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Vascular and Interventional Radiology |
1 From the Division of Diagnostic and Interventional Radiology, Department of Oncology, Transplants and Advanced Technologies in Medicine, University of Pisa, Via Roma 67, I-56125 Pisa, Italy (R.A.L., D.C., L.C., C.B.); and the Departments of Medicine II (H.P.A., P.D., H.F., I.Z., H.E.B.), Medical Biometry (M.O.), and Radiology (J.L.), University Hospital Freiburg, Germany. From the 2001 RSNA scientific assembly. Received June 17, 2002; revision requested August 8; final revision received November 26; accepted December 19. Address correspondence to R.A.L. (e-mail: lencioni@do.med.unipi.it).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: A series of 102 patients with hepatic cirrhosis and either single HCC 5 cm in diameter or smaller or as many as three HCCs each 3 cm or smaller (overall number of lesions, 142) randomly received either RF ablation (n = 52) or PEI (n = 50) as the sole first-line anticancer treatment. Mean follow-up was 22.9 months ± 9.4 (SD) in the RF group and 22.4 months ± 8.6 in the PEI group. Prognostic value of treatment techniques was assessed with univariate and multivariate Cox proportional hazards regression models.
RESULTS: One- and 2-year survival rates were 100% and 98% in the RF group and 96% and 88% in the PEI group, respectively (univariate relative risk [RR] = 0.20; 95% CI: 0.02, 1.69; P = .138). One- and 2-year local recurrence-free survival rates were 98% and 96% in the RF group and 83% and 62% in the PEI group, respectively (univariate RR = 0.17; 95% CI: 0.06, 0.51; P = .002). One- and 2-year event-free survival rates were 86% and 64% for the RF group and 77% and 43% for the PEI group, respectively (univariate RR = 0.48; 95% CI: 0.27, 0.85; P = .012). RF treatment was confirmed as an independent prognostic factor for local recurrence-free survival rates with multivariate analysis (adjusted RR = 0.20; 95% CI: 0.05, 0.73; P = .015).
CONCLUSION: RF ablation is superior to PEI with respect to local recurrence-free survival rates.
© RSNA, 2003
Index terms: Alcohol ablation, 761.1266 • Liver, cirrhosis, 76.794 • Liver, interventional procedures, 761.1266, 761.1269 • Liver neoplasms, 76.323 • Radiofrequency (RF) ablation, 761.1269
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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1-fetoprotein assays in efforts to identify asymptomatic small hepatocellular carcinomas (HCCs) (1). Early detection programs have increased the number of patients suitable for surgical treatment. However, patients with HCC are often poor candidates for resection because of the lack of hepatic reserve as a result of coexisting cirrhosis or the presence of multiple tumors (2,3). Also, the shortage of donors limits the number of patients who can undergo orthotopic hepatic transplantation. Image-guided percutaneous ethanol injection (PEI) is an accepted treatment for patients with unresectable small HCC (1). Results in several articles (4–7) show that PEI can cause complete necrosis of small HCCs and that the long-term survival rates in patients treated with PEI are similar to those in matched patients who underwent resection. Nevertheless, PEI has limitations, including uncertainty of tumor ablation, long treatment times because of the need of multiple sessions to achieve tumor destruction, and a local recurrence rate of 10%–30% (1).
Recently, other local ablation methods to achieve more effective tumor necrosis were developed and clinically tested (8). Radio-frequency (RF) thermal ablation is a safe and effective treatment for hepatic malignancies (9–12). In a pilot clinical study (13), the rate of complete tumor response with RF ablation was higher than that with PEI. One of the current recommendations for research in the field of HCC treatment is to compare PEI and RF ablation through randomized trials to assess not only initial tumor response but also long-term survival outcomes (1). Thus, the purpose of our study was to compare the effectiveness of RF thermal ablation with that of PEI for the treatment of small HCC in patients with cirrhosis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Patients
A series of 104 consecutive patients (67 men, 37 women; age range, 40–82 years; mean age, 68 years) with 144 HCCs who met the criteria were enrolled. The patients were assigned randomly to undergo either RF ablation or PEI according to country by using a computer-generated randomization list that was not available to the treating physician. Fifty-four patients with 71 HCCs formed the RF group, while 50 patients with 73 HCCs formed the PEI group. Two patients with solitary HCC who were assigned to the RF group had to be excluded from the study shortly after randomization, because in one patient the tumor diameter was larger than 5 cm and in the other patient extrahepatic tumor was identified retrospectively. Thus, 102 patients formed the study group.
The number of HCCs and absence of vascular invasion were established on the basis of ultrasonographic (US), color Doppler US, and dual-phase spiral computed tomographic (CT) images. Each imaging study was performed at one of two authors’ institutions and interpreted by three authors (R.A.L., D.C., or H.P.A., J.L., H.E.B.) with consensus.
On US scans, every discrete solid lesion was considered possible HCC. If the lesion detected at US clearly matched with a lesion showing characteristic features of HCC, including arterial hypervascularization, at dual-phase spiral CT, biopsy confirmation was considered unnecessary. According to current noninvasive criteria devised by the European Association for the Study of the Liver (1), HCC can be diagnosed in patients with hepatic cirrhosis by means of coincident findings with at least two modalities—US, CT, or magnetic resonance imaging—that show characteristic features in a focal lesion larger than 2 cm (1).
Percutaneous US-guided biopsy was performed to determine the nature of lesions that could not be diagnosed with noninvasive criteria. Histologic confirmation of HCC was obtained in 45 of 102 patients, while a noninvasive diagnosis of HCC was accepted in the remaining 57, in whom coincident findings from US and dual-phase spiral CT consistently indicated HCC. The maximum dimension of HCCs was estimated with US. The absence of extrahepatic metastases was ascertained by means of full clinical and laboratory assessment, chest radiography, spiral CT of the abdomen, and bone scintigraphy performed by one of several authors (R.A.L., H.P.A., D.C., P.D., H.F., J.L., I.Z., H.E.B., C.B.) according to standard diagnostic criteria.
Treatment Methods
RF thermal ablation and PEI were performed with real-time US guidance with 3.5-MHz convex probes (AU5, Esaote Biomedica, Genoa, Italy; or EUB 525, Hitachi Medical Systems, Wiesbaden, Germany). A dedicated probe for US-guided intervention or a guidance device incorporated into the US probe was used to place the RF electrode needle or the PEI needle. All procedures were performed by one of two authors (R.A.L., H.P.A.).
RF thermal ablation was performed by using a 50-W RF generator (model 500 L; Rita Medical Systems, Mountain View, Calif) in monopolar mode coupled with an active 15-gauge expandable electrode needle with four retractable lateral exit curved electrodes on the tip and a large dispersive electrode. Power output, electrode temperature, tissue impedance, and procedure time were displayed continuously by the RF generator, which was connected to a portable computer. Dedicated software in this computer was used to record continuously the temperature curves obtained during treatment.
Patients were placed in either the supine or left lateral decubitus position, depending on lesion site and planned needle track, and they were prepared and draped in the usual sterile fashion. A local anesthetic (Xylocaine 2%; Astra Zeneca, Milan, Italy) was injected from the insertion point on the skin to the peritoneum along the planned puncture track. The skin was pricked with a small lancet, and the needle was then advanced precisely to the chosen area of the HCC. After the electrodes had been deployed inside the HCC, the RF generator was activated. The power was set in the automatic mode to keep an average temperature of 95°C. The target temperature was usually reached within 2–3 minutes.
In HCCs 3 cm or smaller in the greatest dimension, a single 8-minute time-at-temperature RF thermal ablation was performed. In 3.1–5.0-cm HCCs, multiple overlapping ablations—as many as six—were performed through one to three insertions by using a pullback technique. In these cases, the tip of the needle was placed initially in the deepest margin of the lesion, and the RF generator was activated. Then the electrodes were retracted, the needle was withdrawn about 1.5 cm, and the generator was reactivated. During RF treatment, a hyperechoic area was observed around the electrode tips; this area increased progressively to cover a larger area or all of the HCC. At the end of the procedure, after the automatic cooldown of the RF system, the generator was reactivated to ablate the needle tract to prevent tumor dissemination.
PEI was performed after the patient received the local anesthetic. For each patient, the treatment schedule involved four to eight PEI sessions performed once or twice weekly. The number of PEI sessions for each patient was decided on the basis of the number and size of the HCCs. During each PEI session, one or two ethanol injections were administered in each HCC; 2–10 mL of sterile 95% ethyl alcohol was injected slowly, depending on the size of the tumor and the distribution of the injected ethanol within the nodule.
Alcohol distribution was evaluated with real-time US by observing the spread of the typical hyperechoic image. Injection was stopped when homogeneous alcohol perfusion of the lesion was accomplished or when ethanol leaks outside the nodule were observed repeatedly despite changing the site of alcohol injection. To prevent reflux of ethanol along the needle tract and leakage into the peritoneum, the needle was left in place for 60–120 seconds after completion of injection and then was withdrawn slowly. The needles used for PEI were either 22-gauge noncutting needles (spinal needle; Becton-Dickinson, Rutherford, NJ) or 21-gauge needles with a closed conical tip and multiple terminal side holes (Pflugbeil, Ottobrunn, Germany; and Ethanoject, TSK, Tokyo, Japan).
One of several authors (D.C., P.D., L.C., H.F., I.Z.) carefully monitored the patient during and after each RF ablation or PEI procedure. Any adverse event was evaluated. Pain was graded as absent or as slight discomfort that did not require therapy, mild to moderate pain that required administration of analgesics, or severe pain that required sedation.
Posttreatment Assessment and Follow-up
Short-term therapeutic effectiveness was assessed with dual-phase spiral CT (HiSpeed, GE Medical Systems, Milwaukee, Wis; or PQ6000, Picker International, Highland Heights, Ohio) performed 1 week after treatment. Dual-phase spiral CT studies were optimized for arterial and portal venous phases of contrast material enhancement and were interpreted by three authors with consensus. Hypoattenuating nonenhancing areas in both the arterial and portal venous phases were considered to represent complete tumor necrosis. In contrast, any portion of the treated HCC that showed persistent intranodular enhancement was considered to represent residual viable neoplastic tissue.
In cases of residual viable neoplastic tissue, additional treatment with RF thermal ablation or PEI was scheduled. However, if residual viable neoplastic tissue persisted after repeated RF ablation or PEI, the HCC was considered unresponsive to percutaneous treatment, and further treatment with segmental transcatheter arterial chemoembolization was scheduled.
Follow-up was computed as starting from the beginning of treatment for all patients. The follow-up protocol included measurement of 1-fetoprotein levels and US performed at 3-month intervals and dual-phase spiral CT performed at 6-month intervals. Each imaging study was interpreted by three authors with consensus. Patients were observed for recurrence within or around the treated tumor (ie, local recurrence) and for the emergence of new tumors remote from the treated lesion.
All new HCCs that emerged during follow-up were treated with the same percutaneous technique (RF thermal ablation or PEI) if the patient still met the requirements for these therapies. If multicentric HCC developed, patients underwent transcatheter arterial chemoembolization or other medical treatment, depending on the kind of tumor involvement, the degree of hepatic function, and the overall clinical condition. Mean follow-up was 22.9 months ± 9.4 (SD) in the RF group and 22.4 months ± 8.6 in the PEI group.
Statistical Analysis
Baseline data were presented as mean values plus or minus SD for quantitative variables, except for the skewed 1-fetoprotein levels for which the median and interquartile range were used, and as absolute and relative frequencies for qualitative variables. Differences between the RF and PEI groups in baseline characteristics were analyzed by means of the Wilcoxon rank sum test for quantitative variables and the Fisher exact test for qualitative variables. All survival probabilities were estimated by means of the Kaplan-Meier method.
For overall survival rates, the time from the beginning of RF ablation or PEI treatment to last follow-up US, dual-phase spiral CT, or death was used. For local recurrence-free survival rates, the time to local recurrence or death was used. For event-free survival rates, the time to local recurrence, extrahepatic metastases, new HCCs, or death was used.
Prognostic value of treatment techniques and of baseline characteristics was assessed by means of both univariate and multivariate Cox proportional hazards regression models. Variables with a priori selected cutoff values—a P value less than or equal to .1 in a univariate comparison in at least one of the three end points—were entered into the multivariate analysis. Both univariate and multivariate results were presented as relative risks (RRs) with corresponding 95% CIs with P values from the Wald test. All significance tests were two-sided, and differences with a P value less than .05 were considered statistically significant. Data processing and analysis were performed with commercially available software (Statistical Analysis System; SAS Institute, Cary, NC).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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1-fetoprotein level was 54 µg/L (interquartile range, 8–143). One month after intervention, the median 1-fetoprotein level was 36 µg/L (interquartile range, 7–102), and after 12 months it was 42 µg/L (interquartile range, 10–100).
A single RF ablation session led to complete tumor response in 63 (91%) of 69 HCCs. An average of 1.1 sessions ± 0.5 was performed, with a mean coagulation time of 14.1 minutes ± 8.2 (range, 8–48 minutes) per lesion. In six lesions, a second RF ablation session was performed. After that second intervention, tumor still persisted in one lesion. The median preinterventional 1-fetoprotein level was 27 µg/L (interquartile range, 11–140 µg/L). After 1 month, the median 1-fetoprotein level was 20 µg/L (interquartile range, 11–103 µg/L), and after 12 months it was 17 µg/L (interquartile range, 8–88 µg/L).
Thirteen (26%) of 50 patients experienced mild to moderate pain during and/or immediately after PEI and required administration of analgesics. Fever (temperature higher than 38.5°C) was observed in five patients after PEI. In the RF group, 15 (29%) of 52 patients experienced mild to moderate pain during the procedure; the pain was relieved with administration of analgesics in all patients. No RF ablation had to be interrupted. Postinterventional fever was observed in 10 patients. RF ablation of four lesions localized subdiaphragmatically resulted in pleural effusions that resolved spontaneously. In three patients, spiral CT revealed clinically asymptomatic arteriovenous shunts after RF ablation. One patient developed chemical thrombosis of a portal venous branch after PEI. In both groups, no procedure-related death, hemorrhage, infection, needle-track seeding, or hepatic failure was observed.
During follow-up, five patients in the PEI group died. Four patients died of hepatic failure—two because of tumor progression, one because of advanced cirrhosis, and one because of continuous alcohol abuse—and one patient died of variceal bleeding after malignant portal venous infiltration. In the RF group, one patient died of renal failure that developed after surgery for a humerus fracture. Total survival rates after 1 and 2 years were 96% (95% CI: 90%, 100%) and 88% (95% CI: 78%, 98%) in the PEI group and 100% (95% CI not applicable) and 98% (95% CI: 93%, 100%) in the RF group (RR = 0.20; 95% CI: 0.02, 1.69; P = .138).
Thirteen patients in the PEI group developed a local recurrence compared with recurrence in three patients in the RF group. Local recurrence–free survival rates were 83% (95% CI: 73%, 94%) at 1 year and 62% (95% CI: 46%, 77%) at 2 years in the PEI group compared with 98% (95% CI: 94%, 100%) at 1 year and 96% (95% CI: 90%, 100%) at 2 years in the RF group (RR = 0.17; 95% CI: 0.06, 0.51; P = .002) (Fig 1). New tumors occurred in 11 patients in the PEI group and 13 patients in the RF group. Multicentric HCCs were observed in seven patients in the PEI group and in five in the RF group. Distant metastases were not observed in either treatment group. Portal venous thrombosis was observed in four patients—three with tumor infiltration and one with chemical thrombosis—in the PEI group and in none in the RF group.
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With respect to local recurrence–free survival rates, the superiority of RF treatment was confirmed as independent (adjusted RR = 0.20; 95% CI: 0.05, 0.73; P = .015) (Table 2). The other independent prognostic factor was tumor diameter, with tumors larger than 3 cm having an increased risk of local recurrence and/or death (adjusted RR = 8.67; 95% CI: 1.90, 39.66; P = .005).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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In the current prospective randomized study, we compared PEI with RF ablation for the treatment of small HCC in patients with hepatic cirrhosis. Complete tumor response was achieved in 91% of HCCs treated with RF thermal ablation, with an average of 1.1 treatment sessions ± 0.5, and in 82% of HCCs treated with PEI, with an average of 5.4 treatment sessions ± 1.6. Our data can be used to confirm findings in a previous pilot study (13), in which RF thermal ablation was shown to be superior to PEI in achieving complete tumor response and requiring fewer treatment sessions.
No serious side effects or procedure-related complications (eg, hemorrhage, infection, needle tract seeding, hepatic failure, or death) occurred after RF thermal ablation or PEI. In our series, pain and fever were the most common side effects in both groups, and these symptoms were treated; no intervention had to be stopped. In one patient undergoing PEI, a chemical portal venous thrombosis developed, a complication which was reported (14). After RF thermal ablation, four patients with subdiaphragmatic tumors developed pleural effusions that resolved spontaneously. Iatrogenic tumor dissemination after RF ablation of subcapsular HCCs or HCCs with invasive tumor pattern was reported (15). In our series, we did not observe any case of tumor seeding after RF ablation during long-term follow-up.
Primarily because of the short observation period and low number of deaths in both treatment groups, we were not able to demonstrate a statistically significant difference between RF thermal ablation and PEI with respect to survival rates. Nevertheless, a trend toward increased survival in the RF thermal ablation group is obvious. A trend in the extent of cirrhosis in favor of the RF thermal ablation group would have contributed to better survival; however, no clinical variable showed prognostic relevance with respect to survival rates in multivariate analyses.
Our study results demonstrate that there was local recurrence of small HCCs treated with either method. With respect to local recurrence-free survival, however, RF thermal ablation was clearly superior to PEI according to results of multivariate analysis. This finding reflects the superior local ablation effect of RF thermal ablation compared with that of PEI. PEI is associated with a local recurrence rate as high as 33% if careful long-term follow-up is performed (16). Despite the absence of viable neoplastic tissue on posttreatment spiral CT images, residual microscopic nests of tumor led to local recurrence in some patients. In the multivariate analysis, lesions more than 3 cm in diameter correlated with a higher probability of local recurrence, which probably reflects a higher rate of extracapsular penetration and microscopic vascular invasion of larger tumors.
With respect to event-free survival, RF thermal ablation was of no independent prognostic value in the multivariate analysis. Tumor diameter greater than 3 cm and a bilirubin level higher than 2 mg/dL (34.2 µmol/L), however, could be used to predict a poor outcome. The development of new HCCs was similar in both treatment groups, as expected, because the local treatment strategies did not affect the underlying risks of HCC development.
The RF generator used in this study has been replaced by newer devices that use higher power output and novel electrode needles. Results of several studies (17–19) show that current RF ablation technology may achieve larger volumes of coagulation necrosis. Also, refined techniques for modifying tumor tissue response to RF ablation and combined treatment strategies result in better local tumor response rates (20–23). Therefore, the results of RF ablation might be underestimated in our study. Nevertheless, patients treated with RF ablation had significantly higher local recurrence–free and event-free survival rates than did patients treated with PEI.
Our study results show that RF thermal ablation is more effective than PEI in the treatment of small HCC in patients with cirrhosis. Therefore, RF ablation should be considered the percutaneous treatment of choice for patients who are not candidates for resection or transplantation. Further investigation is warranted to clarify whether current RF ablation technology could offer improved long-term results in patients with more advanced tumors.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, R.A.L.; study concepts and design, all authors; literature research, R.A.L., D.C.; clinical studies, R.A.L., D.C., H.P.A.; data acquisition, R.A.L., H.P.A.; data analysis/interpretation, all authors; statistical analysis, M.O.; manuscript preparation, definition of intellectual content, editing, revision/review, and final version approval, all authors.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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