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Original Research |
1 Division of Gastroenterology and Hepatology, Department of Internal Medicine,
Kinki University School of Medicine, 377-2 Ohno-Higashi, Osaka-Sayama, Osaka
589-8511, Japan.
2 Department of Surgery, Kinki University School of Medicine, Osaka,
Japan.
Received September 2, 2007;
accepted after revision January 2, 2008.
Address correspondence to Y. Minami.
Abstract
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MATERIALS AND METHODS. One hundred one patients enrolled in the study were separated into two groups. Fifty-one patients with 65 hepatocellular carcinomas underwent prospective virtual CT sonography as guidance for radiofrequency ablation. Fifty patients with 63 hepatocellular carcinomas managed with B-mode sonographic guidance were retrospectively selected under the same conditions as the virtual CT sonography group to act as a historical control group.
RESULTS. In the virtual CT sonography group, technically successful ablation was achieved in a single session in 92% (47/51) of the patients and in two sessions in 8% (4/51). In the B-mode sonography group, technical success was achieved in a single session in 72% (36/50) of the patients, in two sessions in 24% (12/50), and in three sessions in 4% (2/50). Treatment analysis showed that the technical success rate after a single treatment session was significantly (p = 0.017) higher for the virtual CT sonography group. The number of treatment sessions was significantly (p = 0.021) lower for the virtual CT sonography group (mean, 1.1 ± 0.1 vs 1.3 ± 0.3 sessions).
CONCLUSION. Virtual CT sonographically assisted radiofrequency ablation is an efficient treatment of patients with hepatocellular carcinoma that is poorly defined on B-mode sonography.
Keywords: hepatocellular carcinoma • magnetic navigation • radiofrequency ablation • virtual CT sonography
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A virtual CT sonographic visualization system has been introduced to the clinical practice of hepatology as the result of development of 2D multiplanar reconstruction (MPR) and a magnetic navigation system. Advances in volumetric image acquisition capabilities with MDCT and computer graphics have led to remarkable improvements in spatial resolution and interactive 3D image-processing techniques [8-14]. Cross-sectional MPR images of the liver from almost isovoxel volume data can be used for virtual sonographic visualization [15-17]. With the magnetic navigation system, a magnetically enabled wire tip can be pointed in any orientation [18-22], producing 3D images and integrating information with that from MDCT. This 3D information can be superimposed on electrophysiologic results [18, 19], used in neurosurgery [20, 21], and used in interventional cardiology [22]. Virtual CT sonography with magnetic navigation can show any cross-sectional image of CT volume data in real time corresponding to the angle of the transducer in the magnetic field. In this study, we evaluated the value of virtual CT sonography for radiofrequency ablation of hepatocellular carcinoma not clearly visualized with B-mode sonography.
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Patients
All patients met the following criteria for treatment with percutaneous
radiofrequency ablation: presence of a viable hepatocellular carcinoma in the
liver with a maximum diameter not greater than 3 cm, percutaneous
accessibility of the tumor, absence of portal venous and extrahepatic
metastasis, presence of liver cirrhosis (Child-Pugh A or B), prothrombin time
ratio greater than 50%, total bilirubin concentration less than 3.0 mg/dL, and
platelet count greater than 50,000/µL. We diagnosed hepatocellular
carcinoma on the basis of the findings on three-phase contrast-enhanced CT.
Hepatocellular carcinomas became enhanced in the arterial phase, and washout
occurred in the portal venous or equilibrium phase of contrast-enhanced CT.
All patients underwent contrast-enhanced CT 1 month before radiofrequency
ablation.
Between September 2005 and February 2006, 51 patients with 65 hepatocellular carcinomas, the nodules of which became enhanced in the arterial phase of dynamic CT but were not well visualized with conventional B-mode sonography, were prospectively enrolled in this study. The patient population included 42 men and nine women (mean age, 66.2 ± 7.2 [SD] years; range, 45-82 years). The mean maximal diameter of the tumors was 1.6 ± 0.6 cm (range, 1.0-3.0 cm) on dynamic CT. Fifty-eight (89%) of the hepatocellular carcinoma nodules had not been previously treated. The other seven (11%) nodules were local tumor progression after various therapies (per cutaneous radiofrequency ablation in three cases, percutaneous ethanol injection in two cases, transcatheter chemoembolization in two cases). Forty-three patients with hepatocellular carcinoma had cirrhosis of the liver, Child-Pugh class A; the other eight patients had Child-Pugh class B cirrhosis.
We retrospectively analyzed the cases of a historical control group of 50 patients who had been treated with radiofrequency ablation before the introduction of real-time virtual CT sonography to our hospital. These patients had 63 hepatocellular carcinoma nodules and were treated with radiofrequency ablation between January 2005 and July 2005. The recruitment conditions were the same as those for the virtual CT sonography group. This control patient population included 42 men and eight women (mean age, 66.6 ± 7.0 years; range, 50-80 years). The mean maximal tumor diameter was 1.7 ± 0.6 cm (range, 1.0-3.0 cm) on dynamic CT. Fifty-five (87%) of the hepatocellular carcinomas had not been previously treated. The other eight (13%) nodules were local tumor pro gression after various percutaneous therapies (per cutaneous radiofrequency ablation in four cases, transcatheter chemoembolization in four cases, percutaneous ethanol injection in two cases). These 63 nodules were managed under sonographic guidance with the conventional radio frequency ablation method. Forty-five patients with hepatocellular carcinoma had liver cirrhosis, Child-Pugh class A; the other five patients had Child-Pugh class B cirrhosis.
Equipment and Techniques
B-mode sonography (EUB 8500 unit, Hitachi Medico) was performed with a
3.5-MHz curved-array transducer. The virtual CT sonographic system was
composed of a main unit (EUB 8500), the body of the magnetic location detector
unit, a magnetic field generator, and a magnetic sensor attached to the
sonographic transducer. This generator produced an interacting magnetic field
yielding an approximately spherical 70-cm uniform magnetic field of 0.03
T.
All radiofrequency ablations were performed percutaneously by one of five experienced hepatologists, each of whom had more than 6 years of experience in sonographically guided interventional procedures and radiofrequency ablation. The treatments were performed with local anesthesia and conscious sedation. Conscious sedation was induced with 5-20 mg of diazepam. Local infiltration anesthesia was induced with 5-15 mL of 1% lidocaine (Liduokayin, Yimin). The patients were conscious when the electrode was placed. Vital signs, including blood pressure, heart rate, and oxygen saturation, were continuously monitored during the procedure.
Patients in both groups were treated with a cooled-tip needle radiofrequency ablation system (Cool-tip, Covidien), which is a 480-kHz alternative current generator that can produce a maximum power of 180 W through a 17-gauge monopolar cooled-tip needle electrode. A thermocouple embedded in the electrode ensures that the temperature at the tip of the needle is constantly monitored. The radiofrequency electrode temperature was maintained at less than 18°C by application of circulating chilled (0°C) saline solution to the cannula sheath [23]. We selected a single 2-cm exposed tip for nodules smaller than 2 cm in diameter and a single 3-cm exposed tip for larger nodules.
CT images were obtained with a 4-MDCT scanner (Aquilion, Toshiba) at 3.0-mm slice thickness, 15-mm table speed per rotation, and 0.5-mm/s gantry rotation time with inspiration breath-hold. Triple-phase contrast-enhanced CT scans were obtained 45, 60, and 180 seconds after initiation of contrast injection for acquisition of the hepatic arterial, portal venous, and equilibrium phase images. A total of 100 mL of nonionic contrast material containing 300 mg I/mL (iomeprol, Iomeron, Eisai) was injected IV with an automatic power injector at a rate of 3 mL/s.
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Virtual CT sonography displayed the image corresponding to the movement of the transducer in the magnetic field. Thus we saw synchronous images from virtual CT sonography and B-mode sonography side by side on the sonographic monitor (Figs. 3A, 3B, 3C and 3D). A smooth virtual CT sonographic image was obtained with a display of 256 x 256 pixel at 10 frames/s. If the images showed a gap between virtual CT sonography and B-mode sonography, we adjusted the view. We searched the view of the umbilical portion or the right portal vein on virtual CT sonography using the sonographic transducer. After we had fixed this image, we released the virtual CT sonographic image with the corresponding B-mode sonographic image. As the procedures were repeated, we adjusted the virtual CT sonographic images to the B-mode sonographic images.
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Assessment of Treatment Response
A few days after treatment, the technical success of ablation was assessed
on the basis of findings on three-phase contrast-enhanced CT scans. A tumor
was considered successfully ablated when no enhanced region was detected
either within the entire tumor in the arterial phase or in a 0.5- to 1.0-cm
margin of apparently normal hepatic tissue surrounding the tumor in the portal
phase. Part of the tumor was diagnosed as remaining viable when images of the
ablated area showed nodular peripheral enhancement
[23]. The residual portion was
managed with additional radiofrequency ablation within a few days of
posttreatment CT assessment. We repeated radiofrequency ablation therapy until
technical success was achieved in a single hospital stay.
Statistical Analysis and Follow-Up
Data were expressed as mean ± SD. Differences in clinical
characteristics between the two groups were compared by use of chi-square and
unpaired Student's t tests. For assessment of therapeutic efficacy,
the number of treatment sessions was compared between the two groups by use of
unpaired Student's t tests. A value of p < 0.05 was
considered significant. If 1-month follow-up CT images showed successful
ablation and no new tumors, three-phase contrast-enhanced CT scans were
repeated at 3-month intervals. All patients participated in follow-up for at
least 6 months after radiofrequency ablation and underwent at least two
follow-up CT examinations. Various complications were recorded.
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Between September 2005 and February 2006, 159 patients with 198 hepatocellular carcinoma nodules were treated by radiofrequency ablation at our hospital. Virtual CT sonographically assisted radiofrequency ablation for hepatocellular carcinoma accounted for 32.1% (51/159) of the overall cases of radiofrequency ablation. Rates of technically successful ablation after a single session were significantly higher for the virtual CT sonography group than for the B-mode sonography group (p = 0.017, Fisher's exact test). In the virtual CT sonography group, technically successful ablation was achieved in a single session in 47 (92%) of 51 patients; two sessions were needed for four (8%) of the patients. The average number of treatment sessions was 1.1 ± 0.3. In the B-mode sonography group, complete tumor necrosis was achieved in a single session in only 36 (72%) of 50 patients; two sessions were needed for 12 (24%) and three sessions for two (4%) of the patients. The average number of treatment sessions was 1.3 ± 0.6. Among four patients with four hepatocellular carcinomas in the virtual CT sonography group who received incomplete treatment at the first session, two tumors were located in segment VII of the liver and one each in segments VI and VIII. Two nodules were local tumor progression after percutaneous radio frequency ablation and transcatheter chemo embolization, and the other two nodules had not been previously treated.
The mean follow-up time was 10.7 ± 4.2 months (range, 2-18 months) for the virtual CT sonography group and 10.8 ± 6.6 months (range, 3-22 months) for the B-mode sonography group. During the follow-up period, two (3%) of the patients in the virtual CT sonography group and two (3%) in the B-mode sonography group had local tumor progression. There was no significant difference in local tumor progression between the groups (p = 0.98, Fisher's exact test). No serious side effects or procedure-related complications (hemorrhage, infection, needle track seeding, hepatic failure, or death) occurred in the CT sonography group. One case of pleural hemorrhage occurred in the B-mode sonography group.
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Magnetic guidance was first used in humans in 1991 for neonatal heart catheterization for the diagnosis of anomalous congenital cardiac drainage [25]. The procedure was based on 3D reconstruction of the vessel lumen from standard angiographic images. Knowledge of the positions of the table and image intensifier during angiography allowed calculation of the vessel coordinates in real space within the patient's chest. As a result, the current magnetic navigation system received regulatory approval for human clinical use in cardiac electrophysiology and interventional cardiology [18].
Our results indicate that percutaneous radiofrequency ablation assisted by virtual CT sonography is a safe procedure and is effective in patients with hepatocellular carcinoma even though the nodules are poorly defined on B-mode sonography. An overall complete tumor response was achieved in all of the patients in an average of 1.1 treatment sessions. A single radiofrequency ablation led to complete tumor response in 90.2% of the patients. Treatment analysis showed a statistically higher success rate in the first treatment session with virtual CT sonographic assistance than with conventional B-mode sonographic guidance. These results reflect correct targeting of ablation with the imaging technique, even though the conditions for percutaneous ablation of hepatocellular carcinoma nodules were difficult in that the nodules were not clearly demarcated with B-mode sonography. Therefore, virtual CT sonography assistance can improve the technical success of radiofrequency ablation of hepatocellular carcinoma nodules not well visualized with conventional B-mode sonography.
Virtual CT sonography with magnetic navigation has three important features for clinical application in radiofrequency ablation therapy. The first is compatibility. We easily compared the virtual CT sonographic images with B-mode sonographic images because the sonographic monitor showed them side by side. The second feature is swift response. With a powerful computer, any MPR cross sections can correspond in real time to the angle of the transducer in the magnetic field. Therefore, enhanced tumors and portal veins on virtual CT sonography can be displayed smoothly for each movement of the transducer. The third feature is synchronicity. This guidance technique is based on immediate feedback to point out small hepatocellular carcinoma nodules that cannot be clearly visualized with B-mode sonography. Therefore, assisted by virtual CT sonography, we were able to insert the radiofrequency electrode into these small nodules seen on B-mode sonography.
In four hepatocellular carcinomas in four patients in the virtual CT sonography group, tumor ablation was incomplete after the first treatment session. Ablations might have been incomplete because virtual CT sonography did not show images coincident with the B-mode sonographic images, making view adjustment difficult. Imaging incompatibility might have occurred because the depths of breath-holds at CT and sonographic examination varied. The difference also increases with an increase in distance between the magnetic sensor attached to the transducer and the magnetic generator. Therefore, incomplete first ablation might have been the result of a large distance between the transducer and the magnetic generator during intercostal examination of patients with hepatocellular carcinoma in the right lobe.
Virtual CT sonography is expected to be useful to patients with hepatic metastasis. The borders of metastatic nodules in the liver frequently are not clear on B-mode sonography because of the lack of a tumor capsule [26] and because of cellular infiltration of metastatic lesions [27]. In many cases, it is difficult to differentiate viable metastatic hepatic tumors from necrotic tissue on B-mode sonography after local ablation therapy. Therefore, local progression of metastatic hepatic tumors after ablation therapy may be effectively targeted with this method. In patients with metastatic hepatic tumors, late arterial phase CT scans can show pale tumor enhancement and clear tumor borders on liver tissue. As for hepatocellular carcinoma, late arterial phase CT scans may be available for MPR of virtual CT sonographic images during radiofrequency ablation of metastatic hepatic tumors.
The sonography unit in the virtual sonography system is standardized in the DICOM format, which is a standard format for clinical CT, MRI, and sonography and is the protocol for communication between clinical imaging machines. With the DICOM standard, digital images from multiple techniques performed by multiple units in a hospital can be transmitted through the local area network. Therefore, not only CT but also MRI can be used for virtual sonography if formatted with DICOM. Virtual sonography with MRI might be available for patients with an allergy to CT contrast medium. The contrast enhancement of tissue on MRI can be visualized more clearly than that of CT without contrast medium. For example, MRI can be used to differentiate viable hepatic malignant tumors with necrosis due to previous ablation therapy. On T2-weighted MRI, there has been a significant association between hypervascular hepatocellular carcinoma and nodule signal intensity [28, 29].
Contrast harmonic sonography with an IV contrast agent has depicted intratumoral microscopic flow sensitively and accurately [30]. It also has been recognized [31, 32] as useful for assessing the therapeutic response to transcatheter arterial chemoembolization and radiofrequency ablation therapy in patients with hepatocellular carcinoma. Small hypervascular hepatocellular carcinomas can be evaluated with contrast-enhanced harmonic sonography even when tumors are not adequately characterized with B-mode sonography. It has been reported [33] that contrast-enhanced harmonic sonography with SH U 508A (Levovist, Bayer Schering Pharma AG) is useful guidance of percutaneous local ablation therapy for hepatocellular carcinoma poorly depicted with conventional B-mode sonography. However, microbubble-based contrast agents such as SH U 508A can collapse easily when exposed to the sonographic pulse.
Maintaining real-time imaging during contrast-enhanced harmonic sonography for guidance of radiofrequency ablation should shorten the enhancement period. Skill is required because the imaging time of contrast harmonic sonography is too short for a search for the enhanced hepatocellular carcinoma nodule and insertion of a radiofrequency electrode. On the other hand, second-generation sonographic contrast agents, such as aqueous suspension of phospholipid-stabilized microbubbles filled with sulfur hexafluoride (SonoVue, Bracco) and perfluorobutane microbubbles (Sonazoid, Amersham) consist of shelled microbubbles and are strongly echogenic in a wide range of frequencies and acoustic pressures [34, 35]. They can be used with conservative contrast bubble-specific imaging methods. The therapeutic effects of radiofrequency ablation performed with CT sonographic guidance should be compared with those of ablation performed with contrast-enhanced harmonic sonographic guidance with a second-generation contrast medium.
The virtual CT sonography system has potential for other clinical uses, such as evaluating therapeutic response to radiofrequency ablation and transcatheter arterial chemoembolization. Axial CT images are often used for this purpose [36, 37], and MPR images can show multiple cross sections. With virtual CT sonography, it may be straightforward to show the sagittal or coronal view of MPR images according to the angles of the transducer. Virtual sonographic images with installed CT images obtained after radiofrequency ablation may be useful for more accurate evaluation of treatment response than can be performed with axial CT images alone.
The principal limitation of this study was the nonrandomized and retrospective design, which inherently decreased the statistical strength. Another limitation was the preliminary nature and therefore the relatively small number of patients. Further prospective randomized studies of this technique with a large number of patients are warranted.
Real-time virtual CT sonography can show the 3D relations between the hepatic vasculature and tumors. The results of this study show the safety and feasibility of real-time virtual CT sonographic guidance of percutaneous radiofrequency ablation in patients with hepatocellular carcinoma even though the nodules are poorly defined on B-mode sonography.
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