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(Radiology. 2000;214:761-768.)
© RSNA, 2000


Vascular and Interventional Radiology

Hepatocellular Carcinoma: Radio-frequency Ablation of Medium and Large Lesions1

Tito Livraghi, MD, S. Nahum Goldberg, MD, Sergio Lazzaroni, MD, Franca Meloni, MD, Tiziana Ierace, MD, Luigi Solbiati, MD and G. Scott Gazelle, MD, MPH, PhD

1 From the Department of Radiology, Ospedale Civile, Via Cereda, 23, 20059 Vimercate, Italy (T.L., F.M.); the Department of Radiology, Beth Israel Deaconess Medical Center, Boston, Mass (S.N.G.); the Department of Internal Medicine, Ospedale San Biagio, Clusone, Italy (S.L.); the Department of Radiology, Ospedale Generale, Busto Arsizio, Italy (T.I., L.S.); and the Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, Mass (G.S.G.). From the 1998 RSNA scientific assembly. Received March 10, 1999; revision requested April 27; revision received June 17; accepted July 21. Supported in part by Radionics. Address reprint requests to T.L. (e-mail: lalivra@tin.it).


    Abstract
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To study local therapeutic efficacy, side effects, and complications of radiofrequency (RF) ablation in the treatment of medium and large hepatocellular carcinoma (HCC) lesions in patients with cirrhosis or chronic hepatitis.

MATERIALS AND METHODS: One-hundred fourteen patients who were under conscious sedation or general anesthesia had 126 HCCs greater than 3.0 cm in diameter treated with RF by using an internally cooled electrode. Eighty tumors were medium (3.1–5.0 cm), and 46 were large (5.1–9.5 cm). The mean diameter for all tumors was 5.4 cm. At imaging, 75 tumors were considered noninfiltrating, and 51 were considered infiltrating.

RESULTS: Complete necrosis was attained in 60 lesions (47.6%), nearly complete (90%–99%) necrosis in 40 lesions (31.7%), and partial (50%–89%) necrosis in the remaining 26 lesions (20.6%). Medium and/or noninfiltrating tumors were treated successfully significantly more often than large and/or infiltrating tumors. Two major complications (death, hemorrhage requiring laparotomy) and five minor complications (self-limited hemorrhage, persistent pain) were observed. The single death was due to a break in sterile technique rather than to the RF procedure itself.

CONCLUSION: RF ablation appears to be an effective, safe, and relatively simple procedure for the treatment of medium and large HCCs.

Index terms: Hepatitis, 761.291 • Liver, cirrhosis, 761.794 • Liver, CT, 761.12112, 761.12115 • Liver, interventional procedures, 761.1269, 761.47 • Liver, US, 761.12983, 761.12985 • Liver neoplasms, therapy, 761.1269, 761.323, 761.47 • Radiofrequency (RF) ablation, 761.1269, 761.47


    Introduction
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Percutaneous ethanol injection (PEI) has become one of the most widely used procedures for treating focal hepatocellular carcinoma (HCC) in the setting of hepatic cirrhosis (1,2). PEI generally is performed for HCCs up to 3–5 cm in diameter, although acceptable results have been attained in larger tumors (3). In an attempt to improve on the results attained with PEI, other percutaneous ablative therapies have been proposed. These include acetic acid injection and thermal ablative techniques in which radio frequency (RF), laser, or microwaves are used (48). These new procedures thus far have been performed principally in patients with small HCC tumors no greater than 3–4 cm in diameter.

Results from a recent prospective study (9) in which PEI and RF ablation were compared in patients with small HCC demonstrated that RF resulted in a 10% increase in the number of completely ablated tumor nodules. Treatment with RF also required fewer treatment sessions than PEI. This study proposed the so-called oven effect, owing to improved heat retention during ablation of lesions surrounded by cirrhotic tissue, as an explanation for the success in achieving relatively larger amounts of induced necrosis than previously seen with other liver tumors.

On the basis of the favorable results attained in this initial study, and to take advantage of ongoing improvements in RF technique, including the development of internally cooled cluster electrodes and pulsed current application (10,11), we treated larger HCCs. The purpose of this study was to report the local therapeutic efficacy, side effects, and complications of RF ablation in the treatment of HCCs 3.1 cm or greater in diameter in patients with cirrhosis or chronic hepatitis.


    MATERIALS AND METHODS
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Patients
The study was performed at two centers with approval from both institutional ethics committees. Written informed consent was obtained from every patient prior to treatment.

Between May 1996 and August 1998, 126 HCC lesions 3.1 cm or greater in diameter in 114 consecutive patients (82 men, 32 women; mean age, 64.4 years; age range, 53–86 years) with cirrhosis or chronic hepatitis were treated by using percutaneous RF therapy at two different institutions: 77 at Vimercate Hospital, Vimercate, Italy, and 37 at Busto Arsizio Hospital, Busto Arsizio, Italy. Both institutions are referral centers for percutaneous ablation procedures.

One hundred six patients were treated for a single tumor (92.9%), four for two tumors (3.5%), and four (3.5%) for three tumors (n = 126 tumors). Four patients had more than three tumors, but because tumor diameter was smaller than 3.1 cm, they were excluded from the results of this study.

One hundred patients had chronic hepatitis or Child-Pugh class A cirrhosis, and 14 had Child-Pugh class B cirrhosis. Hepatitis B surface antigen and antibody to hepatitis C were positive in 29 (25.4%) and 73 patients (64.0%), respectively. Six patients (5.3%) tested positive for both antigens. Four patients (3.5%) without evidence of viral hepatitis reported high alcohol consumption, and two (1.8%) had cirrhosis of unknown origin.

Patients with severe coagulation disorders (prothrombin activity < 40% [prothrombin time > 23 seconds], platelet count < 40,000/mL [0.04 x 109/L]), severe cirrhosis (Child-Pugh class C), or advanced neoplastic disease (ie, tumor diameter > 10 cm, extrahepatic malignancy, or lobar portal venous thrombosis) were excluded from this study. Thus, during this same time period, three patients were excluded owing to tumor location (adjacent to the hepatic hilum), 22 were excluded owing to advanced cirrhosis, and 20 were excluded owing to advanced neoplastic disease. No patients underwent cryotherapy or surgery.

Tumors were classified according to size and the appearance of tumor margins. The mean diameter for all tumors was 5.4 cm. Eighty tumors were 3.1–5.0 cm in diameter (medium), and 46 tumors were 5.1–9.5 cm in diameter (large). Seventy-five tumors had smooth, well-circumscribed margins or were surrounded by a capsule at imaging and were considered noninfiltrating. Fifty-one tumors had irregular margins, peripheral satellite tumors, local portal invasion, and/or appeared encapsulated but had extranodular growth; these tumors were classified as infiltrating.

The goal of RF therapy in patients with noninfiltrating tumors was curative (ie, complete ablation). Therefore, patients in this group who at follow-up imaging had residual areas of vital tissue deemed amenable to further treatment underwent additional RF therapy. Additional treatment was possible only when the residual vital tissue was detectable as a vascularized area at color Doppler ultrasonography (US) with or without enhancement with SH U 508A (Levovist; Schering, Berlin, Germany). The goal of RF therapy in patients with infiltrating HCC was palliative (ie, to attain the greatest amount of necrosis achievable to retard tumor growth). We recognize that the difference in treatment goals between the two types of tumors may have biased the results in favor of noninfiltrative lesions. This issue is further considered in the Discussion.

Pretreatment Diagnostic Work-up
For all patients, pretreatment work-up included gray-scale and color Doppler US examination (AU 5, Esaote, Genoa, Italy; Astro, Hitachi, Tokyo, Japan), as well as nonenhanced and dual-phase contrast material–enhanced helical computed tomography (CT; HiSpeed Advantage, GE Medical Systems, Milwaukee, Wis; Radix Turbo, Hitachi; Xpress, Toshiba Medical Systems, Tokyo, Japan). CT was performed during and after the injection of 150 mL of iopamidol (Iopamiro; Bracco, Milan, Italy) at a rate of 3–4 mL/sec. The entire liver was scanned twice: once beginning 20 seconds (arterial phase) and then again 60 seconds (portal phase) following the initiation of contrast material injection.

In addition, at Vimercate Hospital, {alpha}-fetoprotein and des-{gamma}-carboxy-prothrombin levels were measured before treatment in 77 patients. The diagnosis of HCC was established by means of either fine-needle biopsy or, in 56 patients, the combination of US and CT demonstrating classic imaging manifestations of this tumor and an abnormal {alpha}-fetoprotein level (>200 ng/mL [200 µg/L]) in 43 patients or des-{gamma}-carboxy-prothrombin level in 33 patients. In all patients, the following serum test results were checked before treatment and 24 and 48 hours, 7 days, and 1 month after treatment: transaminase, alkaline phosphatase, bilirubin, electrolyte, creatinine, hemoglobin, fibrinogen, and haptoglobin levels; prothrombin activity; and blood cell count.

Technique
Treatment was performed with the use of conscious sedation, analgesia with assisted ventilation (ie, oxygen given by mask with manual ventilation), or general anesthesia. In cases in which treatment was anticipated to require only one or two electrode insertions (ie, solitary lesions < 4.0 cm in diameter), treatment was performed with the use of conscious sedation with 0.5 mg of atropine sulfate (Atropina; SALF, Bergamo, Italy) administered intramuscularly, one-third drop of diazepam (Ansiolin; Doppel, Piacenza, Italy) administered orally per kilogram of body weight, 2.5 mg of droperidol (Sintodian; Farmitalia, Milan, Italy) administered intravenously, 30 mg of ketorolac tromethamine (Lixidol; Roche, Milan, Italy) administered intravenously 2 hours before treatment, and 200 mg of tramadol hydrochloride (Fortradol; Bayer, Milan, Italy) administered intravenously 30 minutes before treatment, or with administration of analgesia with assisted ventilation after the administration of propofol (Diprivan; Zeneca, Genoa, Italy). In patients treated with the use of either conscious sedation or analgesia with assisted ventilation, local anesthesia was achieved by using 5 mL of 2% xylocaine (Xilocaina, SALF).

Vital signs were continuously monitored during and for 1 hour following the procedure. When a tumor was more than 4.0 cm in diameter, multiple tumors were to be treated, or the patient was particularly anxious, treatment was performed with the use of general anesthesia with endotracheal intubation and mechanical ventilation. This had the additional advantage of allowing temporary suspension of respiration with controlled pulmonary inflation, as necessary, to facilitate electrode placement.

RF ablation was performed with real-time US guidance (AU 5) by using a 3.5-MHz probe (CA B411, Hitachi). A guide device incorporated into the US probe was used for electrode placement. After cleansing of the skin with iodized alcohol (Braunol; Braun Surgical, Milan, Italy), which also served as contact medium, the most appropriate approach for electrode insertion was selected. For lesions located in the right lobe, an intercostal approach with the patient in the left lateral decubitus position generally was preferred. For lesions located in the left lobe, a subcostal approach was used most often.

Two types of 20-cm-long, 18-gauge internally cooled RF electrodes (Radionics, Burlington, Mass) were used, depending on the size and location of the tumor. For all tumors 3.1–4.0 cm in diameter, a single electrode with 3.0 or 4.0 cm of exposed metallic tip was used. In these cases, we attempted to place the electrode into the center of the lesion. For tumors more than 4.0 cm in diameter, a triple electrode cluster with individual electrodes spaced 5 mm apart generally was used. However, in some cases the cluster electrode could not be inserted owing to a narrow intercostal space or because a very oblique subcostal approach was required. These tumors were treated with two to four insertions of a single electrode.

Grounding was achieved by attaching two dispersive pads, each with a surface area greater than 400 cm2, to the patient's thighs. The RF electrodes were attached to a 500-kHz RF generator (series CC-1; Radionics) capable of producing 200 W of power. During the procedure, a thermocouple embedded within the electrode tip continuously measured local tissue temperature. Tissue impedance was monitored by using circuitry incorporated within the generator. A peristaltic pump (Watson-Marlow, Medford, Mass) was used to infuse 0°C normal saline solution into the lumen of the electrodes at a rate sufficient to maintain a tip temperature of 20°–25°C. No more than 3 L of saline solution was required for any patient.

During RF application, generator output was monitored constantly and adjusted to apply maximum current without causing impedance rises of more than approximately 10 {Omega}. As RF energy was applied to the treatment probes, a hyperechoic focus developed around the uninsulated portion of the electrodes. This was attributed to tissue vaporization and cavitation. The area of increased echogenicity was round, most often progressively increased in size over the course of ablation, and generally enveloped the entire tumor with variable extension into the surrounding liver by the end of treatment. Hyperechoic microbubbles were often seen escaping into the hepatic veins during RF application. In some cases, the hyperechoic focus did not develop progressively but appeared rather suddenly and was accompanied with an audible popping sound emanating from the liver.

The appearance and progression of hyperechogenicity was used to guide the duration of therapy. RF was applied until the tumor appeared completely hyperechoic, the hyperechoic focus did not increase in size for several minutes, or both. Furthermore, in cases in which multiple electrode insertions were required, each subsequent electrode placement was directed to an area of the tumor where hyperechogenicity was not evident. In some cases, however, hyperechogenicity obscured the deeper portions of the tumor and made repositioning of the RF electrode difficult. Additional US imaging was not performed after the end of each treatment session.

Each application of RF energy lasted 8–12 minutes, and in all cases the entire treatment session was less than 1 hour. After RF therapy, patients were hospitalized for 2 days, unless complications necessitated longer hospitalization. Patients were hospitalized largely owing to the limited experience with the treatment of large tumors in patients with cirrhosis, in addition to conformity with established practice patterns at the two institutions where the procedures were performed. Similar procedures have been performed elsewhere with outpatients.

Assessment of Therapeutic Efficacy
To evaluate response to RF therapy, contrast-enhanced CT, with the same parameters as at pretreatment scanning, was performed on the day following treatment to check the short-term effects, at 1 month after the procedure, and every 4–5 months thereafter. All follow-up CT scans were interpreted by two investigators from each institution (T.L., F.M., T.I., L.S.) who were unaware of the details of subsequent follow-up imaging studies. In all cases, a consensus of the readers was used to judge treatment efficacy. Follow-up was 5–30 months (mean, 10.2 months).

Tumor necrosis was considered complete when no foci of enhancement were seen within the tumor or at its periphery on CT scans obtained at least 5 months after treatment. When residual tumor enhancement was detected at follow-up imaging, we attempted to estimate whether the volume of tumor necrosis was less than or greater than 90% of the original tumor volume. Results from prior studies (3,12) have confirmed the utility of CT imaging in distinguishing between adequately and incompletely treated tumor, as necrotic tissue does not enhance following administration of contrast material.

At Vimercate Hospital, {alpha}-fetoprotein and des-{gamma}-carboxy-prothrombin assays were performed 1 month and subsequently every 4–5 months after treatment. However, {alpha}-fetoprotein and des-{gamma}-carboxy-prothrombin levels were not used to assess treatment efficacy because they have been observed to normalize when CT scans demonstrate residual viable tissue, likely owing to nearly complete necrosis of tumor tissue, or they may rise when CT shows complete necrosis owing to intra- or extrahepatic lesions that are below the threshold for detection.

Statistical Analysis
To investigate the effect of both tumor size (medium vs large) and morphology (infiltrating vs noninfiltrating) on treatment efficacy, multidimensional contingency table analysis was performed by using the Cochran-Mantel-Haenszel test. The effect of tumor size on treatment efficacy, controlling for tumor morphology, and the effect of tumor morphology on treatment efficacy, controlling for tumor size, were each evaluated. The Breslow-Day statistic was used to test for homogeneity of effect across each of the controlling factors and thus permitted an analysis of the overall effect of tumor size and tumor morphology. Two sets of comparisons were performed: (a) 100% versus less than 100% necrosis and (b) necrosis of 90% or more versus necrosis less than 90%. For all comparisons, significance was at the .05 level.


    RESULTS
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Therapeutic Efficacy
The results of RF treatment, according to tumor size and morphology, are summarized in Table 1. Overall, complete necrosis was attained in 60 (47.6%) of 126 lesions (Fig 1), nearly complete (90%–99%) necrosis in 40 (31.7%) (Fig 2), and partial (50%–89%) necrosis in the remaining 26 (20.6%). In no lesion did RF therapy result in less than 50% necrosis. Eight lesions required repeat treatment within 1–2 months after the initial ablation (Fig 3), and three lesions were re-treated after 6 months of follow-up owing to the identification of small foci of persistent viable tumor that were undetectable at the previous examinations.


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TABLE 1. Summary of Results of RF Therapy in Medium and Large HCCs
 


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Figure 1a. Complete necrosis in a large, noninfiltrating HCC treated with one session of RF therapy in a 74-year-old woman. (a) Portal phase CT scan obtained prior to RF therapy demonstrates a single, noninfiltrating 6.0-cm HCC (arrows) in the hepatic dome in segment 8. (b) Intercostal US scan obtained 1 month after RF therapy with three insertions of a single electrode shows two hyperechoic lines (arrowheads) traversing the lesion. These correspond to the location of two of the RF electrodes during therapy; the third electrode track was visible on other images (not shown). (c) Portal phase CT scan obtained 5 months after therapy shows complete absence of contrast enhancement within the tumor (arrows), which indicates complete necrosis.

 


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Figure 1b. Complete necrosis in a large, noninfiltrating HCC treated with one session of RF therapy in a 74-year-old woman. (a) Portal phase CT scan obtained prior to RF therapy demonstrates a single, noninfiltrating 6.0-cm HCC (arrows) in the hepatic dome in segment 8. (b) Intercostal US scan obtained 1 month after RF therapy with three insertions of a single electrode shows two hyperechoic lines (arrowheads) traversing the lesion. These correspond to the location of two of the RF electrodes during therapy; the third electrode track was visible on other images (not shown). (c) Portal phase CT scan obtained 5 months after therapy shows complete absence of contrast enhancement within the tumor (arrows), which indicates complete necrosis.

 


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Figure 1c. Complete necrosis in a large, noninfiltrating HCC treated with one session of RF therapy in a 74-year-old woman. (a) Portal phase CT scan obtained prior to RF therapy demonstrates a single, noninfiltrating 6.0-cm HCC (arrows) in the hepatic dome in segment 8. (b) Intercostal US scan obtained 1 month after RF therapy with three insertions of a single electrode shows two hyperechoic lines (arrowheads) traversing the lesion. These correspond to the location of two of the RF electrodes during therapy; the third electrode track was visible on other images (not shown). (c) Portal phase CT scan obtained 5 months after therapy shows complete absence of contrast enhancement within the tumor (arrows), which indicates complete necrosis.

 


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Figure 2a. Nearly complete necrosis in a large, noninfiltrating HCC located in segment 8 and treated with one session of RF therapy in a 70-year-old man. (a) Arterial phase CT scan obtained prior to therapy demonstrates a large, noninfiltrating 7.1-cm HCC (arrows). Note the area of central necrosis. (b) Arterial phase CT scan obtained 6 months after RF therapy shows nearly complete tumor necrosis. A small hypervascularized area of viable neoplastic tissue (arrow) remains at the posteromedial aspect of the tumor. In this case, hyperechogenicity within the tumor during the procedure may have obscured this portion of the tumor and prevented repositioning of the RF electrode. Because this area could not be seen on follow-up US scans and remained stable in size on subsequent CT scans, additional treatment was postponed.

 


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Figure 2b. Nearly complete necrosis in a large, noninfiltrating HCC located in segment 8 and treated with one session of RF therapy in a 70-year-old man. (a) Arterial phase CT scan obtained prior to therapy demonstrates a large, noninfiltrating 7.1-cm HCC (arrows). Note the area of central necrosis. (b) Arterial phase CT scan obtained 6 months after RF therapy shows nearly complete tumor necrosis. A small hypervascularized area of viable neoplastic tissue (arrow) remains at the posteromedial aspect of the tumor. In this case, hyperechogenicity within the tumor during the procedure may have obscured this portion of the tumor and prevented repositioning of the RF electrode. Because this area could not be seen on follow-up US scans and remained stable in size on subsequent CT scans, additional treatment was postponed.

 


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Figure 3a. Complete necrosis in a noninfiltrating HCC located in segment 4 and treated with two sessions of RF therapy in a 72-year-old woman. (a) Arterial phase CT scan obtained prior to RF therapy demonstrates a noninfiltrating 4.8-cm HCC (arrows). (b) Portal phase CT scan obtained 1 day after RF therapy with one insertion of a single electrode shows complete absence of contrast enhancement within the tumor. A thin rim of hyperattenuation (arrowheads) surrounds the lesion. This was not visible on the arterial phase images and disappeared on subsequent follow-up images. It is thought to represent reactive hyperemia. (c) Longitudinal US scan obtained 1 month after RF therapy shows a hyperechoic line (arrowheads) traversing the lesion. This corresponds to the location of the RF electrode during therapy. Note the eccentric location of this line, which indicates that the electrode was not centered exactly within the tumor during treatment. (d) Arterial phase CT scan obtained 1 month after RF therapy shows a focus (arrow) of hyperattenuation at the caudal portion of the tumor. Persistence of vital neoplastic tissue in this area was due to the eccentric location of the RF electrode during therapy. The remainder of the tumor showed complete necrosis. (e) Longitudinal contrast-enhanced, power Doppler US scan obtained at the same time as d shows signs of vascularization (arrowheads) at the caudal portion of the tumor, which confirms the CT findings. Repeat RF therapy was performed guided by means of these findings. (f) Portal phase CT scan obtained 4 months after repeat treatment shows complete tumor necrosis. This was confirmed on subsequent follow-up scans.

 


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Figure 3b. Complete necrosis in a noninfiltrating HCC located in segment 4 and treated with two sessions of RF therapy in a 72-year-old woman. (a) Arterial phase CT scan obtained prior to RF therapy demonstrates a noninfiltrating 4.8-cm HCC (arrows). (b) Portal phase CT scan obtained 1 day after RF therapy with one insertion of a single electrode shows complete absence of contrast enhancement within the tumor. A thin rim of hyperattenuation (arrowheads) surrounds the lesion. This was not visible on the arterial phase images and disappeared on subsequent follow-up images. It is thought to represent reactive hyperemia. (c) Longitudinal US scan obtained 1 month after RF therapy shows a hyperechoic line (arrowheads) traversing the lesion. This corresponds to the location of the RF electrode during therapy. Note the eccentric location of this line, which indicates that the electrode was not centered exactly within the tumor during treatment. (d) Arterial phase CT scan obtained 1 month after RF therapy shows a focus (arrow) of hyperattenuation at the caudal portion of the tumor. Persistence of vital neoplastic tissue in this area was due to the eccentric location of the RF electrode during therapy. The remainder of the tumor showed complete necrosis. (e) Longitudinal contrast-enhanced, power Doppler US scan obtained at the same time as d shows signs of vascularization (arrowheads) at the caudal portion of the tumor, which confirms the CT findings. Repeat RF therapy was performed guided by means of these findings. (f) Portal phase CT scan obtained 4 months after repeat treatment shows complete tumor necrosis. This was confirmed on subsequent follow-up scans.

 


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Figure 3c. Complete necrosis in a noninfiltrating HCC located in segment 4 and treated with two sessions of RF therapy in a 72-year-old woman. (a) Arterial phase CT scan obtained prior to RF therapy demonstrates a noninfiltrating 4.8-cm HCC (arrows). (b) Portal phase CT scan obtained 1 day after RF therapy with one insertion of a single electrode shows complete absence of contrast enhancement within the tumor. A thin rim of hyperattenuation (arrowheads) surrounds the lesion. This was not visible on the arterial phase images and disappeared on subsequent follow-up images. It is thought to represent reactive hyperemia. (c) Longitudinal US scan obtained 1 month after RF therapy shows a hyperechoic line (arrowheads) traversing the lesion. This corresponds to the location of the RF electrode during therapy. Note the eccentric location of this line, which indicates that the electrode was not centered exactly within the tumor during treatment. (d) Arterial phase CT scan obtained 1 month after RF therapy shows a focus (arrow) of hyperattenuation at the caudal portion of the tumor. Persistence of vital neoplastic tissue in this area was due to the eccentric location of the RF electrode during therapy. The remainder of the tumor showed complete necrosis. (e) Longitudinal contrast-enhanced, power Doppler US scan obtained at the same time as d shows signs of vascularization (arrowheads) at the caudal portion of the tumor, which confirms the CT findings. Repeat RF therapy was performed guided by means of these findings. (f) Portal phase CT scan obtained 4 months after repeat treatment shows complete tumor necrosis. This was confirmed on subsequent follow-up scans.

 


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Figure 3d. Complete necrosis in a noninfiltrating HCC located in segment 4 and treated with two sessions of RF therapy in a 72-year-old woman. (a) Arterial phase CT scan obtained prior to RF therapy demonstrates a noninfiltrating 4.8-cm HCC (arrows). (b) Portal phase CT scan obtained 1 day after RF therapy with one insertion of a single electrode shows complete absence of contrast enhancement within the tumor. A thin rim of hyperattenuation (arrowheads) surrounds the lesion. This was not visible on the arterial phase images and disappeared on subsequent follow-up images. It is thought to represent reactive hyperemia. (c) Longitudinal US scan obtained 1 month after RF therapy shows a hyperechoic line (arrowheads) traversing the lesion. This corresponds to the location of the RF electrode during therapy. Note the eccentric location of this line, which indicates that the electrode was not centered exactly within the tumor during treatment. (d) Arterial phase CT scan obtained 1 month after RF therapy shows a focus (arrow) of hyperattenuation at the caudal portion of the tumor. Persistence of vital neoplastic tissue in this area was due to the eccentric location of the RF electrode during therapy. The remainder of the tumor showed complete necrosis. (e) Longitudinal contrast-enhanced, power Doppler US scan obtained at the same time as d shows signs of vascularization (arrowheads) at the caudal portion of the tumor, which confirms the CT findings. Repeat RF therapy was performed guided by means of these findings. (f) Portal phase CT scan obtained 4 months after repeat treatment shows complete tumor necrosis. This was confirmed on subsequent follow-up scans.

 


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Figure 3e. Complete necrosis in a noninfiltrating HCC located in segment 4 and treated with two sessions of RF therapy in a 72-year-old woman. (a) Arterial phase CT scan obtained prior to RF therapy demonstrates a noninfiltrating 4.8-cm HCC (arrows). (b) Portal phase CT scan obtained 1 day after RF therapy with one insertion of a single electrode shows complete absence of contrast enhancement within the tumor. A thin rim of hyperattenuation (arrowheads) surrounds the lesion. This was not visible on the arterial phase images and disappeared on subsequent follow-up images. It is thought to represent reactive hyperemia. (c) Longitudinal US scan obtained 1 month after RF therapy shows a hyperechoic line (arrowheads) traversing the lesion. This corresponds to the location of the RF electrode during therapy. Note the eccentric location of this line, which indicates that the electrode was not centered exactly within the tumor during treatment. (d) Arterial phase CT scan obtained 1 month after RF therapy shows a focus (arrow) of hyperattenuation at the caudal portion of the tumor. Persistence of vital neoplastic tissue in this area was due to the eccentric location of the RF electrode during therapy. The remainder of the tumor showed complete necrosis. (e) Longitudinal contrast-enhanced, power Doppler US scan obtained at the same time as d shows signs of vascularization (arrowheads) at the caudal portion of the tumor, which confirms the CT findings. Repeat RF therapy was performed guided by means of these findings. (f) Portal phase CT scan obtained 4 months after repeat treatment shows complete tumor necrosis. This was confirmed on subsequent follow-up scans.

 


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Figure 3f. Complete necrosis in a noninfiltrating HCC located in segment 4 and treated with two sessions of RF therapy in a 72-year-old woman. (a) Arterial phase CT scan obtained prior to RF therapy demonstrates a noninfiltrating 4.8-cm HCC (arrows). (b) Portal phase CT scan obtained 1 day after RF therapy with one insertion of a single electrode shows complete absence of contrast enhancement within the tumor. A thin rim of hyperattenuation (arrowheads) surrounds the lesion. This was not visible on the arterial phase images and disappeared on subsequent follow-up images. It is thought to represent reactive hyperemia. (c) Longitudinal US scan obtained 1 month after RF therapy shows a hyperechoic line (arrowheads) traversing the lesion. This corresponds to the location of the RF electrode during therapy. Note the eccentric location of this line, which indicates that the electrode was not centered exactly within the tumor during treatment. (d) Arterial phase CT scan obtained 1 month after RF therapy shows a focus (arrow) of hyperattenuation at the caudal portion of the tumor. Persistence of vital neoplastic tissue in this area was due to the eccentric location of the RF electrode during therapy. The remainder of the tumor showed complete necrosis. (e) Longitudinal contrast-enhanced, power Doppler US scan obtained at the same time as d shows signs of vascularization (arrowheads) at the caudal portion of the tumor, which confirms the CT findings. Repeat RF therapy was performed guided by means of these findings. (f) Portal phase CT scan obtained 4 months after repeat treatment shows complete tumor necrosis. This was confirmed on subsequent follow-up scans.

 
Overall, when controlling for tumor morphology, tumor size was highly significant in predicting treatment success (Table 2). Tumors 3.1–5.0 cm in diameter were successfully treated significantly more often than tumors greater than 5.0 cm in diameter. This was true whether we used 100% necrosis (P = .001) or 90% or greater necrosis (P = .006) as the criterion for success. When noninfiltrating and infiltrating tumors were considered separately, however, the effect of tumor size was significant only among the noninfiltrating tumors. Once again, this was true whether we used 100% necrosis (P = .001) or 90% or greater necrosis (P = .006) as the criterion for success.


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TABLE 2. Effect of Tumor Size on Outcome of RF Ablation
 
When controlling for tumor size, tumor morphology was also significant in predicting treatment success (Table 3). Noninfiltrating tumors were successfully treated significantly more often than infiltrating tumors. This was true whether we used 100% necrosis (P = .05) or 90% or greater necrosis (P = .03) as the criterion for success. When tumors 3.1–5.0 cm in diameter and tumors greater than 5.0 cm in diameter were considered separately, however, the effect of tumor morphology was significant only among the tumors 3.1–5.0 cm in diameter. Once again, this was true whether we used 100% necrosis (P = .024) or 90% or greater necrosis (P = .018) as the criterion for success.


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TABLE 3. Effect of Tumor Morphology on Outcome of RF Ablation
 
At 6-month follow-up, abnormal {alpha}-fetoprotein levels normalized (<20 ng/mL [20 µg/L]) in 15 of 43 patients, decreased in 20 patients, and increased in eight patients. Des-{gamma}-carboxy-prothrombin levels normalized in 20 of 33 patients, decreased in 10 patients, and increased in three patients.

Imaging Findings
A rim of hyperattenuation surrounding the region of coagulated tumor was apparent in the majority of cases during the portal phase of contrast enhancement on CT scans obtained 24 hours after RF treatment (Fig 3b). This was attributed to reactive hyperemia rather than residual viable tumor and disappeared progressively on subsequent follow-up studies. Thickening of the hepatic capsule was sometimes observed on CT scans obtained 1 month after ablation and beyond, particularly when the tumor was located close to the surface of the liver. This finding also progressively disappeared on subsequent follow-up studies.

Immediately following RF therapy, treated areas of tumor appeared as areas of hypoattenuation relative to both surrounding liver and residual tumor, if present. However, tumor size was unchanged relative to pretreatment tumor size, regardless of treatment response. On subsequent follow-up CT scans, areas of successfully treated tumor either remained unchanged in size or diminished at unpredictable rates.

Although the diameter of the hyperechoic focus seen during treatment was used to guide the duration of RF application, and grossly corresponded to the diameter of necrosis demonstrated at CT, conventional US was not used for the evaluation of therapeutic response. This is principally because of the heterogeneous and variable extent of hyperechogenicity observed after treatment. An additional finding often detected was that of a hyperechoic line corresponding to the electrode track during treatment (Figs 1b, 3c).

Side Effects
The majority of patients treated with the use of sedation or analgesia had mild or moderate pain during the procedure. This disappeared immediately following the cessation of RF application. However, in three of 114 patients, RF application had to be interrupted temporarily because of severe pain. In these cases, propofol and additional analgesia with assisted ventilation were administered to complete the procedure. When multiple insertions were performed, some patients reported slight discomfort in the right hypochondrium for 1–2 days and hyperpyrexia for several days following treatment.

In the majority of patients, a small asymptomatic right pleural effusion that lasted for less than 1 month was observed. In two (1.8%) of 114 patients, a moderate-to-large pleural effusion was documented at 1 month; this resolved by the 5–6-month follow-up CT.

In the majority of patients, transaminase levels increased two to seven times over baseline during the first 3 days following therapy. Moreover, a slight increase in leukocytes and bilirubin and a decrease in platelets and haptoglobin were observed. All of these test results returned to baseline levels by 7 days following RF ablation. No significant changes in other test results were observed.

Complications
Major complications.One 55-year-old obese patient with diabetes and two infiltrating HCC tumors of 7.0- and 4.5-cm diameter died (0.8%). On day 3 after the procedure, this patient had shock without hyperpyrexia or leukocytosis. US documented a small amount of fluid, and paracentesis yielded purulent material due to Staphylococcus aureus peritonitis. During the following days, the patient developed multiorgan failure and subsequently died 8 days after the procedure, despite massive antibiotic treatment and intensive care.

Given a lack of evidence for infection in the liver and adequate treatment of the tumor, this complication was attributed to a break in sterile technique and not to the application of RF per se. As a result of this complication, however, antibiotic prophylaxis with 1,000 mg of ceftriaxone sodium (Rocephin, Roche) is currently administered to all patients.

One patient with a superficially located tumor had intraperitoneal hemorrhage on the day of the procedure and required laparotomy. This patient developed strong hiccups secondary to insufficient diaphragmatic paralysis during general anesthesia. As a result, the cluster electrode became malpositioned during the procedure. This, in turn, resulted in tearing of the tumor and the hepatic capsule.

Minor complications.—Two (1.8%) of 114 patients developed self-limited intraperitoneal hemorrhage (the appearance of peritoneal effusion with an associated 3–4 g/dL decrease in serum hemoglobin). These patients did not require blood transfusion or other interventions.

Three (2.6%) of 114 patients, all with superficially located tumors, complained of pain and required nonsteroidal analgesics for 2–3 days following treatment. None of these complications required further treatment, although hospital discharge was delayed.


    DISCUSSION
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The management of large HCC is challenging. Several techniques have proved useful for lesions smaller than 3 cm. These include ethanol or acetic acid injection, interstitial laser hyperthermia, RF ablation, and microwave therapy (1,2,48). However, experience with these techniques in tumors larger than 3–4 cm is limited. The results of this series, in which 126 HCC tumors 3.1 cm or greater in diameter were treated with RF, suggest that RF therapy may be a useful technique for treating larger HCC. To our knowledge, this is the first article describing the use of percutaneous RF therapy in patients with large HCC. These results also add to the growing body of literature that suggests that percutaneous RF ablation is a safe and effective method for the treatment of focal hepatic neoplasms.

Our success rate in achieving complete tumor necrosis was lower than has been reported with smaller HCC (ie, 90% [9]). Our data also suggest that tumor size, controlling for tumor morphology, and morphology, controlling for tumor size, are important determinants of treatment success. The greatest success rate was achieved in noninfiltrating tumors 3.1–5.0 cm in diameter; RF therapy resulted in complete necrosis in 71% of cases and nearly complete necrosis (90%–99%) in 24%. Complete necrosis was achieved significantly less frequently in tumors that were more than 5.0 cm in diameter, infiltrating, or both. However, even in these lesions, complete or nearly complete necrosis was achieved in the majority of cases.

Furthermore, it is important to note that small residual foci of untreated or locally recurrent tumor were not targeted for repeat treatment when the tumor was infiltrating, whereas similar areas generally were re-treated when the tumor was noninfiltrating. This may have biased our results in favor of noninfiltrating tumors and likely accounts for some of the difference in local control rates. In the future, it may be possible to increase the rates of complete necrosis if small foci of residual tumor are either more readily detected or more aggressively re-treated. However, with respect to prognostic improvement, 100% and 90%–99% necrosis are probably similar, and it is important to note that no other therapy is more effective than RF therapy for the treatment of large infiltrating HCC (3,6,8).

In comparison with the other currently available percutaneous thermal therapies for HCC, RF appears to have several advantages. RF can create larger volumes of tumor necrosis in a shorter period of time (68) than either laser or microwave therapy. In addition, equipment used for RF ablation is less expensive than either laser or microwave equipment.

The results of RF therapy appear to be roughly comparable to those of PEI, although it is difficult to compare the results of this series with those obtained with PEI. PEI has been reported to result in complete necrosis in 70%–75% of HCC tumors 3–5 cm in diameter (1,12,13). However, treatment of these tumors with PEI generally requires multiple outpatient treatment sessions, whereas RF ablation usually can be accomplished in a single treatment session during a short hospitalization. In a series of HCC tumors larger than 5 cm that were treated with single-session PEI performed with the use of general anesthesia (3), complete necrosis was achieved in 58% of noninfiltrating tumors but in no infiltrating tumors. In these patients, treatment duration is similar to that required for RF, but side effects, complications, and length of hospitalization are greater (3).

An additional advantage of RF therapy over PEI relates to procedural complexity. To destroy medium-sized tumors by using PEI, the physician must carefully plan multiple treatment sessions and needle insertions to ensure that ethanol has been distributed throughout the entire volume of tumor to be treated (1). On the other hand, RF therapy needs only one or two insertions. Furthermore, our success rates may be somewhat conservative, since at the beginning of the study we attempted to treat all lesions by using only one RF probe insertion. This generally was insufficient in tumors larger than 5.0 cm.

RF therapy also appears to be more effective than conventional transarterial chemoembolization. In multiple lesions, when conventional nonsegmental transarterial chemoembolization is used, complete necrosis can be achieved in 15%–35% (14,15). This is considerably lower than results attained with RF. Moreover, the side effects and the long-term impairment of liver function associated with transarterial chemoembolization (16,17) further support the use of RF therapy. In medium-sized tumor, the results of RF therapy appear to be roughly comparable to those of segmental transarterial chemoembolization (18).

On the basis of prior experience treating small HCC, we described the "oven effect" (9), whereby cirrhotic liver surrounding individual HCC nodules acts as a thermal insulator that increases tissue heating during RF therapy. The results of this study further support the importance of this effect. In several cases, we were able to treat noninfiltrating tumors in a single treatment session. These tumors, if located in normal liver, ordinarily would be difficult to treat without using multiple electrodes, multiple treatment sessions, or both.

The oven effect may also partially explain our limited success in treating satellite lesions (Fig 4). These nodules remain a limitation for RF ablation, despite continued technical improvements. We believe that peritumoral fibrotic tissue that is interposed between the main tumor and satellite lesions may limit heat diffusion from the tumor center to the satellites. Regardless of the mechanism, however, these lesions are much more difficult to treat successfully with RF. Longer follow-up will be required to determine the prognostic improvement, if any, that results from treatment of the central tumor alone.



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Figure 4a. Treatment failure in an infiltrating HCC located in segment 7 with satellite lesions in a 64-year-old man. (a) Arterial phase CT scan obtained prior to RF therapy demonstrates a large 7.6-cm HCC (large arrows). Another small hypervascular tumor (small arrow) is adjacent to the Glisson capsule. (b) Portal phase CT scan obtained 6 months after RF therapy with one insertion of a cluster electrode shows complete necrosis of the tumor and a small area previously occupied by extranodular tumor growth (short arrow). In this case, the proximity of the vena cava did not limit heating of tumor adjacent to the vessel. Note the persistent contrast enhancement within satellite lesions (lower long arrows), which, because of interposed fibrotic tissue, remained untreated. The small superficial lesion (upper long arrow) received a treatment with PEI during the interval between the RF procedure and the present follow-up after the RF procedure.

 


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Figure 4b. Treatment failure in an infiltrating HCC located in segment 7 with satellite lesions in a 64-year-old man. (a) Arterial phase CT scan obtained prior to RF therapy demonstrates a large 7.6-cm HCC (large arrows). Another small hypervascular tumor (small arrow) is adjacent to the Glisson capsule. (b) Portal phase CT scan obtained 6 months after RF therapy with one insertion of a cluster electrode shows complete necrosis of the tumor and a small area previously occupied by extranodular tumor growth (short arrow). In this case, the proximity of the vena cava did not limit heating of tumor adjacent to the vessel. Note the persistent contrast enhancement within satellite lesions (lower long arrows), which, because of interposed fibrotic tissue, remained untreated. The small superficial lesion (upper long arrow) received a treatment with PEI during the interval between the RF procedure and the present follow-up after the RF procedure.

 
Only two major complications, and few minor complications or substantial side effects, were observed in this series. Both of the major complications appeared largely attributable to surgeon error rather than to the RF procedure itself. The one patient who died had a combination of comorbid conditions that we would now probably consider a contraindication to treatment: diabetes, cirrhosis, advanced neoplastic disease, and obesity. This patient died from overwhelming sepsis, likely owing to seeding of the peritoneum with S aureus from the skin. Treatment was delayed because of the delayed onset of signs and symptoms of sepsis (fever, leukocytosis) because the patient was diabetic.

The other major complication, massive bleeding from the liver capsule, was related to insufficient anesthesia. This patient had severe hiccups that led to erratic diaphragmatic movement during electrode placement. As a result, the tumor and liver capsule were lacerated. In retrospect, the procedure should have been temporarily halted until the patient's hiccups were better controlled.

The rate of minor complications and side effects was also acceptably low, especially given the size of the lesions treated and the overall medical condition of the patients. Leukocytosis can be attributed to inflammatory phenomena connected with repair of the tissue. Increase in bilirubin and decrease in haptoglobin and platelets probably are attributable to initial intravascular hemolysis and microhemorrhage. Transient pleural effusions are likely related to irritation of the liver capsule and diaphragm.

It is important to point out that several tumors near the hepatic capsule, gallbladder, and major blood vessels were successfully treated without complications. Previously, we and others have suggested that hepatic metastases in close proximity to these structures either should not or could not be treated successfully (19). It is possible that differences in heat conduction between cirrhotic liver and normal liver generally seen in patients with metastases also accounts for these differences. Thus, the oven effect not only promotes complete tumor destruction but also may protect surrounding structures. In addition, unlike metastases, in which a 5–10-mm rim of normal liver around the tumor must be treated, with HCC it is generally sufficient to treat just the tumor itself.

In conclusion, percutaneous RF ablation appears to be an effective, safe, and relatively simple procedure for the treatment of HCC lesions 3.1 cm or greater in diameter in patients with cirrhosis or chronic hepatitis. In comparison with PEI, the principal alternative, RF appears easier to perform and capable of achieving complete tumor necrosis in fewer treatment sessions compared with multisession PEI or with fewer complications compared with single-session PEI. We currently prefer to use RF rather than PEI when treating infiltrating and noninfiltrating medium HCC, infiltrating large HCC, and noninfiltrating large HCC in patients with risk factors for complications with single-session PEI (ie, marked portal hypertension, esophageal varices at risk of bleeding, Child-Pugh class B cirrhosis, chronic renal insufficiency). In noninfiltrating large HCC in patients without these risk factors, a higher rate of complete ablation probably will be achieved by performing more insertions than used in this study.


    Footnotes
 
Abbreviations: HCC = hepatocellular carcinoma PEI = percutaneous ethanol injection RF = radio frequency

Author contributions: Guarantors of integrity of entire study, T.L., G.S.G., L.S.; study concepts, T.L.; study design, T.L., S.L., F.M., L.S.; definition of intellectual content, T.L.; literature research, T.L.; clinical studies, T.L., S.L., F.M., L.S., T.I.; experimental studies, S.N.G., G.S.G.; data acquisition, T.L., S.L., F.M., L.S.; data analysis, T.L., G.S.G.; statistical analysis, G.S.G.; manuscript preparation, T.L., G.S.G., S.N.G., L.S.; manuscript editing, G.S.G., S.N.G.; manuscript review, T.L., G.S.G., S.N.G.


    References
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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  5. Rossi S, Buscarini E, Garbagnati F, et al. Percutaneous treatment of small hepatic tumors by an expandable RF needle electrode. AJR Am J Roentgenol 1988; 170:1015-1022.[Abstract/Free Full Text]
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RF Ablation of Hepatocellular Carcinoma
Francesco Garbagnati, MD
Radiology Online, 7 Aug 2000 [Full text]

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