AJR 2004; 183:1065-1070
© American Roentgen Ray Society
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
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,
2060 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 05 mm, 610 mm,
1115 mm, 1620 mm, or 2125 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
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
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; 400500 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 3.55.0 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 proximaldistal 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:
05 mm, 610 mm, 1115 mm, 1620 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.
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Results
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 3 Relationship in Visualization on 3D CT Hepatic Venography Between Branch
Order and Distance from Hepatic Surface
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Discussion
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. 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.
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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.
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