Correspondence *Robotic Urologic Surgery, Glickman Urological Institute, Cleveland Clinic, A100, 9500 Euclid Avenue, Cleveland, OH 44195, USA

Email kaoukj@ccf.org

Introduction

The incidence of renal cell carcinoma in the US has been increasing by 3.8–5.6% annually, mainly owing to the increased incidental detection of renal masses as a result of the widespread use of cross-sectional imaging.¹ The majority of these lesions are of low stage and have excellent prognoses.^{2, 3, 4} Nephron-sparing surgery for lesions smaller than 4 cm has been shown to be oncologically equivalent to radical nephrectomy, but additionally allows preservation of overall renal function.^{5, 6} As such, partial nephrectomy became the first-line treatment option for localized small renal masses. Partial nephrectomy (whether open or laparoscopic) is not ideal for all patients, however, especially those at raised risk of complications during surgery. Consequently, probe-ablative techniques—in particular cryoablation, radiofrequency ablation (RFA), and high-intensity focused ultrasound (HIFU)—are being investigated as possible alternatives to partial nephrectomy in selected patients. Advances in imaging, ablative system technologies, and early evidence that in situ tumor ablation can yield similar results to those achieved with tumor resection in selected cases, has sparked significant interest in these minimally invasive techniques. The aim of this article is to provide a critical evaluation of cryoablation, RFA, and HIFU, and in doing so to highlight the advantages and disadvantages of the various technologies.

Cryotherapy

Cryosurgery was originally described as a treatment for renal tumors during the 1960s.^{7, 8} In the 1990s, newly developed technologies led to a dramatic decrease in the size of cryoprobes and an increase in their cryogenic efficacy. These advances sparked new interest in renal cryosurgery. In 1995, Uchida⁹ reported the first use of percutaneous renal cryoablation, followed by the open approach a few years later.¹⁰ In 1998, Gill and colleagues¹¹ reported their first series of cases; they used a laparoscopic approach that incorporated real-time ultrasonographic visualization and renal biopsy. Initial clinical reports with intermediate follow-up data indicate that renal cryotherapy is technically feasible, safe, and has good oncological outcomes.^{12, 13} Until long-term data become available, however, cryoablation should be limited to small (<4 cm), solid, enhancing, renal tumors in older patients who are at high risk of complications during surgery.¹⁴

Laparoscopic cryotherapy

With laparoscopic techniques, the kidney is partially mobilized within Gerota's fascia and the perirenal fat surrounding the renal mass is excised and undergoes pathological examination. Renal assessment by use of a laparoscopic, flexible, ultrasound probe aids localization of the renal mass, guides the biopsy needle, and directs insertion of the cryoprobe(s). One or more cryoprobes (according to the size and configuration of the kidney mass) are positioned so as to ensure that the intended ice ball will extend beyond the renal mass margin by at least 1 cm. Each cryoprobe is inserted perpendicularly into the renal lesion, via a laparoscopic port or directly through a small skin incision, under laparoscopic visualization. Under real-time ultrasonographic guidance, the tip of the cryoprobe is advanced into and just beyond the inner margin of the renal mass, and a rapid freeze cycle is performed. The renal epithelial tissue is completely ablated and necrosis ensues once a tissue temperature of -19.4 °C or lower is achieved.¹⁶

Rapid tissue freezing is efficiently achieved with the current argon-based systems, with which the cryoprobe tip can reach a temperature of -150 °C within 2–3 min. Inclusion of the renal mass within the ice ball is not an absolute predictor of cellular death; in fact, the ice ball must extend beyond the tumor's edge by a minimum of 3.1 mm in order to achieve a target temperature of less than -20 °C at the tumor margin.¹⁷ For this reason, the hyperechoic leading edge of the ice ball as seen on ultrasound monitoring should extend circumferentially beyond the renal mass by at least 1 cm.

A slow, passive thaw is then performed after the initial rapid freeze cycle, until the temperature at the center of the renal mass (as monitored through the cryoprobe) reaches 0 °C. Two freeze–thaw cycles are performed because previous studies have shown improved tissue necrosis with this approach.¹⁸ Typically, real-time ultrasound guidance is of limited use during the second freeze–thaw cycle because the ablated renal mass becomes anechoic. A bluish halo can be seen on laparoscopy, however, which marks the hemorrhagic edge of the tissue that was frozen in first cycle and indicates the boundary that should be used for the second rapid freeze cycle. Upon completion of the second freeze, an active thaw is performed by heating the cryoprobe with pressurized helium.

The cryoprobe is gently removed once the probe temperature reaches 0 °C; the probe can then be easily retracted from the renal lesion. Once the cryoprobe has been removed, our technical preference is to inject FloSeal^® hemostatic matrix (Baxter International Inc, Deerfield, IL) into the cryoprobe tract to quickly halt bleeding, followed by compression with Surgicel^® (Johnson & Johnson, Piscataway, NJ) absorbable hemostatic dressing for approximately 10–15 min. No drains are left, and the laparoscopic exit is accomplished in the usual manner after confirming adequate hemostasis at zero intraperitoneal insufflation pressure (Figure 1).

Figure 1 Intraoperative images obtained during laparoscopic cryoablation of a renal mass

Ultrasonography was used to monitor the developing ice ball.

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Intermediate-term follow-up results of cryotherapy have been encouraging and support ongoing investigations. Gill et al.¹³ reported that 51 patients who underwent laparoscopic cryotherapy for a unilateral, sporadic renal tumor had cancer-specific survival of 98%, with a minimum follow-up of 3 years. No conversions to open surgery, hemorrhages, urinary fistulas, dialysis requirements, perirenal or port-site recurrences occurred in any of these patients. In this series, follow-up included routine renal biopsy of the cryolesion 6 months after treatment. Two patients developed local renal recurrences at 18 and 30 months, respectively.

Davol and colleagues¹² treated 48 patients in whom the median tumor size was 2.6 cm. They applied renal cryoablation by either an open or laparoscopic approach, and patients were followed up for 36–110 months (median 5 years) after the initial procedure. Cancer-free survival was 87.5% after one cryoablation treatment, and 97.5% after repeated cryoablation. Repeat procedures were required in 12.5% of the initially treated patients. Even though these initial 5-year results seemed promising, the authors reported that more than 30% of the patients failed to comply with postablation radiological monitoring, which could have exaggerated their cancer-specific risk. According to these results, a successful course of cryoablative treatment might require multiple procedures, close radiological monitoring, and patient education to encourage strict compliance with radiological follow-up.

Percutaneous cryotherapy

Percutaneous cryotherapy is an attractive approach for ablation of small renal masses because it can be performed with minimal surgical manipulation and, for most patients, requires only conscious sedation and a local anesthetic. This technique is, however, limited to posterior and posterolateral renal masses that are accessible percutaneously.

Early results for percutaneous cryoablation were reported by Uchida et al.,⁹ who used ultrasonographic guidance to monitor the renal ice ball. Although ultrasonography provides real-time images, the quality of the images is limited and only the near edge of the ice ball can be visualized. By contrast, CT fluoroscopy provides superior monitoring during percutaneous cryotherapy because a complete cross-section of the ice ball can be displayed.¹⁹ CT fluoroscopy also allows real-time guidance for placement of the cryoprobes and is readily available in most centers. Gupta and colleagues²⁰ demonstrated that CT-guided ablation is technically feasible under conscious sedation, and reported only one complication—a perirenal hematoma that required a blood transfusion—in 20 patients with 27 lesions. No signs of enhancement were seen in 15 of the 16 cryoablated lesions for which at least 1 month of follow-up (mean 5.9 months) was available.

MRI-guided cryoablation has also been developed and studied. MRI guidance during cryotherapy delivers high-resolution images with real-time monitoring of the ice ball, along with the added important benefit of no radiation exposure.²¹ Access to interventional MRI equipment is, however, limited. Shingleton and Sewell²² have reported the most extensive experience to date; they documented treatment of 120 lesions by MRI-guided cryotherapy in 103 patients. With a median follow-up of 35.5 months, the authors reported disease-specific survival of 97%. Of note, 14.5% of patients required re-treatment, but only one major complication—a perinephric hematoma that required a blood transfusion—was reported. This same group also assessed MRI-guided percutaneous cryotherapy in patients with von Hippel–Lindau disease.²³ In a feasibility study, five tumors (diameter range 2.8–5.0 cm) were treated in four patients. All patients underwent cryoablation without difficulty. Re-treatment was required in two cases because of residual tumor. Imaging at 2–23 months of follow-up revealed no radiographic evidence of recurrence in the cryoablated areas.

Percutaneous cryotherapy, whether done under CT or MRI guidance, is an attractive method of treatment for renal masses, but its oncological efficacy needs to be validated in long-term studies. Ultrasound guidance during cryoablation is an evolving technique, but significantly improved clinical outcomes have yet to be demonstrated (Figure 2).

Figure 2 CT scan during percutaneous cryoablation of a renal mass

Note the hypoechoic appearance of the developing ice ball.

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Radiofrequency ablation

In 1997, Zlotta et al.²⁴ first described the use of RFA to produce extensive, localized necrosis of renal tumors. Findings were reported for three lesions in three patients. Following RFA, the tumors were resected and underwent histological examination; the results indicated that RFA could safely produce localized necrosis in the targeted tumor tissue. Subsequently, McGovern and colleagues²⁵ reported placement of an RFA electrode under ultrasound guidance. Following these initial series, many centers have studied the use of percutaneous and laparoscopic applications of RFA for the treatment of renal masses (Figure 3).^{26, 27, 28, 29, 30, 31, 32, 33, 34}

Figure 3 CT scan during percutaneous radiofrequency ablation of a renal mass, using a probe with multiple tines

 

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During RFA, a high-frequency (460–500 kHz) alternating electrical current is passed between an electrode placed into targeted tissue and a grounding pad placed on the patient's thighs. Ionic agitation of the tissue adjacent to the RFA electrode causes friction that is subsequently converted into heat.³⁵ The heating process induces cellular damage, then death, after the temperature exceeds 50–52 °C for 4–6 min.³⁶ At temperatures higher than 60 °C cell death is immediate.³⁷ The goal of RFA is, therefore, to achieve and maintain a 50–100 °C temperature range throughout the targeted tissue volume.³⁸ Temperatures higher than 105 °C result in tissue vaporization and charring, which retards energy transmission and reduces the effectiveness of tissue ablation.³⁹

Three radiofrequency generators are commercially available: RITA^® Model 1500X—a temperature-based feedback system (RITA Medical Systems, Fremont, CA); the Cool-tip^™ Radiofrequency Ablation System (Valleylab, Boulder, CO), which is an impedance-based feedback system; and another impedance-based feedback system, the RF 3000^® Radiofrequency Ablation System (Boston Scientific, Natick, MA). The various electrodes available for each system are listed in Table 1. No comparative studies have yet established any advantage of one system over another. Studies in several series have assessed the efficacy of RFA, but most had short follow-up durations and small numbers of patients.^{26, 27} Nevertheless, the findings from these early studies could still provide insight into this evolving technology. Hwang et al.²⁸ reported the use of a 200 W generator to perform renal RFA in 17 patients with a total of 24 hereditary renal tumors. Tumor recurrence was seen in only one (4%) patient at 12-month follow-up. By contrast, in an earlier series reported by the same investigators in which 19 patients were treated with a first-generation 50 W device, residual enhancement was seen in 40% of the ablated tumors after a median follow-up of 24 months. On the basis of the disparity in results between these two series, the authors concluded that use of the 200 W generator provided superior results because this system reduced convective heat losses and provided a more consistent distribution of energy throughout the tumor compared with the 50 W system.

Table 1 Commercially available radiofrequency ablation systems

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The size and location of renal tumors might affect the efficacy of RFA. Varkarakis et al.³⁰ reported that size had an effect on efficacy in 46 patients with 56 tumors who were treated with RFA while under conscious sedation. The success rate for tumors smaller than 3 cm was 100% compared with 78% for those larger than 3 cm, while treatment of peripheral renal tumors was also 100% successful, compared with an 82% success rate for central renal tumors. In this series, 24 patients had histologically confirmed malignancy; within this subset of patients the success rate of RFA was 96.3%. Further evidence in support of the use of CT-guided RFA for treating small tumors was provided by Zagoria and colleagues,³¹ who used this technique in 27 sessions with 22 patients. Complete tumor ablation was achieved in 91% of the patients at a mean of 7 months' follow-up, and in all tumors smaller than 3 cm treated with only a single session of RFA.³¹ Furthermore, in one of the largest series reported, which had a mean follow-up of 2.3 years, Gervais et al.³² treated 100 renal tumors in 85 patients, and concluded that all tumors <4 cm were completely ablated.³² Multivariate analysis that assessed the effect of tumor size and location on the likelihood of complete ablation after the first treatment showed that both small size (<3 cm) and peripheral location were independent predictors of success (P <0.0001 and P = 0.0049, respectively). The most common complication, hemorrhage, occurred in five patients, two of whom required transfusion; no delayed hemorrhages were noted.

A phase II clinical trial that used MRI-guided RFA to treat 10 patients whose lesions had a mean diameter of 2.3 cm showed no evidence of tumor recurrence after a mean of 25 months' follow-up.³³ All procedures were completed under conscious sedation and the RFA was monitored throughout. The procedure continued until the entire ablated tumor was replaced by low-intensity signals on MRI. The investigators felt that the ability of MRI to detect inadequately treated parts of the tumor during RFA was critical to limitation of RFA to ablate the entire lesion in one session.

Laparoscopic application of RFA is possible, as demonstrated by Jacomides et al.³⁴ in the treatment of 17 renal tumors. Five ablated tumors were excised immediately after RFA. One of the five had a focally positive margin, yet the patient remained disease-free 1 year after treatment. All other patients in whom in situ ablation was performed remained recurrence-free after a mean of 9.8 months of follow-up.

Radiofrequency ablation versus cryoablation

The probes available for ablation, the mechanisms of ablation, and the properties associated with RFA and cryoablation highlight some of the differences between these two technologies. A single-institution, retrospective comparison of 164 laparoscopic cryoablations and 82 CT-guided percutaneous RFA procedures indicated that treated patients had a cancer-specific survival of 98% at a median follow-up of 3 years after laparoscopic cryotherapy, and 100% at a median follow-up of 1 year after percutaneous RFA.⁴⁰ Complication rates were minimal in both groups of patients, despite significant preoperative comorbidities. Clearly, extended-duration studies are required to compare the effectiveness and clinical outcomes of these two treatments. Several technical variations in application between RFA and cryoablation are listed in Table 2.

Table 2 Comparison of the renal ablative technologies

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One major advantage of cryotherapy over RFA is the ability to monitor an evolving ice ball intraoperatively during cryotherapy. The surgeon is able to monitor the progress of ablation and can ensure complete destruction of the renal mass with an adequate treatment margin. During RFA, the ablated zone cannot be monitored effectively with currently available technology.

On the basis of findings from animal studies, cryoinjury to the renal collecting system does not seem to result in substantial urinary extravasation or caliceal fistula formation.⁴¹ Other experimental evidence for RFA, however, demonstrates that this procedure does not spare the collecting system.⁴² This feature of RFA could have important clinical ramifications if renal masses are deep. Oncologically, concern has been expressed that skip lesions with viable cancer cells might persist in the ablated zone after RFA.⁴³ Moreover, some reports have expressed concern over the adequacy of various imaging techniques for the detection of tumor recurrence during follow-up of RFA-treated patients.⁴⁴ Overall, however, cryoablation and RFA techniques are associated with a low complication rate; complications are mostly limited to pain or paresthesia at the probe site (Table 3).⁴⁵

Table 3 Comparison of cryoablation and radiofrequency ablation for renal tumors

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High intensity focused ultrasound

Extracorporeal or percutaneous applications of HIFU (so-called no-touch techniques) are an appealing concept for the treatment of small renal lesions. Essentially, a highly focused ultrasound wave is generated at a specific focus and depth within the body. By moving the HIFU transducer over the patient's skin, the entire renal lesion can be treated. The high-energy ultrasound beam is generated by a cylindrical piezoceramic element, with a parabolic reflector that allows precise focusing of the beam at a desired target within the patient's body.⁴⁶ Hacker et al.,⁴⁷ in a pilot clinical study of 19 patients scheduled to undergo radical nephrectomy for renal tumors, applied HIFU before nephrectomy to investigate the safety and effect of this technique on healthy renal tissue. HIFU effects in the focal zone immediately after application were interstitial hemorrhages, fiber rupture, shrinking of collagen fibers, and coagulation necrosis, but these events occurred sporadically and did not correlate with the number of HIFU pulses applied. Interestingly, on histological analysis, the mechanical effects (cavitation, acoustic streaming, and oscillatory motion) of HIFU were deemed to prevail over the thermal effects. The authors concluded that further refinements in the technology are required to enable complete and reliable tissue ablation.

Few clinical trials have assessed the application of HIFU as a treatment for renal tumors. Kormann and colleagues⁴⁸ reported an initial clinical trial of HIFU in one patient who had three renal tumors. In this case, two lower-pole kidney tumors shrank after treatment, but the upper-pole tumor was not affected because the energy waves were absorbed by the ribs. Marberger et al.⁴⁹ reported the sonication of 16 renal tumors: in two elderly patients, HIFU was performed with curative intent and resulted in incomplete radiological remission. In the other 14 patients, the tumors were excised after HIFU treatment, in the same session. Histological changes suggestive of necrosis were detected in nine tumors; however, HIFU had ablated only 15–35% of the targeted area. During this study, many modifications were made in the HIFU treatment parameters, including changes in the electrical power, diameter of the reflector, diameter of the aperture, and, most notably, the addition of a mechanical arm to direct the transducer. This study highlighted many of the shortcomings of currently available HIFU technology in relation to treatment of renal tumors. Specifically, respiratory movement is a significant problem, and upper-pole renal masses with an overlying rib are difficult to treat. Moreover, the structural heterogeneity within small renal masses affects the acoustic interfaces of the HIFU beam, which produces inconsistent tissue ablation.

Wu and colleagues⁵⁰ reported their experience of treating renal tumors with a HIFU system from Chongqing, China. This device has the ability to 'paint' the target area in sequential linear tracks. A low complication rate was seen in the 13 treated patients; hematuria resolved in 7 of 8 patients and tumor-related pain decreased in 9 of 10 patients. Complete ablation was achieved in 3 out of 13 renal tumors, and the remaining 10 tumors were partly ablated. A similar system was evaluated by Marberger et al. in a phase II clinical trial in which four patients were treated with HIFU.⁴⁹ Three of the four lesions were excised 6 weeks after HIFU, but there was no evidence of ablation within the specimens. Currently, renal applications of HIFU are experimental, owing to its limited success; further refinements are clearly necessary in order for HIFU to be used clinically in the treatment of renal lesions.

Imaging follow-up

Given that many renal lesions treated with probe-ablative procedures are not excised and the margin of excision is not confirmed by pathological examination, a rigorous follow-up protocol needs to be implemented for treated patients. At the Cleveland Clinic, follow-up MRI is performed the day after ablation, then at 3, 6, and 12 months after the procedure, and annually thereafter.⁵¹ This comprehensive follow-up is necessary because probe ablation is an evolving technology. As more data on the oncological efficacy of probe-ablative procedures become available, the hope is that the evidence will support use of a simplified follow-up in the future, perhaps comprising MRI or CT of the kidney at 3 months and then yearly thereafter. Ideally, the cryolesion should show no evidence of enhancement on follow-up CT or MRI, and the ablated tumor size should have stayed the same or decreased.⁵²

Conclusions

Significant amounts of data are accumulating on ablative technologies. The early data on cryotherapy suggest that this technique is an effective treatment for renal lesions smaller than 4 cm. For RFA, although initial results are promising, long-term follow-up data should be awaited before the technique can be widely recommended. Use of HIFU in the ablation of renal masses remains experimental, since no significant clinical studies have demonstrated consistent results. Until reliable, long-term, oncologic data become available, these technologies are second-line treatment options for localized renal tumors, and their use should be restricted to patients who are unwilling or unable to undergo an open or laparoscopic partial nephrectomy.

References

1. Chow WH et al. (1999) Rising incidence of renal cell cancer in the United States. JAMA 281: 1628–1631 | Article | PubMed | ISI | ChemPort |
2. Bretheau D et al. (1995) Prognostic significance of incidental renal cell carcinoma. Eur Urol 27: 319–323 | PubMed | ChemPort |
3. Jayson M and Sanders H (1998) Increased incidence of serendipitously discovered renal cell carcinoma. Urology 51: 203–205 | Article | PubMed | ISI | ChemPort |
4. Homma Y et al. (1995) Increased incidental detection and reduced mortality in renal cancer—recent retrospective analysis at eight institutions. Int J Urol 2: 77–80 | PubMed | ChemPort |
5. Fergany AF et al. (2000) Long-term results of nephron sparing surgery for localized renal cell carcinoma: 10-year followup. J Urol 163: 442–445 | Article | PubMed | ISI | ChemPort |
6. Lee CT et al. (2000) Surgical management of renal tumors 4 cm or less in a contemporary cohort. J Urol 163: 730–736 | Article | PubMed | ISI | ChemPort |
7. Lutzeyer W (1972) Advancements in operative therapy (urology). Langenbecks Arch Chir 332: 137–145 | Article | PubMed | ChemPort |
8. Lutzeyer W et al. (1968) Experimental cryosurgery of the kidney. Langenbecks Arch Chir 322: 843–847 | PubMed | ChemPort |
9. Uchida M et al. (1995) Percutaneous cryosurgery for renal tumours. Br J Urol 75: 132–136 | PubMed | ChemPort |
10. Delworth MG et al. (1996) Cryotherapy for renal cell carcinoma and angiomyolipoma. J Urol 155: 252–255 | Article | PubMed | ChemPort |
11. Gill IS et al. (1998) Laparoscopic renal cryoablation: initial clinical series. Urology 52: 543–551 | Article | PubMed | ISI | ChemPort |
12. Davol PE et al. (2006) Long-term results of cryoablation for renal cancer and complex renal masses. Urology 68 (Suppl): 2–6 | Article |
13. Gill IS et al. (2005) Renal cryoablation: outcome at 3 years. J Urol 173: 1903–1907 | Article | PubMed | ISI |
14. Kaouk JH et al. (2006) Cryotherapy: clinical end points and their experimental foundations. Urology 68: 38–44 | Article | PubMed |
15. Hoffmann NE and Bischof JC (2002) The cryobiology of cryosurgical injury. Urology 60 (Suppl 1): 40–49 | Article |
16. Chosy SG et al. (1998) Monitoring renal cryosurgery: predictors of tissue necrosis in swine. J Urol 159: 1370–1374 | Article | PubMed | ISI | ChemPort |
17. Campbell SC et al. (1998) Renal cryosurgery: experimental evaluation of treatment parameters. Urology 52: 29–34 | Article | PubMed | ISI | ChemPort |
18. Woolley ML et al. (2002) Effect of freezing parameters (freeze cycle and thaw process) on tissue destruction following renal cryoablation. J Endourol 16: 519–522 | Article | PubMed |
19. Permpongkosol S et al. (2006) Percutaneous renal cryoablation. Urology 68 (Suppl): 19–25 | Article |
20. Gupta A et al. (2006) Computerized tomography guided percutaneous renal cryoablation with the patient under conscious sedation: initial clinical experience. J Urol 175: 447–453 | Article | PubMed | ISI |
21. Shingleton WB and Sewell PE Jr (2001) Percutaneous renal tumor cryoablation with magnetic resonance imaging guidance. J Urol 165: 773–776 | Article | PubMed | ISI | ChemPort |
22. Sewell P and Shingleton WB (2004) Five-year treatment success and survival of patients treated with percutaneous IMRI guided and monitored renal cell carcinoma cryoablation. BJU Int 94 (Suppl 2): S106
23. Shingleton WB and Sewell PE Jr (2002) Percutaneous renal cryoablation of renal tumors in patients with von Hippel–Lindau disease. J Urol 167: 1268–1270 | Article | PubMed | ISI |
24. Zlotta AR et al. (1997) Radiofrequency interstitial tumor ablation (RITA) is a possible new modality for treatment of renal cancer: ex vivo and in vivo experience. J Endourol 11: 251–258 | PubMed | ChemPort |
25. McGovern FJ et al. (1999) Radio frequency ablation of renal cell carcinoma via image guided needle electrodes. J Urol 161: 599–600 | Article | PubMed | ChemPort |
26. Farrell MA et al. (2003) Imaging-guided radiofrequency ablation of solid renal tumors. AJR Am J Roentgenol 180: 1509–1513 | PubMed | ChemPort |
27. Roy-Choudhury SH et al. (2003) Early experience with percutaneous radiofrequency ablation of small solid renal masses. AJR Am J Roentgenol 180: 1055–1061 | PubMed |
28. Hwang JJ et al. (2004) Radio frequency ablation of small renal tumors: intermediate results. J Urol 171: 1814–1818 | Article | PubMed | ChemPort |
29. Pavlovich CP et al. (2002) Percutaneous radio frequency ablation of small renal tumors: initial results. J Urol 167: 10–15 | Article | PubMed | ISI |
30. Varkarakis IM et al. (2005) Percutaneous radio frequency ablation of renal masses: results at a 2-year mean followup. J Urol 174: 456–460 | Article | PubMed | ISI |
31. Zagoria RJ et al. (2004) Percutaneous CT-guided radiofrequency ablation of renal neoplasms: factors influencing success. AJR Am J Roentgenol 183: 201–207 | PubMed |
32. Gervais DA et al. (2005) Radiofrequency ablation of renal cell carcinoma: part 1, indications, results, and role in patient management over a 6-year period and ablation of 100 tumors. AJR Am J Roentgenol 185: 64–71 | PubMed |
33. Lewin JS et al. (2004) Phase II clinical trial of interactive MR imaging-guided interstitial radiofrequency thermal ablation of primary kidney tumors: initial experience. Radiology 232: 835–845 | Article | PubMed |
34. Jacomides L et al. (2003) Laparoscopic application of radio frequency energy enables in situ renal tumor ablation and partial nephrectomy. J Urol 169: 49–53 | Article | PubMed |
35. Lui KW et al. (2003) Radiofrequency ablation of renal cell carcinoma. Clin Radiol 58: 905–913 | Article | PubMed |
36. Goldberg SN et al. (1996) Radio-frequency tissue ablation of VX2 tumor nodules in the rabbit lung. Acad Radiol 3: 929–935 | PubMed | ChemPort |
37. Chong WK (2001) Radiofrequency ablation of liver tumors. J Clin Gastroenterol 32: 372–374 | Article | PubMed | ChemPort |
38. Goldberg SN et al. (2000) Thermal ablation therapy for focal malignancy: a unified approach to underlying principles, techniques, and diagnostic imaging guidance. AJR Am J Roentgenol 174: 323–331 | PubMed | ChemPort |
39. Goldberg SN et al. (1996) Radiofrequency tissue ablation: importance of local temperature along the electrode tip exposure in determining lesion shape and size. Acad Radiol 3: 212–218 | Article | PubMed | ChemPort |
40. Hegarty NJ et al. (2006) Probe-ablative nephron-sparing surgery: cryoablation versus radiofrequency ablation. Urology 68 (Suppl): 7–13 | Article |
41. Sung GT et al. (2003) Effect of intentional cryo-injury to the renal collecting system. J Urol 170: 619–622 | Article | PubMed |
42. Janzen NK et al. (2005) The effects of intentional cryoablation and radio frequency ablation of renal tissue involving the collecting system in a porcine model. J Urol 173: 1368–1374 | Article | PubMed |
43. Michaels MJ et al. (2002) Incomplete renal tumor destruction using radio frequency interstitial ablation. J Urol 168: 2406–2410 | Article | PubMed |
44. Hegarty NJ et al. (2006) Lack of enhancement on 6-month MRI does not guarantee complete cancer cell kill following radiofrequency ablation of small renal tumors [abstract]. J Urol 175 (Suppl): 552 | Article |
45. Johnson DB et al. (2004) Defining the complications of cryoablation and radio frequency ablation of small renal tumors: a multi-institutional review. J Urol 172: 874–877 | Article | PubMed |
46. Kohrmann KU et al. (2002) Technical characterization of an ultrasound source for noninvasive thermoablation by high-intensity focused ultrasound. BJU Int 90: 248–252 | Article | PubMed | ISI | ChemPort |
47. Hacker A et al. (2006) Extracorporeally induced ablation of renal tissue by high-intensity focused ultrasound. BJU Int 97: 779–785 | Article | PubMed |
48. Kohrmann KU et al. (2002) High intensity focused ultrasound as noninvasive therapy for multilocal renal cell carcinoma: case study and review of the literature. J Urol 167: 2397–2403 | Article | PubMed | ISI |
49. Marberger M et al. (2005) Extracorporeal ablation of renal tumours with high-intensity focused ultrasound. BJU Int 95 (Suppl 2): 52–55 | Article |
50. Wu F et al. (2003) Preliminary experience using high intensity focused ultrasound for the treatment of patients with advanced stage renal malignancy. J Urol 170: 2237–2240 | Article | PubMed | ISI |
51. Remer EM et al. (2000) MR imaging of the kidneys after laparoscopic cryoablation. AJR Am J Roentgenol 174: 635–640 | PubMed | ChemPort |
52. Anderson JK et al. (2006) Imaging associated with percutaneous and intraoperative management of renal tumors. Urol Clin North Am 33: 339–352 | Article | PubMed |

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Subject areas under which this article appears: Urologic oncology (nonprostatic)