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Original Research |
1 All authors: Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50, Ilwon-dong, Kangnam-ku, Seoul 135-710, Korea.
Received August 2, 2007;
accepted after revision November 28, 2007.
Address correspondence to H. Rhim
(rhimhc{at}skku.edu).
Abstract
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MATERIALS AND METHODS. We retrospectively evaluated 248 patients who had been referred for planning sonography at our department between October 2005 and February 2006. We reviewed the radiologic reports of 256 planning sonography examinations in terms of the rate of feasible cases and the reasons for infeasibility. The reasons for infeasibility were classified in six categories: an inconspicuous tumor, an inadequate electrode path, an organ vulnerable to collateral thermal damage, a tumor that was too large or too many tumors, and a high risk of the heat sink effect. In addition, we assessed the treatment modality for the patients who were determined to have HCCs for which percutaneous radiofrequency ablation was not feasible.
RESULTS. In 141 (55%) of the 256 planning sonography examinations, percutaneous radiofrequency ablation was feasible. The remaining 115 (45%) planning sonography examinations revealed that radiofrequency ablation was not a feasible procedure. The reasons for infeasibility included an inconspicuous tumor in 77 patients (55.8%), an inadequate electrode path in 33 patients (23.9%), an organ vulnerable to collateral thermal damage in 14 patients (10.1%), a tumor that was too large or too many tumors in eight patients (5.8%), a high risk of the heat sink effect in five patients (3.6%), and a portal vein thrombosis in one patient (0.7%). One reason for infeasibility was found in 96 patients, two reasons in 19 patients, and four reasons in one patient. Seventy (61.9%) of 113 patients for whom radiofrequency ablation was not feasible underwent transcatheter arterial chemoembolization as an alternative treatment.
CONCLUSION. In approximately half of the patients for whom percutaneous radiofrequency ablation of HCC is requested, the procedure is not feasible, mainly due to inconspicuous tumors, at planning sonography. Additional objective criteria for assessing the feasibility of radiofrequency ablation and therapeutic strategies according to the reasons for infeasibility should be investigated further.
Keywords: hepatocellular carcinoma • imaging-guided tumor ablation • local ablation • radiofrequency ablation • sonography-guided intervention
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Imaging techniques, including sonography, CT, and MRI, are used to determine whether patients are suitable candidates for radiofrequency ablation. Imaging aspects that are particularly important include tumor size and shape, the number of tumors, and the location of a tumor or tumors relative to blood vessels and to critical structures that might be at risk for injury during an ablative procedure [10–12]. If sonography is used as the guiding technique, a sonography examination before radiofrequency ablation by the operator who will perform the radiofrequency ablation is mandatory. We refer to the sonography examination during which the feasibility of radiofrequency ablation is assessed as "planning sonography." The planning sonography examination is essential to decide whether sonography-guided percutaneous radiofrequency ablation is feasible and to plan ablation strategies, including the electrode path, electrode type, and overlapping ablation plan.
Although most physicians perform planning sonography before radiofrequency ablation, to our knowledge, no investigation has been performed to determine the feasibility rate after planning sonography and the reasons for infeasibility of the procedure. The purpose of this study was to evaluate the feasibility rate and the reasons for infeasibility of percutaneous radiofrequency ablation of HCC at planning sonography.
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There were 197 men and 51 women (age range, 32–89 years; mean, 57.7 years; median, 58.0 years) in the study group. One hundred eighty-two patients were considered ineligible for hepatic resection, and 66 patients voluntarily preferred radiofrequency ablation despite surgery also being feasible. Two hundred thirty-four patients had liver cirrhosis due to hepatitis B infection (n = 180), hepatitis C infection (n = 33), hepatitis B and C infections (n = 3), or alcoholism (n = 18). Thirteen patients had chronic hepatitis B (n = 12) or chronic hepatitis C (n = 1). One patient was a hepatitis B carrier. At the time of planning sonography, 204 patients had Child-Pugh class A cirrhosis and 44 patients had Child-Pugh class B cirrhosis.
The study group of 248 patients had 326 tumors. They underwent 256 planning sonography examinations: a single tumor was found in 203 planning sonography examinations; two tumors, in 39 examinations; three tumors, in 11 examinations; and more than four tumors, in three examinations. The tumors measured 0.5–5.0 cm at their maximum diameters (mean, 1.89 cm; median, 1.7 cm). The tumors were located at segment I in one patient, segment II in six patients, segments II and III in one patient, segment III in 19 patients, segment IV in 40 patients, segments IV and VIII in 12 patients, segments III and IV in 11 patients, segment V in 33 patients, segments V and VI in nine patients, segments V and VIII in 14 patients, segment VI in 44 patients, segment VII in 54 patients, segments VII and VIII in six patients, and segment VIII in 76 patients.
The diagnosis of HCC was confirmed by percutaneous needle biopsies in eight
tumors of eight patients. The remaining 318 tumors in 240 patients were
considered to be HCCs on the basis of characteristic imaging findings and an
elevated serum tumor marker level (
-fetoprotein > 400 mg/L)
(n = 17 patients) or satisfaction of at least two coincident
radiologic findings that were compatible with HCC on CT, MRI, sonography, or
angio graphy (n = 223 patients)
[13].
Planning Sonography
In eight of the 248 patients, planning sono graphy was performed for two
index tumors within the time interval during the study period; therefore, a
total of 256 planning sonography examinations were included in this study. The
examinations were performed by one of five radiologists (radiologist 1,
n = 10; radiologist 2, n = 48; radiologist 3, n =
39; radiologist 4, n = 142; radiologist 5, n = 17).
Radiologists 1, 2, and 3 had experience performing fewer than 50
radiofrequency ablation procedures for hepatic tumors, whereas radiologists 4
and 5 had ex perience performing more than 1,000 radio frequency ablation
procedures.
After evaluating prior imaging studies, including CT or MRI, one of the five radiologists on duty performed planning sonography to assess the feasibility of performing sonography-guided percutaneous radiofrequency ablation. All planning sonography examinations were performed with a 1-4–MHz convex probe of the same sonography equipment (Acuson Sequoia, Siemens Medical Solutions). The basic criteria for feasibility were based on whether the referred patient with an HCC or HCCs could be treated safely and completely by sonography-guided radio frequency ablation. In our institution, the criteria of an infeasible case at planning sonography are as follows: no adequate radiofrequency electrode path due to organs at risk for thermal injury along the expected path, an organ or organs (i.e., diaphragm, colon, gallbladder, main bile duct, stomach) abut ting the expected radio frequency ablation zone, an inconspicuous index tumor, or a large vessel (> 3 mm in diameter) abutting the index tumor.
Data Assessment
We reviewed the radiologic reports of planning sonography in terms of the
rate of feasibility and the reasons for infeasibility. The reasons for
infeasibility were classified in one of five categories: an inadequate
radiofrequency electrode path, an organ vulnerable to collateral thermal
damage, a tumor that was too large or too many tumors, an invisible or
inconspicuous tumor, and a high risk of the heat sink effect. In addition, we
assessed the treatment modality for the patients for whom percutaneous
radiofrequency ablation was not feasible. Data analyses for calculating the
mean and median values of a measurement and comparisons using the Student's
t test were performed with commercially available software (Excel
2000 for Windows, Microsoft). A p value of < 0.05 was considered a
significant difference.
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The reasons, as determined by planning sonography, that percutaneous radiofrequency ablation was not feasible included inconspicuous tumors in 77 patients (55.8%), inadequate radiofrequency electrode paths in 33 patients (23.9%), organs vulnerable to collateral thermal damage in 14 patients (10.1%), a high risk of the heat sink effect in five patients (3.6%), too large a tumor or too many tumors in eight patients (5.8%), and portal vein thrombosis in one patient (0.7%) (Table 1). One reason for infeasibility was found for 96 patients, two reasons for 19 patients, and four reasons for one patient.
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The largest mean (± SD) diameter of the 159 nodules deemed feasible for radiofrequency ablation at 141 planning sonography examinations was significantly larger than that of the 167 nodules found infeasible at 115 planning sonography examinations (1.91 ± 0.50 vs 1.68±0.69 cm, respectively; p = 0.014). The largest mean diameter of the 77 inconspicuous nodules at planning sonography was 1.57±0.63 cm. The locations of the 77 inconspicuous tumor nodules were segment I in one patient, segment II in four patients, segment III in four patients (Fig. 1A, 1B, 1C, 1D), segment IV in 10 patients, segment V in seven patients, segment VI in eight patients, segment VII in 13 patients, segment VIII in 19 patients, segments IV and VIII in four patients, and segments V and VIII in seven patients.
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The anatomic structures found to be a reason radiofrequency ablation was not feasible are summarized in Table 1. The radiofrequency electrode path was inadequate due to the following structures: a portal vein (Fig. 2A, 2B, 2C, 2D), a hepatic vein, a costochondral junction or rib, a perihepatic collateral vessel, the gallbladder, the main bile duct, and the hepatic flexure of the colon (Fig. 3A, 3B). The organ vulnerable to collateral thermal damage was the gallbladder in four patients, the colon in three, the diaphragm in three, the main bile duct in two, the gallbladder and colon in one patient, and the stomach in one. The abutting vessels with potential heat sink effect were a portal vein in four tumors and a hepatic vein in one tumor.
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The treatment modalities for the 113 cases for which sonography-guided percutaneous radiofrequency ablation was not feasible were intraoperative radiofrequency ablation in seven patients, surgical resection in eight patients, transcatheter arterial chemoembolization (TACE) in 70 patients, and radiation therapy in one patient. Four patients received sonography-guided percutaneous radiofrequency ablation after follow-up for a mean of 5.3 months (range, 1 week–10 months). One patient was referred to another radiologist who determined that the procedure was feasible at second planning sonography and performed percutaneous radiofrequency ablation 1 week after the first planning sonography. Thirteen patients received follow-up without any treatment at the time of preparing this manuscript. Nine patients were lost to follow-up after planning sonography.
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The results of the current study show that sonography-guided percutaneous radiofrequency ablation was considered infeasible in approximately half (45%) of the planning sonography examinations performed for referred tumors. The rate of feasibility was lower than we had expected at the time of planning this study. The reasons for the low rate of feasibility might be the following: the diameter of the index tumor referred for radiofrequency ablation in our institution became smaller over time because regular imaging screening was performed in patients at high risk for HCC and the basic policy of our department for the management of HCC is multimodality treatment. We believe that regular imaging screening of high-risk patients and managing HCC with multimodality treatment are the best ways to improve patient survival with minimal morbidity. Thus, if any reason at planning sonography is identified that indicates radiofrequency ablation may be unsafe or incomplete, we consider and present alternative solutions such as different approaches (open laparotomy or laparoscopic surgery), a different guiding technique (e.g., CT guidance), or an alternative ablative modality (e.g., TACE, ethanol ablation) to the clinicians [15–17].
To the best of our knowledge, few studies have specifically reported on the rate of feasibility at planning sonography in the literature. Recently, Tateishi et al. [8] and Choi et al. [9] reported excellent long-term survival results with minimal morbidity in large series. However, we could not find any specific comments about the infeasible cases except for a general description of inclusion criteria. We assume that the investigators of both studies might have focused on the safety and therapeutic efficacy of the radiofrequency ablation procedure. In 2005, Lencioni et al. [7] reported that only 19 (9%) of 206 consecutive patients were excluded from undergoing radiofrequency ablation because of an unfavorable location of the tumor, although the inclusion criteria were very similar to those used in our study. Those investigators used the term "unfavorable location" in a broad sense, which might have included most categories of infeasibility that we used in the current study. An inconspicuous tumor was the most common reason for infeasibility in our study. However, the authors [7] did not comment on a case being unsuitable due to an inconspicuous tumor.
The two most common reasons for infeasibility in our study were an inconspicuous tumor and an inadequate electrode path. Most patients in this study had chronic liver disease with cirrhotic changes and the size of the index tumor was less than 2 cm in diameter. A small tumor in a contracted cirrhotic liver might contribute to the increasing number of reasons for the infeasible cases. However, the feasibility rate and the reasons for infeasibility may vary depending on factors such as the institution, the patient population, tumor characteristics, operator experience, and available alternative treatment modalities [10, 11].
Correct targeting (placement) of the radiofrequency electrode inside the index tumor is critical for successful ablation. Thus, an inconspicuous tumor is the most challenging for any kind of local ablation therapy. If the tumor is inconspicuous or is partially visible, it will be difficult to place the electrode at the desired portion of tumor with confidence. Therefore, an inconspicuous tumor can be incompletely ablated, leaving residual tumor that requires an additional session of radiofrequency ablation or TACE [12, 18, 19].
Several investigations to improve the accuracy of radiofrequency ablation in treating an inconspicuous tumor due to a small isoechoic lesion have been performed. Contrast-enhanced sonography has been shown to improve the sensitivity of unenhanced sonography in many studies. This technique can be used for the evaluation of posttherapeutic response and for preprocedural planning [20, 21]. An inconspicuous index tumor at planning sonography can be clearly visible on a CT image. Hence, CT-guided radiofrequency ablation is accepted as a good alternative to sonography-guided radiofrequency ablation for a tumor that is not visible on planning sonography [22, 23]. Recently, a novel guiding technique integrating CT and MR images with real-time sonography images has been under investigation. Kudo et al. [24] have shown that a CT virtual sonography system supported treatment by providing preoperative simulation in 51 patients with an HCC.
The most important factors for safe ablation are an adequate electrode path and no organs abutting the expected ablation zone [1–3, 19]. The former may result in mechanical injury by puncturing an organ including the vessels, whereas the latter may cause collateral thermal injury resulting in bowel or diaphragmatic perforation. These risks should be carefully evaluated at the planning phase, and one should provide an alternative approach, guidance technique, or treatment for the patient with high risk [10, 11, 25]. In our series, many alternative treatments were provided to patients for whom percutaneous radiofrequency ablation was not feasible. Although TACE was the mainstay of the alternative treatments, intraoperative radiofrequency ablation or close follow-up were also good solutions. In an earlier study by Lencioni et al. [7], ethanol ablation and TACE were the alternative treatment modalities for patients with tumors unsuitable for radiofrequency ablation. However, we did not perform ethanol ablation because of its well-known limitations including the need for multiple treatment sessions and lower therapeutic efficacy. In addition, we could not perform CT-guided radiofrequency ablation because the CT machines at our institution were overloaded with examinations for diagnostic workup.
We believe that the feasibility of performing radiofrequency ablation of HCC as determined at planning sonography does not follow the rule of "all or none" but has a broad spectrum. Even in a patient in whom radiofrequency ablation is feasible, there is a broad range of the degree of technical difficulty for technical success. We know of no objective grading system for assessing the feasibility of sonography-guided percutaneous radiofrequency ablation of HCC. In the era of standardization in imaging-guided tumor ablation, further investigation of more objective classification of feasibility is warranted to provide predictive indicators for successful ablation. It will help an operator perform more sophisticated planning with tailor-made ablation strategies for each tumor, which will result in improving the outcome of radiofrequency ablation of hepatic tumors [26].
This study has several limitations. First, this study was retrospective from a single institute for a certain period. The feasibility of sonography-guided ablation therapy may be different depending on operator experience and the alternative guidance or treatment modalities available in the institution. Therefore, direct comparison of this study with another study should be considered with caution. A multicenter study may be useful to validate the current results and draw a consensus for the feasibility assessment. Second, we did not perform any statistical analysis about how much the degree of operator experience for radiofrequency ablation influenced the feasibility rate at planning sonography because of a too heterogenous number of examinations for each observer. However, the rate of feasibility at planning sonography might be affected by observer experience for the radiofrequency ablation procedure [27].
In conclusion, in approximately half of the examinations for which percutaneous radiofrequency ablation of HCC is requested, the procedure is not feasible, mainly due to inconspicuous tumors, at planning sonography. Additional objective criteria for assessing feasibility and planning therapeutic strategies according to the reasons for infeasibility should be investigated further.
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