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British Journal of Radiology (2004) 77, 944-949
© 2004 British Institute of Radiology
doi: 10.1259/bjr/67069976
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Full Paper

Hepatic bipolar radiofrequency ablation using perfused-cooled electrodes: a comparative study in the ex vivo bovine liver

J M Lee, MD 1,2 J K Han, MD 1,2 S H Kim, MD 1,2 J Y Lee, MD 1,2 S H Choi, MD 1,2 and B I Choi, MD 1,2

1 Department of Radiology and Institute of Radiation Medicine, Seoul National University College of Medicine and 2 Clinical Research Institute, Seoul National University Hospital, 28 Yongon-dong, Chongno-gu, Seoul, 110-744 Korea

Correspondence: Dr Jeong Min Lee, Department of Diagnostic Radiology, Seoul National University Hospital, 28 Yongon-dong, Chongno-gu, Seoul 110-744, Korea


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 References
 
The purpose of this paper was to demonstrate the efficacy of the dual probe bipolar radiofrequency (RF) system with the perfused-cooled electrodes inducing coagulation necrosis in the ex vivo bovine liver. The perfused-cooled electrode that allows simultaneous internal cooling and interstitial hypertonic saline perfusion has been developed for RF ablation (RFA). RF was applied to excised bovine liver in a bipolar mode at 150 W using a 200 W generator with two perfused-cooled electrodes for 10 min. After placing the electrodes at 3 cm spacing in the explanted liver, 45 ablation zones were created with three different regimens: Group A, using both intraelectrode cooling and interstitial perfusion; group B, using only the intraelectrode cooling; and group C, using only interstitial perfusion. In groups A and C, RFA was performed with the infusion of 6% hypertonic saline at the rate of 2 ml min–1. During RFA, we measured the tissue temperature at the midpoint between the two electrodes. The dimensions of the ablation zones and the changes in impedance, currents and liver temperature during RFA were compared in these three groups. The mean tissue impedance during RFA in group A (56.7±21.7 {Omega}) and group C (56.9±20.6 {Omega}) was significantly lower than group B (112±19.7 {Omega}) (p<0.001). The mean current was higher in group A (1765±128 mA) than groups B (760±321 mA) and C (1298±349 mA) (p<0.05). In addition, the shortest vertical diameter of coagulation necrosis was greater in groups A (4.9±0.5 cm) and C (4.6±0.7 cm) than in group B (3.5±0.4 cm) (p<0.05). The temperature at the mid-point between the two probes was higher in group A than other groups: 99°C in group A, 88.9°C in group B, and 94.3°C in group C (p>0.05). The ratios of the diameter of the long-axis to the diameter of the vertical-axis of groups A, B and C were 1.1±0.1, 1.2±0.1, and 1.1±0.2, respectively (p<0.05). Bipolar RFA using intraelectrode cooling and the interstitial saline perfusion simultaneously produced ablation zones significantly larger than the area produced by only one measure.


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 References
 
Image-guided percutaneous tumour ablation using radiofrequency (RF) energy has become increasingly popular in recent years and its use for the treatment of primary and secondary hepatic malignancy is increasing [1–4]. RF ablation (RFA) successfully induces complete necrosis of small liver cancers. However, a moderate to high recurrence rate in local tumours (25–55%) has been reported [5–10]. The recurrence after RFA treatment may be related to the limitation of currently existing RF technology which can ablate only tumours 3.5–4.5 cm in diameter in a single cycle [2–4, 11, 12]. To achieve complete necrosis of tumours, RFA must produce a coagulation area that is large enough to include focal liver malignancies and the safety margin (5–10 mm) in normal tissue [3, 12]. Therefore, strategies that increase the size of the ablated region must be developed for the induction of complete necrosis of tumours [3, 13].

Several attempts have been made to overcome this limitation of the standard RFA, such as saline-enhanced RFA [14–16], RFA with hepatic vascular inflow occlusion [17, 18], combined RFA with chemoablation [19–21] and bipolar RFA with/without saline infusion [22–26]. A few reports demonstrated that saline-enhanced bipolar RFA creates larger coagulation necrosis than the standard RFA [22, 26]. However, in the previous study reported by Lee et al [26] regarding bipolar RFA using the Berchtold system (Elektrotom HiTT®; Tuttlingen, Germany) and perfused electrodes, rapid increases in impedance over 700 {Omega} occurred several times. This may be due to the rapid boiling of liver tissues adjacent to the electrode, which may be caused by the very high current created between two electrodes. Ni et al [27] and Miao et al [28] reported that hepatic monopolar RFA using a cooled wet electrode that allows simultaneous use of internal cooling perfusion and the interstitial saline infusion was more efficient in creating ablation zones larger than the zone created by other monopolar electrodes. Based on these reports [27, 28], we developed the prototype perfused-cooled electrode by modifying a 17-gauge internally cooled electrode (Radionics, Burlington, MA) that can perform the interstitial infusion of saline and the intraelectrode cooling simultaneously. We examined whether the use of intraelectrode cooling and saline interstitial perfusion are required to optimize the RF energy delivery in a bipolar mode, in regard to the dimension of the ablation zone in the liver and the temperature at the midpoint between two electrodes.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 References
 
Design of perfused-cooled electrode
Based on the previous study by Miao et al [28], we developed the perfused-cooled electrode that performs intraelectrode cooling perfusion and interstitial saline infusion simultaneously (Figure 1Go). We modified a 17-gauge cooled-tip electrode with a 3 cm active tip (Radionics) by covering it with a 15-gauge outer sheath, except for a 3.5 cm distal portion. The outer sheath was made of metal and electrically insulated. The space between the 15-gauge sheath and the cooled tip electrode permitted saline infusion along the electrode. A peristaltic pump (Watson-Marlow, Medford, MA) was used to infuse the cold saline solution (0°C) into the lumen of the electrodes at rates sufficient to maintain the temperature of the tip at 20–25°C.



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  		Figure 1. A photograph of a perfused-cooled electrode that contains two coaxial lumina that enable cooling water to circulate through the electrode, and a separate lumen for saline interstitial infusion.

 
The RFA settings
Experiments performed with ex vivo beef liver have been shown to generate reproducible results [26, 28]. We thus used excised beef liver purchased from a local butcher. The experiments were performed with 10 freshly excised bovine livers weighing approximately 7 kg. The livers were cut into blocks, 10 cm x 10 cm x 10 cm, and immersed in a 50 cm x 20 cm saline-filled bath. Based on our preliminary studies (unpublished data), two 15-gauge perfused-cooled electrodes (Figure 1Go) were placed in the liver at a 3 cm distance on an acrylic plate with multiple holes at 5 mm intervals. The tip of the electrode, at least 4 cm, was placed inside the liver. For the continuous measurement of temperature in the liver during the procedure, a thermocouple was inserted at the midpoint between the two electrodes. The tissue impedance was monitored using a circuitry incorporated into the generator. For bipolar RFA, two electrodes were used, one active and one dispersive.

The Radionics RFA system consists of two 15-gauge perfused-cooled electrodes with the 3 cm tip exposure and the 480 kHz generator (CC-3, RadionicsTM) used at 150 W. The applied current, power output and impedance were continuously monitored during the RFA. The data were recorded automatically using a computer program (Real Time Graphics Software V 2.0; Radionics). Based on our preliminary data regarding optimization of concentration and injection rates of NaCl solutions for bipolar RFA (unpublished), 6% hypertonic saline was infused at the rate of 2 ml min–1 through the perfused-cooled electrode using an infusion pump (Pilotec IS; Fresenius Medical Care, Alzenau, Germany).

The ablation protocol
To validate the efficacy of the perfused-cooled electrode for hepatic bipolar RFA, intraelectrode cooling perfusion and saline interstitial infusion were applied simultaneously (group A) or only one measure used (groups B and C). Using the Radionics system® with perfused-cooled electrodes in bipolar mode, 15 ablation zones were created as follows: group A, using both intraelectrode cooling and interstitial perfusion function; group B, using only the intraelectrode cooling function; group C, using only the interstitial perfusion function. RF was applied for 10 min at a generator output of 150 W. Energy delivery was performed using an automatic impedance controlled algorithm (pulsing algorithm). In this mode, power is automatically switched off for 15 s if impedance rises more than 10 {Omega} above the baseline value; thereafter, it is switched on again at the same or a lower level [29].

The efficacy of RFA such as the impedance, wattage changes, tissue temperature at the midpoint, and the dimensions of the RF-coagulated area were compared for the three groups.

Measurement of the lesion size
The liver blocks with RFA lesions were cut along the longitudinal plane passing through the axes of both probes (L-plane) and then cut transversely perpendicular to L-plane (T-plane). Previously, the white central area of the RF-induced ablation zone has been shown to correspond to the zone of coagulation necrosis [30]. Thus, two investigators measured the vertical-axis diameter (Dv) along the probe, the long-axis diameter (Dl) perpendicular to Dv in the longitudinal plane, and the short-axis diameter of ablation zone (Ds) in the T-plane. The volume of ablation area was assessed by converting the lesion to a sphere using the formula: {pi}(Dv x Dl x Ds)/6. The shape of the RF-induced ablation zone was determined by the Dl/Dv diameter ratio.

Statistical analysis
One-way analysis of variance (ANOVA) with Scheffe test (p=0.05, two-tailed test) was performed to compare the mean of the diameter of the dimension of the thermal ablation area and the technical parameters of the three groups. The data represent the means±standard deviation (SD). To compare the temperature at the midpoint between two electrode tips, the repeated measure of ANOVA test was performed. For all statistical analyses, p-value less than 0.05 was considered significant. The statistical analysis was performed using the Instat program (GraphPad Software, Inc., San Diego, CA).


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 References
 
Electrical measurements
Before RF energy application, the mean of initial tissue impedance in three groups was 120±11.8 {Omega}. In group A, with applied intraelectrode cooling and interstitial saline perfusion, during RFA, impedance gradually decreased with saline infusion to lower than 60 {Omega}. The pulsing technique was activated only in four cases (less than 3 times). In group B, the impedance rose and fluctuated between 80 {Omega} and 350 {Omega}. The pulsed technique was activated more than 15 times (mean). In group C using the interstitial saline infusion, the impedance gradually decreased, but rose to higher than 250 {Omega} intermittently. The pulsed technique was activated 7 times (mean). The frequent activation of the pulsed technique in groups B and C, induced a gradual reduction of the current output to the level determined by the previously designed algorithm.

The mean of the accumulated energy output was 1765±128 mA in group A, 760±321 mA in group B, and 1298±348.9 mA in group C. The difference of the mean current between group A and groups B or C was significant (p<0.05).

Temperature
Figure 2Go shows the mean temperature at the midpoint between two electrode tips. The mean temperature at the final midpoint was 99±2.8°C in group A, 88.9±13.6°C in group B, and 94.3±8.4°C in group C (p>0.05).



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  		Figure 2. A graph showing changes of mean temperatures at the midpoint between the two electrode tips in each group during radiofrequency ablation (RFA).

 
Dimension of the ablation area
After RFA, a well-defined area with a white centre was detected in the ablated zone sections. The mean of Dl of the RF-induced central white zone was 5.2±0.7 cm in group A, 4.1±0.3 cm in group B and 5.1±0.6 cm in group C (p<0.05) (Table 1Go). The mean of Dv was 4.9±0.5 cm in group A, 3.5±0.4 cm in group B, and 4.6±0.7 cm in group C (p<0.05) (Figure 3Go). The mean of Ds of the ablated sphere was 4.3±0.4 cm in group A, 2.0±0.6 cm in group B, and 3.8±0.9 cm in group C (p<0.05). The difference in Dl, Dv and Ds between groups A and B was statistically significant (p<0.05). The difference between groups A and C was not significant (p>0.05). Furthermore, the volume of the ablation zone in groups A, B, and C was 57.1±14.2 cm3, 17.4±4.0 cm3, and 43.8±18.4 cm3, respectively. The difference in groups A and B was statistically significant (p<0.05). Similarly, the difference in groups B and C was statistically significant (p=0.05).


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  		Table 1. The value of the radiofrequency-induced coagulation necrosis and tissue temperature

 


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  		Figure 3. Comparison of radiofrequency-induced coagulation in the three groups. Note that the mean shortest coagulation diameters at midpoint between the two electrode tips were larger in group A than in groups B and C. (a) Photograph of specimen from group A. (b) Photograph of specimen from group B. (c) Photograph of specimen from group C.

 
The ratio of Dl/Dv was 1.1±0.1 in group A, 1.2±0.1 in group B and 1.1±0.2 cm in group C, and there was no significant difference between the groups (p>0.05).


   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
References
 
Recent improvement in RF technique has contributed to the high success rates of RFA in the treatment of primary and secondary liver tumours [1–4]. However, even with the improved techniques, liver tumours with a diameter less than 3 cm (about 14 cm3) are generally considered to be ideal for RFA [3, 4, 31–33]. Successful tumour ablation by RF energy application is achieved when the area of destruction is extended 0.5 cm to 1 cm beyond tumour targets [12, 32, 33]. Therefore, multiple overlapping ablations are required to achieve complete necrosis of the target tumour. However, in clinical situations, overlapping ablations might not be easy to perform under the guidance of ultrasound because of the echogenic microbubbles created during RFA [12]. Furthermore, errors can be made easily during multiple positioning operations. To decrease the number of applications required for large tumours and to increase the probability of complete tumour necrosis, the maximization of the coagulation necrosis area by a single RF application is required.

This inherent limitation of monopolar RFA is due to the desiccation and charring of tissues near the tip of electrode that occurs as the temperature at the tissue–electrode interface increases rapidly during RF energy application [13, 31]. This charring of tissues also prevents RF energy conduction beyond the desiccated tissue and thus halts further tissue coagulation. Several studies [23–25] demonstrated that bipolar RFA could induce coagulation necrosis in a larger area than monopolar RFA by increasing current density between the electrodes. However, the bipolar mode could intensify the shortcomings of tissue desiccation and charring at the electrode tip because of increased current density between the two electrodes. One of most effective approaches to overcoming this shortcoming is to infuse saline solution that increases both electrical conductance and thermal conductivity [14–16, 27, 28]. In addition, Goldberg et al [13], and Miao et al [28] have demonstrated that cooling of the electrode internally could prevent the boiling of the liver adjacent to the electrode more effectively. Based on these reports, we speculated that the combination of bipolar mode RFA with perfused-cooled electrodes may improve the efficacy of the RF-induced coagulation necrosis.

Our results show that the bipolar RFA combined with intraelectrode cooling and interstitial saline perfusion create larger lesions than either measure alone: 57.1 cm3 vs 17.4 cm3 vs 43.8 cm3 (p<0.05). This difference may be due to the delivery of higher currents throughout the procedure. The higher energy delivery was attributed to the constant low impedance (below 100 {Omega}) achieved with the use of intraelectrode cooling and interstitial saline perfusion simultaneously. On the other hand, bipolar RFA using either intraelectrode cooling or interstitial saline infusion could not prevent the sudden increase in impedance to more than 350 {Omega} resulting in the reduction of the power output. The lower tissue impedance during RFA and higher energy delivery in group A could be explained by the combined effect of intraelectrode cooling and interstitial saline perfusion simultaneously. Although a portion of the energy delivered by the perfused-cooled electrode generator was absorbed by the cooling liquid, intraelectrode cooling could decrease the boiling of the adjacent tissue (>100°C), and the total energy delivered to the tissue could be increased [3, 13]. Furthermore, tissue boiling could be prevented by interstitial saline perfusion because the interstitial electrolyte may perfuse the RF current further into the tissue and away from the surface of the electrode [5, 27, 28]. This will allow the delivery of more RF energy to the tissue without the current reaching the critical level and avoid the desiccation and the char formation at the tissue–electrode interface [11, 27, 28].

We have observed that bipolar RF application using simultaneous intraelectrode cooling and interstitial perfusion for 10 min created an ablation zone with a volume of 57.1±14 cm3. This large volume of coagulation necrosis at 10 min could improve the efficacy of RFA therapy. In addition, the ratio of Dl to Dv was 1.1, which suggests that its shape is almost spherical. This is of importance as most liver tumours are spherical.

Although hypertonic saline-enhanced bipolar RFA more efficiently created coagulation necrosis of tumours than bipolar RFA without infusion of saline (dry bipolar system) in this study, its concerns in vivo include the unexpected burn injury of the adjacent vital structures by the boiling saline, and irregular shapes of coagulation due to fluid diffusion along fascial planes. Since the risk of burn injury is increased as the amount of saline increased, further studies optimizing the amount and the concentration of saline are required.

Compared with monopolar RFA, the drawbacks of bipolar RFA are that only two electrodes can be used at one time and all currents originated from one electrode must enter the second electrode [13]. Moreover, in bipolar mode, the amount of heat generated in the vicinity of the electrodes cannot be controlled independently. If the degree of cooling of the electrodes were different due to the difference in vascular perfusion, one electrode may reach a higher temperature than the other, which may lead to boiling and a rapid increase in impedance [25]. In addition, the electrodes must be parallel and the tumour must be located between them. However, in the clinical situation, the insertion of two parallel electrodes can be difficult. Furthermore, the use of two electrodes increases the cost of the RFA procedure as well as increasing the risk of complications related to the electrode insertion, such as bleeding or traumatic injury of the treated organ.

Recently, several minimally invasive, image-guided tumour ablation therapies are gaining increasing attention as an alternative to standard surgical techniques in the treatment of primary and hepatic metastases. These include thermal ablation techniques using RF energy, microwave, and laser, chemoablation using ethanol or acetic acid, chemoembolisation and cryoablation [34–37]. Benefits over surgical resection include the anticipated reduction in morbidity and mortality, low cost, the ability to perform ablative procedures on outpatients, and the potential application in a wider spectrum of patients, including non-surgical candidates [35]. Although further outcomes data and randomized control trials are needed, it appears that RFA is superior to ethanol injection in terms of local recurrence rate and number of sessions required for complete ablation of the tumour [38]. In addition, percutaneous cryoablation therapy is still limited by the large diameter of current cryoprobes [36]. Despite that, thermal ablation therapies using RF energy, microwave and laser share a lot of similarity in the mechanism of tumour cell killing. Microwave ablation or laser ablation have a greater limitation in the ability to achieve the appropriate volume of coagulation necrosis with a single application compared with RFA and therefore, needs multiple punctures [35]. Chemoembolisation has an advantage for multifocal liver tumours compared with other percutaneous therapies [35, 36]. As current limitations are addressed, these modalities will receive even greater attention as viable alternatives for the treatment of hepatocellular carcinoma.

Nevertheless, the efficacy of RFA is also dependent on the size of the treated lesion [37]. Therefore, as demonstrated in this study, an extended volume of coagulation necrosis created by the new bipolar RF system may increase the clinical utility of RFA therapy by allowing the successful treatment of larger hepatic tumours or reducing the number of sessions needed for the treatment of a given tumour. Before applying our HS-enhanced bipolar RFA technique to humans, it is necessary to evaluate its therapeutic efficacy and safety using the liver tumour model in large animals.

Our study has certain limitations. First, experiments have been performed with normal liver parenchyma ex vivo, not tumours in situ. Living tumour tissues have the cooling "sink" effect due to the blood flow, resulting in rapid heat exchange [39]. It is unclear to what extent the results obtained in this study accurately represent the real situation. However, despite these drawbacks, our model provides the basis for comparing the efficiency of different RF settings. Second, based on our unpublished preliminary data, we tested NaCl only under one condition: 6% solution at the flow rate 2 ml min–1. It follows that further experiments optimizing the concentration and the amount of the saline solution are required. In addition, the parameters that we used for bipolar RFA may not be optimal.

In conclusion, bipolar RFA using intraelectrode cooling and interstitial saline perfusion simultaneously produced significantly larger ablation zones than those produced by only one measure. Coagulation necrosis in the large volume produced by the perfused-cooled electrode may be due to the effect of the delivery of higher energy than that feasible by electrode cooling and the increased electrical conductance with hypertonic saline instillation.


   Footnotes
 
This study was supported by the grant No. 09-2003-012-0 from the Seoul National University Hospital Research Fund. Back

Received for publication January 5, 2004. Revision received June 21, 2004. Accepted for publication July 12, 2004.


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 

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C. Schraml, C. Aube, H. Graf, A. Boss, S. Clasen, T. Herberts, D. Schmidt, F. Schick, C. D. Claussen, and P. L. Pereira
MR-guided Radiofrequency Ablation: Do Magnetic Fields Influence Extent of Coagulation in ex Vivo Bovine Livers?
Radiology, December 1, 2006; 241(3): 746 - 752.
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