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AJR 2002; 179:429-434
© American Roentgen Ray Society


Diagnosis of Intrahepatic Stones: Superiority of MR Cholangiopancreatography over Endoscopic Retrograde Cholangiopancreatography

Tae Kyoung Kim1, Bong Soo Kim, Jung Hoon Kim, Hyun Kwon Ha, Pyo Nyun Kim, Ah Young Kim and Moon-Gyu Lee

1 All authors: Department of Radiology, Asan Medical Center, University of Ulsan College of Medicine, 388-1, Poongnab-dong, Songpa-ku, Seoul 138-736, Korea.

Received September 4, 2001; accepted after revision January 29, 2002.

 
Address correspondence to T. K. Kim.


Abstract
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. The purpose of this study was to compare the efficacy of MR cholangiopancreatography (MRCP) and endoscopic retrograde cholangiopancreatography (ERCP) for the diagnosis of intrahepatic stones.

MATERIALS AND METHODS. Of the 318 patients who underwent MRCP examinations at our institution during an 18-month period, we identified 49 patients who subsequently underwent surgery or cholangioscopic stone removal with proof of intrahepatic stones. Thirty-four of these patients also underwent ERCP; they made up our study population. All images were interpreted for the presence of bile duct stones: MRCP images were interpreted independently by two reviewers, and ERCP studies were interpreted by one reviewer who was unaware of the MRCP findings.

RESULTS. The sensitivity and specificity of MRCP for detecting intrahepatic stones were 97% and 93%, respectively, whereas those of ERCP were 59% and 97%, respectively. MRCP showed a significantly higher sensitivity than ERCP in the diagnosis of intrahepatic stones (p < 0.001). We found no significant difference between MRCP and ERCP in sensitivity or specificity for detecting calculi in the common duct or gallbladder.

CONCLUSION. MRCP is a more effective diagnostic method than ERCP for the evaluation of intrahepatic stones.


Introduction
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
MR cholangiopancreatography (MRCP) is a noninvasive imaging technique that has proven to be accurate in the diagnosis of bile duct stones [1,2,3,4,5,6,7,8,9,10]. Although endoscopic retrograde cholangiopancreatography (ERCP) has long been considered the standard of reference, MRCP has begun to replace ERCP for examination of bile duct stones. According to recent studies, the diagnostic accuracy of MRCP is comparable to that of ERCP for the evaluation of choledocholithiasis [1,2,3]. MRCP offers an alternative to ERCP as a noninvasive, easily performed outpatient technique that allows direct visualization of the biliary tract and avoids the complications of ERCP. Furthermore, it is the method of choice in cases in which ERCP is incomplete or when duct cannulation is not possible [11].

The chief disadvantage of MRCP is that it is purely diagnostic, whereas ERCP is both diagnostic and therapeutic. However, although common bile duct stones are managed effectively by ERCP and sphincterotomy in many instances, the treatment of intrahepatic stones via the transpapillary route is difficult because of commonly accompanying ductal strictures, peripheral stone impaction, or ductal angulation [12]. Because ERCP is not considered to have a significant therapeutic role in the management of intrahepatic stones [12], MRCP may replace ERCP if it proves to be equal or superior to ERCP in the diagnosis of intrahepatic stones.

The purpose of our study was to compare the efficacy of MRCP with that of ERCP for the diagnosis of intrahepatic duct stones.


Materials and Methods
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Patients
During an 18-month period (October 1998 to March 2000), 318 patients underwent MRCP examinations at our institution. The indications for MRCP included diverse pancreaticobiliary diseases: bile duct stones, bile duct carcinoma, pancreatic carcinoma, bile duct stricture from unknown cause, and recurrent pancreatitis. In our hospital, most patients who are thought to have intrahepatic stones undergo MRCP to determine the treatment method. After reviewing the surgical and medical records of these patients, we identified 49 patients with proven intrahepatic stones. Thirty-four of these patients also underwent ERCP; this group composes the study population. ERCP was usually performed to drain obstructed bile duct and to diagnose and remove bile duct stones. The decision to perform ERCP was made by clinicians after considering the patient's clinical condition and the adequacy of performing surgery in each patient. Nine patients (26%) of our study group had a history of recent biliary intervention (n = 7) or biliary—enteric anastomosis (n = 2) and therefore had pneumobilia. The interval between biliary intervention and MRCP was 3-28 months (mean, 8 months), and the interval between biliary—enteric anastomosis and MRCP was 50-109 months (mean, 80 months).

Our study included 22 women (65%) and 12 men (35%) from 33 to 70 years old (mean age, 54 years). ERCP was performed within 16 days (mean, 3 days) of MRCP examination. MRCP preceded ERCP in eight patients, and ERCP preceded MRCP in the remaining 26 patients. The patients had various clinical symptoms of biliary obstruction with or without concomitant infection; these symptoms included abdominal discomfort or pain, abdominal tenderness, fever, chills, and jaundice.

Intrahepatic stones were confirmed by surgery (hepatic resection) in 21 patients and by stone removal using percutaneous transhepatic cholangioscopy in 13 patients. The decision to perform surgery or cholangioscopy was made from the findings of both MRCP and ERCP. For purposes of this study, the findings at surgery or cholangioscopic stone removal were accepted as the standard reference for evaluation of MRCP and ERCP. Therefore, we excluded patients who showed radiologic evidence of intrahepatic stones but underwent neither of the two treatment procedures.

Imaging Techniques
MRCP examinations were performed on a 1.5-T MR system (Magnetom Vision; Siemens, Erlangen, Germany). A circular polarized phased array body coil with four elements was used. No medication or contrast medium was administered before imaging. Before MRCP was performed, T1-weighted axial and coronal gradient-echo MR imaging (TR/TE, 149/4.8; flip angle, 70°; section thickness, 8 mm; 18 sections in a 20-sec breath-hold) was performed to localize the biliary system. These images were then used as guides to perform MRCP. Two MRCP techniques were applied: single-slab rapid acquisition with relaxation enhancement (RARE) and multislice half-Fourier acquisition single-shot turbo spin-echo (HASTE). A radiologist was present during the entire examination and determined the acquisition angles that optimally delineated the biliary ducts. The slabs of a single-shot RARE sequence were obtained at various angles to allow optimal visualization of the bile ducts; the number of thick-slab acquisitions per patient ranged from three to 10 (mean, six acquisitions). Then multislice HASTE images were obtained in the coronal and oblique planes. Typically, the oblique plane was at an angle of 20-35° to the coronal plane to simulate a right anterior oblique projection on direct cholangiography. Each examination was performed during a single breath-hold.

The imaging parameters for the single-shot RARE sequence were TR/effective TE, infinite/1200; echo spacing, 11.5 msec; echo-train length, 240; flip angle, 150°; slab thickness, 70-96 mm; field of view, 300 mm; number of signals acquired, 1; matrix, 240 x 256; and acquisition time, 6.32 sec. The imaging parameters for the multislice HASTE sequence were TR/effective TE, infinite/95; echo spacing, 11.9 msec; echo-train length, 128; flip angle, 150°; section thickness, 4 mm with no gap; number of slices, 13-15 (range of coverage, 52-60 mm); field of view, 300 mm; number of signals acquired, 1; matrix, 240 x 256; and acquisition time, 20-23 sec. Fat saturation was used to reduce strong fat signal during image acquisition. The total acquisition time for all MR imaging steps was less than 15 min. Postprocessing of the multislice HASTE images was not performed.

ERCP was performed with the patient under conscious sedation. An under-couch fluoroscopic unit was used for screening and taking the hardcopy conventional films. Under fluoroscopic guidance, 10-30 mL of water-soluble contrast material was injected. Then multiple images of the bile ducts were obtained under the supervision of a radiologist to optimally show the entire ductal anatomy and reveal any abnormality. An average of 15 images were acquired per examination to reveal the presence of stones, sludge, and air bubbles in various planes and patient positions. Because one of the purposes of the ERCP examination was to localize bile duct stones, the examiners attempted to fully opacify the intrahepatic ductal system.

Analysis
All MRCP and ERCP images were retrospectively reviewed to compare MRCP and ERCP results. The MRCP images were reviewed independently by two radiologists who were unaware of the ERCP and final results. Both reviewers were experienced in abdominal MR imaging; neither had participated in the clinical interpretation of the MRCP images. However, both reviewers were aware that stones were present in the studies they were evaluating. All MRCP sequences in each patient were reviewed, but no attempt was made to evaluate separately the accuracy of the individual acquisitions. All direct ERCP images were reviewed by one radiologist who was unaware of the MRCP findings. Both MRCP and ERCP images were evaluated for the presence or absence of stones in each segment of the bile ducts (i.e., right or left intrahepatic ducts, common duct) and the gallbladder and for ancillary findings such as intrahepatic fluid collections or masses. Biliary calculi were diagnosed on MRCP as round, oval, or multiangular signal voids seen in the lumen. Surgical and pathologic findings (n = 21) or cholangioscopic findings identified during the procedure of stone removal (n = 13) were used as the standard of reference for determining the diagnostic performance of MRCP and ERCP.

We determined the statistical differences between findings on MRCP and on ERCP indicating the presence of stones in each segment of the bile ducts and gallbladder by applying the McNemar test with a significance level of p as less than 0.05. The sensitivity and specificity of MRCP and ERCP for the diagnosis of stones in the intrahepatic ducts, common duct, and gallbladder were calculated. Finally, agreement between the MRCP reviewers was evaluated using kappa values. Interobserver agreement was interpreted as very good ({kappa} > 0.80), good ({kappa} = 0.80-0.61), moderate ({kappa} = 0.60-0.41), fair ({kappa} = 0.41-0.21), or poor ({kappa} <= 0.20) [13].


Results
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
On the basis of the final diagnosis obtained at surgery or from cholangioscopic stone removal, 13 patients had stones in the right intrahepatic ducts, and 26 had stones in the left intrahepatic ducts. Common duct stones were found in eight patients, and gallbladder stones were found in three patients.

All MRCP examinations were adequate for analysis. The sensitivity and specificity of MRCP for detecting right intrahepatic duct stones were 92% and 95%, respectively; two independent reviewers had the same diagnostic performance (Table 1). The sensitivity and specificity of ERCP for detecting right intrahepatic duct stones were 38% and 100%, respectively. For the two reviewers, the sensitivity of MRCP for detecting left intrahepatic duct stones was 96% and 100%, and the specificity was 88%. The sensitivity and specificity of ERCP for detecting left intrahepatic duct stones were 69% and 88%, respectively. The low sensitivity of ERCP for detecting intrahepatic duct stones appeared to be caused by incomplete filling of the contrast material in the stone-containing intrahepatic ducts because of severe ductal stenosis (Figs. 1A,1B,1C and 2A,2B,2C). MRCP showed significantly higher sensitivity than ERCP for the diagnosis of intrahepatic stones (p < 0.001). We found no significant difference between MRCP and ERCP in the specificity for the diagnosis of intrahepatic stones (p > 0.05). Although individual sequences were not directly compared in this study, the multislice HASTE images appeared to be superior to the single-slab RARE images for confidence in diagnosing intrahepatic stones (Figs. 1A,1B,1C and 2A,2B,2C).


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TABLE 1 Detection of Stones in Bile Duct and Gallbladder: Diagnostic Performance of MR Cholangiopancreatography and Endoscopic Retrograde Cholangiopancreatography in 34 Patients

 


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Fig. 1A. 43-year-old woman with intrahepatic bile duct stones. ERCP image obtained after injection of contrast material with balloon occlusion of duct (arrow) shows dilatation of intrahepatic and extrahepatic bile ducts. No definite stones are seen in bile ducts.

 


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Fig. 1B. 43-year-old woman with intrahepatic bile duct stones. Coronal multislice half-Fourier acquisition single-shot turbo spin-echo MR cholangiopancreatography (MRCP) image (TR/TE, infinite/95) clearly shows intrahepatic stones (arrows) in right posteroinferior segment of liver.

 


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Fig. 1C. 43-year-old woman with intrahepatic bile duct stones. Coronal single-slab rapid acquisition with relaxation enhancement MRCP image (infinite/1200) also shows intrahepatic stones (solid arrow) in right lobe. However, conspicuity of intrahepatic stones is poor compared with visualization in B. Extrahepatic bile duct is not visualized because of biliary air (open arrows).

 


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Fig. 2A. 66-year-old man with intrahepatic bile duct stones. ERCP image shows dilatation of intrahepatic and extrahepatic bile ducts. No definite bile duct stones are visualized.

 


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Fig. 2B. 66-year-old man with intrahepatic bile duct stones. Coronal multislice half-Fourier acquisition single-shot turbo spin-echo MR cholangiopancreatography (MRCP) image (TR/TE, infinite/95) clearly shows intrahepatic stones (arrows) in liver segment IV.

 


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Fig. 2C. 66-year-old man with intrahepatic bile duct stones. Coronal single-slab rapid acquisition with relaxation enhancement MRCP image (infinite/1200) shows intrahepatic stones (arrow) inadequately compared with B.

 

For detecting calculi in the common duct or gallbladder, ERCP showed a slightly better diagnostic performance than MRCP; however, no statistically significant difference was seen between MRCP and ERCP in the sensitivity or specificity (p > 0.05). One of the MRCP reviewers interpreted biliary air as a common duct stone (Fig. 3A,3B,3C) in three patients, and the other reviewer made that interpretation in two patients (Table 1).



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Fig. 3A. 57-year-old woman with bile duct stones and biliary air. ERCP image obtained after injection of contrast material with balloon occlusion of duct (arrowhead) shows dilatation of intrahepatic and extrahepatic bile ducts and intrahepatic duct stones (arrow) in left lobe of liver.

 


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Fig. 3B. 57-year-old woman with bile duct stones and biliary air. Coronal single-slab rapid acquisition with relaxation enhancement (RARE) MR cholangiopancreatography image (TR/TE, infinite/1200) also shows intrahepatic duct stones in left lobe (open arrow). Poorly defined, hypointense lesion (solid arrow) is seen in proximal common duct.

 


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Fig. 3C. 57-year-old woman with bile duct stones and biliary air. Lateral single-slab RARE image (infinite/1200) produces air—fluid level (arrow) in proximal common duct, suggesting that lesion in proximal common duct is biliary air instead of stones.

 

In the diagnosis of right and left intrahepatic duct stones, interobserver agreement between the two MRCP reviewers was very good, with kappa values of 0.92 and 0.85, respectively. In common duct stones and gallbladder stones, the observed agreement was good and very good, respectively, and the kappa values were 0.67 and 0.88, respectively.

An intrahepatic fluid collection suggesting an abscess was diagnosed on MRCP by both reviewers, but it was not detected on ERCP. Aspiration performed under sonographic guidance confirmed that this lesion was an abscess. In two patients (10%) who underwent surgery, intrahepatic stones were associated with cholangiocarcinoma; however, neither the MRCP reviewers nor the ERCP reviewer had suggested the possibility of cholangiocarcinoma.


Discussion
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Intrahepatic stones are reported mainly in Far Eastern Asian populations and are not frequently encountered in the West [12, 14]. However, this disease is now being seen more frequently in Western societies, largely as a result of increased immigration from Asian countries [14]. Bile infection seems to play an important role in the pathogenesis of intrahepatic stones; the calculi are usually brown, bilirubin-pigmented, and friable. Generally, patients with intrahepatic stones have a prolonged history of recurrent complaints of abdominal pain, fever, chills, and jaundice [12, 14, 15]. Bile duct dilatation may be present in the ducts both proximal and distal to the calculi and may be disproportionately severe in the extrahepatic bile duct [14].

Compared with common bile duct stones, which can be managed effectively by therapeutic procedures during ERCP, endoscopic removal of intrahepatic stones is not easy [12]. Therefore, surgical intervention is indicated when the stones and strictures are localized to a single atrophic liver segment or lobe. Radiologic intervention also plays a significant role in the treatment of intrahepatic stones, particularly in patients who present with symptoms and signs of cholangitis. After effective percutaneous drainage has been established, subsequent cholangioscopic stone removal using a small-caliber endoscope [12] or fluoroscopy-guided stone removal using preshaped catheters and stone baskets [16] is commonly used. Accurate localization of intrahepatic stones is important for determining the treatment of choice for this disease.

Intrahepatic stones can be depicted on unenhanced CT, but the detection rate is not satisfactory (63-81%) because pigmented stones are sometimes not sufficiently hyperattenuating to be visible on CT [14]. With the improved spatial resolution provided by recently implemented MR techniques, MRCP has become an important technique in the evaluation of biliary calculi. Because of the narrow spacing of the radiofrequency refocusing pulses, single-shot RARE and multislice HASTE MRCP eliminate artifacts arising from respiratory motion and negligible susceptibility effects from bowel gas and metallic foreign bodies [17, 18]. The capability of MRCP to visualize peripheral intrahepatic bile ducts makes this technique well suited to the evaluation of intrahepatic stones. The combination of thick-slab RARE and multislice HASTE imaging takes no more than 15 min and results in a reliable test for evaluating the biliary tree.

Our findings showed that MRCP was superior to ERCP for the diagnosis of intrahepatic stones. This conclusion was based on the fact that ERCP could not opacify peripheral intrahepatic bile ducts because of the common occurrence of associated severe ductal stricture. Visualization of the intrahepatic ducts peripheral to the ductal stricture is often possible with ERCP but necessitates forced injection of contrast material, which may increase the risk of cholangitis and may actually worsen the course of the disease. In addition, the right intrahepatic bile ducts are normally more difficult to fill on ERCP performed with the patient prone, because they are the nondependent ducts. Air block may also be a factor in patients with intraductal air (Fig. 1A). These observations may be additional explanations for the lower sensitivity of ERCP in right intrahepatic stones. Moreover, ERCP has the disadvantage of being highly operator-dependent and of having procedure-related complications, including pancreatitis, sepsis, perforation, and hemorrhage. The principal advantage of MRCP for the diagnosis of intrahepatic stones is its ability to depict the entire biliary tract and to allow identification of dominant strictures without instrumentation [4]. In addition to the excellent diagnostic performance of MRCP, the very good ({kappa} > 0.80) interobserver agreement indicates that MRCP interpretation is objective and reliable.

Another potential advantage of MRCP is the simultaneous imaging of the hepatic parenchyma, which allows better differentiation between benign stenosis and the malignant processes that can be associated with intrahepatic stone disease. A number of investigations suggest that chronic infection and bile stasis induced by intrahepatic stones can lead to the development of epithelial adenomatous hyperplasia and cholangiocarcinoma [12, 14, 19]. However, the diagnosis of cholangiocarcinoma associated with intrahepatic stones is difficult to make because inflammatory lesions often show similar radiologic findings. Cholangiocarcinomas associated with intrahepatic stones have a poor prognosis because of the usually delayed diagnosis [19]. In our study, two patients (10%) were proven to have cholangiocarcinoma, but neither of the MRCP reviewers made this diagnosis. This failure to detect cholangiocarcinoma might be partly attributable to the fact that the imaging sequences performed in this study were not adequate for a comprehensive evaluation of the hepatic parenchyma. MRCP can also detect other abnormalities associated with intrahepatic stones, such as perihepatic biloma or the collection of free fluid in the perihepatic spaces [15].

Biliary air may also be confused with biliary calculi because both appear as filling defects in the high-signal-intensity bile on MRCP images. Many of our patients had a history of recent biliary intervention or biliary—enteric anastomosis and therefore had pneumobilia. However, differentiation is usually possible because biliary air is located in nondependent portions of the bile duct, whereas calculi tend to be located in dependent positions. Because stones have the typical appearance of biliary air, axial T2-weighted MR images and lateral projection of single-shot RARE MRCP images are helpful in differentiating biliary air from stone; the filling defects sometimes produce an air—fluid level on axial or sagittal images [1, 4, 20, 21] (Fig. 3A,3B,3C).

Our study has limitations. Because all patients were referred for MRCP examination rather than for both MRCP and ERCP, a selection bias was introduced. Specifically, this method of selection may result in examining a large number of patients who present technical difficulties or who have undergone incomplete ERCP examinations. However, because most patients in our hospital who were suspected of having intrahepatic stones underwent MRCP to determine treatment method, the selection bias might be small. In addition, most patients in our study had moderately or markedly dilated intrahepatic bile ducts. Therefore, our results may not apply to patients with mildly dilated or non-dilated ducts.

In summary, MRCP is a rapid, accurate, noninvasive means of showing the presence of intrahepatic stones. Findings in our study show the clinical applications of MRCP in intrahepatic stone disease. Because ERCP is neither an effective treatment method nor an accurate diagnostic modality, MRCP is a more effective diagnostic method for the evaluation of intrahepatic stones.


Acknowledgments
 
We thank Bonnie Hami, Department of Radiology, University Hospitals of Cleveland, for her editorial assistance in the preparation of this manuscript.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

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