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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 April 7, 2007;
accepted after revision June 24, 2007.
Address correspondence to H. K. Lim.
Abstract
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MATERIALS AND METHODS. Sonographically guided percutaneous radiofrequency ablation with artificial ascites was performed in 25 patients with 34 HCCs using an internally cooled electrode radiofrequency system. At least one hepatic dome tumor in each patient was considered difficult to treat percutaneously because of partially visible tumor (n = 16) or poor electrode path (n = 9) on planning sonography. We artificially induced ascites before radiofrequency ablation by dripping 5% dextrose in water (D/W) solution to improve tumor visibility or electrode path and to separate the radiofrequency ablation zone from the diaphragm. We assessed the technical feasibility, safety, and efficacy of this technique with clinical and CT follow-up for at least 4 months (mean, 281.4 days)
RESULTS. Artificial ascites was successfully achieved in 22 (88%) of 25 patients with the administration of a mean of 348 mL of D/W solution for an additional mean time of 9.3 minutes. There was substantial improvement in the visibility in 93.4% (15/16) of the partially visible tumors and in achieving a better path in 77.8% (7/9) of the tumors with a poor electrode path. The primary technique effectiveness rate for hepatic dome tumors was 96% (24/25) at 1-month follow-up CT. There was no diaphragmatic thermal injury in all but one case. No complication related to artificial ascites occurred during the follow-up period.
CONCLUSION. Percutaneous radiofrequency ablation with artificial ascites appears a feasible, safe, and effective technique for treating HCC of the hepatic dome.
Keywords: artificial ascites • complication • hepatocellular carcinoma • imaging-guided tumor ablation • radiofrequency ablation
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Imaging-guided tumor ablation can be performed via various approaches from the percutaneous route to open laparotomy. Most operators prefer the percutaneous approach, but it is not always possible depending on the characteristics of the index tumor. If the tumor is located high in the subcapsular portion of the hepatic dome, sonographically guided percutaneous radiofrequency ablation is technically challenging because of partial visibility of the tumor or a poor electrode path because of overlapped lungs or ribs, and there is risk of collateral thermal damage to the diaphragm [11-13].
Several technical measures have been suggested to solve this problem. They include different approaches (e.g., percutaneous transthoracic, laparoscopic, or open laparotomy) [14], different guiding techniques [15, 16], or artificial fluid into the pleural or peritoneal space [17-25]. However, to our best knowledge, there have been no large-series studies investigating the usefulness of artificial ascites in treating HCCs of the hepatic dome. The purpose of this study was to assess the feasibility, safety, and efficacy of sonographically guided percutaneous radiofrequency ablation with artificial ascites for HCC in the hepatic dome.
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5 cm in maximum diameter, multinodular (up to three) HCCs 3 cm
in maximum diameter each, absence of portal venous thrombosis, Child-Pugh
class A or B liver cirrhosis, prothrombin time ratio > 50% (prothrombin
time with international normalized ratio < 1.7), and a platelet count >
70,000 cells/mm3 (70 cells x 109/L). Among them,
25 patients with 34 nodular HCCs underwent radiofrequency ablation with
assistance of artificial ascites because at least one tumor was inaccessible
via the percutaneous approach because of the high location of the tumor. This
study was approved by our institutional review board. Informed consent was
obtained from all patients by one interventional radiologist who performed the
procedure. There were 18 men and seven women (age range, 48-81 years; mean, 62.5 years). Thirteen patients were considered not eligible for hepatic resection, and 12 patients voluntarily preferred radiofrequency ablation despite surgery also being feasible. All patients had liver cirrhosis as a result of hepatitis B (n = 18), hepatitis C (n = 5), hepatitis B and C (n = 1), or alcoholism (n = 1). At the time of the radiofrequency ablation, 21 patients had Child-Pugh class A cirrhosis and four had Child-Pugh class B cirrhosis. Fourteen patients underwent radiofrequency ablation with artificial ascites as a first-line treatment, whereas 11 patients had undergone surgery (n = 2), transarterial chemoembolization (TACE) (n = 6), radiofrequency ablation (n = 1), or combined treatment (n = 2) before radiofrequency ablation with artificial ascites.
A total of 25 patients had 34 tumors: a single tumor in 17 patients, two tumors in seven, and three tumors in one. The 25 tumors in the hepatic dome measured 1.0-3.0 cm at their maximum diameters (mean, 2.1 cm). The tumors in the hepatic dome were located at segment VIII in 13 patients, segment VII and VIII in four, segment VII in three, segment IV in four, and segment II in one. All 25 tumors in the hepatic dome were located at the subcapsular portion of each segment. The reasons that tumors were considered inaccessible via the percutaneous approach at sonography were that the tumor was only partially visible in 16 tumors and there was no adequate radiofrequency electrode path because of the lung parenchyma or costochondral junction in nine tumors (Table 1).
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The diagnosis of HCC was confirmed by percutaneous needle biopsy in three
tumors of three patients. The remaining 31 tumors in 22 patients were
considered to be HCC on the basis of characteristic imaging findings and an
elevated serum tumor marker (
-fetoprotein > 400 mg/L) (n =
2) or satisfaction of at least two coincident radiologic findings that were
compatible with HCC among CT, MRI, sonography, and angiography (n =
29) [27].
Induction of Artificial Ascites
We selected the peritoneal space under sonographic guidance with a 6-French
angiosheath using the Seldinger technique. All procedures for induction of
artificial ascites were performed by one interventional radiologist with 13
years of experience in sonographically guided intervention. For the tumor in
the right lobe and segment IV right to the falciform ligament, we selected the
right 7-8 intercostal space along the anterior axillary line. For the tumor in
segments II and III, we selected the epigastric area.
After administering local anesthetic to the skin at the puncture site using 2% lidocaine, we inserted an 18-gauge sheathed needle just to the peritoneum. To effectively select the peritoneal space, we instructed the patient to slightly inhale downward to displace the level of the liver parenchyma and to breath-hold. Then we advanced the sheath needle into the subcapsular portion of the liver parenchyma. After removal of the inner stylet of the sheath needle, we instructed the patient to fully exhale and breath-hold again. At this moment, the tip of the sheath usually remained in the peritoneal space because of its retraction from upward-displaced hepatic parenchyma with full expiration. At this moment, we quickly inserted a 0.035-inch guidewire through the sheath and checked by sonography whether the wire was located in the peritoneal space. Finally, we placed a 6-French angiosheath over the guidewire.
After placement of the angiosheath into the peritoneal space, we opened a three-way stopcock at the side arm of the angiosheath. This stopcock was connected to 1,000 mL of 5% dextrose in water (D/W) solution at room temperature. We did not try any position change of the patient to collect the infused fluid at the desired portion. If the entire boundary of the index tumor could be visualized and a safe radiofrequency electrode path could be achieved by downward displacement of the liver with sonographic monitoring, we considered the induction of artificial ascites technically successful. We then performed the conventional radiofrequency ablation procedure (Fig. 1).
Radiofrequency Ablation
All radiofrequency ablation procedures were also performed on an inpatient
basis by the same interventional radiologist with 9 years of experience in
radiofrequency ablation. We used internally cooled electrodes and a 200-W
generator (Cool-tip, Valleylab). All the patients were treated under IV
conscious sedation and local anesthesia. Our therapeutic strategy of
radiofrequency ablation was to include a peripheral margin of at least 0.5 mm
of normal hepatic parenchyma surrounding the tumor and the entire tumor
itself. Depending on tumor size and electrode type, we performed a total of 28
sessions in 25 patients (1 or 2 sessions per patient; mean, 1.12) with single
or multiple overlapping ablations (1-4 overlapping ablations; mean, 1.8). We
used a single (3-cm active tip) electrode in 33 of 34 tumors and a cluster
electrode in one tumor. We cauterized the electrode path during retraction of
the electrode to minimize bleeding after ablation. We did not aspirate or
drain the infused artificial ascites after the ablation procedure.
Follow-Up After Ablation
For the early evaluation of the therapeutic response, we performed
contrast-enhanced CT immediately after radiofrequency ablation. Postprocedural
CT examinations were performed immediately (within 4 hours) with one of two
helical scanners (HiSpeed or LightSpeed QX/i, GE Healthcare). The axial images
were obtained before and at 30, 60-70, and 180 seconds after IV contrast
material injection. Coronal and sagittal reformatted images were also
obtained. The radiologist who performed the radiofrequency ablation procedure
also evaluated the therapeutic response and any immediate complications
including hemoperitoneum and diaphragmatic thermal injury.
All the patients underwent a follow-up four-phase CT 1 month after radiofrequency ablation. Residual tumors were defined as irregular peripheral-enhancing foci in the ablation zone at contrast-enhanced follow-up CT, immediately or 1 month after radiofrequency ablation. In cases of complete ablation of the tumor with no appearance of a new tumor in other sites of the liver at 1-month follow-up CT, subsequent CT examinations were repeated every 2-4 months as part of our follow-up protocol.
Assessment of Technical Feasibility and Safety of Artificial Ascites
To evaluate the technical feasibility of artificial ascites, we recorded
how many needle punctures were required to select the peritoneal space, time
for selection of the peritoneal space (from skin anesthesia to placement of
the angiosheath into the peritoneal space), time for successful induction of
artificial ascites, total amount of artificial ascites infused, and maximum
distance between the peritoneum and hepatic capsule at sonography. We also
assessed whether artificial ascites improved the visibility of the index tumor
or radiofrequency electrode path and technical problems in the induction of
artificial ascites.
To assess the safety related to artificial ascites, we evaluated whether the artificial ascites was shifted into the pleural space and measured the Hounsfield units of the artificial ascites around the radiofrequency ablation zone on the immediate CT to evaluate whether artificial ascites may have a role in the development of hemoperitoneum after radiofrequency ablation. In addition, abdominal sonography was performed to evaluate whether artificial ascites remained and caused any intermediate complication at 1 week after the procedure in the initial seven patients. Delayed complications related to artificial ascites were assessed with a follow-up four-phase CT 1 month after radiofrequency ablation and then at every 2-4 months for at least 6 months. Complications were assigned to major and minor categories [27].
Assessment of Diaphragmatic Injury and Therapeutic Effectiveness
To assess the protective effect of artificial ascites, we evaluated whether
the diaphragm adjacent to the radiofrequency ablation zone in the hepatic dome
showed any evidence of swelling at immediate follow-up CT compared with
pretreatment CT or whether any patient complained of sustained shoulder pain
during the follow-up period.
To assess the therapeutic efficacy of ablation, we evaluated the primary (technique) effectiveness in terms of residual tumor with 1-month follow-up CT. Local tumor progression was determined when a subsequent follow-up CT showed any growing and enhancing tumor in the ablation zone where there had been complete primary effectiveness (i.e., no evidence of residual tumor) for at least 6 months. Evaluation of secondary (technique) effectiveness or survival analysis was beyond the scope of the current study.
Statistical Analysis
Data analyses in calculating the mean and median value of measurement were
performed with commercially available software (Excel 2000, Microsoft).
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Safety of Artificial Ascites
The artificial ascites was partially shifted into the right pleural space
in 14 of 25 patients at immediate follow-up CT. The attenuation of artificial
ascites around the radiofrequency ablation zone ranged from -8 to 28 H (mean,
12.7 H). No patients showed abnormal vital signs and decreasing hemoglobin
levels until the day after the procedure. The artificial ascites in six of
seven patients who underwent 1-week follow-up sonography had completely
disappeared, and a minimal amount of ascites was noted in the perihepatic
space in one patient with no irritating peritoneal signs. All patients showed
complete absorption of artificial ascites and the shifted pleural effusion at
1-month follow-up CT. No patients showed any clinical signs of delayed
complications such as hemoperitoneum or peritonitis during follow-up of at
least 4 months.
Diaphragmatic Injury and Therapeutic Effectiveness
One patient with technical failure of artificial ascites because of
postoperative adhesions showed reversible thermal injury of the diaphragm
(Fig. 4A,
4B,
4C,
4D,
4E). The remaining 24 patients
did not show diaphragmatic swelling at immediate follow-up CT, and none
complained of sustained shoulder pain. The primary technique effectiveness was
96% (24/25) at 1-month follow-up CT. On the basis of tumor in the hepatic
dome, the rate of local tumor progression was 16% (4/25). On the patient
basis, the rate of new recurrent tumors was 36% (9/25).
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Regarding the techniques for induction of artificial ascites, Raman et al. [24] in an experimental model used an 18-gauge Chiba needle for insertion into the pocket of lidocaine at the plane between the peritoneum and the liver capsule. This method seems to be the most popular technique for induction of artificial ascites. However, during the procedure an operator should monitor closely whether the tip of the needle is located in the peritoneal space. Our technique using the angiosheath may provide rapid induction of artificial ascites because of the larger bore of the route without the necessity of monitoring the tip of the needle during the ablation.
Our study also showed that induction of artificial ascites is a safe procedure. Traditionally, the ascitic fluid was thought to wash away thrombogenic material at the puncture site and decrease or eliminate the "tamponade effect" from the opposing parietal peritoneum against the liver [24, 32]. However, in our study, there was no case of complication related to artificial ascites, such as hemoperitoneum. This may result from coagulation of the electrode path during removal of the electrode. Furthermore, based on our results, we now doubt whether ascites should be regarded as a relative contraindication for percutaneous radiofrequency ablation in patients with correctable coagulopathy [33].
The main limitation of artificial ascites appears to be peritoneal adhesions due to previous treatments (surgical resection, TACE, or thermal ablation) and the tumor in the bare area of liver [24, 34]. In our results, two of three cases with technical failure had a history of previous surgery located in segment VII. Therefore, an operator should keep in mind that these two factors can be a cause of technical failure for induction of artificial ascites and consider an alternative approach or treatment.
Many studies have reported on improving the sonic window using artificial pleural effusion [10, 20, 21]. Minami et al. [20] and Koda et al. [10] reported the feasibility and safety of artificial pleural effusion in radiofrequency ablation for HCC in the hepatic dome. Both studies reported a high local control rate of 92-96% with the assistance of artificial pleural effusion. The adverse effect was minimal, including mild cough and dyspnea in some patients. Toyoda et al. [15] and Shibata et al. [16] reported CT-guided transpulmonary radiofrequency ablation without any artificial fluid. Complete ablation was achieved in most cases, but there were major complications including major pneumothorax and pleural effusion in 29-45% of cases [15, 16, 28].
The rate of local tumor progression in the current study seems to be somewhat higher than that of previous reports for small HCC. We can assume that a slightly higher rate of local tumor progression may have several reasons: the possible heat sink effect of artificial ascites, difficulty in accurate placement of the electrode in the small hepatic nodule floating in the artificial ascites, and some effect of a learning curve period. We may decrease the rate of local tumor progression using artificial hydrothorax, but we need to trade-off substantial thoracic complications. However, we believe that sonographically guided radiofrequency ablation using artificial fluid is a safer procedure and has the clear advantage of separating the radiofrequency ablation zone from the abutting dangerous organs, including the diaphragm and gastrointestinal tract, compared with sonographically guided or CT-guided radiofrequency ablation with artificial pleural effusion.
Recently, Laeseke et al. [30] investigated the characteristics and usefulness of artificial fluid. They showed instillation of 5% D/W into the peritoneal cavity before hepatic radiofrequency ablation decreases the risk and severity of diaphragm injuries compared with no pretreatment or pretreatment with 0.9% saline in a swine model. Because of its isomolarity and nonionic composition, 5% D/W is a nearly ideal protective buffer to infuse into the abdomen before thermal ablation [30]. In another study, the authors also reported pretreatment with intraperitoneal 5% D/W before radiofrequency ablation of peripheral liver tumors in 10 patients decreased pain, narcotic use, and length of hospital stay compared with 10 control patients [31].
This study has several inherent limitations. First, we could not evaluate the true benefit of artificial ascites in allowing successful percutaneous ablation and minimizing thermal injury of the diaphragm because we could not perform a randomized controlled study with a control group. Second, because of the small number of our subjects and because of the short-term follow-up, we do not know whether artificial ascites increases the possibility of hemoperitoneum in a patient with significant coagulopathy or delayed needle track seeding. Third, in this study, we could not find more subjective criteria for assessing the outcome regarding tumor visibility and radiofrequency electrode path. More subjective criteria will be necessary when the controlled trials are performed. Finally, our study was limited to those tumors that were partially visualized at sonography whereas the application of artificial ascites for those sonographically invisible tumors is ongoing in our institution.
In summary, we performed percutaneous radiofrequency ablation with artificial ascites for HCC in the hepatic dome, which has been considered a difficult procedure to perform percutaneously because of a poor sonic window or radiofrequency electrode path. We have proven that artificial ascites can improve the radiofrequency electrode path by downward displacement of the hepatic parenchyma and separate the radiofrequency ablation zone from the diaphragm. Thus, sonographically guided percutaneous radiofrequency ablation with artificial ascites appears a feasible, safe, and effective technique for treating HCC of the hepatic dome.
Acknowledgments
We thank Jung Hwan Han, Hyun Ja Jee, and Kyong Mee Lee at Samsung
Biomedical Research Institute for assistance in procedure and data
collection.
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