Caroli s disease: magnetic resonance imaging features
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1 Eur Radiol (2002) 12: DOI /s HEPATOBILIARY PANCREAS France Guy François Cognet Marie Dranssart Jean-Pierre Cercueil Laurent Conciatori Denis Krausé Caroli s disease: magnetic resonance imaging features Received: 14 August 2001 Revised: 19 March 2002 Accepted: 25 March 2002 Published online: 4 June 2002 Springer-Verlag 2002 F. Guy F. Cognet ( ) M. Dranssart J.-P. Cercueil L. Conciatori D. Krausé Department of Radiology and Imaging, Dijon Le Bocage University Hospital, 2 Blvd. Maréchal de Lattre de Tassigny, BP 1542, Dijon Cedex, France francog@ipac.fr Tel.: Fax: Abstract Our objective was to describe the main aspects of MR imaging in Caroli s disease. Magnetic resonance cholangiography with a dynamic contrast-enhanced study was performed in nine patients with Caroli s disease. Bile duct abnormalities, lithiasis, dot signs, hepatic enhancement, renal abnormalities, and evidence of portal hypertension were evaluated. Three MR imaging patterns of Caroli s disease were found. In all but two patients, MR imaging findings were sufficient to confirm the diagnosis. Moreover, MR imaging provided information about the severity, location, and extent of liver involvement. This information was useful in planning the best therapeutic strategy. Magnetic resonance cholangiography with a dynamic contrast-enhanced study is a good screening tool for Caroli s disease. Direct cholangiography should be reserved for confirming doubtful cases. Keywords Caroli s disease Magnetic resonance MR cholangiography Introduction Caroli s disease, also known as communicating cavernous ectasias of the biliary tree, is a rare congenital disorder first described by Caroli in 1958 [1]. This condition is characterized by non-obstructive, saccular, or fusiform dilatations of the intrahepatic bile ducts. The dilatations involve the entire liver or only a lobe or segment. Two primary types of the disease have been identified [2]. The non-hereditary form (type I), also known as the sporadic pure type, is often limited to one hepatic lobe (usually the left lobe). Multifocal saccular dilatations of segmental bile ducts are frequently accompanied with calculi formation and recurrent bacterial cholangitis. The hereditary form (type II) involves the entire liver. Most patients with type-i disease have not only biliary tract abnormalities but also congenital hepatic fibrosis. The bile duct dilatation is usually less prominent than in type I, and the patients present with abnormalities related to hepatic fibrosis and portal hypertension. Associated conditions, including choledochal cysts and cystic lesions of the kidney known as autosomic-recessive polycystic kidney disease (ARPKD) [2, 3], occur mainly in the hereditary form. Direct bile duct opacification by endoscopic retrograde cholangiopancreatography (ERCP) or percutaneous transhepatic cholangiography (PTC) is the most sensitive method for investigating bile duct abnormalities and, more specifically, for demonstrating communications between cystic dilatations and bile ducts; however, both techniques are invasive and carry a risk of complications including sepsis and bleeding [4]. Magnetic resonance cholangiography (MRC) is a new non-invasive imaging modality that has been proven effective for investigating bile duct obstruction [5, 6]. Magnetic resonance cholangiography may be an alternative to direct cholangiography in patients with congenital bile duct abnormalities. Few articles on MRC findings in Caroli s disease have been published [7, 8, 9, 10, 11], and none have described results obtained using dynamic gadolinium enhancement. The goal of our study was to describe the usefulness of MRC with dynamic gadolinium enhancement in the investigation of Caroli s disease.
2 2731 Table 1 Clinical features and imaging study findings. ADP- KD autosomal-dominant polycystic kidney disease; ARPKD autosomal-recessive polycystic kidney disease; PTC percutaneous transhepatic cholangiography Patient Gender, Previous history Method of MR imaging features no. age and clinical features diagnosis (years) 1 F, 41 Recurrent cholangitis Histology Diffuse large cystic ectasias, intrahepatic calculi, dot signs 2 F, 65 Recurrent cholangitis Histology Diffuse large cystic ectasias, intrahepatic calculi, dot signs, parenchymal contrast enhancement 3 M, 40 Recurrent cholangitis Histology Diffuse large cystic ectasias, intrahepatic calculi, dot signs 4 M, 30 Congenital hepatic Histology Diffuse small cystic ectasias, fibrosis and ARPKD, dot signs acute cholangitis 5 F, 22 Portal hypertension Diffuse small cystic ectasias, dot signs 6 F, 44 Recurrent cholangitis Histology Diffuse fusiform dilatations Intrahepatic calculi 7 F, 28 Acute cholangitis PTC Fusiform dilatations in the left lobe, intrahepatic calculi 8 M, 67 ADPKD PTC Monoliform dilatations in the left (renal transplantation), lobe, intrahepatic calculi, recurrent episodes parenchymal cysts of septicemia 9 M, 48 Primary hemochromatosis, PTC, Fusiform dilatations in the left lobe dilatation of the left histology intrahepatic bile ducts on US Materials and methods From January 1996 to August 1999, the medical records of nine consecutive patients with Caroli s disease (5 women and 4 men; age range years, mean age 41 years) were retrospectively reviewed: They all had undergone abdominal MR imaging. The reason for MR imaging was recurrent sepsis in seven patients, isolated portal hypertension in one, and left intrahepatic bile duct dilatation by ultrasound scanning in one patient. This last patient presented with hemochromatosis. Confirmation of the diagnosis of Caroli s disease was provided by liver histology in 6 patients who underwent transplantation or lobar resection of the liver, by PTC in two patients, and by the demonstration of both congenital hepatic fibrosis and bile duct abnormalities in one patient (Table 1). In three patients the diagnosis of Caroli s disease was made before the MR study based on examination of a right lobar resection specimen (n=1) or on cholangiography findings (n=2). All MR studies were performed using a 1.5-T system (Magnetom Vision, Siemens, Erlangen, Germany) with a body phasedarray receive coil. For MRC a multislice imaging technique was used with the following parameters: half-fourier acquisition single-shot turbo spin-echo sequence (HASTE) with effective TE 87 ms, number of excitations 1, 5-mm slice thickness, and a matrix. Images were acquired in the axial and 40 coronal oblique planes. A single-slice imaging technique was used to obtain a turbo spin-echo sequence with the following parameters: effective TE 1100 ms; echo train length 240; number of excitations 1; 50-mm slice thickness; and a matrix. Acquisition time was 7 s. A multiphase contrast-enhanced study was performed in the axial plane with a T1-weighted gradient-echo sequence [2D fast low-angle shot (FLASH; TR ms, TE 4.1 ms, flip angle 70 )]. Slice thickness was 8 mm. The MR images were obtained before and after administration of gadopentetate dimeglumine in a dose of 0.1 mmol/kg injected intravenously as a rapid bolus followed by 10 ml of normal saline. Contrast-enhanced imaging was initiated immediately after completion of the saline injection and was repeated three times within 2 min to obtain images at the arterial, portal, and equilibrium phases, respectively. This protocol was used in eight patients. In the remaining patient, MRC was performed using only the HASTE sequence in the axial plane. The MR images were evaluated for intrahepatic and extrahepatic bile duct abnormalities, dot signs, hepatic enhancement, renal abnormalities, and evidence of portal hypertension (splenomegaly and/or varicoses). Intrahepatic bile duct abnormalities seen on MRC images were classified based on location in the liver, type of dilatations (fusiform, moniliform, or cystic), size of cystic dilatations, and whether lithiasis was present. The extrahepatic bile duct was considered dilated if its diameter exceeded 8 mm. The dot sign at the portal phase of the dynamic contrast-enhanced study was defined as a tiny dot or an internal septum showing strong contrast enhancement within a segmental bile duct dilatation. Increased enhancement of the liver parenchyma was evaluated subjectively on the dynamic contrast-enhanced study. In the three patients who underwent cholangiography within 1 month after the MR study, the findings obtained by the two investigations were compared.
3 2732 Fig. 1a d Pure form of Caroli s disease involving the entire liver in a 65-year-old woman. a Unenhanced T1-weighted gradientecho image. b Portal-phase contrast-enhanced dynamic T1- weighted gradient-echo image showing abnormal enhancement of the liver parenchyma in the posterior segment suggestive of cholangitis (arrowhead). A dot sign is visible (arrow). c Single-shot turbo spin-echo T2-weighted MR sequence (thick slice) in the coronal oblique plane showing diffuse large cystic ectasias. d Half- Fourier acquisition single-shot turbo spin-echo sequence MR cholangiography sequence in the axial plane showing biliary ectasias and calculi (arrows) Results Results are summarized in Table 1. Duct abnormalities Intrahepatic bile duct dilatation was diffuse in six cases and confined to the left lobe in three cases. Five patients had fusiform and cystic dilatations of the intrahepatic biliary tract (Figs. 1, 2). Three of these patients had cystic ectasias larger than 2 cm in diameter with intrahepatic calculi (Fig. 1), and two had cystic ectasias smaller than 2 cm in diameter (Fig. 2). Extrahepatic bile duct dilatation was present in two patients, without obstruction. Dot signs were seen in all five patients (Figs. 1, 2). Three other patients had only fusiform dilatations, which were diffuse in one patient and confined to the left lobe in two patients (Fig. 3). Intrahepatic lithiasis was present in two of these patients. Findings in the remaining patient consisted of moniliform dilatations of the left intrahepatic bile ducts with some intrahepatic calculi (Fig. 4). This 67-year-old patient had autosomal-dominant polycystic kidney disease (ADPKD). Three patients underwent both MR imaging and PTC. In the two patients with fusiform dilatations of the left intrahepatic bile ducts, the two investigations yielded similar findings (Fig. 3). In the remaining patient, a man
4 2733 Fig. 2a c Congenital hepatic fibrosis and autosomal-recessive polycystic kidney disease (ARPKD) in a 22-year-old woman. a Portal-phase contrast-enhanced T1-weighted gradient-echo image showing signs of portal hypertension with splenomegaly, small and cystic ectasias (<2 cm in diameter), and dot signs (arrows). b A HASTE MR cholangiography sequence in the axial plane demonstrating diffuse small ectasias of the intrahepatic biliary tree. c A HASTE MR image in the frontal plane showing biliary abnormalities (arrows) and ectasias of the kidney medulla characteristic of recessive polycystic kidney disease (arrowheads) with ADPKD, PTC disclosed cystic dilatations of the left intrahepatic bile ducts and multiple calculi, whereas MRC failed to distinguish between hepatic cysts and biliary saccular ectasias (Fig. 4). Hepatic enhancement In one patient focal and persistent liver parenchyma enhancement was seen near cystic ectasias in one segment (Fig. 1). It was interpreted as a highly probable focus of cholangitis. Concomitant conditions Renal tubular ectasias with evidence of portal hypertension was found in two patients (Fig. 2). Discussion Caroli s disease is an uncommon form of congenital dilatation of the intrahepatic bile ducts. Although its cause remains unclear, Jorgensen [12] and others have suggested involvement of ductal plate malformation. During normal development, the circular ductal plates surrounding the portal vein are remodeled, leaving a network of small bile ducts around the portal veins. In ductal plate malformation, resorption of the circular plates is incomplete, resulting in a semicircular or cylindrical lumen that contains a portal radicle [12]. Because hepatic resection can be curative in Caroli s disease, the diagnosis is essential. Early treatment protects the patient from complications, which include calculus formation, cholangitis, abscess, and cholangiocarcinoma. Imaging is essential in planning the surgical treatment, which can consist of enterostomy, segmental or lobar hepatic resection, or liver transplantation [13, 14].
5 2734 Fig. 3a, b Pure form of Caroli s disease confined to the left lobe in a 28-year-old woman. a A HASTE MR cholangiography in the coronal oblique plane showing fusiform dilatations of the left intrahepatic bile ducts (arrowhead) with small intrahepatic calculi (arrow). b Percutaneous transhepatic cholangiogram displaying similar findings Although US and CT are widely used to investigate patients with symptoms suggesting biliary disease, direct cholangiography is often necessary for an accurate diagnosis [4]; however, both ERCP and PTC carry a high risk of bacterial cholangitis. Advantages of MRC consist of depiction of the entire biliary tree, a low complication rate, and a spatial resolution as high as 1.5 mm. Using an MR imaging protocol which included MRC and a contrast-enhanced study, we identified three main patterns of Caroli s disease. The first pattern (n=5) was characterized by multiple cystic ectasias connected with fusiform dilatations of the intrahepatic bile ducts Fig. 4a, b Autosomal-dominant polycystic kidney disease and pure form of Caroli s disease in a 67-year-old man. a A HASTE MR cholangiography in the axial plane showing moniliform dilatations of the left intrahepatic biliary tree (short arrow) with some calculi (long arrow) and several cystic lesions. b Percutaneous transhepatic cholangiogram demonstrating saccular dilatations with multiple calculi of the left intrahepatic bile ducts (arrows). Note a dilated main bile duct upstream from obstruction by a large stone (double arrow) throughout the liver. In all five patients with this pattern, MRC demonstrated the communications between the saccular ectasias and the biliary tract, thus establishing the diagnosis of Caroli s disease and ruling out other conditions such as polycystic liver disease, peribiliary cysts, or multiple abscesses. In addition, all five patients had dot signs. The dot sign was described first on US scans and subsequently on CT scans [3, 15]; however,
6 2735 we are not aware of previous reports of the dot sign demonstrated by MR imaging. It appears on gadoliniumenhanced scans as a tiny dot or an internal septum showing strong contrast enhancement. The dot sign is located within a segmental bile duct dilatation. A reasonable assumption is that each dot sign is produced by a portal radicle surrounded by a dilated bile duct. The five patients with this pattern fell into two groups. Three patients exhibited large cystic dilatations of more than 2 cm in diameter with intrahepatic calculi. These patients had a pure form of Caroli s disease with symptoms of cholangitis. Among them, one patient exhibited liver parenchyma enhancement confined to a segment near a cystic ectasia. Histology confirmed that this finding was ascribable to cholangitis. The remaining two patients exhibited small cystic dilatations smaller than 2 cm in diameter without intrahepatic calculi; both had congenital hepatic fibrosis and MR evidence of renal tubular ectasias (ARPKD). Besides, portal hypertension was suggested by the presence of splenomegaly and by a perihilar and periportal hypersignal on the T2-weighted sequences; thus, the diagnosis of Caroli s syndrome was finally retained for both patients. The second pattern (n=3) was characterized by isolated fusiform dilatations of the intrahepatic bile ducts. In two of these patients the diagnosis of Caroli s disease was suggested by the presence of multiple intrahepatic calculi. The remaining patient had isolated tubular dilatation of the left intrahepatic bile ducts without lithiasis, suggesting cholangiocarcinoma despite the absence of MR evidence of obstruction. The two patients with bile duct abnormalities confined to the left lobe underwent PTC, which confirmed the MRC findings. This pattern appears more difficult to differentiate from chronic cholangitis due to a chronic obstruction or from sclerosing cholangitis, although in this pattern of Caroli s disease, intrahepatic stones can be seen without a stenosis on the biliary tract. The final diagnosis was made by examination of an operative specimen in the last patient. The third pattern, seen in a single patient, was characterized by a monoliform dilatation of the left intrahepatic bile ducts with hepatic cystic lesions. This patient had ADPKD. The HASTE sequence in the axial plane was unable to distinguish between intrahepatic cysts and saccular dilatations. The PTC showed communicating cystic ectasias with multiple calculi. Images were not obtained in the coronal oblique plane, and no dynamic contrastenhanced study was performed. This case has been described in a previous report [16]. Conclusion In conclusion, we describe various MR imaging patterns in Caroli s disease. Magnetic resonance cholangiography completed by a contrast-enhanced study may be useful in the diagnosis of Caroli s disease or Caroli s syndrome. This noninvasive technique can confirm the diagnosis especially in the large or small cystic patterns. In these cases the use of gadolinium-enhanced sequences may allow the visualization of the dot sign which seems to be very specific of the malformation of the ductal plate. The diagnosis is more difficult to establish in the case of fusiform dilatations of the biliary tract. The information it provides about the severity, location, and extent of liver involvement is invaluable in devising the best therapeutic strategy especially in the planning of surgery [17]. Moreover, MR imaging can suggest accompanying abnormalities, such as portal hypertension, cirrhosis, or renal involvement. In typical cases, MR imaging can be used as the only imaging modality in the diagnostic evaluation of patients with suspected Caroli s disease. Direct cholangiography should be reserved for cases with doubtful MR imaging findings. References 1. Caroli J, Soupault R, Kossakowski J et al. (1958) La dilatation polycystique congénitale des voies biliaires intrahépatiques. Semin Hop Paris 14: Desmet VJ (1998) Pathogenesis of ductal plate abnormalities. Mayo Clin Proc 73: Miller WJ, Sechtin AG, Campbell WL (1995) Imaging findings in Caroli s disease. Am J Roentgenol 165: Missavage AE, Sugawa C (1983) Caroli s disease: role of endoscopic retrograde cholangiopancreatography. Am J Gastroenterol 78: Reinhold C, Bret P (1996) Current status of MR cholangiopancreatography. Am J Roentgenol 166: Govil S, Justus A, Korak I, Perakath A, Zachariah N, Sen S (1998) Choledochal cysts: evaluation with MR cholangiography. Abdom Imaging 23: Asselah T, Ernst O, Sergent G (1998) Caroli s disease: a resonance magnetic cholangiopancreatography diagnosis. Am J Gastroenterol 93: Ernst O, Gottrand F, Calvo M et al. (1998) Congenital hepatic fibrosis: findings at MR cholangiopancreatography. Am J Roentgenol 170: Pavone P, Laghi A, Catalano C (1996) Caroli s disease: evaluation with MR cholangiography. Am J Roentgenol 166: Chan YL, Yeung CK, Lam WW, Fok TF, Metreweli C (1998) Magnetic resonance cholangiography: feasibility and application in the pediatric population. Pediatr Radiol 28: Jung G, Benz-Bohm G, Kugel H, Keller KM, Querfeld U (1999) MR cholangiography in children with autosomal recessive polycystic kidney disease. Pediatr Radiol 29: Jorgensen MJ (1977) The ductal plate malformation. Acta Pathol Microbiol Scand 257 (Suppl):1 87
7 Boyle MJ, Doyle GD, McNulty JG (1989) Monolobar Caroli s disease. Am J Gastroenterol 84: Sans M, Rimola A, Navasa M (1997) Liver transplantation in patients with Caroli s disease and recurrent cholangitis. Transpl Int 10: Ahmadi T, Minami M (1997) Central dot sign in entities other than Caroli disease. Radiat Med 15: Mousson C, Rabec M, Cercueil JP (1997) Caroli s disease and autosomal dominant polycystic kidney disease: a rare association? Nephrol Dial Transplant 12: Larsen TH, Sondenaa K, Jensen DK, Horn A, Larsen TB (2000) Preoperative magnetic resonance cholangiography of a severe case with Caroli s disease complicated by hepatolithiasis. Eur Radiol 10:1034
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