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Original Report |
1 Department of Radiology, Hôpital Erasme, University Clinics of Brussels,
Free University of Brussels, Route de Lennik, 808, Brussels B-1070,
Belgium.
2 Department of Gastroenterology, Hôpital Erasme, University Clinics of
Brussels, Free University of Brussels, Brussels, Belgium.
Received June 4, 2003;
accepted after revision August 26, 2004.
Address corerspondence to N. Hottat
(nhottat{at}hotmail.com).
Abstract
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CONCLUSION. Mn-DPDP-enhanced T1-weighted MR cholangiography may provide useful functional information and may aid in the assessment of the patency of biliary–enteric anastomoses.
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Mangafodipir trisodium (Teslascan, Amersham Health) is a safe and approved hepatobiliary MR contrast agent [4] composed of the manganese ion (Mn++) and the ligand dipyridoxyl diphosphate (DPDP), a vitamin B6 (pyridoxine hydrochloride) analog. This contrast medium causes T1 shortening as a result of the paramagnetic effects of the manganese metal ion. Mn-DPDP (molecular weight, 757.33) is isotonic with blood and has a low viscosity.
After IV administration of Mn-DPDP, the manganese is released gradually from the ligand and bound to plasma proteins, being replaced in the compound by zinc. The manganese is taken up by mitochondria of parenchymatous cells in the liver principally and also in the pancreas, adrenal glands, kidneys, and myocytes. Sixty percent of the manganese is excreted in the feces over the following 4 days. Patients with hepatic dysfunction, such as a cirrhotic liver, may not have normal excretion of the contrast medium in the biliary system and delayed excretion may occur [5].
Mn-DPDP was first developed to improve the detection and the characterization of hepatic lesions but can also be used as a biliary contrast agent with T1-weighted MRI. In this setting, it has been used to detect bile duct leaks, to define intrahepatic biliary anatomy in healthy transplant donor candidates, and to improve diagnostic performance for functional biliary disorders [6–9]. Previous reports have shown that liver enhancement begins at 1 min after injection, reaching a steady-state enhancement at 5–10 min that lasts 4 hr [4, 10]. Mitchell and Alam [11] showed that normal biliary systems present intra- and extrahepatic bile duct enhancement on 3D gradient-echo T1-weighted images, respectively, within 10 and 20 min after IV administration of Mn-DPDP. Shepard et al. [12] recommended a timing of 60 min to achieve optimal opacification of the biliary tree in a heterogeneous population of patients with normal and abnormal results on liver function tests.
Our study was devoted to the evaluation of patients with biliary–enteric anastomoses using high-resolution 3D gradient-echo T1-weighted MR cholangiography acquired at least 1 hr after IV administration of Mn-DPDP. Mn-DPDP-enhanced MR cholangiography was compared with T2-weighted MR cholangiography, and both were compared with percutaneous transhepatic cholangiography when available or with clinical and biologic follow-up.
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Imaging Technique
All MRI studies were performed using a fixed imaging protocol with a 1.5-T
superconducting magnet (Intera, Philips Medical Systems) equipped with a
synergy body coil and having the coil sensitivity-encoding (SENSE) technique
available [13].
After a scout view was obtained, a reference measurement scan was obtained using the coils and related images acquired with the homogeneous quadrature body coil for a reliable sensitivity mapping of each coil element. Axial and coronal multislice single-shot turbo spin-echo T2-weighted imaging with SENSE and respiratory triggering covering the entire liver was then performed with the following parameters: TR/TEeff, infinite/60; echo-train length, 72; section thickness, 4–5 mm with 0.4-mm slice gap; field of view, 400–450 mm with rectangular field of view depending on the body habitus; 1 signal acquired; matrix, 380 x 512; and acquisition time, 650 msec per slice. Conventional MR cholangiography was performed with a breath-hold half-Fourier thick-slab single-shot turbo spin-echo T2-weighted sequence in the coronal oblique and axial planes at various angles with the following parameters: infinite/1,000; echo-train length, 256; section thickness, 20–40 mm; field of view, 250 x 250 mm; 1 signal acquired; matrix, 256 x 512; and acquisition time, 2.5 sec per slice. With these three data acquisition techniques (axial and coronal multislice and single-slice T2-weighted scans), depiction of the biliary tract and liver parenchyma was achieved in approximately 5 min.
Subsequently, a breath-hold axial and coronal high-resolution volumetric 3D gradient-echo T1-weighted sequence with SENSE (5.2/1.46; flip angle, 35°; 65 slices; slice thickness, 2.5 mm with 50% overlap; imaging matrix, 400 x 512; field of view, 450 mm with rectangular field of view depending on the body habitus; acquisition time, 20 sec) was performed 60 min after a slow IV infusion (2 mL/min) of Mn-DPDP at a dose of 0.5 mL/kg of body weight. After this period, if no contrast medium was observed in the digestive tract, the sequence was repeated every 30 min until the biliary–enteric anastomoses were filled with contrast material. The 3D image sets were postprocessed with a maximum-intensity-projection reconstruction algorithm that was completed immediately after the acquisition. Patients were screened for potential adverse reactions during the infusion and scanning periods.
Image Analysis
All the MR sequences were interpreted at an interactive workstation (Easy
Vision, Philips Medical Systems) independently by two experienced MR
radiologists not involved in image acquisition who were blinded to patient
identification and all clinical, laboratory, pathologic, and prior imaging
examination findings. Axial and coronal multislice and single-slice
T2-weighted scans were interpreted independent of the volumetric 3D
gradient-echo T1-weighted scans during a separate session. The MRI findings of
both sequences were recorded on standardized data sheets.
The observers evaluated the images for the following signs: depiction of intrahepatic bile ducts and biliary–enteric anastomoses, dilatation of intrahepatic bile ducts, signs of cholangitis, obstruction of the anastomoses, intrahepatic bile duct strictures, and presence of stones and anastomotic leakage. The diagnosis of dilatation of the intrahepatic bile ducts was based on measurement of dilated ducts according to previously published criteria (diameter, > 3 mm without gentle tapering) [2]. Intrahepatic bile ducts strictures were diagnosed as disparities in ductal caliber. Cholangitis was diagnosed on the basis of findings of irregularities and a beaded appearance of the bile ducts. Stones were diagnosed when filling defects lying in the posterior portion of the ducts on the axial scans were detected, and anastomotic leakage was diagnosed when a fluid collection independent of the anastomotic jejunal loop and connected to the bile ducts or the anastomoses was evident.
The observers were asked to grade the depiction of the morphologic signs separately on T2-weighted and Mn-DPDP-enhanced T1-weighted images using a 3-point scale defined as follows: 1, absent sign; 2, visible sign; and 3, excellent depiction of the sign.
On T2-weighted images, obstruction of the biliary–enteric anastomoses was considered if intrahepatic biliary ducts were dilated and a signal void was present between the ducts and a fluid-filled jejunal loop. On Mn-DPDP-enhanced MR cholangiography, obstruction was considered when the anastomosis was not depicted and if no contrast material was detected in the jejunal loop 1 hr after the administration of Mn-DPDP. The MR results concerning the functionality of the anastomoses were separately compared with the results from percutaneous transhepatic cholangiography or with findings from clinical and biologic follow-up.
Statistical Analysis
The delineation of morphologic signs on T2-weighted and Mn-DPDP-enhanced
T1-weighted MR cholangiography and interobserver variability were studied by
comparing point-by-point the morphologic observations recorded on standardized
data sheets and their respective grading. The Cohen's kappa coefficient was
computed to evaluate the agreement of the grading between observers.
To assess the quality of morphologic depiction, we compared the grading of the T2-weighted and Mn-DPDP-enhanced T1-weighted MR cholangiography images using a Wilcoxon's signed rank test. Differences were considered statistically significant when the p value was less than 0.001.
The sensitivity and specificity of T2-weighted and Mn-DPDP-enhanced T1-weighted MR cholangiography were determined for the assessment of the functionality of the anastomoses considering percutaneous transhepatic cholangiography as the standard of reference.
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= 1). The reason for
referral and comparative results regarding the visualization of the
biliary–enteric anastomoses and biliary tract dilatation and obstruction
compared with percutaneous transhepatic cholangiography and follow-up are
shown in Table 1. None of the
patients presented with jaundice, and the highest bilirubin level was detected
in patient 8 (2.5 mg/dL; normal range, 0–1.2 mg/dL).
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Morphologic Signs
The grading of the visualization of the intrahepatic bile ducts was
statistically significantly superior on T2-weighted MR cholangiography
compared with Mn-DPDP-enhanced T1-weighted MR cholangiography (p <
0.0001). T2-weighted images were also graded significantly higher than
Mn-DPDP-enhanced T1-weighted images for the depiction of dilatation of
intrahepatic bile ducts, signs of cholangitis, and intrahepatic bile duct
strictures (p = 0.0002).
Dilatation of intrahepatic bile ducts was detected with both techniques in seven of the 13 patients, and contrast filling of the intrahepatic biliary ducts was asymmetric in three patients with focal dilatation of the intrahepatic bile ducts (Fig. 1A, 1B). Signs of cholangitis were detected in four of the 13 patients and in three of the 13 patients, respectively, on conventional T2-weighted MR cholangiography and contrast-enhanced T1-weighted MR cholangiography. Multiple intrahepatic bile duct strictures were identified in four of the 13 patients with both techniques, but delineation of the strictures was superior on conventional T2-weighted MR cholangiography (Fig. 2A, 2B, 2C, 2D).
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Patency of the Biliary–Enteric Anastomoses
On T2-weighted MR cholangiography, the biliary–enteric anastomoses
could be visualized in 85% (11/13) of the patients and were obscured in the
remaining two due to overlapping fluid (patients 8 and 12). On
contrast-enhanced T1-weighted MR cholangiography, the biliary–enteric
anastomoses were visualized in 100% (13/13) of the patients (Fig.
3A,
3B,
3C,
3D). Excretion of Mn-DPDP into
the anastomoses was observed within 1 hr in all but two patients (patients 2
and 12) in whom the anastomoses were opacified, respectively, 2.5 and 3 hr
after the administration of Mn-DPDP. In these two patients, the anastomoses
were interpreted as obstructed.
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Contrast-enhanced T1-weighted MR cholangiography results were confirmed by
percutaneous transhepatic cholangiography in nine patients. However, on
conventional T2-weighted MR cholangiography two false-positive results of
obstructed anastomoses (patients 6 and 13) and one inconclusive result
(patient 12 in whom the site of the anastomoses was not visualized at all and
who had intrahepatic bile duct dilatation because of intrahepatic strictures)
were observed. None of the patients presented with stones or had bile duct
leakage.
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Using percutaneous transhepatic cholangiography as the standard of reference, we found that contrast-enhanced T1-weighted MR cholangiography assessed the functionality of the anastomoses with a sensitivity of 100% (2/2) and a specificity of 100% (7/7), whereas T2-weighted MR cholangiography had a sensitivity of 50% (1/2) and a specificity of 57% (4/7). Concerning the four patients for whom only a clinical follow-up was required, contrast-enhanced T1-weighted MR cholangiography and T2-weighted MR cholangiography showed functional anastomoses and normal intrahepatic bile ducts.
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Conventional MR cholangiography uses heavily T2-weighted images to illustrate biliary anatomy without the use of contrast agents and has been reported as an accurate technique to evaluate biliary–enteric anastomoses in patients with jaundice [2]. However, the lack of functional information concerning bile excretion may constitute an inherent limitation of conventional MR cholangiography, particularly in differentiating patients with obstructive and nonobstructive dilatation of the intrahepatic bile ducts. Contrast-enhanced T1-weighted MR cholangiography after Mn-DPDP administration has the potential to provide morphologic and functional information and has been used as an alternative to conventional MR cholangiography in assessing intrahepatic biliary anatomy [7, 8], bile duct leaks [6], and functional biliary disorders [5, 9].
In this study, contrast-enhanced MR cholangiography images obtained at least 1 hr after the administration of Mn-DPDP were compared with conventional T2-weighted MR cholangiography images in a series of 13 patients with biliary–enteric anastomoses. Biliary–enteric anastomoses were depicted in all 13 patients on Mn-DPDP-enhanced T1-weighted MR cholangiography and in 11 of the 13 patients on conventional T2-weighted MR cholangiography. This discrepancy was not related to the presence of susceptibility artifacts but mainly to the presence of ascites that precluded visualization of the anastomoses on T2-weighted MR cholangiography.
We considered that an obstruction of the anastomoses was present on T2-weighted MR cholangiography when the intrahepatic bile ducts were dilated and the morphology of the anastomoses could not be depicted. Accordingly, an obstruction of the anastomoses was suggested on conventional T2-weighted MR cholangiography in three patients, but only one case was confirmed with percutaneous transhepatic cholangiography and the two other cases were false-positive results.
On the other hand, opacification of the anastomoses and the jejunal loop was observed with contrast-enhanced MR cholangiography 1 hr after the administration of Mn-DPDP in all patients but two. Both patients presented with delayed excretion of Mn-DPDP (> 2 hr), and at percutaneous transhepatic cholangiography they presented with a stricture that was treated by dilatation with a balloon. The detection of adequate contrast filling of the jejunal loop on contrast-enhanced MR cholangiography provides direct visualization of the patency of the anastomoses unlike conventional T2-weighted MR cholangiography, for which this assessment was shown to be less robust. This observation is interesting because seven of 13 patients presented with dilated intrahepatic bile ducts and only two of them had an obstruction of the biliary–enteric anastomoses at percutaneous transhepatic cholangiography. The remaining patients had dilated bile ducts because of primary sclerosing cholangitis, cholangitis, or intrahepatic bile duct strictures. Therefore, the presence of dilated bile ducts seems to be not sufficient to diagnose biliary–enteric anastomoses obstruction and to justify going further with percutaneous transhepatic cholangiography.
Although these results are encouraging, the present study has some limitations. The standard of reference used in assessing the patency of the anastomoses (percutaneous transhepatic cholangiography) was lacking in four patients in whom satisfactory findings at 6-month clinical and biologic follow-up were obtained. Despite the fact that we used a high-resolution volumetric 3D T1-weighted sequence, delineation of third-order intrahepatic bile ducts and intrahepatic strictures was inferior compared with conventional T2-weighted MR cholangiography, which may be a limitation in assessing primary sclerosing cholangitis recurrence. We could argue that this finding may be related to the temporal window chosen for scanning after Mn-DPDP administration. However, in those patients with primary sclerosing cholangitis recurrence, we observed delayed contrast enhancement of the more dilated intrahepatic bile ducts displayed on T2-weighted MR cholangiography.
Contrast-enhanced T1-weighted MR cholangiography with Mn-DPDP lengthens the scanning time and increases the cost of MR cholangiography; therefore, this technique should be used in patients presenting with intrahepatic bile duct dilatation in whom conventional MR cholangiography is inconclusive to avoid unnecessary invasive and expensive procedures. Unfortunately, conventional T2-weighted MR cholangiography must be performed before or immediately after (within 5 min) administering Mn-DPDP because this contrast agent decreases the T2 relaxation time and thereby the signal intensity of the bile within the bile ducts [11, 9]. However, in case of nondilated intrahepatic bile ducts on T2-weighted MR cholangiography, biliary obstruction is excluded and the administration of this contrast medium is useless, which means that performing T2-weighted sequences first is mandatory to make a decision about whether to inject Mn-DPDP.
In this study, excretion of Mn-DPDP was not related to the serum bilirubin level. Moreover, both patients presenting an obstruction of the anastomoses had a normal serum bilirubin level. Further investigation of a larger number of patients with serial dynamic acquisitions may be interesting to confirm and refine the optimal temporal window of contrast-enhanced MR cholangiography with Mn-DPDP in patients with surgically modified bile ducts and possible underlying liver disease.
In conclusion, contrast-enhanced T1-weighted MR cholangiography with IV Mn-DPDP provides useful anatomic and functional information in patients with biliary–enteric anastomoses suspected of having biliary obstruction on conventional T2-weighted MR cholangiography.
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