319

ORIGINAL
Evaluation of the use of intraoperative real-time virtual
sonography with sonazoid enhancement for detecting
small liver metastatic lesions after chemotherapy inhepatic resection
Kenichiro Araki, M.D., Ph.D., Norifumi Harimoto, M.D., Ph.D, Ryo Muranushi, M.D., Kouki Hoshino, M.D.,
Kei Hagiwara, M.D., Takahiro Yamanaka, M.D., Norihiro Ishii, M.D., Ph.D, Mariko Tsukagoshi, M.D., Ph.D,
Takamichi Igarashi, M.D., Ph.D, Akira Watanabe, M.D., Ph.D, Norio Kubo, M.D., Ph.D., and Ken Shirabe, M.D., Ph.D.
Division of Hepatobiliary and Pancreatic Surgery, Department of General Surgical Science, Gunma University Graduate School of Medicine,Gunma, Japan

Abstract : Background : Systemic chemotherapy can drastically downsize metastatic liver tumors and thesesmall liver lesions could sometimes be difficult for surgeons to detect during hepatectomy. We assessed the usefulness of intraoperative real-time virtual sonography (RVS) with contrast-enhanced ultrasonography (CEUS)
using ‘Sonazoid’ contrast agent (RVS-CEUS). Methods : We performed the intraoperative RVS-CEUS techniqueon 10 tumor lesions in six cases, which were scheduled for hepatic resection of < 10 mm in diameter in our liver
metastases series. These lesions were preoperatively diagnosed by contrast enhanced-computed tomography(CE-CT) or Gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid (Gd-EOB-DTPA)-enhanced magnetic
resonance imaging (EOB-MRI). We assessed the detectability of a tumor with RVS-CEUS during surgery andcompared it with that of preoperative CE-CT or EOB-MRI. Results : Detectability of RVS-CEUS for 10 small lesions was 90% (n = 9/10) and that of other preoperative modalities were 50% (n = 5/10, CE-CT) and 100% (n = 10/10,
EOB-MRI). Minimum tumor size detected was 3.0 mm in diameter, and maximum depth of detection with RVSCEUS was 43.5 mm ; these results could be an advantage when compared with other intraoperative diagnostic
modalities. Conclusion : Intraoperative RVS-CEUS was useful for detecting small metastatic liver lesions after
chemotherapy and could be an effective intraoperative diagnostic technique for hepatic resection of a size < 10mm. J. Med. Invest. 66 : 319-323, August, 2019
Keywords : real-time virtual sonography, small liver metastatic lesion, sonazoid enhancement, hepatectomy, chemotherapy

INTRODUCTION
Since considerable advancements have been made in systemic
chemotherapies for the treatment of colorectal cancer, aggressive surgical resection combined with systemic chemotherapy
for colorectal liver metastases (CRLM) has become a standard
treatment (1). These chemotherapies can reduce the tumor size of
CRLM, allowing radical resection unless tumors were initiallyunresectable (2, 3). Several reports described that the incidenceof ‘disappearing’ liver metastases (DLM) in patients receiving
preoperative systemic chemotherapy ranged from 7-37% (4-6).
The phenomenon of disappearing small liver metastases seems
to be a radiological rather than an actual biological occurrence,
because the rates of macroscopic and microscopic residual disease are high and the local recurrence rates are high as well(7). Therefore, surgeons must detect these downsized and small
lesions of metastatic liver tumors accurately during surgery forradical resection.
Preoperative imaging for the diagnosis of hepatic lesions has
been extremely developed with the advent of contrast-enhanced
ultrasonography (CEUS) and Gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid-enhanced magnetic resonance(MR) images (EOB-MRI). Ultrasoundcontrast microbubbles(MBs), such as Sonazoid MBs, make it possible to render a specific phase caused by phagocytosis of Sonazoid MBs by Kuppfercells as late vascular phase (8). Gd-EOB-DTPA, which is taken
up by hepatocytes and excreted in the bile, can make it easy
to improve the detection and characterization of small hepatic
tumors (9-11). Using these new modalities, hepatic lesions of afew millimeters in size could be detected. However, these small
hepatic lesions are often difficult to detect using intraoperative
ultrasound (IOUS) during surgery, because of the dissociation
between images and intraoperative real-vision of the liver.
Real-time virtual sonography (RVS), also known as real-time
fusion imaging (Fusion Imaging), is an innovative techniquethat can visualize both scanned ultrasound images and reconstruction images of computed tomography (CT) and/or magnetic
resonance (MR) on the same screen of the ultrasound system.
This imaging technique has already been applied for navigation,
to guide needle puncture in radiofrequency ablation therapy(12), prostate biopsy (13), and identification of breast lesions (14).
From these facts, we applied the RVS system and CEUS technology (RVS-CEUS) for intraoperative use in hepatic resection. In
this article, we report the significance of RVS-CEUS in detecting small liver lesions as a novel technique in hepatic resection.

Received for publication May 13, 2019 ; accepted July 12, 2019.
Address correspondence and reprint requests to Kenichiro Araki,
M.D., Ph.D. Division of Hepatobiliary and Pancreatic Surgery, Department of General Surgical Science, Gunma University Graduate
School of Medicine, 3-39-22 Showa-machi, Maebashi, Gunma 3718511, Japan and Fax : +81-27-220-8230.

METHODS

Patients and Inclusion criteria
From June 2016 to December 2018, the RVS-CEUS method

The Journal of Medical Investigation Vol. 66 2019

K. Araki, et al. RVS for small lesion in hepatectomy

320

was indicated in six cases of hepatic resection, which included
10 liver lesions, at the Gunma University Hospital. The patientswere selected as follows : malignant hepatic lesions scheduled
for liver resection ; small lesion less than 10 millimeters ; bothdynamic CT and EOB-MRI performed preoperatively ; lesion expected to be very difficult to detect intraoperatively by surgeons ;and anticipated curative resection of the liver lesions by hepatic
resection. The patient characteristics are shown in Table 1. Our
institutional ethics committee approved the study protocol (Approval No. : 2018-247).

Preoperative imaging analysis
Routinely, we reconstruct virtual reality images from CT
images using SYNAPSE VINCENT software (Fujifilm medical,
Tokyo, Japan) for preoperative three-dimensional (3D) simulation of hepatic resection. To prepare for using the intraoperative RVS method, preoperative CT or MRI images and digital
imaging and communication in medicine (DICOM) data were
uploaded to the RVS ultrasound system before surgery, and wereconstructed real-time fusion imaging on the monitor of the
RVS ultrasound system during surgery (the operative procedure
is described below).

Procedural steps of RVS technique and Sonazoid enhancement
For the RVS technique, we used the APLIO i800 system(Toshiba Medical Systems Corp., Otawara, Japan). The procedural steps of IO-RVS were as follows : RVS ultrasound system
was placed on the left side of the patient’s head. The electromagnetic transmitter/receiver, which is connected to the RVS
ultrasound system, was placed on the left side of the patient’s
neck. The convex type of IOUS probe was attached to the sterilized magnetic sensor. This electromagnetic transmitter and thesensor detect the spatial position and direction of the ultrasoundprobe using a magnetic field. Then, the spatial positions of boththe ultrasound and CT/MR images were adjusted appropriately.
The axial plane of CT/MR images was screened with landmarksof the liver such as the portal and hepatic veins for adjustment.

Next, the probe was placed on the liver surface to adjust fusion
visualization between the ultrasound image and CT/MR images.
When the ultrasound probe was moved on surface of the liver,real-time multiplanar reconstruction (MPR) images of CT/MR
could be visualized intraoperatively in the RVS system (Fig. 1A).
The procedural steps of Sonazoid enhancement were as follows : after preparation of the RVS system, the ultrasound probe
was put around the target lesion on the surface of the liver withreference to preoperative 3D simulation images. The 0.5 ml
solution of Sonazoid MBs was injected into the patients intravenously, and then we observed and detected target lesions withthe ultrasound system. Metastatic tumors are almost visualized
as low echoic lesions in late vascular phase, which is after fiveto-ten minutes after injection of Sonazoid MBs. The APLIO i800
system is able to visualize both the Sonazoid-enhanced ultrasound image and the RVS image on the same monitor (Fig. 1B).

Statistical analysis
Continuous data are presented as mean (standard deviation[SD]) and median (range). Differences between the two cohorts
were assessed using Fisher’s exact test and the Mann–Whitney
U test, as appropriate. All statistical analyses were performed
using SPSS Statistics software version 24.0 (IBM SPSS Inc.,
Chicago, IL). P < 0.05 was considered statistically significant.

RESULTSThe results of the study are summarized in Table 1. All of
the target lesions were from six cases and 10 lesions (n = 10)of metastatic liver tumors, which were derived from patientswith colorectal cancer (n = 5), and adenosquamous carcinomaof the uterus (n = 1). The regimens of chemotherapy were as follows : XELOX base (n = 3), FOLFOX base Bevacizumab (n = 1),
and paclitaxel + CDDP (n = 1). Macroscopic pathological findingsof the liver were revealed in three cases with a normal liver,two with a steatotic liver, and one with a blue liver. Microscopic

Table 1. Summary of case series performed RVS using Sonazoid enhancement
Case Tumor
Age Sex
No.
No.

Diagnosis

Segment Tumor
Depth
Regimen ofof lesion diameter of tumor chemotherapy

macroscopicchange ofliver

microscopicchange ofliver

Detection Detection Detection
by CE- of EOB- of RVSCT
MRI
CEUS

1

1

62

M

CRLM

7

5.0

43.5

FOLFOX+Bev

normalInflammatory
cell
infiltration

+

+

+

2

2

54

F

CRLM

6

4.5

0

XELOX

steatotic
liverlarge fat
droplet

−

+

+

3

6

4.0

7.3

−

+

+

4

8

4.6

11.6

+

+

+

3
4

5
6

52
49

M

CRLM

5

4.8

20.0

XELOX+Bev

normalnormal+++F

Metastasis fromadenosquamous
carcinoma of
uterus

5

5.2

13.4

Paclitaxel+CDDP

steatotic
liverlarge fat
droplet

−

+

+

7

6.2

21.4

−

+

−

5/6

4.0

3.0

+

+

+

7

7.0

17.6

+

+

+

5

3.0

0

−

+

+

7
5

8

65

M

CRLM

9
6

10

51

M

CRLM

FOLFOXXELOX+Bev

blue liver

normalsinusoidal
obstruction
normalRVS, real-time virtual sonography ; CE-CT, contrast-enhanced-computed tomography ; EOB-MRI, gadolinium-ethoxybenzyl-diethylene-triaminepentaacetic acid-enhanced magnetic resonance image ; RVS-CEUS, contrast-enhanced ultrasonography with real-time
virtual sonography ; CRLM, Colorectal liver metastases ; Bev, Bevacizumab

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The Journal of Medical Investigation Vol. 66 August 2019

Figure 1. Image references of the RVS system. A: RVS image adjusting spatial positions of both ultrasound and CT

image. The left side of the monitor indicates a CT image and the right side of the monitor indicates an ultrasound image. B: RVS image using Sonazoid enhancement for the liver tumor located on segment 8. The left side of the monitor
indicates a fusion imaging of the hepatobiliary phase in EOB-MRI, and right side of the monitor indicates Sonazoidenhancement. RVS, real-time virtual sonography; CT, computed tomography; EOB-MRI, gadolinium-ethoxybenzyl-diethylene-triaminepentaacetic acid-enhanced magnetic resonance image.

pathological findings were revealed in the post-chemotherapy
state, shown as large fat droplet (n = 2), and sinusoidal obstruction (n = 1).
The locations of target lesions were segment 3, 5, 6, 7, and 8,
respectively (Table 1). Depth of tumors from the liver surface
ranged from 0.5 to 43.5 mm. The maximum depth of detectedlesions was 43.5 mm, which indicates that this method has anadvantage for detecting deep lesions (Fig. 2A, 2B). The minimum size of a liver lesion that could be detected with RVS with
Sonazoid enhancement was 3.0 mm in diameter in Case No.6.
The usefulness of the system was limited in cases where the lesion existed in the subphrenic portion (segment 7 and 8) near theroot of the hepatic veins into the inferior vena cava, because theultrasound probe could not be inserted into this space. However,some lesions located in segment 7 and 8 could be detected withRVS-CEUS (Fig. 2C, 2D). There were no severe postoperativecomplications (Clavien-Dindo classification : grade III or more)or any mortality in the patients.
Ten of eleven tumors scheduled for resection were successfully
identified by this system ; the detection rate was 90% (Table2). Of these, one liver tumor located in S7 (case No.4, tumor
No.7) was difficult to visualize clearly with the RVS system.
The tumor was located in the dorsal part of segment 7 ; hence,the convex probe of RVS was difficult to insert into the dorsal
space of the right lobe and attach to the liver surface on the posterior side. Detectability of each modality shown in Table 2, revealed the superiority of EOB-MRI (100%) to contrast-enhanced
MDCT (50%).
Table 2. Detectability of imaging modalities for liver metastatic
tumorsModality

CE-CT

EOB-MRIRVS-CEUS

Detectability, number (%)

5/10 (50%)

10/10 (100%)

9/10 (90%)

CE-CT, contrast-enhanced computed tomography ; EOB-MRI,
gadolinium-ethoxybenzyl-diethylene-triaminepentaacetic acid-enhanced magnetic resonance image ; RVS-CEUS, contrast-enhanced ultrasonography with real-time virtual sonography

DISCUSSION

Figure 2. A : A liver lesion of segment 7 detected in the hepatobi-

liary phase by EOB-MRI in case No.1 (tumor No.1). The tumor size
was 5.0 mm in diameter (arrow). B : Macroscopic finding of surgical
specimen of the liver tumor (arrowhead). C : A liver lesion of segment
7 detected in the hepatobiliary phase by EOB-MRI in case No.5 (tumor
No.9). The tumor size was 6.2 mm in diameter (arrow). D : Macroscopic finding of surgical specimen of the liver tumor (arrowhead).
EOB-MRI, gadolinium-ethoxybenzyl-diethylene-triaminepentaacetic
acid-enhanced magnetic resonance image.

In this article, we described a novel technique using RVS with
Sonazoid enhancement for the detection of small liver lesions,which are less than 10 mm in size, diagnosed by preoperative
imaging such as multidetector CT or EOB-MRI. In the era of
EOB-MRI and CEUS, small liver lesions downsized a few millimeters after chemotherapy are often detected with these newmodalities preoperatively. Therefore, hepatobiliary surgeons
sometimes recognize these small lesions for hepatic resection
during surgery, and sometimes find it very difficult to detect
them intraoperatively with the existing traditional modalities
such as the normal ultrasound. Arita et al. reported the usefulness of IO-CEUS in identifying disappearing liver metastases
from colorectal cancer after chemotherapy (15). For intraoperative diagnosis of liver lesions, IO-CEUS with Sonazoid enhancement has the highest detection rate (sensitivity) and may be themost variable modality. This RVS with CEUS method can add tothe position or recognition diagnostic ability of IO-CEUS. To ourknowledge, this is a novel report about intraoperative RVS using
CEUS (Sonazoid enhancement) for hepatic resection.

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K. Araki, et al. RVS for small lesion in hepatectomy

Previously, very few technical papers about RVS for hepatic
resection were reported. Kasuya et al. described that RVS withindocyanine green (ICG) fluorescence navigation was usefulfor resecting US invisible liver tumors (16). ICG fluorescencenavigation is an excellent surgical navigation method utilizing
the rapid binding of ICG to plasma protein in vivo and the incorporation of most ICG into hepatic parenchymal cells. However,the detection of liver tumors with ICG fluorescence imaging
could be indicated for only superficial liver lesions, because
the excitation light of ICG fluorescence does not reach the deep
layer of the liver. In this study, we could detect a tumor of 43.5
mm maximum depth from the liver surface ; that depth is only
dependent on the ability of the ultrasound system with Sonazoidenhancement. Satou et al. reported the usefulness of an RVS
system combined with preoperative 3D simulation images tonavigate the detection of tumors and for navigation of the resection plane for hepatic resection (17). This system may be very
useful for intraoperative tumor detection and recognition of liver
anatomy in hepatic resection. Since this system was not usedwith CEUS technique such as RVS with Sonazoid enhancement,
small isoechoic tumors may not be visualized on the ultrasoundmonitor as a real-time reference image. We believe that theultrasound reference image on the monitor should visualize
the target tumor for precise guiding of transection plane, whichleads to radical resection. From the advantage of our RVS with
CEUS method and the result of this study, when the target liverlesion is very small with a size less than 10 mm, we prefer thisRVS system with CEUS for the surgery.
This method has a few limitations. In cases of the lesion
located in the subphrenic, posterior, or caudate segments, the ultrasound probe could not be inserted into the space, because theconvex type probe is only available for RVS technology at present. In such cases where the lesion is located in these segments,
it is difficult to reconstruct the fusion image on the monitor.
Additionally, the lesion located in very right-posterior side needto mobilize the right lobe of the liver to attach the ultrasoundprobe. During liver mobilization, the liver is transformed to adifferent form from the preoperative imaging. Therefore, it is
too difficult to merge the ultrasound images of liver mobilization
and CT/MRI images together in RVS system. In the future, it isexpected that a smaller ultrasound probe compatible with both
RVS and MBs enhancement would be developed, and this probe
would make it possible to use this method for difficult situations.
Recently, several intraoperative navigation technologies forliver surgery have been reported, e.g. 3D printed liver models,augmented reality by projection mapping technology, and so on.
The usefulness of 3D printed synthetic liver has been reported inliver surgery fields such as hepatic resection, liver transplantation, and resection perihilar cholangiocarcinoma (18-21). Having
the physical model during operations provides greater intuitive
navigation for critical areas, and this helps to overcome difficult
orientation because these models can be physically positioned
in the most desired fashion (19). Igami et al. reported that 3D
printed liver could be useful in hepatic resection for small tumorsthat are invisible by intraoperative ultrasonography (18). They
described that there are some disadvantages of 3D printing technology, such as requirement of long time to print 3D liver models
and high cost of production. Augmented reality with projection
mapping technology could also be a promising navigation tool forthe detection of small tumors in liver surgery. Ntourakis et al. reported that augmented reality might be a helpful navigation tool
for the resection of small liver metastases that have been shrunkby preoperative chemotherapy (22). These technologies are estimated with virtual reconstruction from preoperative images, so
surgeons should consider accuracy and that errors of a few millimeters may occur during virtual reconstruction. Our strategyof this study is presented tumor detection by the real existence
diagnosis using Sonazoid-enhancing ultrasound. Therefore, thismethod may minimize the error between visualization with RVS
system and real positioning of the target tumor. Moreover, thecombined use of these navigation technologies would make iteasier to detect small or missing liver tumors. To our knowledge,
the laparoscopic system for RVS is not yet available for commercial use. Recently, laparoscopic liver resections have been widely
applied for liver metastases. The laparoscopic system for RVSCEUS could be extremely useful for the detection of tumors when
performing this surgery, since laparoscopic liver resection islimited to manipulating instruments and surgical space rather
than being an open liver resection.
In conclusion, this study indicated that intraoperative RVS
with Sonazoid enhancement was useful for detecting small metastatic liver lesions after chemotherapy and is a viable option forhepatic resection of a size less than 10 mm in diameter.

ACKNOWLEDGEMENTNone.

DISCLOSURE
There were no conflicts of interest or financial support.

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