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Congenital Choledochal Cysts in Adults
Brendan C. Visser, MD;
Insoo Suh, BS;
Lawrence W. Way, MD;
Sang-Mo Kang, MD
Arch Surg. 2004;139:855-862.
ABSTRACT
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Hypothesis Excision of the extrahepatic portion of congenital choledochal cysts (CCs) avoids the risk of cancer. The standard classification scheme is out of date.
Design Retrospective case series and literature review.
Setting Tertiary care university hospital.
Patients Thirty-eight adult patients diagnosed as having CC from 1990 to 2004 .
Main Outcome Measures Clinical and radiographic imaging findings, operative treatment, pathologic features, and clinical outcome.
Results Thirty-nine adult patients were treated for CCs (mean [SD] age at diagnosis, 31 [17] years, and mean [SD] age at surgery 37 [14] years). The primary report was abdominal pain (36 of 39 patients). Eight patients had cholangitis, 5 had jaundice, and 6 had pancreatitis. Radiographic imaging studies and operative findings showed that the abnormality predominantly involved the extrahepatic bile duct in 30 patients, the intrahepatic and extrahepatic bile ducts in 7 patients; and 2 were diverticula attached to the common bile duct. Surgical treatment in 29 (90%) of 31 patients with benign cysts (regardless of intrahepatic changes) consisted of resection of the enlarged extrahepatic bile duct and gallbladder and Roux-en-Y hepaticojejunostomy. Eight patients (21%) were initially seen with associated cancer (cholangiocarcinoma of the extrahepatic duct in 6; gallbladder cancer in 2). Seven of 8 patients had a prior diagnosis of CC but had undergone a drainage operation (3 patients), expectant treatment (3 patients), or incomplete excision (1patient). In none of the patients with cancer was surgery not curative. Nine patients had previously undergone a cystoduodenostomy and/or cystojejunostomy as children. Four of them had cancer on presentation as adults. There were no postoperative deaths. Cancer subsequently developed in no patient whose benign extrahepatic cyst was excised, regardless of the extent of enlargement of the intrahepatic bile duct.
Conclusions Congenital CCs consist principally of congenital dilation of the extrahepatic bile duct with a variable amount of intrahepatic involvement. We believe that the standard classification scheme is confusing, unsupported by evidence, misleading, and serves no purpose. The distinction between type I and type IV CCs has to be arbitrary, for the intrahepatic ducts were never completely normal. Although Caroli disease may resemble CCs morphologically, with respect to cause and clinical course, the 2 are unrelated. The other rare anomalies (gallbladderlike diverticula; choledochocele) are also unrelated to CC. Therefore, the term "congential choledochal cyst" should be exclusively reserved for congenital dilation of the extrahepatic and intrahepatic bile ducts apart from Caroli disease, and the other conditions should be referred to by their names, for example, choledochocele, and should no longer be thought of as subtypes of CC. Our data demonstrate once again a persistent tendency to recommend expectant treatment in patients without symptoms and the extreme risk of nonexcisional treatment. The entire extrahepatic biliary tree should be removed when CC is diagnosed whether or not symptoms are present. The outcome of that approach was excellent.
INTRODUCTION
Described initially in 1852,1 congenital choledochal cysts (CCs) were separated into 3 types by Alonso-Lej et al 2 in 1959. Todani and colleagues3 modified this classification in 1977 adding types IV and V, and more recently Todani4 revised it further to reflect the presence of pancreaticobiliary maljunction. The Todani classification system, which has been widely adopted, includes no less than 8 separate alphanumeric subtypes (Figure 1). 5
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Figure 1. Todani classification of choledochal cysts (reprinted with permission from Todani et al5).
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Though the diagnosis of CC is most often made in childhood, 25% of patients are initially seen as adults.6-7 In the past, CCs were often treated using drainage procedures (cystoduodenostomy or cystojejunostomy),8-10 but it has since become clear that these operations have not only an unacceptable rate of long-term complications, most particularly malignant transformation, but also anastomotic stricture formation, cholangitis, pancreatitis, and biliary calculi.11-14 To prevent these long-term complications, cyst excision has been recommended for all patients, including those who have previously undergone drainage procedures.6-7,15-16 Our experience, however, indicates that the risks of temporizing are still underappreciated. In addition, confusion persists regarding the appropriate proximal and distal extent of cyst excision, particularly with regard to the treatment of intrahepatic disease. Our analysis of a large group of adult patients with this condition leads us to challenge the validity of the accepted classification system and to reemphasize the critical need for complete removal of the extrahepatic biliary tree.
METHODS
The clinical and laboratory findings of 39 adult patients who were treated for CCs at the University of California, San Francisco, from 1990 to 2004 were analyzed for demographic and clinical information. The preoperative data included the patient's age at diagnosis, manifesting symptoms, and the results of diagnostic tests. Preoperative radiographic imaging findings were reviewed to verify the morphologic condition of the biliary abnormalities. Ten patients had previously undergone 1 or more operations on the biliary tree (ie, cystoduodenostomy or cystojejunostomy) at other institutions. Details of the operations conducted at University of California, San Francisco were determined, including the extent of excision, technique of biliary reconstruction, perioperative course, complications, and outcome. Data are given as mean (SD) values unless otherwise noted. This study was reviewed and approved by the University of California, San Francisco Committee on Human Research.
RESULTS
Thirty-nine adults, 7 men (18%) and 32 women (82%), with congential CCs were treated between 1990 and 2004. Ten patients (26%) were Asian and 29 patients (74%) were white or Hispanic. The patient's mean age at initial diagnosis of CCs was 31 (17) years. The patient's mean age at the time of treatment at the University of California, San Francisco was 37 (14) years. The primary presenting symptom in 36 patients (92%) was abdominal pain. Eight patients (21%) had episodes of cholangitis, 6 (16%) pancreatitis, 5 (13%) jaundice or impaired liver function, and 4 (11%) weight loss. Three of 5 patients presenting with jaundice and 3 of 4 patients reporting weight loss were found to have cancer, which had arisen within the abnormal extrahepatic biliary tree. Nonspecific mild to moderate elevations of preoperative liver function test results and amylase levels were observed. The laboratory findings in patients with cancer did not differ from those with benign disease. Imaging studies were performed with the following frequency: endoscopic retrograde cholangiopancreaticography, 79%; computed tomography, 68%; ultrasonography, 65%; percutaneous transhepatic cholangiography, 18%; magnetic resonance imaging, 9%; oral cholecystogram, 3%; and hepato-iminodiacetic acid (lidofenin) scan, 3%. Each patient underwent a mean of 2.4 (0.9) preoperative imaging tests. In 30 patients (74%) the abnormality consisted primarily of dilation of the extrahepatic bile duct with less prominent dilation of the intrahepatic ducts (Todani type I); in 7 patients (18%) dilation of the extrahepatic bile ducts was accompanied by equally prominent dilation of the intrahepatic ducts (Todani type IVa); and 2 patients (5%) had lesions consisting of a polypoid diverticulum (similar in appearance to a gallbladder) attached to an otherwise normal bile duct (Todani type II). Deciding whether to call the disease type I or type IVa was arbitrary, because the intrahepatic ducts were never entirely normal in any patient with congenital dilation of the extrahepatic bile duct. The presence or absence of pancreaticobiliary maljunction was poorly documented in the patients who had undergone endoscopic retrograde cholangiopancreaticography.
Among the 31 patients with benign disease, 28 patients (90%) were treated by excision of the extrahepatic bile duct and gallbladder and reconstruction with a Roux-en-Y hepaticojejunostomy. One patient had excision of the duct and end-to-side hepaticoduodenostomy, 1 underwent a Whipple pancreaticoduodenectomy, and 1 underwent excision of a large distal remnant of a cyst that remained after partial resection and hepaticojejunostomy at another hospital. No patient underwent liver resection for intrahepatic involvement.
Eight patients (21%), whose mean age was 52 (15) years, presented with an invasive cancer. Six had cholangiocarcinoma and 2 had gallbladder cancer. The presence of the CC had been known for many years in 7 of 8 patients, whose earlier treatment had been limited to drainage (3 patients), expectant treatment (3 patients), or partial excision (1 patient). These patients and their operations are summarized in Table 1. In none of the patients with cancer was surgery not curative. One patient with carcinoma in situ in the excised cyst has had no evidence of further disease after 31 months.
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Table 1. Patients Presenting With Cancer
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Ten patients had undergone previous operations on their biliary tree at other hospitals (Table 2). Four (40%) of 10 patients were found to have cancer on evaluation at our institution. The mean interval between the first operation and the diagnosis of cancer in these patients was 26 years.
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Table 2. Patients Who Had Prior Operations
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Postoperative complications, most of which were minor, developed in 11 (29%) of 38 patients who underwent surgery. One patient required a second operation to revise a stricture at the hepaticojejunostomy anastomosis. One patient died of gastrointestinal hemorrhage from an arteriobiliary fistula after percutaneous transhepatic dilation of an anastomotic stricture.
COMMENT
As now used, the term choledochal cyst is unfaithful to the usual meaning of these words. Choledoch, a word that refers to the common bile duct, comes from the Greek words chole (bile) and dechomai (to receive). The word cyst, from the Greek kystis (sac, bladder), is conventionally defined as a closed cavity or sac lined by epithelium. Choledochal cyst, however, has escaped from this etymology and is used to cover the entire spectrum of congenital dilation throughout the biliary tree. Furthermore, the lesions are not really cysts
The cause of CCs is uncertain. Most patients with types I and IV lesions also have an anomalous pancreaticobiliary junction, in which the pancreatic duct joins the bile duct 1 to 2 cm proximal to the sphincter of Oddi.15, 17-18 This results in a common channel of 15 mm or more, which has been thought to allow reflux of pancreatic enzymes into the bile duct, increasing ductal pressure, and causing it to dilate.19 Experimental diversion of pancreatic juice into the bile duct produces progressive dilation in dogs.20 Nevertheless, a high junction is seen in about 9% of endoscopic retrograde cholangiopancreaticograms performed in patients without congenital choledochal cysts.18 Others have postulated that partial distal obstruction, whether due to a stricture, web, or sphincter of Oddi dysfunction, might have a causative role.15, 21-22 These theories are interesting but supported by sparse evidence. At most, they could only partially explain the pathogenesis since CCs occur without an anomalous biliary-pancreatic junction, anomalous junction is common in the absence of biliary disease, and pancreatic enzymes are not universally found within congenital CCs.
The first classification system for CCs was proposed by Alonso-Lej et al,2 but the most widely used one, authored by Todani and colleagues,3-4 includes 8 separate alphanumeric subtypes (Figure 1). Types I and IVa, which are variations of a single disease, account for more than 90% of the patients.6, 23-24 Type III cysts are better known as choledochoceles, and type V refers to Caroli disease. The type II lesions appear as a diverticulum of the common bile duct. Some such cases closely resemble gallbladder duplication while others are more rudimentary diverticular structures. There is no reason to believe that these choledochal diverticula are related to the more common congenital ductal dilation. In choledochoceles, the duct terminates in a small intramural cystic lesion lined by duodenal mucosa. Choledochocele has no clinical, pathologic, or etiologic relationship to CC, and most observers consider it to be a variant of duodenal duplication. Caroli disease is thought to arise from ductal plate malformation and is often associated with congenital hepatic fibrosis (with cirrhosis and portal hypertension).25 It is an autosomal recessive inherited condition with specific chromosomal abnormalities26-27 and clinically is associated with intrahepatic gallstone formation and a high incidence of renal disease. Although the radiologic findings in Caroli disease may resemble a CC, the other features show it to be a distinct, unrelated entity.
In the current series as well as in other reports,7, 28-29 many patients with CC presented with concomitant cancer. In the Japanese registry of 1353 patients, 16% overall had coincident cancer, increasing with each age of life decade from 2% for patients in their 20s, to 43% for those in their 60s.30 Type I and IV cysts have the highest risk of cancer,31 while cancer is rare in choledochoceles and gallbladder duplications.32-33 Caroli disease carries a small (about 7%) risk of cholangiocarcinoma,34-35 but most patients with Caroli disease require treatment for cholangitis or compromised liver function well before cancer appears.36 While most of the reported cases of cancer arising in CCs are cholangiocarcinoma within dilated extrahepatic bile ducts, 10% are gallbladder cancers.29 The overall survival following the diagnosis of cancer is poor, regardless of treatment. Few patients survive beyond 2 years.7, 28, 37-38
Thus, the pathogenesis, risk of malignancy, natural history, and treatment of CCs vary with each of the Todani subtypes except I and IV, which are the same condition. We believe the current classification system is a cause of confusion and has no discernible purpose. First, it incorporates 4 distinct diseases, and by grouping them together incorrectly suggests that they are related. Second, by separating types I and IV into different subtypes, a distinction is made that is artificial or at least greatly exaggerated. The intrahepatic ducts are almost always abnormal; just the magnitude varies (Figure 2). Furthermore, the intrahepatic dilation could either reflect congenital ectasia or stasis from the extrahepatic disease, and the contribution of each may be impossible to judge. We think discussions of these anomalies would be simplified and made more understandable by abandoning the numerical designations altogether and just re ferring to them according to the descriptive terms already in common use: CC, choledochal diverticulum, choledochocele, and Caroli disease (Figure 3). The term congenital CC should be reserved for the single condition made up of Todani types Ia through Ic and IVa. It would then be unnecessary to include cases of the unrelated anomalies in articles on congenital CCs.
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Figure 2. Endoscopic retrograde cholangiopancreaticogram showing Todani type I choledochal cyst (arrowhead), although the intrahepatic biliary tree is also abnormally dilated (arrows).
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Figure 3. Proposed new nomenclature of biliary lesions formerly all termed "choledochal cysts." The choledolchal cysts depicted are not meant to represent distinct subtypes, but merely to depict the spectrum of intrahepatic involvement.
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It has been suggested that cystenterostomy, by exposing the mucosa of the abnormal duct to pancreatic juice, may hasten the development of cancer in a choledochal cyst.24 But as mentioned earlier, time seems to be the dominant factor. Thus, the principal risk of a drainage procedure may be to render the patient asymptomatic until cancer appears many years later. Although for 30 years the literature on the surgical treatment of congenital CCs has stressed the superiority of cyst excision over a drainage procedure, drainage procedures may still be required under circumstances in which a more aggressive operation is too risky for technical or clinical reasons. What needs emphasis at this point is the importance of electively excising the abnormal bile duct later after the patient has recovered from the palliative bypass. Even some recent authors have equivocated on the indications for surgery in patients who have had a bypass. Two people in our series who had cystoduodenostomies in childhood had been told that they might some day need another operation but that they could wait until symptoms developed. The first symptoms, several decades later turned out to be from incurable cancer in the cyst. Three (30%) of 10 patients in the current series who had previously undergone cystenterostomy were found to have cancer on presentation at our institution. We recommend that any patient with a congenital CC who had had a bypass operation in childhood have the cyst excised before the age of 30 years whether or not symptoms are present.
Despite near universal recognition of the importance of excision, the specific surgical technique remains controversial, particularly with regard to the proximal and distal extent of resection 6, 39-40 and the conduit for reconstruction (ie, hepaticojejunostomy7, 41 vs hepaticojejuno-duodenostomy 42-43 vs appendicoduodenostomy44). The appropriate treatment for most patients with benign types I and IV cysts (regardless of any intrahepatic changes) is resection of the extrahepatic biliary tree and Roux-en-Y hepaticojejunostomy. This procedure, performed in 28 (90%) of our 31 patients with benign disease, eliminates the mucosa at highest risk for malignant degeneration. The resection should extend from the bifurcation of the lobar hepatic ducts into the parenchyma of the pancreas to a point just short of where the duct abruptly narrows to a 1- to 3-mm diameter. For the rare patient with extensive intrahepatic biliary dilation complicated by gallstone formation, cholangitis, or biliary cirrhosis, liver resection (for unilobar disease)2, 45 or transplantation (for bilobar disease)46 may be indicated. But we did not see such a case.
Several recent reports have described cases of cholangiocarcinoma that developed after excision of CCs.47-49 Cancer after excision is rare (<1%),30 with fewer than 30 cases reported to date. In most such cases the previous excision has been found to be incomplete.30, 47 After complete cyst removal, the risk of cholangiocarcinoma developing in the remaining ductal system is small. In fact, malignant degeneration in the intrahepatic ducts may be related to the enteric anastomosis itself rather than to any intrinsic quality of the biliary epithelium associated with CC disease.50 Therefore, more radical procedures—hepatic resection and transplantation—are unwarranted as prophylaxis against cancer, regardless of the extent of dilation of the intrahepatic ducts.
CONCLUSIONS
This series, one of the largest in North America, demonstrated the extreme risk of nonexcisional treatment of CCs. The standard classification scheme for CCs is confusing and inaccurate. The distinction between Todani type I and type IV cysts is arbitrary because the intrahepatic ducts are never completely normal. We believe that the numbered system of types should be abandoned, the term congenital CC should be reserved for the anomaly consisting of extrahepatic and variable degrees of intrahepatic dilation, and the other conditions should be called choledochocele, choledochal diverticulum, and Caroli disease. Patients whose cyst was bypassed in childhood should have the lesion excised before the age of 30 years. Patients diagnosed as having CCs as adults, regardless of symptoms, should undergo complete excision of the extrahepatic duct, cholecystectomy, and Roux-en-Y hepaticojejunostomy. The outcome of that approach was excellent.
AUTHOR INFORMATION
Correspondence: Lawrence W. Way, MD, University of California, San Francisco, 505 Parnassus Ave, Room S-550, San Francisco, CA 94143-0470 (wayl{at}surgery.ucsf.edu).
Accepted for publication April 9, 2004.
This paper was presented at the 75th Annual Meeting of the Pacific Coast Surgical Association; February 14, 2004; Maui, Hawaii; and is published after peer review and revision. The discussions that follow this article are based on the originally submitted manuscript and not the revised manuscript.
We thank Jeanne Koelling for the illustrations.
From the Department of Surgery, University of California, San Francisco.
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