Intrabiliary Rupture of Hepatic Hydatid Cysts: Diagnostic Accuracy of MR Cholangiopancreatography

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1 Erden et al. MR Cholangiopancreatography of Hydatid Cyst Hepatobiliary Imaging Clinical Observations Ayşe Erden 1 Necati Örmeci 2 Suat Fitoz 1 İlhan Erden 1 Sumru Tanju 1 Yasemin Genç 3 Erden A, Örmeci N, Fitoz S, Erden İ, Tanju S, Genç Y Keywords: hydatid cyst, liver, MR cholangiopancreatography DOI: /AJR Received November 23, 2006; accepted after revision March 26, Department of Radiology, Ankara University School of Medicine, Talatpaşa Bulvarı, Sıhhiye, 06100, Ankara, Turkey. Address correspondence to A. Erden (ayse.erden@medicine.ankara.edu.tr). 2 Department of Gastroenterology, Ankara University School of Medicine, Ankara, Turkey. 3 Department of Biostatistics, Ankara University School of Medicine, Talatpaşa Bulvarı, Sıhhiye, 06100, Ankara, Turkey. WEB This is a Web exclusive article. AJR 2007; 189:W84 W X/07/1892 W84 American Roentgen Ray Society Intrabiliary Rupture of Hepatic Hydatid Cysts: Diagnostic Accuracy of MR Cholangiopancreatography OBJECTIVE. The purpose of this study was to establish the role of MR cholangiopancreatography (MRCP) in the diagnosis of biliary rupture in hepatic hydatid disease. We sought to determine whether the morphologic features of cysts and bile duct abnormalities detected on MRCP are specific enough for identification of intrabiliary rupture. CONCLUSION. If one of the following MRCP findings of apparent connection between hydatid cyst and biliary system, deformation of cyst, focal defect in cyst wall, or beaklike projection extending from cyst wall was present in a patient with hepatic hydatid cyst, the sensitivity of MRCP was 91.7% and the specificity was 82.8% for identification of intrabiliary rupture. ne of the most frequent complications of hepatic hydatid disease is O rupture of cysts into the bile ducts. The communication between the biliary tree and the hydatid cyst can be frank or occult. The most common clinical manifestations of frank intrabiliary rupture are colicky right hypochondrial pain and obstructive jaundice accompanied by fever and chills [1, 2]. Occult rupture, on the other hand, usually has no clinical signs, and the most common symptom, if present, is abdominal pain. Occult cystobiliary communication can cause postoperative biliary fistulas unless the opening in the bile duct is detected and properly sutured during the surgery [2]. Laboratory investigations show an elevated WBC count and serum bilirubin level and cholestasis [2] in patients with positive results of serologic tests. The diagnosis can be suspected in the presence of these clinical findings and laboratory data [1, 2]. Imaging, however, is needed for detection of the hydatid cyst and prompt localization of the intrabiliary rupture, which necessitates early surgical intervention [1, 2]. ERCP is the reference standard in the diagnosis of many biliary tract abnormalities and probably is the most reliable preoperative imaging method for visualization of biliary rupture [3]. Galati et al. [4] reported that preoperative ERCP is useful in the care of patients with cystobiliary fistula because it allows visualization of the fistula and drainage of the biliary tree and is associated with an 11.1% to 7.6% reduction in the incidence of postoperative complications. MR cholangiopancreatography (MRCP) is rapidly replacing diagnostic ERCP in the management of various biliary diseases. MRCP is a promising tool in the detection of cystobiliary communication and provides complementary information about the entire region affected by the hydatid cyst [5]. However, the diagnostic accuracy of MRCP in patients with intrabiliary rupture has not been quantified, to our knowledge. Most of the MR cholangiographic information about biliary rupture has been provided in the form of isolated case reports [6, 7] describing frank communication. There remains a poor understanding of the indirect MRCP findings. Therefore, we aimed to establish the role of MRCP in the diagnosis of biliary rupture associated with hepatic hydatid disease. We also sought to determine whether the morphologic features of the cysts and bile duct abnormalities detected on MRCP are specific enough for identification of intrabiliary rupture. Materials and Methods Study Group Fifty-four patients (39 females and 15 males; mean age, 46.7 years) with liver hydatid disease diagnosed on the basis of results of serologic tests and abdominal sonography were referred for MRCP to exclude biliary tract involvement. Eighteen of the patients had undergone surgery. No data regarding postoperative complications, such as the possibility of communication with the biliary system, were present in their records. Twenty-nine of the 54 patients with symptoms and laboratory results suggesting biliary involvement un- W84 AJR:189, August 2007

2 MR Cholangiopancreatography of Hydatid Cyst derwent ERCP as part of the pretreatment evaluation. Five other patients, who had symptoms of acute abdomen, underwent emergency surgical intervention without undergoing ERCP. The surgical records and postoperative T-tube cholangiograms of these five patients were used for comparison with MRCP findings. These 34 patients whose ERCP findings or surgical data and T-tube cholangiograms were available as reference standards for the analysis of MRCP signs made up the study group (27 females and seven males; mean age, 45.9 years; age range, years). The interval between MRCP and ERCP or surgery was 5 43 days (mean, 18 days). In 20 of the original 54 cases, standard reference information was not available, and the patients were excluded from the study. MRI Technique MRI was performed with a torso phased-array coil in a 1-T unit (Signa LX Horizon, GE Healthcare). MRCP was heavily T2-weighted by use of a singleshot fast spin-echo sequence and both thin (multiple sections) and thick collimation (single section). Thincollimation images were obtained in the axial and coronal planes with respiratory triggering at a section thickness of 3 mm. For 14 patients whose initial images suggested intrabiliary rupture, 3-mm sections obtained in the sagittal plane also were included. The imaging parameters were as follows: TR/TE, 3,000 30,000/ adapted automatically with software according to the patient s respiration pattern and the number of slices; echo-train length, 25; bandwidth, 31.2 khz; matrix size, ; number of excitations, 0.5; field of view, cm. From the thin-collimation source images, reconstructions of the biliary system were generated with a maximum-intensity-projection (MIP) algorithm. Thickcollimation images were obtained in the coronal or coronal oblique plane with breath-hold technique. During the single-section acquisition, coronal sections mm thick were obtained. The breathhold duration for each thick slice was 2 seconds. Parameters for the thick-collimation images were as follows: 1,700 15,000/900 1,100; bandwidth, khz; matrix size, ; number of excitations, ; field of view, cm. In addition, axial T2-weighted fast spin-echo images (TR varied according to the patient s breathing pattern; TE, 102 milliseconds; echo-train length, 4 18; section thickness, 8 mm; intersection gap, 1.5; bandwidth, 41.7 khz; matrix size, ; number of excitations, 4; field of view, cm; acquisition time, minutes) of the upper abdomen were obtained for better characterization of soft-tissue details. Review of Data All of the source, MIP, thick-slab, and T2- weighted fast spin-echo axial images were evaluated in a retrospective manner by two observers unaware of the clinical and laboratory data and blinded to the results of other imaging studies, ERCP, and surgery. The focus of image analysis was to identify apparent cystobiliary communication, which was assumed to be the direct sign of intrabiliary rupture [8]. The observers were asked to record the following three findings that suggest the presence of communication between a cyst and the biliary system: deformity of the cyst, defect in the wall of the hydatid cyst, and presence of a beaklike projection extending from the cyst wall. These findings were considered indirect signs of intrabiliary rupture. Deformed cyst was defined as a cyst that had lost its natural smooth round or oval shape. Because it can be a sequela of intervention or surgical treatment, focal interruption in the cyst wall also was considered a sign of ruptured hydatid cyst [8]. Beaklike projection was assigned to a conical extension of a bile duct with the base faced toward the cyst [5, 9]. The presence of dilated pericytic ducts distal to a cyst [8, 10] and intraductal focal loss of signal intensity (bile ducts containing hydatid cyst material), which have been reported as indirect signs [8], also was examined on all images and tabulated. Dilatation of the pericystic bile ducts was thought to be related to leakage of cystic fluid into the bile ducts. The reviewers were asked to record the presence of detached cyst membrane and to document bile duct changes consisting of displacement of pericystic ducts; stenosis or complete blockage of the bile ducts due to mass effect of the cyst; and findings of cholangitis, such as irregularities and focal dilatation associated with strictures in the course of the bile ducts. Discordant interpretations were resolved by consensus. Pericyst is the result of a reaction around a cyst as the cyst grows in compressed liver tissue [10]. Low signal intensity of this rim on T2-weighted images represents dense fibrous tissue. The presence of hypointense pericyst on T2-weighted images was sought in each lesion, and the thickness was measured. A thickness of 5 mm or less was considered thin pericyst, and a thickness greater than 5 mm was considered thick pericyst. Statistical Analysis To predict the presence of cystobiliary communication, a scoring system was instituted according to the presence of the following MRCP findings: 1, apparent connection between the hydatid cyst and the biliary system; 2, deformation of the cyst; 3, focal defect in cyst wall; 4, beaklike projection extending from the cyst wall. Each of these findings was scored 1 if present on MR images and 0 if absent. A patient had a maximum score of 4 when all of these findings were present. A receiver operating characteristic (ROC) curve was used to describe the performance of the diagnostic value of the MRCP score. Youden s index was calculated to detect the best reflected optimal sensitivity and specificity. The kappa statistic was used for assessment of interobserver agreement. A kappa value of was considered slight agreement; , fair; , moderate; , substantial; and , almost perfect. Results Communication between the cyst and the biliary tree was found at ERCP and surgery in 12 (35%) of the 34 patients. In these patients, a total of 16 cysts were found to be ruptured into the biliary ducts. Ten of the ruptured cysts were in the right lobe of the liver, and six were in the left lobe. The diameters of the cysts ranged from 2 to 10 cm (mean ± SD, 5.6 ± 2.3 cm). In all patients with intrabiliary rupture, the pericysts were less than 5 mm thick. The frequency of MRCP findings in patients with intrabiliary rupture is shown in Table 1. Apparent cystobiliary communication (Figs. 1 and 2) was detected in four patients. The sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of MRCP for apparent cystobiliary communication were 33.3%, 100%, 100%, 73.3%, and 76.5%, respectively. During analysis, rupture was identified with MRCP in eight cases, which were ultimately coded as true-positive diagnoses (Figs. 1 3). Eighteen examinations had true-negative findings for intrabiliary rupture (Fig. 4), four had false-positive findings (Fig. 5), and another TABLE 1: Frequency of MR Cholangiopancreatographic Findings in Patients with Confirmed Intrabiliary Rupture (n =12) Finding n Displacement of pericystic bile ducts 10 (90.9) Deformation of cyst 9 (75) Stenosis or complete block of bile 9 (75) ducts with upstream dilatation Bile duct changes due to cholangitis 8 (66.7) Focal interruption in cyst wall 8 (66.7) Dilatation of downstream bile ducts a 6 (50) Detachment of cyst membrane b 6 (50) Beaklike projection 6 (50) Apparent cystobiliary communication 4 (33.3) Intraductal cyst content 3 (25) Note Values in parentheses are percentages. a Ductal dilatation was attributed to neither cystic compression nor cholangitis. Distal duct dilatation was thought to be related to stagnation of flow due to leakage of cystic content. b Can be due to aging or rupture. AJR:189, August 2007 W85

3 Erden et al. four had false-negative findings (Fig. 6). Review of four false-positive diagnoses showed that dilatation of the distal pericystic bile ducts in all cases was misinterpreted as an indicator of leaked cystic content (Fig. 5). In two patients, rupture seemed highly probable on MRCP, but no communication was found on ERCP. Both deformation in the cyst and detachment of the cyst membrane were present in two of the patients with false-positive diagnoses. In one of the four false-negative diagnoses, the reviewers interpreted two cysts measuring 2.5 and 4.5 cm in diameter connected with each other as unruptured, although deformation and focal interruption of the walls of the cysts were present. In another false-negative diagnosis, A C proximity of seven large hepatic cysts 6 10 cm in diameter made evaluation difficult. No sign suggesting rupture was identified even during retrospective analysis. In the third case, two cysts exhibited membrane detachment. Vague focal interruption of the cyst wall was seen in one of the cysts, but alone it might not have been accepted as suggesting the presence of rupture. In the last case, 17 cysts were present in the liver parenchyma, and two of them proved ruptured. The only sign suggesting the rupture was a deformed appearance of the cysts (Fig. 6). The ROC plot showed the relation between the true-positive rate (sensitivity) and the falsepositive rate (1 specificity) over all possible decision values. The area under the ROC curve Fig year-old man with five hepatic hydatid cysts cm in diameter and true-positive imaging findings. CBD = common bile duct. A, Coronal thick-slab MR cholangiopancreatogram shows multiple hydatid cysts and marked cholangitic changes (open arrow) in proximal bile ducts. B, T-tube cholangiogram obtained 9 days after surgery shows irregular pooling of contrast material reflecting three residual cavities (thick arrows). Also evident are fragment of retained hydatid material (thin arrow) in cavity and diffuse cholangitic changes (open arrow) involving left lobe. C, Sagittal heavily T2-weighted source image shows interruption of cyst wall and cystobiliary communication (arrows). was ± and was considered statistically significant (p < 0.001) at separating patients without rupture of hepatic hydatid disease from patients with intrabiliary rupture. We defined cutoff values for different levels of sensitivity and specificity using the ROC curve and Youden s index. A score of 0.5 appeared to be an optimum threshold for determining whether a patient had rupture at a sensitivity of 91.7% and a specificity of 82.8%. In another words, if any of the four signs was present in a patient, the sensitivity of the method was 91.7%, and the specificity was 82.8%. The kappa values ± SE of interobserver agreement for apparent cystobiliary communication, deformity of the cyst, defect in the hy- B W86 AJR:189, August 2007

4 MR Cholangiopancreatography of Hydatid Cyst A Fig year-old woman with surgically confirmed biliary rupture and true-positive imaging findings. A, Axial heavily T2-weighted MR image shows hydatid cyst in right lobe of liver. Cystobiliary communication and defect in posterolateral aspect of pericyst are apparent. Tiny area of low signal intensity (arrow) represents intraductal hydatid material. B, Maximum-intensity-projection MR image in coronal plane shows crowding and dilatation of proximal bile ducts associated with cystobiliary communication (arrow). Splaying of left intrahepatic bile ducts is secondary to hypertrophy of left lobe. CBD = common bile duct. Fig year-old boy with hydatid cyst in right lobe of liver and truepositive imaging findings. MR cholangiopancreatogram shows beaklike projection (arrow) of bile duct from cyst wall. datid cyst wall, and beaklike projection extending from the cyst wall were κ =1 (p =0.000), κ = ± (p = 0.007), κ = ± (p = 0.004), and κ = ± (p = 0.000), respectively. The kappa statistics for the two reviewers had a statistically signifi- cant level of agreement regarding the presence of MRCP findings. Discussion The radiologic findings of intrabiliary rupture include direct and indirect signs [8]. The only direct sign of rupture is visible communication between the cyst and the biliary tree. Although the probability of rupture is very high in the presence of this finding, it was present in only 33% of cases of ruptured cyst in our study. Deformation of a cyst suggests decreased intracystic pressure and may be the only indirect sign of intrabiliary rupture. This finding was seen in 75% of our cases of biliary rupture. However, deformation can be a result of medical or surgical treatment and does not necessarily indicate rupture. For this reason, collapse of or decrease in the size of a cyst in the follow-up of untreated patients may be a more significant sign of rupture. Pericyst is the outer layer of a cyst and consists of thick and avascular fibrous tissue containing bile ducts [10]. A focal defect in the pericyst on T2-weighted images was seen in 66.7% of our patients with rupture. Cyst wall discontinuity is considered a direct sign of rupture and is found in 75% of cases [9]. The diag- B AJR:189, August 2007 W87

5 Erden et al. A B C Fig year-old woman without intrabiliary rupture of hepatic hydatid cyst and true-negative imaging findings. A, Axial T2-weighted fast spin-echo MR image shows noncommunicating hydatid cyst. Integrity of pericyst is preserved. Bile ducts around cyst are massively dilated and appear somewhat distorted. B, Coronal thick-slab MR cholangiopancreatogram shows pericystic bile duct changes characteristic of cholangitis ectasia, irregularity, and tortuosity. Intraductal cyst content and discontinuity of cyst wall are not present. C, T-tube cholangiogram shows ductal changes similar to those in B. Lack of opacification of residual cavity excludes possible cystobiliary communication. Fig year-old woman with hydatid cyst in lateral segment of left lobe of liver and falsepositive imaging findings. Coronal maximumintensity-projection MR image shows moderate dilatation (arrow) of bile duct draining this segment and its close relation to cyst, which falsely suggest possible cystobiliary communication. CBD = common bile duct. nosis of rupture is likely if a bile duct extending from the interrupted wall points toward the porta hepatis [5, 9]. Beaklike projection from the cyst wall was seen in 50% of our patients with intrabiliary rupture. A surgical defect should be considered in the differential diagnosis of cyst wall defect. The inner layer of a hydatid cyst, known as endocyst, grows faster than pericyst, becomes redundant, and folds on itself [10]. Although it can be the consequence of aging and ischemia, detachment of endocyst manifesting as undulating membrane also can be the result of percutaneous treatment and contained or communicating rupture [11]. In our study, detachment of the membrane was seen in 50% of cases of rupture (Table 1). If a cyst ruptures to the biliary system, hydatid fragments and particles entering the biliary tree can cause clinical symptoms simulating cholelithiasis. MRCP showed linear or leaflike intraductal areas of low signal intensity representing cyst material in our three patients with frank cystobiliary communication. Air fluid [12] and fat fluid [8] levels inside the cyst, rare signs of cystobiliary communication, were not found in our patients. Ductal displacement by extrinsic compression was the most common (90.9%) finding in our patients with intrabiliary rupture. Obstructive cholangitis induced by insufficient biliary drainage was found on MRCP in two thirds of the cases of rupture. Dilatation of proximal ducts was the most prominent finding in such cases. However, dilatation of any duct not attributed to mass effect, particularly of ducts distal to the hydatid cyst, can be misinterpreted as an indirect sign of rupture. Leakage of cyst fluid into the bile ducts through an occult wall defect can be considered responsible for the ductal dilatation. Such dilated pericystic ducts were the main causes of the four false-positive results in our study. We believe dilated pericystic ducts should be considered significant only when their entrance into the defective wall is seen. Visible dilated ducts in the vicinity of a hydatid cyst not complicated by rupture is seen in 25% of patients [10]. Inherent limitations of surgery and ERCP might have affected the results of our study. We chose to use ERCP and surgical findings as the reference standards for confirming our imaging findings, but the possibility of false-negative results existed, even at surgery. If the cyst content is not stained with bile during surgery, simple openings can be missed [13]. These occult communications are responsible for the high recurrence rate of complex hydatid cysts in the postoperative period. Several investigations have shown that in the presence of suggestive symptoms, cystobiliary communication should continue to be suspected even in the absence of ERCP findings. Magistrelli et al. [3] found the W88 AJR:189, August 2007

6 MR Cholangiopancreatography of Hydatid Cyst A B C Fig year-old woman with multiple hydatid cysts of various sizes and false-negative imaging findings. A, Coronal thick-slab MR cholangiopancreatogram shows moderately dilated and distorted bile ducts superimposed on cysts; however, intrabiliary rupture was not suspected, even on source images. Thick arrow indicates ruptured cyst. Thin arrow indicates distribution of biliary radicles similar to that in B. CBD = common bile duct. B, ERCP image shows straightening and separation of left intrahepatic bile ducts suggesting mass effect caused by multiple space-occupying lesions. Collection of contrast material in diaphragmatic surface of liver is in ruptured hydatid cyst (black arrow). Smooth cyst (arrowhead) in right lobe is outlined by contrast material. White arrow indicates distribution of biliary radicles similar to that in A. GB = gallbladder. C, Coronal source MR image shows ruptured cyst (thick arrow) with triangular deformity (thin arrow) found at retrospective evaluation. false-negative ratio of ERCP was 17% [3]. In a study by Shemesh and Friedman [14], communications detected during surgical exploration were not found on ERCP in three of six cases. The investigators speculated that the cause of the false-negative results was intermittent or temporary occlusion of the rupture site by cyst content. In these instances, visualization of the cyst with contrast material usually is difficult despite correct injection pressure [14]. In addition, small ruptures are often kept closed by high intracystic pressure and may be identified only after evacuation of the cyst content [3]. According to our observations, an advantage of MRCP over ERCP is capability for assessing ducts proximal to an obstruction in cases in which ERCP may be unsuccessful. A possible cystobiliary communication facing the surface of the liver also may remain unopacified during ERCP. The combination of ERCP and cross-sectional techniques is preferred for investigation of biliary rupture of hydatid cysts. Although they are not considered effective in the detection of intrabiliary rupture, imaging methods can accurately show the location and morphologic properties of the cysts. Many reports [5, 8, 11, 12] have shown the usefulness of sonography, CT, and conventional MRI in the preoperative detection of ruptured hepatic hydatid cysts. The imaging signs of rupture are documented in these reports. Except for a study [5] of a series of nine cases of ruptured hydatid cyst, in only a few case reports [6, 7] to our knowledge have MRCP observations of biliary rupture been described. These reports emphasize signs of frank rupture. Thus comparison of our observations with similar data was not possible. MRCP depicts the entire biliary tree despite obstruction. It enables topographic evaluation of hydatid cysts and the level of obstruction. Apparent cystobiliary communication had high specificity as a direct sign of rupture, the presence of this sign suggesting the diagnosis. Because the sensitivity was low, the absence of visible communication did not exclude the diagnosis of rupture. If any of the four signs (apparent cystobiliary communication, deformation of the hydatid cyst, focal defect in the cyst wall, and beaklike projection extending from the cyst wall) was present in a patient, the sensitivity of MRCP was 91.7%, and the specificity was 82.8%. In conclusion, MRCP findings are sensitive in the identification of intrabiliary rupture due to hepatic hydatid disease. References 1. Dadoukis J, Gamvros O, Aletras H. Intrabiliary rupture of the hydatid cyst of the liver. World J Surg 1984; 8: Alper A, Ariogul O, Emre A, Uras A, Okten A. Choledochoduodenostomy for intrabiliary rupture of hydatid cysts of liver. Br J Surg 1987; 74: Magistrelli P, Masetti R, Coppola R, et al. Value of ERCP in the diagnosis and management of pre- and postoperative biliary complications in hydatid disease of the liver. Gastrointest Radiol 1989; 14: Galati G, Sterpetti AV, Caputo M, et al. Endoscopic retrograde cholangiography for intrabiliary rupture of hydatid cyst. Am J Surg 2006; 191: Tsitouridis J, Kouklakis G, Tsitouridis K, Melidis D, Krokos N, Emmanoyilidoy M. Intrabiliary obstruction due to ruptured hepatic hydatid cyst: evaluation with computed tomography and magnetic resonance imaging. Dig Endosc 2001; 13: Little AF, Lee WK, Mathison K. MR cholangiography in the evaluation of suspected intrabiliary rupture of the hepatic hydatid cyst. Abdom Imaging 2002; 27: Dutta U, Sinha SK, Singh P, et al. Hepatobiliary and pancreatic: complications of hydatid disease. J Gastroenterol Hepatol 2004; 19: Mendez Montero JV, Arrazola Garcia J, Lopez Lafuente JL, Antela Lopez J, Mendez Fernandez R, Saiz Ayala A. Fat fluid level in hepatic hydatid cyst: a new sign of rupture into the biliary tree? AJR 1996; 167: Marti-Bonmati L, Menor F, Ballesta A. Hydatid cyst of the liver: rupture into the biliary tree. AJR 1988; 150: Lewall DB, Nyak P. Hydatid cysts of the liver: two cautionary signs. Br J Radiol 1998; 71: Lewall DB, McCorkell SJ. Rupture of echinococcal cysts: diagnosis, classification, and clinical implications. AJR 1986; 146: Marti-Bonmati L, Menor Serrano F. Complications of hepatic hydatid cysts: ultrasound, computed tomography and magnetic resonance diagnosis. Gastrointest Radiol 1990; 15: Ozmen MM, Coskun F. New technique for finding the ruptured bile duct into the liver cysts: scope in the cave technique. Surg Laparosc Endosc Percutan Tech 2002; 12: Shemesh E, Friedman E. Radiologic and endoscopic appearance of intrabiliary rupture of hydatid liver disease. Digestion 1987; 36: AJR:189, August 2007 W89