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Original Research |
1 Department of Medical Imaging, Princess Margaret Hospital, University Health
Network, University of Toronto, 610 University Ave., Toronto, ON M5G 2M9,
Canada.
2 MultiOrgan Transplantation Unit, Department of Surgery, University Health
Network, Toronto General Hospital, University of Toronto, ON, Canada.
3 Department of Biostatistics, University Health Network, Princess Margaret
Hospital, Toronto, ON, Canada.
Received July 13, 2004;
accepted after revision September 30, 2004.
Presented at 2004 annual meeting of the American Roentgen Ray Society,
Miami Beach, FL.
Abstract
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MATERIALS AND METHODS. Two radiologists independently reviewed preoperative hepatic CT scans and intraoperative cholangiograms from 39 consecutive living liver donors. The portal venous and hepatic arterial anatomy was classified on the basis of the preoperative CT scans and the biliary anatomy was classified on the basis the intraoperative cholangiograms into one of two groups: conventional or anomalous. Variables were tested for association using Fisher's exact test.
RESULTS. Anomalous vascular branching variants were common, being present in 23 (59%) of 39 patients. Hepatic arterial anomalies were present in 18 (46%); portal venous anomalies, in seven (18%); and both, in two (5%). Biliary anomalies were present in 15 (38%) of the 39 patients. Of the 23 patients with anomalous vascular anatomy, seven (30%) had biliary anomalies. Of the 16 patients with conventional vascular anatomy, eight (50%) had biliary anomalies. There was no significant association between hepatic arterial anomalies, portal venous anomalies, or the combination of arterial and portal venous anomalies and anomalous biliary drainage.
CONCLUSION. Portal venous and hepatic arterial branching patterns do not correlate well with biliary anatomic variants. In patients with normal hepatic vascular anatomy, biliary anomalies are common.
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On the basis of the anatomic relationship of the portal veins, hepatic arterial branches, and biliary radicals in the intrahepatic portal triad, one might postulate that there may be an association between the presence of anomalous vascular and biliary branching patterns. If such an association existed, it could help in accurately diagnosing biliary variants missed preoperatively with MRCP or CT cholangiography. The purpose of this study was to determine whether there is an association between portal venous or hepatic arterial branching patterns (or a combination of both) and biliary anatomic variants.
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A chart review and review of the operative reports were performed in the 140 patients considered for potential living related donor liver transplantation in the same time period. Of the 101 patients who were not used as donors, one patient was excluded from transplantation on the basis of vascular supply (variant portal vein: early branch to segments VI and VII determined by CT), and this patient did not have variant biliary branching as determined from mangafodipir trisodium-enhanced MRCP. The remaining patients were excluded as living related donor candidates on the basis of serology, ABO group, medical comorbidity, or another preferred donor. Others had not yet been called on to donate.
All 39 liver donors underwent preoperative CT and intraoperative cholangiography. All CT examinations were performed using a 4- or 8-row multidetector helical CT scanner (LightSpeed QX/i or LightSpeed Ultra, GE Healthcare) with 290-330 mA (arterial phase) and 200-260 mA (portal venous phase) at 0.8-sec table speed to obtain slice collimations of 2.5 mm (arterial phase) and 5 mm (portal venous phase) with 50% reconstruction overlap through the abdomen. Either iohexol (Omnipaque 300, Amersham Health) or iodixanol (Visipaque 270, Amersham Health) was injected IV at a dose of 2 mL/kg (maximum, 150 mL) and a rate of 4-5 mL/sec. Arterial phase scanning was initiated using bolus triggering over the abdominal aorta with a threshold of 30 H. Portal venous phase scanning was initiated 60 sec after injection.
Intraoperative cholangiography was used as the reference standard for determining the biliary branching pattern. After open cholecystectomy, the cystic duct was cannulated. Approximately 10-20 mL of iohexol was hand-injected with fluoroscopic guidance. Anteroposterior views were obtained using a fluoroscopic C-arm system (OEC 9800, GE Healthcare) at different time points during contrast injection to optimally visualize the biliary branching pattern. Supplemental right anterior oblique and left anterior oblique projections were obtained if deemed necessary by the surgeon.
The preoperative hepatic CT scans and intraoperative cholangiograms were loaded on an off-line DICOM viewer (Merge, eFilm) without the patient-identifying data. One radiologist specializing in abdominal imaging reviewed the CT scans, and another abdominal radiologist independently reviewed the intraoperative cholangiograms. The portal venous and hepatic arterial supplies were classified from the preoperative CT scans and the biliary anatomy from the intraoperative cholangiograms into one of two categories: conventional or anomalous. Any branching pattern that was not conventional was considered anomalous (Figs. 1, 2, 3). The portal venous, arterial, and biliary branching patterns were further classified using previously published classification schemes [13-15]. Multiplanar reconstructions of CT images were used to help define vascular branching patterns.
The CT reviewer measured the length of the right portal vein. This was defined as the distance from the right wall of the left portal vein at the main portal vein bifurcation to the bifurcation of the right portal vein. Oblique multiplanar reconstructions were used when necessary to measure the length accurately.
Variables were tested for association using Fisher's exact test. Contingency coefficients were calculated to quantify the level of association. A p value of less than 0.05 was considered significant. Exact 95% confidence intervals (CIs) were calculated for proportions using the binomial distribution. A t test was used to compare the length of the right portal vein in patients with biliary anomalies with that of patients without anomalies.
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All biliary variants and portal vein variants required modifications in the surgical technique: multiple biliary anastomoses and biliary enterostomies or multiple portal vein anastomoses to the recipient structures. Hepatic arterial variants did not require modification of the surgical approach in 17 of the 18 cases. One case required dual hepatic arterial anastomoses to accommodate an accessory right hepatic artery.
There was no significant association between hepatic arterial anomalies, portal venous anomalies, or the combination of arterial and portal venous anomalies and anomalous biliary drainage (contingency coefficient, 0.20 [95% CI, -0.10 to 0.51]; contingency coefficient, 0.04 [95% CI, -0.28 to 0.36]; contingency coefficient, 0.20 [95% CI, -0.11 to 0.51], respectively).
The mean length of the right portal vein was shorter in patients with normal biliary branching patterns (0.82 vs 1.25 cm) (Fig. 4). However, this difference did not reach statistical significance (p = 0.09). Four patients had a right portal vein that was 2 cm or longer; none of these patients had a biliary branching anomaly.
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The factors that determine the branching patterns of the extrahepatic bile duct during embryologic development are poorly understood. The extrahepatic bile duct, comprising the common hepatic duct and common bile duct, is a well-formed structure by the fifth week of gestation and develops from an elongation of the hepatic diverticulum. The extrahepatic bile duct is attached to the liver proximally. During the fifth week of gestation, the endoderm of the extrahepatic bile duct proliferates and is molded by the surrounding parenchyma to form ductal branches that connect to the liver.
The intrahepatic bile ducts develop differently and at a later time. They originate from the ductal plate, which is observed at the sixth to seventh week of gestation. The ductal plate remodels during the eleventh week of gestation and progresses to the periphery of the liver while remaining in contact with the extrahepatic bile duct. Proliferation of the surrounding mesenchyme is suspected to play an important role in the remodeling process; however, the triggers and determining factors for the remodeling process remain unknown [17].
The hypothesis that vascular and biliary branching patterns are correlated is based on a proposed embryologic pathway where biliary and hepatic arterial development occur along the established architecture of the portal vein. It has been established that bile ducts and hepatic arteries differentiate embryologically after the portal veins. Based on the anatomic and developmental proximity of these structures, one might expect an association between the branching patterns of the vascular and biliary systems. However, to our knowledge, an association of biliary and vascular variations has not been previously reported.
In this study, there was no statistically significant association between portal venous anomalies and biliary anomalies; hepatic arterial anomalies and biliary anomalies; or the presence of any arterial or portal venous anomaly and biliary anomaly. The upper limits of the 95% CIs on the contingency coefficients were not more than 0.51; these findings suggest that the likelihood of a strong association is small. It is possible that an association exists between a particular subtype of vascular anomaly and a particular subtype of biliary anomaly; however, our sample size does not allow us to determine to what degree such an association exists, if any.
From a clinical perspective, it is important to note that 12 of 32 patients with normal portal venous anatomy had biliary anomalies and that three of seven patients with portal venous anomalies had coexistent biliary anomalies. Therefore, portal venous branching patterns have poor predictive values for anomalous biliary branching.
One limitation of this study is the potential for selection bias. Patients who were living related donor liver transplantation candidates but who did not undergo surgery were excluded from our study group. This was necessary because our standard of reference for biliary anatomy was intraoperative cholangiography. MRCP has a reported accuracy of 81-84% for delineating biliary anatomy [4, 18]. Thus, MRCP is insufficient as a gold standard because 16-19% of variants may be incorrectly reported. Although the accuracy can be further increased with the use of contrast agents such as mangafodipir trisodium excreted through the biliary system [7-9], this agent is not readily available in North America, and intraoperative cholangiography or other forms of direct cholangiography such as endoscopic retrograde cholangiography remain the gold standard.
Because of selection bias, one might expect the incidence of biliary or vascular anomalies in the excluded group to have been higher than in the population who underwent surgery; thus, it is possible that our population is composed of patients with a lower prevalence of biliary and vascular anomalies. However, the prevalence of anomalies in this study was similar to that reported in prior large series [13, 15, 19]. In addition, a chart review of the 101 patients who were excluded from donation revealed that only one patient was excluded because of an anatomic anomaly. In this patient, there was a portal venous anomaly with a normal biliary branching pattern. Thus, it is likely that bias was limited in our study population.
The right portal vein was longer in patients with normal biliary branching patterns, but this difference was not statistically significant. However, no patient with a right portal vein that was 2 cm or longer had a biliary branching anomaly in this study. Further evaluation with a larger series would be required to determine if a 2-cm cutoff value would be a good predictor of a normal biliary branching pattern. If this were the case, then this could be valuable in cases for which MRCP was not of diagnostic quality or was difficult to interpret [4].
In conclusion, portal venous and hepatic arterial branching patterns do not correlate well with the presence of anomalous biliary drainage. In patients with normal hepatic vascular anatomy, biliary anomalies are common. Therefore, biliary anomalies cannot be predicted reliably from knowledge of hepatic vascular branching patterns.
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