DOI:10.2214/AJR.06.1063
AJR 2007; 188:W464-W466
© American Roentgen Ray Society
Three-Dimensional Visualization of Liver Segments on Contrast-Enhanced Intraoperative Sonography
Junichi Arita1,
Norihiro Kokudo,
Keming Zhang and
Masatoshi Makuuchi
1 All authors: Hepato-Biliary-Pancreatic Surgery Division, Department of
Surgery, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo,
Bunkyo-ku, Tokyo 113-8655, Japan.
Received August 10, 2006;
accepted after revision November 8, 2006.
Address correspondence to J. Arita
(jarita-tky{at}umin.ac.jp).
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Abstract
OBJECTIVE. The purpose of this study was to describe a novel
technique for the 3D visualization of a liver segment on sonography, using a
second-generation contrast agent in a dog, that would be applicable for
anatomic hepatic resection.
CONCLUSION. After a mixture of YM454 and indigo carmine was injected
into a portal vein branch, well-delineated 3D segmental staining was seen for
approximately 10 minutes in harmonic mode sonography. The addition of indigo
carmine significantly prolonged the contrast effect of YM454.
Keywords: animal studies • contrast media • harmonic sonography • liver • sonography
Introduction
Intraoperative sonography is indispensable for liver surgery,
especially for anatomic hepatic resection, which improves the prognosis of
patients with hepatocellular carcinoma
[1,
2]. Most of the following
procedures in the anatomic hepatic resection are done under intraoperative
sonography: a portal vein branch is punctured to inject dye under
intraoperative sonography, liver transection is begun from the liver surface
along the border of the dyed area under intraoperative sonography, and the
procedure continues toward the root of the portal vein branch under
intraoperative sonography [3].
In this original technique, the segmental border is recognized only in 2D on
the surface of the liver by the injected dye. The 3D segmental border in the
cutting plane is not visible on intraoperative sonography and is reconstructed
only in the surgeon's brain. There have been a few reports of sonographic
visualization of a liver segment using microbubbles of carbon dioxide
[4,
5]. However, the technique has
not been clinically applicable for anatomic hepatic resection because the
contrast effect decreased in only a few minutes
[4]. Levovist (SH U 508A,
Schering), a first-generation contrast agent, would also not be applicable
because it provides only short and intermittent views
[6].
The purpose of our study was to develop a novel technique for the
sonographic visualization of a segment of the dog liver using a mixture of a
second-generation contrast agent and indigo carmine that would be applicable
for anatomic hepatic resection in a clinical setting.
Materials and Methods
This study was approved by the Institute for Animal Experimentation,
Faculty of Medicine, University of Tokyo. In compliance with the guidelines of
the institute, four adult German shepherd dogs weighing 29-32 kg with healthy
livers were fed and laparotomized under general anesthesia. After the
intramuscular injection of 40 mg/kg of ketamine, the dogs received intubation
and were kept anesthetized by inhaling halothane. After laparotomy, a 3-French
catheter was inserted through the main portal vein trunk and its tip was
placed in an appropriate third- or fourth-order intrahepatic portal
branch.
A second-generation contrast agent, YM454 (perflutren lipid microspheres,
Yamanouchi), a perfluoropropane gas-filled lipid stabilized microbubble, was
used in this study as a contrast agent. A mixture of 3, 5, or 10 µL/kg of
YM454 and 3 mL of indigo carmine was injected at a rate of 0.5 mL/s through
the catheter. An immediate flush with 2 mL of saline followed. Intraoperative
sonography, either in the fundamental mode or in the harmonic mode, was begun
just after injection, with the probe put on the liver surface. For each YM454
dose, sonography was performed in both modes. After every two injections at
the same YM454 dose, the tip of the catheter was repositioned in another
portal vein branch. In one of the four dogs, a control experiment assessing
the effect of indigo carmine was performed. In this control experiment, 3, 5,
and 10 µL/kg of YM454 with 3 mL of normal saline, instead of indigo
carmine, was administered, and sonography was performed only in the harmonic
mode.
An SSD-6500 sonographic scanner (Aloka) and a small convex probe capable of
harmonic imaging were used for contrast-enhanced intraoperative sonography.
The Extended Pure Harmonic Detection mode (Aloka) was adopted for all harmonic
imaging. The transmit and receive center frequencies were both 3.75 MHz in the
fundamental mode and were 1.875 and 3.75 MHz, respectively, in the harmonic
mode. In all experiments, the frame rate was set at 15 Hz so that continuous
images could be obtained. The gain, the time-gain control, and the focus point
were set to optimally visualize the intrahepatic vasculature just before the
injection of the contrast agent and were not altered thereafter. The
mechanical index was set at 0.21 for the fundamental mode and 0.12 for the
harmonic mode. A linear gray-scale map was used in this study for both
fundamental and harmonic imaging. The sonographic images were recorded on
S-VHS videotapes from the injection until the contrast effect disappeared.
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Fig. 1A —Intraoperative sonography with injection of 3 µL/kg of YM454
(perflutren lipid microspheres, Yamanouchi) and 3 mL of indigo carmine in a
canine model. Baseline sonogram shows catheter in portal vein branch
(arrow).
|
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Fig. 1B —Intraoperative sonography with injection of 3 µL/kg of YM454
(perflutren lipid microspheres, Yamanouchi) and 3 mL of indigo carmine in a
canine model. Well-delineated 3D segmental staining (arrows) was seen
after injection. Catheter in portal vein branch (arrowhead) also is
seen.
|
|
The contrast effect of segmental staining of a portal area was judged as
"well delineated" or "faint," in terms that the
boundary of the segment was easily recognized. The term "3D" was
used when the total shape of the segment was recognized by scanning with the
probe.
Results
In the harmonic mode, the injected portal vein and its tributaries were
clearly enhanced after the injection. A few seconds later, the hepatic veins
running through this portal area were also enhanced. When the YM454 dose was 3
µL/kg, well-delineated 3D segmental staining was subsequently seen in all
four dogs (Table 1 and Figs.
1A,
1B and
2). When the YM454 doses were 5
or 10 µL/kg, a wide acoustic shadow subsequently appeared and interfered
with visualization before well-delineated 3D segmental staining in all four
dogs (Table 1 and
Fig. 3).
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Fig. 2 —Well-delineated 3D segmental staining was seen (arrows)
after injection of 3 µL/kg of YM454 (perflutren lipid microspheres,
Yamanouchi) and 3 mL of indigo carmine in a canine model. Catheter in portal
vein branch (arrowhead) is also seen.
|
|
In the fundamental mode, the portal vein branches and the hepatic veins
were seen in the same order; however, the contrast effect was smaller.
Well-delineated 3D segmental staining was seen in fewer dogs and the durations
were shorter (Table 1).
In all the experiments using a mixture of YM454 and indigo carmine, a dyed
area appeared on the liver surface just after injection and persisted for 2-3
minutes (Fig. 4). In the
control experiments using normal saline for the mixture instead of indigo
carmine, well-delineated 3D segmental staining was not seen when the YM454
dose was 3 µL/kg, was seen for 5 minutes after 5 minutes of wide acoustic
shadow when the YM454 dose was 5 µL/kg, and was seen for 3 minutes after 3
minutes of wide acoustic shadow when the YM454 dose was 10 µL/kg.
Discussion
Using a mixture of a second-generation contrast agent and indigo carmine,
we have established a technique for 3D segmental staining of the dog liver.
This technique may be applicable for anatomic hepatic resection in a clinical
setting because of the clear contrast, continuous real-time visualization, and
long duration of the contrast effect. It may guide surgeons into the proper
transection plane for anatomic hepatic resection and also show them
objectively whether the tumor is confined inside the segment planned for
resection. The technique may also warn surgeons when the tumor is near or
across the planned transection plane. Although the duration of the contrast
effect in this study was not long enough to complete the actual hepatic
resection, which requires 30-60 minutes, recorded sonograms could be used for
guidance in the latter part of the hepatic transection. The most prominent
advantage of this technique may be continuous real-time visualization of the
contrast effect, which is made possible because of the properties of YM454,
which has a bubble that is tolerant of acoustic power and is highly sensitive
to ultrasound [6].
The best setting for intraoperative sonography was harmonic mode using 3
µL/kg of YM454 mixed with 3 mL of indigo carmine. The reasons are that the
contrast effect obtained in the harmonic mode was much better than in the
fundamental mode, the disturbing acoustic shadow did not appear at the YM454
dose of 3 µL/kg, and the addition of indigo carmine significantly prolonged
the duration of enhancement. To our knowledge, no explanation for the
prolongation of enhancement by indigo carmine has been reported in the
literature.
A clinical study in humans would be necessary to assess the utility and
safety of this technique and to establish appropriate conditions for its use
in humans. Modifications to extend the duration of the contrast effect, if
possible, may be useful for clinical application.
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Abstract
Introduction
