Published online before print March 13, 2003, 10.1148/radiol.2272020207
(Radiology 2003;227:580-584.)
© RSNA, 2003
Acute Cholecystitis at T2-weighted and Manganese–enhanced T1-weighted MR Cholangiography: Preliminary Study1
Ki Whang Kim, MD,
Mi-Suk Park, MD,
Jeong-Sik Yu, MD,
Jun Pyo Chung, MD,
Young Hoon Ryu, MD,
Sang In Lee, MD,
Kwan Sik Lee, MD,
Sang-Wook Yoon, MD and
Kwang-Hun Lee, MD
1 From the Department of Diagnostic Radiology and Research Institute of Radiological Science (K.W.K., M.S.P., J.S.Y., Y.H.R., S.W.Y., K.H.L.) and the Department of Internal Medicine (J.P.C., S.I.L., K.S.L., H.J.P.), Yonsei University College of Medicine, YongDong Severance Hospital, 146-92 Dokok-Dong, Kangnam-Ku, Seoul 135-270, South Korea. Received March 6, 2002; revision requested April 25; final revision received August 30; accepted September 24. Address correspondence to K.W.K. (e-mail: kwkimyd@yumc.yonsei.ac.kr).
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ABSTRACT
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Twelve patients with symptoms of acute cholecystitis underwent heavily T2-weighted and mangafodipir trisodium–enhanced T1-weighted magnetic resonance (MR) cholangiography and cholescintigraphy before they underwent cholecystectomy. On T2-weighted MR cholangiographic images, morphologic evidence of outflow obstruction of the gallbladder was definitive in seven patients, equivocal in one, and absent in four. In all 12 patients, biliary dynamics depicted at manganese-enhanced T1-weighted MR cholangiography agreed completely with those depicted at hepatobiliary scintigraphy. T2-weighted MR cholangiography combined with manganese-enhanced T1-weighted MR cholangiography provides not only morphologic information but also functional information about the biliary system.
© RSNA, 2003
Index terms: Cholecystitis, 762.285, 763.285 • Gallbladder, calculi, 762.289, 763.289 • Gallbladder, MR, 762.121415, 762.12143 • Gallbladder, radionuclide studies, 762.12161
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INTRODUCTION
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Heavily T2-weighted magnetic resonance (MR) cholangiography is a noninvasive modality that has been proven to be accurate in the diagnosis of bile duct obstruction and choledocholithiasis (1,2). A previous report concerning the usefulness of MR cholangiography in the assessment of acute cholecystitis is focused on the detectability of impacted calculi in the cystic duct or gallbladder neck—the most important causes of acute cholecystitis (3). However, heavily T2-weighted MR cholangiography cannot depict the dynamics of bile.
Mangafodipir trisodium (Teslascan; Nycomed Amersham, Oslo, Norway) is a safe and approved hepatocyte-selective T1-weighted MR contrast agent that is eliminated through the biliary system; therefore, it can theoretically be used as a biliary contrast agent with T1-weighted MR imaging (4–7). To our knowledge, however, the potential role of this biliary contrast agent in the evaluation of acute cholecystitis has not been reported.
The purpose of this prospective and preliminary study was to evaluate the use of mangafodipir trisodium–enhanced T1-weighted MR cholangiography in conjunction with conventional heavily T2-weighted MR cholangiography in patients with acute cholecystitis.
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Materials and Methods
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Patient Population
Between September 2001 and January 2002, 14 consecutive patients who were suspected of having acute cholecystitis clinically (sudden onset of right upper quadrant tenderness, low-grade fever, and leukocytosis without jaundice) and at ultrasonography (US) (visualization of impacted stones in the gallbladder neck or cystic duct or positive US Murphy sign with gallbladder wall thickening or distention) were examined prospectively with MR cholangiography and hepatobiliary scintigraphy at our institution. Twelve of the 14 patients underwent cholecystectomy (open, n = 2; laparoscopic, n = 10), and they constituted our study population (six men, six women; age range, 25–73 years; mean age, 58 years). The study protocol was approved by the local ethics committee, and informed consent was obtained from all patients.
MR Cholangiography and Hepatobiliary Scintigraphy
Patients were asked to fast for a minimum of 6 hours. MR cholangiography was performed with a 1.5-T superconducting unit (Magnetom Vision; Siemens Medical Systems, Erlangen, Germany) and a phased-array torso coil. Routine MR cholangiography was performed with a half-Fourier rapid acquisition with relaxation enhancement (RARE) sequence with breath holds (repetition time msec/echo time [effective] msec of 
/95, flip angle of 150°, matrix of 240 x 256, field of view of 300–350 mm). We performed sequential multisection acquisitions (section thickness, 3–5 mm; imaging time, 18 seconds) followed by multiplanar reformatting techniques, and we usually obtained oblique coronal or sagittal images. After the patient was removed from the imager bore, an intravenous injection of mangafodipir trisodium at a standard dose of 5 µmol per kilogram of body weight (0.5 mL/kg; maximum dose, 50 mL) was administered as a slow injection at a rate of 2–3 mL/min followed by a 10-mL saline flush.
From 45 to 60 minutes after injection, we obtained three-dimensional T1-weighted fat-saturated volumetric interpolated breath-hold images (4.2/1.6; flip angle, 12°; matrix, 205 x 256; field of view, 300–350 mm; and 24 partitions interpolated to 48 sections with a thickness of 1.3 mm). All MR cholangiographic images were reviewed at the console by an abdominal radiologist (M.S.P.) before the patient was removed from the imager bore. A study was terminated when mangafodipir trisodium was seen clearly to fill the gallbladder or when, despite the fact that mangafodipir trisodium was not seen in the gallbladder on contrast material– enhanced T1-weighted MR images, impacted calculi in the cystic duct or gallbladder neck were definitively depicted on precontrast T2-weighted MR images.
Additional images were obtained with a delay of 4 hours when mangafodipir trisodium was not seen in the gallbladder, and impacted calculi in the cystic duct or gallbladder neck were not detected at RARE MR cholangiography. In one patient, 24-hour delayed images were obtained because the gallbladder was hyperintense at manganese-enhanced T1-weighted MR cholangiography despite the fact that there was a large impacted gallbladder neck calculus, which suggested complete obstruction.
Cholescintigraphy was performed after intravenous administration of 5 mCi (175 MBq) of technetium 99m–tagged diisopropyl–iminodiacetic acid (IDA) (Disofenin; New England Nuclear, North Billerica, Mass). Serial 15-minute-long imaging in the anterior projection was performed up to 60 minutes with a standard camera with a large field of view and a high-resolution collimator.
One hour after injection, additional lateral and left anterior oblique images were obtained. If gallbladder activity was not visualized, the study was then continued every hour up to 4 hours after injection of IDA.
Nine of the 12 patients underwent MR cholangiography before cholescintigraphy, and the remaining three patients underwent cholescintigraphy before MR cholangiography. The interval between MR cholangiography and cholescintigraphy was less than 12 hours.
Image Analysis
The MR cholangiographic images were interpreted by two abdominal radiologists (K.W.K., M.S.P.) in consensus. The source images and the three-dimensional reconstruction images were reviewed as hard copies. However, all diagnostic decisions were made on the basis of the source image findings. Image analysis focused on the presence and location of calculi in the gallbladder and on the associated findings, such as gallbladder wall thickening, fluid collection around the gallbladder, or common bile duct calculi seen at conventional heavily T2-weighted MR cholangiography. Outflow obstruction of the gallbladder was definitively defined when a signal void was identified within the cystic duct or gallbladder neck on images obtained in at least two projections. At manganese-enhanced T1-weighted MR cholangiography, the presence and time of visualization of the gallbladder and bile duct were evaluated.
Hepatobiliary MR images were interpreted prospectively by two radiologists (M.S.P., Y.H.R.). The presence and time of visualization of the gallbladder were evaluated.
Surgical and pathologic reports were evaluated by one author (S.W.Y.) with respect to the presence of calculi and the type of inflammation of the gallbladder.
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Results
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Clinical, radiologic, and pathologic results are summarized in the Table. At surgery, disease in 10 patients was diagnosed as acute calculus cholecystitis; in one patient, acute acalculous cholecystitis; and in one patient, chronic calculus cholecystitis. At conventional T2-weighted MR cholangiography, morphologic evidence of outflow obstruction of the gallbladder was definitive in seven patients, equivocal in one, and absent in four. At manganese-enhanced T1-weighted MR cholangiography, contrast enhancement of the gallbladder was not seen in nine patients, although it was seen in three.
In seven of the 12 patients, conventional heavily T2-weighted MR cholangiography demonstrated cystic duct or gallbladder neck calculi clearly, and morphologic evidence of gallbladder obstruction was definitive. Three-dimensional volume-interpolated T1-weighted MR cholangiography after the administration of mangafodipir trisodium depicted an enhanced common bile duct and hepatic duct but not the gallbladder; these findings suggest a flow obstruction in the gallbladder. For all seven patients, the diisopropyl-IDA scan failed to depict the gallbladder for up to 4 hours after injection of IDA (Fig 1).
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Figure 1a. Patient 1. (a) Coronal MR image obtained with a thin-section half-Fourier RARE sequence (/95 [effective]; flip angle, 150°) shows two cystic duct calculi (arrows). (b) Maximum intensity projection from coronal three-dimensional volumetric-interpolated T1-weighted gradient-echo image (4.2/1.6; flip angle, 12°) obtained 45 minutes after injection of mangafodipir trisodium shows the enhanced extrahepatic duct, but the gallbladder cannot be visualized. (c) Anterior hepatobiliary scintigraphic image obtained 60 minutes after injection of IDA demonstrates visualization of the extrahepatic duct (thin arrows) and small bowel (thick arrows) but fails to depict the gallbladder.
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Figure 1b. Patient 1. (a) Coronal MR image obtained with a thin-section half-Fourier RARE sequence (/95 [effective]; flip angle, 150°) shows two cystic duct calculi (arrows). (b) Maximum intensity projection from coronal three-dimensional volumetric-interpolated T1-weighted gradient-echo image (4.2/1.6; flip angle, 12°) obtained 45 minutes after injection of mangafodipir trisodium shows the enhanced extrahepatic duct, but the gallbladder cannot be visualized. (c) Anterior hepatobiliary scintigraphic image obtained 60 minutes after injection of IDA demonstrates visualization of the extrahepatic duct (thin arrows) and small bowel (thick arrows) but fails to depict the gallbladder.
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Figure 1c. Patient 1. (a) Coronal MR image obtained with a thin-section half-Fourier RARE sequence (/95 [effective]; flip angle, 150°) shows two cystic duct calculi (arrows). (b) Maximum intensity projection from coronal three-dimensional volumetric-interpolated T1-weighted gradient-echo image (4.2/1.6; flip angle, 12°) obtained 45 minutes after injection of mangafodipir trisodium shows the enhanced extrahepatic duct, but the gallbladder cannot be visualized. (c) Anterior hepatobiliary scintigraphic image obtained 60 minutes after injection of IDA demonstrates visualization of the extrahepatic duct (thin arrows) and small bowel (thick arrows) but fails to depict the gallbladder.
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In three of the 12 patients, heavily T2-weighted MR cholangiography demonstrated only floating calculi in the gallbladder lumen, without cystic duct or gallbladder neck calculus, and there was no evidence of outflow obstruction in the gallbladder. After the administration of mangafodipir trisodium, T1-weighted MR cholangiography depicted contrast enhancement of the gallbladder in two patients (later at surgery, one patient was found to have acute cholecystitis and the other had chronic cholecystitis), which suggests a patent cystic duct. In these patients, the gallbladder was visualized on the IDA scan obtained 45 minutes after IDA injection. In one patient, however, the gallbladder was not visualized at manganese-enhanced T1-weighted MR cholangiography up to 4 hours, and it was not visualized at IDA scanning up to 4 hours after IDA injection. In that patient (with diagnosis of acute cholecystitis at surgery), the findings at heavily T2-weighted MR cholangiography were mismatched with those at manganese-enhanced T1-weighted MR cholangiography and at IDA scanning.
In one patient (with diagnosis of acute cholecystitis at surgery) of the 12 patients, a cystic duct calculus was suspected at heavily T2-weighted MR cholangiography, although it could not be differentiated from part of the normal cystic duct. The gallbladder was not enhanced at T1-weighted MR cholangiography after mangafodipir trisodium injection. The IDA scan failed to depict the gallbladder for up to 4 hours after IDA injection (Fig 2).
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Figure 2a. Patient 6. (a) Coronal MR image obtained with a thin-section half-Fourier RARE sequence (/95 [effective]; flip angle, 150°) shows signal void lesions (arrows) in the cystic duct that are suspicious. However, they cannot be differentiated from a tortuous normal cystic duct. (b) Maximum intensity projection from coronal three-dimensional volumetric-interpolated T1-weighted gradient-echo MR image (4.2/1.6; flip angle, 12°) obtained 60 minutes after injection of mangafodipir trisodium shows the enhanced extrahepatic duct (arrows), but the gallbladder is not enhanced. (c) Anterior hepatobiliary scintigraphic image obtained 50 minutes after injection of IDA demonstrates visualization of the extrahepatic duct (thin arrow) and small bowel (thick arrows), but it does not depict the gallbladder.
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Figure 2b. Patient 6. (a) Coronal MR image obtained with a thin-section half-Fourier RARE sequence (/95 [effective]; flip angle, 150°) shows signal void lesions (arrows) in the cystic duct that are suspicious. However, they cannot be differentiated from a tortuous normal cystic duct. (b) Maximum intensity projection from coronal three-dimensional volumetric-interpolated T1-weighted gradient-echo MR image (4.2/1.6; flip angle, 12°) obtained 60 minutes after injection of mangafodipir trisodium shows the enhanced extrahepatic duct (arrows), but the gallbladder is not enhanced. (c) Anterior hepatobiliary scintigraphic image obtained 50 minutes after injection of IDA demonstrates visualization of the extrahepatic duct (thin arrow) and small bowel (thick arrows), but it does not depict the gallbladder.
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Figure 2c. Patient 6. (a) Coronal MR image obtained with a thin-section half-Fourier RARE sequence (/95 [effective]; flip angle, 150°) shows signal void lesions (arrows) in the cystic duct that are suspicious. However, they cannot be differentiated from a tortuous normal cystic duct. (b) Maximum intensity projection from coronal three-dimensional volumetric-interpolated T1-weighted gradient-echo MR image (4.2/1.6; flip angle, 12°) obtained 60 minutes after injection of mangafodipir trisodium shows the enhanced extrahepatic duct (arrows), but the gallbladder is not enhanced. (c) Anterior hepatobiliary scintigraphic image obtained 50 minutes after injection of IDA demonstrates visualization of the extrahepatic duct (thin arrow) and small bowel (thick arrows), but it does not depict the gallbladder.
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Patient 8 (with diagnosis of cardiovascular disorder) had simultaneous clinical symptoms of acute cholecystitis and acute pancreatitis. In this patient, findings at cholescintigraphy were interpreted as visualization of the gallbladder at 45 minutes after IDA injection, and the study was stopped at 60 minutes. Precontrast heavily T2-weighted MR cholangiography showed a distended gallbladder without calculus. The gallbladder was angulated between the neck and body. After injection of mangafodipir trisodium, T1-weighted MR cholangiography depicted the bile duct and the neck portion of the gallbladder as areas with high signal intensity. These findings were the same at 4 hours after injection. We reviewed the findings at cholescintigraphy and found that only the neck portion of the gallbladder and not the entire gallbladder had been visualized on the IDA scan (diagnosis of acute acalculous cholecystitis at surgery) (Fig 3).
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Figure 3a. Patient 8. (a) Coronal MR image obtained with a thin-section half-Fourier RARE sequence (/95 [effective]; flip angle, 150°) shows distended gallbladder (black and white long thick arrows) and ascites (short thick arrows). The gallbladder is angulated (thin arrow) between the neck and body. There is no calculus in the gallbladder or bile duct. (b) Coronal three-dimensional volumetric-interpolated T1-weighted gradient-echo source MR cholangiographic image (4.2/1.6; flip angle, 12°) obtained 60 minutes after injection of mangafodipir trisodium shows the enhanced extrahepatic duct and neck portion (black arrow) of the gallbladder. The body and fundal portion (white arrows) of the gallbladder are not enhanced. These findings were the same at 4 hours after injection (not shown). (c) Hepatobiliary scintigraphic image in the anterior projection obtained at 60 minutes after injection of IDA demonstrates visualization of the neck portion (white arrow) of the gallbladder, the extrahepatic duct (open), and the small bowel (black arrow). The body and fundal portion of the gallbladder cannot be visualized.
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Figure 3b. Patient 8. (a) Coronal MR image obtained with a thin-section half-Fourier RARE sequence (/95 [effective]; flip angle, 150°) shows distended gallbladder (black and white long thick arrows) and ascites (short thick arrows). The gallbladder is angulated (thin arrow) between the neck and body. There is no calculus in the gallbladder or bile duct. (b) Coronal three-dimensional volumetric-interpolated T1-weighted gradient-echo source MR cholangiographic image (4.2/1.6; flip angle, 12°) obtained 60 minutes after injection of mangafodipir trisodium shows the enhanced extrahepatic duct and neck portion (black arrow) of the gallbladder. The body and fundal portion (white arrows) of the gallbladder are not enhanced. These findings were the same at 4 hours after injection (not shown). (c) Hepatobiliary scintigraphic image in the anterior projection obtained at 60 minutes after injection of IDA demonstrates visualization of the neck portion (white arrow) of the gallbladder, the extrahepatic duct (open), and the small bowel (black arrow). The body and fundal portion of the gallbladder cannot be visualized.
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Figure 3c. Patient 8. (a) Coronal MR image obtained with a thin-section half-Fourier RARE sequence (/95 [effective]; flip angle, 150°) shows distended gallbladder (black and white long thick arrows) and ascites (short thick arrows). The gallbladder is angulated (thin arrow) between the neck and body. There is no calculus in the gallbladder or bile duct. (b) Coronal three-dimensional volumetric-interpolated T1-weighted gradient-echo source MR cholangiographic image (4.2/1.6; flip angle, 12°) obtained 60 minutes after injection of mangafodipir trisodium shows the enhanced extrahepatic duct and neck portion (black arrow) of the gallbladder. The body and fundal portion (white arrows) of the gallbladder are not enhanced. These findings were the same at 4 hours after injection (not shown). (c) Hepatobiliary scintigraphic image in the anterior projection obtained at 60 minutes after injection of IDA demonstrates visualization of the neck portion (white arrow) of the gallbladder, the extrahepatic duct (open), and the small bowel (black arrow). The body and fundal portion of the gallbladder cannot be visualized.
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Discussion
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Mangafodipir trisodium is a paramagnetic contrast agent that was originally designed for liver imaging. This contrast agent consists of manganese bound to N, N'-dipryidoxylethylenediamine-N, N'-diacetate 5, 5'-bis (phosphate), or DPDP, is taken up by functioning hepatocytes and is primarily excreted in bile into the feces (5–7). Because manganese is a paramagnetic metal ion, it acts primarily on T1 and results in T1 shortening, although it also acts on T2 and results in T2 shortening (5–7). Therefore, enhanced liver and functioning bile ducts have a higher signal intensity on T1-weighted MR images and a lower signal intensity on T2-weighted MR images (5–7). The signal intensity of bile ducts that are obstructed or otherwise not functioning as a result of stasis may not be affected because biliary stasis in the setting of strictures or stones reduces the excretion of biliary manganese (5). Theoretically, this characteristic property of manganese-enhanced MR cholangiography could allow noninvasive imaging in the evaluation of biliary dynamics (5).
Results in our study regarding the presence of cystic duct patency at manganese-enhanced T1-weighted MR cholangiography agreed completely with those at hepatobiliary scintigraphy. In the patents with a patent cystic duct, manganese-enhanced T1-weighted MR cholangiography demonstrated both the bile duct and gallbladder as areas with high signal intensity that reflect the normal flow of the biliary system without obstruction or stasis. In the patients with cystic duct obstruction, however, the gallbladder was not enhanced. Therefore, manganese-enhanced MR cholangiography depicts biliary dynamics as they are depicted at cholescintigraphy and provides functional information about the biliary system.
Conventional heavily T2-weighted MR cholangiography is able to depict stones smaller than 3 mm and to show both the proximal and distal parts of the obstruction site despite a complete obstruction. Therefore, it can provide accurate information concerning the site and the cause of obstruction. MR cholangiography has been used to examine the gallbladder and cystic duct in the setting of acute cholecystitis, and it demonstrates a high sensitivity for depiction of an impacted cystic duct or gallbladder neck stones (3,8).
In this study, an impacted cystic duct or gallbladder neck calculi were demonstrated accurately to a resolution as small as 3 mm. Images in seven patients clearly depicted the impacted calculi as the cause of cystic duct obstruction, and we were confident in our determination of outflow obstruction of the gallbladder. In one patient, conventional heavily T2-weighted MR cholangiography depicted a signal void lesion in the cystic duct that was suspicious. We were unable to differentiate the calculus from part of the normal cystic duct in that patient. In another patient, many floating stones were seen in the gallbladder lumen, but no stones were seen in the cystic duct or gallbladder neck at conventional heavily T2-weighted MR cholangiography. After injection of mangafodipir trisodium in both patients, however, MR cholangiography clearly depicted the cystic duct obstruction, but the gallbladder was not depicted on T1-weighted images acquired for up to 60 minutes. Cholescintigraphy did not depict the gallbladder but did depict the normal common bile duct and bowel (diagnosis of acute cholecystitis at surgery).
Results with MR cholangiography in conjunction with conventional heavily T2-weighted and manganese-enhanced T1-weighted MR imaging are superior to those with conventional heavily T2-weighted MR cholangiography without mangafodipir trisodium in the diagnosis of acute cholecystitis, particularly when evidence of cystic duct obstruction is equivocal or negative.
In patients with acalculous cholecystitis, diagnosis and definitive treatment are frequently delayed because a demonstrable cause of obstruction is not present. In such patients, therefore, other imaging modalities (US and computed tomography [CT]) are less sensitive than cholescintigraphy because they cannot provide functional information concerning biliary dynamics (9). The case of acalculous cholecystitis in our study was more complicated. Findings at cholescintigraphy in this case were interpreted as visualization of the gallbladder. However, the gallbladder that was visualized was proven to be only a portion of the gallbladder neck and not the entire gallbladder. In contrast with cholescintigraphy, MR cholangiography performed with T1- and T2-weighted MR imaging combined with imaging before and after injection of mangafodipir trisodium was able to depict the portion of the gallbladder with contrast material filling in connection with the remaining portion. In this case, therefore, it was easier to achieve accurate findings with MR cholangiography than with cholescintigraphy.
Several limitations exist in this study. One limitation is the small number of patients. A second limitation is that we did not obtain serial images at manganese-enhanced MR cholangiography. It has been reported that the optimal time to evaluate liver parenchyma and the bile duct is between 15 and 20 minutes after injection, which roughly corresponds to the hepatocyte and biliary tract phase at hepatobiliary scintigraphy (5–7). Therefore, we used the criterion of acute cholecystitis at manganese-enhanced T1-weighted MR cholangiography as nonvisualization of the gallbladder with visualization of the normal common bile duct and bowel up to 60 minutes; this criterion was consistent with that for hepatobiliary scintigraphy. A third limitation of this study is that we did not perform T1-weighted MR cholangiography before the administration of mangafodipir trisodium. In patient 3, high signal intensity persisted in the gallbladder at manganese-enhanced T1-weighted MR cholangiography, despite the fact that there was a large impacted gallbladder neck calculus; this finding suggested complete obstruction.
We repeated T1-weighted MR cholangiography after 24 hours, and the high signal intensity persisted in the gallbladder; this finding suggests that the gallbladder was hyperintense from the beginning (ie, the hyperintensity did not occur after the injection of contrast agent). A fourth limitation is that the use of mangafodipir trisodium for anything other than depiction of focal liver lesions has not been approved by the U.S. Food and Drug Administration. The only adverse reaction to the mangafodipir trisodium infusion in our study was in one patient who felt nauseous.
In conclusion, T2-weighted MR cholangiography combined with manganese-enhanced T1-weighted MR cholangiography provides not only anatomic details but also functional details of the biliary system. Mangafodipir trisodium–enhanced T1-weighted MR cholangiography is useful in the diagnosis of acute cholecystitis, especially when evidence of cystic duct obstruction at heavily T2-weighted MR cholangiography is equivocal or negative but the clinical suspicion is high. Large-scale studies will be necessary to determine if this combined imaging technique can replace other cross-sectional modalities, such as CT and US, and the functional modality of hepatobiliary scintigraphy.
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FOOTNOTES
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Abbreviations: IDA = diisopropyl–iminodiacetic acid,
RARE = rapid acquisition with relaxation enhancement
Author contributions: Guarantor of integrity of entire study, K.W.K.; study concepts and design, K.W.K., M.S.P.; literature research, M.S.P.; clinical studies, J.P.C., S.I.L., K.S.L.; data acquisition, S.W.Y., K.H.L.; data analysis/interpretation, K.W.K., M.S.P., Y.H.R.; manuscript preparation, M.S.P.; manuscript definition of intellectual content, J.S.Y.; manuscript editing, M.S.P.; manuscript revision/review, J.S.Y.; manuscript final version approval, K.W.K.
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ABSTRACT
INTRODUCTION
