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Contrast Harmonic Sonography-Guided Radiofrequency Ablation Therapy Versus B-Mode Sonography in Hepatocellular Carcinoma: Prospective Randomized Controlled Trial

¹ Division of Gastroenterology and Hepatology, Department of Internal Medicine, Kinki University School of Medicine, 377-2 Ohno-Higashi, Osaka-Sayma, Osaka 589-8511, Japan.
² Department of Radiology, Kinki University School of Medicine, Osaka 589-8511, Japan.
³ Department of Surgery, Kinki University School of Medicine, Osaka 589-8511, Japan.

Received August 10, 2005; accepted after revision March 30, 2006.

 
Address correspondence to Y. Minami (minkun{at}med.kindai.ac.jp).

Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
OBJECTIVE. The purpose of this study was to evaluate the effectiveness of contrast harmonic sonographic guidance in radiofrequency ablation of locally progressive hepatocellular carcinoma poorly depicted with B-mode sonography.

SUBJECTS AND METHODS. A series of 40 patients with hepatocellular carcinoma with local tumor progression poorly depicted with B-mode sonography were randomly treated with radiofrequency ablation guided by either contrast harmonic sonography (n = 20) or conventional B-mode sonography (n = 20). Unpaired Student's t tests were performed to compare numbers of treatment sessions.

RESULTS. Treatment analysis showed that the complete ablation rate after a single treatment session was significantly higher in the contrast harmonic sonography group than in the B-mode sonography group (94.7% vs 65.0%; p = 0.043) and that the number of treatment sessions was significantly lower in the contrast harmonic sonography group (mean, 1.1 ± 0.2 vs 1.4 ± 0.6; p =0.037).

CONCLUSION. Contrast harmonic sonography-guided radiofrequency ablation is an efficient technique for guiding further ablation of local tumor progression not clearly demarcated with B-mode sonography.

Keywords: contrast harmonic sonography • hepatobiliary imaging • hepatocellular carcinoma • percutaneous ablation • radiofrequency ablation

Introduction

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Radiofrequency ablation has received increasing attention and is considered safe and effective for management of small hepatocellular carcinomas (HCCs) and other malignant hepatic tumors [1-6]. However, multiple sessions of radiofrequency ablation therapy are needed for locally progressive HCC because it is frequently difficult to differentiate viable tumors from necrotic tissue on B-mode sonography [7]. CT fluoroscopy-guided and CO₂-enhanced sonography-guided procedures have been shown effective in the management of hypervascular HCC poorly depicted with B-mode sonography [8-10]. However, these methods may not always be available in routine clinical practice and increase exposure to radiation when multiple CT scans are needed. In addition, methods that involve angiographic procedures are invasive.

Contrast harmonic sonography with an IV contrast agent has been found sensitive and accurate in the depiction of tumor vascularity in real time [11-14] and is considered useful for assessing the therapeutic response to transcatheter arterial chemoembolization (TACE) and radiofrequency ablation therapy in patients with HCC [15-19]. Contrast harmonic sonography can be used to evaluate small hypervascular HCC even when tumors cannot be adequately characterized with B-mode sonography. Contrast harmonic sonography-guided percutaneous local ablation therapy has been found useful in the management of HCC poorly depicted with conventional B-mode sonography [20-22], but the studies were not controlled or randomized. Our randomized controlled trial was conducted to assess the therapeutic efficacy and safety of contrast harmonic sonography for radiofrequency electrode placement in the management of HCC poorly localized with B-mode sonography.

Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Patient Selection and Eligibility
The ethics committee of our institution approved the study protocol. Written informed consent was obtained from all patients at the time of enrollment. Between January 2002 and May 2003, 40 patients (37 men, three women; age range, 51-87 years; mean age, 67 years) with local tumor progression of 40 HCCs were consecutively enrolled in the study. Nodules were enhanced on contrast-enhanced CT but were not clearly depicted on conventional B-mode sonography because differentiation of necrotic tissue from residual tumor tissue is a limitation of the method. The subjects were randomized into two groups by computer-generated allocation with instructions in sealed envelopes to treat equal numbers of patients with radiofrequency ablation guided by contrast harmonic sonography (n = 20) and conventional B-mode sonography (n = 20).

All patients met the following criteria for treatment with percutaneous radiofrequency ablation: local tumor progression of HCC after intended curative treatment such as radiofrequency ablation or selective TACE, presence in the liver of viable HCC 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 class A or B), prothrombin time ratio greater than 50%, and platelet count greater than 50,000/µL.

Local progression of HCC was diagnosed on the basis of findings on three-phase contrast-enhanced CT. The locally progressive HCCs were adjacent to tumor tissue necrotic as the result of previous therapy and were positively enhanced during the arterial phase and washed out during the equilibrium phase of contrast-enhanced CT (Fig. 1A, 1B, 1C, 1D).

View larger version (159K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A —71-year-old man with 2.0-cm local progression of hepatocellular carcinoma after intraoperative radiofrequency ablation therapy for large hepatocellular carcinoma in right hepatic lobe. Early-phase dynamic CT scan shows outgrowth pattern of locally progressive hepatocellular carcinoma (arrow) in right hepatic lobe. Lesion borders on unenhanced area, which was previously treated.

View larger version (78K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B —71-year-old man with 2.0-cm local progression of hepatocellular carcinoma after intraoperative radiofrequency ablation therapy for large hepatocellular carcinoma in right hepatic lobe. Contrast harmonic sonogram shows enhancement of viable focus of hepatocellular carcinoma (arrow).

View larger version (92K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C —71-year-old man with 2.0-cm local progression of hepatocellular carcinoma after intraoperative radiofrequency ablation therapy for large hepatocellular carcinoma in right hepatic lobe. Contrast harmonic sonogram shows radiofrequency electrode needle (arrows) inserted into viable focus of hepatocellular carcinoma.

View larger version (163K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D —71-year-old man with 2.0-cm local progression of hepatocellular carcinoma after intraoperative radiofrequency ablation therapy for large hepatocellular carcinoma in right hepatic lobe. Early-phase dynamic CT scan obtained 2 days after radiofrequency ablation therapy shows tumor and surrounding area are not enhanced, indicating complete necrosis.

Patients in both groups were treated with a cooled-tip needle radiofrequency system. The cooled-tip needle radiofrequency system is a 480-kHz alternating current generator that can produce 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. Radiofrequency electrode temperature was maintained below 18°C by circulation of chilled saline solution (0°C) to its cannula sheath [23].

MDCT (Aquillion, Toshiba) was used for diagnosis. Three-phase contrast-enhanced CT scans were obtained 30, 60, and 180 seconds after initiation of the injection of contrast medium with a 7.0-mm slice thickness to obtain hepatic arterial, portal venous, and equilibrium phase images, respectively. A total of 100 mL of nonionic contrast material containing 300 mg I/mL (iomeprol, Iomeron, Eisai) was injected IV at a rate of 3 mL/s with use of an automatic power injector.

Contrast Harmonic Sonography-Guided Radiofrequency Ablation
After the plane of view was selected, B-mode sonography was adjusted to the contrast harmonic imaging mode in the contrast harmonic sonography group. White flashes on the screen, which represent simultaneous collapse of accumulated microbubbles produced by the sonographic pulse, were used to show viable HCC parenchymal flow during the vascular phase. This phenomenon occurs less than 2 minutes after bolus injection of SH U 508A while real-time imaging is maintained by changes in the scanning plane and enables continuous visualization of the contrast signal (Figs. 1B and 2B). Therefore, an enhanced tumor was identified as a target for insertion of a single radiofrequency electrode in real time [20] (Figs. 1C and 2C). After the enhanced tumor was penetrated by the radiofrequency electrode guided by real-time contrast harmonic sonography, each ablation was performed for a period of 12 minutes, as recommended by the manufacturer. Additional contrast agent was injected if tumors were poorly enhanced after the previous injection. No more than three vials of SH U 508A were given to any patient. In the B-mode sonography group, the location for insertion of the radiofrequency electrode to be guided by B-mode sonography was determined according to CT information. All radiofrequency ablations were performed percutaneously by one of three hepatologists with 8, 7, and 7 years of experience in sonography-guided interventional procedures and radiofrequency ablation.

View larger version (125K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B —69-year-old man with 1.5-cm local tumor progression of hepatocellular carcinoma after percutaneous radiofrequency ablation in segment VIII of liver. Contrast harmonic sonogram shows enhancement of viable focus of hepatocellular carcinoma (arrow).

View larger version (136K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C —69-year-old man with 1.5-cm local tumor progression of hepatocellular carcinoma after percutaneous radiofrequency ablation in segment VIII of liver. Contrast harmonic sonogram shows radiofrequency electrode needle (arrows) inserted into viable hepatocellular carcinoma.

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. To assess therapeutic efficacy, the numbers of treatment sessions and CT findings for evaluation of treatment response were compared between the two groups by use of unpaired Student's t tests. Statistical significance was considered p < 0.05. If 1-month follow-up CT images showed successful ablation and no new tumors, three-phase contrast-enhanced CT was repeated at 3-month intervals. All patients underwent follow-up for at least 6 months after radiofrequency ablation and underwent at least two follow-up CT examinations. The various complications were recorded.

Results

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Characteristics (age, sex, size of local tumor progression, and previous treatments) did not differ significantly between patients in the contrast harmonic sonography and the B-mode sonography groups (Table 1). The mean sizes of local tumor progression and the entire tumor (local tumor progression plus necrotic tumor tissue) ranged from 1.2 to 1.3 cm and from 3.0 to 3.3 cm, respectively, for the two groups.

Two patterns of local tumor progression on contrast-enhanced CT were categorized as either enhanced tissue within the edge of the treated nodule on arterial phase images or enhanced tissue around the treated nodule but continuous with its border on arterial phase images [25]. The first pattern (designated ingrowth) was identified in no tumor managed with radiofrequency ablation, one tumor managed with percutaneous ethanol injection, and four tumors managed with TACE. The second pattern (designated outgrowth) was identified in 22 tumors managed with radiofrequency ablation, one tumor managed with percutaneous ethanol injection, and 11 tumors managed with TACE. In the contrast harmonic sonography group, local tumor progression consisted of seven tumors with the ingrowth pattern and 12 with the outgrowth pattern. In the B-mode sonography group, local tumor progression consisted of five tumors with the ingrowth pattern and 15 with the outgrowth pattern.

Only one insertion was needed for each treatment session in all patients. One patient with HCC in the contrast harmonic sonography group, however, was not treated because tumor enhancement was not obtained. The other 19 patients underwent percutaneous radiofrequency ablation guided by contrast harmonic sonography. Among the 19 cases of locally progressive HCC in the contrast harmonic sonography group, in 15 nodules there was no distinction with regard to viable HCC and necrotic tissue on B-mode sonography; four nodules without distinct margins were detected on B-mode sonography. Among the 20 cases of locally progressive HCC in the B-mode sonography group, in 17 cases there was no distinction with regard to viable tumor and necrotic tumor tissue; three nodules without distinct margins were detected on B-mode sonography.

View larger version (148K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A —69-year-old man with 1.5-cm local tumor progression of hepatocellular carcinoma after percutaneous radiofrequency ablation in segment VIII of liver. Early-phase dynamic CT scan shows outgrowth pattern of local tumor progression of hepatocellular carcinoma as enhanced lesion (arrow) between unenhanced warped area, which was previously treated.

View larger version (147K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2D —69-year-old man with 1.5-cm local tumor progression of hepatocellular carcinoma after percutaneous radiofrequency ablation in segment VIII of liver. Early-phase dynamic CT scan obtained 3 days after radiofrequency ablation therapy shows tumor and surrounding area are not enhanced.

One patient in the contrast harmonic sonography group who had incomplete treatment at the first session was identified as having the outgrowth pattern from previous treatment with radiofrequency ablation. Among seven patients with incomplete treatment at the first session in the B-mode sonography group, six tumors had an outgrowth pattern from previous treatment by radiofrequency ablation and one tumor had the ingrowth pattern from previous treatment by TACE.

In the contrast harmonic sonography group, in six (32%) of the 19 patients one vial of SH U 508A per session was used for the first treatment. Two vials per session were used in 10 (53%) of the patients, and three vials were used in three (16%) of the patients.

Follow-up time ranged from 4 to 34 months (21.5 ± 7.7 months) in the contrast harmonic sonography group and from 4 to 32 months (19.4 ± 7.5 months) in the B-mode sonography group. During the follow-up period, two (10.5%) of the patients in the contrast harmonic sonography group and two patients (10%) in the B-mode sonography group had local tumor progression (p = 0.96, Fisher's exact test).

No serious side effects or procedure-related complications (e.g., hemorrhage, infection, needle track seeding, hepatic failure, or death) occurred in either of the radiofrequency ablation groups. Pain and fever were the most common side effects in both groups (n =5, contrast harmonic sonography group; n =6, B-mode sonography group). All of these symptoms were controlled; no procedure was discontinued in any of the cases. Pleural effusion (n =1, B-mode sonography group) and ascites (n =1, contrast harmonic sonography group; n =1, B-mode sonography group) without symptoms occurred in a small number of patients and spontaneously resolved. The rate of complications did not differ significantly between groups (p = 0.71, Fisher's exact test).

Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Sonographic hemodynamic imaging with sonographic contrast agents has been used to differentiate viable tumor from necrotic tumor tissue [15-18]. Specifically, coded phase-inversion harmonic sonography is an advanced technique in which phase- or pulse-inversion harmonic imaging is used with coded technology that entails amplifying weak microbubble signals and suppressing tissue signals by transmitting coded pulse sequences and decoding them on receipt [26, 27]. Focal vascularity can be regarded as indicating viability of HCC with high sensitivity and accuracy in real time [28]. In our study, 95% (19/20) of HCC nodule enhancement was shown in the contrast harmonic sonography group. Using real-time observation of the vascular phase, the operators selected the location at which percutaneous radiofrequency ablation should be performed. However, one deeply located HCC nodule was not readily enhanced with this method. Most false-negative nodules detected with SH U 508A were located more than 7 cm from the abdominal wall because sonography does not have strength or sensitivity for detection of nodules at that distance [12].

In the current prospective randomized study, complete treatment response was achieved with an average of 1.1 treatment sessions in the contrast harmonic sonography group and an average of 1.4 treatment sessions in the B-mode sonography group. Thus, treatment analysis showed a statistically higher success rate in the first treatment session with contrast harmonic sonography than with conventional B-mode sonographic guidance. Contrast harmonic sonographic guidance improves the therapeutic efficiency of radiofrequency ablation for HCC nodules not clearly demarcated with B-mode sonography.

In eight study patients from both groups, tumor ablation was incomplete at the first treatment session; all had an outgrowth pattern from previous radiofrequency ablation. In all patients with the ingrowth pattern, ablation was complete at the first treatment session. Thus, it may be easier to manage locally progressive HCC with an ingrowth pattern than that with an outgrowth pattern with percutaneous radiofrequency ablation. Conventional B-mode sonography showed the presence of four lesions in the area after radiofrequency ablation: local tumor progression, ablated tumor, ablated normal liver tissue, and unablated liver tissue. This method, however, showed three areas after TACE: local tumor progression, tumor necrosis, and normal liver tissue. In the patients with an outgrowth pattern of local tumor progression, that extra lesion on B-mode sonography might have made it difficult to select for new radiofrequency ablation.

Solbiati et al. [15, 29] reported that contrast-enhanced sonography can be used to monitor the extent of radiofrequency ablation in the same treatment session. They used contrast-enhanced sonography immediately at the end of radiofrequency ablation procedures to assess the therapeutic result. The rate of partially unablated tumors after radiofrequency ablation decreased from 16.1% to 5.9%. In our study, use of contrast harmonic sonography immediately before radiofrequency needle insertion increased treatment efficiency.

There were limitations to this study. First, HCCs larger than 3 cm in diameter were excluded. However, contrast harmonic sonographic guidance is expected to be useful in the radical management of large HCCs even if complete necrosis is not attained at initial radiofrequency ablation. Small residual foci of untreated tumors may be treated with contrast harmonic sonographic guidance in second or subsequent sessions. Second, not all patients in either group underwent approximately 20 months of follow-up. However, there was no difference in the local tumor progression rate between groups during the follow-up period.

In conclusion, contrast harmonic sonographic guidance is an efficient approach to radiofrequency ablation of HCC nodules that are not clearly demarcated with B-mode sonography, particularly in the case of local tumor progression of HCC.

Acknowledgments
 
We thank Toyokazu Fukunaga, Tatsuo Inoue, and Kiyoshi Maekawa for technical assistance.

References

Top Abstract Introduction Subjects and Methods Results Discussion References

 

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This Article Abstract Figures Only Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Minami, Y. Articles by Shiozaki, H. Search for Related Content PubMed PubMed Citation Articles by Minami, Y. Articles by Shiozaki, H. Social Bookmarking                      What's this? Hotlight (NEW!) What's Hotlight?