EMBRYOLOGY, ANATOMY, AND SURGICAL APPLICATIONS OF THE EXTRAHEPATIC BILIARY SYSTEM

SURGICAL ANATOMY AND EMBRYOLOGY

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EMBRYOLOGY, ANATOMY, AND SURGICAL APPLICATIONS OF THE EXTRAHEPATIC BILIARY SYSTEM Robert Benton Adkins, Jr, MD, William C. Chapman, MD, and V. Sreenath Reddy, MD

EMBRYOLOGY OF THE GALLBLADDER AND BILIARY SYSTEM

At the fourth week of embryologic development, a diverticulum develops on the ventral surface of the foregut just cephalad to the yolk sac and just caudad to the fusiform dilation that is the gastric precursor (Fig. 1).This ventral diverticulum grows more ventrally into the septum transversum. Two buds of solid epithelial cells develop at its tip and create the right and left lobes of the liver by developing into hepatic cylinders and forming a meshlike network with rich vascular channels? The early developing liver is like a vascular sponge attached to the duodenum by the original hepatic diverticulum, which soon becomes the bile duct system. The bile duct system starts out as a solid outgrowth, from which another bud arises to become the cystic duct and gallbladder. As the distal portion of the bile duct branches into right and left limbs and enters the developing right and left lobes of the liver, it vacuolates and then canalizes and forms into one continuous epithelial-lined lumen. The same type of canalization occurs in the cystic duct and finally in the gallbladder at about 3 months’ gestation. The right and left ducts, which also begin as solid outgrowths from the original diverticulum, likewise canalize and drain the liver of its bile.3 A migration across the right face of the foregut brings the origin of the bile duct toward the dorsal mesentery of the second portion of the duodenum, where it is joined with the ventral pancreatic duct, another bud from the proximal portion

From the Departments of Surgery (RBA, WCC, VSR) and Cell Biology (RBA) and Divisions of Hepatobiliary Surgery and Liver Transplantation (WCC) and General Surgery (VSR), Vanderbilt University Medical Center, Nashville, Tennessee

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Dorsal pancreas

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Common duct-

Minor papilla

Major papilla

Duodel; E Figure 1. Development of the gallbladder, pancreas, and biliary tract. A, At 5 weeks (6 mm). 6,Sixth week (8 mm). C, At the end of the sixth week (12 mm). D,At the end of the seventh week (16 mm). €, At birth. Note right to left migration of the common bile duct and the ventral pancreatic primordium. (From Brainerd Avery L: The digestive tube and associated glands. Arey LB: Developmental Anatomy, ed 7. Philadelphia, WB Saunders, 1965, p 260; with permission.)

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of the hepatic diverticulum. After its migration, the entrance of the bile duct passes through the sphincter of Oddi and finally by the ampulla of Vater, where it empties into the second part of the duodenum of the fully developed embryo (Fig. 1 ) . 1 2 This simplified story represents a remarkable series of complicated events. Mishaps of development occasionally occur. That all people do not have some type of biliary tract defect of embryologic origin seems impossible. The complete developmental history of the biliary system is beautifully told in the second edition of Embryology for Surgeons by Skandalakis et a1.I2 COMMON DEVELOPMENTAL ANOMALIES

Common anomalies of the biliary system and gallbladder include variations of number and location of the gallbladder. Ductal and arterial anomalies must also be considered by surgeons in all biliary tract procedures. Multiple Gallbladders

Multiple gallbladders may have separate cystic ducts, or two or more may share one cystic duct. These extra gallbladders may lie beneath the right or left lobe of the liver or within the liver or gastrohepatic ligament. They may arise from the common bile duct (CBD), hepatic duct, or right or left hepatic duct (Fig. 2). In some cases, a separate duct from the liver enters the gallbladder, cystic duct, or junction of the cystic duct and CBD. These ducts have become known as Luschka’s ducts. In the era of laparoscopy, these extra ducts should be treated by ligation, suture, clipping, cauterization, or exclusion when they are recognized. Absent Gallbladders

The gallbladder may be absent if a separate bud failed to develop from the hepatic diverticulum or when failure of vacuolization and canalization of the gallbladder occurred at its solid embryonic stage at approximately 2 or 3 months’ gestation. SURGICAL IMPLICATIONS OF THE VARIATIONS IN THE VASCULAR SUPPLY OF THE EXTRAHEPATIC BILIARY SYSTEM Anatomic Variations

The usual arterial supply of the gallbladder and the extrahepatic biliary tree is from branches of the celiac trunk. This trunk gives rise to the hepatic artery and one of its branches, the gastroduodenal artery. The hepatic artery further branches into the right gastric and right and left hepatic arteries. The gastroduodenal artery has anterior and posterior pancreaticoduodenal arteries. The gallbladder receives its primary blood supply from the cystic artery. It is usually a branch of the right hepatic artery or of the gastroduodenal artery. The cystic artery is usually anterior to the CBD and superior to the cystic duct. It is sometimes a paired artery. It may be immediately adjacent to the cystic

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Figure 2. Main variations in gallbladder and cystic duct anatomy: bilobed gallbladder (A), septum of the gallbladder (B), diverticulum of the gallbladder (C), and variations in cystic (From Smadja C, Blumgart LH: The biliary tract and the anatomy of ductal anatomy (0). biliary exposure. In Blumgart LH (ed):Surgery of the Liver and.Biliary Tract, ed 2. London, Churchill Livingstone, 1994, p 19; with permission.)

duct. Paired cystic veins course along either side of the artery, and they usually empty into the right portal vein. The extrahepatic portion of the biliary ductal system has multiple sources of blood supply. The arteries supplying the ductal system, in their descending order of participation, are: posterosuperior pancreaticoduodenal (PSPD), right hepatic, posteroinferior pancreaticoduodenal, right gastric, hepatic, anteroinfer-

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ior pancreaticoduodenal, cystic, and superior pancreaticoduodenal arteries (Fig. 3). Numerous variations and anomalies of the arterial supply to the gallbladder and extrahepatic biliary tree occur. These anomalies can represent significant challenges to surgeons. The hepatic artery can have an accessory right hepatic artery from the superior mesenteric artery. An abnormal course for the hepatic artery occurs when it crosses anterior to the hepatic duct or when the right branch is located anterior to the right hepatic duct. One should be aware of possible venous varicosities or aneurysmal dilations of the right hepatic artery, either of which may occur in Calot’s triangle. In some cases, an accessory cystic artery arises from the main hepatic artery or from the right hepatic artery. During open cholecystectomy or laparoscopic cholecystectomy, incomplete visualization before dissection of the cystic artery can inadvertently lead to damage of these other major vessels. The course and location relative to other structures of the cystic artery can be highly variable (Fig. 4). The cystic artery can be found between the hepatic ducts or even behind the common hepatic duct. In 95% of cases, the cystic artery arises from the right hepatic artery and runs parallel and medial to the cystic duct. If the cystic artery arises more proximally, it arises from the common hepatic artery (in 33% of cases) or, rarely, from the celiac trunk.14 In these instances, the artery runs more parallel to the CBD. This abnormality poses obvious problems to surgeons, who must clearly identify this vessel in preparation for and during cholecystectomy. At or near the region of the neck of the gallbladder, the cystic artery divides into anterior and posterior divisions. Double cystic arteries exist in 8% to 15%

Figure 3. The bile duct blood supply. Note the axial arrangement of the vasculature of the supraduodenal portion of the main bile duct and the rich network enclosing the right and left hepatic ducts: right branch of the hepatic artery (a), 9-o’clock artery (b), retroduodenal artery (c), left branch of the hepatic artery (d), hepatic artery (e), 3-o’clock artery (f), common hepatic artery (g), gastroduodenal artery (h). (From Smadja C, Blumgart LH: The biliary tract and the anatomy of biliary exposure. ln Blumgart LH (ed): Surgery of the Liver and Biliary Tract, ed 2. London, Churchill Livingstone, 1994, p 19; with permission.)

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Figure 4. Main variations of the cystic artery: typical course (A), double cystic artery (B), cystic artery crossing anterior to main bile duct (C), cystic artery originating from the right branch of the hepatic artery and crossing the common hepatic duct anteriorly (D), cystic artery originating from the left branch of the hepatic artery (€), and cystic artery originating from the gastroduodenal artery (F). (From Smadja C, Blumgart LH: The biliary tract and the anatomy of biliary exposure. In Blumgart LH (ed):Surgery of the Liver and Biliary Tract, ed 2. London, Churchill Livingstone, 1994, p 16; with permission.)

of patients, and a few (0.3%) patients have a triplicate arterial supply to the gallbladder. The third vessel may be of diminutive size. In 12% of patients, accessory cystic arteries are present.I9 For routine cholecystectomy and for procedures involving exploration of the biliary tree, surgeons must have knowledge of the potential variations in the location and course of the arterial supply of the region. Although the usual course of the cystic artery places it parallel and medial to the cystic duct, of cases in which this relationship does not exist, it is located anterior to the hepatic duct in 84%. In the remaining 16% of cases, the arteries lie posterior to the hepatic duct.I9The most common surgical pitfalls include inadequate visualization and exposure of the cystic artery at the level of the gallbladder neck. Regardless of its proximal origin, the cystic artery by default must at some point terminate at the gallbladder. This termination almost invariably occurs at or near the level of the gallbladder neck, so confirmation of the terminus of an artery at the gallbladder neck and direct visualization of the branch vessels entering the wall of the gallbladder positively identify this vessel as the cystic artery and usually preclude injury to the other vessels in the region. In most cases, surgical dissection of the cystic duct and cystic artery should begin adjacent to or near the point of origin of the cystic duct or near the point of entry of the branch vessels of the artery into the gallbladder wall. This is

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probably the most important step in the prevention of accidental bile duct or hepatic arterial injury during open or laparoscopic cholecystectomy. Blood Supply of the Biliary Tree

The primary blood supply to the CBD is usually derived from branches of the PSPD or anterosuperior pancreaticoduodenal artery and the gastroduodenal artery. The proximal portion of the CBD may receive some circulation from the right hepatic and right gastric arteries. Branch vessels course along the CBD medially and laterally in the 3-o’clock and 9-o’clock positions (the so-called 3 o’clock and 9 o’clock arteries). The right and left hepatic ducts receive their blood supply from small side branches arising from the right and left branches of the hepatic artery proper. The cystic duct receives its blood supply from branches of the cystic and right hepatic arteries (see Fig. 3). The middle and distal segments of the CBD receive their blood supply from the supraduodenal artery, often the first branch of the gastroduodenal artery. The most distal portion of the CBD receives its blood supply predominantly from the PSPD and posteroinferior pancreaticoduodenal arteries. The unique aspect of the arterial supply of the CBD is that it is composed of a multilayered arcade of vessels, the most superficial of which is the epicholedochal plexus, comprised of the 3-o’clock and 9-o’clock vessels and their connecting branches. These vessels give rise to penetrating branches that form an intramural and subepithelial plexus. Given the variety of biliary drainage procedures and the increasing necessity for corrective biliary tract procedures because of iatrogenic injury, an adequate understanding of the extrahepatic biliary blood supply is imperative. The association of the blood supply of the biliary tree is important when constructing choledochoenteric anastomoses and when performing orthotopic liver transplantation. Recommendations for handling the CBD include: (1) avoidance of stripping of the main bile duct during surgical exposure and during harvesting for transplantation, (2) avoidance of opening the CBD longitudinally through a relatively avascular area, (3) avoidance of the plexus of epicholedochal vessels while suturing an anastomosis, (4) always ligating the cystic artery close to the gallbladder to avoid taking branches of the cystic artery that may supply the CBD. Terblanche et all6 carried out important anatomic studies in normal human cadavers that have helped to define the anatomic basis now used for planning and performing biliary bypass and biliary-enteric anastomosis. Using a resindye-casting technique, these investigators demonstrated that the extrahepatic bile duct receives its blood supply from two paired arteries that run laterally and directly adjacent to the bile duct, that is, the 3 o’clock and 9 o’clock vessels, based on their location in relationship to the duct. These laterally placed vessels have been shown to receive their inflow proximally from the hepatic artery at the hilum of the liver, often by branches of the right hepatic artery. The distal segment of the CBD derives most of its blood supply from branches of the PSPD and retroduodenal arteries. Unlike in other animal species, typically few, if any, additional tributaries from branches of the hepatic artery exist along the course of the CBD of humans, so when the CBD is divided or ligated, the lateral 3 o’clock and 9 o’clock vessels are also interrupted. Depending on the level at the point of division, this may result in ischemia to the proximal or distal portion of the transected duct, which undoubtedly is a major explanation for the poor results and late stricture development that often occur when end-to-end bile

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duct reconstruction is used following bile duct transection because one side of the divided and anastomosed bile duct is likely to suffer relative ischemia. Northover et al,9Terblanche et al,19 and others have argued that most, if not all, biliary reconstruction should be performed with a hepaticojejunostomy using the most proximal bile duct in the hilum of the liver as the biliary segment. This short upper segment is likely to be well vascularized. This anatomic consideration should always be kept in mind when transection of the CBD is required in an operative procedure (e.g., liver transplantation or pancreaticoduodenectomy). In this setting, the authors agree that dividing and anastomosing the duct above the cystic duct entry point and closer to the hilum may be better, as recommended by Northover and Terblanche.loA long common hepatic duct or upper CBD segment is always associated with a greater risk for ductal ischemia for the distalmost portion of the long, proximal segment. The longer the proximal segment, the higher the risk for anastomotic breakdown or late stricture formation.I0 SURGICAL IMPLICATIONS OF ANATOMIC VARIATIONS OF THE GALLBLADDER AND BlLlARY TREE

The gallbladder is a hollow, pear-shaped viscus. It most commonly lies on the inferior surface of the right lobe of the liver in the region, defined by C ~ u i n a u d as , ~ segments IV and V. The exposed portion of the gallbladder is invested with a layer of peritoneum that covers 50% to 70% of its surface. The remainder of the organ is in direct continuity with the liver in the gallbladder fossa. The peritoneum may completely envelop the gallbladder and act as a mesentery. Conversely, the gallbladder may be partially or completely intrahepatic. Another aspect of the variability of the gallbladder is its relationship to the margin of the liver. In approximately 55% of cases, the gallbladder is inframarginal. Thirty percent of gallbladders are present at the margin, and 15% are considered supramarginal. The gallbladder may have an infundibulum at its neck, known as Hartmann's pouch, and, in some cases, another outcropping, known as a Phrygian cap, is present at its fundus. The location of the gallbladder varies. It is rarely unattached to the liver but, in these instances, may be located in the gastrohepatic ligament. Some gallbladders may be found under the left lobe of the liver. Absence of the gallbladder is reported to occur in only 1 of 4000 patients.14Multiple gallbladders are also rare, with a reported prevalence of 0.5% to l.O%.l4In cases of multiple gallbladders, a duplication of the cystic duct is almost always present. The second duct may empty separately into the CBD or enter as a common channel with the primary cystic duct. In some cases, the duplicate cystic duct may empty into the right or left hepatic ducts (see Fig. 2). The gallbladder is innervated by the hepatic branches of the left division of the vagus trunk. Its sympathetic innervation arises from levels T7 to T10 and courses through the celiac plexus and splanchnic ganglia. The sensation of biliary colic is mediated by those afferent nerve fibers passing by sympathetic splanchnic nerves, which usually causes a sensation of referred pain along those dermatomes to the region of the right upper quadrant of the abdomen or to the right scapula area of the back, regardless of the location of the gallbladder. This is also true for those gallbladders located on the left. Given the high frequency of cholecystectomies and the fact that most of these procedures are done laparoscopically, knowledge of the possible variations in gallbladder anatomy is critical. This knowledge is important for any nonrou-

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tine presentation of patients with cholecystic abnormalities. In cases of a peritoneal mesenteric attachment of the gallbladder, cystic volvulus is possible, is usually in the clockwise direction, and can result in symptoms akin to severe biliary colic. Cases of near complete or complete intrahepatic gallbladder can present a significant challenge to surgeons performing laparoscopic cholecystectomies and may necessitate a conversion to an open procedure for adequate dissection and hemostasis. Absence of the gallbladder from its usual location does not preclude its existence elsewhere. Although rare, alternate locations of the gallbladder may require surgeons to explore all regions, including those to the left of the falciform ligament. In these instances, surgeons should be careful to delineate the blood supply of the organ and the route of its bile drainage. Despite its occasional translocation, the cystic artery is typically virtually always anterior to the CBD. In cases of sinistroposition of the gallbladder, the preoperative clinical presentation provides little information regarding the anatomic variation in location of the organ. Given that the afferent nerve supply of the gallbladder is by the right sympathetic splanchnic nerves, patients with left-sided gallbladders experiencing biliary colic complain of right upper quadrant pain or right scapula pain. Although preoperative sonography may give information regarding the aberrant location of the gallbladder, surgeons must always be prepared for this contingency, especially if the procedure is attempted laparoscopically. Commonly, the abnormal location of the gallbladder may not be appreciated by the sonographer, or this finding, if noted, may not be relayed to the surgeon, resulting in a rare surprise finding at the time of cholecystectomy.

EXTRAHEPATIC BILIARY TREE AND ITS VARIATIONS Cystic Duct

The cystic duct is more commonly found with some type of anatomic variation than it is found to be running its most commonly reported course. In fact, only 33% of patients have the ”classic” anatomic relationship between the cystic duct and the extrahepatic bile ducts and the related arteries. In the “usual” presentation, the cystic duct is found to a patient’s right, slightly posterior to the hepatoduodenal ligament. In two thirds to three fourths of cases, the cystic duct has an angular entry into the CBD, thereby making its identification easier. In 17% to 20% of cases, the cystic duct has a parallel course and less angular entry into the CBD.2,l3 In 5% to 8% of cases, the cystic duct is tortuous and may be spiral in shape, allowing for variable entry angles into the CBD (Fig. 5).13,l 4 Fortunately, the most common location of the cystic duct is to the right of the hepatic artery. The potential routes of drainage of the cystic duct into the remainder of biliary tree are myriad. The classic region of entrance of the cystic duct is into a site near the midportion of the main duct. The point is between the convergence of the right and left hepatic ducts and the segment of the duct that becomes retroduodenal. Another site of drainage is into the right hepatic duct, although this is reported to occur in less than 1% of cases.2 In some cases, the cystic duct drains into the retroduodenal portion or even into the intrapancreatic portion of the main duct. Rarely, the cystic duct drains into the left hepatic duct. Accessory cystic ducts are rare, as is the absence of a cystic duct. In these cases, one usually finds scarring or stricture of the cystic duct associated with

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Figure 5. Different types of union of the cystic duct and common hepatic duct: angular union (A) (75%), parallel union (6) (20%), and spiral union (C) (5%). (From Smadja C, Blumgart LH: The biliary tract and the anatomy of biliary exposure. ln Blumgart LH (ed): Surgery of the Liver and Biliary Tract, ed 2. London, Churchill Livingstone, 1994, p 19; with permission.)

gallstone disease and occasionally with an acquired fistulous connection between the gallbladder and the CBD or between the gallbladder and the duodenum. The length of the cystic duct also varies. Twenty percent of ducts are less than 2 cm in length, with most between 2 cm and 4 cm.I9 A unique feature of the cystic duct, in contrast to the remainder of the biliary tree, is the presence of mucosal folds (i.e., the spiral valves of Heister). These valves can provide partial obstruction to the passage of catheters or cannulas used for intraoperative cholangiography,but their presence can be of some aid in the positive identification of the cystic duct during intraoperative cholangiography because of their characteristic appearance seen on cholangiography. Given the highly protean course of the cystic duct and the extensive variability of its drainage, unnecessary operative manipulation of the duct can be hazardous. Caution should be used during open or laparoscopic cholecystectomy to avoid inadvertent injury to the main bile ducts and arteries. Injury may be caused by overzealous dissection and clipping of the cystic duct. Limited dissection of the cystic duct and cystic artery in the region of the gallbladder neck of sufficient length for identification purposes and for safe clip or suture ligation and division should minimize accidental injury to the hepatic artery or bile duct. During routine cholecystectomy, definition of the cystic duct-common duct interface is rarely necessary. Several investigators have reported that the risk for injury to the common duct and to the associated arterial supply in that region increases with extensive dissection in this region of cystic duct-common duct Positive identification of the cystic duct is best made at its beginning, at the level of the gallbladder neck. When it has been found and encircled, an intraoperative cholangiogram should be obtained to verify its location and anatomy and to identify stones. Given the multiple possibilities of the drainage of the cystic duct, dissection at a level below its upper limits may only lead to confusion regarding the identity of the structure. In addition, dissection of the distal portion of the cystic duct increases the risk for injury to a right hepatic artery that crosses anterior to the CBD or to the cystic artery branches that supply the main duct. This could result in a devascularization injury, rendering a segment of the main duct ischemic.

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Common Bile Duct The CBD, unlike the cystic duct, is more constant in its course and size, but some variations exist, especially in the region of the hepatic hilum and at the intrapancreatic portion of the duct. In addition, the size of the CBD varies greatly at its different portions and from person to person. The greatest variation in CBD anatomy occurs with the different levels where the hepatic ducts may converge. The second most common variation is the point of entry of the cystic duct into the CBD. Rarely, nonconvergence of the right and left hepatic ducts occurs, resulting in their separate drainage into the d u ~ d e n u mThese .~ are often referred to as sectoral ducts because they drain specific sectors of the liver. Most often, a right sectoral duct drains segments VI and VII or segments V and VIIL4 In these cases, the cystic duct almost invariably drains into the right-sided sectoral duct.13 The usual location of the CBD is in the anterior aspect of the portal pedicle. The duct is most commonly on the right lateral side of the proper hepatic artery at its proximal portion and lateral to the gastroduodenal artery at its distal portion. Usually, the distal CBD lies in a groove on the posterior aspect of the pancreas, but occasionally it may be intrapancreatic for a significant portion of its distal segment. The CBD classically empties into the second portion of the duodenum, typically at an oblique angle. Kune6 described a band of connective tissue that connects approximately 10 mm to 20 mm of the distal CBD to the medial wall of the duodenum. This connective tissue "stabilizes" the distal portion of the duct, thereby facilitating some endoscopic procedures, such as endoscopic sphincteroplasty. The size of the typical CBD is a matter of controversy. Many studies have attempted to determine a standard length, diameter, and thickness of the various portions of the duct, but significant normal variability in duct size and length may be encountered. Mahour et als have noted that duct size may increase by 0.4 mm for each decade of life. The commonly accepted upper limit of normal diameter for the main bile duct is 4 mm to 5 mm when sonography is used as the diagnostic modality (detects inner diameter) and 10 mm when a contrast study is used. This difference is explained by the magnification factor of the imaging equipment. When directly measured in an open procedure, it should be 10 mm in diameter because this is a measure of the outer diameter of the CBD. As in cases of arterial and cystic duct aberrancies, CBD variations have significant surgical implications. They may be encountered during a variety of biliary procedures but are probably most significant during laparoscopic cholecystectomy. Because operations being done laparoscopically often focus on a narrow region of dissection and in a limited field of view, ductal anomalies may go unrecognized. Physicians must recognize cases in which a sectoral duct is present and proceed cautiously so that inadvertent injury is avoided. As in cases of cystic duct variations, careful dissection of the cystic duct, confirmation of its origin from the gallbladder, and careful cholangiography are the best methods to confirm its identity and to avoid injury to adjacent ductal structures. Similarly, the presence of a sectoral duct may be realized by noticing the presence of another ductlike structure in the porta hepatis and then verified by its identification during cholangiography. In cases in which choledochoenteric anastomosis is necessary, surgeons must realize the presence of any sectoral duct and define its anatomy. Because the left duct usually drains a larger portion of the liver than the right and a single duct to bowel anastomosis is done, one may inadvertently leave a significant portion of the liver without adequate or any biliary drainage. This error may

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result in cholestasis of the affected segments of the liver or in the development of biliary fistulas arising from the sectoral duct that was cut and left open without bowel drainage. In either case, the previously delineated caveats for ductal dissection and anastornotic technique apply. In general, longer proximal segments of duct are more prone to devascularization and ischemia, thereby rendering the anastomoses at greater risk for failure. Sectoral ducts also present a challenge during liver transplantation. The presence of separate segmental biliary drainage of the liver must be recognized in donor organs and dealt with properly at the time of harvest. At the time of organ transplantation, it must then be syndactylized and incorporated into the remainder of the biliary tree because the recipients likely have only one common bile duct to receive the bile. The anastomoses between donor and recipient ducts must be constructed with the blood supply of each end in mind. Adequate vascularization and circulation are essential to anastomotic success and to the prevention of later breakdown, fistula formation, or ductal anastomotic stricture. AGENESIS OF THE BlLlARY TREE Biliary Agenesis When the entire biliary system seems to be completely absent, it is reduced to a fibrous band that may be overlooked. The authors agree with Skandalakis et all2 and othersI3 that this must always represent the extreme case of biliary atresia and not biliary agenesis. As Skandalakis et all2 point out, it is hard to imagine that a liver could be present if biliary structures, other than the cystic duct and gallbladder, had never been present at some point during gestation. If they had not, a liver could not have developed. Only with agenesis of the liver can true biliary agenesis occur. Biliary Atresia Biliary atresia is the most severe anomaly of the biliary tree and is perhaps the most difficult to treat. It may involve a short or long segment, but an entire duct or the whole biliary system is commonly The atresia of the biliary tree may be either partial or, in some cases, may include the entire biliary system. Many of the variety of atresias that can occur have been reported by Holmes5 and Th~rnpson.'~ All of these are categorized and discussed in the comprehensive book by Skandalakis et Much discussion and considerable consensus exists that the cause of biliary atresia is viral infection. Most investigators agree that biliary atresia is not the result of a single embryologic event but most likely the result of an inflammatory or infectious disease beginning late in fetal life after the liver has developed or immediately after birth and then progressing to the usual form, which is now generally considered to be acquired or of viral origin." The cause of this devastating event is still unknown but likely represents a sclerotic process involving previously normal bile ducts. Patients with this condition often have an anomalous junction of the pancreatic and distal bile duct resulting in a long common channel and with reflux of pancreatic juice into the bile duct, as commonly occurs in cases of choledochal cysts. The significance of this finding and the reasons why it might be associated with cystic dilatation in some patients and bile duct sclerosis in others are unknown.

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Over the past century, many classification schemes have been proposed and used by surgeons and physicians who care for infants with biliary atresia. These classifications are of questionable value for determining proper treatment or for predicting long-term outcomes. The most important diagnostic factors include differentiating neonatal hepatitis from obstructive jaundice. They may be distinguished by a liver biopsy and also by the clinical course in the early neonatal period. Jaundiced infants undergoing surgical exploration require careful assessment of the gallbladder and extrahepatic biliary tree to determine whether patent ducts are present and whether they contain bile. If atretic ducts are found, then these and the gallbladder are resected, together with some residual ductal tissue at the level of the bile duct bifurcation. A portoenterostomy procedure is completed by anastomosing a 40-cm Roux-en-Y limb to the raw portal plate at this level (Kasai procedure).13 The most favorable outcomes with the Kasai procedure have been realized in cases in which the finding of residual patent atretic ducts of at least 150 (*m was possible. A few successful cases have been reported with smaller or even no visualized ductal remnants. The timing of operative intervention is also a critical factor in these infants, and most investigators suggest operative intervention as soon as this diagnosis is made. Diagnosis should be made before 10 weeks of age. The progressive fibrosis that occurs in these infants is associated with poor results in infants undergoing portoenterostomy beyond this age. Although many infants born with biliary atresia and who undergo a successful Kasai procedure have resolution of their jaundice in childhood, many unfortunately develop portal hypertension and late liver failure, which are successfully treated only with liver transplantation. The treatment approach should be tailored to individual cases and may reasonably involve the Kasai procedure for infants found to have biliary atresia before 7 or 8 weeks of age. Liver transplantation should be considered for all patients who fail the Kasai procedure, who develop late postoperative complications thereof, or whose diagnoses are discovered after 10 weeks of age, when the success of the Kasai procedure is significantly reduced.13 Cystic Dilation of the Common Bile Duct

A single area of ductal dilation of the CBD is the most common type of cyst and is the classic choledochal cyst. It is usually located below the bifurcation of right and left ducts and involves the origin of the cystic duct. The size of these cysts may be large. They are typically thick walled, commonly inflamed, and occasionally undergo malignant change. Diverticular Dilatation

Diverticular dilatation has been recognized as a different type of developmental defect from the cystic dilation of the common bile duct defect. This defect presents as an area of dilatation that may occur as a result of localized weakness in the developing bile duct wall. The connecting pedicle may be short or long and may be mistaken for an accessory gallbladder. Low Choledochal Cysts or Choledochoceles

Choledochal cysts may occur low on the bile duct and are found at the terminal end of the bile duct, at the ampulla of Vater. The developmental error

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that causes this to develop is hard to explain, but it may be similar to a ureterocele located at the ureter-bladder wall junction. SURGICAL IMPLICATIONS OF CYSTIC DILATIONS OF THE BlLlARY TREE

Choledochal cysts usually present in childhood but do not cause sufficient significant symptoms to lead to their detection until adulthood in at least 20% of patients. Although the classic triad of right upper quadrant pain, jaundice, and a palpable epigastric mass may be present, most patients present with symptoms that are suggestive of gallstone disease. This presentation usually leads to an abdominal sonogram with the finding of a cystic mass in the region of the porta hepatis. CT scanning usually confirms the finding of a cystic mass. Nuclear medicine scanning using technetium-99m-labeled agents often shows biliary ductal communication with the cystic region and eliminates other causes of cystic disease in the region (e.g., pancreatic pseudocyst). Successful cholangiography (endoscopic retrograde cholangiopancreatography or percutaneous transhepatic cholangiography) defines the full extent of the cystic dilatation and the relationship of the cystic dilatation to the pancreatic duct. Like biliary atresia, the cause of choledochal cyst formation is unknown but has been associated with an anomalous junction of the biliary and pancreatic ducts, with a long, 2-cm to 4-cm common channel in many patients. Several classification schemes have been proposed, but most investigators favor the scheme proposed by Todani et alls in 1977 (Fig. 6). In this system, the most common choledochal cyst is classified as a type 1 cyst, representing more than 80% of cases. It is a single fusiform type of extrahepatic cyst. The other, less common types of cysts include single and multiple extrahepatic and intrahepatic cysts. Type 5 choledochal cysts, also known as Caroli’s disease, are represented by multiple intrahepatic areas of cystic dilatation.

“i Type

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Solitary fusiform cvst extrahepatic

Extrahepatic supraduodenal diverticulum 111

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lntraduodenal diverticulum; choledochocele

Type

&!

Findings Fusiform extra- and intrahepatic cysts Multiple . extrahepatic cysts

Multiple intrahepatic cysts: Caroli’s Disease

Figure 6. Todani classification of bile duct cysts. (From Altman RP: Choledochal cyst. In

Blumgart LH (ed): Surgery of the Liver and Biliary Tract, ed 2. London, Churchill Livingstone, 1994, p 1184; with permission.)

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The preferred method of treatment for choledochal cysts is surgical excision, whenever possible. Past methods of enteric bypass using cystenterostomy have produced suboptimal long-term results and should be avoided. Surgically bypassed but not resected segments of choledochal cysts lead to bile stasis with recurrent cholangitis and associated biliary sludge and stone formation. Another significant consideration is the definite strong association of neoplastic transformation with choledochal cysts. An approximately 20-fold increase in the incidence of cholangiocarcinoma in the affected ductal segment occurs compared with the incidence found in the normal biliary tree.I8 This provides additional impetus for cyst excision whenever possible. All choledochal cysts should be completely excised and bile flow re-established with a biliary-enteric anastomosis (usually by a Roux-en-Y limb of jejunum). Long-term external drainage has no role in the management of these patients. For patients with type 3 cysts (i.e., choledochoceles), transduodenal sphincteroplasty is probably the best procedure. Patients with type 4 cysts are best treated by excision of extrahepatic cysts with hepaticojejunostomy. Some patients with type 5 cystic dilatation (i.e., Caroli's disease) can be treated by resection and hepaticojejunostomy for improved biliary drainage (Fig. 6). Definitive treatment for this abnormality requires liver transplantation, especially in patients with cirrhosis or with recurrent episodes of sepsis and liver decompensation, which eventually lead to hepatic failure. ANATOMIC CONSIDERATIONS OF LIVER TRANSPLANTATION

Biliary tract-related complications are among the most common problems encountered following liver transplantation and occur in 20% to 30% of pat i e n t ~ . These '~ complications include early anastomotic leak cholangitis and late bile duct stricture formation. Several specific measures are used during the donor procurement operative procedure and in the recipient part of surgery to minimize the risk for biliary-related complications. First, during the donor procurement operation, the donor bile duct is divided distally, just above the upper border of the pancreas. This procedure is done with careful, sharp dissection to avoid thermal injury to the bile duct. No ligatures are placed on the duct. The biliary tree is thoroughly flushed with saline to remove toxic bile salts that may cause damage during the period of cold storage. During transplantation, the duct is shortened during "back-table" dissection. A short duct with open nutrient vessels minimizes distal duct ischemia related to poor perfusion from the donor hepatic arterial system, which may occur following transplantation and reperfusion. Specific techniques for biliary reconstruction vary according to the transplanting surgeon's preferences. Several general techniques are used by most centers. If minimal size disparity exists between donor and recipient ducts and if no evidence of biliary tract disease ( e g , primary sclerosing cholangitis) exists in the recipient, the authors, like most transplanting surgeons, use direct endto-end anastomosis with fine, absorbable, single-layered, interrupted suture. This is often performed over a small T-tube exited from the lower recipient CBD segment, which may be left in place for as long as 3 to 6 months postoperatively. In transplant recipients with biliary tract disease or with significant size mismatch, in most split-liver grafts, and in pediatric patients, a Roux-en-Y limb is used to perform a hepaticojejunostomy. Operative cholangiography should be performed in all patients in whom any question remains regarding biliary

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anatomy. The surgeon must be certain that all sectoral ducts are included in the anastomosis. SUMMARY

As technology has improved and the ability to apply this technology in the surgical arena has grown, surgeons have been able to perform more sophisticated operative procedures. Hepatobiliary surgeons are now able to use laparoscopy, immunosuppressive drugs, and technical advances in cryosurgery to accomplish magnificent results. The success and safety of laparoscopic cholecystectomy, orthotopic liver transplantation, and trisegmentectomy for hepatic tumors depend on a high regard for and an accurate knowledge of the anatomy and some of the common embryologic anomalies of the biliary tree. The blood supply, ductal variations, and gallbladder anatomy of this area are often the source of major challenge to unprepared and unaware surgeons. The authors have attempted to stimulate an interest in, a respect for, and perhaps some desire to learn more about the important and fascinating anatomy of this region. References 1. Adams DB: The importance of extrahepatic biliary anatomy in preventing complications at laparoscopic cholecystectomy. Surg Clin North Am 74:861-871, 1993 2. Benson EA, Page RE: A practical reappraisal of the anatomy of the extrahepatic bile duct and arteries. Br J Surg 632353460, 1976 3. Clearfield HR: Embryology, malformations, malposition of the liver. In Bockus HL (ed): Gastroenterology. Philadelphia, WB Saunders, 1976 4. Couinaud C: Etudes Anatomiques et Chirurgicales, vol 1. Paris, Masson, 1957 5. Holmes JB: Congenital obliteration of the bile ducts: Diagnosis and suggestions for treatment. Am J Dis Child 11:405-431, 1916 6. Kune GA: Surgical anatomy of the common bile duct. Arch Surg 89:995-1004, 1964 7. Lindner HH, Pena VA, Ruggeri RA: A clinical and anatomical study of anomalous terminations of the common bile duct into the duodenum. Ann Surg 184626-632, 1976 8. Mahour GR, Wakin KG, Ferns DO: The common bile duct in man: Its diameter and circumference. Ann Surg 165:415419, 1967 9. Northover JMA, Hickman R, Watson RGK, et al: Healing of the bile duct anastomosis after transverse choledochotomy or transplantation of the liver in the pig. Surg Gynecol Obstet 160:33-36, 1985 10. Northover JMA, Terblanche J: A new look at the arterial blood supply of the bile duct in man and its surgical implications. Br J Surg 66379-384, 1979 11. Raffensperger JG: Swenson’s Pediatric Surgery. Norwalk, CT, Appleton & Lange, 1990, p 650 12. Skandalakis JE, Gray SW, Ricketts R, et al: The extrahepatic biliary ducts and the gallbladder. In Skandalakis JE, Gray SW (eds): Embryology for Surgeons, ed 2. Baltimore, Williams & Wilkins, 1994, pp 296-333 13. Smadja C, Blumgart LH: The biliary tract and the anatomy of biliary exposure. In Blumgart LH (ed): Surgery of the Liver and Biliary Tract, ed 2, vol 1. London, Churchill Livingstone, 1994, pp 11-24 14. Sterling J A The Biliary Tract. Baltimore, Williams & Wilkins, 1955 15. Strasberg SM, Callery MP, Soper NJ: Laparoscopic surgery of the bile ducts. Gastrointest Endosc Clin North Am 6%-105, 1996 16. Terblanche J, Allison HF, Northover JMA: An ischemic basis for biliary strictures. Surgery 94:52-57, 1983 17. Thompson J: On congenital obliteration of the bile ducts. Edinb Med J 37523, 604, 724, 1892

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18. Todani T, Watanabe Y, Narusue M, et al: Congenital bile duct cysts: Classifications,

operative procedures, and review of thirty-seven cases including cancer arising from choledochal cyst. Am J Surg 134:263-269, 1977 19. Toouli J: Surgery of the Biliary Tract. New York, Churchill Livingstone, 1993 20. Warwick R, Williams P: Embryology. In Williams P, Warwick R (eds): Gray’s Anatomy, ed 36. Philadelphia, WB Saunders, 1980, pp 200-207

Address reprint requests to Robert Benton Adkins, Jr, MD Department of Surgery Vanderbilt University Medical Center D-5220 Medical Center North Nashville, TN 37232-2543