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Annals of Surgical Oncology 8:651-657 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Radiofrequency Ablation for Eradication of Renal Tumor in a Rabbit Model by Using a Cooled-tip Electrode Technique

Yi Miao, MD, PhD, Yicheng Ni, MD, PhD, Hilde Bosmans, PhD, Jie Yu, MD, Johan Vaninbroukx, MD, Steven Dymarkowski, MD, Hao Zhang, MD and Guy Marchal, MD, PhD

From the Department of Radiology (YM, YN, HB, JY, JV, SD, HZ, GM), University Hospitals, Catholic University of Leuven, Leuven, Belgium; and the Department of Surgery (YM), First Affiliated Hospital, Nanjing Medical University, Nanjing, People’s Republic of China.

Correspondence: Address correspondence and reprint requests to Dr. Yicheng Ni, Department of Radiology, University Hospitals, K.U. Leuven, Herestraat 49, B-3000 Leuven, Belgium; Fax: 32-16-343765; E-mail: yicheng.ni{at}med.kuleuven.ac.be


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Radiofrequency ablation (RFA) has emerged as a potential alternative for surgery in clinical oncology. This animal experiment was conducted to evaluate the feasibility of RFA in the treatment of renal tumor.

Methods: Eighteen rabbits with renal implantation of VX2 tumors were divided into two groups. Group A (n = 12) was treated with RFA by using a cooled-tip RF system at 30 W for 80 to 180 seconds. Group B (n = 6) received a sham operation. The therapeutic efficacy was evaluated by survival rate, magnetic resonance imaging (MRI), and histology.

Results: All animals in group B died within 3 months after tumor implantation. Total tumor eradication was achieved in 10 of 12 rabbits (83.3%) in group A, of which 5 rabbits survived longer than 6 months (absolute eradication) and another 5 rabbits were found free of viable tumor when killed (relative eradication). Two rabbits experienced local tumor relapse, lung metastasis, or both. Six-month survival rate of RFA-treated rabbits was significantly higher (P < .01) than that of control rabbits. The typical MRI appearances of the acute RFA lesion consisted of five characteristic concentric zones, which corresponded to central needle track (zone A), tumor coagulation (zone B), renal tissue coagulation (zone C), peripheral hemorrhage (zone D), and inflammatory layer (zone E) on histology.

Conclusions: RFA may become a promising therapy for the treatment of renal tumor. MRI is a useful modality for assessment of renal tumor ablation.

Key Words: Animal experiment • Renal neoplasms • Magnetic resonance imaging • Minimally invasive surgery • Radiofrequency ablation


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIAL AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The kidney tumors, including primary renal cell carcinoma and metastasis, are not uncommon. Incidental discovery of small renal tumors (<3.5 cm in diameter) has become more frequent with the use of widely available imaging modalities such as ultrasonography, computed tomography, and magnetic resonance imaging (MRI).1 The early diagnosis has increased the possibility of successfully removing these small tumors. The recent rapid development of image-guided interventional and video-assisted surgical techniques has largely facilitated minimally invasive renal tumor therapies such as laser ablation,2,3 microwave ablation,4 embolization,5 cryoablation,6–8 and radiofrequency ablation (RFA).9–15 Since the mid-1990s, RFA has emerged as the most promising minimally invasive modality for cancer therapy because of the recent development of various novel RF electrodes.16–21 This development constitutes the most important advance of RFA technique. One of the newly developed electrodes is the cooled-tip electrode.16 The use of this electrode has enabled the creation of larger lesions, in the order of several centimeters compared with the several millimeters in diameter reported previously.22 This advancement has ignited an explosion of basic and clinical research involving RF tumor ablation. Promising results have been reported in the treatment of various solid tumors in different organs, especially in the treatment of primary and secondary hepatic malignances.23–26 However, there are only a few studies on RFA in renal tumors. There seems to be a lack of systematic preclinical investigation. Particularly, there is no evidence for the therapeutic benefit of RFA for renal tumors because of an absence of survival studies.

This animal experiment was conducted to explore the feasibility of cooled-tip electrode-mediated RFA technique for the treatment of renal VX2 carcinoma in rabbits and to evaluate the therapeutic efficacy with survival rate and MRI in correlation with microangiography and histopathology.


   MATERIAL AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Renal Tumor Model
Adult male New Zealand rabbits weighing 2 to 3.0 kg were anesthetized with intramuscular injection of a mixed solution of Ketalar (ketamine hydrochloride, Parke-Davis N.V. Warner-Lambert, Belgium SA) and Rompun (xylazine hydrochloride, Bayer AG, Levekusen, Germany) at 0.5 ml/kg each. A tumor implantation method was adapted from a previous liver study.27 Briefly, a right subcostal incision was made parallel to the 12th rib. The right kidney was exposed with the section of perinephrium. After a small incision of the renal capsule, a minipocket in the renal cortex was made with blunt division and temporary insertion of a piece of gelatin sponge (Spongostan, Ferrosan Co., Soeborj, Denmark). A cubic VX2 tumor fragment of 2 x 2 x 2 mm (acquired from research and development, Schering AG, Berlin, Germany) was inserted into the pocket after removal of the sponge. The renal capsule incision was sealed with the tissue adhesive Histoacryl (B. Braun AG, Melsungen, Germany), and the subcostal incision was closed in layers. The animals were scanned with MRI from 14 days after implantation to monitor tumor growth. VX2 lesions of 1.5 to 3.0 cm were considered appropriate for the treatment. The tumor growth was 100% (18 of 18) in the implantation sites.

Experimental Protocol
All together, 18 VX2 carcinoma nodules of 1.7 ± 0.5 cm in diameter in 18 rabbits were included in this study with the following treatments: RFA group, 12 rabbits with 12 VX2 tumors in the right kidney were treated with RFA; and control group, 6 rabbits with 6 renal VX2 tumors received sham operation and served as untreated controls.

Under the same anesthesia as in tumor implantation, the rabbit was laid in a left lateral position. A right subcostal incision was made along the primary incision for tumor implantation. The right kidney was exposed and immersed in the perinephric space with normal saline. Under visual inspection and manual palpation, an 18-gauge cooled-tip electrode (Radionics, Burlington, MA) was directly inserted into the tumor. This electrode contains two coaxial lumens that enable circulation of cooling water through the electrode. RF current was delivered from an RF generator (RFG-3E, Radionics) under power control mode at 30 W for 80 to 180 seconds, depending on the size of the tumor. The ablation volume covered both the entire tumor and a 5-mm rim of peritumoral renal parenchyma, as determined with direct visual inspection and manual palpation. After RFA, the electrode was withdrawn and the incision closed.

Under similar anesthesia and subcostal incision, the six control rabbits received sham operation without intratumoral electrode placement and were compared for survival with microangiographical and histological examinations at autopsy.

Therapeutic Evaluation
The efficacy of the therapy was evaluated with survival rate, MRI, microangiography, and histology. MRI was performed at days 0 and 1, weeks 1 and 2, and months 1 and 3, up to 6, after therapy. At the above-mentioned time points, one animal each was killed for systemic microangiography and histological examinations. Therapeutic assessment was based on the following criteria: (1) absolute tumor eradication, animals surviving longer than 6 months without any evidence of viable tumor; (2) relative tumor eradication (pathologic response), animals killed within 6 months after therapy and found free of viable tumor with MRI, microangiography, and histology; and (3) tumor local recurrence, remote metastasis with histological proof, or both.

MRI Follow-Up
Transverse T1 (repetition time/echo time [TR/TE] = 450/12 msec)- and T2 (TR/TE = 2500/90 msec)-weighted spin echo MRI (slice thickness of 3 mm) was obtained with a knee-coil in a 1.5 Tesla Magnetom Vision (Siemens, Erlangen, Germany) to follow the tumor growth after implantation and to monitor the ablation effects. Gadopentetatedimeglumine (Gd-DTPA; Magnevist, Schering AG) was injected intravenously with an MR-compatible injection system (Spectris, Medrad Europe, Maastricht, Netherlands) for contrast-enhanced imaging.

Postmortem Microangiography
As designed, the rabbit was killed with an intravenous overdose of pentobarbital (Nembutal, Sanofi Sante Animale, Benelux Brussels, Belgium) at above-mentioned time points, the same as MRI follow-up. Before excision of the kidney, the renal artery was injected with 50% barium suspension. Magnified angiography was performed on the excised samples by using a clinical mammography unit (Mammomat-2, Siemens) with Agfa Mammoray MR3-II films (Agfa-Gevaet N.V., Mortsel, Belgium).

Histopathological Examination
After death, the animals were autopsied. The presence of tumor invasion or metastases, if any, was recorded. The tissue specimens were suspended in 10% formalin solution for fixation. Histological processing consisted in paraffin imbedding sectioning at 5 µm thick and hematoxylin and eosin staining for light microscopy. The histological study was performed with a camera-ready light microscope (Axioskop 50, Carl Zeiss, Oberkochen, Germany). Different zones of the thermal ablation lesion were photographed for correlation and interpretations of the observed changes on imaging.

Statistics
The values were expressed as mean ± SD. Six-month survival was compared by using the {chi}2 test.. P < .05 was considered to be significant. This experiment complied with the current guidelines for use and care of laboratory animals of this institute.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
General Aspects of the Study
All rabbits tolerated the experimental procedures well, without clinical signs of renal failure such as poor general condition, anuria, uremia, or systematic edema. One week after RFA, one rabbit with tumor eradication developed a perinephric abscess caused by fistula of urine. Macroscopic hematuria was met in two rabbits during the first 2 days after RFA.

Tumor Ablation Effect
The animals in untreated control group died of end-stage malignancy at 80.7 ± 15.7 days with lymph node and lung metastasis. In the RFA group, tumor eradication was achieved in 10 rabbits (83.3%) without any evidence of tumor recurrence and metastasis. Among them, five rabbits survived longer than 6 months free of disease. Another five rabbits were found free of viable tumor when killed at days 0 and 1, week 1, and months 3 and 6. Two rabbits were found with local relapse at week 2 and month 1, and one had lung metastasis. The 6-month survival rate of RFA-treated rabbits was significantly higher (P < .01) than that of the control group (Table 1).


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  		TABLE 1. Summary of radiofrequency renal tumor ablation
 
MRI Findings
Before RFA, on T1-weighted spin echo images, most of the implanted VX2 tumors displayed almost identical but more heterogeneous signal intensity than normal cortical parenchyma (Figs. 1A and 2A). The tumors were inhomogeneously hypointense on T2-weighted images, with a hyperintense peritumoral rim (Figs. 1B and 2A'). After injection of Gd-DTPA, while the renal cortex was strongly enhanced, the tumors were inhomogeneously enhanced with a rim of high signal intensity (Fig. 1C).



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  		FIG. 1. Magnetic resonance images (MRI; A–C, A'–C'), microangiogram (D), macroscopic specimen (E), and microscopic view (F and G) from a rabbit with a renal VX2 tumor before and after radiofrequency ablation (RFA). (A–C) T1- and T2-weighted MRI (A, B) before RFA, and T1-weighted MRI (C) after gadopentetatedimeglumine (Gd-DTPA; 0.2 mmol/kg) injection. Before RFA, the VX2 tumor appeared iso- and hypointense on T1-weighted (A) and T2-weighted (B) images, respectively, and showed as a hypoenhanced area 3 minutes (C) after contrast because of a strong enhancement of renal parenchyma. (A'–C') T1- and T2-weighted MRI (A', B') after RFA, and T1-weighted MRI (C') after Gd-DTPA (0.2 mmol/kg) injection. On both T1-weighted (A') and T2-weighted (B') images, the RFA lesion including the VX2 tumor and a margin of normal kidney was well demarcated by a hypointense rim (arrows) presumably representing peripheral hemorrhage. The lesion was not enhanced by Gd-DTPA, suggesting a complete destruction of tumoral vasculature by RFA (C'). Arrowheads indicate the enhancement of peripheral edema and inflammatory zone. (D) Microangiogram displayed an area of barium filling defect resembling contrast enhanced MRI (C'). (E) Gross section of the kidney matched well with the MRI (A'–C') and angiographic (D) findings. T and R represent VX2 tumor and ablated renal tissue (approximately 5 mm thick), respectively. Arrowheads indicate the peripheral hemorrhage rim. The square indicates where the microscopy (F and G) was taken for pathological examination. (F and G) Microscopic view across the transition areas of ablated tumor (T) and renal tissues (R) up to perilesional normal kidney with inflammatory tissue reaction displays more remarkable ghost phenomenon in the central part of the lesion (F) with typical coagulative and hemorrhagic necrosis (arrow) close to the edge of the lesion (G). Hematoxylin and eosin staining with original magnification x200 and x100, respectively.

 


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  		FIG. 2. Magnetic resonance images (A–D, A'–D'), macroscopic section (E), and microangiogram (F) from a rabbit with a renal VX2 tumor before and serially after radiofrequency ablation (RFA). Plain (A–D) and gadopentetatedimeglumine-enhanced (A'–D') T1-weighted magnetic resonance images before (A, A') and 1 hour (B, B'), 4 weeks (C, C'), 6 months (D, D') after RFA revealed a tumor eradication by dynamic imaging follow-up of the therapy. T indicates tumor (A). Arrowhead indicates a layer of compressed peritumoral renal tissue (A'). Long arrows delineate peripheral hemorrhage caused by RFA (B, B'). Small arrows label the remaining scar tissue (D, D'). The gross section (E) shows an atrophied nodule of scar tissue (arrow), which matches the microangiogram (F).

 
Immediately after RFA, the signal intensity of tumors slightly increased in comparison with that of untreated tumors on T1-weighted images (Figs. 1A' and 2B). The ablated area, including the tumor and adjacent normal tissue (safety margin), became better delineated on both contrast-enhanced T1-weighted images (Fig. 1C') and plain T2-weighted images, on which a hypointense rim presumably corresponded to a hemorrhagic layer (Figs. 1B' and 2B').

During the follow-up, the ablated tumor and the part of the adjacent normal parenchyma showed progressive atrophy, with hyper- and hypointense signals on T1- and T2-weighted images, respectively. The remaining parenchyma showed a normal appearance (Fig. 2C, C', D, and D').

Microangiographic Findings
In comparison with the extremely hypervascularized normal renal parenchyma, the implanted VX2 tumors seemed relatively hypovascularized. After RFA, VX2 tumors, as well as the adjacent renal tissue, were completely or largely devascularized and appeared on microangiography as a barium-filling defect (Fig. 1D and E). Relapsing tumors showed the typical tumoral blood supply.

Histopathological Examination
Shortly after RFA, the following components could be identified macroscopically on the cross-section of the kidney (Fig. 1E): zone A, a needle track; zone B, a large pale area of tumoral coagulative necrosis; zone C, a layer of ablated normal renal parenchyma; zone D, a dark rim corresponding to congestion and hemorrhage; and zone E, a vague outer band corresponding to edema and peripheral inflammatory tissue reaction. Microscopically, the lesion early after RFA could also be defined into various areas: zone A, a small vacuolated or charred area around the needle track; zone B, a large area of coagulation necrosis of VX2 tumor but with almost intact tissue architecture (ghost phenomenon, Fig. 1F); zone C, a peritumoral band of ablated renal parenchyma, with similar ghost phenomenon (Fig. 1F); zone D, which could be divided into two parts, the inner part, in which necrosis is mixed with ghost red blood cells and eosinophilic matrix, and the outer part, in which hemorrhage with a large amount of normal red blood cells could be found (Fig. 1G); and zone E, edema and peripheral inflammatory tissue reaction (better visible than macroscopic view).

Months after RFA, the eradicated tumors and adjacent parenchyma became an atrophic mass with a fibrotic capsule and central coagulation necrosis (Fig. 2E).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
RFA is a heat-mediated method of tissue destruction. During the RFA, an electrode is inserted into the target tissue. High-frequency AC moves from the electrode through the surrounding tissue into the indifferent electrode. Ionic agitation is produced within the tissue as the ions attempt to follow the change in direction of the AC, which results in frictional heating of the tissue (resistive heating). When the temperature increases to a certain level (>70°C), coagulation necrosis develops in the tissue.28 The resistive heating is proportional to the square of the current density; the latter is inversely proportional to the square of the distance from the ablation electrode. Thus, power absorption is concentrated near the electrode-tissue interface and decreases rapidly with distance, roughly as 1/r2. Therefore, resistive heating decreases with the distance from the ablation electrode to the fourth power, i.e., 1/r4. The significant resistive heating occurs only within a narrow (<1 mm) rim of tissue in direct contact with the electrode because of the high local current density.29,30 It leads to overheating and boiling, tissue desiccation, and carbonization, and rapid impedance increase will quickly limit further current flow and tissue heating. Lesion volume will therefore be much smaller than desired. This intrinsic drawback has been largely circumvented because of the introduction of this cooled-tip electrode technique. With the internal cooling perfusion, the temperature of the electrode-tissue interface can be decreased and, therefore, the RF energy delivery and lesion size can be increased by means of preventing or postponing tissue carbonization.16

The major limitation of the previous studies on renal VX2 tumor ablation was a lack of survival assessment, which, however, represents the only gold standard in the studies of cancer therapies.12,13 VX2 carcinoma is a rabbit tumor of epithelial origin, derived from a virus-induced pappiloma.31 This tumor line is extremely malignant and can be allogeneously transplanted almost anywhere in rabbits.32 The discouraging therapeutic effects in previous studies can be partially attributed to the aggressiveness of this tumor line and to the disseminative tendency with inoculation of VX2 tumor cell suspension. As demonstrated in this study (Table 1), a substantial percentage of rabbits with VX2 renal tumors were radically treated with current RFA therapy. The eradication of VX2 tumors in this study was either absolutely proved by follow-up longer than 6 months free of disease after tumor implantation (any tumor relapse would cause animal death within this period) or relatively supported by MRI and microangiographical and histological findings. To our knowledge, this is the first report in which survival was used as an end point of the study and a large percentage of renal VX2 tumors were eradicated. This result can be attributable to several things. First, in this study the RFA was performed under open surgery, which enabled us to accurately target the tumor, control the lesion size, and avoid injury to the adjacent organs. Second, VX2 tumor fragment implantation, instead of tumor cell suspension injection, was used. This method can induce a localized tumor nodule and largely avoids simultaneous malignant dissemination via blood or lymph circulation, as seen with VX2 suspension inoculation. The sealing procedure avoids any tumor cell reflux from the incision and unexpected seeding to perinephrium. Third, the energy delivered through the cooled-tip electrode proved sufficient to encompass the entire tumor together with a peripheral safety margin. Finally, the immersion of the kidney in normal saline ensured a more homogeneous electric conductivity and prevented heat damage at the level of the renal hilus. Indeed, because the fat-containing perinephric sac has a lower electric conductivity in comparison to the renal hilus, which contains the main vessels, the concentration of RF current during the application may cause overheating and thermal damage to the hilus. For percutaneous ablation, we therefore suggest infusing normal saline into perinephric space to improve tissue conductivity and to avoid the hilar injury. Perinephric saline injection may also increase the distance between the heated tumor and other adjacent organs, such as the colon and adrenal gland, and, therefore, protect them from heat injury.

The peripheral hemorrhagic zone seen as a dark rim on both T1- and T2-weighted MRI is characteristic for in vivo RFA. This rim cannot be enhanced by Gd-DTPA and represents the true margin of the RFA lesion, which could be a useful symbol for monitoring the procedure. However, histology shows that the peritumoral hyperintense on T2 images or the Gd-DTPA–enhanced band on T1-weighted images corresponds to normal but compressed renal tissue with impaired drainage.

As in the liver tumors, various histological changes were observed according to the temperature gradient. The typical ghost phenomenon is in the area closer to the ablation center because of preservation of tumoral morphology by sudden tissue coagulation with intense heat.27 The typical coagulation necrosis is more to the periphery of the RFA lesion, presumably as a result of autolysis trigged by the moderate temperature increase in the periphery. This should be recognized for precise evaluation of therapeutic efficacy.

Potential complications of renal RFA include perinephric urinary fistula caused by electrode penetration into the pelvis or calyx, infections, and surrounding organ injury.

This study suggested that the kidney still could partially be spared while the tumor is eradicated. This would be most beneficial to patients who have a poor renal functional reserve, a poor general condition, or bilateral disease. An RFA therapy seems to be less invasive, safer, and more feasible than a surgery of partial nephrectomy.

In conclusion, the cooled-tip electrode mediated RFA seems to be a safe therapeutic method for eradication of localized renal tumors. MRI may prove useful for assessment of renal tumor ablation by viewing several characteristic bands.

Received for publication December 5, 2000. Accepted for publication June 4, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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