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Published online before print October 29, 2004, 10.1148/radiol.2333031977
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(Radiology 2004;233:659-666.)
© RSNA, 2004


Gastrointestinal Imaging

Defining Intrahepatic Biliary Anatomy in Living Liver Transplant Donor Candidates at Mangafodipir Trisodium–enhanced MR Cholangiography versus Conventional T2-weighted MR Cholangiography1

Vivian S. Lee, MD, PhD, Glenn A. Krinsky, MD, Carol A. Nazzaro, RN, Jerry S. Chang, MD, James S. Babb, PhD, Jennifer C. Lin, BS, Glyn R. Morgan, MD and Lewis W. Teperman, MD

1 From the Departments of Radiology (V.S.L., G.A.K., C.A.N., J.S.C., J.S.B., J.C.L.) and Transplant Surgery (G.R.M., L.W.T.), New York University Medical Center, 530 First Ave, New York, NY 10016. Received December 6, 2003; revision requested February 6, 2004; revision received February 26; accepted March 29. Supported by Amersham Health, Princeton, NJ. Address correspondence to V.S.L. (e-mail: vivian.lee@med.nyu.edu).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To compare three-dimensional (3D) mangafodipir trisodium–enhanced T1-weighted magnetic resonance (MR) cholangiography with conventional T2-weighted MR cholangiography for depiction and definition of intrahepatic biliary anatomy in liver transplant donor candidates.

MATERIALS AND METHODS: One hundred eight healthy liver transplant donor candidates were examined with two MR cholangiographic methods. All candidates gave written informed consent, and the study was approved by the institutional review board. First, breath-hold transverse and coronal half-Fourier single-shot turbo spin-echo and breath-hold oblique coronal heavily T2-weighted turbo spin-echo sequences were performed. Second, mangafodipir trisodium–enhanced breath-hold fat-suppressed 3D gradient-echo sequences were performed through the ducts (oblique coronal plane) and through the entire liver (transverse plane). Interpretation of biliary anatomy findings, particularly variants affecting right liver lobe biliary drainage, and degree of interpretation confidence at both 3D mangafodipir trisodium–enhanced MR cholangiography and T2-weighted MR cholangiography were recorded and compared by using the Wilcoxon signed rank test. Then, consensus interpretations of both MR image sets together were performed. Intraoperative cholangiography was the reference-standard examination for 51 subjects who underwent right lobe hepatectomy. The McNemar test was used to compare the accuracies of the individual MR techniques with that of the consensus interpretation of both image sets together and to compare each technique with intraoperative cholangiography.

RESULTS: Biliary anatomy was visualized with mangafodipir trisodium enhancement in all patients. Mangafodipir trisodium–enhanced image findings agreed with findings seen at combined interpretations significantly more often than did T2-weighted image findings (in 107 [99%] vs 88 [82%] of 108 donor candidates, P < .001). Confidence was significantly higher with the mangafodipir trisodium–enhanced images than with the T2-weighted images (mean confidence score, 4.5 vs 3.4; P < .001). In the 51 candidates who underwent intraoperative cholangiography, mangafodipir trisodium–enhanced imaging correctly depicted the biliary anatomy more often than did T2-weighted imaging (in 47 [92%] vs 43 [84%] donor candidates, P = .14), whereas the two MR imaging techniques combined correctly depicted the anatomy in 48 (94%) candidates.

CONCLUSION: Mangafodipir trisodium–enhanced 3D MR cholangiography depicts intrahepatic biliary anatomy, especially right duct variants, more accurately than does conventional T2-weighted MR cholangiography.

© RSNA, 2004

Index terms: Bile ducts, anatomy • Bile ducts, MR, 768.121411, 768.121412, 768.121416, 768.12142, 768.12143 • Liver, MR, 768.121411, 768.121412, 768.121416, 768.12142, 768.12143 • Liver, transplantation


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The shortage of cadaveric livers for transplantation has fueled the recent increase in adult-to-adult liver transplantations in which the right hepatic lobe of a living donor is transplanted into a recipient (13). This procedure is complex and poses risks to both the recipient and the donor. One of the most important challenges is that of managing the biliary ducts during liver lobe resection and reimplantation. Like the hepatic arterial anatomy, the biliary anatomy is quite variable: As many as 24%–57% of individuals have variant biliary patterns (48). Most such cases are from those of right lobe drainage that typically involves anomalous insertion of the right posterior duct (draining segments VI and VII) into the left hepatic duct, common hepatic duct, or common bile duct, among others (4,6).

Consequently, in living adult–to-adult transplantations, biliary anatomy variants are associated with an increased risk of postoperative complications, including biliary leaks and strictures, in both the donor and the recipient (6,8). Although anomalous anatomy is not always a contraindication for liver donation, knowledge of variant anatomy is critical to ensuring the safety of donors and aids in the selection of suitable candidates (2,3,8).

State-of-the-art magnetic resonance (MR) cholangiographic techniques typically involve the use of heavily T2-weighted fast spin-echo sequences, which have been shown to be highly accurate in the identification of biliary abnormalities and variant extrahepatic biliary anatomy that is relevant to laparoscopic cholecystectomy (9). However, the detection and definition of intrahepatic anatomic anomalies, particularly in nondilated systems, are often inadequate (10). Although endoscopic retrograde cholangiopancreatography is an accurate, albeit invasive, alternative imaging technique, its association with quantifiable morbidity makes it difficult to justify the use of this examination for the routine screening of otherwise healthy liver donor candidates (11).

An alternative approach to improving delineation of the biliary anatomy in liver donor candidates has been proposed (1217). Mangafodipir trisodium (Teslascan; Amersham Health, Princeton, NJ), a safe U.S. Food and Drug Administration–approved hepatobiliary MR imaging contrast agent (18), is excreted primarily by way of the biliary system and can be used as a T1-weighted MR imaging biliary contrast agent because of the T1 shortening caused by the manganese metal ion. The use of this agent for the examination of living liver donor candidates, although promising, has been limited to a few small studies (13,15,16). Thus, the purpose of our study was to compare three-dimensional (3D) mangafodipir trisodium–enhanced T1-weighted MR cholangiography with conventional T2-weighted MR cholangiography for the depiction of intrahepatic biliary anatomy in living liver transplant donor candidates.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Study Subjects
Between March 2000 and September 2002, 108 consecutive healthy candidates (mean age, 35.9 years; age range, 18–55 years) for living adult–to-adult right-lobe liver transplantation were referred for routine preoperative clinical evaluation. There were a total of 48 men with a mean age of 35.8 years ± 10.3 (standard deviation) and 60 women with a mean age of 36.1 years ± 8.7. No significant difference in age between the two groups (P = .9, t test) was found. After giving written informed consent, all candidates underwent MR imaging performed at 1.5 T (Vision, Symphony, or Symphony with Quantum gradients; Siemens, Erlangen, Germany) with a torso phased-array coil according to an institutional review board–approved protocol. Both the candidate consent and the protocol approval included permission to perform subsequent analysis of the imaging results.

The donor candidates were instructed to fast for 4 hours before the MR imaging examination. In addition to undergoing MR cholangiography (described in subsequent paragraphs), the subjects underwent routine breath-hold transverse T1-weighted in- and opposed-phase gradient-echo MR imaging, short-tau inversion-recovery turbo spin-echo MR imaging for a fat-suppressed T2-weighted sequence, and 3D spoiled gradient-echo MR imaging before and after administration of a single dose (0.1 mmol per kilogram of body weight) of gadolinium-based contrast agent, gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne NJ), for assessment of the hepatic vasculature and parenchymal disease.

The clinical and imaging findings in all the donor candidates were reviewed at a monthly radiology–transplant surgery conference to assess surgical candidacy. For the subset of 51 candidates who subsequently underwent laparotomy for donor right-lobe hepatectomy, the intraoperative cholangiographic results were used for comparison with the MR cholangiographic findings.

MR Imaging Protocol
Two methods for evaluation of the biliary anatomy were used, and no oral contrast agent was administered. First, before the administration of any contrast material, breath-hold transverse and coronal half-Fourier single-shot turbo spin-echo MR cholangiograms were acquired by using the following parameters: {infty}/62 (repetition time msec/effective echo time msec), 140°–160° refocusing flip angle, 128 x 256 matrix, echo train length of 68, 300–375-mm field of view, 4-mm section thickness, rectangular field of view (depending on body habitus), and 15–20 sections acquired per breath hold. At least three oblique coronal heavily T2-weighted turbo spin-echo acquisitions (2800/1100, 150°–180° flip angle, single shot with echo train length of 240, 240 x 256 matrix, 300–375-mm field of view, and 20–60-mm section thickness with optional rectangular field of view), each within a single breath hold, also were performed.

Second, immediately following the gadolinium-enhanced portion of the MR imaging examination and routine MR cholangiography, a standard dose of mangafodipir trisodium, 5 µmol/kg (0.1 mL/kg, up to a maximum of 15 mL), was administered intravenously by means of slow injection for 1–2 minutes and followed by a 10-mL saline flush. Ten minutes after the injection, transverse and coronal volumetric 3D spoiled gradient-echo imaging of the liver and biliary system was performed by using two volumetric interpolated breath-hold sequences with intermittent fat-suppression pulses: a higher spatial resolution sequence performed coronally with coverage limited to the biliary ducts (6.8/2.3 [repetition time msec/echo time msec], 25°–40° flip angle, 128–256 x 512 matrix, 350–450-mm field of view with use of a rectangular field of view depending on body habitus, and 24 partitions interpolated to 48 sections with ≤1.5-mm thickness) and a lower spatial resolution sequence performed transversely to include the entire liver (4.5/1.9, 25°–40° flip angle, 128–160 x 256 matrix, 300–375-mm field of view with use of a rectangular field of view, and 80–112 interpolated sections with ≤2.0-mm thickness) (19).

To facilitate breath holding during the acquisitions, the imaging time for all sequences was less than 25 seconds. The subjects experienced no serious adverse events. Some did have mild nausea, which is commonly caused by the contrast agent.

Image Interpretation
For analysis, the MR cholangiographic images obtained in each subject were categorized into one of two groups: those obtained with conventional T2-weighted sequences—that is, all half-Fourier single-shot turbo spin-echo and heavily T2-weighted two-dimensional thick-slab images—and those obtained with 3D mangafodipir trisodium enhancement. A total of 216 image sets were obtained. Blinded to the subjects’ identities, two readers (V.S.L. and G.A.K.), each with more than 5 years experience in evaluating liver transplant donor candidates with MR imaging, independently and retrospectively interpreted the image sets in a random order by using a commercially available workstation (Virtuoso; Siemens) that enabled postprocessing with volume-rendered and maximum intensity projection displays in addition to standard viewing of the source images.

The readers had no knowledge of which T2-weighted images corresponded to which mangafodipir trisodium–enhanced 3D T1-weighted images. For each image set, the two readers recorded their interpretation of the biliary anatomy and their degree of confidence on a scale of 1–5, on which 1 meant not confident; 2, mildly confident; 3, moderately confident; 4, highly confident; and 5, completely confident. Differences in interpretation, which were encountered in 24 of the 108 T2-weighted imaging cases and in 19 of the 108 3D mangafodipir trisodium–enhanced imaging cases, were resolved by consensus.

To establish a reference standard for depiction of the biliary anatomy, the images obtained with both MR cholangiographic techniques were reviewed together by both readers. Presented with the matched data sets for a given subject, the readers performed a consensus interpretation of the biliary anatomy.

The biliary anatomy was defined as follows: (a) normal when there was confluence of the right posterior and anterior hepatic ducts to form the right hepatic duct, which joined the left hepatic duct to form the common hepatic duct; (b) having a trifurcation pattern when there was common confluence of the right posterior, right anterior, and left hepatic ducts; (c) having the right posterior duct draining into the left hepatic duct; (d) having the right posterior duct draining into the common hepatic duct; (e) having the right posterior duct draining into the common bile duct; or (f) "other," for which the reader was asked to describe the imaging findings.

Intraoperative Cholangiography
As of this writing, a total of 51 (47%) subjects have undergone laparotomy and 50 have undergone successful liver transplant donation. One subject was considered to have biliary trifurcation at preoperative MR imaging, but intraoperative cholangiography depicted aberrant drainage of the right posterior duct into the left hepatic duct, and, consequently, the right hepatectomy was aborted. Intraoperative cholangiography was performed in all 51 subjects and was used as the reference-standard examination in this subset of candidates. In the cases in which the intraoperative cholangiographic and MR cholangiographic findings were discordant, the MR and intraoperative cholangiographic images were compared side-by-side to assess the causes of the discrepancy.

Statistical Analyses
For the initial analysis, the consensus interpretations (performed by V.S.L. and G.A.K.) of all the MR cholangiographic images were used as the reference standard for overall assessment of the accuracy of each MR cholangiographic technique. The two techniques were compared in terms of the average degree of confidence (ie, mean score) of the two readers by using the Wilcoxon signed rank test. The McNemar test was used to compare the accuracies of the individual MR approaches with that of consensus interpretation of both image sets together. Statistical analyses were performed by using computer software (SAS, version 9; SAS Institute, Cary, NC).

We performed a separate analysis of the data for the subset of 51 subjects who underwent intraoperative cholangiography, which was considered the reference-standard examination. The McNemar test was also used to compare the individual accuracies of the two MR cholangiographic techniques with that of intraoperative cholangiography. P ≤ .05 was considered to indicate statistical significance.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Consensus Interpretation of All MR Cholangiographic Images as Reference Standard
The biliary anatomy was visualized with mangafodipir trisodium–enhanced MR cholangiography in all patients. With the consensus interpretations of all MR cholangiographic images used as the reference standard, a total of 78 (72%) liver donor candidates were considered to have normal biliary anatomy, whereas 30 (28%) were considered to have variants of the biliary anatomy of the right hepatic lobe: 12 (11%) candidates had the right posterior duct draining into the left duct, six (6%) had a trifurcation pattern, and seven (6%) had the right posterior duct draining into the common hepatic duct (n = 4, Fig 1) or common bile duct (n = 3). The remaining five candidates had accessory right and left ducts (n = 2), an aberrant right posterior duct draining into the cystic duct (n = 1), or a low bifurcation of the common hepatic duct (n = 2).



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Figure 1a. Aberrant biliary anatomy in 42-year-old female liver transplant donor candidate. (a) Volume-rendered reconstruction of mangafodipir-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) shows aberrant biliary anatomy, with right posterior duct (arrowhead) draining into common hepatic duct (arrow). (b) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) shows findings similar to those in a but less well delineated. (c) Intraoperative cholangiogram (with catheter in cystic duct) findings confirm aberrant biliary anatomy. Although surgeons at our institution prefer to perform a single duct-to-duct anastomosis in liver transplant recipients, in this case, the pressing need of the recipient for transplantation was believed to be justification for performing choledochojejunostomy to accommodate the two separate biliary ducts draining the right lobe.

 


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Figure 1b. Aberrant biliary anatomy in 42-year-old female liver transplant donor candidate. (a) Volume-rendered reconstruction of mangafodipir-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) shows aberrant biliary anatomy, with right posterior duct (arrowhead) draining into common hepatic duct (arrow). (b) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) shows findings similar to those in a but less well delineated. (c) Intraoperative cholangiogram (with catheter in cystic duct) findings confirm aberrant biliary anatomy. Although surgeons at our institution prefer to perform a single duct-to-duct anastomosis in liver transplant recipients, in this case, the pressing need of the recipient for transplantation was believed to be justification for performing choledochojejunostomy to accommodate the two separate biliary ducts draining the right lobe.

 


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Figure 1c. Aberrant biliary anatomy in 42-year-old female liver transplant donor candidate. (a) Volume-rendered reconstruction of mangafodipir-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) shows aberrant biliary anatomy, with right posterior duct (arrowhead) draining into common hepatic duct (arrow). (b) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) shows findings similar to those in a but less well delineated. (c) Intraoperative cholangiogram (with catheter in cystic duct) findings confirm aberrant biliary anatomy. Although surgeons at our institution prefer to perform a single duct-to-duct anastomosis in liver transplant recipients, in this case, the pressing need of the recipient for transplantation was believed to be justification for performing choledochojejunostomy to accommodate the two separate biliary ducts draining the right lobe.

 
When both MR cholangiographic image sets (conventional T2-weighted and mangafodipir trisodium–enhanced T1-weighted images) were interpreted together as the reference standard, the 3D mangafodipir trisodium–enhanced image findings were in agreement with the reference-standard findings significantly more often (in 107 [99%] of 108 cases) than were the T2-weighted image findings (in 88 [82%] of 108 cases, P < .001). In the 78 cases in which consensus interpretation of all MR cholangiographic images revealed a normal biliary anatomy, the anatomy was considered to be normal according to mangafodipir trisodium–enhanced image findings alone in all 78 cases and according to T2-weighted image findings alone in 73 (94%) of the 78 cases (Fig 2). This difference was statistically significant (P = .036).



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Figure 2a. Intraoperatively proved normal biliary anatomy in 30-year-old male liver transplant donor candidate with conventional T2-weighted MR cholangiographic findings that were interpreted to be abnormal and mangafodipir trisodium-enhanced MR cholangiographic findings that were considered normal. (a, b) Two views of volume-rendered reconstructions of mangafodipir-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) show normal biliary anatomy, with low insertion of the right posterior duct (arrowhead) into the right hepatic duct (arrow). (c) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) interpreted as showing right posterior duct (arrowhead) draining into left hepatic duct (arrow). Intraoperative cholangiographic findings (not shown) confirmed the mangafodipir trisodium-enhanced image findings.

 


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Figure 2b. Intraoperatively proved normal biliary anatomy in 30-year-old male liver transplant donor candidate with conventional T2-weighted MR cholangiographic findings that were interpreted to be abnormal and mangafodipir trisodium-enhanced MR cholangiographic findings that were considered normal. (a, b) Two views of volume-rendered reconstructions of mangafodipir-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) show normal biliary anatomy, with low insertion of the right posterior duct (arrowhead) into the right hepatic duct (arrow). (c) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) interpreted as showing right posterior duct (arrowhead) draining into left hepatic duct (arrow). Intraoperative cholangiographic findings (not shown) confirmed the mangafodipir trisodium-enhanced image findings.

 


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Figure 2c. Intraoperatively proved normal biliary anatomy in 30-year-old male liver transplant donor candidate with conventional T2-weighted MR cholangiographic findings that were interpreted to be abnormal and mangafodipir trisodium-enhanced MR cholangiographic findings that were considered normal. (a, b) Two views of volume-rendered reconstructions of mangafodipir-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) show normal biliary anatomy, with low insertion of the right posterior duct (arrowhead) into the right hepatic duct (arrow). (c) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) interpreted as showing right posterior duct (arrowhead) draining into left hepatic duct (arrow). Intraoperative cholangiographic findings (not shown) confirmed the mangafodipir trisodium-enhanced image findings.

 
In the 30 cases in which consensus interpretation of all MR cholangiographic images revealed a variant biliary anatomy, the mangafodipir trisodium–enhanced images depicted the variant anatomy in a significantly higher (P < .001) percentage of cases (n = 29, 97%) than did the T2-weighted images (n = 15, 50%). Overall, the degree of confidence in defining the biliary anatomy was significantly higher with 3D mangafodipir trisodium–enhanced MR cholangiography than with T2-weighted MR cholangiography (mean confidence score, 4.5 vs 3.4; P < .001).

A total of 29 patients had variants of the right posterior duct at 3D mangafodipir trisodium–enhanced imaging versus 26 with these variants at T2-weighted imaging. There were 21 discrepant cases: An abnormal anatomy was depicted at mangafodipir trisodium–enhanced imaging in nine, at T2-weighted imaging in six, and at both examinations—but with different interpretations of the variant type—in six cases. Review of both image sets together resulted in agreement with the original mangafodipir trisodium–enhanced image interpretation in 20 (95%) of these 21 cases.

In the one case in which the T2-weighted image interpretation was upheld at review of all the MR cholangiographic images, the T2-weighted image findings were predictive of right posterior duct draining into the left duct, whereas the mangafodipir trisodium–enhanced images were interpreted as showing normal anatomy. In this case, the consensus interpretation of both MR image sets together—of the right posterior duct draining into the left duct—was confirmed intraoperatively (Fig 3).



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Figure 3a. Intraoperatively proved variant biliary anatomy in 34-year-old male liver transplant donor candidate with mangafodipir trisodium-enhanced MR cholangiographic findings that were interpreted as normal but conventional T2-weighted MR cholangiographic findings that were considered to show variant anatomy. (a) Volume-rendered reconstruction of mangafodipir trisodium-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) shows relatively poor biliary excretion of the contrast agent and poor visualization of the duct anatomy. Image was interpreted as showing normal biliary anatomy. (b) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) shows right posterior duct (arrowhead) draining into left hepatic duct (arrow). (c) Intraoperative cholangiographic findings confirm the T2-weighted image findings.

 


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Figure 3b. Intraoperatively proved variant biliary anatomy in 34-year-old male liver transplant donor candidate with mangafodipir trisodium-enhanced MR cholangiographic findings that were interpreted as normal but conventional T2-weighted MR cholangiographic findings that were considered to show variant anatomy. (a) Volume-rendered reconstruction of mangafodipir trisodium-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) shows relatively poor biliary excretion of the contrast agent and poor visualization of the duct anatomy. Image was interpreted as showing normal biliary anatomy. (b) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) shows right posterior duct (arrowhead) draining into left hepatic duct (arrow). (c) Intraoperative cholangiographic findings confirm the T2-weighted image findings.

 


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Figure 3c. Intraoperatively proved variant biliary anatomy in 34-year-old male liver transplant donor candidate with mangafodipir trisodium-enhanced MR cholangiographic findings that were interpreted as normal but conventional T2-weighted MR cholangiographic findings that were considered to show variant anatomy. (a) Volume-rendered reconstruction of mangafodipir trisodium-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) shows relatively poor biliary excretion of the contrast agent and poor visualization of the duct anatomy. Image was interpreted as showing normal biliary anatomy. (b) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) shows right posterior duct (arrowhead) draining into left hepatic duct (arrow). (c) Intraoperative cholangiographic findings confirm the T2-weighted image findings.

 
It may be useful to note that there were two cases in which the T2-weighted image findings favored the diagnosis of aberrant right posterior duct draining into the common hepatic duct but the mangafodipir trisodium–enhanced image findings and the combined interpretation favored a low bifurcation of the common hepatic duct. In both cases, the ability to perform 3D reconstructions with the mangafodipir trisodium–enhanced technique enabled readers to determine that the duct arising from the lower region of the common hepatic duct was in fact the main right hepatic duct and not the right posterior duct (Fig 4). At the time of this writing, neither candidate had undergone surgery for donor transplantation.



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Figure 4a. Discrepant biliary anatomy findings in 44-year-old male liver transplant donor candidate. (a, b) Oblique coronal (a) and transverse (b) volume-rendered reconstructions of mangafodipir trisodium-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (4.5/1.9, 25° flip angle) show right-sided duct (arrow) draining the entire right lobe; therefore, the biliary anatomy consists of a low bifurcation of the common hepatic duct. (c) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) interpreted as showing aberrant right posterior duct (arrowhead) draining into common hepatic duct (arrow). The 3D technique used with mangafodipir-enhanced imaging allows the generation of useful reconstructions to localize specific biliary ducts in three dimensions, which is more difficult to accomplish with conventional two-dimensional T2-weighted approaches. At the time of this writing, this subject had not undergone right liver lobe transplant donation, so intraoperative confirmation was not available.

 


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Figure 4b. Discrepant biliary anatomy findings in 44-year-old male liver transplant donor candidate. (a, b) Oblique coronal (a) and transverse (b) volume-rendered reconstructions of mangafodipir trisodium-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (4.5/1.9, 25° flip angle) show right-sided duct (arrow) draining the entire right lobe; therefore, the biliary anatomy consists of a low bifurcation of the common hepatic duct. (c) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) interpreted as showing aberrant right posterior duct (arrowhead) draining into common hepatic duct (arrow). The 3D technique used with mangafodipir-enhanced imaging allows the generation of useful reconstructions to localize specific biliary ducts in three dimensions, which is more difficult to accomplish with conventional two-dimensional T2-weighted approaches. At the time of this writing, this subject had not undergone right liver lobe transplant donation, so intraoperative confirmation was not available.

 


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Figure 4c. Discrepant biliary anatomy findings in 44-year-old male liver transplant donor candidate. (a, b) Oblique coronal (a) and transverse (b) volume-rendered reconstructions of mangafodipir trisodium-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (4.5/1.9, 25° flip angle) show right-sided duct (arrow) draining the entire right lobe; therefore, the biliary anatomy consists of a low bifurcation of the common hepatic duct. (c) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) interpreted as showing aberrant right posterior duct (arrowhead) draining into common hepatic duct (arrow). The 3D technique used with mangafodipir-enhanced imaging allows the generation of useful reconstructions to localize specific biliary ducts in three dimensions, which is more difficult to accomplish with conventional two-dimensional T2-weighted approaches. At the time of this writing, this subject had not undergone right liver lobe transplant donation, so intraoperative confirmation was not available.

 
MR Cholangiography versus Intraoperative Cholangiography
In our series, 51 subjects underwent laparotomy for right hepatectomy, and all of them underwent intraoperative cholangiography. Of the 57 subjects who did not undergo laparotomy, 20 (35%) had biliary anatomy variants—and in some cases, other reasons—that made them unsuitable for liver transplant donation. Compared with interpretation of the intraoperative cholangiographic images as the reference standard, combined interpretation of both MR cholangiographic image sets resulted in an accurate definition of the biliary anatomy in 48 (94%) of the 51 candidates, including all 41 of the subjects with a normal biliary anatomy and seven of 10 with biliary anatomy variants. These results represented an overall sensitivity of 70% and an overall specificity of 100% for the detection of biliary anatomy variants.

When considered separately, mangafodipir trisodium–enhanced T1-weighted MR cholangiography correctly depicted the biliary anatomy in 47 (92%) of the 51 subjects, including all 41 donors with a normal anatomy and six of 10 with variants, for a sensitivity of 60% and a specificity of 100% for the detection of variants. In contrast, conventional T2-weighted MR cholangiography correctly depicted the biliary anatomy in 43 (84%) of the 51 subjects, including 38 of the 41 donors with a normal biliary anatomy and five of the 10 donors with variants, for a sensitivity of 50% and a specificity of 93% for the detection of variants. Mangafodipir trisodium–enhanced imaging was more accurate than T2-weighted imaging in the detection of anatomic variants (P = .14), although differences did not reach statistical significance.

In two subjects, the variant biliary anatomy was not depicted with either MR cholangiographic method. In one case, intraoperative cholangiography depicted a small right posterior duct that drained into the cystic duct and was considered too small to preserve. In the second case, an aberrant right posterior duct drained into the common hepatic duct that was "missed" on all the MR cholangiographic images (Fig 5). In retrospect, both missed ducts could be visualized on the mangafodipir trisodium–enhanced T1-weighted images but not on the T2-weighted images.



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Figure 5a. Intraoperatively proved aberrant biliary anatomy in 27-year-old male liver transplant donor that was missed at preoperative MR imaging. (a) Volume-rendered reconstruction of mangafodipir trisodium-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) shows apparently normal biliary anatomy. (b) Multiplanar reconstruction of mangafodipir-enhanced image in a obtained after that image was compared with the intraoperative cholangiogram shows subtle appearance of right posterior duct (arrowheads) draining into common hepatic duct (arrow); this finding was visible only in retrospect. (c) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) findings also suggest normal anatomy. Even in retrospect, the aberrant right posterior duct was not visible. (d) Intraoperative cholangiogram shows small right posterior duct (arrowheads) draining into common hepatic duct (arrow); this finding was not suspected on the basis of results of preoperative MR imaging evaluation.

 


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Figure 5b. Intraoperatively proved aberrant biliary anatomy in 27-year-old male liver transplant donor that was missed at preoperative MR imaging. (a) Volume-rendered reconstruction of mangafodipir trisodium-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) shows apparently normal biliary anatomy. (b) Multiplanar reconstruction of mangafodipir-enhanced image in a obtained after that image was compared with the intraoperative cholangiogram shows subtle appearance of right posterior duct (arrowheads) draining into common hepatic duct (arrow); this finding was visible only in retrospect. (c) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) findings also suggest normal anatomy. Even in retrospect, the aberrant right posterior duct was not visible. (d) Intraoperative cholangiogram shows small right posterior duct (arrowheads) draining into common hepatic duct (arrow); this finding was not suspected on the basis of results of preoperative MR imaging evaluation.

 


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Figure 5c. Intraoperatively proved aberrant biliary anatomy in 27-year-old male liver transplant donor that was missed at preoperative MR imaging. (a) Volume-rendered reconstruction of mangafodipir trisodium-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) shows apparently normal biliary anatomy. (b) Multiplanar reconstruction of mangafodipir-enhanced image in a obtained after that image was compared with the intraoperative cholangiogram shows subtle appearance of right posterior duct (arrowheads) draining into common hepatic duct (arrow); this finding was visible only in retrospect. (c) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) findings also suggest normal anatomy. Even in retrospect, the aberrant right posterior duct was not visible. (d) Intraoperative cholangiogram shows small right posterior duct (arrowheads) draining into common hepatic duct (arrow); this finding was not suspected on the basis of results of preoperative MR imaging evaluation.

 


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Figure 5d. Intraoperatively proved aberrant biliary anatomy in 27-year-old male liver transplant donor that was missed at preoperative MR imaging. (a) Volume-rendered reconstruction of mangafodipir trisodium-enhanced 3D T1-weighted gradient-echo MR cholangiographic data (6.8/2.3, 25° flip angle) shows apparently normal biliary anatomy. (b) Multiplanar reconstruction of mangafodipir-enhanced image in a obtained after that image was compared with the intraoperative cholangiogram shows subtle appearance of right posterior duct (arrowheads) draining into common hepatic duct (arrow); this finding was visible only in retrospect. (c) Coronal heavily T2-weighted turbo spin-echo MR cholangiogram (2800/1100, 180° flip angle) findings also suggest normal anatomy. Even in retrospect, the aberrant right posterior duct was not visible. (d) Intraoperative cholangiogram shows small right posterior duct (arrowheads) draining into common hepatic duct (arrow); this finding was not suspected on the basis of results of preoperative MR imaging evaluation.

 
In a third case, the surgery was aborted because intraoperative cholangiography depicted aberrant drainage of the right posterior duct into the left hepatic duct. Preoperative interpretation of T2-weighted images concurred with this finding. However, consensus reading of all MR images favored a trifurcation pattern. The distinction between the trifurcation pattern and a low aberrant insertion of the right posterior duct was challenging in this case.

Eight donors who underwent intraoperative cholangiography had discrepant findings at both T2-weighted imaging and mangafodipir trisodium–enhanced imaging. In six of these cases, the intraoperative findings supported the mangafodipir trisodium–enhanced image interpretation: a normal biliary anatomy in three subjects and a variant anatomy in three subjects. In the remaining two cases (discussed earlier), the T2-weighted image interpretations favored a variant biliary anatomy: right posterior duct draining into the left duct, which was confirmed intraoperatively (Fig 3). In one case (Fig 3), this finding was expected and surgery was successful. In the other case, which occurred much earlier, the consensus MR interpretation supported a trifurcation pattern. Because at that time, our surgeons were reluctant to perform right hepatectomies in subjects with an anomalous right posterior duct inserting into the left hepatic duct, surgery was aborted after intraoperative cholangiography was performed (as described above).


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Our study results show that the addition of mangafodipir trisodium–enhanced volumetric MR cholangiography to conventional T2-weighted methods leads to significantly improved identification of biliary anatomic variants, particularly right biliary duct variants, the detection of which can be critical in right-lobe living adult–to-adult liver transplantation.

The use of mangafodipir trisodium–enhanced MR cholangiography to define the biliary anatomy has been reported in three smaller studies (13,15,16), each with a small number (one, eight, and 18) of subjects with intraoperative cholangiographic correlation. In our larger study, our findings confirmed the good results of mangafodipir trisodium–enhanced imaging for the depiction and definition of intrahepatic biliary variants. Of the 51 subjects who underwent intraoperative cholangiography, two had a biliary variant involving small aberrant right posterior ducts that was missed at combined conventional MR cholangiography and mangafodipir trisodium–enhanced MR cholangiography. In retrospect, with knowledge of the intraoperative findings, both variants were visualized on the mangafodipir trisodium–enhanced images, although the findings were subtle.

Our findings of superior definition of the biliary anatomy with use of mangafodipir trisodium enhancement, as compared with the definition that is possible with conventional T2-weighted imaging, support the results of the earlier smaller studies (13,16). The advantages of mangafodipir trisodium–enhanced imaging include higher contrast between the biliary ducts and the background tissue, as compared with the contrast generated at conventional T2-weighted imaging (13,14), and the ability to implement high-spatial-resolution 3D T1-weighted imaging techniques with mangafodipir trisodium enhancement.

The complex orthogonal relationships between the right anterior duct, right posterior duct, left hepatic duct, and common hepatic duct are often difficult to define with confidence on conventional two-dimensional MR images. Use of volume-rendering algorithms for reconstruction of mangafodipir trisodium–enhanced 3D data sets facilitates definition of these relationships for surgical planning. With 3D interpolated sequences, mangafodipir trisodium–enhanced imaging can be performed with a pixel size on the order of 1.0 x 2.0 x 1.5 mm, as compared with a pixel size of 3.0 x 1.5 x 4.0 mm with conventional two-dimensional T2-weighted rapid acquisition with relaxation enhancement imaging. This difference can be critical when, for example, distinguishing between biliary trifurcation (with which single duct-to-duct anastomosis might still be performed in a recipient) and right posterior duct draining into the left hepatic duct (which precludes single duct-to-duct anastomosis) and consequently to appropriate patient selection and surgical planning. In one of our cases, even with use of both MR methods, this distinction could not be made accurately.

Nevertheless, the use of mangafodipir trisodium–enhanced imaging is not without potential disadvantages. This agent is expensive, and with the described use of it, patients become susceptible to the risks associated with exposure to an additional contrast agent. Also, the imaging protocol involves added table time owing to the requirement of a 10–15-minute delay for biliary contrast agent excretion before imaging. Yet, given the limitations of existing T2-weighted MR imaging techniques, and particularly the challenging nature of the combined surgical procedures and the desire to minimize the risks of complications for both the healthy donor and the recipient, we consider the improvements in accuracy and diagnostic confidence well worth the added costs.

Our study had recognized limitations. Although the intraoperative cholangiographic findings were available as the reference standard for biliary anatomy definition for nearly half of the study cohort, for the remaining subjects, we relied on combined T2-weighted MR cholangiography and mangafodipir trisodium–enhanced volumetric T1-weighted MR cholangiography as the reference-standard examination. On the basis of data for the subset of liver donor candidates who did have intraoperative confirmation, we determined that the combination of T2-weighted imaging and mangafodipir trisodium–enhanced volumetric imaging was 94% accurate. However, because variant anatomy frequently precluded the selection of a donor, the intraoperative confirmation of variant biliary anatomy was limited (to 10 subjects). The use of more definitive invasive examinations, such as endoscopic retrograde cholangiography, could not be justified in the subjects who did not undergo surgery because most of these candidates were excluded as donors on the basis of other findings, such as vascular variants or parenchymal abnormalities. Nevertheless, the identification of normal biliary anatomy, which was equally important in this population, was confirmed in all 41 donor candidates who underwent intraoperative cholangiography.

With the described MR cholangiographic protocol, both gadopentetate dimeglumine and mangafodipir trisodium are administered to examine donor candidates for a comprehensive evaluation of the hepatic parenchymal and vascular anatomy (with gadopentetate dimeglumine enhancement) and the biliary anatomy (with mangafodipir trisodium enhancement). Alternative approaches include the use of a single contrast agent, such as a hepatobiliary gadolinium-based MR imaging contrast material, with which dynamic T1-weighted imaging during bolus infusion may be used to evaluate the liver parenchyma and the vascular anatomy and delayed imaging following biliary excretion may be used for cholangiography (20).

Alternatively, one may perform a dual-contrast-agent computed tomographic (CT) evaluation at which conventional contrast materials are used to assess the hepatic parenchyma and vasculature and a separate injection of iopipamide meglumine (Cholografin; Squibb Diagnostics, New Brunswick, NJ) is used to perform CT cholangiography (21,22). Recent developments in MR imaging technology may obviate additional biliary contrast agents. Improvements in T2-weighted techniques, including 3D methods and parallel imaging technologies to increase spatial resolution, remain to be assessed.


    FOOTNOTES
 
Abbreviation: 3D = three dimensional

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, V.S.L.; study concepts and design, V.S.L., G.A.K.; literature research, V.S.L., G.A.K., J.C.L.; clinical studies, V.S.L., G.A.K., G.R.M., L.W.T.; data acquisition, V.S.L., G.A.K., C.A.N., J.S.C., G.R.M., L.W.T.; data analysis/interpretation, V.S.L., G.A.K., J.S.B.; statistical analysis, J.S.B.; manuscript preparation, editing, revision/review, and final version approval, all authors; manuscript definition of intellectual content, V.S.L., G.A.K.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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