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Original Research |
1 Department of Diagnostic Radiology, Chonbuk National University Hospital and
Medical School, Jeonju, South Korea.
2 Department of Radiology and Institute of Radiation Medicine, Seoul National
University Hospital, Seoul, Korea, 28, Yongon-dong, Chongno-gu, Seoul 110-744,
South Korea.
Received August 11, 2004;
accepted after revision January 28, 2005.
Address correspondence to J. M. Lee.
Abstract
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SUBJECTS AND METHODS. Nineteen patients with 26 HCC nodules (range, 0.8-5 cm; mean, 1.96 cm) and decompensated liver cirrhosis (mean Child score, 10.7) were treated with radiofrequency ablation using cooled-tip electrodes and a 200-W generator. Radiofrequency ablation was performed under the guidance of sonography or CT. Procedure-related complications, therapeutic efficacy, each patient's survival, changes in blood test results—that is, serum aminotransferase and bilirubin—and changes in the Child score before and after ablation therapy were analyzed. To assess the therapeutic response of the tumor to radiofrequency ablation, we performed contrast-enhanced CT after the procedure and during follow-up.
RESULTS. Complete necrosis without marginal recurrence at the 6-month follow-up was attained in 23 lesions (88.5%). During follow-up (mean, 13.3 months), one patient experienced a remote tumor recurrence in the liver. The median survival time was 12.0 ± 1.7 months. Two patients died of liver failure—one at 2 months and one at 4 months after treatment. The other patients were followed for at least 6 months (range, 6-28 months; mean, 12 months). The first and second weeks after therapy, the serum aminotransferase and bilirubin levels were significantly higher than were pretreatment levels (p < 0.05). However, 3 weeks after therapy, those figures were nearly restored to the pretreatment levels. The mean Child scores 3 weeks after radiofrequency ablation (10.8) were similar to those before treatment (10.7).
CONCLUSION. Radiofrequency ablation can be used selectively for treatment of HCC in patients with decompensated cirrhosis but has the potential to aggravate the preexisting hepatic dysfunction.
Keywords: cirrhosis • decompensation • hepatocellular carcinoma • liver • radiofrequency ablation
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Liver transplantation, which eradicates HCC and replaces damaged noncancerous hepatic parenchyma, is regarded as the best treatment for HCC in patients with decompensated liver cirrhosis [16]. However, the shortage of donors and the high cost of liver transplantation limit its widespread use. Furthermore, the long and continually increasing waits for liver transplantation allow tumor progression and reduce patient survival [18]. Given this long wait, there is a reasonable clinical need in the meantime for minimally invasive methods to avoid progression of HCC in patients with decompensated liver cirrhosis. A few studies have shown that treatment by TACE before liver transplantation may impede tumor progression while the patient is on the waiting list and leads to a better outcome than does no presurgical treatment [18-20].
Radiofrequency ablation has gained wide acceptance as a minimally invasive treatment for the management of primary or secondary liver malignancies [21-23]. The benefits over surgery include reduced mortality, morbidity, and hospitalization. During the past 4 years, we have treated more than 200 HCC patients using radiofrequency ablation. On the basis of our successful preliminary results in these patients, we planned to determine the possible role of radiofrequency ablation as a minimally invasive treatment for patients with HCC and decompensated liver cirrhosis. In this study, we analyzed the therapeutic efficacy and complications of the procedure and the changes in liver function results before and after radiofrequency ablation in patients with HCC and severely decompensated liver cirrhosis, defined as a Child-Pugh-Turcotte score (i.e., Child score) of greater than 9 [24].
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Patients
Between January 2000 and February 2004, 19 consecutive patients with HCC
and severely decompensated liver cirrhosis, as evidenced by a Child score of
greater than 9, were treated with radiofrequency ablation
[24,
25]. Seventeen were men, and
two were women (age range, 38-68 years; mean, 56 years). The cause of liver
cirrhosis in all patients was viral hepatitis B. The Child scores ranged from
10 to 12 (mean, 10.7) (Table
1).
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Patients who fulfilled the following criteria were included in the study: the presence of a single tumor nodule not more than 5 cm in diameter or not more than three tumor nodules less than 3.0 cm in diameter; the absence of extrahepatic metastasis, portal vein thrombosis, severe coagulation disorders, and hepatic encephalopathy; prothrombin activity greater than 40%; and a platelet count greater than 40,000/µL. In addition, all patients and their families desired treatment of the HCC for complete eradication or palliation, and the medical team judged the potential survival of each patient to be more than 6 months and chose radiofrequency ablation as a minimally invasive therapeutic option for that patient. In two patients, TACE had been performed previously for the treatment of hypervascular HCC, but newly growing HCC nodules had been detected during the 14- or 18-month follow-up examination. One patient underwent radiofrequency ablation twice within 8 months because of marginal HCC recurrence (Figs. 1A, 1B, 1C, 1D, and 1E). The Child score at the first ablation session was 9 (classified as Child B), whereas that at the second session was 10 (classified as Child C).
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-fetoprotein level
(200-400 ng/mL). Before ablation therapy, the following serum test results
were checked in all patients: aminotransferase, alkaline phosphatase,
bilirubin, albumin, creatinine, hemoglobin, platelet count, prothrombin time,
and electrolytes.
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The procedure was performed under CT guidance on nine patients and under sonographic guidance on 10 patients. When the lesion was not visible on sonography or was in the hepatic dome, the electrode was introduced into the lesion under CT guidance (Figs. 1A, 1B, 1C, 1D, 1E, 2A, 2B, 2C, and 2D). For the CT-guided approach, a Somatom Plus-4 scanner (Siemens Medical Solutions) was used, and the scanning parameters were 110 kVp, 200 mA, a collimation of 5 mm, and a table speed of 7 mm/sec. On the basis of the pretreatment diagnostic-workup images, the most probable tumor location and the most appropriate route to that location were chosen. For sonographic guidance, a 3.5-MHz convex probe (Sequoia, Siemens Medical Solutions) was used. All procedures were performed by one or both of two board-certificated radiologists and one nurse. The two radiologists had 10 and 5 years' daily clinical experience in local ablation therapy of liver malignancy, including radiofrequency ablation, and in interpreting liver images, including postablation scans.
Grounding was achieved by attaching one steel-mesh pad to the thigh and one to the back. After the skin had been sterilized with iodine and alcohol, local anesthesia was administered by a subcutaneous injection of 1% lidocaine from the skin to the peritoneum, and the skin was pricked with a lancet. In all patients, internally cooled 17-gauge electrodes (Cool-Tip, Valleylab) with 3.0 cm of exposed tip delivered radiofrequency energy to the tumors. Once proper positioning of the electrode in the tumor area had been confirmed by CT or sonography, the electrodes were connected to a 500-KHz monopolar radiofrequency generator (CC-1, Valleylab) capable of producing 200 W. Tissue impedance was monitored by circuitry incorporated into the generator, and an impedance-controlled, automated pulsed-radiofrequency algorithm was used [26]. In 10 patients, radiofrequency therapy was performed under conscious sedation, and analgesia was achieved by IV administration of 1-2 mg of midazolam (Dormicum, Roche) and 50-100 g of fentanyl citrate (Fentanyl, Myengmun). For nine patients, 50-100 g of fentanyl citrate was used to control pain. Vital signs were monitored continuously during the procedure.
A peristaltic pump (Watson-Marlow) was used to infuse normal saline solution at 0°C into the lumen of the radiofrequency electrodes at a rate sufficient to maintain a tip temperature of 0-20°C. For tumor nodules smaller than 2.5 cm in diameter, a single electrode was positioned in the center of the tumor and radiofrequency was applied for 10-12 min, depending on the tumor size. For tumors larger than 2.5 cm, a multiple-overlap technique (two to four overlaps) using a single radiofrequency electrode was chosen. Radiofrequency was applied initially for 12 min and for subsequent ablations for 6-12 min, depending on the tumor size. In the case of six patients with two or three tumor nodules each, one therapy session was provided for five patients and two sessions at a 3-day interval were provided for the one patient with two HCC nodules. During withdrawal of the electrode, the entire electrode track was heated briefly to a temperature of 80°C by application of radiofrequency.
Assessment of Therapeutic Efficacy and Follow-up Studies
Within 6 hr after the procedure, contrast-enhanced helical CT was performed
using the same protocol as for the pretreatment workup to evaluate the
short-term effect of the therapy. The two experienced radiologists jointly
assessed the therapeutic efficacy of radiofrequency ablation on posttreatment
CT, comparing the findings with those of pretreatment CT or MRI. In each case,
one of the two radiologists performed the radiofrequency ablation but the
other did not. Tumor necrosis was considered complete when a nonenhancing area
equal to or larger than the original tumor was seen
[21-23].
If residual tumors remained on posttreatment CT, another ablation session was
performed within 3 days. Thereafter, CT or MRI was performed every 3 months.
The duration of imaging follow-up ranged from 6 to 28 months (mean, 13
months).
Immediately after treatment and during follow-up, all patients underwent blood tests including aminotransferase (alanine aminotransferase and aspartate aminotransferase), alkaline phosphatase, bilirubin, albumin, creatinine, platelet count, and prothrombin time to evaluate liver function and possible procedure-related complications. The follow-up interval for blood testing was 1-6 days during the first 3 weeks after radiofrequency ablation, depending on the severity of hepatic dysfunction. Thereafter, follow-up blood tests were performed in step with follow-up imaging studies.
Statistical Analysis
Mean and median patient survival times were calculated using the
Kaplan-Meier method. To evaluate the influence of radiofrequency ablation on
hepatic function, we compared the aminotransferase level, bilirubin level, and
Child score before treatment with those during the first 3 weeks after
treatment. The statistical analysis was based on the paired t test. A
two-tailed p value of less than 0.05 was considered significant.
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During follow-up (mean, 13.3 ± 8.4 months), one patient showed multiple newly growing HCC nodules in the liver on the 15-month follow-up examination despite no marginal recurrence in the treated area. No patients had distant metastases. Twelve patients died, after survivals of 2-28 months after radiofrequency ablation. The mean and median survivals were 9.8 ± 2.0 months and 7.0 ± 1.2 months, respectively. The cause of death was hepatic failure in 10 patients and hepatic encephalopathy in two patients. The remaining seven patients, at 9-28 months after radiofrequency ablation therapy, were still alive (Figs. 3A, 3B, and 3C). The median and mean survival times of all patients were 12.0 ± 1.7 months and 15.3 ± 2.5 months, respectively.
Before treatment, the mean levels of serum alanine aminotransferase, aspartate aminotransferase, and total bilirubin were 43.8 IU/L, 99.5 IU/L, and 3.0 mg/dL, respectively. The mean peak levels of serum alanine aminotransferase, aspartate aminotransferase, and total bilirubin during the first week after treatment were 86.3 IU/L, 204.8 IU/L, and 5.9 mg/dL, respectively. The mean levels of serum alanine aminotransferase, aspartate aminotransferase, and total bilirubin 2 weeks after treatment were 61.0 IU/L, 127.5 IU/L, and 3.9 mg/dL, respectively. The mean levels of alanine aminotransferase, aspartate aminotransferase, and total bilirubin were markedly less at 3 weeks after treatment (43.4 IU/L, 86.4 IU/L, and 3.8 mg/dL, respectively) than during the first 2 weeks after treatment (p > 0.05). The mean Child score at the third posttreatment week was 10.8, which was not significantly different from the pretreatment Child score of 10.7.
No acute major complications were related to the procedure. All patients had mild to moderate abdominal pain during the procedure. The five patients with HCC in the hepatic dome experienced shoulder pain related to diaphragmatic irritation. Most pain was controllable within 2 days with the use of analgesia. Four patients experienced mild fever during the first 2 days after treatment. No remarkable intraperitoneal or hepatic hemorrhage was observed. No peritoneal tumor seeding was observed during follow-up.
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In our study, which evaluated the therapeutic efficacy and safety of radiofrequency ablation in patients with severely decompensated liver cirrhosis (Child score > 9), radiofrequency ablation achieved complete necrosis in 23 (88.5%) of 26 lesions at 6 months, and only one patient showed multiple remote recurrences at the 15-month follow-up. Although not all of our study patients could be followed up long-term, this relatively high success rate for complete ablation of HCC is believed to result from the relatively small size of the tumors (mean diameter, 1.96 cm) and from their morphology—encapsulated and nodular. This result is similar to the therapeutic results of a previous study (90%) of radiofrequency ablation in patients with compensated liver cirrhosis and HCC nodules with a mean diameter of 2.3 cm [29].
In our study, 12 of the 19 patients died during the follow-up period, and their survival ranged from 2 to 28 months after completion of radiofrequency ablation (mean, 9.8 ± 2.0 months; median, 7.0 ± 1.2 months). Also, seven study patients were still alive 9-28 months after therapy (mean, 16.7 months); the overall median and mean patient survivals were 12.0 ± 1.7 months and 15.3 ± 2.5 months, respectively. The one patient whose pretreatment bilirubin level was 4.50 mg/dL died because of hepatic failure 2 months after ablation therapy. In retrospect, the high level of serum bilirubin and the relatively high Child score, compared with those of the other patients, might have contributed to aggravation of hepatic dysfunction and the subsequently poor outcome. These mean and median survival times were much longer than the reported median survival (2-5 months) of patient groups with severely advanced liver cirrhosis and HCC who received no specific treatment for HCC [30-32]. In addition, the 12-month cumulative survival of our study was not lower that that of a reported study of patients who were classified as Child class C (Child score range, 10-13; mean, 11) [25].
Our findings suggest that the use of radiofrequency ablation alone as a minimally invasive technique will not bring about irreversible hepatic dysfunction in most patients with decompensated cirrhosis (Child C). This premise is supported by the results of the blood tests in this study. When we compared the pretreatment serum levels of aminotransferase and bilirubin with the levels during the third posttreatment week, the third-week levels of aminotransferase were restored to the pretreatment levels and the bilirubin levels also were markedly decreased 3 weeks after treatment, except in one patient. These data were similar to those of a previous study [33], which showed a transient elevation of liver enzyme shortly after radiofrequency ablation. Also, the mean Child score at posttreatment week 3 was not significantly elevated, compared with that before treatment.
Ueno et al. [34] evaluated the prognosis of patients with HCC complicating Child B and C cirrhosis treated with various strategies. However, TACE—even superselective TACE— may not be recommended for patients with decompensated liver cirrhosis because of the possibility that nontumorous liver tissue will be damaged and liver function worsened [35, 36]. With PEI, a multisession procedure is needed in most patients, even those with the smallest HCC nodules [7]. Furthermore, in a single PEI procedure using a large amount of ethanol, variceal bleeding was reported as a major complication [7]. Considering these shortcomings of TACE and PEI, radiofrequency ablation still may be used in the management of patients with HCC complicating decompensated cirrhosis, even though transient hepatic dysfunction could result. Furthermore, thermal ablation itself has a role in bleeding control that may be a strong point in the treatment of patients with marked hepatic dysfunction and a resultant coagulation disorder. In our study, no hemorrhagic complications were found during the procedure or its follow-up, even in patients with decreased coagulation function.
A previous study reported the therapeutic results of PEI for patients with a single HCC 5 cm or less in diameter and with Child C liver cirrhosis [7]. The 12-month cumulative survival was higher in that study than in our study (64% vs 42%), but the 28-month cumulative survival in our study (23%) was relatively higher than the 24-month cumulative survival in that study (12%). However, because of the different patient populations and follow-up periods of the two studies, a precise comparison of survival benefit is difficult.
Our study had some limitations. First, not all lesions were histologically
confirmed. Confirming all tumors histologically would have been difficult
because of the latent bleeding tendency and high risk of peritoneal seeding
due to decreased coagulation in patients with decompensated liver cirrhosis.
However, we performed radiofrequency ablation of HCC nodules confirmed by
elevated -fetoprotein level and typical radiologic findings on CT or
MRI. Another shortcoming of this study was that the population was too small
to establish the safety and efficacy of radiofrequency ablation in patients
with HCC complicating Child C cirrhosis.
In conclusion, when used with caution, radiofrequency ablation can treat HCC effectively in patients with decompensated liver cirrhosis. We believe that radiofrequency ablation, by preventing tumor progression, can bridge the long wait for liver transplantation.
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