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1 Department of Radiology, Beth Israel Deaconess Medical Center and Harvard
Medical School, 330 Brookline Ave., Boston, MA 02215.
2 Present address: Department of Radiology, Lahey Clinic Medical Center, 41 Mall
Rd., Burlington, MA 01805.
3 Institute of Transplantation, Lahey Clinic Medical Center, Burlington, MA
01805.
4 Present address: Russell H. Morgan Department of Radiology and Radiological
Sciences, Johns Hopkins Medical Center, 600 N. Wolfe St., Baltimore, MD
21287.
Received August 20, 2002;
accepted after revision January 20, 2003.
Presented at the annual meeting of the American Roentgen Ray Society,
Seattle, AprilMay 2001.
Abstract
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MATERIALS AND METHODS. We conducted a retrospective study of 107 adult living donor liver transplant candidates. From this pool of candidates, 50 sets of close relatives were selected to undergo transplantation. As part of the preoperative evaluation, all underwent multidetector CT angiography for evaluation of arterial and venous anatomy. Nonionic IV contrast material (180 mL) was given at a rate of 5 mL/sec, and collimations of 1.25 and 2.50 mm were used for true arterial and portal hepatic venous phase scanning, respectively. Image processing included three-dimensional volume renderings and multiplanar reformations. Two radiologists assessed the prevalence of vascular variants that were important for surgical planning and execution.
RESULTS. We identified surgically important hepatic vascular variants in 70 (65%) of the 107 patients. A total of 129 variants were identified, of which 27 were important surgical considerations for recipients, 37 were important for donors, and 65 were important for both recipients (19 variants) and donors (46 variants). Of the 50 pairs of close relatives, 10 (20%) of the pairs were found to have the same hepatic vascular variant or one that was similar. However, when the pairs were set randomly, with no genetically related pairs included, similar variants were noted in 11 pairs (22%). The most common hepatic arterial variant in all candidates was an accessory right or left hepatic artery. The most common hepatic venous variant was an accessory right inferior hepatic vein.
CONCLUSION. We observed a high prevalence of surgically important vascular variants in living adult candidates for living liver transplant donation and receipt. Because of the frequent occurrence, similar variants are to be expected among these sets of patients, regardless of whether they are closely related.
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Multidetector CT (MDCT) angiography or MR angiography is being used to noninvasively evaluate the liver and its vascular anatomy [4, 10, 11]. MDCT angiography is useful for evaluation of the vascular anatomy, liver parenchyma, and other intraabdominal disease or abnormality, thus replacing the many imaging studies once needed to obtain that information.
In addition, the optimal volume of liver to give to the recipient and the amount of tissue in the left lobe needed to sustain the donor (not < 30% of the original amount) can be determined accurately with this method [12, 13]. On occasion, this balance can be delicate, and consideration of intrahepatic vascular variants may be important to surgical planning and execution. The level of importance varies depending on whether the variants appear in the donor or the recipient. For example, a replaced or accessory left hepatic artery is important in a recipient because during native liver removal, that artery has to be ligated at its origin from the left gastric artery. However, this variant is not important if present in a donor because the left lobe is not removed. Conversely, a variant origin of the artery to the medial segment of the left hepatic lobe (segment IV) is important in the donor because the hepatectomy line would cross the arterial supply of this segment; the variant is not important in the recipient because the whole native liver is resected. Some variants, such as a replaced right hepatic artery from the superior mesenteric artery, are important in both donor and recipient because extra steps are required for both removal and reimplantation of the liver tissue.
Many vascular liver variants have been described [2, 4, 10, 11], but their importance in surgical planning of adult living donor transplantation has not been studied systematically. In addition, living donor transplantation candidates are usually chosen from among close relatives, but the similarity of vascular variants among the candidate pairs is not known. Although the surgical importance of vascular variants differs for donors and recipients, the presence of a certain type of vascular variant should prompt one to look more closely for similar or additional variants in genetically related candidates.
During surgical planning conferences for transplantation or posttransplantation assessments, we noticed that many of the variants considered important seemed to be similar in donorrecipient pairs. The purpose of our study was to determine the frequency with which surgically important hepatic vascular variants occur independently and among genetically related adult donor and recipient liver transplantation candidates. We also calculated the frequency of occurrence among randomly paired candidates.
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A four-channel MDCT scanner (LightSpeed, General Electric Medical Systems, Milwaukee, WI) was used. The separate CT protocols used for donors and recipients were similar to those described in previously published reports [4, 10, 13]. These scanning techniques evolved as we gained experience. The latest technique involves using milk as oral contrast material unless the patient has lactose intolerance, in which case water is used as an oral contrast medium [14]. Unenhanced CT scans of the liver (including the spleen) are acquired, and in a single slice, dual-energy CT scans are acquired at 80 and 140 kVp to evaluate for fatty infiltration of the liver [15]. Arterial injection timing is determined with a test injection of contrast agent, the amount of which is three times the injection rate to be used for CT angiography. Timedensity curves are taken from the aorta at the level of celiac artery. The peak enhancement plus 2 sec is deemed to be the beginning of the hepatic arterial phase. For multiphase CT, 180 mL of nonionic contrast is administered at a rate of 5 or 6 mL/sec (equal to the rate of the test injection). Arterial phase imaging is performed with 1.25-mm collimation, 0.5-sec gantry rotation, and 7.5-mm table feed per gantry rotation. The 1.25-mm collimation is considered crucial for displaying intrahepatic artery detail.
For the donors, portal hepatic venous phase scanning is initiated 45 sec after the start of the arterial phase. In this phase, 2.5-mm collimation is used with 15-mm table feed per gantry rotation. The recipients are scanned 20 sec after the start of the arterial phase, during the late arterialearly portal venous phase, and during the portal hepatic venous phases beginning 20 sec after the start of the previous sequence. The late arterialearly portal venous phase is used to enhance detection and characterization of hepatocellular carcinoma [16]. For this phase, 3.75- or 5-mm collimation is used. Both donor and recipient candidates also undergo 180-sec delayed CT of the abdomen and pelvis (using 7-mm collimation) for further evaluation of the abdomen and for detection and characterization of liver abnormalities [17].
In all patients in our study, axial CT scans were reconstructed using a standard algorithm. Postprocessing was performed on a commercially available workstation. Maximum intensity projections and three-dimensional surface- or volume-rendered images of the major vessels were generated. All images were reconstructed at 1.25 x 0.7 mm for the arterial and at 2.5 x 1.25 mm for the venous phases. All images, including two-dimensional reformations and three-dimensional reconstructed models, were sent to PACS (picture archiving and communication system) workstations.
Two radiologists retrospectively reviewed the CT scans acquired in potential donors or recipients on PACS workstations. Both axial scans and the processed data were analyzed. Using the three-dimensional models and two-dimensional reformations, the radiologists evaluated the anatomy of hepatic arteries, hepatic veins, and portal veins. Before undertaking the review, they defined what would be considered classic vascular anatomy for arteries and veins: For the arteries, the common hepatic artery arises from the celiac axis and branches into the gastroduodenal artery and proper hepatic artery. The latter gives rise to the left hepatic artery (for the lateral segments of the left lobe) and shortly thereafter gives rise to the middle hepatic artery (for the medial segment of the left lobe, segment IV). The artery continues as the right hepatic artery, which branches to the anterior and posterior branches at a variable distance. The portal vein branches at the liver hilum into the left and right portal veins. The right vein bifurcates to the anterior and posterior right portal veins at a variable distance. There are three main hepatic veins: right, middle, and left. The hepatectomy plane is largely determined by the hepatic vein drainage of the liver. Classically, the drainage runs to the right of the middle hepatic vein from its juncture with the inferior vena cava superiorly and to the gallbladder fossa inferiorly.
Although multiple hepatic vascular variants exist, only those that had any bearing on surgical management were considered in our study (Table 1). Important variants were determined to be those that were frequently discussed during the surgical planning conferences of our transplantation team or the postsurgical assessments. These included arterial variants such as replaced or aberrant right and left hepatic arteries or a hepatic artery branch supplying segment IV. For hepatic venous variants, we analyzed the pattern of venous drainage into the inferior vena cava (the number of main veins or early branching) and around the hemihepatectomy plane. We noted the hepatic venous branches draining segments VIII and V (right superior anterior and right inferior anterior), which may drain into the middle hepatic vein. In addition, we noted the drainage of segment VI (right inferior posterior) that may drain directly into the inferior vena cava. Portal vein branching also has an impact on surgical management, the most important aspect being the distance between the bifurcation of the left portal vein and the bifurcation of the right portal vein.
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The occurrence of surgically important vascular variants and the standard error of proportion were calculated. In addition, the occurrence of the same type of surgically important vascular variants and the standard error of proportion were calculated for the 50 donorrecipient pairs. The sets of genetically related donors and recipients were then unmatched, and new donorrecipient candidate pairs were randomly set to determine whether the prevalence of surgically important vascular variants was different between related and unrelated candidates. The seven donor candidates who ultimately did not participate in the transplantation procedure were not included in the pairs comparison.
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Numerous hepatic arterial branching patterns and anatomic variations were found. We identified a replaced or accessory left hepatic artery from left gastric artery, replaced or accessory right hepatic artery from the superior mesenteric artery, artery supplying segment IV of the liver arising from the right hepatic artery, and variations in the branching of the celiac artery. The most common hepatic artery variants were an accessory (n = 10) or replaced (n = 11) left hepatic artery from the left gastric artery and an accessory (n = 10) or replaced (n = 5) right hepatic artery from the superior mesenteric artery (Figs. 1 and 2). A surgically important middle hepatic artery supplying segment IV from right hepatic artery was noted in five patients (9% ± 3.7% of the 57 donors or 4% ± 1.7% of the 129 important variants). This variant has a marked impact on the surgical procedure and selection criteria of the donor (Fig. 3). Other surgically important arterial variants included a separate origin of the hepatic artery from the aorta; origin of the right or left hepatic artery from common hepatic artery occurring before the origin of the gastroduodenal artery; trifurcation of the common hepatic artery to the gastroduodenal and to the right and left hepatic arteries; short right hepatic artery; and origin of the left hepatic artery from the celiac axis.
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The most common hepatic venous variant noted was an accessory inferior right hepatic vein, which was seen in 33 (47% ± 5.2%) of 70 patients with important vascular variants (Fig. 4). Although most of the patients had a single accessory inferior right hepatic vein, four had two accessory veins. This variant was seen in both donors and recipients. However, it is surgically more important in the evaluation of donors; 26 (79% ± 7.1%) of the 33 accessory inferior right hepatic veins were found in donors. Our liver transplantation surgeons consider the size of the accessory vein and the distance of the drainage site from the main hepatic venous drainage site along the inferior vena cava to be important information. The second surgically important hepatic venous variant is the branch draining the right superior anterior segment (segment VIII) to the middle hepatic vein (Fig. 5). Although this variant is not commonfound in only six (9% ± 3.3%) of our 70 patients with important variantsit has important implications. The transplantation surgeon must be aware of the presence of the anomaly because the segment VIII venous branch may have to be implanted in the recipient. Other important variations were branching of the middle hepatic vein, which affects the location of the hepatectomy plane. Several large branches of the middle hepatic vein that are draining important segments of the liver present a challenge that should be addressed [18]. Other surgically important venous variants included dominant drainage of segments V (right inferior anterior) and VII (right superior posterior) to middle hepatic vein, which we found in two donor candidates.
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Portal vein variants were seen in 26 (37% ± 5.8%) of 70 patients with important vascular variations. Trifurcation of the portal vein was the most common variation, present in 13 (19% ± 4.6%) of the patients with variants. An accessory right posterior portal vein arising from the main portal vein was seen in nine (13% ± 4%) of the 70 patients with variants (Figs. 6 and 7). Other portal vein variants included a short main or right portal vein in two recipients and right superior segment branches originating from the left portal vein in two donors.
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The same vascular variant was seen in 10 (20% ± 5.7%) of the matched 50 pairs. The most common variant noted in both relatives of the donorrecipient pairs was an accessory inferior right hepatic vein, seen in five pairs. Three other pairs also had the same variant (replaced left hepatic artery and replaced or accessory right hepatic artery). The same portal vein variants were seen in two of the 50 pairs of relatives. When the donorrecipient pairs of the 100 patients were rearranged to exclude relative matching, the same vascular variant was seen in 11 (22% ± 5.9%) of the 50 pairs of unrelated individuals, a similar number to that found in the sets of relatives.
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Classic vascular anatomy serves as a guide to understanding the vascular supply and drainage patterns. Multiple vascular variants exist, but their importance varies. In our selected patients, the classic vascular anatomy was seen in only 35% of the 107 patients. Most (65%) of the recipients and donors had some form of anatomic vascular variant detected on the MDCT angiography. In addition to axial CT data, maximum intensity projections and volume renderings were presented to the transplantation surgeon in a form similar to that of an angiogram. Interactive workstations and PACS further aided in the assessment of liver anatomy and planning for the transplantation.
Knowledge of the hepatic venous anatomy is essential to the transplantation surgeon. The anatomy of middle hepatic vein is critically important because the hepatectomy plane in living donors courses approximately 1 cm to the right of the vein. Large veins draining into the middle hepatic vein from the adjacent segments of the right lobe (segments VVIII) could alter the hepatectomy plane or require a change in surgical planning. In such a case, the vessels would have to be reanastomosed in the recipient; otherwise, the transplanted right lobe of the liver could become congested, potentially leading to organ rejection. Thus, the drainage pattern of the middle hepatic vein must be thoroughly evaluated.
Another important hepatic venous variant is an accessory or replaced inferior right hepatic vein. This variant was the most common in our patients and is important in both donors and recipients, but more so in the donor. Before transplantation, the size of the vein must be determined as well as the distance between the main right hepatic vein (at the confluence of the hepatic vein with the inferior vena cava) and the drainage site of the inferior right hepatic vein into the inferior vena cava. The size of the accessory inferior right hepatic vein is important because it can affect the surgical approach. If the cross-sectional diameter is greater than 5 mm, the vessel has to be preserved and reanastomosed in the recipient's inferior vena cava; otherwise, it can result in a congested graft and lead to organ rejection [18, 19].
The portal vein anatomy is also crucial, although its variants were noted less frequently. In our patients, portal vein variants constituted 20% of important variants. The most common was trifurcation of the main portal vein (10% of the total important variants). The branching pattern of the left and right portal veins from the main portal vein is important for surgical planning. In trifurcation, the left portal vein and the anterior and posterior branches of right portal vein branch at the same location, creating a surgical problem because there is no segment of the portal vein onto which a clamp can be placed. The portal vein supply of segment VII (superior posterior) of the right lobe should also be evaluated. In most patients, the dorsal branches of segment VII supply the dorsalcranial area of the right lobe posterior relative to the right hepatic vein. The medial branches of segment VII arising near the porta hepatis are important in preoperative evaluation of tumors, but their importance in living donor liver transplantation in adults has not been shown [20]. In our study, we did not encounter anomalies in the segment VII or segment IV portal vein supply. The portal venules to segment IV have been shown to be important for collateral pathways, and knowledge of this anatomy has been found to have clinical importance [21].
Hepatic arterial vascular variants were seen in 49% of our patients, a finding similar to 45% reported in other studies [22, 23]. An important hepatic arterial variant is the supply to segment IV from the right hepatic artery. This variant affects a donor who requires a full arterial supply to the left lobe of the liver. Although Kostelic et al. [23] believe that 50% of the anomalous hepatic arterial configurations are technically incompatible or have potentially adverse effects on the outcome of the surgery; our liver transplantation team rarely excludes patients with such variants from being donors. However, knowledge of these variants is vital to the transplantation surgeon. Although certain variants are more crucial than others because they may produce different technical difficulties or challenges, all of the variants noted on CT are discussed with the surgeon.
We found the same or a similar vascular variant to be present in at least 10 of 50 pairs of genetically related candidates. However, the same or a similar variant was also seen in 11 of 50 unrelated donorrecipient pairs. The high incidence of variants likely accounts for their simultaneous occurrence in the pairs. Thus, if a vascular variant is noted in a recipient or a donor, it is sensible to thoroughly examine the other partner in the pair for a similar variant. The most common variant noted in related and unrelated pairs was an accessory inferior right hepatic vein.
In summary, MDCT angiography provides a complete evaluation of the liver as well as the hepatic vascular anatomy in adult living donor liver transplantation candidates. The occurrence of the conventional classic vascular anatomy is uncommon, and some form of important hepatic vascular variation is to be expected in most candidates. MDCT scans as well as maximum intensity projections and three-dimensional volume renderings accurately depict the vascular anatomy in a form that is helpful to the transplantation surgeon. Any of the noted vascular variants should be discussed with the liver transplantation team. Rarely are candidates excluded because of vascular anatomy, but the surgeon frequently alters surgical plans on the basis of CT data.
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