Current Opinion in Urology:
NEPHRON-SPARING SURGERY FOR RENAL CANCERS: Edited by Tobias Klatte
Thermal ablation in renal cell carcinoma management: a comprehensive review
Wagstaff, Peter*; Ingels, Alexandre*; Zondervan, Patricia; de la Rosette, Jean J.M.C.H.; Laguna, M. Pilar
Department of Urology, Academic Medical Center, Amsterdam, Netherlands
*Peter Wagstaff and Alexandre Ingels contributed equally to the writing of this article.
Correspondence to M. Pilar Laguna, MD, PhD, Department of Urology, Academic Medical Center, PO Box 22660, Amsterdam 1100DD, Netherlands. Tel: +31 20-5668637; e-mail: firstname.lastname@example.org
Purpose of review: This article provides an overview of recent developments in the field of thermal ablation for renal cell carcinoma and focuses on current standard techniques, new technologies, imaging for ablation guidance and evaluation, and future perspectives.
Recent findings: Emerging long-term data on cryoablation and radiofrequency ablation (RFA) show marginally lower oncologic outcomes compared to surgical treatment, balanced by better functional and perioperative outcomes. Reports on residual disease vary widely, influenced by different definitions and strategies in determining ablation failure. Stratifying disease-free survival after RFA according to tumor size suggests 3 cm to be a reasonable cut off for RFA tumor selection. Microwave ablation and high-intensity focal ultrasound are modalities with the potential of creating localized high temperatures. However, difficulties in renal implementation are impairing sufficient ablation results. Irreversible electroporation, although not strictly thermal, is a new technology showing promising results in animal and early human research.
Summary: Although high-level randomized controlled trials comparing thermal ablation techniques are lacking, evidence shows that thermal ablation for small renal masses is a safe procedure for both long-term oncologic and functional outcomes. Thermal ablation continues to be associated with a low risk of residual disease, for which candidates should be properly informed. RFA and cryoablation remain the standard techniques whereas alternative techniques require further studies.
Treatment of renal cell carcinoma (RCC) has tremendously changed during the past decades. Increasing incidence of small renal masses, incidentally diagnosed from routinely performed imaging, has led to question the sense of systematically removing the entire kidney in this setting. Sparing nephrons through partial instead of radical nephrectomy has demonstrated to prevent long-term renal failure, cardiovascular disease, and overall mortality . It eventually has become the reference standard of care . For the last decade, focal therapy has been positioned as an alternative to partial nephrectomy in selected cases. This strategy is mostly based on thermal ablation by freezing (cryoablation) or heating (radiofrequency) the tumor. Although those recent technologies present obvious advantages for patients and the healthcare system in terms of surgery-related morbidity, length of procedure time, and hospital stay, their relevant application in practice is still debated. Recent European Association of Urology and American Urological Association guidelines on RCC remain cautious with their indication [2,3]. Because of a lack of long-term evaluation of oncologic outcomes and prospective randomized trials, it is still reserved for poor surgical candidates when a compromise has to be found between tumor management and procedure morbidity. We present here the current knowledge on thermal ablation and have reviewed the recent literature including the evaluation of standard techniques, development of new technologies, and the future perspectives envisioned through basic science reports.
UPDATE ON STANDARD TECHNIQUES
Cryoablation and radiofrequency ablation (RFA) are the standard techniques in thermal ablation practice. Early 5 and 10-year oncological results showed cryoablation and RFA to be slightly inferior to partial nephrectomy, balanced by a lower complication rate.
A global update with longer evaluation of oncologic outcomes for thermal ablation techniques is summarized in Table 1. A study by Psutka et al. [4▪▪] reported a series of 185 patients treated with percutaneous RFA for sporadic T1 RCC. Median follow-up was of 6.43 years and minimum follow-up was of 5 years. Disease-free survival (DFS), overall survival (OS), and cancer-specific survival (CSS) at 5 years were 87.6, 73.3, and 99.4%, respectively. In all the studies reporting these data, DFS, OS, and CSS at 5 years ranged from 83.1 to 97% [4▪▪,5,6▪,7▪,10,11,14▪,15,17], 63 to 97.8% [4▪▪,5,6▪,7▪,12▪,14▪,15,16], and 96.4 to 100% [4▪▪,5,6▪,7▪,9,10,14▪,15], respectively. This long-term oncological evidence proves that thermal ablation is a safe strategy for RCC management, comparable to partial nephrectomy, in terms of oncologic outcomes. It has been reported that thermal ablation presents a high rate of residual disease. When it was reported, the range was 1.3–8.2% for cryoablation [5,8,12▪] versus 0–19% for RFA [5,6▪,7▪,10,11,15–18,20,21]. This wide range can be explained by discrepancies in tumor size, nonsystematic pathological confirmation of RCC before ablation (a significant amount of treated tumors might not be malignant), and the lack of standardized definition of residual disease – some recurrences are defined by biopsy-proven residual cancer while others solely on signal enhancement around the ablation zone on contrast-enhanced computed tomography. As it will be discussed further, these two definitions present limitations and the different strategies to diagnose ablation recurrence make series hardly comparable.
Another major input from recent literature on thermal ablation is the role of tumor size for oncologic outcomes. Best et al.  reported their experience on RFA (laparoscopic and percutaneous) of 159 tumors (142 patients) by stratifying their analysis by tumor size. With a median follow-up of 4.5 years, the 3-year DFS was of 96% for tumors less than 3 cm versus 79% for tumors 3 cm or larger (P = 0.001). However, there was no significant difference when comparing tumors with ranges smaller than 3 cm. This study suggests that 3 cm would be a reasonable threshold to set the indication of thermal ablation in RCC management. Other studies confirmed the significant role of tumor size to predict recurrence [4▪▪,7▪,9].
Who is the good candidate?
Although the European Association of Urology and the American Urological Association guidelines reserve focal therapy for poor surgical candidates [2,3], Ma et al. [6▪] analyzed long-term outcomes of 52 healthy adults after RFA of T1a renal tumors. With a mean tumor size of 2.2 cm and a median follow-up of 60 months, 5 and 10-year DFSs were of 94.2%. It is hazardous to draw conclusions from a noncomparative retrospective study. However, these results are comparable with partial nephrectomies and should encourage controlled trials to open indications for well selected healthy patients harboring small renal tumors.
Schmit et al. [12▪] compared morbidity and technical failures between nonobese, obese, and morbidly obese patients from their 367 patients series on percutaneous cryoablation. There was no significant difference between the three populations in terms of complication rates or residual disease. Percutaneous thermal ablation is certainly a relevant strategy to treat small renal masses for overweight population where surgical extirpation through an open or laparoscopic approach remains challenging.
Perioperative and functional outcomes
Many articles have reported on functional outcomes of thermal ablations (Table 2). In order to compare the studies and to get clear information from this review, our analysis focused on length of hospital stay, complications from thermal ablations, and impact of the procedure on renal function. When reported, hospital stay ranged from 1 to 2.8 days [7▪,8–10,12▪,13,21,22]. In their retrospective study, Panumatrassamee et al.  compared outcomes from 29 cryoablations (laparoscopic and percutaneous) versus 33 partial nephrectomies. Median hospital stay was significantly longer in the partial nephrectomy arm (4 versus 1 day). For procedure-related morbidity, the rates ranged from 5 to 16% for minors and 2 to 9.5% for major complications [5,7▪,8–10,12▪,13,16,23–25]. However, we should cautiously interpret these data since studies are hardly comparable to each other. Indeed, severe complications could be Dindo-Clavien greater than 2 or greater than 3 depending on the series. Moreover, some studies based their analyses on Dindo-Clavien while others on the society of interventional radiology [7▪,16] classification. Regarding kidney function damage, the decrease from preoperative to postoperative glomerular filtration rate ranged from 1 to 13.6% [6▪,7▪,9,10,13,14▪,16,18,19,21]. Again, the wide range can be explained by discrepancies between baseline renal function before treatment – from 54.7 to 106.3 ml/min/1.73 m2 [6▪,7▪] – and by different end points between studies. When RFA was performed for patients harboring a tumor on a solitary kidney, the mean function decrease was of 18.8% .
Although prospective trials to compare techniques are still awaited to rigorously define the right place of each thermal ablation technique in regard to partial nephrectomy or active surveillance, there are some recent comparative studies between techniques.
Cryotherapy to nephrectomy
Panumatrassamee et al.  stated that cryoablation was safer in terms of perioperative outcomes, per-se median operative time, estimated blood loss, transfusion, hospital stay, and complications. Tanagho et al. [14▪] retrospectively reviewed their single-center experience on laparoscopic or percutaneous cryoablation (n = 267) versus robot-assisted partial nephrectomy (RAPN) (n = 233). They concluded that cryoablation was safer to preserve kidney function with a 6% decrease in estimated glomerular filtration rate at the last follow-up in the cryoablation group versus 13% in the RAPN group (P < 0.01). However, cryoablation was associated with an increased risk of recurrence (hazard ratio = 11.4; P = 0.01). Emara et al.  compared their institutional results of 56 laparoscopic cryotherapy cases with 47 RAPN cases. No significant difference was found in procedural time, blood loss, or hospital stay. Two patients in the RAPN group were converted to a laparoscopic radical nephrectomy. Two patients in the cryoablation group had a recurrence that was treated with a recryoablation. Klatte et al. [27▪▪] performed a meta-analysis on perioperative and oncologic outcomes of laparoscopic partial nephrectomy versus laparoscopic cryoablation, combining 13 studies. They found laparoscopic cryoablation to be associated with shorter procedural times, shorter length of stay, lower blood loss, and a lower risk of complications [relative risk (RR) 1.82]. This was countered by an increased risk of local recurrence (RR 9.39) and metastatic progression (RR 4.68) for laparoscopic cryoablation [27▪▪].
Radiofrequency ablation to nephrectomy
Takaki et al.  retrospectively compared populations treated with percutaneous RFA (n = 21) or radical nephrectomy (n = 39) for pT1b tumors (>4 cm), and renal function decrease were of 12.5 and 32.5%, respectively. Olweny et al.  retrospectively reviewed their series of laparoscopic or percutaneous RFA (n = 37) versus partial nephrectomy (n = 37) for histologically proven RCC. Median follow-up was of 6.5 and 6.1 years, respectively. There was no significant difference between the two groups in terms of OS (97.2 versus 100%; P = 0.31), CSS (97.2 versus 100%; P = 0.31), DFS (89.2 versus 89.2%; P = 0.78), local recurrence-free survival (91.7 versus 94.6%; P = 0.96), or metastases-free survival (97.2 versus 91.8%; P = 0.35). However, these cohorts are pretty limited and no difference might reflect an underpowered analysis.
Cryoablation to radiofrequency ablation
A meta-analysis reviewed 31 case series on cryoablation  and RFA [15,28]. Despite inconsistency in clinical and methodological aspects, the authors concluded no significant difference between the two techniques in terms of complications rate and clinical efficacy.
Radiofrequency ablation to radiofrequency ablation
Moddaber et al. [29▪] conducted a meta-analysis across 27 studies comparing thermal versus impedance-based RFA. No difference could be drawn from the current literature neither for perioperative nor for follow-up outcomes.
Three epidemiological studies have been recently published on thermal ablation for RCC. The first one is based on the Surveillance, Epidemiology, and End Results-Medicare database . The authors analyzed 1682 patients diagnosed with small renal masses between 2005 and 2007 including 211 treated with ablative techniques. Although ablative techniques increased during this period, radical nephrectomy remained the predominant approach for this technique in 2007. The benefits of ablation were shorter lengths of stay and a low-cost strategy. Overall mortality was significantly higher but cancer-specific mortality was not. This is probably because of the selected older patients with worst performance status who are generally poor surgical candidates. The second study is based on the nationwide inpatient sample that evaluates the trends in small renal masses management between 1998 and 2008 . Here, the authors also conclude that radical nephrectomy remains the predominant strategy over nephron-sparing modalities in the USA. Finally, the Clinical Research Office of the Endourological Society have recently reported a prospective survey on renal masses management in 98 centers worldwide over a 1-year period (in 2010) . The results confirmed the young age (mean 61.5 years) of patients harboring renal tumors and a large part of nephron-sparing techniques (52%) that seems to increase from previous epidemiological reports. Although the overall percentage of ablation was low with only 3.5% of the cases treated by Cryo or RF ablation. Overall, these reports emphasize a growing interest of urological community for ablative techniques of small renal masses.
UPDATE ON NEW TECHNOLOGIES
New techniques, or variations on existing techniques, are continuously under investigation, attempting to increase thermal energy delivery while minimizing damage to surrounding healthy tissue.
Attempts are being made to increase RFA ablation volume and to avoid ‘heat sink’-related asymmetric ablation borders. Okhunov et al.  evaluated the use of a novel bipolar RFA probe, consisting of a straight inner electrode surrounded by a corkscrew-shaped outer electrode. RFA effect is confined to area between the electrodes, providing a constant heating while protecting adjacent tissues from radiofrequency. RFA was successfully performed on 10 tumors (2–7 cm), during laparoscopic partial or radical nephrectomy. Final pathology confirmed complete ablation in all cases .
Takaki et al.  evaluated a multiple-electrode switching RFA system, enabling the use of up to three RFA electrodes. Sequentially switching power between electrodes creates a confluent ablation zone with a larger volume than conventional RFA systems. Direct success was achieved in 31 cases over 33; the remaining two cases required a second RFA session. Three patients experienced grade 2 complications and no serious adverse event occurred .
Microwave ablation (MWA) utilizes electromagnetic energy to rapidly rotate adjacent water molecules creating high temperatures in the targeted tissue . MWA has theoretical advantages over RFA, namely, larger ablation volumes, shorter ablation time, and higher target temperatures . However, clinical series have so far shown mixed results. An initial series of 10 renal tumors (2–5.5 cm), published by Castle et al. , resulted in a recurrence rate of 38% and intraoperative and postoperative complication rates of 20 and 40%, respectively. Yu et al.  retrospectively evaluated ultrasound-guided MWA of 49 tumors (0.6–7.7 cm). Technical effectiveness at 1 month was achieved in 48 cases (98%). The 1, 2, and 3-year DFS rates were 95.4, 92.3, and 92.3%, respectively. No severe complications occurred. Lin et al.  investigated the effect of MWA on renal function in 16 solitary kidney tumors (1–8.4 cm). Renal function seemed to be preserved and complete ablation, confirmed through contrast enhanced imaging at 1 month, was achieved in 15 cases (93.8%). Guan et al.  conducted a prospective randomized trial among 102 patients, comparing open or laparoscopic partial nephrectomy to open or laparoscopic MWA. Complication rates were significantly lower in the MWA group (12.5%) compared to the partial nephrectomy group (33.3%). The postoperative decline in renal function, determined by estimated glomerular filtration rate, was 5.5% for MWA and 19.4% for partial nephrectomy. At 3 months follow-up, however, a similar decline in renal function was found for both groups. Recurrence-free survival at 3 years for MWA versus partial nephrectomy was 91.3 and 96.0%, for all tumors, and 90.4 and 96.6%, for RCC, respectively. Bartoletti et al.  reported a phase 1 clinical trial where they assessed efficiency of a new MWA device with Amica-probe (Hospital Services SpA, Aprilia, Italy). Fourteen patients were included and received MWA followed by radical nephrectomy in the same procedure. The authors concluded total ablation of the tumor and no complications. These results are certainly limited by the protocol timeline. Indeed, removing the kidney immediately after treating cannot bring interpretable results on MWA-specific complications and on clinical recurrence.
As was mentioned previously, new focal therapies technologies have been neglected in clinical trials lately. High-intensity focal ultrasound (HIFU) is a promising modality, gaining interest for the treatment of prostate cancer. However, despite an original enthusiasm , no new reports have recently appeared in the treatment of renal tumors. Two challenges make it less applicable for small renal masses management. Unlike prostate, renal targeting implies ultrasound going through different media (skin, fat, or muscle). An in-vitro experiment by Ritchie et al.  demonstrated that energy deposition and random beam shifting (1 mm for a 2–3 mm beam size) through subcutaneous and perinephric fat layers crossed by HIFU beam might significantly attenuate ablative energy delivered on the target. Another limitation is the important and complex 3-D kidney movement during HIFU procedure. For this issue, Abhilash and Chauhan [40,41] offer an interesting solution through a computerized model of real-time kidney positions based on movements of skin markers recorded through a stereo camera and coupled with ultrasound (US) device. Histotripsy is another form of focal US ablative technique with different features relying more on mechanical cavitation leading to tissue homogenization than thermal effect. Styn et al.  report a series of histotripsy on rabbit model for RCC. The aim was to explore the controversy of metastatic spread being launched by mechanical energy delivered on targeted tumor. Although there was no statistical difference on their analysis, the number of animals tested is limited and the method to assess metastatic burden is discussable.
Irreversible electroporation (IRE) is a recently developed technology for focal therapy. It is not a thermal ablative technique per se since tissue ablation is based on cell death through membrane nanopores achieved with high-voltage pulse. Two studies [43,44] based on pig experiments reported on the safety of IRE on the hilum of the kidney and the preservation of collecting system structures. Wendler et al.  reported on the accuracy of MRI to follow IRE lesions on short and middle term. In a rodent experiment comparing the effect of incomplete IRE on RCC in immunocompetent versus immunodeficient mice, Neal et al. [45▪] stated that IRE, by preserving proteins from denaturation thanks to nonthermal effect, could trigger a systemic immune response potentially protective for subsequent recurrence. Interestingly, a similar experiment using the same immunocompetent rodent strain and RCC cell lines showed at the opposite that incomplete thermal ablation using RFA or cryoablation enhanced a peak proliferation into the ablation area . This fact might be explained by regional hypoxia, theoretically absent with IRE thanks to vasculature sparing.
Despite a lack of high-level evidence appealing for randomized controlled trials comparing the different current strategies for small renal masses management, thermal ablation is a safe procedure for long-term oncologic as well as functional outcomes. However, a patient opting for ablation should be informed of the possible risk of residual disease and /or recurrent disease imposing a second treatment within the first months after the first procedure. Less than 3 cm tumors seem to be the best target. Healthy patient could be included in the frame of clinical studies. Alternatives to RFA and cryoablation remain controversial and need technological improvements. Finally, new technologies such as IRE showed promising perspectives on preclinical trials and might call interest for clinical studies in the near future.
P.W. benefits from funding of the Cure for Cancer foundation. A.I. benefits from the EUSP scholarship, granted by the European Association of Urology.
Conflicts of interest
There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING
Papers of particular interest, published within the period of review, have been highlighted as:
▪ of special interest
▪▪ of outstanding interest
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cryoablation; radiofrequency ablation; renal cell carcinoma; renal mass; thermal ablation
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