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1 Department of Radiology, 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.
3 Biostatistics Unit, Samsung Medical Center, Sungkyunkwan University School of
Medicine, Seoul 135-710, South Korea.
Received July 29, 2004;
accepted after revision September 25, 2004.
Address correspondence to H. K. Lim.
Abstract
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MATERIALS AND METHODS. Over a 4-year period, 603 patients with 831 hepatocellular carcinomas measuring 5 cm or less in maximum diameter who underwent a total of 751 percutaneous radiofrequency ablation procedures were enrolled in this study. We retrospectively reviewed the medical records and analyzed the overall frequency of liver abscess, risk factors for abscess, and clinical features of the patients. The relationships between liver abscess and potential risk factors were analyzed using either generalized estimating equations or multiple logistic regression analysis.
RESULTS. Liver abscess developed in 14 tumors of 13 patients after 13 (13/751 [1.7%]) ablation procedures. Generalized estimating equations and multiple logistic regression analysis of various potential risk factors revealed that preexisting biliary abnormality prone to ascending biliary infection (p = 0.0088), tumor with retention of iodized oil from previous transcatheter arterial chemoembolization (p = 0.040), and treatment with an internally cooled electrode system (p = 0.016) were associated with a significant risk of liver abscess formation. No patient died of liver abscess, and all successfully recovered from liver abscess with parenteral antibiotics and percutaneous clearance of pus.
CONCLUSION. Although liver abscess formation was infrequent in patients who underwent percutaneous radiofrequency ablation for hepatocellular carcinoma, the patients with significant risk factors—preexisting biliary abnormality prone to ascending biliary infection, tumor with retention of iodized oil, and treatment with an internally cooled electrode system—for liver abscess formation should be closely monitored after treatment.
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Although percutaneous radiofrequency ablation is considered a safe treatment technique, a variety of complications have been reported [13-17]. Of these, liver abscess is one of the most common complications. A liver abscess-related mortality after radiofrequency ablation has been documented [13]. To the best of our knowledge, however, no study has previously focused on the risk factors for developing liver abscess after percutaneous radiofrequency ablation [18]. The purpose of this study was to clarify the frequency and risk factors of liver abscess formation after percutaneous radiofrequency ablation in patients with hepatocellular carcinoma.
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All patients met the following criteria for treatment with percutaneous
radiofrequency ablation: a single nodular hepatocellular carcinoma 5 cm or
less in maximum diameter; multinodular hepatocellular carcinomas (
3), with
each tumor measuring up to 3 cm in maximum diameter; tumors visible at
sonography; tumors accessible via percutaneous approach; absence of portal
venous thrombosis and extrahepatic metastases; Child-Pugh class A or B liver
cirrhosis; prothrombin time ratio greater than 50% (prothrombin time with
international normalized ratio [INR] < 1.7); and platelet count greater
than 70,000 cells/mm3 (70 cells x 109/L). The
institutional review board approved this study, and written informed consent
was obtained from all patients.
The diagnosis of hepatocellular carcinoma was confirmed by percutaneous
needle biopsy in 128 tumors of 124 patients. The 703 tumors of the remaining
479 patients were considered to be hepatocellular carcinomas on the basis of
imaging findings and elevated serum tumor marker (
-fetoprotein level
> 200 ng/mL [> 200 µg/L]) (n = 345) or satisfaction of at
least two coincident radiologic findings compatible with hepatocellular
carcinoma on sonography, CT, and MRI (n = 358). The imaging findings
interpreted as suggestive of hepatocellular carcinoma were newly presenting,
residual, or recurrent tumors at follow-up sonography or CT in patients with
chronic liver disease or characteristic enhancement pattern on
contrast-enhanced multiphase CT or dynamic contrast-enhanced MRI (i.e.,
hypervascularization on hepatic artery phase and washout pattern on
equilibrium phase).
Of the 603 patients, 259 were considered not eligible for hepatectomy and were referred for percutaneous radiofrequency ablation because of prior hepatic resections (n = 104) or poor medical condition, including insufficient hepatic reserve (n = 155). The remaining 344 patients refused hepatectomy and wanted percutaneous radiofrequency ablation. Five hundred sixty-seven patients (94%) had liver cirrhosis as a result of hepatitis B (n = 413), hepatitis C (n = 112), alcoholism (n = 34), or unknown cause (n = 8). Twenty-four patients had chronic hepatitis B without cirrhosis. The remaining 12 patients had no chronic hepatocellular disease.
At the time of radiofrequency ablation, 385 patients had Child-Pugh class A cirrhosis and 182 had Child-Pugh class B cirrhosis. The 237 patients with liver cirrhosis and eight patients with chronic hepatitis were confirmed by percutaneous biopsy, and liver diseases of the remaining patients were clinically diagnosed using imaging (sonography and CT) and laboratory findings.
Radiofrequency Ablation Procedure
Various radiofrequency devices, manufactured by three companies, were used
for percutaneous radiofrequency ablation
[7,
11,
19]. From April 1999 to
February 2000, we used only a 50-W monopolar radiofrequency generator (model
500 series, Radiofrequency Interstitial Thermal Ablation Medical Systems) and
a multitined expandable electrode with four or seven retractable lateral
prongs because no other device was available during that period. Later, we
also used the more recent model 1500 series (Radiofrequency Interstitial
Thermal Ablation Medical Systems), which is equipped with a more powerful
generator (150 W) and a larger multitined expandable electrode that is 5 cm in
diameter. The other device (radiofrequency 2000 system, RadioTherapeutics)
incorporated a 100-W generator; a LeVeen 15-gauge monopolar array electrode
with 10 individual hooklike arms; and needle electrodes 2, 3, and 3.5 cm in
diameter. Since July 2000, we have usually used the internally cooled
electrode system (Cool-tip RF System, Radionics). This system includes an
electrode, the tip of which is internally cooled by chilled water. 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 in a
triangular arrangement on a common handle.
In this study, the model 500 series was used in 191 tumors, the model 1500 series in 82, the radiofrequency 2000 system in 133, and the internally cooled electrode in 425. We selected the type of radiofrequency devices on a case-by-case basis depending on the availability of the electrode in stock and the size and location of the tumors. All radiofrequency ablation procedures were performed percutaneously under real-time sonographic guidance by four experienced radiologists. Details in patient preparation and ablation techniques have been reported previously [19, 20].
All patients were treated under IV conscious sedation and local anesthesia. Patients' cardiovascular and respiratory systems were continuously monitored during the procedures. 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 and the entire tumor itself, we were not able to obtain the satisfactory ablative margin in the parts abutting bowel or greater vessels. For tumors larger than 3 cm in maximum diameter, we performed, if it was possible, multiple overlapping ablations (2-5 overlapping ablations; mean, 2.6). A total of 174 procedures involved overlapping ablations. No patients received prophylactic antibiotics at the time of ablation procedures.
Follow-Up Imaging
Immediately after radiofrequency ablation, all patients were evaluated with
gray-scale sonographic examinations to ascertain whether any acute
complications had occurred. For the early evaluation of therapeutic response,
we performed contrast-enhanced sonography, CT, or both depending on the
location of the ablation zone and the status of the acoustic window. If either
multiple tumors or a bad sonic window was present, patients underwent
immediate follow-up CT.
Postprocedural contrast-enhanced CT examinations were performed with one of two kinds of helical scanners (HiSpeed or LightSpeed QX/I, GE Healthcare) immediately (within 2 hr) after 311 radiofrequency ablation procedures. A total of 120 mL of nonionic contrast material (Ultravist 300 [300 mg I/mL iopromide], Schering) was administered with an automatic power injector at a rate of 3-4 mL/sec. Images were obtained before and 30, 60-70, and 180 sec after the initiation of IV contrast material injection, representing the unenhanced, hepatic arterial, portal venous, and equilibrium phases, respectively.
Using a single-detector helical CT scanner, we obtained images in a craniocaudal direction with 7-mm collimation and 7-mm/sec table speed during a single breath-hold acquisition of 25-30 sec, depending on liver size. The parameters of the MDCT examination were a 4 x 2.5 mm detector configuration, a table speed of 15.0 mm/sec (pitch of 0.75), and a 5-mm slice thickness.
After 522 procedures, the radiologist who had performed radiofrequency ablation evaluated therapeutic response and complications using contrast-enhanced sonography. These evaluations were made the morning after the procedure. We used a microbubble contrast agent, SH U 508A (Levovist, Schering), which is a suspension of galactose in sterile distilled water. Details on the contrast-enhanced sonographic techniques have been reported in other studies [21, 22].
All patients underwent follow-up four-phase helical CT—both unenhanced and contrast-enhanced three-phase scanning—1 month after radiofrequency ablation. These scans were used as a baseline study to evaluate therapeutic efficacy. Residual unablated tumors were defined as irregular peripheral enhancing foci in the ablation zone on either contrast-enhanced sonography or early follow-up CT immediately or 1 month after radiofrequency ablation [20, 23]. When found, residual unablated tumors were usually treated with additional radiofrequency ablation. If additional radiofrequency ablation was not feasible because of poor conspicuity on sonography or the presence of concurrent multiple new lesions transcatheter arterial chemoembolization was performed. In cases of complete ablation of the tumor with no appearance of new tumor in other sites of the liver at 1-month follow-up CT, subsequent contrast-enhanced three-phase helical CT examinations were repeated every 2-4 months as our follow-up strategy. In 21 patients, however, un-scheduled follow-up CT examinations were performed 3-20 days after ablation procedures because of suspected complications or operator preference.
Clinical Diagnosis
During the follow-up period, we attempted to detect acute complications,
most notably liver abscesses. An ablation zone with a peripheral enhancing rim
on CT was considered diagnostic of liver abscess if the patients met any of
the three following conditions: bacteria were cultured from the aspirate or
blood samples; aspirate from the ablation zone had a purulent appearance at
macroscopic or microscopic examination; or the associated fever was higher
than 38.5°C, lasted more than 5 days, and the leukocyte count was greater
than 12 x 109/L without other causes
[18]. Anaerobic and aerobic
aspirate and blood cultures were performed.
The treatment given for the liver abscess and its outcome were evaluated by means of the review of medical records. Of the patients with abscesses, sepsis was considered if the patients met two or more of the four following conditions: a body temperature higher than 38°C or lower than 36°C, a heart rate higher than 90 beats/min, a respiratory rate higher than 20 breaths/min, or a leukocyte count greater than 12,000 or less than 4,000 cells/mm3 [24].
Evaluation of Risk Factors
We defined multiple preablation conditions as potential risk factors for
liver abscess formation after radiofrequency ablation
[18,
25,
26]. These included a history
of transcatheter arterial chemoembolization, biliary abnormalities, diabetes
mellitus, multiple tumors, Child-Pugh class B cirrhosis, tumor with retention
of iodized oil, local tumor progression after prior radiofrequency ablation,
and relatively large tumors. We also evaluated the type of electrode system
used in the ablation procedures with respect to the development of liver
abscesses. Retrospectively reviewing the medical records and radiologic
examinations, we noted the coexistence of each predisposing factor for every
radiofrequency ablation procedure.
We classified biliary abnormalities into two types, as suggested in a previous report [25]. One was a biliary abnormality that was prone to ascending biliary infection after biliary tract manipulation. Biliary tract manipulation includes endoscopic papillotomy, external biliary drainage, and bilioenteric anastomoses after surgical procedures. Rare bilioenteric anastomosis without biliary tract manipulation, such as choledochoduodenal fistula, was also included in this type of biliary abnormality. Another biliary abnormality was defined as simple dilatation of the intrahepatic ducts. This simple dilatation could be caused by tumor invasion, extrinsic compression, stricture, or Clonorchis sinensis infections in the bile duct. Such conditions were shown on imaging studies, including CT and cholangiography.
Statistical Analysis
The frequency of liver abscess was based on the 751 ablation procedures
performed. The relationships between liver abscess and the six
variables—history of transcatheter arterial chemoembolization, biliary
abnormality prone to ascending biliary infection, simple dilatation of
intrahepatic bile ducts, diabetes mellitus, multiplicity of tumor, and
Child-Pugh class B—were analyzed by using generalized estimating
equations because of clustering effects in a single patient. The relationships
between liver abscess and the four variables—tumor with retention of
iodized oil from previous transcatheter arterial chemoembolization, local
tumor progression after prior radiofrequency ablation, size of tumor, and
treatment with internally cooled electrode system—were analyzed by
multiple logistic regression analysis. A p value of less than 0.05
was considered to indicate a statistically significant difference. Statistical
calculations were performed with a commercially available software package
(SAS software [version 8.2], SAS Institute).
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The statistical analysis of various potential risk factors revealed that preexisting biliary abnormality prone to ascending biliary infection (p = 0.0088), tumor with retention of iodized oil from previous transcatheter arterial chemoembolization (p = 0.040), and treatment with an internally cooled electrode system (p = 0.016) were the three most significant risk factors for developing liver abscess after percutaneous radiofrequency ablation (Table 2).
CT Findings
Five (38%) of the 13 patients with abscess formation underwent immediate
follow-up CT. In two of these patients, a wedge-shaped perfusion defect
(possible infarct) was noted in the liver peripheral to the ablation zone
(Table 3).
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In all patients, liver abscesses were identified on CT within 3-30 days after ablation. The CT findings of the abscesses that developed in the ablation zone were similar to those of other usual abscesses. All of the abscesses appeared as low-attenuation lesions, and eight (57%) of the 14 abscesses had enhancing rims with characteristic layering pattern (Figs. 2A, 2B, 2C, and 2D). However, clustering of small cystic lesions was not seen. In 11 (79%) of the 14 abscesses, a substantial amount of air was found at CT. It mostly appeared as bubbles, and air-fluid level was observed in only one abscess.
In two patients with air bubbles at immediate follow-up CT, the air showed an interval increase in the amount at later follow-up CT performed 3 and 5 days after ablation procedures. In one of three other patients with immediate follow-up CT in which air had not been found, air bubbles were newly observed in the infected ablation zone (abscess) at later follow-up CT 30 days after ablation. During the CT examinations in which the abscesses were identified, venous thrombosis was noted in the right main portal vein in one patient and in the right hepatic vein in another patient.
Clinical Features
Of the 13 patients with abscess formation, 10 (77%) who had a fever or
experienced abdominal pain for 3-20 days (mean, 8.8 days; median, 5.5 days) or
both after ablation procedures visited the emergency department of our
institution (Table 3).
Three of these patients underwent sonography, which showed hyperechogenicity
resulting from air bubbles in the ablation zones
(Fig. 1B). These patients
underwent additional CT to determine the definite diagnosis and the treatment
plan. Seven other patients underwent CT without sonography. Two patients (15%)
who were asymptomatic and subfebrile did not visit the hospital before the
scheduled 1-month follow-up CT examination, at which time abscesses were
discovered. The remaining one visited a local clinic near his home 5 days
before visiting our hospital on the scheduled day. He had a fever (38.5°C)
and took antipyretics.
Six (43%) of the 14 abscesses were punctured under sonographic guidance for clearing pus. Two abscesses (14%) were drained with a 10.5-French catheter for 7 and 10 days before removal of the drain, and four (29%) were aspirated with a needle only once (n = 2) or twice (n = 2). Aspirate cultures tested positive for Clostridium perfringens, Staphylococcus aureus, Aeromonas hydrophila, and Klebsiella pneumoniae. Blood cultures from other patients tested positive for Enterococcus species and gram-negative bacilli. All 13 patients were treated with IV and oral antibiotics. Four (31%) of 13 patients had sepsis, but all patients recovered after adequate treatment.
During the follow-up period (range, 6-36 months; mean, 12.8 months), no local tumor progression was noted in the ablation zones of 14 abscesses at subsequent follow-up CT. Five (38%) of 13 patients showed new hepatocellular carcinomas in other parts of the liver before either additional radiofrequency ablation or transcatheter arterial chemoembolization. One of these five patients was treated with additional radiofrequency ablations, and the remaining four received transcatheter arterial chemoembolization.
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One study by the Italian Multicenter Radiofrequency Study Group [16] listed six deaths (0.3%) and 50 major complications (2.2%), including six liver abscesses (0.3%), in 2,320 patients. Another multicenter study by the Korean Radiofrequency Study Group [15] showed 37 major complications (2.4%) of 1,520 radiofrequency ablation procedures in 1,139 patients with hepatic tumors, among which liver abscess (n = 10, 0.66%) was the most common major complication. In a more recent study [17], liver abscess (n = 7, 2.0%) was also the most common major complication in 350 radiofrequency ablation sessions of 582 hepatic tumors in 312 patients. The frequency of abscess formation after radiofrequency ablation in our study (1.7%) is similar to those of the aforementioned studies.
Although the actual mechanism of abscess formation after radiofrequency ablation is still not fully understood, subsequent bacterial contamination and growth in the zone of coagulation necrosis may result in abscess [15]. Bilioenteric anastomosis leads to a colonized biliary tree and may enhance the development of abscess after ablation. According to a prior report [28], bilioenteric anastomosis is related to retrograde enteric bacterial contamination of the biliary tract in 90% of patients with abscess after intervention procedures. Radiofrequency ablation can connect the biliary tract and ablation zone by thermal injury to the bile ducts, and then the ablation zone can be contaminated by enteric bacteria.
In the study of the Italian Multicenter Radiofrequency Study Group [16], two of the six patients with abscesses had pneumobilia related to previous gastrointestinal surgery. Vogl et al. [29] found that patients with liver metastasis from pancreatic carcinoma who had undergone Whipple's operation had significantly more abscesses than those with metastases from other primary tumors undergoing laser-induced thermotherapy. In our study, nine patients had the conditions with biliary abnormality prone to ascending biliary infection. In two (22%) of these, abscesses occurred after ablation procedures. In one patient, cultured organisms (Enterococcus species) were found to be from an enteric source. In this case, previous hepaticojejunostomy was likely responsible for abscess formation.
Analyzing 12 tumors from 11 other patients, we found that the index tumors with retained iodized oil may have been related to the development of abscess in five patients. During the ablation procedures, decreased blood flow after embolization and the oil content in the tumors could have induced severe destruction of the tumors by enhancing thermal effects [30, 31]. In five other patients, we suppose that the use of an internally cooled electrode system was one of the main causes of abscess development. The greater power (200 W) of the internally cooled electrode system (in comparison with the lower power, multitined, expandable electrode systems) is likely to be the most important reason why its use became a significant risk factor. In the last patient (patient 4 in Table 1), the cause of liver abscess could not be determined.
Spies et al. [28] previously reported that prophylactic antibiotic administration was effective in the prevention of infectious complications in interventional procedures. In two recent reports [18, 26], however, a prophylactic regimen failed to prevent the development of cholangitis or liver abscess after either chemoembolization or percutaneous ethanol injection therapy for patients with bilioenteric anastomosis. The study of the Italian Multicenter Radiofrequency Study Group [16] also reported that liver abscesses after radiofrequency ablation developed in patients with prior biliary reconstructive surgery (n = 2) or diabetes mellitus (n = 1) despite prophylactic antibiotics.
Further prospective studies are needed to determine the effectiveness of aggressive antibiotic prophylaxis when ablation therapy is planned in patients with bilioenteric anastomosis or other risk factors. The presence of bilioenteric anastomosis may not be a contraindication to ablation therapy because liver abscesses do not always occur in these patients. In a study for which a literature review was conducted, the authors suggested that prophylactic antibiotics might be appropriate in high-risk patients with biliary abnormalities, immunosuppression, concomitant infection, or severe cirrhosis to prevent liver abscesses after radiofrequency ablation [6].
In patients with abscess who underwent sonographic examinations at our emergency department, massive air echogenicity was visualized in the ablation zones. The increased echogenicity, due to microbubbles of gas produced by radiofrequency ablation, is known to remain for 15-180 min after radiofrequency ablation [32]. Thus, we strongly suspect abscess when substantial air echogenicity is detected at sonography 1 day or more after ablation. Unlike sonography, CT can detect minimal gas bubbles, in some patients, on follow-up examinations 1 day or more after treatment [20]. Gas bubbles detected on CT several days after ablation can easily be misdiagnosed as abscesses, especially if the patient shows postablation syndrome [33]. C-reactive protein concentration in serum, a relatively specific indicator of infection, may distinguish patients with postablation syndrome from those with infection [34].
After percutaneous radiofrequency ablation for hepatocellular carcinomas, the rate of local tumor progression generally exceeded 10% [21, 22]. In our patients with abscess formation, however, local tumor progression was not found at subsequent follow-up CT. We can attribute the absence of local tumor progression to excessive destruction of adjacent liver parenchyma surrounding the ablation zone, in which the microscopic residual tumor could regrow. However, we need further studies with more patients to define the relationship between abscess formation in the ablation zone and local tumor progression.
This study has several limitations. First, symptomatic patients who had been suspected by clinicians to have an abscess could have been among the cases with the diagnosis of an abscess. The frequency of liver abscess in our study was presumably underestimated because a small number of patients with abscess had neither symptoms nor signs indicating infection. Second, only five (38%) of 13 patients with abscess formation underwent immediate follow-up CT because this study was performed retrospectively. Thus, it is difficult to evaluate which predictors (e.g., infarct, early venous thrombosis, and so on) for abscess development are evident on immediate follow-up CT. Finally, we recently prefer to use internally cooled electrodes because of the simplicity of technique and good therapeutic effect.
As our experience with radiofrequency ablation of hepatocellular carcinomas increases, we have become more aggressive in performing radiofrequency ablation even for difficult cases, which may increase the incidence of major complications. This might have influenced our result that the use of an internally cooled electrode was a significant risk factor.
Our results suggest that operators should pay attention to the risks of abscess formation after radiofrequency ablation for hepatocellular carcinoma in patients with preexisting biliary abnormality prone to ascending biliary infection, tumor with retention of iodized oil, and treatment with an internally cooled electrode system. Prophylactic use of antibiotics might be recommended for patients meeting these conditions. However, a meticulous aseptic procedure and closer monitoring of the patients during and after radiofrequency ablation procedures are more important to prevent an abscess from forming and detect an abscess early. When patients are discharged after radiofrequency ablation, they should be advised to return if they continue to have a fever and experience abdominal pain.
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