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Original Research |
1 Department of Radiology, Seoul Veterans Hospital, 6-2 Dunchon-dong,
Gangdong-gu, Seoul, 134-060, South Korea.
2 Department of Radiology and Center for Imaging Science, Samsung Medical
Center, Sungkyunkwan University School of Medicine, Seoul 135-230, South
Korea.
Received August 26, 2004;
accepted after revision January 27, 2005.
Address correspondence to Y. K. Cho.
Abstract
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MATERIALS AND METHODS. Some controversies exist about the clinical usefulness of percutaneous radiofrequency ablation of subcapsular hepatocellular carcinoma. Twenty-eight patients underwent percutaneous radiofrequency ablation of 43 hepatocellular carcinomas using multitined expandable electrodes. Twelve tumors were subcapsular and 31 were nonsubcapsular. We attempted to use normal liver as a pathway to the tumor when possible. Tumor size ranged from 1.0 to 4.2 cm (mean, 1.8 cm). Median follow-up was 16 months. Initial ablation was considered to have been complete when no enhancement was seen in the region of the ablated lesion on 1-month follow-up CT or on follow-up CT performed immediately after repeated ablation. Initial complete ablation and local tumor progression rates were compared between subcapsular and nonsubcapsular tumors. Eleven patients had subcapsular tumors (group 1), whereas the other 17 patients did not have subcapsular tumors (group 2). Major complication and mortality rates were compared between the two groups.
RESULTS. No significant differences in initial complete ablation rate (100% vs 96.7%, p = 1.000) or local tumor progression rate (0% vs 10.0%, p = 0.545) were found between subcapsular and nonsubcapsular tumors. No procedure-related major complication or mortality occurred. The overall 1- and 3-year survival rates were 89.3% and 60.3%, respectively.
CONCLUSION. The rates of local tumor progression and complications for radiofrequency ablation using multitined expandable electrodes for subcapsular hepatocellular carcinomas were comparable to those for nonsubcapsular hepatocellular carcinomas.
Keywords: ablation • liver disease • radiofrequency
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Although the prognostic factors of local progression of HCC tumors after radiofrequency ablation are relatively well known [1, 2], only a few studies have analyzed the prognostic factors of subcapsular tumors [4, 5]. Some controversy exists about the prognosis of subcapsular HCCs after radiofrequency ablation. Until recently, subcapsular tumors were reported to show a statistically significant, shorter recurrence-free interval than do nonsubcapsular tumors after radiofrequency ablation [4, 5]. In addition, subcapsular hematoma, needle track seeding of tumor, and diaphragmatic injury were reported to be more frequent after radiofrequency ablation of subcapsular HCCs [6–9]. However, Poon et al. [10] recently reported that the results for radiofrequency ablation of subcapsular HCC using internally cooled electrodes were comparable in local tumor progression rate and complication rate to the results for radiofrequency ablation of nonsubcapsular HCC. However, as far as we know, the English-language literature includes no reports about the prognosis of subcapsular tumors after radiofrequency ablation using multitined electrodes. In this study, we tried to analyze whether subcapsular location influences local tumor progression and complication rates after radiofrequency ablation of HCC using multitined expandable electrodes.
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From February 2000 to April 2004, radiofrequency ablation was performed on 126 HCC tumors in 84 patients in our hospital. Most of the patients were poor surgical candidates or had unresectable lesions, but 19 patients had resectable lesions but refused surgical treatment. Patients were deemed to have unresectable hepatic disease on the basis of the number or bilobar location of the tumors (although some patients did undergo resection of disease in one lobe and ablation of tumor in the remaining lobe concurrently in the operating room), tumor proximity to major vascular structures precluding margin-negative resection, or the presence of cirrhosis with functional hepatic reserve that was inadequate to tolerate major hepatic resection [11].
Among the 126 tumors, 97 were newly appearing and the other 29 were a local progression of previously chemoembolized tumors. Among the 97 newly appearing tumors, radiofrequency ablation was performed percutaneously by sonographic guidance on 89, by laparoscopy on one, and by open surgery on seven. Among the 89 percutaneously treated tumors, radiofrequency ablation using internally cooled cluster electrodes was performed on nine and radiofrequency ablation using multitined expandable electrodes was performed on 80 in 54 patients. Among these patients, 26 received transarterial chemoembolization (TACE) as a combination therapy with radiofrequency ablation. Thus, 28 patients with 43 tumors received only radiofrequency ablation as the treatment. The prognosis of patients with HCC tumor might be influenced by the type of radiofrequency device (internally cooled electrode or multitined expandable electrode) and by the access route (percutaneous, laparoscopic, or open surgical). Studying patients treated with such a heterogeneous mixture of radiofrequency devices and approaches would make analysis of the clinical results difficult. Most radiofrequency ablation in our study was performed using multitined expandable electrodes. We therefore confined our study group to patients with HCC tumors treated by percutaneous technique using the same kind of radiofrequency device (multitined expandable electrodes) [8, 9]. We retrospectively analyzed the prognosis of these 28 patients with 43 HCCs.
In most patients, the cause of cirrhosis was chronic viral hepatitis B or C. Of the 28 patients, 24 presented with hepatitis B or C, two had no evidence of chronic viral hepatitis, and the other two were not checked for the viral markers. All but four patients were of Child-Pugh class A.
The diagnosis of HCC was confirmed by sonographically guided percutaneous
needle biopsy for four tumors in four patients. The remaining 39 tumors were
considered to be HCC because of characteristic imaging findings (three-phase
helical CT and conventional angiography for 27 tumors), elevated levels of
tumor marker in the blood serum (
-fetoprotein level > 200 ng/mL for
14 tumors), or both [12,
13].
Technique and Equipment for Radiofrequency Ablation
Radiofrequency ablation was performed on inpatients who were under
conscious sedation using a combination of IV fentanyl citrate (Myoungmoon) and
midazolam (Bukwang) [14,
15].
After 10 mL of 2% lidocaine hydrochloride (Huons) had been injected into the peritoneum along the puncture line, the electrode was introduced under real-time ultrasonic guidance into the mass. When a patient complained of severe pain and showed bradycardia due to vasovagal reflex during the procedure, 0.5 mg of fentanyl citrate and atropine sulfate (Huons) was given IV as additional analgesia. All tumors were treated with hooked, 15-gauge, 15-cm-long electrodes, which are expandable by 10 hooks to a maximum dimension of 3, 3.5, or 4 cm (LeVeen needle electrode, RadioTherapeutics), and radiofrequency ablation was applied using the RF 2000 generator system (RadioTherapeutics). Electrodes with a maximum dimension of 3 and 3.5 cm were used for two and 41 tumors, respectively.
This radiofrequency ablation system is based on an electrical measurement of tissue impedance to determine that tissue is being ablated. We selected the radiofrequency device to be used in each procedure on the basis of the availability of the device and the size and location of the tumor. All sonographic procedures were performed with a 3.5-MHz convex-array transducer (Sequoia, Siemens) using a free-hand technique. Percutaneous radiofrequency ablation was performed under real-time sonographic guidance by a radiologist with 3 years of experience with sonographically guided interventional procedures such as percutaneous ethanol injection therapy.
The output was set initially to 50 W and then was increased by 10 W every 60 sec until peak power (90 W) was attained. Ablation was maintained at peak power for at least 15 min unless a rapid rise in impedance stopped the flow of current and the ablation. After the first ablation, the hooks were retracted and the electrodes were rotated by 90°. The hooks were then redeployed, and the radiofrequency generator was reactivated using the same technique as for the first ablation. The radiofrequency ablation procedure was ended when the ablated area of the lesion on sonography exceeded that of the pretreated lesion. Vital signs were monitored during the entire procedure.
We avoided direct perpendicular puncture of the tumor through the capsular surface of the tumor. Instead, we punctured the tumor obliquely through a layer of nontumorous liver when possible. The needle track was thermocoagulated in patients with subcapsular HCCs.
Prognostic Factors
Tumor size was classified according to whether the greatest diameter was 3
cm or less or was more than 3 cm. Small tumors were defined as those with a
diameter of 3 cm or less. Intermediate tumors were defined as those with a
diameter of 3–5 cm. Tumor location was classified as subcapsular
(abutting the hepatic capsule) or nonsubcapsular. The tumors were assigned to
one of two groups—contacting or noncontacting—on the basis of
whether part of the tumor was attached to the adjacent visible (> 1-mm
diameter) blood vessel [5].
When an HCC nodule had a poorly defined margin or had multiple adjacent
satellite nodules, it was regarded as a non-nodular HCC tumor. Other HCC
tumors were regarded as nodular.
Imaging Follow-Up and Outcome Measures
This study was retrospective, and the treatment protocol and method of data
collection were approved by the institutional review board of our hospital.
Patients were grouped according to the presence (group 1) or absence (group 2)
of subcapsular tumors. The outcome measures that were compared between the two
groups included the rates of major complications and mortality from
treatment.
To evaluate the response to radiofrequency ablation, we performed contrast-enhanced CT with a helical scanner (HiSpeed, GE Healthcare) 1 month after the radiofrequency ablation. A total of 120 mL of nonionic contrast material containing 300 mg of iodine per milliliter (Ultravist 300 [iopromide], Schering) was administered IV at a rate of 3 mL/sec with an automatic power injector. Scanning was performed before the injection and at 30, 60, and 180 sec after initiation of the injection to obtain unenhanced images and images during the hepatic arterial, portal venous, and equilibrium phases, respectively. Scanning was performed in a craniocaudal direction and during a single patient breath-hold, with a collimation of 10 mm. The tumors were considered completely ablated when no enhancement was seen in the region of the ablated lesion on images acquired during the hepatic arterial and portal venous phases. The first postprocedural CT examination was performed 1 month after radiofrequency ablation. When images of the ablated area showed nodular peripheral enhancement during either the hepatic arterial phase or the portal venous phase, we considered part of the tumor nonablated [16]. The residual part of the tumor was usually treated with additional radiofrequency ablation within several days after detection, and follow-up CT was performed within 3 days after the repeated radiofrequency ablation. If no residual viable tumor was evident on 1-month follow-up CT or on immediate postprocedural follow-up CT after reablation, we decided that initial ablation had been complete. If a residual viable portion of the tumor remained even after repeated radiofrequency ablation, we decided that the initial tumor ablation had not been complete for the tumors. If the geometry of the residual tumor was such that additional radiofrequency ablation was unfeasible, TACE was performed.
If the 1-month follow-up CT images showed successful ablation and no new
lesion, monitoring of serum -fetoprotein level and contrast-enhanced
three-phase helical CT were repeated at 3- to 4-month intervals to detect
tumor progression. We considered an imaging finding of residual nonablated
tumor or local tumor progression at the margins of the ablated tumor to
represent unsuccessful radiofrequency ablation
[16].
The follow-up period was considered to start from the last session of radiofrequency ablation for each patient. When follow-up CT showed an enhancing area at the margin of the treated tumors or enlargement of the treated tumors, this finding was designated as local tumor progression [17]. The rates of local tumor progression were calculated for those HCC tumors that had been examined by CT at a follow-up interval of at least 1 month. Tumors for which the initial ablation had not been complete were also included in the calculation of the overall rate of local tumor progression. The rates of initial complete ablation and local tumor progression were compared between subcapsular and nonsubcapsular tumors.
The rates of major complications and overall survival were calculated for the 28 patients who underwent percutaneous radiofrequency ablation using only the multitined expandable electrodes. These rates were compared between groups 1 and 2.
We defined major and minor complications according to the definition of the Society of Cardiovascular and Interventional Radiology [18]. A major complication was one that, if left untreated, might threaten the patient's life, lead to substantial morbidity and disability, or result in a lengthened hospital stay. All other complications were considered minor. We excluded transient fever or pain from the analysis. Treatment mortality was defined as any death within 30 days of radiofrequency ablation.
All follow-up CT scans were interpreted by two experienced radiologists who were unaware of the details of subsequent follow-up imaging studies. In all cases, a consensus of the reviewers' opinions was used to judge treatment efficacy.
Statistical Analysis
Continuous data, expressed as mean or median and range, were compared
between groups using the Mann-Whitney U test. Categoric variables
were compared using the chi-square test (or Fisher's exact test when
appropriate). One-, 2-, and 3-year overall survival rates were calculated
using Kaplan-Meyer estimation. Major complication rates were compared between
groups 1 and 2 using the chi-square test.
The rates of initial complete ablation and local tumor progression were compared between subcapsular and nonsubcapsular tumors using the chi-square test. Univariate analysis was performed for factors such as tumor size, tumor nodularity, whether CT showed the tumor contacting a vessel, and tumor subcapsularity. All p values were two-sided. A p value of less than 0.05 was considered statistically significant. The SPSS software package (version 11.5, SPSS Inc.) was used for the statistical analysis.
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A comparison of baseline characteristics between groups 1 and 2 is summarized in Table 1. All 28 patients were male. The age distribution was similar in the two groups. The median value for largest tumor was 1.8 cm, with a range of 1.0–4.2 cm, and these values were similar in the two groups, without statistical significance. The two groups did not significantly differ in Child-Pugh class or in serum bilirubin or albumin levels. Other patient and tumor characteristics are also described in Table 1.
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A comparison of tumor characteristics and technical factors between subcapsular and nonsubcapsular tumors is summarized in Table 2. All 43 tumors were nodular. The subcapsular and nonsubcapsular tumors did not significantly differ in size, in the proportion contacting an intrahepatic vessel, or in the number of treatment sessions (Table 2).
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Treatment Mortality and Morbidity
For the 12 subcapsular tumors, 13 sessions of radiofrequency ablation were
performed. For the 31 nonsubcapsular tumors, 33 sessions of radiofrequency
ablation were performed. No procedure-related major complications occurred for
any patient. The rate of major complications was 0% on a procedure basis and
on a patient basis. The rate of major complications was 0% both for group 1
and group 2. No procedure-related mortality occurred.
The mean coagulation time was 22 ± 11 (± SD) min (range, 7–40 min) per session, and large tumors needed more ablations. Multiple sessions of radiofrequency ablation were performed on three tumors: two sessions for each. The mean number of treatment sessions was 1.08 ± 0.29 for the 12 subcapsular tumors and 1.06 ± 0.25 for the 31 nonsubcapsular tumors. The subcapsular tumors and nonsubcapsular tumors showed no statistically significant differences (p = 1.000).
Follow-Up
Follow-up ranged from 1 to 36 months (median, 16 months). The median
follow-up periods for groups 1 and 2 were 18 and 12 months, respectively. The
median follow-up periods for subcapsular and nonsubcapsular tumors were 11.5
and 18 months, respectively. Among the 43 tumors, 1-month follow-up CT was
performed on all except one, which was nonsubcapsular. Of the other 42 tumors,
one nonsubcapsular tumor showed evidence of residual viable tumor on the
1-month follow-up CT. We decided that for the other 41 tumors, the initial
tumor ablation was complete. For the one tumor that was not initially
completely ablated, TACE was, in addition, performed but did not result in
local tumor control. Among the 42 tumors, all 12 that were subcapsular and 29
of the 30 that were nonsubcapsular showed complete tumor ablation on the
1-month follow-up CT. Thus, the overall rate of initial complete ablation was
97.6%. The initial complete ablation rates for subcapsular and nonsubcapsular
tumors were 100% and 96.7%, respectively. The subcapsular tumors and
nonsubcapsular tumors showed no statistically significant differences
(p = 1.000).
During the later follow-up period—more than 1 month—two other tumors showed evidence of local progression. Both were nonsubcapsular. Additional radiofrequency ablation was performed for one of these tumors, and additional TACE was performed for the other. Local control was achieved only for the tumor that underwent additional radiofrequency ablation.
The overall rate of local tumor progression was 7.1%. All three tumors showing local tumor progression at various follow-up periods were nonsubcapsular. The local progression rates for subcapsular and nonsubcapsular tumors were 0% and 10.0%, respectively (Figs. 1A and 1B). The subcapsular tumors and nonsubcapsular tumors showed no statistically significant differences (p = 0.545).
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The estimated rates of overall survival for the 28 patients at 1, 2, and 3 years were 89.3%, 75.3%, and 60.3%, respectively. Five patients died during the follow-up period. The death was tumor-related in three patients and due to other causes in the other two patients. Among the five dead patients, two were in group 1 and three in group 2.
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We could find no article in the English-language literature about the prognosis for subcapsular HCC tumors after percutaneous radiofrequency ablation using multitined electrodes. Radiofrequency ablation using multitined expandable electrodes can make spheroid necrotic lesions [20, 21], and most HCC tumors included in our study were spheroid. Therefore, we performed many of the radiofrequency ablation procedures using multitined expandable electrodes.
The overall rate of local progression among all tumors in this study (7.1%) was comparable to other rates (4–12%) reported after percutaneous radiofrequency ablation for HCC [1–3, 22, 23], and in this study, the local rate of progression of subcapsular tumors was similar to that of nonsubcapsular tumors. Considering that the tumor characteristics and technical factors were comparable in both groups, our study strongly suggests that radiofrequency ablation for subcapsular tumors can be performed using multitined expandable electrodes without a significant increase in the rate of local tumor progression.
The complication rates for radiofrequency ablation are known to be generally high for subcapsular tumors compared with nonsubcapsular tumors, and the most commonly reported complications have been subcapsular hematoma, track seeding, or diaphragmatic injury [6–9]. An open approach may be beneficial in reducing the complication rate in some cases of subcapsular tumors, especially tumors near visceral organs or the diaphragm [19]. Moreover, with an intraoperative approach, inflow vascular occlusion can be performed more easily [19], although percutaneous techniques can be used for this purpose [24–27].
The percutaneous approach is the least invasive approach among the various options. If the tumor is not adjacent to visceral organs, then the percutaneous approach can be selected without a significant increase in the complication rate. The rate of major complications in this study—0%— was comparable to that of other studies [10, 19, 28]. Poon et al. [19] reported that radiofrequency ablation of subcapsular HCC could be performed without increasing the complication rate, but unlike our study, their study did not discriminate between the percutaneous, laparoscopic, and open surgical approaches. We think that if radiofrequency ablation is avoided for subcapsular tumors having a large exophytic component, then the chance of life-threatening procedure-related complications might be reduced markedly. This possibility would, of course, require further study.
Needle track seeding of tumor and subcapsular hematoma are important potential complications of HCC after radiofrequency ablation [6–9]. However, these problems may be prevented by careful attention to technique: First, subcapsular HCCs should be punctured indirectly by going through a layer of nontumoral liver tissue, if possible; second, the needle track should be thermocoagulated in patients with subcapsular HCCs [19]. In this study, we abided by these techniques, and no patient showed needle track seeding or subcapsular hematoma after radiofrequency ablation. Diaphragmatic injury also has been reported sporadically after radiofrequency ablation of subcapsular tumors [7]. However, in this study, no patient complained of symptoms associated with diaphragmatic paresis after radiofrequency ablation of liver tumors.
This study was limited by the relatively small number of patients, making it difficult to analyze and compare the expected survival between patients with and without subcapsular tumors.
In conclusion, using multitined expandable electrodes, one can perform radiofrequency ablation on patients with subcapsular HCC tumors without significantly increasing the rate of local tumor progression or of major complications, compared with the rates in patients without subcapsular tumors.
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