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1 Department of Radiology and Center for Imaging Science, Samsung Medical
Center, Sungkyunkwan University School of Medicine, 50 Ilwon-Dong, Kangnam-ku,
Seoul 135-710, South Korea.
2 Department of Internal Medicine, Samsung Medical Center, Sungkyunkwan
University School of Medicine, Seoul 135-710, South Korea.
Received January 8, 2004;
accepted after revision April 28, 2004.
Address correspondence to H. K. Lim.
Abstract
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MATERIALS AND METHODS. Forty-one patients with hepatocellular carcinomas abutting the gastrointestinal tract underwent sonographically guided percutaneous radiofrequency ablation. Forty-one tumors (1.2–4.3 cm in maximum diameter) had parts 5 mm or greater (or at least one quarter of their circumferences) abutting the stomach in 23 patients and the colon in 18 patients. Thirty tumors were ablated with internally cooled electrodes and 11 with multitined expandable electrodes. All patients were followed up for at least 1 year after ablation. Therapeutic efficacy and safety were evaluated with follow-up sonography and multiphase helical CT.
RESULTS. At 1-month follow-up CT, three (7%) of the 41 tumors showed residual unablated tumor in the ablation zone. Of the remaining 38 hepatocellular carcinomas (93%) with no evidence of residual unablated tumor, four (11%) showed local tumor progression in the ablation zones on subsequent follow-up CT. We observed one major complication—a small perihepatic abscess—that needed specific treatment.
CONCLUSION. Percutaneous radiofrequency ablation is an effective and safe technique for treating hepatocellular carcinomas abutting the gastrointestinal tract.
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Although percutaneous radiofrequency ablation is considered safe, complications resulting from untoward or excessive thermal injury are possible because radiofrequency energy kills tumors with heat generated from the delivery of current [9, 12, 16]. Several investigators have warned that radiofrequency ablation of subcapsular tumors abutting the bowel could result in collateral thermal damage to the bowel [8, 14, 16–19]. To our knowledge, however, no study has focused on the usefulness of percutaneous radiofrequency ablation in the treatment of hepatic tumors abutting the bowel.
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All patients met the following criteria for treatment with percutaneous radiofrequency ablation: a single nodular hepatocellular carcinoma not greater than 5 cm in maximum diameter; up to three multinodular hepatocellular carcinomas, with each tumor measuring up to 3 cm in diameter; tumors visible on sonography; tumors accessible via a percutaneous approach; no portal venous thrombosis or extrahepatic metastases; Child-Pugh classification A or B liver cirrhosis, prothrombin time ratio greater than 50% (prothrombin time with international normalized ratio [INR] < 1.7); and a platelet count greater than 70,000/mm3 (70 cells x 109/L). This study was approved by the institutional review board, and written informed consent was obtained from all patients.
The diagnosis of hepatocellular carcinoma was confirmed by percutaneous
needle biopsy in 18 tumors. The remaining 23 tumors were considered to be
hepatocellular carcinomas on the basis of imaging findings (n = 20;
newly presenting tumor on follow-up sonography in patients with chronic liver
disease and characteristic enhancement pattern on contrast-enhanced multiphase
helical CT or dynamic contrast-enhanced MRI) or elevated serum tumor markers
(n = 12; 
-fetoprotein level > 200 ng/mL [> 200 µg/L])
or both (n = 9). Of the 41 patients, 23 were not considered for
hepatectomy and were referred for percutaneous radiofrequency ablation because
of poor medical condition, including insufficient hepatic reserve (n
= 18) and prior hepatic resections (n = 5). The remaining 18 patients
refused hepatectomy and wanted percutaneous radiofrequency ablation.
Thirty-two patients (78%) had liver cirrhosis as a result of hepatitis B
(n = 21), hepatitis C (n = 8), or alcoholism (n =
3). Six patients had chronic hepatitis B without cirrhosis, and three patients
had chronic hepatitis C without cirrhosis. At the time of radiofrequency
ablation, the patients with Child-Pugh classifications A and B cirrhosis
numbered 19 and 13, respectively. Eighteen patients with liver cirrhosis and
seven patients with chronic hepatitis were confirmed using percutaneous biopsy
(n = 20) and hepatic resection (n = 5). The remaining 14
patients with cirrhosis and two patients with chronic hepatitis were diagnosed
using imaging studies (sonography and CT) and laboratory findings.
Radiofrequency Ablation Procedure
For percutaneous radiofrequency ablation, various radiofrequency devices
manufactured by three companies were used
[13]. Between April 1999 and
February 2000, we used only a 50-W monopolar radiofrequency generator (model
500 series, Radiofrequency Interstitial Thermal Ablation Medical System) and a
multitined expandable electrode with four or seven retractable lateral prongs
because no other device was available. We also used the more recent model 1500
series, manufactured by the same company, and equipped with a more powerful
generator (150 W) and a larger multitined expandable electrode, 5 cm in
diameter. The other device (RF 2000 system, RadioTherapeutics) incorporates a
100-W generator; a LeVeen 15-gauge monopolar array needle electrode with 10
individual hooklike arms; and electrodes 2, 3, and 3.5 cm in diameter. The
largest electrode in diameter can induce thermal lesions with a diameter up to
4 cm. Since July 2000, we have usually used the internally cooled electrode
system (Cool-tip, Radionics). This system includes an electrode whose tip is
internally cooled with chilled saline. The device is equipped with a 200-W
generator and uses either a single 17-gauge straight electrode or a cluster
electrode consisting of three electrodes mounted on a common handle in a
triangular fashion. With the device, ablation zones up to 5 cm in diameter can
be created. In our study, radiofrequency ablation procedures were performed
with the model 500 series in four, the model 1500 series in three, the RF 2000
system in four, and the internally cooled electrode in 30 patients. We
selected the radiofrequency device on a case-by-case basis, depending on the
availability of the electrodes in stock and the size and location of the
tumors.
All radiofrequency ablations were performed percutaneously under real-time sonographic guidance by three experienced radiologists. Details of patient preparation and ablation techniques have been reported previously [13, 20]. All patients were treated under IV conscious sedation with 50 mg of pethidine HCl. Local anesthesia was provided by injecting lidocaine from the skin to the liver capsule along a specified insertion route. Whenever patients complained of intolerable pain during ablation, we administered IV an additional 50 mg of pethidine HCl, continuously monitoring the cardiovascular and respiratory systems. Although our strategy for complete necrosis of the tumor was to ablate a peripheral margin of 0.5–1 cm of normal hepatic tissue surrounding the tumor as well as the entire tumor itself, it was impossible to obtain a satisfactory ablative margin in the parts abutting the bowel loops. For tumors larger than 3 cm in maximum diameter, we performed multiple overlapping ablations whenever possible (two to four overlapping ablations; mean, 2.6 ablations) in nine patients. The mean number of ablations at the initial treatment was 1.3 (range, 1–4 ablations) in all patients, 2.0 (range, 1–4 ablations) in the group treated with multitined expandable electrodes, and 1.1 (range, 1–2 ablations) in the group treated with internally cooled electrodes.
Follow-Up Imaging
Immediately after radiofrequency ablation, all patients were evaluated with
gray-scale sonography to detect whether any acute complications had occurred.
For the early evaluation of therapeutic response, we performed
contrast-enhanced sonography or CT or both, depending on the location of the
ablation zone and the status of the acoustic window. Postprocedural
contrast-enhanced CT examinations were performed with a helical scanner
(HiSpeed, GE Healthcare) immediately after (within 2 hr) radiofrequency
ablation in 18 patients. A total of 120 mL of nonionic contrast material
(Ultravist 300 [iopromide, 300 mg I/mL], Schering) was administered at a rate
of 3 mL/sec with an automatic power injector. Images were obtained before and
30, 60, and 180 sec after the initiation of IV contrast material injection,
representing the nonenhanced, hepatic arterial, portal venous, and equilibrium
phases, respectively. Images were obtained in a craniocaudal direction with
7-mm collimation and 7 mm/sec table speed during a single breath-hold helical
acquisition of 25–30 sec, depending on the size of the liver.
Thirty patients were evaluated with contrast-enhanced sonography the next morning by the radiologist who had performed the radiofrequency ablation. All sonographic examinations were performed before and after injection of a microbubble contrast agent. Details on the contrast-enhanced sonography techniques have been reported previously [21].
All patients underwent follow-up four-phase helical CT with both unenhanced and contrast-enhanced three-phase scanning 1 month after radiofrequency ablation as a baseline study for the evaluation of therapeutic efficacy. We used contrast-enhanced sonography or immediate CT or both for the early assessment of any complications or residual unablated tumors; however, the final decision on the early therapeutic efficacy was made on the basis of 1-month follow-up CT findings. The reactive hyperemia is usually known to be resolved by then [13, 20]. All CT images were retrospectively reviewed by three other experienced radiologists in an attempt to assess the complications and therapeutic efficacy. When found, residual unablated tumors were usually treated with additional radiofrequency ablation. If the residual tumor was not adequate for additional radiofrequency ablation because of poor conspicuity on sonography or the presence of multiple new lesions, transcatheter arterial chemoembolization was performed. If there was evidence of complete ablation of the tumor and no new hepatocellular carcinoma in the liver at 1-month follow-up CT, subsequent contrast-enhanced three-phase helical CT was repeated at 3-month intervals as in our follow-up strategy. In five patients, however, follow-up CT examinations were repeated at 1- to 4-month intervals because of personal preference. All patients were followed up for at least 1 year after radiofrequency ablation (range, 12–58 months; mean, 26 months; SD, 10.6 months) and underwent at least four follow-up CT examinations.
Data Analysis
On immediate follow-up sonography, immediate follow-up CT, and
contrast-enhanced sonography the morning after radiofrequency ablation, we
evaluated acute complications such as abnormal fluid collection and adjacent
bowel wall change. Compared with CT findings before radiofrequency ablation,
either thickening of the adjacent bowel wall greater than 5 mm or lack of
normal layering enhancement was considered an abnormal bowel wall change.
Residual unablated tumor was defined as irregular peripherally enhancing foci in the ablation zone on either contrast-enhanced sonography or early follow-up CT immediately or 1 month after radiofrequency ablation [20, 22]. Local tumor progression was considered to be the presence of growing enhancing tumors at the margin of the ablation zone on later follow-up CT when no evidence of residual unablated tumor existed on contrast-enhanced sonography and early follow-up CT [22]. One radiologist reviewed the medical records of all patients in an attempt to evaluate symptoms and specific treatments during and after radiofrequency ablation.
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Local Tumor Progression
Of the 38 hepatocellular carcinomas with no evidence of residual tumor on
1-month follow-up CT, four (11%) showed local tumor progression in the
ablation zones on subsequent follow-up CT obtained 4 months (n = 2)
and 7 months (n = 2) after radiofrequency ablation (Fig.
3A,
3B,
3C,
3D,
3E). The four index tumors had
abutted the stomach (n = 2) and colon (n = 2), and local
tumor progressions were found in the vicinity of the adjacent bowel loop. The
maximum diameters of the index tumors measured on sonography were 2.2, 2.8,
3.0, and 3.4 cm (mean, 2.9 cm). Local tumor progression was found in three
(27%) of 11 patients treated with multitined expandable electrodes and in one
(3%) of 30 patients treated with internally cooled electrodes
(Table 1). The four tumors were
treated with the model 500 series (four prongs), the model 500 series (seven
prongs), the RF 2000 system (3.5 cm in diameter), and the Cool-tip system
(3-cm active tip), respectively. These four patients underwent either
additional radiofrequency ablations (n = 2) or transcatheter arterial
chemoembolization (n = 2). During the follow-up period, 13 (34%) of
38 patients showed 21 new hepatocellular carcinomas in other parts of the
liver on CT before either additional radiofrequency ablation or transcatheter
arterial chemoembolization. Of these, eight tumors in seven patients were
treated with additional radiofrequency ablation, and the remaining six
patients received transcatheter arterial chemoembolization.
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Complications
We found no procedure-related mortality and only one major complication
requiring specific treatment. The complication occurred in a patient who was
in an afebrile state but did not visit the hospital before a small perihepatic
abscess was discovered during the scheduled 1-month follow-up CT (Fig.
3A,
3B,
3C,
3D,
3E). The patient had a normal
WBC of less than 8,000 cells/mm3 (8 cells x 109/L)
and was treated with IV and oral antibiotics. No evidence was seen of
associated colon injury. In the other patients, we found neither abnormal
fluid collection nor adjacent bowel wall change at follow-up sonography and CT
after radiofrequency ablation.
Despite receiving IV conscious sedation with 50 mg of pethidine HCl just before radiofrequency ablation, 21 (51%) of 41 patients complained of upper abdominal pain of various degrees during the ablation procedure. Seven (17%) of 41 patients with intolerable pain needed administration of an additional 50 mg of pethidine HCl. Of these, six were treated with internally cooled electrodes and the seventh was treated with multitined expandable electrodes. During radiofrequency ablation, four (10%) of 41 patients complained of right shoulder pain, and three (7%) complained of nausea. After radiofrequency ablation, 11 (27%) of 41 patients complained of upper abdominal pain; eight (20%), of low-grade fever and general malaise; and three (7%), of nausea. Fifteen (37%) of 41 patients experienced symptoms of postablation syndrome [23], and all symptoms were resolved with conservative treatment.
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Some complications can be expected and prevented. Several previous reports have claimed that the index tumor for percutaneous radiofrequency ablation should be carefully selected and followed up closely when tumors are located in the liver adjacent to the bowel, gallbladder, major bile ducts, and diaphragm [1, 14, 16, 18, 19, 25, 26]. In an animal study [27], full-thickness burns of the adjacent stomach and colon were found when the boundary of the thermal lesion was less than 1 cm from the surface of the liver. Hence, some investigators recommend either an open or a laparoscopic approach in radiofrequency ablation of subcapsular tumors adjacent to hollow viscera [7, 27–29]. A recent report [30] also showed that hepatic tumors adjacent to bowel loops were successfully treated by radiofrequency ablation after a balloon was percutaneously interposed between the tumor and the gastrointestinal tract. In some patients, the change to the decubitus position to separate the liver from the bowel loop could avert bowel injury.
After radiofrequency ablation for hepatic tumor, bowel injury such as perforation caused by unintended thermal damage is a rare major complication [16, 18, 19, 24]. The Italian radiofrequency study of 3,554 tumors in 2,320 patients had seven cases of bowel perforation [16]. Of 1,486 radiofrequency ablation procedures for liver cancers performed in our institution during a recent 59-month period, none of the patients had bowel injury. After percutaneous radiofrequency ablation of the tumors abutting bowel loops, the patients' oral intake can be restricted until the absence of bowel injury is proven on the basis of follow-up imaging or clinical findings.
Although the follow-up period after the ablation was significantly longer in our study in the group treated with multitined expandable electrodes than in the group treated with internally cooled electrodes, this factor did not significantly influence the therapeutic results of the two groups because the local tumor progression mostly occurred within 1 year. Therapeutic results in the patients treated with multitined expandable electrodes appeared to be less favorable than those treated with internally cooled electrodes in spite of a greater number of ablations. These results are believed to be caused mainly by the operator's effort to avoid bowel penetration with the tines of the expandable electrode. In the patient with a small perihepatic abscess, the only major complication in our study, an operator's conservative strategy to avoid bowel injury by tines likely resulted in injury to the adjacent liver capsule and peritoneum (Fig. 3A, 3B, 3C, 3D, 3E). However, all cases of bowel injury in the Italian radiofrequency group study were in patients treated with internally cooled electrodes [16]. It is important to use imaging guidance to place the internally cooled electrode more than 1 cm from the liver capsule.
This study has some limitations. First, selection was biased because this study was performed retrospectively. On the basis of our experience, we prefer internally cooled electrodes for treating the tumor located in the vicinity of organs that might be perforated. Multitined expandable electrodes used in the earlier cases in this study are outdated radiofrequency devices (50-, 100-, or 150-W generators). Thus, the therapeutic results in the patients treated with internally cooled electrodes (200-W generator) seemed to be more favorable than those treated with multitined expandable electrodes. Second, all hepatologists in our institution are familiar with our indications for percutaneous radiofrequency ablation of liver cancer. They referred the patients after triage according to our inclusion and exclusion criteria. The retrospective nature of this study thus made it difficult to evaluate how many patients with hepatocellular carcinoma abutting a potentially perforated structure were not referred for percutaneous radiofrequency ablation by hepatologists during the study period.
Our results—7% (3/41) residual unablated tumors, 11% (4/38) local tumor progression, 3% (1/41) major complication, and 37% (15/41) postablation syndrome—are similar to those reported by other investigators [8, 9, 12, 20, 23, 31]. As reported in hepatocellular carcinomas in other locations, percutaneous radiofrequency ablation appears effective and, with appropriate care, can represent a safe technique for treating hepatocellular carcinomas abutting bowel loops.
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