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1 Department of Internal Medicine, Division of Gastroenterology and Hepatology,
Kinki University School of Medicine, 377-2 Ohno-Higashi, Osaka-Sayama
589-8511, Japan.
2 Department of Surgery, Kinki University School of Medicine, Osaka-Sayama
589-8511, Japan.
Received May 9, 2003;
accepted after revision January 20, 2004.
Address correspondence to M. Kudo.
Abstract
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SUBJECTS AND METHODS. Twenty-one patients with 21 hepatocellular carcinomas prospectively underwent radiofrequency ablation treatment with contrast harmonic sonography as guidance. Twenty-five patients with 25 hepatocellular carcinomas were retrospectively selected as the historical control group under the same conditions as the study group; the control group patients were treated under B-mode sonography guidance.
RESULTS. Twenty (95.2%) of the 21 patients were successfully treated during a single treatment session, and the remaining patient (4.8%) required two treatment sessions with contrast harmonic guidance. On the other hand, only eight (32%) of the 25 control subjects were successfully treated during a single treatment session using B-mode sonographic guidance without contrast imaging. The difference between these two groups was statistically significant (p = 0.002).
CONCLUSION. Contrast harmonic sonography helps in the placement of radiofrequency ablation electrodes in hypervascular hepatocellular carcinomas that cannot be adequately depicted by B-mode sonography.
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Recently, contrast harmonic sonography has been shown to depict tumor vascularity sensitively and accurately [14–19]. Several studies have assessed the usefulness of this technique as a diagnostic tool and the therapeutic response of patients with hepatocellular carcinoma to transcatheter arterial embolization, percutaneous ethanol injection, and radiofrequency ablation therapy [17–19]. Contrast harmonic sonography can improve the detectability and localization of hypervascular hepatocellular carcinoma if the lesion cannot be adequately characterized on B-mode sonography. Therefore, contrast harmonic sonography can help to decrease the number of radiofrequency ablation treatment sessions in difficult cases. The purpose of this study was to clarify the usefulness of contrast harmonic sonography for guidance of radiofrequency electrode placement for treatment of hepatocellular carcinoma that cannot be adequately localized using B-mode sonography.
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Control group.—Twenty-five hepatocellular carcinoma nodules in 25 patients treated between January 1999 and August 2000 without the use of contrast harmonic sonography were retrospectively selected as the historical control group. None of these nodules could be adequately characterized by B-mode sonography, whereas they were well enhanced on dynamic CT. The control group included 19 men and six women (age range, 48–86 years; mean ± SD, 68.3 ± 6.9 years). The maximal diameter of hepatocellular carcinoma nodules ranged from 0.8 to 3.1 cm (1.7 ± 0.8 cm) on dynamic CT. Twelve hepatocellular carcinoma nodules in 12 patients had not previously been treated. Of these 12 nodules initially treated, 11 were not detected correctly on B-mode sonography because many large regenerated nodules were shown in cirrhotic livers, and the remaining nodule was not detected at all. On the other hand, 13 nodules were local recurrences after various percutaneous therapies (percutaneous ethanol injection, n = 10; microwave coagulation therapy, n = 3). Ten local recurrence nodules were not distinguished at all from viable lesions and necrotic lesions, and three nodules were detected but had indistinct margins. These 25 nodules were also treated with reference to the location in the CT images.
The ethics committee of our institution approved the study protocol. Written informed consent was obtained from all patients at the time of enrollment.
Equipment
The B-mode sonographic scans were obtained using a LOGIQ 700 Expert Series
unit (GE Healthcare) with a 2-4–MHz curved array wide-band transducer.
Coded phase-inversion harmonic sonography using a LOGIQ 700 Expert Series unit
was performed to depict hypervascular lesions. The acoustic power of coded
phase-inversion harmonic sonography was set at the default setting with a
mechanical index of 0.6–0.8.
The sonographic contrast agent used in this study was SH U 508A (Levovist, Schering). A total of 2.5 g of Levovist (400 mg/mL concentration) was injected manually through a 20-gauge canula into an antecubital vein.
The patients in this series were treated using a Cool-Tip needle radiofrequency system (Radionics). This system is a 480-kHz generator capable of producing a maximum power of 160 W through a 17-gauge monopolar cooled-tip needle electrode. Both the contrast harmonic sonographic guidance group and conventional B-mode guidance group were treated with the Cool-Tip radiofrequency system.
Technique of Harmonic Imaging-Guided Radiofrequency Ablation
After the plane of view was selected, B-mode sonography was adjusted to the
contrast harmonic imaging mode. Maintaining real-time imaging by slightly
changing the scanning plane, flash imaging, which is the simultaneous collapse
of accumulated microbubbles caused by a sonography pulse, was performed to
show the viable tumor parenchymal flow during the vascular phase that occurs
less than 2 min after injection of Levovist. The collapse of microbubbles in
viable hepatocellular carcinoma lesions is seen as white flashes on the
screen. Therefore, enhanced lesions could be used as a target for insertion of
a single radiofrequency electrode (Fig.
1A,
1B,
1C,
1D,
1E). Percutaneous insertion of
a radiofrequency electrode guided by real-time contrast harmonic sonography
should be performed within 2 min of injection of Levovist. After the enhanced
lesion was penetrated, each ablation was performed for a period of 12 min, as
recommended by the manufacturer. Additional contrast agent was injected when
we could not insert the radiofrequency needle because the hepatocellular
carcinoma lesions had become poorly enhanced after the previous injection. No
more than three vials of Levovist were given to any of the patients.
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Assessment of Treatment Effectiveness
Approximately 1 week after treatment, the treatment response was assessed
on the basis of three-phase dynamic CT findings (AQUILION, Toshiba). After
percutaneous radiofrequency ablation, areas of hypoattenuation, which were not
enhanced after contrast agent administration, were considered to be ablated
tissue, whereas enhanced tumor regions were considered to be residual foci of
tumor. We finished the treatment when the treated lesion showed a lack of
nodular enhancement and the distance from the ablated lesion margin to the
tumor edge remained more than 5 mm on dynamic CT. If the treatment was
incomplete, a second radiofrequency treatment session was performed within 1
week of the posttreatment CT assessment.
Analysis
The data are expressed as mean ± SD. Differences in the number of
treatment sessions were compared using the chi-square test for the two groups.
A p value of less than 0.05 was considered significant.
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The distance from the skin to the deepest edge of the tumor lesions ranged from 4.0 to 10 cm (6.2 ± 1.7 cm) in the contrast harmonic sonographic guidance group and from 3.0 to 10 cm (5.5 ± 1.9 cm) in the conventional B-mode guidance group. There were no significant differences between the groups (p = 0.272, Mann-Whitney U test).
Between September 2000 and June 2002, 405 patients with 485 hepatocellular carcinoma nodules were treated by radiofrequency ablation at our hospital. Hepatocellular carcinomas that were not well visualized on B-mode sonography accounted for 5.2% (n = 25) of the total nodules treated with radiofrequency ablation.
The number of treatment sessions of percutaneous radiofrequency ablation required for complete response in the contrast harmonic guidance group and in the control group was recorded. Complete tumor necrosis was achieved in a single session in 20 (95.2%) of the 21 lesions and two sessions of radiofrequency ablation were required for the remaining lesion (4.8%) in the group treated using contrast harmonic sonographic guidance. On the other hand, in the control group treated using conventional B-mode guidance, complete coagulation was achieved in a single session in only eight (32%) of the 25 lesions, two sessions in 11 lesions (44%), three sessions in four lesions (16%), and four sessions in two lesions (8%). Significantly fewer treatment sessions of radiofrequency ablation were required in cases with concurrent use of contrast harmonic sonography during the treatment in comparison with B-mode sonography guidance only (p = 0.002, chi-square test).
In the group treated using contrast harmonic sonographic guidance, six (24%) of the 25 patients received one vial of Levovist per session at first treatment. Ten patients (40%) received two vials of Levovist per session, and nine patients (36%) received three vials of Levovist per session. Four nodules in four patients were not enhanced.
No major complications occurred during and after radiofrequency ablation therapy in either group.
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Recently, sonographic hemodynamic imaging has been used to depict viable hepatocellular carcinoma lesions [14–19]. In our study, contrast harmonic sonography improved the efficiency of radiofrequency ablation for hepatocellular carcinoma nodules that were not clearly demarcated on B-mode sonography. Significantly fewer treatment sessions of radiofrequency ablation were needed in cases treated with concurrent use of harmonic sonography than in those in which only B-mode sonographic guidance was used (p < 0.05, chi-square test).
Another choice of imaging guidance for detection of hepatocellular carcinoma, which is hard to depict, is intraarterial injected CO2-enhanced sonography [20–22]. Some reports have shown that percutaneous ethanol injection guided by CO2-enhanced sonography is effective for identifying hypervascular hepatocellular carcinoma lesions that are not depicted by B-mode sonography [10, 22]. However, this technique requires angiographic procedures that are too complicated and invasive for routine clinical use. On the other hand, contrast harmonic sonography can be performed easily by repeated IV injection. Three vials of Levovist can be used at one time, as permitted by the manufacturer. Few drug toxicities have been reported; these being pain at the point of injection (3.0%), sense of heat (1.7%), and sense of cold (1.0%). However, our patients did not experience any drug toxicities.
Another choice of therapeutic method is CT-guided treatment [23–25]. CT-guided procedures are also effective in treating sonographically invisible hepatocellular carcinomas by visualizing them as spots of iodized oil (Lipiodol, Andre Guerbet) [23, 24]. Takayasu et al. [24] reported that the overall success rate in puncturing lesions that were not revealed by sonography was 94.4% (17/18 sessions). However, this method also requires arterial injection of iodized oil before CT-guided treatment. Radiofrequency ablation guided by contrast harmonic sonography is a minimally invasive therapy without radiation exposure.
The limitation of contrast harmonic sonography is that microbubble-based contrast agents such as Levovist are extremely sensitive and collapse easily when exposed to ultrasound pulse [26]. Maintaining real-time imaging in percutaneous radiofrequency ablation guided by contrast harmonic sonography could shorten the enhancement period. In many cases, the imaging time is too short to search and target the enhanced hepatocellular carcinoma nodule and insert a radiofrequency electrode into that enhanced lesion during real-time imaging on contrast harmonic sonography. There was another limitation when scanning wide lesions on contrast harmonic sonography at the same time. Although it was difficult to depict large hepatocellular carcinoma nodules, nodules smaller than 3 cm in diameter could be enhanced on contrast harmonic sonography in this study. However, new generations of sonographic contrast agents have been reported to be promising and currently are a growing area of sonography research [27, 28]. The newer contrast agents are expected to allow longer periods of enhancement so that radiofrequency ablation guided by contrast harmonic sonography is easier and more efficient.
In conclusion, percutaneous radiofrequency ablation guided by contrast harmonic sonography is an efficient approach for the treatment of hepatocellular carcinoma nodules that are not clearly demarcated by B-mode sonography in both untreated and locally recurrent hepatocellular carcinomas.
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