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AJR 2004; 183:1065-1070
© American Roentgen Ray Society


Hepatobiliary Imaging

Peripheral Anatomic Evaluation Using 3D CT Hepatic Venography in Donors: Significance of Peripheral Venous Visualization in Living-Donor Liver Transplantation

Yuya Onodera1, Tokuhiko Omatsu1, Jun Nakayama1, Toshiya Kamiyama2, Hiroyuki Furukawa3, Satoru Todo2, Takeshi Nishioka1 and Kazuo Miyasaka1

1 Department of Radiology, Hokkaido University Graduate School of Medicine, North 15 West 7, Kita-Ku, Sapporo 060-8638, Japan.
2 First Department of Surgery, Hokkaido University Graduate School of Medicine, Sapporo, Japan.
3 Department of Organ Transplantation and Regenerative Medicine, Hokkaido University Graduate School of Medicine, Sapporo, Japan.

Received February 23, 2004; accepted after revision April 15, 2004.

 
Address correspondence to Y. Onodera (yono{at}radi.med.hokudai.ac.jp).


Abstract
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. The purpose of this study was to determine clinical roles for 3D CT hepatic venography in the evaluation of peripheral hepatic venous anatomy during living-donor liver transplantation.

MATERIALS AND METHODS. Subjects comprised 54 donors (age range, 20–60 years) who had undergone surgery to donate a liver for transplantation. Visualization of each hepatic venous branch and total visualization using 3D CT hepatic venography were evaluated. Maximum venous branch order visualized was graded as nil, first branch, second branch, or third branch or more. The distance between the hepatic surface and the tip of each hepatic venous branch was classified as 0–5 mm, 6–10 mm, 11–15 mm, 16–20 mm, or 21–25 mm. Quality of total 3D CT hepatic venography was evaluated subjectively as poor, good, fair, or excellent. Dominance of large hepatic veins in the right lobe, peripheral branching pattern of the middle hepatic vein, and branching pattern of the vein draining segment IVb were also assessed.

RESULTS. Most hepatic venous branches (96.2% [275/286]) were visualized up to at least the second-order branches, and 93.7% (268/286) of branches were within 10 mm of the hepatic surface. As for total visualization, 98% (53/54) of cases were regarded as excellent. The dominant vein in the right lobe was the right hepatic vein in 27 cases, inferior hepatic vein in 25, and middle hepatic vein in one. The branching pattern of the middle hepatic vein was type 1 in 36 cases, type 2 in nine, and type 3 in eight. Segment IVb vein branched from the middle hepatic vein in 20 patients, and from the left hepatic vein in 34.

CONCLUSION. Because 3D CT hepatic venography visualizes peripheral hepatic venous branches in detail, the technique is useful for determining operative indications in living-donor liver transplantation.


Introduction
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The number of living-donor liver transplantations has been increasing because cadaveric livers are not readily available [1, 2]. In adult living-donor liver transplantation, preoperative evaluation of hepatic venous anatomy is crucial for reducing surgical complications. Hepatic resection is typically performed in a plane parallel to the middle hepatic vein. The hepatic venous system can display a number of anatomic variations [3], and surgical procedures without prior knowledge of the venous anatomy can lead to serious consequences. At some institutions, the procedure is performed without clamping the portal vein to keep postoperative graft function [4], increasing the risk of hemorrhage. Our experience with living-donor liver transplantation suggests that postoperative venous congestion can occur unexpectedly in regions covered by the thin branch of the middle hepatic vein, especially in the dorsal site of the anterior sector. In patients with a hepatic venous branch covering a wide drainage area, venous reconstruction is needed to prevent postoperative liver dysfunction, even if the branch is thin. Detailed preoperative evaluation for peripheral hepatic venous anatomy is necessary.

Two-dimensional imaging techniques such as CT, MRI, and sonography have been used to evaluate the hepatic venous system, but each technique has particular limitations [57]. Since the development of MDCT, recent 3D CT studies have suggested that 3D depiction is more useful than 2D imaging in understanding complicated branching anatomies [8]. Just as important, 3D hepatic venography on CT has now become clinically feasible [920]. Imaging of hepatic veins in 3D represents an attractive, noninvasive preoperative examination in living-donor liver transplantation. However, to the best of our knowledge, studies of 3D imaging focusing on peripheral hepatic veins are scarce, and the quality of 3D images of this complicated branching system has been unclear [10]. Our study investigated the abilities and limitations of 3D CT hepatic venography.


Materials and Methods
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Data Acquisition
Subjects comprised 54 consecutive donors who were examined with MDCT for living-donor liver transplantation between April 2001 and September 2003. All CT scans were obtained using a 4-MDCT scanner (Aquilion, Toshiba). Scanning conditions were as follows: slice collimation, 2 mm x 4 detectors; helical pitch, 6; 200 kVp; 400–500 mA. All data sets acquired by helical scanning were reconstructed to isotropic voxel data sets. Reconstructed data were transferred to a 3D workstation (Virtual Place, Medical Imaging Laboratory). Either 100 mL of Iopamiron 370 (iopamidol, Schering) or 150 mL of Omnipaque 300 (iohexol, Amersham) was injected as contrast medium through the right antecubital vein at a flow rate of 3.5–5.0 mL/sec with a 40-mL saline flush. Data acquisition for 3D CT hepatic venography started 70 sec after injection of contrast medium [4, 1315], and 3D CT hepatic venography was reconstructed using maximum intensity projection or volume rendering. Three-dimensional objects were made by radiographic technologists on 3D workstations. Bones such as ribs and vertebrae that prevented image interpretation were removed from maximum-intensity-projection and volume-rendered objects. Volume-rendered objects were optimized using a presetting to depict hepatic venous branches on a 3D workstation. Unnecessary opacities were removed manually or automatically.

Data Analysis
Image interpretation was performed on a 3D workstation independently by three board-certified radiologists. Data for analysis were made by consensus. Couinaud [21] and Bismuth [22] classifications were used for determining hepatic venous anatomy. The branching pattern of peripheral hepatic veins was evaluated for the right inferior hepatic vein and veins draining segments IVa, IVb, V, and VIII. On 3D hepatic venography, 286 hepatic venous branches (veins in segments VIII, V, IV, etc.) were recognized by the three radiologists in a proximal–distal direction, and maximum branch order visualized was reported. Branch order was classified as "nil," "first order," "second order," or "third order or more." Distance between the liver surface and the most peripheral point of veins was measured and categorized as follows: 0–5 mm, 6–10 mm, 11–15 mm, 16–20 mm, and 21 mm or more. Spearman's rank correlation was used to determine relationships between branch order and distance from the hepatic surface. A p value less than 0.05 was considered statistically significant. Quality of total 3D CT hepatic venography was classified as poor, fair, good, or excellent. When no hepatic vein was visualized, quality was defined as poor. Visualization up to a first branch order was defined as fair; to a second branch order, as good; and to a third branch order or more, as excellent. Correlations between 3D CT hepatic venography and three anatomic classifications [2325] were analyzed. The first classification was Nakamura and Tsuzuki's classification [24], with a dominant hepatic vein in the right lobe and venous drainage from the right hepatic vein, inferior hepatic vein, and middle hepatic vein (Figs. 1A, 1B, 1C, and 1D). The second was the classification of Marcos et al. [23] of a peripheral venous branching pattern for the middle hepatic vein (Figs. 2A, 2B, and 2C). The third was the classification of Kawasaki et al. [25] of segment IVb vein arising from the middle hepatic vein or left hepatic vein (Figs. 3A and 3B).



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Fig. 1A. Nakamura and Tsuzuki's classification [24]. Volume-rendered reconstructions show hepatic venous drainage pattern at right liver lobe. Pattern is classified according to dominant development among right hepatic vein (RHV), inferior right hepatic vein (IHV), and middle hepatic vein (MHV). LHV = left hepatic vein. In type 1 (n = 27, 50.9%), right hepatic vein is large and drains lateral sector and dorsal or lateral part of paramedian sector. Middle hepatic vein drains ventral or medial part of paramedian sector.

 


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Fig. 1B. Nakamura and Tsuzuki's classification [24]. Volume-rendered reconstructions show hepatic venous drainage pattern at right liver lobe. Pattern is classified according to dominant development among right hepatic vein (RHV), inferior right hepatic vein (IHV), and middle hepatic vein (MHV). LHV = left hepatic vein. In type 2 (n = 25, 47.1%), right hepatic vein is of medium size and thick, and some inferior hepatic veins are present. Inferior hepatic veins drain inferior part of lateral sector, and drainage area depends on peripheral development of inferior hepatic vein. Right hepatic vein drains residual superior part of lateral sector.

 


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Fig. 1C. Nakamura and Tsuzuki's classification [24]. Volume-rendered reconstructions show hepatic venous drainage pattern at right liver lobe. Pattern is classified according to dominant development among right hepatic vein (RHV), inferior right hepatic vein (IHV), and middle hepatic vein (MHV). LHV = left hepatic vein. In type 3 (n = 1, 2%), large middle hepatic vein is present and drains paramedian sector and inferior part of lateral sector. Right hepatic vein is small and drains superior part of lateral sector. Also, thick inferior hepatic vein is present.

 


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Fig. 1D. Nakamura and Tsuzuki's classification [24]. Volume-rendered reconstructions show hepatic venous drainage pattern at right liver lobe. Pattern is classified according to dominant development among right hepatic vein (RHV), inferior right hepatic vein (IHV), and middle hepatic vein (MHV). LHV = left hepatic vein. In type 3 (n = 1, 2%), large middle hepatic vein is present and drains paramedian sector and inferior part of lateral sector. Right hepatic vein is small and drains superior part of lateral sector. Also, thick inferior hepatic vein is present.

 


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Fig. 2A. Classification of Marcos et al. [23]. In reconstructions showing peripheral branching pattern of middle hepatic vein, various branching patterns are displayed in inferior part of paramedian sector. Dashed lines indicate proposed line of hepatic transection based on intrahepatic venous collaterals. In type 1 (n = 36, 67.9%), thick veins draining segments IVa (green arrows) and V (yellow arrows) are branches with equal size and almost equal drainage areas.

 


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Fig. 2B. Classification of Marcos et al. [23]. In reconstructions showing peripheral branching pattern of middle hepatic vein, various branching patterns are displayed in inferior part of paramedian sector. Dashed lines indicate proposed line of hepatic transection based on intrahepatic venous collaterals. In type 2 (n = 9, 17%), segment V vein (yellow arrow) is small and short. Segment IVa veins (green arrows) are thin and have relatively larger drainage area than segment V vein.

 


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Fig. 2C. Classification of Marcos et al. [23]. In reconstructions showing peripheral branching pattern of middle hepatic vein, various branching patterns are displayed in inferior part of paramedian sector. Dashed lines indicate proposed line of hepatic transection based on intrahepatic venous collaterals. In type 3 (n = 8, 15.1%), early proximal branching occurs and some medium-sized branches are present in both segment IVa (vein indicated by green arrows) and segment V (vein indicated by yellow arrows). In original report, type 1 constituted 70%; type 2, 20%; and type 3, 10%. Our results are consistent with original report.

 


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Fig. 3A. In reconstructions, classification of Kawasaki et al. [25] defines two drainage patterns for segment IVb vein (arrow). In type 1 (n = 20, 37.7%), segment IVb vein flows into middle hepatic vein (MHV). LHV = left hepatic vein.

 


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Fig. 3B. In reconstructions, classification of Kawasaki et al. [25] defines two drainage patterns for segment IVb vein (arrow). In type 2 (n = 34, 62.3%), segment IVb vein flows into left hepatic vein (LHV). MHV = middle hepatic vein.

 


Results
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Results for each hepatic branch are summarized in Tables 1, 2, 3. Most (96.2% [275/286]) hepatic venous branches were visualized up to second branch order or more, and 93.7% (268/286) of branches reached to within 10 mm of the hepatic surface. A significant relationship was identified between branch order and distance from the hepatic surface (p < 0.05). As for total visualization of 3D CT hepatic venography, 98% (53/54) of cases were deemed excellent. Hepatic branching patterns according to previous classifications are shown in Figures 1A, 1B, 1C, 1D, 2A, 2B, 2C, 3A, and 3B.


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TABLE 1 Hepatic Branch Order on 3D CT Hepatic Venography

 

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TABLE 2 Distance from Hepatic Surface by Hepatic Vein on 3D CT Hepatic Venography

 

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TABLE 3 Relationship in Visualization on 3D CT Hepatic Venography Between Branch Order and Distance from Hepatic Surface

 


Discussion
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Graft volume is an important factor for determining operative indications in living-donor liver transplantation because both donor and recipient are affected by liver function within the graft or residual liver [2628]. Volume of the graft and residual liver depend on the line of hepatic resection, which is determined using a longitudinal line from the middle hepatic vein. Marcos et al. [23] classified peripheral branching patterns of the middle hepatic vein into three types and emphasized the importance of determining hepatic resection lines according to this classification. The method proposed in their study estimated functional venous anatomy of the liver graft, and the idea of optimizing outflow of the graft in the study was theoretically sound, but detailed information on hepatic venous anatomy was required. However, their report did not clearly document how venous anatomy was depicted and clarified. Furthermore, hepatic venous congestion is a common complication in living-donor liver transplantation [2] and is attributed to an immature intrahepatic collateral venous system [2, 23]. Loss of liver volume unfortunately results in liver dysfunction in either the recipient or the donor, compromising safety. To prevent this outcome, we reconstructed several venous branches in the recipient; reconstruction of only the major vein in the graft is insufficient. The hepatic venous branching pattern displays many variations [2, 3], and sometimes unexpectedly large branches exist. Leaving such veins unreconstructed can cause venous congestion. The inferior hepatic vein and veins draining segments VIII, V, and IVb often need reconstruction. Preoperative evaluation of peripheral hepatic venous anatomy is thus extremely important for determining the proper volume of graft liver to be resected.

In our study, 3D CT hepatic venography allowed visualization of detailed venous anatomies and complicated resection lines could be determined. Visualization of branches to more than the second order was achieved in 96.2% of the 286 branches using 3D CT hepatic venography, and 93.7% of branches reached to within 1 cm of the liver surface. Total visualization in 3D CT hepatic venography was excellent in 98% of the 54 cases. Insufficient 3D CT hepatic venography makes it difficult to decide the appropriate hepatic resection line and hinders hepatic venous reconstruction [16]. Our results indicate that 3D CT hepatic venography offers sufficient image quality to facilitate good understanding of the peripheral hepatic venous system and should be performed preoperatively in living-donor liver transplantation. Indeed, several recent reports have shown the usefulness of 3D CT for depicting vascular anatomies in living-donor liver transplantation [920]. However, central vascular anatomy has been the focus in most studies; and to the best of our knowledge, the significance of peripheral hepatic branches has not been the subject of much research.

Regarding the middle hepatic vein, branching patterns in our study were type 1 defined by Marcos et al. [23] in 36 donors (67.9%), type 2 in nine (15%), and type 3 in eight (17.1%). These frequencies are consistent with the vessel cast model study by Marcos et al. (type 1 was seen in 70%; type 2, in 20%; and type 3, in 10%). Our results indicate that detailed venous anatomy, which used to be visualized only by postmortem cast models of vessels [23], can be preoperatively and sufficiently visualized on 3D CT hepatic venography. In living-donor liver transplantation, intraoperative sonography has been the only procedure for evaluating functional venous anatomy for middle hepatic vein branching. Sonographic findings, however, are affected by individual skill, and the observed area is limited.

As mentioned earlier, reconstruction of other venous branches (i.e., veins other than the main trunk of the right hepatic vein) are sometimes required, but the indications for such reconstruction have not yet been determined [29, 30]. One report has suggested the importance of inferior hepatic vein reconstruction [31]. Our institutional policy is to reconstruct hepatic veins to prevent hepatic venous congestion if the veins are assumed on 3D CT hepatic venography to drain wide areas. According to the classifications of Nakamura and Tsuzuki [24] and Kawasaki et al. [25], venous drainage patterns in the right hepatic lobe and segment IVb vein branching patterns were as follows: In 26 of the 54 donors, inferior hepatic veins were type 2 or 3, consistent with a previous report [3, 24]. Visualization of type 2 and 3 inferior hepatic veins was excellent in all 26 cases. Unlike the previous report, venous drainage via a large middle hepatic vein from the posterior segment (type 3) was seen only in one patient. In 62% (33/53) of patients, segment IVb vein branched from the left hepatic vein. Living-donor liver transplantation using a right liver graft with reconstruction of the inferior hepatic vein was performed in 12 patients. Large middle hepatic vein branches with wide drainage areas were reconstructed in the recipients (Figs. 4A and 4B). Left grafts without a middle hepatic vein, as an optional technique for liver transplantation, are possible if the segment IVb vein has a large diameter and larger drainage volume than the segment IVa vein and the total left lobe has adequate volume for living-donor liver transplantation. In our two patients with large segment IVb vein branching from the left hepatic vein (Figs. 3A and 3B), transplantation using left grafts without the middle hepatic vein was performed. No complications occurred in these two patients. These cases indicate that visualizing peripheral branches on 3D CT hepatic venography is useful in living-donor liver transplantation using a hemiliver graft.



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Fig. 4A. 25-year-old male donor for right liver transplantation. On 3D CT hepatic venography, donor displays thick vein draining segment V (arrow) with wide drainage area.

 


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Fig. 4B. 25-year-old male donor for right liver transplantation. Drainage volume and virtual area of congestion in segment V vein were calculated from venous visualized area (arrows) on workstation. Calculated volume was 15%, and wide postoperative venous congestion in recipient graft was suggested. Venous reconstruction was considered additional option.

 

The process for 3D CT hepatic venography is generally time-consuming, although some specialized technologists routinely reconstruct every object within 30 min at our institution. However, 3D workstations and software are developing rapidly, and time will not long remain an issue. Failure to visualize peripheral hepatic venous branches on 3D CT was encountered in only one patient because the administered volume of contrast medium was too small. Our study did not examine correlations between 3D CT hepatic venography and conventional hepatic venography. However, venography can cause unnecessary complications, and given the high-quality 3D images obtained in this and other studies, the diagnostic value of conventional venography appears likely to wane for donor selection in liver transplantation.

In conclusion, 3D CT hepatic venography is useful for preoperative evaluation in living-donor liver transplantation. CT hepatic venography allows clear depiction of the peripheral hepatic venous system. In the future, 3D CT hepatic venography can visualize more peripheral branches with the development of CT technologies such as 16-MDCT. Surgeons can obtain sufficient information on branching patterns of the middle hepatic vein and venous variations to determine a suitable hepatic resection line and to make appropriate plans for venous reconstruction.


References
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

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P. T. Johnson and E. K. Fishman
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Am. J. Roentgenol., February 1, 2006; 186(2): 406 - 415.
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