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1 Department of Diagnostic Radiology and Research Institute of Radiological
Science, Yonsei University College of Medicine, Seoul, South Korea.
2 Department of Radiology, YongDong Severance Hospital, 146-92 Dokok-Dong,
Kangnam-Ku, Seoul 135-270, South Korea.
3 Department of Diagnostic Radiology, Asan Medical Center, University of Ulsan
College of Medicine, Seoul, South Korea.
4 Department of General Surgery, Yonsei University College of Medicine, Seoul,
South Korea.
5 Department of Internal Medicine, Yonsei University College of Medicine, Seoul,
South Korea.
6 Department of Nuclear Medicine, Yonsei University College of Medicine, Seoul,
South Korea.
Received February 16, 2004;
accepted after revision May 6, 2004.
Address correspondence to M.-S. Park
(radpms{at}yumc.yonsei.ac.kr).
Abstract
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SUBJECTS AND METHODS. Conventional heavily T2-weighted MR cholangiography with MnDPDP-enhanced T1-weighted MR cholangiography and ERCP were performed in seven patients with high clinical suspicion of biliary complications after laparoscopic cholecystectomy. The final diagnoses of complications were classified according to the presence and degree of bile duct injury, bile leakage, and retained stones.
RESULTS. The diagnoses on MR cholangiography were as follows: complete transection and occlusion of the common bile duct with bile leakage (n = 3), partial strictures of the common bile duct with bile leakage (n = 1), cystic duct leakage (n = 1), partial ligation of an aberrant right hepatic duct (n = 1), and hemorrhage without biliary complication (n = 1). The final diagnoses at surgery (n = 2) and ERCP (n = 5) were as follows: complete transection and occlusion of the common bile duct with bile leakage (n = 2), partial strictures of the common bile duct with bile leakage (n = 2), cystic duct leakage (n = 1), partial ligation of an aberrant right hepatic duct (n = 1), and hemorrhage without biliary complication (n = 1). MR cholangiography accurately yielded the same findings as the final diagnoses, except in one case with partial stricture of the bile duct with bile leakage (overdiagnosed as complete occlusion on MR cholangiography).
CONCLUSION. Combined conventional T2-weighted and MnDPDP-enhanced T1-weighted MR cholangiography may eliminate the use of other studies for the imaging of biliary complications after cholecystectomy if this preliminary data can be verified in a larger study.
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Since its introduction in 1991, technical advances in MR cholangiopancreatography have made it possible to generate high-quality images of the bile ducts, comparable to or superior to those of direct cholangiography [5–7]. Recently, MR cholangiography has been applied to various biliary diseases, not only in evaluating choledocholithiasis and malignant obstruction but also in assessing anatomic variants of the biliary tract, postsurgical anatomy and related complications, primary sclerosing cholangitis, and diseases of the gallbladder or cystic duct [8–11]. Coakley et al. [9] reported that conventional heavily T2-weighted MR cholangiography was an accurate noninvasive imaging technique for the assessment of complex biliary complications of cholecystectomy. However, heavily T2-weighted MR cholangiography cannot depict the dynamics of bile. Mangafodipir trisodium (MnDPDP) (Teslascan, Nycomed Amersham) is a safe and approved hepatocyte-selective T1-weighted MRI contrast agent, eliminated through the biliary system; therefore, theoretically it can be used as a biliary contrast agent with T1-weighted MRI [12–17]. Vitellas et al. [14, 16] reported that MnDPDP-enhanced MR cholangiography could show the presence of bile duct leaks after cholecystectomy. However, they did not evaluate other biliary complications, especially bile duct injury, which is usually accompanied by bile duct leak and is more important for management and prognosis.
The purpose of this prospective preliminary study was to determine the usefulness of heavily T2-weighted and fat-suppressed T1-weighted MR cholangiography before and after MnDPDP enhancement in evaluating early biliary complications of laparoscopic cholecystectomy.
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MR Cholangiography and ERCP
Patients were asked to fast for a minimum of 6 hr before their
examinations. MR cholangiography was performed with a 1.5-T superconducting
unit (Magnetom Vision, Siemens Medical Systems) and a phased-array torso coil.
We applied two MR cholangiographic techniques: single-shot RARE and multislice
half-Fourier RARE sequences (HASTE). The slab of a single-shot RARE sequence
was obtained at various angles to allow optimal visualization of the bile
ducts. The multislice half-Fourier RARE images were obtained at an angle of
20–35° to the coronal plane to simulate a right anterior oblique
projection on direct cholangiography. The imaging parameters for the
single-shot RARE sequence were TR/effective TE, infinite/1,200; echo-train
length, 240; flip angle, 150°; slab thickness, 50–70 mm; field of
view, 300–350 mm; matrix, 240 x 256; and acquisition time, 2.32
sec. The imaging parameters for multislice half-Fourier RARE sequence were
infinite/95; echotrain length, 128; flip angle, 150°; slab thickness,
3–5 mm with no gap; number of slices, 13–15 (range of coverage,
52–60 mm); field of view, 300–350 mm; matrix, 240 x 256; and
acquisition time, 18 sec. Postprocessing of the multislice half-Fourier RARE
images was performed.
After the patients were removed from the magnet, an IV injection of MnDPDP at a standard dose of 5 mmol/kg (0.1 mL/kg; maximum dose, 15 mL) was administered via a slow injection at 2–3 mL/min followed by a 10-mL saline flush. A contrastrelated adverse event, flushing, occurred in only one patient. Twenty-five to thirty minutes after injection, we obtained 3D T1-weighted fat-saturated volumetric interpolated breath-hold images (TR/TE, 4.2/1.6; flip angle, 12°; matrix, 205 x 256; field of view, 300–350 mm; and 24 partitions interpolated to 48 slices with a thickness of 1.3 mm). Routine heavily T2-weighted MR cholangiography using the same half-Fourier RARE sequence was repeatedly performed. Because MnDPDP is a negative contrast agent on T2-weighted images, we obtained enhanced heavily T2-weighted MR cholangiograms to compare with unenhanced T2-weighted MR cholangiograms. All MR cholangiograms were reviewed at the console by an abdominal radiologist before the patient was removed from the magnet, as a standard protocol.
ERCP examinations were performed by experienced gastroenterologists with the patient under conscious sedation. The gastroenterologist injected 10–30 mL of water-soluble contrast material under fluoroscopic guidance. Multiple images of the bile ducts then were obtained to show optimally the entire ductal anatomy and reveal any abnormalities.
Image Analysis
The MR cholangiograms were interpreted prospectively by the consensus of
two abdominal radiologists who were blinded to the patients' clinical
information and the ERCP findings. The source images and the 3D reconstruction
images of conventional heavily T2-weighted MR cholangiography and
MnDPDP-enhanced T1- and T2-weighted MR cholangiography were reviewed on a PACS
workstation monitor. Image analysis focused on the presence and location of
bile duct leaks, complete bile duct transection or occlusion, partial
stricture of bile duct, or retained bile duct stones. Bile duct leakage was
defined as contrast agent extravasation adjacent to a bile duct or contrast
agent opacification of a peritoneal drain on MnDPDP-enhanced T1-weighted MR
cholangiography with abnormal peritoneal fluid collection on conventional
heavily T2-weighted MR cholangiography and a signal loss of abnormal
peritoneal fluid collection on enhanced heavily T2-weighted MR
cholangiography. A complete transection or occlusion of the bile duct was
defined as an absence of opacification of the extrahepatic bile duct on
MnDPDP-enhanced MR cholangiography and persistence of signal of that on
enhanced heavily T2-weighted MR cholangiography with disconnection of
extrahepatic bile duct on conventional heavily T2-weighted MR cholangiography.
Stricture of the bile duct was defined as the opacification of the
extrahepatic bile duct on MnDPDP-enhanced MR cholangiography and signal loss
of the extrahepatic duct on enhanced heavily T2-weighted MR cholangiography,
despite the presence of a narrowing or a disconnected segment of the bile duct
on conventional heavily T2-weighted MR cholangiography.
The diagnosis of complications was classified as described in previous articles: complete transections and occlusions of the bile duct with or without bile leakage, partial strictures of the bile duct with or without bile leakage, cystic duct leakage and accessory bile duct leakage, occlusion of part of the intrahepatic duct, and residual stones [3, 18]. The same investigators reviewed the ERCP images using the method used for the MR cholangiograms. The diagnoses on MR cholangiography were compared with the final diagnoses at surgery or on ERCP.
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The final diagnoses at surgery (n = 2) and ERCP (n = 5) were as follows: complete transection and occlusion of the common bile duct with bile leakage (n = 2); partial strictures of the common bile duct with bile leakage (n = 2); cystic duct leakage (n = 1); partial ligation of an aberrant right hepatic duct (n = 1); and hemorrhage without biliary complication (n = 1). MR cholangiography accurately yielded the same findings as the final diagnoses, except one case with partial stricture of the bile duct with bile leakage (overdiagnosed as complete occlusion on MR cholangiography).
In two patients with complete transection and occlusion of the bile duct with bile leakage, ERCP was not diagnostic. Because ERCP could not show the proximal part of the obstructed site, it could not reveal bile leakage and the exact site of injury. MR cholangiography was diagnostic in those cases. Conventional T2-weighted MR cholangiography showed not only the distal but also the proximal parts of the disconnected site of the bile duct with abnormal peritoneal fluid collection. MnDPDP-enhanced T1-weighted MR cholangiography could reveal the presence and the exact site of bile leakage by showing contrast agent extravasation adjacent to the bile duct. Moreover, it could reveal the complete disconnection of the bile duct by showing the absence of opacification of the common bile duct. The two patients underwent operations, which confirmed the MR cholangiographic findings.
In one patient with partial strictures of the common bile duct with bile leakage, MR cholangiography was diagnostic. Conventional T2-weighted MR cholangiography showed an abnormal fluid collection with narrowing of the extrahepatic bile duct. MnDPDP-enhanced T1-weighted MR cholangiography showed contrast agent extravasation adjacent to the clipping site with opacification of the extrahepatic bile duct, suggesting partial stricture. The patient underwent ERCP with an internal stent, which confirmed the MR cholangiographic findings.
Another patient with partial strictures of the common bile duct with bile leakage was overdiagnosed on MR cholangiography. Conventional T2-weighted MR cholangiography showed an abnormal fluid collection with narrowing of the extrahepatic bile duct. MnDPDP-enhanced T1-weighted MR cholangiography showed contrast agent opacification of the peritoneal drain without opacification of the common bile duct. On MR cholangiography, this case was interpreted as the complete obstruction of the bile duct with bile leakage. The patient underwent ERCP with an internal stent, which showed the communication of the extrahepatic bile duct with bile leakage.
In one patient with cystic duct leakage, MR cholangiography was diagnostic. Conventional T2-weighted MR cholangiography showed an abnormal fluid collection without narrowing of the extrahepatic bile duct. MnDPDP-enhanced T1-weighted MR cholangiography showed contrast agent extravasation adjacent to the clipping site with normal opacification of the extrahepatic bile duct. The patients underwent ERCP with an internal stent, which confirmed the MR cholangiographic findings.
In a patient with an aberrant right hepatic duct ligation, MR cholangiography was diagnostic. Conventional T2-weighted MR cholangiography showed a dilated right posterior duct without an abnormal fluid collection. MnDPDP-enhanced T1-weighted MR cholangiography showed opacification of the right posterior duct without connection to the remaining hepatic duct. We interpreted the findings on MR cholangiography as partial ligation of the aberrant right posterior duct. ERCP did not show the right posterior duct. After 2 months, the patient underwent hepatobiliary scintigraphy, showing a photon-defect area of the right posterior segment, which confirmed the MR cholangiographic finding.
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Most patients with complications after laparoscopic cholecystectomy usually undergo a multitude of imaging examinations: sonography, CT, hepatobiliary scintigraphy, percutaneous aspiration, endoscopic retrograde cholangiography, or percutaneous cholangiography because no single test can provide complete and final diagnosis and some of them are too invasive to perform as the first examination [1–3, 16, 18, 19]. The main roles of CT or sonography with or without percutaneous aspiration are to establish the presence of bile in the peritoneal cavity and to drain it. However, they cannot establish the combined bile duct injury and the exact location of the bile leak. The main role of hepatobiliary scintigraphy is to establish the presence of a continuing bile leak. However, these techniques cannot provide the anatomic information. ERCP and percutaneous cholangiography can establish the presence of a continuing bile leak, provide exact anatomic diagnosis, and treat injury by decompressing the biliary tree or by dilating it. However, these techniques are invasive and could miss the proximal or distal part of the complete obstruction site; in this case, they are not diagnostic.
MnDPDP is a paramagnetic contrast agent originally designed for liver imaging. This contrast agent, consisting of manganese bound to dipyridoxyl diphosphate, is taken up by functioning hepatocytes and is primarily excreted via bile into the feces [13–17]. Therefore, MnDPDP-enhanced MR cholangiography provides information about biliary dynamics similar to that obtained on hepatobiliary scintigraphy or direct cholangiography [13–17].
Because manganese is a paramagnetic metal ion, it acts primarily on T1, resulting in T1 shortening, although it also acts on T2, resulting in T2 shortening [13–17]. Enhanced liver and functioning bile ducts, therefore, have higher signal intensity on T1-weighted images and lower signal intensity on T2-weighted images [13–17]. Therefore, MnDPDP is primarily used as a positive contrast agent in T1-weighted MR cholangiography. Additionally, it acts as a negative contrast agent on conventional heavily T2-weighted MR cholangiography. On T2-weighted MR cholangiography after MnDPDP administration, signal intensity is lost in the functioning bile duct but persists in the nonfunctioning bile duct. This characteristic property of combined T1- and T2-weighted MR cholangiography before and after administration of MnDPDP could be used as an excellent imaging tool in the evaluation of biliary dynamics [13–17].
Vitellas et al. [14, 16] reported that MnDPDP-enhanced MR cholangiography could show the presence of bile duct leaks, one of the biliary complications after cholecystectomy. However, they did not evaluate conventional T2-weighted MR cholangiography in conjunction with contrast-enhanced T1-weighted MR cholangiography, and they did not evaluate other biliary complications, especially regarding the presence and degree of bile duct injury. Bile duct injury usually is accompanied by a bile duct leak, which is important in a treatment plan and is a decisive factor in the prognosis of biliary complications.
Differentiating complete obstruction from partial stricture of the bile duct is important because the former is a definite indication for surgical treatment, whereas the latter is an indication for ERCP with an internal stent rather than surgery [18]. In our study, MnDPDP-enhanced T1-weighted MR cholangiography differentiated complete obstruction from partial stricture. MnDPDP-enhanced T1-weighted MR cholangiography clearly showed the two cases of complete obstruction with bile leakage by revealing extravasation of the contrast material from the bile duct without opacification of the distal part of the extrahepatic bile duct. On the other hand, because ERCP could not depict the proximal portion of the disconnected site of the bile duct, it could not reveal the presence of bile leakage and the distance of the injured bile duct from the confluence level; this information is important for surgical planning. ERCP has limitations in evaluating the completely obstructed cases.
In our study, MnDPDP-enhanced T1-weighted MR cholangiography clearly revealed a case of partial stricture with bile leakage by showing extravasation of the contrast agent from the bile duct with opacification of the extrahepatic bile duct, despite the presence of an abnormal narrowing segment of the bile duct on conventional T2-weighted MR cholangiography. In this case, the patient did not have a peritoneal drain. However, in a patient with a peritoneal drain, contrast opacification of the extrahepatic duct was absent on MnDPDP-enhanced T1-weighted MR cholangiography, suggesting the complete occlusion or transection of the bile duct. However, ERCP showed a partial stricture of the bile duct and not complete obstruction. It may be because the main bile flow was into the peritoneal drain rather than the extrahepatic duct, causing the degree of obstruction to be overestimated on MnDPDP-enhanced T1-weighted MR cholangiography in the patient with a peritoneal drain.
In our study, MnDPDP-enhanced T1-weighted MR cholangiography differentiated an abnormal fluid collection of biliary origin from that of nonbiliary origin. MnDPDP-enhanced T1-weighted MR cholangiography showed normal contrast filling of the biliary system without leakage or obstruction in a patient with a large amount of fluid collection on sonography and conventional T2-weighted MR cholangiography, suggesting a nonbiliary origin of fluid collection. It was diagnosed as hemorrhage.
We used 3D fat-saturated volumetric interpolated breath-hold examination (VIBE) as a T1-weighted MR cholangiographic sequence. A properly structured 3D gradient-echo sequence provides a higher signal-to-noise ratio, thinner sections, no gaps, and more comparable image contrast than a 2D gradient-echo sequence [20]. Moreover, a VIBE sequence provides isotropic or nearly isotropic spatial resolution, which allows multiplanar reconstruction images to be generated in any desired plane [20]. Lee et al. [15] reported that MnDPDP-enhanced T1-weighted MR cholangiography using a 3D VIBE sequence provided the definition of intrahepatic bile duct anatomy in nonobstructed biliary systems with excellent image quality. In our study, the slice thickness of MnDPDP-enhanced 3D T1-weighted MR cholangiography was 1.3 mm with no gap and hardly any partial volume artifact on maximum-intensity-projection images. Therefore, the image quality of coronal 3D T1-weighted MR cholangiography was excellent for evaluating the degree and location of the bile duct stricture and bile leakage. However, we did not compare the image quality of 3D MR cholangiography with that of 2D MR cholangiography because that was beyond the scope of our study.
Several limitations existed in this study. One limitation was the small number of patients. However, the cases in our study were various and showed the spectrum of biliary complications. A second limitation was that MnDPDP could not be used for the patients with jaundice, and the patient population in our study was restricted to the cases with biliary complications without jaundice. In our institutions, the patients with suspected biliary complications occurring within 1 month after laparoscopic cholecystectomy did not have jaundice. Therefore, the study population was restricted to the patients with early biliary complications after laparoscopic cholecystectomy. A third limitation was that bile duct injury could be overdiagnosed in patients with peritoneal drains. It is an important pitfall in the interpretation of not only MnDPDP-enhanced MR cholangiography but also unenhanced MR cholangiography. Because the main bile flow is into the peritoneal drain rather than the extrahepatic duct, on unenhanced T2-weighted MR cholangiography, the signal intensity of the common bile duct distal to the leaking site is weak and it is difficult to evaluate the distal common bile duct. On MnDPDP-enhanced T1-weighted MR cholangiography, the flow of contrast material is not into the distal common bile duct, and the signal intensity of the distal common bile duct is dark, resulting in overestimation of the bile duct injury.
The traditional algorithm for the imaging of postcholecystectomy biliary complications has been sonography, CT, or hepatobiliary scintigraphy, followed by diagnostic or therapeutic ERCP or percutaneous cholangiography; and some patients with biliary complications underwent surgery. We think that combined conventional T2-weighted and MnDPDP-enhanced T1-weighted MR cholangiography can be used to differentiate biliary complications from nonbiliary complications, simple leakage without bile duct injury from that with bile duct injury, and complete obstruction of the bile duct from partial stricture of the bile duct. Moreover, these techniques are noninvasive; therefore, they could be used as the first-line study for biliary complications after cholecystectomy (Fig. 5). After a diagnosis of simple leakage without bile duct injury is made on combined MR cholangiography, ERCP with sphincterotomy with or without an internal stent may be performed. After a diagnosis of partial stricture of the bile duct with or without bile leakage is made on combined MR cholangiography, ERCP with an internal stent may also be performed. Furthermore, after a diagnosis of a complete transection or occlusion of the bile duct with or without bile leakage is made on combined MR cholangiography, prompt surgical repair should be performed. ERCP or percutaneous transhepatic cholangiography is not necessary in these cases.
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In conclusion, this series suggests that combined conventional T2-weighted and MnDPDP-enhanced 3D T1-weighted MR cholangiography may eliminate the need for other studies for the imaging of early biliary complications after cholecystectomy if our preliminary data can be verified in a larger study,
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