-to-end primary venorrhaphy (without the need for an interposition conduit) can usually be fashioned.


Figure 12. Resection of Middle-Third and Proximal Bile Duct Tumors: Level of Resection

Figure 13. Resection of Middle-Third and Proximal Bile Duct Tumors: Right and Left Hepatectomy

The point at which the hepatic parenchyma will be divided is marked, and the parenchymal transection is performed. Division of the hepatic duct (or ducts) to the part of the liver being preserved is done as far from the tumor as possible.

Step 4: Reconstruction

After resection of the bifurcation or intrahepatic bile ducts, an intrahepatic cholangiojejunostomy is performed. The duct tissue is usually healthy enough and the duct lumen large enough to allow mucosa-to-mucosa repair without stenting.

Step 5: Closure and Postoperative Care

Close the abdomen in the standard fashion and place closed suction drains. In the early postoperative period, particularly when a major liver resection has been performed, mild abnormalities in coagulation test results are common. In the absence of active bleeding or severe coagulopathy, we do not administer fresh frozen plasma. Drains are removed 2 to 3 days postoperatively if there is no evidence of a bile leak.

complications

Bile leakage, bleeding, and infection are the most important complications of bile duct resection for tumor. Following major hepatectomy, expect a transient rise in liver function
studies. A moderate increase in coagulation studies is also common, and we do not transfuse fresh frozen plasma for an international normalized ratio of 2.0 or less unless clinical bleeding is evident. Nevertheless, these laboratory values should be monitored closely in the early postoperative period as persistent elevation of liver function tests or coagulation studies is an indication of hepatic insufficiency. Parahepatic collections are treated with percutaneous drainage, and significant early postoperative bleeding is usually best managed by reexploration.

Repair of Biliary Injuries

Biliary injuries during laparoscopic cholecystectomy are estimated to occur in only 0.4 to 0.6% of cases, but with approximately 500,000 procedures yearly in the United States, this seemingly low injury rate translates into significantly increased cost, resource use, morbidity, and mortality.17–21 In as many as 50% of cases, the injury may be discovered at the time of operation, and depending on the type of injury, the surgeon may attempt an immediate repair.22,23 General surgeons who perform laparoscopic cholecystectomies should be adequately trained to repair Strasberg type A and D injuries [see Figure 17]. Strasberg type A injuries include cystic duct stump leaks or leakage from small ducts in the liver bed (e.g., duct of Luschka). If a type A injury is detected during laparoscopic cholecystectomy, oversew the offending duct (laparoscopically or open) and place a drain. A type D injury is a lateral injury to a major duct. One may safely perform a primary repair of the duct at the time of operation under the following conditions: (1) less than 25% of the circumference of the duct is involved, (2) the injury is not thermal (i.e., from a cautery burn), and (3) the duct is of sufficient caliber to allow insertion of a T tube. Place a T tube across the injury (via a separate incision in the duct) and perform a primary repair using fine absorbable monofilament suture. If any one of the above conditions is absent, the surgeon should instead perform a choledochojejunostomy as previously described or refer the patient to a hepatobiliary surgeon if necessary. Type B injuries usually involve ligation of an aberrant right hepatic duct and are rarely detected at the time of surgery. Type C injuries involve transection, but not ligation, of an aberrant (usually right hepatic) duct. If discovered at the time of operation, such injuries are best repaired immediately with cholangiojejunostomy. Strasberg type E injuries parallel the Bismuth classification system of biliary strictures. These injuries occur higher on the biliary tree, may be very complex, and are often accompanied by a vascular component. When such injuries are noted at the time of cholecystectomy, the surgeon must honestly assess his or her expertise in the repair of complex biliary injuries and do nothing that might worsen the injury. In general, this means that once any hemorrhage is carefully controlled, a drain should be placed, the wound should be closed, and the patient should be transferred without delay to the nearest specialty center with provider teams experienced in the management of complex biliary injuries.24

Injuries not discovered at the time of initial operation may present days, weeks, or even years later.25,26 Signs and symptoms of delayed presentation vary depending on the nature of the injury and whether obstruction or bile leakage

Figure 14. Resection of Middle-Third and Proximal Bile Duct Tumors: Type IIIb
is the dominant pathology at the time. Persistent but usually mild, unexplained pain and malaise in the postoperative period are the most common initial symptoms, and the nonspecific nature of these symptoms may lead to further delay in diagnosis.27 Patients may also present with nausea, anorexia, elevated white blood cell count and liver function studies, fever, jaundice, cholangitis, or sepsis. Initial management depends on the clinical state of the patient. Correct any fluid and electrolyte derangements, administer appropriate analgesia to control the pain associated with bile peritonitis, and initiate broad-spectrum antibiotic coverage in any patient with infection. High-quality cross-sectional imaging—multiphase CT, MRI/MRCP, or both—is essential to evaluate the extent of injury and detect abdominal fluid collections or major vascular injury. Patients with signs or symptoms of cholangitis or sepsis should undergo percutaneous drainage of any biloma or abscess seen on imaging, followed by PTC with placement of an external biliary drainage catheter (or bilateral catheters for type E4injuries). No attempt should be made to internalize the biliary drainage catheter(s) until the patient becomes clinically stable.28 Stable patients with jaundice and/or biloma may also undergo ERCP, and if a type A injury is clearly demonstrated, then drainage of the biloma and temporary biliary stenting until the leak ceases will usually solve the problem. To adequately define anatomy and plan repair of most other injuries, specifically those
involving excluded ducts, requires imaging of both the upper and lower bile ducts with both ERCP and PTC. Failure to adequately define the biliary anatomy and extent of injury by cholangiography predicts eventual failure of any repair.24 Although there is no level 1 evidence to guide the timing of repair, we generally complete the necessary perioperative imaging studies and repair injuries within 24 hours of transfer under the following conditions: (1) the transfer occurs within 0 to 3 days of the injury, (2) peritoneal contamination is minimal and well drained, (3) the patient has no signs or symptoms of cholangitis or sepsis, and (4) there is no radiographic evidence of major vascular injury. Patients with bile peritonitis, abscesses, and cholangitis are managed as described above, and definitive repair is delayed for at least 3 months. Likewise, repair is delayed 3 months in patients with major vascular injuries to better establish the level of associated ductal ischemia and resulting stricture.

operative technique

Step 1: Exposure of the Porta Hepatis

In patients who have sustained a biliary injury, particularly those who have already undergone attempted repair, local inflammation may obliterate the normal tissue planes and lead to significant distortions of the normal portal anatomy. The following are some useful techniques for safely

Figure 15. Resection of Middle-Third and Proximal Bile Duct Tumors: Type II, IIIa, IV
defining the anatomy and avoiding potentially devascularizing dissection within the porta hepatis.
  1. Use the round ligament to find the true porta hepatis. Patients who have already undergone one or more operations on the bile duct often have adhesions between the hepatoduodenal ligament and segment 4 of the liver. If one dissects this area via the anterior approach, one may think that the actual porta hepatis has been reached but notice that the hepatoduodenal ligament appears unusually short. In most cases, one can safely find the true porta by tracing the round ligament to the point where it joins the left portal pedicle and the umbilical portion (or ascending branch) of the left portal vein. To completely expose the umbilical fissure, the bridge of liver tissue between segment 4b and the left lateral section must first be divided. This tissue is devoid of any major vascular or biliary structures and may be safely divided with electrocautery. One may then follow the pedicle toward the right along the true porta. The adhesions between the hepatoduodenal ligament and segment 4b are more easily divided from the left than from the front.

  2. Use aids to dissection. Usually, structures in the hepatoduodenal ligament can be identified by inspection and palpation, especially if a biliary stent is in place. When repairing complex, high biliary injuries (e.g., types E4 and E5), we routinely place percutaneous stents preoperatively for this purpose. Intraoperative Doppler ultrasonography may be useful in identifying the hepatic artery and the portal vein. Intraoperative ultrasonography may also be helpful in identifying the bile duct, and needle aspiration may be used [see video 2
    ] before the duct is incised if there is any doubt about its location. Either blunt or sharp dissection is effective in this area. Our preference is to use a long fine rightangle clamp to obtain exposure in a layer-by-layer fashion. We then carefully cauterize or ligate and divide the exposed tissue.

Step 2: Defining the Duct

Carefully débride crushed, cauterized, or devitalized tissue back to normal healthy tissue. When performing a delayed repair, it is not necessary to resect all scar tissue around the duct. Just be certain that the anastomosis is constructed to healthy duct mucosa proximal to the injury and not to granulation tissue at the opening in the duct.


Figure 16. Resection of Middle-Third and Proximal Bile Duct Tumors: Portal Vein Bifurcation

Step 3: Anastomosis

For all types of repair, construct a Roux-en-Y loop of sufficient length to make a tension-free anastomosis and perform a biliary-enteric anastomosis as previously described.

injury-specific repairs

E1- and E2-Type Injuries

Make a longitudinal incision in the anterior portion of the exposed duct and perform a vertical side-to-side anastomosis.

E3-Type Injuries

It is very rare for the left duct to be injured during a laparoscopic cholecystectomy; therefore, the left duct is also

Figure 17. Strasberg Classification of Biliary Injuries
less involved in the ensuing inflammatory processes that affect the common and right hepatic ducts. The surgeon can take advantage of this fact when repairing an E3-type injury. This injury is at the level of the confluence, but the confluence remains intact, and drainage of the left hepatic duct alone is sufficient to establish drainage for the entire liver. Using the techniques described above, identify and expose the extrahepatic left duct at the base of segment 4, make a longitudinal incision in the duct, and perform a transverse side-to-side bilioenteric anastomosis [see Figure 18]. This technique,

Figure 18. Hepp-Couinaud Approach to a Type E3 bile duct injury
described by Hepp and Couinaud in 1956,29 is known as the Hepp-Couinaud technique. We recently published our experience with this technique, which provides excellent long-term results.30

E4- and E5-Type Injuries

In these types of injuries, all (E4) or some portion (E5) of the right ductal system is isolated from the left ductal system. Therefore, the Hepp-Couinaud approach provides adequate drainage only for those segments of liver with bile ducts in continuity with the left hepatic duct. The excluded right side must be drained separately, but inflammation and scar tissue make exposing the right duct more challenging. Rather than attempting to dissect out the right duct directly, begin the dissection along the left hepatic duct and under the base of

segment 4, rolling the base of segment 4 upward (lowering the hilar plate). The takeoff of the right duct is located within the same coronal plane as the left duct, so keep the dissection in this same plane, continuing to the right until encountering the attachment of the cystic plate to the right portal pedicle. Divide this fibrous tissue band and then elevate and dissect the liver at the base of segment 5, exposing the sheath of the right portal pedicle. Palpate the previously placed stent to confirm the position of the right bile duct within the sheath. Intrahepatic exposure of the right pedicle is usually possible and a well-vascularized, uninjured duct can be identified for anastomosis. In extremely rare cases of very proximal right-sided injuries, hepatic resection may be required.31

Financial Disclosures: None Reported.

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19. Strasberg SM, Hertl M, Soper NJ. An analysis of the problem of biliary injury during laparoscopic cholecystectomy. J Am Coll Surg 1995;180:101–25.

20. De Frances CJ, Lucas CA, Buie VC, et al. 2006 National Hospital Discharge Survey. National Health Statistics Reports No. 5, July 30, 2008. Available at http://www.cdc.gov/nchs/data/nhsr/nhsr005.pdf (accessed January 15, 2010).

21. Flum DR, Cheadle A, Prela C, et al. Bile duct injury during cholecystectomy and survival in medicare beneficiaries. JAMA 2003;290: 2168–73.

22. Mercado MA, Strong RW, Wall DR, et al. Early versus late repair of bile duct injuries. Surg Endosc 2006;20:1644–7.

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Additional Reading


Blumgart LH, Hann LE. Surgical and radiologic anatomy of the liver, biliary tract and pancreas. In: Blumgart LH, editor. Surgery of the liver and biliary tract and pancreas. Philadelphia: Saunders Elsevier; 2007. p. 3–29.

Corvera CU, Blumgart LH, Darvishian F, et al. Clinical and pathologic features of proximal biliary strictures masquerading as hilar cholangiocarcinoma. J Am Coll Surg 2005; 201:862–9.

Edil BE, Cameron JL, Reddy S, et al. Choledochal cyst disease in children and adults: a 30year single-institution experience. J Am Coll Surg 2008;206:1000–8.

Hepp J. Hepaticojejunostomy using the left biliary trunk for iatrogenic biliary lesions: the French connection. World J Surg 1985;9:507–11.

Kendrick ML, Nagorney DM. Bile duct cysts: contemporary surgical management. Curr Opin Gastroenterol 2009;25:240–4.

Acknowledgments

The authors wish to acknowledge Drs. Bryce Taylor MD, FACS, FRCSC, and Bernard Langer MD, FACS, FRCSC, for their contributions to the previous rendition of this chapter on which we have based this update.

Figures 1 to 17 Elizabeth Hayden Figure 18 Christine Kenney