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1 All authors: Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50, Ilwon-dong, Kangnam-ku, Seoul 135-710, South Korea.
Received February 16, 2004;
accepted after revision May 25, 2004.
Address correspondence to H. K. Lim
(hklim{at}smc.samsung.co.kr).
Abstract
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MATERIALS AND METHODS. Between April 1999 and August 2003, 389 patients with 521 hepatocellular carcinomas underwent a total of 571 sessions of radiofrequency ablation. The maximum dimension of the tumors measured on sonography was 2.4 ± 0.9 cm (mean ± SD) (range, 0.5–5.0 cm). The frequency and type of bile duct changes resulting from radiofrequency ablation, the time interval between radiofrequency ablation and the first appearance of bile duct changes, and the serial changes at follow-up CT were analyzed. Complications related to bile duct changes were also evaluated by reviewing medical records and CT scans.
RESULTS. Bile duct changes occurred in 69 (12%) of 571 sessions and 66 (17%) of 389 patients. Bile duct changes seen on CT included mild dilatation of upstream bile ducts surrounding the ablation zone in 57 patients (82.6%), biloma in the ablation zone in four patients (5.8%), and both in eight patients (11.6%). The mean time interval between radiofrequency ablation and the initial appearance of bile duct change was 1.6 months (range, immediate–9 months). Most (87%) of the 69 patients with bile duct changes showed no progression on follow-up CT, and only nine (13%) had slight progression. All patients but one, in whom cholangitis developed, had no major complications requiring specific treatment during the follow-up period.
CONCLUSION. Although bile duct changes were frequent after the radiofrequency ablation of hepatocellular carcinoma, most were of no clinical significance, and major complications requiring additional treatment were rare.
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In the past decade, a variety of complications related to thermal ablation procedures have been reported [11–25]. These include early complications such as bleeding, infection, ground pad burn, hepatic vascular damage, visceral damage, and late complications such as bile duct injury and tumor seeding along the electrode track [11, 12, 18, 21]. Of these, bile duct injuries including biliary stricture; biloma; bilioperitoneum; hemobilia; and biliovenous, biliocutaneous, and biliopleural fistula have been reported intermittently [11–23]. Bile duct injury by thermal ablation has been reported to occur in the range of 0.1–1.0% [18, 21, 24, 25]. In our experience, bile duct changes were frequently found as a result of radiofrequency ablation for hepatocellular carcinoma. Our study was performed to determine the frequency of bile duct changes after radiofrequency ablation for hepatocellular carcinoma and to evaluate their clinical significance with serial follow-up.
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The study was performed with the approval of our institutional review board. Written informed consent was obtained from all patients at the time of enrollment.
The diagnosis of hepatocellular carcinoma was confirmed using
sonographically guided percutaneous needle biopsy for 232 tumors, although the
remaining 289 tumors were determined to be hepatocellular carcinoma by means
of imaging findings, a new appearance of the tumor at follow-up sonography and
characteristic enhancement pattern (high enhancement during arterial phase
followed by washout during the portal or equilibrium phase) on
contrast-enhanced multiphase helical CT, and an elevated level of serum tumor
marker (
-fetoprotein level > 200 ng/mL [> 200 µg/L]). The
maximum dimension of the tumors measured on sonography was 2.4 ± 0.9 cm
(mean ± SD) (range, 0.5–5.0 cm). In our study, 312 patients had
liver cirrhosis as a result of hepatitis B (n = 282) or hepatitis C
(n = 30). The remaining 77 patients had either chronic hepatitis B
(n = 66) or hepatitis C (n = 11) without liver cirrhosis.
Biliary manipulation such as papillotomy or balloon dilatation of the papilla
was performed in two patients before radiofrequency ablation. None of the
patients underwent bilioenteric anastomosis.
Between April 1999 and June 2000, we exclusively used a multitined expandable electrode system (model 500 or model 1500 series, RITA Medical Systems or RF 2000 system, RadioTherapeutics) because no other device was available. Since July 2000, we most often used an internally cooled electrode system (Cool-tip, Radionics). This system includes an electrode with a tip internally cooled with saline, a process thought to increase the size of the ablation zone. The device is equipped with a 200-W generator and uses either a single 17-gauge electrode or cluster electrodes designed in a triangular shape. We treated 271 tumors with multitined expandable electrodes and 250 tumors with internally cooled electrodes.
Radiofrequency ablation was performed either percutaneously (368 patients with 493 tumors) or intraoperatively after laparotomy (21 patients with 28 tumors) under real-time sonography guidance with a 2-5–MHz convex-array transducer (HDI 5000, Advanced Technology Laboratories) by one of four experienced radiologists. Details on patient preparation and ablation techniques have been reported previously [9, 10]. Our descriptions of the radiofrequency ablation procedures and data are based on the proposed standardization of terms and reporting criteria [26]. For percutaneous radiofrequency ablation, all patients were treated under IV conscious sedation with 50 mg of pethidine hydrochloride. Lidocaine, a local anesthetic, was injected through the skin into the liver capsule along a predetermined insertion route. Whenever patients reported intolerable pain during ablation, we administered an additional 50 mg of pethidine hydrochloride. The intraoperative radiofrequency ablation was performed in the operating room while the patient was under general anesthesia.
Our strategy for complete tumor ablation was to ablate a peripheral margin of 0.5–1.0 cm of the healthy hepatic tissue surrounding the tumor in addition to the entire tumor itself. For tumors smaller than 2.5 cm in diameter, one ablation was usually enough to destroy the entire tumor. For larger tumors, we performed multiple overlapping ablations (range, two to six overlapping ablations; mean, three overlapping ablations) according to the size and shape of the tumor. Multiple overlapping ablations were made through the initial electrode tract rather than using a different tract. Multiple overlapping ablations for the same tumor at the same time were considered to be one session of radiofrequency ablation. If a residual tumor in the same ablation zone after the first radiofrequency ablation was treated with a second radiofrequency ablation at a different time and through a different tract, this tumor was considered to have been treated with two sessions of radiofrequency ablation. Therefore, 571 sessions of radiofrequency ablation were performed.
CT examinations were performed using a helical scanner (HiSpeed Advantage, GE Healthcare) with 5-mm slice thickness. A total of 120 mL of nonionic contrast material (Ultravist 300, 300 mg I/mL, [iopromide], Schering) was administered with a power injector (OP 100, Medrad) at a rate of 3 mL/sec. CT scans were obtained 30, 70, and 180 sec after the initiation of IV contrast material injection for imaging during the hepatic arterial, portal venous, and equilibrium phases, respectively. All patients underwent contrast-enhanced three-phase helical CT examinations before and after radiofrequency ablation according to our protocol. For early evaluation of residual unablated tumor and any acute complications after radiofrequency ablation, either contrast-enhanced immediate CT (within 2 hr) after radiofrequency ablation or contrast-enhanced sonography 1 day after radiofrequency ablation using SH U 508A (Levovist, Schering) was performed, depending on the location and number of treated tumors. Contrast-enhanced sonography was preferred for the early evaluation of potential residual unablated tumor and acute complications after radiofrequency ablation in patients with a single lesion and good acoustic window, whereas immediate CT was performed in patients in whom the ablation zone was located deep in the liver or who had two or more ablation zones. If residual unablated tumor was found in the ablation zone on contrast-enhanced sonography or immediate CT, it was most often treated with additional radiofrequency ablation when it was technically feasible.
If the tumors were completely treated and no new hepatocellular carcinoma was found at 1-month follow-up CT, contrast-enhanced three-phase CT was repeated at 2- to 4-month intervals. Most patients (257/389) were followed up for more than 1 year (range, 13–57 months; mean, 22 months), and the remaining 132 patients were followed up for 12 months or less (range, 4–12 months; mean, 7 months). On follow-up CT, if residual unablated tumor, local tumor progression at the ablation zone, or new hepatocellular carcinoma was found and considered not appropriate to be treated with additional radiofrequency ablation because of poor conspicuity on sonography or multiplicity of the new lesions, transcatheter arterial chemoembolization was performed. After recurrent tumors or new tumors received additional treatment, they were followed up with contrast-enhanced CT using the same protocol. In two patients, percutaneous transhepatic or endoscopic retrograde cholangiography was performed during the follow-up period.
Three of four radiologists who performed radiofrequency ablation procedures retrospectively reviewed all CT scans obtained before or after radiofrequency ablation in 389 patients. A final decision was reached by consensus. The frequency of bile duct changes resulting from radiofrequency ablation was assessed on a treatment session basis and on an individual patient basis. The type of bile duct changes resulting from radiofrequency ablation, the time interval between radiofrequency ablation and the first appearance of bile duct changes, and the serial changes on follow-up CT were evaluated. If the patients underwent multiple sessions of radiofrequency ablation for the same tumor, the last session of radiofrequency ablation was used as a starting point to calculate the time lag between radiofrequency ablation and the appearance of bile duct change. Changes in bile ducts were considered to be present if CT depicted any abnormalities either in the intrahepatic or in the extrahepatic bile ducts directly resulting from radiofrequency ablation. CT diagnosis of bile duct dilatation was made when disproportional dilatation of bile ducts was newly found after radiofrequency ablation. If bile duct changes after radiofrequency ablation were present on CT before radiofrequency ablation or if bile duct changes developed after treatment other than radiofrequency ablation, they were not considered to be caused by radiofrequency ablation. Biloma was diagnosed when a circumferential fluid collection was found on CT for more than 4 months in the space surrounding the necrotic tissue of the ablation zone or when a communication between the bile duct and circumferential fluid collection was confirmed on cholangiography or CT.
The morbidity and mortality rates associated with bile duct changes were evaluated by the review of medical records during the entire follow-up period for the patients with bile duct changes after radiofrequency ablation. Using the medical records, we evaluated basic patient information related to history, adverse clinical symptoms, and signs attributed to radiofrequency ablation.
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Sixty-nine patients with bile duct changes were followed up for a mean period of 17 months (range, 4–57 months). The time of the initial appearance of bile duct changes after radiofrequency ablation was variable, ranging from immediately after radiofrequency ablation to 9 months after (mean, 1.6 months) (Fig. 4A, 4B, 4C). Two (3%) and 52 (75%) of 69 patients with bile duct changes were found on immediate and 1-month follow-up CT, although 12 (15%) and three (4%) of 69 patients were found between 3 and 4 months and after 5 months, respectively. Nine (13%) of 69 patients with bile duct changes after radiofrequency ablation showed slight progression. Fifty-one patients (74%) showed persistent changes in bile ducts with no progression on follow-up CT. The remaining nine patients (13%) showed atrophy of the liver parenchyma peripheral to the ablation zone, and in these patients bile duct dilatation either decreased or disappeared on subsequent follow-up CT. Cholangitis occurred in one (1.4%) of 69 patients (Fig. 2A, 2B, 2C), which showed dilatation of an upstream bile duct with progressive biloma on follow-up CT. Endoscopic retrograde cholangiography revealed a communication between the bile duct and the biloma. The patient successfully recovered after treatment with IV antibiotics. Percutaneous transhepatic cholangiography was performed in one patient with obstructive jaundice resulting from central bile duct invasion of the recurrent tumor after radiofrequency ablation. Cholangiography showed leakage of the contrast medium through the injured bile duct into the biloma. One patient had an evident communication between bile duct and biloma on follow-up CT. Sixty-eight (98.6%) of 69 patients showed no major complications requiring specific treatment during the follow-up period.
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Bile duct injury by thermal ablation has been reported to be in the range of 0.1–1.0%, but only rarely [18, 21, 24, 25], because these reports include only symptomatic biliary complications after radiofrequency ablation. The limited number of bile duct changes with or without complications that have been reported most likely relates to the warnings of biliary complication from the early days of radiofrequency ablation, which resulted in the exclusion of at-risk patients with tumors close to the main bile ducts [27, 28]. In addition, the true frequency of bile duct changes after radiofrequency ablation may have been underestimated because some investigators ignored minor bile duct changes in patients without either clinical or laboratory abnormality after radiofrequency ablation. Some studies [29, 30] have reported dilatation of the upstream bile duct in the liver peripheral to the ablation zone as incidental findings on follow-up CT. However, to our knowledge, no study has focused on the frequency of bile duct changes after radiofrequency ablation and their clinical significance with serial follow-up CT.
In our study, bile duct changes after radiofrequency ablation occurred frequently: 12% on a per-treatment basis and 17% on a per-patient basis. All cases of bile duct changes after radiofrequency ablation occurred in the area of the liver peripheral to or within the ablation zones. Upstream bile duct dilatation peripheral to the ablation zone was the most common type of change, followed by fluid collection surrounding the necrotic tissue, which suggested biloma with or without accompanying bile duct dilatation. Bile duct dilatation surrounding the ablation zone can be caused by bile stasis or biliary stricture. We believe that transient dilatation of the bile duct caused by simple biliary stasis should disappear because the ablation zone decreases in volume in the follow-up period. In our study, however, most cases (86%, 56/65) of bile duct dilatation surrounding the ablation zone continued to be seen on follow-up CT after 4 months in spite of a decrease in the volume of the ablation zone. This result indicates that persistent upstream bile duct dilatation in the liver peripheral to the ablation zone is not a transient finding but an irreversible change caused by thermal damage to bile ducts after radiofrequency ablation.
Fluid collection surrounding the necrotic tissue with or without upstream bile duct dilatation occurred less commonly after radiofrequency ablation. Fluid collection surrounding the necrotic tissue could be caused by hematoma, liquefactive necrosis, or biloma [29]. In our study, 12 of 69 patients with bile duct changes had fluid collection surrounding the necrotic tissue. All patients continued to be seen for more than 4 months. Two of these patients were found to have a communication between the bile duct and the fluid collection at percutaneous transhepatic or endoscopic cholangiography, and another patient was found on CT to have an evident communication between the dilated bile duct and the fluid collection. Therefore, we assume that the fluid collection surrounding the necrotic tissue is most likely a biloma caused by bile from the injured bile duct, rather than hematoma or liquefactive necrosis, which usually disappears within 4 months [29].
Intrahepatic bile ducts are supplied exclusively by the peribiliary capillary plexus. Bile duct injury after transcatheter arterial chemoembolization is known to result from damage to the peribiliary capillary plexus [31], whereas bile duct injury after radiofrequency ablation is caused by direct thermal damage to the bile ducts [32].
Previous investigations [32–34] suggested that large bile ducts are protected from thermal damage by the cooling effects of the portal vein and hepatic artery that run alongside them and that main bile duct injury was seen only after radiofrequency ablation after laparotomy with a Pringle maneuver (temporary occlusion of vascular inflow by clamping the hepatic artery and portal vein). Hansen et al. [32] reported that when intact blood flow is present, the small bile ducts associated with thrombosed blood vessels smaller than 3 mm in diameter were histologically destroyed, although larger bile ducts adjacent to blood vessels greater than 3 mm in diameter were not destroyed. In our study, most bile duct changes involved dilatation of the intrahepatic bile duct adjacent to blood vessels equal to or less than 3 mm in diameter peripheral to the ablation zone, as reported by other investigators [12–18]. Neither the central intrahepatic nor the extrahepatic bile ducts were dilated.
Because some patients did not show bile duct change until late, one cannot assume that it will not occur if it is not present on short-term follow-up CT performed within 4 months after radiofrequency ablation [16]. In our study, bile duct changes in three (4%) of 69 patients were not seen on CT performed within 4 months after radiofrequency ablation. We speculate that a variable time period is needed for thermal injury to induce bile duct stricture.
It is reported that radiofrequency ablation–induced bile duct dilatation can progress during a subsequent follow-up period and may require interventional drainage for its decompression [15–18]. Recently, prophylactic placement of a biliary stent or radiofrequency ablation while cooling the biliary ducts with saline has been used to attempt to prevent biliary damage when treating tumors close to or adjacent to the main bile ducts [17, 35]. The definitive role of those preliminary techniques, however, remains undetermined. In our study, none of the patients showed changes in either central intrahepatic or extrahepatic bile ducts. Although nine (13%) of 69 patients with bile duct changes showed a slight progression during the follow-up period and three of these tumors were adjacent to main bile ducts, no interventional procedures were warranted.
In our study, only one (1.5%) of 69 patients showed a symptomatic complication of cholangitis. The cause of the cholangitis was unknown. Since the first description of infectious complication of radiofrequency ablation such as cholangitis or liver abscess, several authors [36, 37] have reported that they provide prophylactic antibiotics. However, we still have no consensus on the need for prophylactic antibiotics in all patients who are preparing to undergo radiofrequency ablation, because the frequency of infectious complication reported was too low [12]. In our study, two patients with bile duct changes after radiofrequency ablation had a history of biliary tract manipulation, but they were found to have no infectious complication after radiofrequency ablation, despite the fact that prophylactic antibiotics were not administered. On the basis of our results, therefore, we do not recommend the routine use of prophylactic antibiotics before radiofrequency ablation.
Our study has some limitations. First, some biases inherent to its
retrospective design exist. We selected only those patients who were treated
with radiofrequency ablation as the first-line treatment. Therefore, if all
patients treated by combined therapy with radiofrequency ablation and
transcatheter arterial chemoembolization were included in the study, the
frequency of bile duct changes after radiofrequency ablation might have
changed. Second, many tumors were not pathologically proven but were
considered to be hepatocellular carcinoma on the basis of characteristic
imaging findings coupled with an elevated level of serum -fetoprotein.
We had pathologic proof in a substantial number of the tumors, but it is
impractical to perform invasive biopsy for the confirmation of all tumors seen
on CT, especially in patients with cirrhosis. In addition, we focused on
assessing a complication of radiofrequency ablation, not proving that the
tumors treated with radiofrequency ablation were hepatocellular carcinoma.
Third, bile duct changes in the liver surrounding the ablation zone were not
pathologically proven to have resulted from thermal damage to the bile ducts
or for any reason. Pathologic proof in these patients was not possible because
most patients with bile duct changes were asymptomatic. Also, only three of 12
patients with biloma were confirmed to have a communication between the bile
duct and the biloma by means of percutaneous transhepatic or endoscopic
retrograde cholangiography or CT, and the remaining nine cases were not
confirmed. However, confirmatory diagnostic studies were not necessary because
most patients with biloma did not present any symptoms.
In conclusion, bile duct changes were frequent after radiofrequency ablation of hepatocellular carcinoma. Our results indicate that most bile duct changes were not transient findings but rather were irreversible changes caused by thermal damage to the bile ducts after radiofrequency ablation. However, most changes were of no clinical significance, and major complications requiring additional treatment were rare.
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