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1 Department of Radiology and the Institute of Radiation Medicine, Seoul
National University College of Medicine, 28 Yongon-dong, Chongno-gu, Seoul
110-744, South Korea.
2 Department of Radiology, Chungnam National University College of Medicine, 6
Munhwa-dong, Daejeon 301-747, Korea.
Received February 22, 2004;
accepted after revision August 10, 2004.
Address correspondence to J. K. Han
(hanjk{at}radcom.snu.ac.kr).
Abstract
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MATERIALS AND METHODS. Using a 200-W generator and bipolar perfused-cooled electrodes or a monopolar cooled-tip electrode, we performed 14 radiofrequency ablations in explanted bovine kidneys. Radiofrequency was applied in standard monopolar (n = 7) or bipolar (n = 7) modes at 100 W for 10 min. In the bipolar mode, the perfused-cooled electrodes were placed at interelectrode distances of 3 cm, and a 6% sodium chloride solution was instilled into tissue at a rate of 2 mL/min through the electrodes. For in vivo experiments, either monopolar (n = 7) or HS-augmented bipolar (n = 7) radiofrequency ablation was performed in the lower pole of canine kidneys. Three days after the procedure, contrast-enhanced CT scans were obtained to evaluate the volumes of the ablation regions, and the kidneys were harvested for gross measurements. Technical parameters such as changes in impedance and current during radiofrequency ablation and dimensions of the thermal ablation zones were compared between the two groups.
RESULTS. In ex vivo and in vivo experiments, the frequency of the pulsed radiofrequency application caused by rises in impedance was higher in the monopolar mode than in the bipolar mode during the application of radiofrequency energy. The in vivo study showed that the bipolar radiofrequency ablation allowed larger mean current flows than the monopolar radiofrequency ablation (i.e., mean ± SD, 1,654 ± 144 mA vs 967 ± 597 mA) (p < 0.05). Ex vivo studies revealed that the volumes of bipolar radiofrequency-induced ablation regions were substantially larger than those of monopolar radiofrequency-induced ablation regions (26.1 ± 10.5 cm3 vs 10.2 ± 4.2 cm3). In vivo studies showed bipolar radiofrequency ablation achieved larger coagulation necrosis than monopolar radiofrequency (3.2 ± 0.3 cm vs 2.4 ± 0.4 cm) (p < 0.05). This was confirmed by the measured volume of nonenhancing area on contrast-enhanced CT (20.4 ± 6.4 cm3 vs 13.5 ± 6.0 cm3).
CONCLUSION. HS-augmented bipolar radiofrequency ablation using perfused-cooled electrodes shows better performance in creating coagulation necrosis than monopolar radiofrequency ablation in the kidney of an animal model.
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Several experimental studies on hepatic radiofrequency ablation [23, 24] found that saline-augmented bipolar radiofrequency ablation can create larger dimensions of coagulation necrosis than monopolar radiofrequency ablation because bipolar radiofrequency allows a higher current density and more uniform tissue heating than monopolar radiofrequency. Recently, Nakada et al. [25] reported that bipolar radiofrequency creates larger ablation regions in the kidney than monopolar radiofrequency. However, the problem with radiofrequency application, either in monopolar or bipolar mode, is that tissue impedance often rises dramatically during treatment. This is the most important limiting factor with respect to the creation of large lesions [26–29]. Hypertonic saline (HS) infusion during bipolar radiofrequency ablation could solve this problem because the higher conductivity of the saline translates into less resistive heating near the electrode tip [26, 27]. In this context, we present the results of our systematic evaluation of HS-augmented bipolar radiofrequency ablation using a developed perfused-cooled electrode versus the standard monopolar mode with respect to the dimensions of ablation zones in renal tissue.
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Ex Vivo Studies
Experimental preparation.—Radiofrequency ablation was
performed in 14 freshly excised bovine kidneys. They were immersed into a 50
x 20 x 25 cm saline-filled bath (room temperature) and treated
with either monopolar radiofrequency (seven kidneys) or bipolar radiofrequency
(seven kidneys) using a 200-W generator (CC-3, Valleylab) and a 17-gauge
cooled-tip electrode or two 15-gauge prototype perfused-cooled electrodes with
a tip exposure of 3 cm. The tips of the electrodes were advanced at least 35
mm into the lower pole of the kidney. One radiofrequency-induced ablation
region was created in each treated kidney. A peristaltic pump was used to
infuse normal saline solution at 0°C into the lumen of the electrode at a
rate sufficient to maintain a tip temperature of 20–25°C. To monitor
the local tissue temperature during the procedure, we inserted a thermocouple
15 mm from the electrode.
Radiofrequency energy delivery modes.—Seven ablation zones
were created both in a monopolar mode (group A) and in a wet bipolar mode
(group B). In the monopolar mode, radiofrequency was applied to the 17-gauge
cooled-tip electrode at an initial generator output of 100 W and flowed from
the electrode to a metallic dispersive pad. The initial impedance was
controlled at 80 
by altering the distance between the electrodes and
the dispersive metallic pad. The radiofrequency power was manually increased
to 100 W in 1 min and held for a total of 10 min. Energy delivery was
performed using an automatic impedance-controlled algorithm (pulsing
algorithm). In this mode, power is automatically switched off for 15 sec if
impedance rises more than 10 above the baseline value; thereafter, it
is switched on again at the same or a lower level
[31].
In the HS-augmented bipolar radiofrequency delivery mode, one electrode tip was connected to the radiofrequency generator output and the other to the generator "ground" output. In this mode, current flowed from one electrode to the other, and therefore, a dispersive pad was not necessary. The two perfused-cooled electrodes were placed in the kidney at an interelectrode distance of 3 cm through an acrylic plate containing multiple holes set at 5-mm intervals. Radiofrequency power was increased manually to 100 W and then automatically changed according to the measured impedance. During radiofrequency energy application for bipolar radiofrequency ablation, a 6% HS solution was continuously infused by a syringe pump (Pilot C, Fresenius Medical Care) at a rate of 2 mL/min via the sheaths. In this experiment, we used a 3-cm interelectrode spacing and a 6% HS solution infusion during radiofrequency ablation on the basis of our ex vivo data in the liver (unpublished data, Lee et al., 2003).
The applied current, power output, and impedance were continuously monitored by the generator system during radiofrequency ablation and were recorded automatically (Real-Time Graphics software, version 2.0, Radionics) (Figs. 2A and 2B). The technical aspects of radiofrequency ablation including impedance and wattage changes, tissue temperature 15 mm from the electrode tip, and the dimensions of the radiofrequency-coagulated area for both techniques were compared.
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Lesion size measurement.—Kidneys containing lesions were
sliced along the axis of the probe insertion in the coronal plane at 5-mm
intervals. Because the white central area of the radiofrequency-induced
ablation zone has been previously shown to correspond to the zone of
coagulation necrosis by macroscopic examination
[32], two observers working in
consensus with calipers measured the long-axis diameter (Dl) and the
short-axis diameter (Ds) of the central white region of the
radiofrequency-induced ablation zones at the slice showing the maximum area.
The transverse diameter (Dt) was measured by the number of slices
showing discoloration. The volume of the radiofrequency ablation zone was
evaluated by approximating the lesion to a sphere using the following formula:
(Dt x Dl x Ds)/6. The shape of the
radiofrequency-induced ablation zone was characterized by the ratio between
the long-axis diameter and the short-axis diameter (Dl/Ds).
In Vivo Studies
Animals, anesthetics, and surgical technique.— In accordance
with the animal research committee protocol at our institution, we
anesthetized 10 domestic dogs (20 kg each) using an intramuscular injection of
50 mg/kg of ketamine hydrochloride (Ketamine, Yuhan) and 5 mg/kg of xylazine
(Rumpun, Bayer Korea) and prepared for surgery. Booster injections of up to
one half of the initial dose were administered as needed. Endotracheal
intubation was performed, and anesthesia was maintained with inhaled enflurane
gas (Gerolan, Choongwae Pharma). The dogs were placed in the supine position
and prepared at the midline and draped. Through a midline incision, one kidney
was dissected free to expose the lower pole. Because of difficulty in
obtaining access to a CT scanner at our institute, we performed the
radiofrequency ablation procedure using a laparotomy instead of CT
guidance.
Radiofrequency ablation protocol.—The 10 dogs were allocated to one of two groups: the monopolar radiofrequency ablation group (group A) or the HS-augmented bipolar radiofrequency ablation group (group B). In group A, a 17-gauge cooled-tip electrode was inserted into the lower pole of the kidney to a depth of 35 mm. The radiofrequency power was then manually increased to 100 W and held for a total of 10 min. Because the canine kidney is relatively small (< 5 cm in short diameter), we had to use radiofrequency power of up to 100 W. Grounding for the radiofrequency procedure was done via an externally (dorsally) attached grounding pad, such that the radiofrequency currents were distributed evenly through tissue in the direction of the grounding pad. To monitor the local tissue temperature during the procedure, we inserted a thermocouple 15 mm from the electrode. The kidney was then allowed to cool to body temperature and was replaced in situ. The incision was closed using nonabsorbable sutures.
In group B, a pair of prototype perfused-cooled bipolar electrodes were inserted at an interelectrode distance of 3 cm into the kidney (Figs. 1A and 1B). The radiofrequency ablation was performed at 100 W for 10 min with a 6% HS infusion delivered at a rate of 2 mL/min. Grounding was achieved via a ground probe (one of the two probes) such that the radiofrequency waves were concentrated between the two probes, creating a zone of targeted ablation. The kidney was allowed to cool to body temperature before being replaced in situ, and the incision was closed using nonabsorbable sutures.
Imaging follow-up.—An MDCT scanner (Mx8000; Marconi Medical Systems) was used to monitor ablations 3 days after the procedure. Axial CT scans were obtained with a 2.5-mm detector collimation, a 3-mm reconstruction increment, and a 1.0–1.6 pitch. The scans included both lower lobes of the lung and the abdomen including the kidneys; images were obtained before and after injection of 60 mL of contrast medium (iopromide, Ultravist 370, Schering Korea). The contrast medium was injected at a rate of 2 mL/sec through an ear vein. Contrast-enhanced CT scans were obtained 60 sec after contrast administration.
Assessment of coagulation necrosis (imaging and pathologic studies).—Nonenhancing ablation areas in treated kidneys on contrast-enhanced CT images were measured using Image J software (NIH Image software, National Institutes of Health, U. S. Department of Health and Human Services; available at http://rsb.info.nih.gov). The area and volume of the nonenhancing region were recorded for each slice. Volume was computed by integrating the area of each slice across the entire lesion.
The dogs were allowed to survive for 72 hr and then were sacrificed after the CT images were obtained. Once harvested, the kidneys were cut along the electrode insertion axis. The histopathologic study included staining for mitochondrial enzyme activity by incubating thin representative tissue sections for 30 min in 2% 2,3,5,-triphenyltetrazolium chloride (TTC, Sigma) at 20–25°C. This test can be used to determine irreversible cellular injury during the early stages of radiofrequency-induced necrosis [33]. Because the unstained area of a radiofrequency ablation region has been shown to correspond to the zone of necrosis [31], two observers measured the Ds and Dl of the ablation area and reached consensus.
The radiofrequency-induced ablation regions of a representative case of each group were fixed in 10% formalin for routine histologic processing and were finally processed by paraffin sectioning and H and E staining for light microscopic study.
Statistical Analysis
Technical parameters of the two radiofrequency delivery modes (monopolar vs
bipolar) were also compared using the unpaired Student's t test. To
compare changes in tissue temperature measured 15 mm from the electrode during
radiofrequency ablation, we used a repeated measure of analysis of variance
test. The measured three diameters for all monopolar and bipolar
radiofrequency-induced ablation regions and total lesion volumes calculated
from CT scans and gross specimens were averaged for each group and compared
using the unpaired Student's t test. Statistical significance was
established using Student's two-tailed t test. For all statistical
analyses, a p value of less than 0.05 was considered statistically
significant. All statistical analyses were performed with Statistical Package
for the Social Sciences (version 9.0, SPSS).
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375 sec; median, 245
sec) and then rapidly increased by 20 more than the initial impedance,
which induced the activation of the pulsed radiofrequency application. In the
HS-augmented bipolar mode (group B), impedance was well maintained during the
radiofrequency instillation without rapid rises in impedance. The mean current
flow in both groups was 943 ± 560 mA for group A (monopolar mode) and
1,565 ± 190 mA for group B (bipolar mode). The difference in mean
current between the two groups was statistically significant (p =
0.017). Tissue temperatures measured 15 mm from the electrode were also higher
in group B (75° ± 9°C in group A; 96° ± 6°C in
group B) (Table 1), and there
was a significant difference between the tissue temperature changes over time
during radiofrequency ablation in the two groups (p = 0.001) (Figs.
3A and
3B).
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Grossly, radiofrequency ablation in monopolar or bipolar modes created white discolored areas in the cortex and a dark brown area in the medulla (Figs. 4A and 4B). Gross assessment revealed that the monopolar radiofrequency-induced ablation regions were 3.0 ± 0.4 cm in Dl, 2.5 ± 0.4 cm in Ds, and 2.6 ± 0.3 cm in Dt (Table 1). However, HS-augmented bipolar radiofrequency-induced ablation regions were substantially larger: 4.2 ± 0.5 cm in Dl, 3.5 ± 0.4 cm in Ds, and 3.4 ± 0.6 cm in Dt (Table 1), and these differences were significant (p < 0.05). In addition, the mean volumes of the ablation regions in monopolar and bipolar modes were 10.2 ± 4.2 cm3 and 26.1 ± 10.5 cm3, respectively, and this difference was statistically significant (p = 0.003).
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In Vivo Studies
As was observed in the ex vivo experiment, the impedance was not changed
during radiofrequency instillation in group B, but in group A, it was rapidly
increased by 20 more than the initial impedance (80 ) 3–6
min (mean, 273.7 ± 83 sec; median, 302 sec) after the beginning of the
radiofrequency application, which resulted in the activation of the pulsed
radiofrequency application (Figs.
2A and
2B). The mean current flow was
967 ± 597 mA for group A and 1,654 ± 144 mA for group B
(Table 2), which was
significant (p = 0.01). Tissue temperatures measured 15 mm from the
electrode were also higher in group B (73° ± 12°C in group A
and 94° ± 13°C in group B) (p = 0.013) (Figs.
3A and
3B).
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The radiofrequency ablation regions created in all treated kidneys exhibited a characteristic central white zone surrounded by a red hemorrhagic zone (Figs. 5A, 5B, 5C, 5D, 5E, and 5F). After staining with 2% 2,3,5,-triphenyltetrazolium chloride, the normal renal parenchyma and the peripheral hemorrhagic zone appeared pink, but the central white zone was unstained (Figs. 5A, 5B, 5C, 5D, 5E, and 5F). The Dl of the central white zones in groups A and B averaged 3.0 ± 0.3 cm and 3.5 ± 0.5 cm, respectively (p = 0.03). The Ds of the central white zones in groups A and B were 2.4 ± 0.4 cm and 3.2 ± 0.3 cm, respectively (p = 0.003) (Figs. 5A, 5B, 5C, 5D, 5E, and 5F). The ratios of Dl/Ds of groups A and B were 1.3 ± 0.2 and 1.1 ± 0.2, respectively (p = 0.09). A significant difference was seen between the Dl of the bipolar radiofrequency-induced ablation regions in vivo (3.5 ± 0.5 cm) and ex vivo (4.2 ± 0.5 cm) (p = 0.0136). However, the difference between the in vivo Ds (3.2 ± 0.3 cm) and ex vivo Ds (3.5 ± 0.4 cm) was not significant (p = 0.17).
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In contrast-enhanced CT scans obtained 3 days after the ablation, all radiofrequency-ablated lesions showed nonenhanced, hypoattenuated regions (Figs. 5A, 5B, 5C, 5D, 5E, and 5F). The mean volumes of the nonenhancing zones induced by monopolar or bipolar radiofrequency ablation were 13.5 ± 6.0 cm3 and 20.4 ± 6.4 cm3, respectively (p = 0.0498). The Ds diameters of the monopolar and bipolar radiofrequency-induced ablation regions measured on contrast-enhanced CT images were 2.4 ± 0.51 cm and 3.3 ± 0.54 cm, respectively. No significant difference was seen between those figures measured on gross specimens and on CT scans (p > 0.05).
Histopathologically, the radiofrequency-induced ablation regions of the representative cases showed a central necrotic zone surrounded by a peripheral zone consisting of necrotic renal tubules and glomeruli, interstitial hemorrhage, and fragmented polymorphonuclear leukocyte infiltrate (Figs. 5A, 5B, 5C, 5D, 5E, and 5F). The eosinophilia of this central zone contrasted with the more basophilic normal renal parenchyma surrounding the lesions. Within the central necrotic zone, no definite viable cells were found, but within hemorrhagic lesions, areas of vascular congestion and hemorrhage were accompanied by advanced necrotic changes and patches of living cells. Similar histologic changes were observed in the bipolar and monopolar lesions.
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Radiofrequency ablation involves the application of radiofrequency current and can produce theoretically predictable tumor destruction on the basis of the well-defined variables of the bio-heat equation [35]. Conventional radiofrequency ablation using single-electrode devices in the monopolar mode is limited in terms of creating an ablation region because of the precipitous drop in current density that occurs with distance from the energy source (1/r2), which makes the periphery of the radiofrequency-induced lesion particularly prone to vascular cooling [36, 37]. This limitation could be accentuated in renal tumor radiofrequency ablation because most renal cell carcinomas are hypervascular and the renal parenchyma has a high natural blood flow. This problem could be related to the limitations of monopolar radiofrequency ablation for renal tumors, which include a small ablation region and questions about the reliability of cell kill [21, 22, 25]. To circumvent these problems, several investigators have used saline instillation during radiofrequency ablation and have achieved increased radiofrequency heating [28]. Furthermore, the combination of saline infusion and bipolar radiofrequency allows higher current densities to be used, which probably enhances ablation.
In our in vivo study, HS-augmented bipolar radiofrequency ablation created a larger area of coagulation necrosis than monopolar radiofrequency ablation: 2.4 ± 0.4 cm in monopolar radiofrequency ablation versus 3.2 ± 0.3 cm in bipolar radiofrequency ablation (Figs. 5A, 5B, 5C, 5D, 5E, and 5F). In addition, our ex vivo study also showed that the mean volume of ablation zones of group B (bipolar mode) was larger than that of group A (monopolar mode): 10.2 ± 4.2 cm3 versus 26.1 ± 10.5 cm3 (p < 0.05). The larger lesions created using the perfused-cooled electrode in the bipolar mode could be attributed to several factors. First, it could be related to the greater amount of heat produced at a given current level in the bipolar mode [23, 26]. In the monopolar mode, heat is diverted from the ablation site in all directions and a precipitous drop in current density occurs with distance from the energy source [36]. In contrast, in the bipolar mode, one electrode is thermally shielded by the opposing second electrode, which also actively heats tissue in its proximity. Therefore, heat is trapped between the two electrodes, and higher temperatures are achieved because less cooling occurs in the direction of the collateral electrode than is the case with monopolar ablation [26]. Second, current is passed through the region between the electrodes in bipolar mode. Third, HS infusion during bipolar radiofrequency ablation prevents the marked rise in impedance by increasing the electrical conductance of the tissue and thus facilitates greater energy delivery. Furthermore, HS infusion into the liver tissue increases thermal conductance.
However, the degree of improvement in the ablation zone by bipolar radiofrequency ablation compared with monopolar radiofrequency ablation was less in the in vivo study (p = 0.498) than in the ex vivo study (p = 0.0029). This difference could be explained by the fact that the dimension of the canine kidney is rather small, and therefore, bipolar radiofrequency ablation could not further increase the dimension of coagulation along the short and transverse axes of the kidney.
In our study, we evaluated the tissue damage from radiofrequency ablation using H and E staining and 2% 2,3,5,-triphenyltetrazolium chloride staining, which indicates mitochondrial enzyme activity [33]. Previous studies regarding radiologic–histopathologic correlation of radiofrequency ablation zones have shown that it is difficult to determine the degree of cell damage on light microscopic examination in acute phase (from immediately after the procedure to 1 day later) [32, 38]. However, in our study, the specimen that was obtained at least 3 days after the procedure showed a clearly defined area of coagulation necrosis with ghostlike tubular profiles; very faintly staining nuclei and peripheral zones of hemorrhage were found (Figs. 5A, 5B, 5C, 5D, 5E, and 5F). These findings are well matched with results of the previous study regarding renal radiofrequency ablation in rabbit kidneys [38]. Furthermore, we found that the 2% 2,3,5,-triphenyltetrazolium chloride staining made a more clear distinction on gross specimens between the area of coagulation necrosis and viable renal tissue, as a previous study showed in the liver [32].
One of the major problems of renal radiofrequency ablation is the difficulty of monitoring the ablation area during treatment. In our in vivo study, wet bipolar radiofrequency ablation generated a complete necrotic zone between the two electrodes, which was confirmed by the lack of 2% 2,3,5,-triphenyltetrazolium chloride staining, indicating no mitochondrial enzyme activity. In one previous study comparing cryoablation with monopolar radiofrequency ablation [39], radiofrequency ablation showed "skip lesions" between electrodes. These skip lesions may have been related to the precipitous drop in current density that occurs with distance from the energy source in the standard monopolar radiofrequency application mode, which makes the periphery of the radiofrequency-ablated lesion particularly prone to vascular cooling. The lack of current dispersion favors bipolar radiofrequency for renal tumor ablation. Haemmerich et al. [40] showed that symmetric bipolar radiofrequency ablation creates coagulation zones that are significantly closer to blood vessels than are produced by monopolar radiofrequency ablation and explained that this could be attributed to the higher current densities allowed by bipolar radiofrequency ablation. Given that bipolar radiofrequency ablation kills cells between the two electrodes and provides a higher current density with greater, more uniform coagulation necrosis, the use of bipolar electrodes to "frame" the lesion is advantageous [25].
Possible problems associated with the use of HS-augmented bipolar radiofrequency ablation include the risk of unexpected thermal injury related to hot saline diffusing through vital structures. However, our present study supports bipolar radiofrequency application as showing clear advantage in terms of the size and consistency of the lesions produced.
Some limitations of our study should be mentioned. First, the radiofrequency ablation procedure was performed as open surgery due to difficulty in gaining access to the CT scanner in our institute. Because intraoperative radiofrequency ablation enables us to accurately target the kidney and avoid injury to the adjacent bowel, the results of this study might not represent those of the percutaneous radiofrequency ablation procedure of renal tumors. Second, the results obtained in ex vivo bovine kidneys and in vivo canine kidneys may not reflect the results in human renal tumors because of the different tissue textures and cell biologies. Nevertheless, the use of our wet bipolar radiofrequency system offers substantial clinical advantages. Third, we compared the in vitro and in vivo efficiencies of two radiofrequency application modes at 3-cm interelectrode spacing. Given that the ideal interelectrode spacing between the two electrodes depends on the local properties of the ablation site (which differ for each ablation), more experimental study is needed at different interelectrode distances. Fourth, the canine kidney is relatively small, and therefore, we tested the two radiofrequency delivery modes at 100 W, which limited the dimensions of the lesions administered. Finally, the large volumes of coagulation created may not always be beneficial or desirable. In certain circumstances, coagulation extending beyond the tumor boundaries could be detrimental if surrounding structures are damaged or if insufficient tissue is preserved to permit normal organ function.
The clinical role of radiofrequency ablation in the treatment of renal cell carcinoma is not well established at present but will probably evolve. Given the low biologic activity of small renal tumors and close follow-up, recurrence of these small tumors after radiofrequency ablation may be detected early enough to allow more radical treatment before systemic spreading occurs [41]. At the same time, percutaneous radiofrequency ablation increases the renal reserve by sparing healthy normal tissue and reduces surgical morbidity and recovery time. As seen in this study, an extended volume of coagulation necrosis created by the new bipolar radiofrequency system may increase the clinical utility of radiofrequency ablation therapy by allowing the successful treatment of larger renal tumors or reducing the number of sessions needed for the treatment of a given tumor. Before applying our HS-augmented bipolar radiofrequency ablation technique to humans, it is necessary to evaluate its therapeutic efficacy and safety using the renal tumor model in large animals.
In summary, wet bipolar radiofrequency ablation using dual electrodes was found to produce better results than the monopolar radiofrequency ablation and created larger lesions. If our bipolar probe units become clinically available, large lesions could be treated more effectively than with conventional single-probe units at potentially decreased procedure time.
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= monopolar radiofrequency ablation, 
= bipolar radiofrequency ablation. Error bars represent 95% confidence
interval for mean temperature.
