DOI:10.2214/AJR.04.1252
AJR 2006; 186:S255-S260
© American Roentgen Ray Society
Virtual Sonographic Radiofrequency Ablation of Hepatocellular Carcinoma Visualized on CT but Not on Conventional Sonography
Masashi Hirooka1,
Hidehito Iuchi1,
Teru Kumagi1,
Shuichiro Shigematsu1,
Atsushi Hiraoka1,
Takahide Uehara1,
Kiyotaka Kurose1,
Norio Horiike1 and
Morikazu Onji1
1 All authors: Third Department of Internal Medicine, Ehime University,
Sigenobutyo Sizukawa, Ehime, Japan.
Received August 6, 2004;
accepted after revision March 24, 2005.
Address correspondence to M. Hirooka.
Abstract
OBJECTIVE. Some nodules cannot be visualized clearly on conventional
sonography but can be visualized on CT. In the present study, we evaluated the
usefulness of real-time percutaneous ablation therapy under virtual
sonographic guidance for these nodules.
SUBJECTS AND METHODS. In vitro experiments were performed with
gelatin gel to evaluate the accuracy of virtual sonography. We also studied 50
patients with 58 hepatocellular carcinoma nodules, of whom 18 patients (21
nodules) underwent radiofrequency ablation by virtual sonography. This was the
initial treatment for seven of these patients and an additional treatment for
11 patients. Thirty-two patients (37 nodules) received radiofrequency ablation
without virtual imaging. The patients receiving standard radiofrequency
ablation were retrospectively selected as the historical control group under
the same conditions as the study group.
RESULTS. The in vitro gelatin gel study revealed that all punctures
had been performed accurately. In both the initial-treatment group and the
additional-treatment group, the mean number of treatments with virtual
sonography was significantly lower than that without virtual sonography
(p = 0.003 for both groups). The rates of local recurrence and
complications did not differ significantly between the two groups.
CONCLUSION. In the treatment of nodules not depicted on sonography,
radiofrequency ablation assisted by virtual sonography is an efficacious
alternative.
Keywords: abdominal imaging • ablation • cancer • liver disease • MDCT • radiofrequency
Introduction
Percutaneous ethanol injection
[1-4],
microwave coagulation therapy
[5], and radiofrequency
ablation
[6-11]
are widely performed as a percutaneous local treatment for small
hepatocellular carcinomas (HCCs). Most of these treatments have been performed
under real-time sonographic guidance
[3,
4,
9,
10]. Sonographic targeting
requires adequate visualization. However, some nodules cannot be detected
clearly on conventional sonography, such as nodules in the hepatic dome,
lesions deep in relation to the body surface, lesions on the liver surface,
and lesions smaller than 1 cm. In addition, determination of the residual
viable portion of the HCC on conventional sonography after treatment with
transcatheter arterial embolization, percutaneous ethanol injection, microwave
coagulation therapy, or radiofrequency ablation has also been difficult. In
these cases, clinicians must mentally reconstruct a 3D model of the body from
multiple 2D horizontal CT images, creating the equivalent of a sonographic
image, and puncture the nodule using this conventional sonographic image for
guidance. Mental reconstruction is the most important and difficult task in
conventional sonography. The target site imaged by conventional sonography
often differs from the site determined by CT.
MDCT offers the ability to scan large longitudinal volumes rapidly and can
scan volumes over a large range within a short time with thin slices
[12,
13]. MDCT images are then used
to reconstruct 3D images. Multiplanar reconstructed images resemble
conventional sonographic images. Using a computer system, slices are animated
continuously, and the user becomes immersed in and interacts with a purely
virtual, nonreal environment. We confirmed that the virtual sonographic images
produced by MDCT data were equal to, and sometimes more clearly interpretable
than, those of conventional sonography. In addition, we confirmed that HCC
nodules depicted by virtual sonography but not by conventional sonography
could be treated adequately
[14]. In the present study, we
evaluated the usefulness of real-time percutaneous ablation therapy under
guidance using virtual sonography for HCC not visualized on sonography but
visualized on CT.
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Fig. 1A —Puncture procedure used for virtual sonography in gelatin gel. MDCT
image of gelatin gel shows small ball of contrast medium (arrow) and
4-French catheters (arrowheads) placed in phantom in such a way as to
imitate tumor and vessels.
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Fig. 1C —Puncture procedure used for virtual sonography in gelatin gel.
Conventional sonographic image is depicted in same slice as that shown by
virtual sonography. Arrowheads indicate catheters.
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Subjects and Methods
Virtual Sonography
For synthesis of 3D images and generation of virtual sonographic images,
Virtual Place Advance software (Medical Imaging Laboratory;
www.milab.jp)
was used. This has been described in detail in a previous communication from
our laboratory [14]. In short,
this system runs smoothly on a PC with Windows 2000 (Microsoft), a Xeon
2.0-GHz dual processor (Intel), 2.0 GB of random-access memory, and a graphic
card with Quadro4 900XGL (NVIDIA Corp.). First, a 3D image was synthesized by
CT (LightSpeed Ultra 16, GE Healthcare). The scanning parameters were a
0.625-mm collimation x 16.6 mm/sec (pitch of 1.75) table speed, 300-400
mA, 120 kV, and a 512 x 512 matrix. Then, a virtual sonographic image of
the CT scan was generated. Multiplanar images were reconstructed using MDCT
data, and slices were displayed in a fan shape to resemble conventional
sonographic images [14].
In Vitro Experience
To evaluate the accuracy of the puncture using the virtual sonographic
images, we conducted an in vitro experiment using a 16 x 9 cm piece of
gelatin gel. In the gel, a target lesion modeled on the HCC nodule was made by
injecting 1 mL of iomeprol contrast medium (Iomeron 300, Eisai) just before
the gelatin became hard. The target lesions were placed at different depths
(2.7, 3.1, 3.5, 6.4, 7.0, and 7.6 cm). A 4.0-French catheter modeled on a
vessel was placed around the target (Figs.
1A,
1B,
1C, and
1D), and CT of the gelatin gel
was then performed. A 1-cm piece of the 4.0-French catheter was placed on the
surface of the gelatin gel, and a virtual sonographic image was then
reconstructed through the piece. The conventional sonographic probe was placed
on the site where the piece was placed, enabling sonographic images identical
to the virtual sonographic images to be obtained. A 21-gauge needle was used
to puncture the gelatin gel through the spot where the sonographic B-mode
image was identical to the virtual sonographic image. After puncture of the
gel, the distance from the target to the needle tip was measured by CT. Six
target nodules were made, and each was punctured 24 times.
Clinical Experience
Patients—We examined 18 patients (14 men and 4 women; age
range, 59-89 years; mean, 69.3 ± 8.07 [SD] years) with 21 HCC nodules,
who had been admitted to the Third Department of Internal Medicine, Ehime
University School of Medicine, Japan, between February 2004 and June 2004. All
patients had liver cirrhosis. The pathogenesis of liver cirrhosis was
hepatitis B in three patients and hepatitis C in 15. According to the
Child-Pugh classification, 13 had class A and 5 had class B cirrhosis. The
mean maximum diameter of the HCC nodules was 14.0 ± 7.81 mm (range,
5-35 mm). Of the 21 nodules, eight were in the anterior segment, eight in the
posterior segment, two in the lateral segment, and three in the medial
segment. HCC was diagnosed using imaging analysis, including helical dynamic
CT, CT hepatic arteriography, CT during portography, and iodized oil
(Lipiodol, Andre Guerbet)-enhanced CT. The patients with HCC nodules were
confirmed to have elevated levels of 
-fetoprotein or
des-
-carboxy-prothrombin. All HCC nodules were visualized on helical
dynamic CT, CT hepatic arteriography, CT during portography, or iodized
oil-enhanced CT but could not be visualized clearly on conventional
sonography. Of the 21 nodules, seven had not been previously treated
(initial-treatment group). The remaining 14 nodules were residual viable
lesions that developed after previous treatment (additional-treatment group),
with one nodule a local recurrence and the other 13 the result of an
inadequate safety margin taken during initial surgery. These 14 nodules could
not be distinguished from viable lesions and necrotic areas after one cycle of
radiofrequency ablation.
Thirty-two patients (37 nodules; 26 men and 6 women; age range, 59-80
years; mean, 68.6 ± 5.28 years) treated between January 2002 and
January 2004 without the use of virtual sonography were selected as historical
control data. All these nodules were visualized on helical dynamic CT, CT
hepatic arteriography, CT during portography, or iodized oil-enhanced CT but
could not be visualized clearly on conventional sonography. The patients had
elevated levels of -fetoprotein or des--carboxy-prothrombin. All
patients had liver cirrhosis, the pathogenesis of which was hepatitis B in six
patients and hepatitis C in 26. According to the Child-Pugh classification, 24
had class A and 8 had class B cirrhosis. The mean maximum diameter of the HCC
nodules was 15.7 ± 8.01 mm (range, 6-40 mm), and 16 nodules were in the
anterior segment, 14 in the posterior segment, four in the lateral segment,
and three in the medial segment. Of the 37 nodules, eight had not been
previously treated (initial-treatment group). The remaining 29 nodules were
residual viable lesions after previous treatment (additional-treatment group).
Of these 29 nodules, three were local recurrences, whereas the other 26 were
the result of an inadequate safety margin taken during previous surgery, and
thus all required additional treatment. However, it is difficult to
distinguish by only sonography those HCC nodules that were previously treated
with one cycle of radiofrequency ablation from those that were not treated.
The following parameters were compared between the virtual sonographic
radiofrequency ablation group and the standard radiofrequency ablation group:
sex, age, cause, Child-Pugh class, tumor size, session number, and local
recurrence rate. Additional treatment was performed until an adequate safety
margin was achieved. Patients with severe coagulation disorders (prothrombin
activity < 40%, platelet count < 30,000/mL), severe cirrhosis
(Child-Pugh class C), extrahepatic malignancy, or tumor thrombus in the main,
left, or right portal trunk were excluded from this study. Patients were asked
to provide written informed consent to enter the study, which was approved by
the ethics committee of Ehime University.
Treatment—Before treatment, 15 mg of pentazocine
hydrochloride and 25 mg of hydroxyzine hydrochloride were administered
intramuscularly. Local anesthesia was induced by 5 mL of 1% lidocaine injected
through the skin into the peritoneum along a predetermined puncture line. We
inserted a 20-cm-long 17-gauge radiofrequency electrode equipped with a 2- or
3-cm-long exposed metallic tip (Cool-tip, Valleylab). First, abdominal CT was
performed and the location of the cancer nodule was ascertained
(Fig. 2A). Then, a virtual
sonogram of the CT scan was prepared from the data of the computer
(Fig. 2B). Finally, a
conventional sonographic image of the virtual sonographic image was prepared.
The location of the cancer nodules on the conventional sonographic image was
confirmed, and they were treated by radiofrequency ablation
(Fig. 2C). By measuring the
distance between the HCC nodule and the vessel (hepatic or portal vein) or the
surface of the liver on virtual sonography, we surmised the site of the HCC
nodule on conventional sonography. If the lung was obstructing the view of the
nodule, 500 mL of saline was injected into the right pleural cavity.
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Fig. 2C —72-year-old man with hepatocellular carcinoma. Construction of
virtual image of hepatocellular nodule. Conventional sonographic image of
B. Black arrowhead indicates cancer nodule; black and white arrows
indicate previously treated areas.
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Estimation of Therapeutic Effect
Dynamic CT was performed between 3 and 5 days after treatment. The necrotic
area of the HCC nodule and surrounding liver parenchyma was seen to be
hypoattenuating during the late phases of dynamic CT. If the necrotic area
depicted on posttreatment dynamic CT was larger than the viable area depicted
on pretreatment dynamic CT, the therapy was considered successful
[15]. If the size of the
necrotic area was almost identical to that of the tumor, additional treatment
was performed. Dynamic CT scans were repeated every 3 months thereafter.
-Fetoprotein and des--carboxy-prothrombin assays were performed
before treatment, 1 month after treatment, and every month subsequently.
Statistical Analysis
The data are expressed as mean ± SD. Statistical analysis was
performed using Student's t test for unpaired data, contingency table
analysis, and the Mann-Whitney U test as appropriate. A p
value of less than 0.05 was considered to represent statistical
significance.
Results
In Vitro Experience
In the in vitro experiment using gelatin gel, the puncture was performed 24
times, and six target lesions were made. The mean distance between the surface
of the gelatin gel and the lesion was 5.1 ± 2.2 cm (measured by CT).
The lesions were divided into two groups according to their depth from the
surface of the gelatin gel: a deep group (> 5 cm deep; mean, 7.0 ±
0.60 cm), and a surface group (< 5 cm deep; mean, 3.1 ± 0.40 cm).
The mean diameter of the target lesions made by contrast medium was 1.53
± 0.25 mm, and the mean distance between the surface of the target and
the tip of the needle was 1.20 ± 0.78 mm (Figs.
1A,
1B,
1C, and
1D). The mean distance was 0.92
± 0.67 mm for the surface group and 1.5 ± 0.80 mm for the deep
group. Although this difference was statistically significant, punctures
tended to be more accurate in the surface group (p = 0.06). These
results confirmed that the punctures assisted by virtual sonography in the
phantom model were accurate.
Clinical Experience
The shape of the liver, the vascular arrangement, and the surrounding
organs indicated that the slices identified by CT and sonography were
identical. We could construct virtual sonographic images identical to
conventional sonographic images for all lesions. No significant difference in
clinical profiles was found between virtual sonographic radiofrequency
ablation and standard radiofrequency ablation in either the initial-treatment
group or the additional-treatment group
(Table 1). In the
initial-treatment group, the mean number of virtual sonographic radiofrequency
ablation treatments was significantly lower (1.3 ± 0.49) than that of
standard radiofrequency ablation treatments (2.5 ± 0.76,
Table 2). In the
additional-treatment group, the mean number of virtual sonographic
radiofrequency ablation treatments was also significantly lower (1.2 ±
0.42) than that of standard radiofrequency ablation treatments (2.0 ±
1.1, Table 2). The local
recurrence rate did not differ significantly between the two initial-treatment
and additional-treatment groups (Table
2). Typical cases are presented in Figures
3A,
3B,
3C,
3D,
3E,
4A,
4B,
4C, and
4D. The patient represented in
Figures 3A,
3B,
3C,
3D, and
3E had an HCC nodule that was
too small to be visualized on conventional sonography in the initial
treatment. This lesion was depicted on virtual sonography and was shown to be
near the hepatic vein. Thus, only one puncture produced an adequate necrotic
area. The patient represented in Figures
4A,
4B,
4C, and
4D received additional
treatment. The nodule that was treated under virtual sonographic guidance was
near the necrotic area produced by previous radiofrequency ablation treatment,
and its visualization was affected by pulsation of the heart. Thus, this
nodule could not be detected clearly on conventional sonography but could be
detected on virtual sonography. Thus, one more radiofrequency ablation
treatment was performed, and after only one session an adequate necrotic area
was obtained.
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TABLE 1: Characteristics of Patients Treated with Virtual Sonographic
Radiofrequency Ablation and Standard Radiofrequency Ablation
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Fig. 3A —61-year-old man with hepatocellular carcinoma (maximum diameter, 6
mm) in superior anterior segment who received initial treatment.
Contrast-enhanced CT scan obtained before treatment shows low-attenuation area
(arrow).
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Fig. 3B —61-year-old man with hepatocellular carcinoma (maximum diameter, 6
mm) in superior anterior segment who received initial treatment. Reconstructed
virtual sonographic image shows branches of portal vein (black arrow)
and hepatic vein (black arrowheads), in addition to low-attenuation
area (white arrow) seen in A.
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Fig. 3C —61-year-old man with hepatocellular carcinoma (maximum diameter, 6
mm) in superior anterior segment who received initial treatment. Nodule was
not visualized clearly on conventional sonography; thus, same slice as in
B is revisualized on conventional sonography and nodule is punctured.
Arrow indicates portal vein; arrowheads indicate hepatic vein.
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Fig. 3D —61-year-old man with hepatocellular carcinoma (maximum diameter, 6
mm) in superior anterior segment who received initial treatment. After
puncture, CT scan shows that needle accurately hits target nodule.
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Fig. 3E —61-year-old man with hepatocellular carcinoma (maximum diameter, 6
mm) in superior anterior segment who received initial treatment. After
treatment, dynamic CT scan reveals completely necrotic area.
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Fig. 4A —71-year-old man with hepatocellular carcinoma who received
additional treatment. Contrast-enhanced CT scan obtained before treatment
showed high-attenuation area in lateral segment (black arrow). This
nodule was adjacent to necrotic area (white arrows), which had
previously undergone percutaneous ethanol injection.
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Fig. 4B —71-year-old man with hepatocellular carcinoma who received
additional treatment. Necrotic area is seen before treatment (white
arrows), but pulsation of heart prevents clear visualization of
nodule.
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Fig. 4C —71-year-old man with hepatocellular carcinoma who received
additional treatment. Reconstructed virtual sonographic image shows necrotic
area as hypoattenuating (white arrows) and target nodule as
hyperattenuating (black arrow). Puncture is performed at area of
hyperattenuation.
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For radiofrequency ablation using virtual sonography, mild complications of
pain and fever were noted, but no severe complications occurred. Neither
-fetoprotein nor des--carboxy-prothrombin was elevated in this
group, and no local recurrence took place.
Discussion
The sonographic B-mode method is most suitable for detecting nodules, and
thus most nonsurgical treatment for HCC has been performed under guidance by
sonography
[7-10].
With the progression of cirrhosis, echo signals in the liver become
heterogeneous, thereby preventing identification of the target HCC nodule on
conventional sonography. With conventional sonography, it has also been
difficult to determine the residual viable portion of HCC after treatment with
transcatheter arterial embolization, percutaneous ethanol injection,
radiofrequency ablation, or combinations thereof, because of the similar
appearances of necrosis and viable tumor tissue. However, sonographic
targeting for these therapies requires adequate visualization of the lesions.
If the lesion is not visualized on sonography but is visualized on CT, the
nodule can be depicted on virtual sonography. Thus, with use of virtual
sonography, HCC nodules not visualized clearly on conventional sonography can
be treated.
Previously, the puncture was performed in these cases under CT guidance
[16], CO2 hepatic
arteriography [17], or
contrast-enhanced sonography
[18-20].
Although it is possible to treat these cases under CT guidance, CT must be
performed several times during therapy by conventional means. On the other
hand, we performed CT only one time in patients who were treated under virtual
sonographic guidance. This CT was performed before the start of therapy. In
fact, several reports have described treatment performed by guided
contrast-enhanced sonography
[18-20].
Such imaging can reveal an enhanced residual lesion that was not visualized
with the conventional sonographic B-mode method. However, identifying the
safety margin may be difficult in some cases, as has been reported
[21-23].
Thus, treatment guided by contrast-enhanced sonography may not serve the
purpose in difficult cases. Moreover, HCC nodules on the liver surface or in
deep tissue may not be depicted on contrast-enhanced sonography.
We previously reported that virtual sonographic images reconstructed by
MDCT were effective in the treatment of HCC
[14]. HCC nodules that are not
visualized on conventional sonography but are visualized on dynamic CT can be
visualized on virtual sonography. In the present study, slices made by virtual
sonography were visualized again on conventional sonography, and then the site
of the target nodule on virtual sonography was punctured. First, a phantom
including modeled tumors that were not depicted by sonography and modeled
vessels, was produced. Referring to the virtual sonographic images, we
performed the punctures on the phantom. These punctures were shown to be
accurate, prompting us to believe that these images could be used in the
clinical setting. Thus, we punctured the HCC nodules in the patients and found
that with only one puncture, the needle had advanced with almost 100% accuracy
to all target nodules, indicating that this method had good efficacy. The
virtual sonographic image revealed an adequate site for puncture, and thus
virtual sonographic radiofrequency ablation was performed significantly fewer
times than was standard radiofrequency ablation in the initial-treatment
(p = 0.003) and additional-treatment (p = 0.003) groups.
Consequently, the length of hospital stay, number of CT examinations required
to estimate therapeutic efficacy, and cost are expected to decrease with use
of this procedure.
No local recurrence was seen in the virtual sonographic radiofrequency
ablation group. Furthermore, no major complications were noted in any
patients, indicating that this treatment is safe. In conclusion, in the
treatment of nodules not depicted on sonography, puncture assisted by virtual
sonography appears efficacious and safe.
Acknowledgments
We thank Teruhito Mochizuki, Seishi Kumano, Toyoaki Haraikawa, and Satoshi
Yamauchi (Department of Radiology, Ehime University School of Medicine) for
their cooperation.
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Top
Abstract
Introduction
