Context
Choledochal cysts are rare and of unknown cause. Their presentation is protean, with the classical triad of pain, jaundice, and mass rarely seen. The potential complications are serious, including pancreatitis, cholangitis, and cholangiocarcinoma.
Objective
To present the current experience and evidence relating to all aspects of choledochal cysts to derive appropriate management recommendations.
Methods
Review of relevant literature in the English language indexed on MEDLINE.
Results
The elaboration of the classification of choledochal cysts. We describe the modes of presentation and optimal investigation and summarize the current theories on etiology and malignant transformation. The results of different management strategies are presented.
Conclusions
Choledochal cysts are often detected during the investigation of nonspecific symptoms, or even incidentally detected. Magnetic resonance imaging is the best imaging modality for the diagnosis and characterization of these cysts. Complete excision and hepaticojejenostomy is the management of choice.
CHOLEDOCHAL CYSTS are uncommon and of unknown cause, with an incidence of 0.1% even among adults referred for endoscopic retrograde cholangiopancreatography (ERCP) investigation.1 In a pediatric surgical unit in Spain, only 0.03% of the cases were for choledochal cyst disease.2 There is a higher incidence in females3,4 and they are more common in the Far East than in populations of Western European origin.5 The presentation is often vague and nonspecific, impeding prompt diagnosis. However, the diagnosis is facilitated by modern imaging techniques, and may be made at any time from the antenatal period to adult life. While some aspects of optimal management have been resolved, others remain controversial. The more severe complications of choledochal cyst disease include pancreatitis, cholangitis, biliary cirrhosis, and cholangiocarcinoma. This review considers the literature on choledochal cysts, concentrating particularly on current issues in management of the disease.
The most commonly used classification, developed by Alonso-Lej et al6 and modified by Todani et al,7 describes 5 broad types of choledochal cysts. The 2 relatively common categories of cyst are types I and IV-A. Type I, the most commonly reported overall, consists of dilatation of the common bile duct, which may be cystic, focal, or fusiform (subtypes A, B, and C, respectively). Type IV-A cysts are the second most common, defined as both intrahepatic and extrahepatic dilatation of the biliary tree. The remaining types are considerably rarer, with no large series published, and only sporadic reports appearing in the literature. Type II describes a saccular diverticulum off the common bile duct. Type III is represented by a cystic dilatation of the intramural portion of the common bile duct and is contended by some to represent a duodenal diverticulum rather than a choledochal cyst8 in view of the anatomical location and the duodenal epithelium with which they are always lined. The rare malformation of multiple extrahepatic cysts is designated type IV-B. Type V is synonymous with Caroli disease,9 describing multiple intrahepatic biliary dilatations.
The most commonly propounded theory for the etiology of choledochal cysts relates to the observation that they are often associated with an anomalous pancreatobiliary junction10 with a long common channel (>15 mm). This is purported to allow pancreatic juice to reflux into the biliary system11 and to cause increased pressure within the common bile duct,12 which, in combination, may cause ductal dilatation. More recently, abnormal function of the sphincter of Oddi has been reported to predispose to pancreatic reflux into the biliary tree,13 and spasm of the sphincter of Oddi has been noted to be associated with choledochal cysts.14 Animal models demonstrating progressive dilatation of the common bile duct following anastomosis of the common bile duct to the pancreatic duct support this theory.15 However, the possibility that such challenging surgery may result in at least partial obstruction of the biliary system, and that in fact obstruction causes the dilatation rather than pancreatic juice reflux, cannot be entirely discounted. There is also some clinical evidence suggesting that anomalous pancreaticobiliary duct union is not responsible for choledochal cysts, at least not entirely.
First, anomalous pancreatobiliary union is detected in 57% to 96%11,12,16-18 of cases of choledochal cyst, and therefore cannot account for the minority of cases with normal ductal entry into the ampulla of Vater. Second, it seems that choledochal cysts diagnosed antenatally do not have pancreatic juice reflux into the common bile duct,19 and that the concentration of biliary amylase rises with age at presentation, increasing the possibility that the reflux may occur in part as a result of choledochal cysts, but not necessarily as the cause. Another study20 of children with choledochal cysts found that 10 of 24 children had no activation of pancreatic enzymes in the common bile duct, and of these, 8 were younger than 2 months; therefore, pancreatic reflux is an unlikely candidate for the cause of these choledochal cysts.
A second possible cause of choledochal cysts has already been alluded to, in suggesting an alternative interpretation of the animal experiments anastomosing the common bile duct to the pancreatic duct as discussed previously.20 Obstruction of the common bile duct is another etiological theory for choledochal cysts and is also supported by other animal models. In neonatal animal models, ligation of the common bile duct causes a dilatation morphologically resembling a type I choledochal cyst; whereas in adults, generalized dilatation of the whole biliary system can be seen.21 Clinically, there is some evidence to support the theory that obstruction of the distal common bile duct may cause choledochal cysts. A case report of an antenatally diagnosed choledochal cyst found complete distal obstruction of the lower end of the common bile duct.22 Another case report found a congenital web at the lower end of the common bile duct in association with a type I choledochal cyst.8 The abnormal function of the sphincter of Oddi, reported in some studies to be associated with choledochal cysts, may represent a functional obstruction to the common bile duct, thus predisposing to choledochal cysts.14,23 This functional obstruction at the sphincter of Oddi also predisposes to pancreatic juice reflux into the biliary tree.24
These putative causes are not necessarily contradictory, as a distal common duct obstruction may coincide with an anomalous pancreaticobiliary union. It is conceivable that when such a coincidence occurs, both mechanisms act in tandem.
Some further observations have been made, which may be relevant to the etiology of choledochal cysts. One such observation is that the distal common bile duct has inadequate autonomic innervation.25,26 Kusunoki et al25 showed that there are abnormally few ganglion cells in the narrow portion if the common bile duct in patients with a choledochal cyst, as compared with controls. Presumably, this would result in a functional obstruction and proximal dilatation in the same manner as achalasia of the esophagus or Hirschprung disease.
Real-time polymerase chain reaction has been used to demonstrate high levels of reoviral RNA in biliary tissues from patients with choledochal cysts compared with controls.27 It is possible only to speculate as to how this may result in choledochal cysts. Perhaps viral infection of ganglion neurons causes the oligoganglionosis as discussed above, and perhaps viral infection triggers an immune response, which is subsequently responsible for fibrosis of the lower end of the biliary tract.
There are few reports of familial cases of choledochal cysts and associated anomalies. A pair of monozygotic twins were discordant for the occurrence of anomalous pancreaticobiliary junction and choledochal cyst, suggesting that there is not a strong genetic basis for these malformations.28 However, there may be some genetic predisposition, as there are reports of a mother and daughter29 and of dizygotic twins30 having choledochal cysts. Interestingly, in both reports, the cysts are of different Todani types; therefore, if there is a genetic basis for the predisposition in the families described, then it would seem to affect the biliary tree globally.
On balance, the weight of the evidence seems to support distal common bile duct obstruction (either anatomical or functional) and raised intraductal pressure as the most likely cause of choledochal cysts. The high incidence of anomalous pancreaticobiliary union cannot be ignored, but may just reflect an association with distal obstruction. Alternatively, pancreatic juice reflux into the common bile duct may be activated by bile,31 and activated enzymes subsequently weaken the common bile duct wall, exacerbating the dilatation.
Type IV-A cysts are more common in adults than in children,32 raising the possibility that although the lesions may be congenital, they may progress with time.
The classical triad of jaundice, right upper quadrant mass, and abdominal pain is present in only a minority of patients (0%-17%).3,17,33-35 It is more commonly seen in cases with onset in childhood rather than in adults, and 85% of children have at least 2 features of the triad at presentation, compared with only 25% of adults.36
Antenatal diagnoses can be made on ultrasound,37 although diagnostic accuracy from this technique has been reported to be as low as 15%,38 and it is not possible to differentiate between biliary atresia and choledochal cysts with antenatal ultrasound.39 Although 1 of 2 case reports suggests that serial antenatal ultrasound may permit the differential according to relative rates of enlargement of the duct diameter,40 further work to substantiate this supposition is required. However, neonates diagnosed antenatally are often asymptomatic at birth,41 so antenatal detection allows surgical intervention prior to the onset of complications from choledochal cysts.
Among the more commonly reported presenting features are cholangitis,34,42,43 pancreatitis,34,43-45 and biliary peritonitis from cyst rupture.34,46-48 Among adults, choledochal cysts are quite often incidental findings during investigation for other problems.34,49-51
Rarer presentations include gastric outlet obstruction,42 neonatal bleeding tendency,52 duodenal intusussecption,53 and portal hypertension.54
The presentations of choledochal cysts are clearly protean, and prompt diagnosis relies on a high index of suspicion, aided by modern imaging techniques. Foremost among the differential diagnoses of dilatation of the common bile duct in children is biliary atresia.40,55-57 In adults, the diagnosis is only sporadically in doubt preoperatively, owing to the quality of modern imaging. Stone impaction with proximal dilatation has been reported to mimic choledochal cysts.58 One adult thought to have a pancreatic pseudocyst was found to have a cholodochal cyst at operation59; this is easy to understand in view of the high incidence of pancreatitis caused by choledochal cysts. Another case report mistook primary sclerosing cholangitis for a cholodochal cyst.60
Ultrasound can diagnose choledochal cysts with a specificity of 97% in children,55 although this drops to 71% if the width criteria are reduced to increase sensitivity, with normal variants and secondary causes of biliary dilatation being misdiagnosed as choledochal cysts. Another study found that ultrasound successfully diagnosed 15 of 19 children younger 6 months with choledochal cysts.37 Ultrasound is therefore an excellent first-line investigation of neonatal jaundice persisting more than 2 weeks after birth,56 and may help to differentiate choledochal cysts from biliary atresia.57
Radionucleotide Scintigraphy
Scintigraphy is safe and atraumatic, and has been used for a long time in the diagnosis of choledochal cysts.59,61 Following the progression of an isotope from the biliary tract into the small intestine is reported to distinguish with 100% accuracy between choledochal cysts and biliary atresia.62 Type I cysts may be diagnosed with a sensitivity of 100%, but only two thirds of type IV disease is detected, and the extent of the intrahepatic disease may be underestimated on scintigraphy.63
Computed Tomographic Scan
Although there are reports of computed tomographic (CT) scans diagnosing choledochal cysts,64 others have found that cysts are missed on CT scans, and picked up on magnetic resonance cholangiopancreatography (MRCP).65 A comparative study of 14 patients with choledochal cysts was performed, in which each patient had both CT cholangiography and MRCP performed.66 The MRCP investigation was superior at detecting and defining lesions. A better role for CT scanning may be in the postoperative period, where it was shown to be superior to MRCP in locating the biliary-enteric anastomosis and in defining any stenosis thereof.
Endoscopic Retrograde Cholangiopancreatography
Investigation with ERCP is an excellent tool for defining biliary anatomy, and as such has been used to diagnose cholodochal cysts.67-69 However, MRCP has been shown to be just as good as70,71 if not better than70 ERCP, without the potential complications of the latter, invasive technique.70
Magnetic Resonance Cholangiopancreatography
For the reasons outlined above, MRCP represents the current "gold standard" in the imaging of choledochal cysts. There are a few caveats to this. Although the technique is excellent for diagnosing and characterizing the cysts themselves, it is not so good at detecting anomalous pancreaticobiliary union.72,73 This is probably not all that important in determining patient management. Also, MRCP may not be as sensitive a tool in pediatric cases as it is in adults,71 where ultrasound has a preeminant role.
This is quite a common presentation of choledochal cysts, as described earlier. This may be due to the activation of pancreatic enzymes by bile reflux,31 in association with an anomalous pancreaticobiliary union. Certainly, the anomalous ductal union seems to predispose to pancreatitis, as in one study, 57% of patients with choledochal cysts had anomalous ductal union demonstrated by ERCP. All of these patients suffered pancreatitis. Only a third of patients with normal ducts had pancreatitis.16
As with pancreatitis, cholangitis is a common complication of choledochal cysts and may be the presenting feature as mentioned earlier. It is also a commonly reported complication after surgical management.
This has been reported to be the presenting feature in 10% of children in one series,34 and in biopsies obtained during surgery, it has been found to occur in 40% to 50% of cases.37,74 In one series, liver changes, including bile duct proliferation, cholestasis, parenchymal damage, inflammatory cell infiltration, and pericentral fibrosis, were present in all livers on which biopsies were performed, irrespective of liver function and macroscopic liver appearance.74 In the same study, postoperative mortality from hepatic insufficiency occurred in 2 of 6 patients found to have biliary cirrhosis at surgery. All the studies cited earlier relate to infants and children, and emphasize the need for prompt treatment prior to the development of established cirrhosis.75
The prognosis for patients with cholangiocarcinoma arising in choledochal cysts is as grim as for cholangiocarcinoma in general, with median survival reported in the range of 6 to 21 months.76-78 The incidence of malignancy in choledochocoeles is reported at between 10% and 30%.18,42,76,78-80 Malignant change in association with choledochal cysts has been reported in pediatric cases,81 and it should therefore be suspected in any choledochal cyst appearing after infancy.
The pathogenesis of cholangiocarcinoma in choledochal cysts may be caused by the carcinogenic effect of pancreatic reflux.79 Supporting this contention is a study noting that the risk of cholangiocarcinoma in cysts is much higher in patients with anomalous pancreaticobiliary union (32%) than in those without (0%).18 It seems that the presence of anomalous ductal union may be even more important than that of choledochal cyst, as one study found a 55% rate of biliary tract malignant neoplasia in patients with duct malunion, and only a 5% rate in patients without, whether (n = 14) or not (n = 4) choledochal cyst was present.82 The incidence of gallbladder carcinoma in patients with ductal malunion without choledochal cyst was 50% in another study, and only 5% in patients with malunion and choledochal cysts.83 In the patients without cysts, all the biliary malignancies were in the gallbladder, whereas in the patients with cysts, in addition to the 5% with gallbladder cancer, 14% had cholangiocarcinoma arising in the cyst.
It has been demonstrated that the histological changes in choledochal cysts progress with patient age at presentation, through epithelial denudement to inflammatory infiltrates, glandular metaplasia, and ultimately, malignancy.84
Putting these findings together, it is conceivable that pancreatic juice reflux secondary to anomalous ductal union is the predisposing factor for biliary tract malignancy, and that malignancy occurs in a region of biliary stasis, where the exposure to the refluxed pancreatic juice is prolonged. In the presence of a cyst of the common bile duct, this would be closer to the anomalous ductal union than the gallbladder, and therefore, more at risk of malignant change. In the absence of a choledochal cyst, the gallbladder is the only site of biliary stagnation.
There are some reports of malignant change in choledochal cysts by Todani classification that are relevant to management. Although it has been reported that type III cysts rarely undergo malignant change,85 there are reports of malignancy arising in choledochocoeles,86 and in a series of 11 patients with type III cysts, 3 contained cholangiocarcinoma at the time of diagnosis.79 In type IV-A disease, there are reports of malignancy arising in the intrahepatic dilated ducts, rather than in the common bile duct cysts.87,88 The management implications of these observations are discussed in the subsequent section.
Excision vs Internal Drainage Procedures
Historically, a cholecystoenterostomy was considered a surgical management option for choledochal cysts. However, the most recent articles to advocate this approach were published in the 1970s.89,90 This approach has been abandoned in favor of cyst excision with hepaticoenterostomy, to reduce the complications of the former procedure. These include malignancy in the remaining cyst,91 pancreatitis,91 and cholangitis.34,92,93
When a patient has previously been treated by a cyst-enterotomy internal drainage procedure, 70% of patients require reoperation for the occurrence of complications, including cholangitis and hepatolithiasis.94 Indeed it has been recommended that patients who have previously undergone internal drainage procedures should undergo reoperation with cyst excision (even if asymptomatic) as prophylaxis against complications in particular cases of malignant cysts,95 even though the complications of surgery for excision after previous internal drainage procedure are more frequent than those seen after primary cyst excision.96
The timing of surgery should be early after diagnosis to reduce the incidence of complications described,97 and particularly to prevent liver damage in neonates.75
Malignant Change After Cyst Excision
Even after cyst excision, there are reports of malignancy occurring, often relating to incomplete cyst excision. There is a series dissenting this, with a zero rate of postexcision malignancy in 37 patients, even though the excision was known to be incomplete in 28 cases.98 However, in a comprehensive review, the incidence of postexcision malignancy has been estimated at 0.7%.99
This may occur in the residual intrapancreatic portion of the choledochal cyst excision.99-102 The recognition of this danger has driven the trend toward excision of the intrapancreatic portion of the common bile duct103 to the point of demonstrating the pancreaticobiliary duct union to ensure complete excision.104
The extent of the resection in type IV-A cysts is controversial. Several authors advocate management by excision of the extrahepatic component only, with hepaticoenterostomy.41,105-107 However, malignancy has been reported to arise in the intrahepatic cysts as described above, and it has also been reported to occur after resection of the extrahepatic cyst with hepaticojejunostomy.108 Clearly, when the intrahepatic cysts are widespread, they cannot be excised; however, when the intrahepatic disease is localized, it would seem reasonable to perform the relevant partial hepatectomy. This approach has been practiced by other authors.32,76,109 For the same reason, partial hepatectomy has been practiced for Caroli disease.110
There is a report of cylindrical intrahepatic ductal dilatation in type IV-A disease regressing spontaneously after common duct excision and hepaticojejunostomy, compared with cystic intrahepatic disease, which does not regress.111 However, it seems likely that the cylindrical intrahepatic disease represents a type I cyst with an element of obstruction causing proximal dilatation, rather than a true type IV-A disease.
Choledochocoeles: An Exception to the Rule?
The malignant potential of type III cysts has been questioned in a review of 65 choledochocoeles,85 and for this reason they are often treated as the exception to the rule, by drainage into the duodenum at the ampulla, rather than by excision.41,64,92,105 The enourmous attraction of this approach is that it may be performed endoscopically by sphincterotomy.107,112-115 However, as described above, malignancy does occur in type III cysts, and in one series in 3 of 11 patients.79 It is perhaps odd then that in the literature there are no advocates for the excision of choledochocoeles.
Reconstruction of Biliary Drainage
The most common reconstruction following cyst excision is a hepaticojejunostomy or choledochojejunostomy,35,37,41,92,105 with the former thought to reduce the incidence of stricture formation postoperatively.116 Alternatives that have been suggested include hepaticoduodenostomy so that the anastomosis is accessible to ERCP in the event of postoperative complications,117 and hepaticoantrostomy apparently for a more physiological result.118 Neither hepaticoduodenostomy nor hepaticoantrostomy have been widely adopted; the former perhaps because there are other ways of providing access to a biliary-enteric anastomosis without the relatively high risk of complications from a duodenal anastomosis. The latter may have had a variety of potential problems if the experience reported following a choledochal cystogastrostomy is anything to go by.119 The technique of appendix interposition hepaticoenterostomy similarly failed to gain widespread acclaim, as the appendix grafts underwent stenosis, and as a result, there was significant hepatic fibrosis secondary to obstruction.120
Postoperative Complications
Postoperative anastomotic strictures are a common problem121-124 and are associated with intrahepatic cholelithiasis123-125 and cholangitis.126 Intrahepatic stones are particularly a problem in cases of type IV-A disease with residual intrahepatic cysts.36
The incidence of anastomotic stricture formation may be reduced by performing a higher anastomosis, as Todani121 found that 9 of 22 choledochojejunostomies had postoperative anastomotic strictures, compared with 1 of 82 hepaticojejunostomies. Choledochoscopy at the time of surgery to detect and remove intrahepatic stones at operation reduces postoperative complications of cholelithiasis.127 Roux-en-Y limb stomas128 and Hutson129 access limbs have been used to facilitate endoscopic access to anastomotic strictures.
Recently, laparoscopic cyst excision and hepaticojejunostomy have been described51,130-132 It is too early to assess the long-term results of this approach in terms of anastomotic strictures and malignancy arising in residual cyst tissue.
Choledochal cysts are uncommon, but when encountered, they may appear nonspecifically rather than classically, and a high index of suspicion will avoid a delay in diagnosis. The imaging modality of choice for diagnosing and characterizing choledochal cysts is MRCP. Delayed diagnosis may have a variety of undesirable sequelae including biliary cirrhosis, cholangiocarcinoma, pancreatitis, and cholangitis. To avoid these complications, choledochal cysts should be treated by complete excision wherever possible, with the possible exception of type III duodenal intramural cysts, which are often treated by endoscopic sphincterotomy. The approaches to intrahepatic disease and postoperative complications have also been discussed.
Corresponding author: Guy J. Maddern, University of Adelaide Department of Surgery, the Queen Elizabeth Hospital, Woodville Rd, Woodville, SA 5011 Australia (e-mail: guy.maddern@adelaide.edu.au).
Accepted for publication November 3, 2002.
1.Schmidt
HGBauer
JWiessner
VSchonekas
H Endoscopic aspects of choledochoceles.
Hepatogastroenterology. 1996;43143- 146
Google Scholar 2.Moreno Gonzalez
EGarcia Garcia
I
et al. Choledochal cyst resection and reconstruction by biliary-jejuno-duodenal diversion.
World J Surg. 1989;13232- 237
Google ScholarCrossref 3.Watanatittan
SNiramis
R Choledochal cyst: review of 74 pediatric cases.
J Med Assoc Thai. 1998;81586- 595
Google Scholar 4.Chen
HMJan
YYChen
MF
et al. Surgical treatment of choledochal cyst in adults: results and long-term follow-up.
Hepatogastroenterology. 1996;431492- 1499
Google Scholar 5.Juttijudata
PChiemchaisri
CPalavatana
CChurnratanakul
S Causes of cholestasis in Thailand: a study of 276 consecutive patients.
Am J Surg. 1984;147360- 366
Google ScholarCrossref 6.Alonso-Lej
FRever
WBJPessagno
DJ Congenital choledochal cysts, with a report of 2, and an analysis of 94 cases.
Surg Gynecol Obstet. 1959;1081- 30
Google Scholar 7.Todani
TWatanabe
YNarusue
MTabuchi
KOkajima
K Congenital bile duct cysts: classification, operative procedures, and review of thirty-seven cases including cancer arising from choledochal cyst.
Am J Surg. 1977;134263- 269
Google ScholarCrossref 8.Gorenstein
LStrasberg
SM Etiology of choledochal cysts: two instructive cases.
Can J Surg. 1985;28363- 367
Google Scholar 9.Caroli
JSoupalt
JKossakowski
LPlocker
LParadowska
M La digitation polykstique congenitale des voico biliares intrahepatiques; essai de classification.
Semin Hop Paris. 1958;34488- 495
Google Scholar 10.Babbitt
DP Congenital choledochal cysts: new etiological concepts on anomalous relationships of the common bile duct and pancreatic bulb.
Ann Radiol (Paris). 1969;12231- 240
Google Scholar 11.Zhao
LLi
ZMa
H
et al. Congenital choledochal cyst with pancreatitis.
Chin Med J (Engl). 1999;112637- 640
Google Scholar 12.Iwai
NYanagihara
JTokiwa
KShimotake
TNakamura
K Congenital choledochal dilatation with emphasis on pathophysiology of the biliary tract.
Ann Surg. 1992;21527- 30
Google ScholarCrossref 13.Imazu
MIwai
NTokiwa
KShimotake
TKimura
OOno
S Factors of biliary carcinogenesis in choledochal cysts.
Eur J Pediatr Surg. 2001;1124- 27
Google ScholarCrossref 14.Schweizer
PSchweizer
M Pancreaticobiliary long common channel syndrome and congenital anomalous dilatation of the choledochal duct: study of 46 patients.
Eur J Pediatr Surg. 1993;315- 21
Google ScholarCrossref 15.Ohkawa
HSawaguchi
SYamazaki
YIshikawa
AKikuchi
M Experimental analysis of the effect of anomalous pancreaticobilliary ductal union.
J Pediatr Surg. 1982;177- 13
Google ScholarCrossref 16.Swisher
SGCates
JAHunt
KK
et al. Pancreatitis associated with adult choledochal cysts.
Pancreas. 1994;9633- 637
Google ScholarCrossref 17.Stringer
MDDhawan
ADavenport
MMieli-Vergani
GMowat
APHoward
ER Choledochal cysts: lessons from a 20 year experience.
Arch Dis Child. 1995;73528- 531
Google ScholarCrossref 18.Song
HKKim
MHMyung
SJ
et al. Choledochal cyst associated the with anomalous union of pancreaticobiliary duct (AUPBD) has a more grave clinical course than choledochal cyst alone.
Korean J Intern Med. 1999;141- 8
Google Scholar 19.Davenport
MStringer
MDHoward
ER Biliary amylase and congenital choledochal dilatation.
J Pediatr Surg. 1995;30474- 477
Google ScholarCrossref 20.Yamashiro
YSato
MShimizu
TOguchi
SMiyano
T How great is the incidence of truly congenital common bile duct dilatation?
J Pediatr Surg. 1993;28622- 625
Google ScholarCrossref 21.Spitz
L Experimental production of cystic dilatation of the comon bile duct in lambs.
J Pediatr Surg. 1977;1239
Google ScholarCrossref 22.Tsang
TMTam
PKChamberlain
P Obliteration of the distal bile duct in the development of congenital choledochal cyst.
J Pediatr Surg. 1994;291582- 1583
Google ScholarCrossref 23.Ponce
JGarrigues
VSala
TPertejo
VBerenguer
J Endoscopic biliary manometry in patients with suspected sphincter of Oddi dysfunction and in patients with cystic dilatation of the bile ducts.
Dig Dis Sci. 1989;34367- 371
Google ScholarCrossref 24.Iwai
NTokiwa
KTsuto
TYanagihara
JTakahashi
T Biliary manometry in choledochal cyst with abnormal choledochopancreatico ductal junction.
J Pediatr Surg. 1986;21873- 876
Google ScholarCrossref 25.Kusunoki
MSaitoh
NYamamura
TFujita
STakahashi
TUtsunomiya
J Choledochal cysts: oligoganglionosis in the narrow portion of the choledochus.
Arch Surg. 1988;123984- 986
Google ScholarCrossref 26.Shimotake
TIwai
NYanagihara
JInoue
KFushiki
S Innervation patterns in congenital biliary dilatation.
Eur J Pediatr Surg. 1995;5265- 270
Google ScholarCrossref 27.Tyler
KLSokol
RJOberhaus
SM
et al. Detection of reovirus RNA in hepatobiliary tissues from patients with extrahepatic biliary atresia and choledochal cysts.
Hepatology. 1998;271475- 1482
Google ScholarCrossref 28.Uchida
MTsukahara
MFuji
TFujihara
TUeki
KKajii
T Discordance for anomalous pancreaticobiliary ductal junction and congenital biliary dilatation in a set of monozygotic twins.
J Pediatr Surg. 1992;271563- 1564
Google ScholarCrossref 29.Iwata
FUchida
AMiyaki
T
et al. Familial occurrence of congenital bile duct cysts.
J Gastroenterol Hepatol. 1998;13316- 319
Google ScholarCrossref 30.Lane
GJYamataka
AKobayashi
HSegawa
OMiyano
T Different types of congenital biliary dilatation in dizygotic twins.
Pediatr Surg Int. 1999;15403- 404
Google ScholarCrossref 31.Nakamura
TOkada
AHigaki
JTojo
HOkamoto
M Pancreaticobiliary maljunction-associated pancreatitis: an experimental study on the activation of pancreatic phospholipase A2.
World J Surg. 1996;20543- 550
Google ScholarCrossref 32.Todani
TNarusue
MWatanabe
YTabuchi
KOkajima
K Management of congenital choledochal cyst with intrahepatic involvement.
Ann Surg. 1978;187272- 280
Google ScholarCrossref 33.Sherman
PKolster
EDavies
CStringer
DWeber
J Choledochal cysts: heterogeneity of clinical presentation.
J Pediatr Gastroenterol Nutr. 1986;5867- 872
Google ScholarCrossref 34.Samuel
MSpitz
L Choledochal cyst: varied clinical presentations and long-term results of surgery.
Eur J Pediatr Surg. 1996;678- 81
Google ScholarCrossref 35.Rattan
KNKhurana
PBudhiraja
SMalik
VPandit
SK Choledochal cyst: a 10-year experience.
Indian J Pediatr. 2000;67657- 659
Google ScholarCrossref 36.Lipsett
PAPitt
HAColombani
PMBoitnott
JKCameron
JL Choledochal cyst disease: a changing pattern of presentation.
Ann Surg. 1994;220644- 652
Google ScholarCrossref 37.Cheng
MTChang
MHHsu
HY
et al. Choledochal cyst in infancy: a follow-up study.
Acta Paediatr Taiwan. 2000;4113- 17
Google Scholar 38.Redkar
RDavenport
MHoward
ER Antenatal diagnosis of congenital anomalies of the biliary tract.
J Pediatr Surg. 1998;33700- 704
Google ScholarCrossref 39.Mackenzie
TCHowell
LJFlake
AWAdzick
NS The management of prenatally diagnosed choledochal cysts.
J Pediatr Surg. 2001;361241- 1243
Google ScholarCrossref 40.Matsubara
HOya
NSuzuki
Y
et al. Is it possible to differentiate between choledochal cyst and congenital biliary atresia (type I cyst) by antenatal ultrasonography?
Fetal Diagn Ther. 1997;12306- 308
Google ScholarCrossref 41.Rha
SYStovroff
MCGlick
PLAllen
JERicketts
RR Choledochal cysts: a ten year experience.
Am Surg. 1996;6230- 34
Google Scholar 42.Jan
YYChen
HMChen
MF Malignancy in choledochal cysts.
Hepatogastroenterology. 2002;49100- 103
Google Scholar 43.Karanikas
IDKoundourakis
SSMacheras
ANPanagiotidis
HCLiakakos
TDDendrinos
SS Long-term results of management of type I choledochal cysts in adults.
Acta Chir Belg. 1997;9713- 18
Google Scholar 44.Lin
JTHChen
YHNi
YHLai
HSPeng
SS Magnetic resonance cholangiopancreatography diagnosed pancreatitis associated choledochal cyst: report of one case.
Acta Paediatr Taiwan. 2001;42363- 366
Google Scholar 45.Weisser
MBennek
JHormann
D Choledochocele: a rare cause of necrotising pancreatitis in childhood.
Eur J Pediatr Surg. 2000;10258- 264
Google ScholarCrossref 46.Seema
Not AvailableSharma
ASeth
ATaluja
VBagga
DAneja
S Spontaneous rupture of choledochal cyst.
Indian J Pediatr. 2000;67155- 156
Google ScholarCrossref 47.Lin
SLShan
KMHung
YBNg
SHLin
CY Choledochal cyst associated with acute acalculous cholecystitis.
J Pediatr Gastroenterol Nutr. 2000;31307- 308
Google ScholarCrossref 48.Ando
KMiyano
TKohno
STakamizawa
SLane
G Spontaneous perforation of choledochal cyst: a study of 13 cases.
Eur J Pediatr Surg. 1998;823- 25
Google ScholarCrossref 49.Sato
MIshida
HKonno
K
et al. Choledochal cyst due to anomalous pancreatobiliary junction in the adult: sonographic findings.
Abdom Imaging. 2001;26395- 400
Google ScholarCrossref 50.Kim
JELee
JKLee
KT
et al. The clinical significance of common bile-duct dilatation in patients without biliary symptoms or causative lesions on ultrasonography.
Endoscopy. 2001;33495- 500
Google ScholarCrossref 51.Liu
DCRodriguez
JAMeric
FGeiger
JL Laparoscopic excision of a rare type II choledochal cyst: case report and review of the literature.
J Pediatr Surg. 2000;351117- 1119
Google ScholarCrossref 52.Ono
STokiwa
KAoi
SIwai
NNakanoin
H A bleeding tendency as the first symptom of a choledochal cyst.
Pediatr Surg Int. 2000;16111- 112
Google ScholarCrossref 53.Ramos
ACastello
JPinto
I Intestinal intussusception as a presenting feature of choledochocele.
Gastrointest Radiol. 1990;15211- 214
Google ScholarCrossref 55.Lee
HCYeung
CYChang
PYSheu
JCWang
NL Dilatation of the biliary tree in children: sonographic diagnosis and its clinical significance.
J Ultrasound Med. 2000;19177- 184
Google Scholar 56.Gubernick
JARosenberg
HKIlaslan
HKessler
A US approach to jaundice in infants and children.
Radiographics. 2000;20173- 195
Google ScholarCrossref 57.Kim
WSKim
IOYeon
KMPark
KWSeo
JKKim
CJ Choledochal cyst with or without biliary atresia in neonates and young infants: US differentiation.
Radiology. 1998;209465- 469
Google Scholar 58.Aggarwal
SKumar
ARoy
SBandhu
S Massive dilatation of the common bile duct resembling a choledochal cyst.
Trop Gastroenterol. 2001;22219- 220
Google Scholar 59.Rosenfield
NGriscom
NT Choledochal cysts: roentgenographic techniques.
Radiology. 1975;114113- 119
Google Scholar 60.Postema
RRHazebroek
FW Choledochal cysts in children: a review of 28 years of treatment in a Dutch children's hospital.
Eur J Surg. 1999;1651159- 1161
Google ScholarCrossref 61.Oshiumi
YNakayama
CMorita
KNumaguchi
YKoga
IMatsuura
K Serial scintigraphy of choledochal cysts using 131I-rose bengal and 131I-bromsulphalein.
AJR Am J Roentgenol. 1977;128769- 771
Google ScholarCrossref 62.Johnson
KAlton
HMChapman
S Evaluation of mebrofenin hepatoscintigraphy in neonatal-onset jaundice.
Pediatr Radiol. 1998;28937- 941
Google ScholarCrossref 63.Rajnish
AGambhir
SDas
BKSaxena
R Classifying choledochal cysts using hepatobiliary scintigraphy.
Clin Nucl Med. 2000;25996- 999
Google ScholarCrossref 64.Groebli
YMeyer
JLTschantz
P Choledochocele demonstrated by computed tomographic cholangiography: report of a case.
Surg Today. 2000;30272- 276
Google ScholarCrossref 65.De Backer
AIVan den Abbeele
KDe Schepper
AMVan Baarle
A Choledochocele: diagnosis by magnetic resonance imaging.
Abdom Imaging. 2000;25508- 510
Google ScholarCrossref 66.Lam
WWLam
TPSaing
HChan
FLChan
KL MR cholangiography and CT cholangiography of pediatric patients with choledochal cysts.
AJR Am J Roentgenol. 1999;173401- 405
Google ScholarCrossref 67.Park
KBAuh
YHKim
JH
et al. Diagnostic pitfalls in the cholangiographic diagnosis of choledochoceles: cholangiographic quality and its effect on visualization.
Abdom Imaging. 2001;2648- 54
Google ScholarCrossref 68.Kabra
VAgarwal
MAdukai
TKDixit
VKAgrawal
AKShukla
VK Choledochal cyst: a changing pattern of presentation.
ANZ J Surg. 2001;71159- 161
Google ScholarCrossref 69.Kim
MHMyung
SJLee
SK
et al. Ballooning of the papilla during contrast injection: the semaphore of a choledochocele.
Gastrointest Endosc. 1998;48258- 262
Google ScholarCrossref 70.Kim
SHLim
JHYoon
HKHan
BKLee
SKKim
YI Choledochal cyst: comparison of MR and conventional cholangiography.
Clin Radiol. 2000;55378- 383
Google ScholarCrossref 71.Irie
HHonda
HJimi
M
et al. Value of MR cholangiopancreatography in evaluating choledochal cysts.
AJR Am J Roentgenol. 1998;1711381- 1385
Google ScholarCrossref 72.Govil
SJustus
AKorah
IPerakath
AZachariah
NSen
S Choledochal cysts: evaluation with MR cholangiography.
Abdom Imaging. 1998;23616- 619
Google ScholarCrossref 73.Miyazaki
TYamashita
YTang
YTsuchigame
TTakahashi
MSera
Y Single-shot MR cholangiopancreatography of neonates, infants, and young children.
AJR Am J Roentgenol. 1998;17033- 37
Google ScholarCrossref 74.Nambirajan
LTaneja
PSingh
MKMitra
DKBhatnagar
V The liver in choledochal cyst.
Trop Gastroenterol. 2000;21135- 139
Google Scholar 75.Suita
SShono
KKinugasa
YKubota
MMatsuo
S Influence of age on the presentation and outcome of choledochal cyst.
J Pediatr Surg. 1999;341765- 1768
Google ScholarCrossref 77.Jan
YYChen
HMChen
MF Malignancy in choledochal cysts.
Hepatogastroenterology. 2000;47337- 340
Google Scholar 80.Tsuchiya
RHarada
NIto
TFurukawa
MYoshihiro
I Malignant tumors in choledochal cysts.
Ann Surg. 1977;18622- 28
Google ScholarCrossref 81.Iwai
NDeguchi
EYanagihara
J
et al. Cancer arising in a choledochal cyst in a 12-year-old girl.
J Pediatr Surg. 1990;251261- 1263
Google ScholarCrossref 82.Kato
OHattori
KSuzuki
TTachino
FYuasa
T Clinical significance of anomalous pancreaticobiliary union.
Gastrointest Endosc. 1983;2994- 98
Google ScholarCrossref 83.Chijiiwa
KKimura
HTanaka
M Malignant potential of the gallbladder in patients with anomalous pancreaticobiliary ductal junction: the difference in risk between patients with and without choledochal cyst.
Int Surg. 1995;8061- 64
Google Scholar 84.Komi
NTamura
TTsuge
SMiyoshi
YUdaka
HTakehara
H Relation of patient age to premalignant alterations in choledochal cyst epithelium: histochemical and immunohistochemical studies.
J Pediatr Surg. 1986;21430- 433
Google ScholarCrossref 85.Tajiri
H Choledochocele-containing stones.
Am J Gastroenterol. 1996;911046- 1048
Google Scholar 86.Pisano
GDonlon
JBPlatell
CHall
JC Cholangiocarcinoma in a type III choledochal cyst.
Aust N Z J Surg. 1991;61855- 857
Google ScholarCrossref 87.Kawamoto
SHiraoka
TMaruta
SWatanabe
EKanemitsu
KTsuji
T A case of early cancer in cystic intrahepatic duct associated with congenital choledochal cyst.
Hepatogastroenterology. 1998;45428- 432
Google Scholar 88.Tajiri
KTakenawa
HYamaoka
KYamane
MMarumo
FSato
C Choledochal cyst with adenocarcinoma in the cystically dilated intrahepatic bile duct.
Abdom Imaging. 1997;22190- 193
Google ScholarCrossref 91.Nagorney
DMMcIlrath
DCAdson
MA Choledochal cysts in adults: clinical management.
Surgery. 1984;96656- 663
Google Scholar 92.Kouraklis
GMisiakos
EGlinavou
AKaratzas
GGogas
JSkalkeas
G Cystic dilatations of the common bile duct in adults.
HPB Surg. 1996;1091- 95
Google ScholarCrossref 93.Takiff
HStone
MFonkalsrud
EW Choledochal cysts: results of primary surgery and need for reoperation in young patients.
Am J Surg. 1985;150141- 146
Google ScholarCrossref 94.Chijiiwa
KKoga
A Surgical management and long-term follow-up of patients with choledochal cysts.
Am J Surg. 1993;165238- 242
Google ScholarCrossref 96.Kaneko
KAndo
HWatanabe
Y
et al. Secondary excision of choledochal cysts after previous cyst-enterostomies.
Hepatogastroenterology. 1999;462772- 2775
Google Scholar 97.Lai
HSDuh
YCChen
WJ
et al. Manifestations and surgical treatment of choledochal cyst in different age group patients.
J Formos Med Assoc. 1997;96242- 246
Google Scholar 98.Ishibashi
TKasahara
KYasuda
YNagai
HMakino
SKanazawa
K Malignant change in the biliary tract after excision of choledochal cyst.
Br J Surg. 1997;841687- 1691
Google ScholarCrossref 99.Watanabe
YToki
ATodani
T Bile duct cancer developed after cyst excision for choledochal cyst.
J Hepatobiliary Pancreat Surg. 1999;6207- 212
Google ScholarCrossref 100.Eriguchi
NAoyagi
SOkuda
K
et al. Carcinoma arising in the pancreas 17 years after primary excision of a choledochal cysts: report of a case.
Surg Today. 2001;31534- 537
Google ScholarCrossref 101.Kurokawa
YHasuike
YTsujinaka
T
et al. Carcinoma of the head of the pancreas after excision of a choledochal cyst.
Hepatogastroenterology. 2001;48578- 580
Google Scholar 102.Fujisaki
SAkiyama
TMiyake
H
et al. A case of carcinoma associated with the remained intrapancreatic biliary tract 17 years after the primary excision of a choledochal cyst.
Hepatogastroenterology. 1999;461655- 1659
Google Scholar 103.Ando
HKaneko
KIto
T
et al. Complete excision of the intrapancreatic portion of choledochal cysts.
J Am Coll Surg. 1996;183317- 321
Google Scholar 104.Jesudason
SRGovil
SMathai
VKuruvilla
RMuthusami
JC Choledochal cysts in adults.
Ann R Coll Surg Engl. 1997;79410- 413
Google Scholar 105.Lopez
RRPinson
CWCampbell
JRHarrison
MKaton
RM Variation in management based on type of choledochal cyst.
Am J Surg. 1991;161612- 615
Google ScholarCrossref 107.Belli
GRotondano
GD'Agostino
AIannelli
AMarano
ISantangelo
ML Cystic dilation of extrahepatic bile ducts in adulthood: diagnosis, surgical treatment and long-term results.
HPB Surg. 1998;10379- 385
Google ScholarCrossref 108.Kobayashi
SAsano
TYamasaki
MKenmochi
TNakagohri
TOchiai
T Risk of bile duct carcinogenesis after excision of extrahepatic bile ducts in pancreaticobiliary maljunction.
Surgery. 1999;126939- 944
Google ScholarCrossref 109.Nakayama
HMasuda
HUgajin
WKoshinaga
TFukuzawa
M Left hepatic lobectomy for type IV-A choledochal cyst.
Am Surg. 2000;661020- 1022
Google Scholar 110.Shito
MShintoku
JMiyazaki
HMukai
M Asymptomatic intrahepatic choledochal cyst associated with chronic active hepatitis C.
Hepatogastroenterology. 1998;452356- 2358
Google Scholar 111.Thambi Dorai
CRVisvanathan
RMcAll
GL Type IVa choledochal cysts: surgical management and literature review.
Aust N Z J Surg. 1991;61505- 510
Google ScholarCrossref 112.Elton
EHanson
BLBiber
BPHowell
DA Dilated common channel syndrome: endoscopic diagnosis, treatment, and relationship to choledochocele formation.
Gastrointest Endosc. 1998;47471- 478
Google ScholarCrossref 113.Adamek
HESchilling
DWeitz
MRiemann
JF Choledochocele imaged with magnetic resonance cholangiography.
Am J Gastroenterol. 2000;951082- 1083
Google ScholarCrossref 114.Siegel
EGFolsch
UR Primary sclerosing cholangitis mimicking choledocal cyst type 1 in a young patient.
Endoscopy. 1999;31200- 203
Google ScholarCrossref 115.Samavedy
RSherman
SLehman
GA Endoscopic therapy in anomalous pancreatobiliary duct junction.
Gastrointest Endosc. 1999;50623- 627
Google ScholarCrossref 116.Todani
TWatanabe
YUrushihara
NNoda
TMorotomi
Y Biliary complications after excisional procedure for choledochal cyst.
J Pediatr Surg. 1995;30478- 481
Google ScholarCrossref 117.Henne-Bruns
DKremer
BThonke
FGrimm
HSoehendra
N "Endoscopy friendly" resection technique of choledochal cysts.
Endoscopy. 1993;25176- 178
Google ScholarCrossref 118.Schimpl
GAigner
RSorantin
EMayr
JSauer
H Comparison of hepaticoantrostomy and hepaticojejunostomy for biliary reconstruction after resection of a choledochal cyst.
Pediatr Surg Int. 1997;12271- 275
Google ScholarCrossref 120.Delarue
AChappuis
JPEsposito
C
et al. Is the appendix graft suitable for routine biliary surgery in children?
J Pediatr Surg. 2000;351312- 1316
Google ScholarCrossref 121.Todani
TWatanabe
YToki
AOgura
KWang
ZQ Co-existing biliary anomalies and anatomical variants in choledochal cyst.
Br J Surg. 1998;85760- 763
Google ScholarCrossref 122.Hamada
YSato
MTakada
KHioki
K Spiral computed tomography for bilioenteric anastomotic stricture.
Pediatr Surg Int. 1998;13424- 425
Google ScholarCrossref 123.Uno
KTsuchida
YKawarasaki
HOhmiya
HHonna
T Development of intrahepatic cholelithiasis long after primary excision of choledochal cysts.
J Am Coll Surg. 1996;183583- 588
Google Scholar 124.Ando
HIto
TKaneko
KSeo
TIto
F Intrahepatic bile duct stenosis causing intrahepatic calculi formation following excision of a choledochal cyst.
J Am Coll Surg. 1996;18356- 60
Google Scholar 125.Hsu
RKYu
ALee
JGLeung
JW Pancreatitis caused by common bile duct stones in a 3-year-old boy with prior surgery for a choledochal cyst.
Am J Gastroenterol. 2001;961919- 1921
Google ScholarCrossref 126.Tsuchida
YTakahashi
ASuzuki
N
et al. Development of intrahepatic biliary stones after excision of choledochal cysts.
J Pediatr Surg. 2002;37165- 167
Google ScholarCrossref 127.Yamataka
AOhshiro
KOkada
Y
et al. Complications after cyst excision with hepaticoenterostomy for choledochal cysts and their surgical management in children versus adults.
J Pediatr Surg. 1997;321097- 1102
Google ScholarCrossref 128.Saing
HChan
KLMya
GHCheng
WFan
STChan
FL Cutaneous stoma in the roux limb of hepaticojejunostomy (hepaticocutaneous jejunostomy): useful access for intrahepatic stone extraction.
J Pediatr Surg. 1996;31247- 250
Google ScholarCrossref 129.Scudamore
CHHemming
AWTeare
JPFache
JSErb
SRWatkinson
AF Surgical management of choledochal cysts.
Am J Surg. 1994;167497- 500
Google ScholarCrossref 130.Tanaka
MShimizu
SMizumoto
K
et al. Laparoscopically assisted resection of choledochal cyst and Roux-en-Y reconstruction.
Surg Endosc. 2001;15545- 552
Google ScholarCrossref 131.Watanabe
YSato
MTokui
KKoga
SYukumi
SKawachi
K Laparoscope-assisted minimally invasive treatment for choledochal cyst.
J Laparoendosc Adv Surg Tech A. 1999;9415- 418
Google ScholarCrossref 132.Shimura
HTanaka
MShimizu
SMizumoto
K Laparoscopic treatment of congenital choledochal cyst.
Surg Endosc. 1998;121268- 1271
Google ScholarCrossref