Current State of Urological Cryosurgery: Prostate and Kidney

REVIEW ARTICLE Current state of urological cryosurgery: prostate and kidney

BJUIBJU INTERNATIONAL David Levy, Anthony Avallone and J. Stephen Jones Department of Urology, Cleveland Clinic, Cleveland, OH, USA

Accepted for publication 17 December 2009

KEYWORDS prostate, kidney, cryosurgery

INTRODUCTION Prostate cancer continues to be the most prevalent cancer in American men and while the lifetime risk of mortality from the disease is ≈4%, we remain unable to identify which individuals actually harbour this risk. PSA measurements alone lack the sensitivity and speciﬁcity to identify men at risk for the disease, as well as in predicting organ-conﬁned disease, yet it remains the best tool we have to date. Thus, we remain with the dilemma of who to biopsy, and if the biopsy is positive who to treat. To date, no study has shown oncological superiority for any type of curative therapy for localized prostate cancer and various options exist [1], which leads us to the initial focus of this article. What is the current state of cryosurgery for localized prostate cancer? The second focus regards the use of cryosurgery for management of localized RCC.

HISTORICAL PERSPECTIVES multiprobe cryosystems marked an improvement in the delivery of this One of the earliest descriptions of the technology, but procedure-related morbidity application of cryosurgery to the prostate was remained an issue [7]. Limited cryosurgical in 1966 by Soanes et al. [2]. A liquid nitrogen- experience continued, and technical problems based system was used and therapeutic revolved around poor control of the liquid application to the prostate was monitored nitrogen cooling agent, lack of an effective through open incisions or transurethrally urethral warming device [8,9] and inability under direct visualization for both benign and to monitor target tissue temperatures. malignant disease. Limitations in the Subsequently, reports on the role of urethral technology and limited ability to accurately warmers coupled with TRUS guidance place the cryoprobes and monitor the extent represented a signiﬁcant technological of freezing in real time were characteristics of advancement, which enhanced delivery of the ﬁrst-generation cryosurgical technique, this therapy with decreased procedure- which ultimately resulted in abandonment related morbidity [10–12]. Target tissue of the technique due to unacceptable temperature monitoring in the form of complication rates [3,4]. Second-generation thermocouple devices became available in the cryotherapy was introduced in the early same period and provided the means to assess 1990s and used TRUS imaging, which allowed the achievement of lethal target tissue for real-time monitoring of the extent of ice temperatures of −40 °C, which became the formation in the tissues [5,6]. This provided endpoint of the freezing cycle. for more accurate cryoprobe placement and more thorough coverage of the prostate. Third-generation cryosurgical technology Transperineal percutaneously introduced became available in 2000, employing delivery

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of pressurized argon gas and helium gas by the AUA in 1996, at which time the Technical components of the procedure through small direct access transperineal treatment was primarily used for patients (freeze rate, achievement of desired target probes, which functioned to deliver cooling with prostate cancer who had failed radiation temperatures and double-freeze technique) and warming properties of the respective therapy [12,13,15]. With continued can enhance cell kill. As stated earlier, the agents based on the Joule–Thompson effect. experience, application of this treatment target tissue temperature to achieve efficient The Joule–Thompson effect is the means by method expanded to individuals with cell kill is −40 °C. Temperatures at the tips of which different gases undergo temperature treatment naïve prostate cancer and today the cryoprobes often exceed −130 °C and changes upon depressurization in accordance cryoablation is used as one component of the while there is no enhanced cell kill beyond with unique gas coefficient properties. minimally invasive approaches to localized −40 °C, those prostate cancer cells in closest Specifically, argon gas undergoes rapid prostate cancer. proximity to the cryoprobes are primarily cooling to – 185.7 °C upon depressurization impacted upon by the freeze-rupture from 20.68 MPa in the storage tank to 0.103 phenomenon, the events that lead to cellular MPa at the tip of the enclosed cryoprobe. The CRYOBIOLOGY rupture due to intracellular ice expansion. expanded gas is then circulated back to the Cells that may not succumb to freeze rupture cryogenic machine through the larger outer Cryosurgical impact on tissues is based on may also undergo necrosis or apoptotic cell lumen of the cryoprobe and attached supply several physiological events. As tissue death [21]. hose to be vented out of the machine into the temperatures decrease to the −15 °C range, surrounding air. Conversely, helium gas extracellular ice forms and results in an warms to 67 °C upon depressurization to osmotic gradient between the newly OUTCOMES provide for active warming of the target dehydrated hyperosmotic extracellular tissues [13] and the historical procedure- compartment and the relatively hypotonic Primary whole gland cryoablation related morbidity and complication rates were intracellular compartments. Intracellular markedly reduced by these developments water flows into the extracellular While biochemical standards of treatment [11,14], as well as by implementation of compartment creating a hyperosmolar toxic success have been established for patients intracelluar undergoing radiation therapy [22] and environment, which surgical extirpation [23], no such criteria exist disrupts vital for the cryosurgical population. In the ‘Cryosurgical ablation of the prostate was intracellular November 2008, publication of the ‘Best removed from the investigative therapies processes. As Practice Statement on Cryosurgery for the list by the AUA in 1996’ temperatures Treatment of Localized Prostate Cancer’ by the decrease to the − AUA [24], there were no data by which the 20 °C range, panel could make a statement about end pinpoint-thermocouple devices that allowed endothelial cell damage occurs [16], resulting points by which cryosurgical treatment for continuous monitoring of target tissue in tissue ischaemia and hypoxia. As success could be measured. temperatures. Additional modifications were temperatures decrease further towards the − new computer software programs that 40 °C range, intracellular ice formation There have been several published reports on provided the surgeon with intraoperative occurs, leading to ‘freeze rupture’ disruption cryosurgical outcomes that have used varying treatment planning and computer-assisted of remaining intracellular structures. PSA threshold levels as one means of assessing cryoprobe placement. Based upon known Components of this degree of thermal insult treatment success. In 2001, Long et al. [25] isotherm data, this allowed the surgeon to have been correlated with apoptosis in the reported 5-year actuarial outcomes from a more strategically place the cryoprobes thus prostate gland [17]. Studies have indicated retrospective multi-institutional cohort of 975 maximizing impact on the targeted tissue, that the lethal temperature for prostate cell risk-stratified patients who underwent while minimizing impact on surrounding death is actually closer to −20 °C [18,19]. prostate cryoablation. In that report the sensitive structures. Variable prostate cell death has been reported biochemical disease-free survival (bDFS) after exposure to temperatures that one outcomes were based upon PSA levels of Cryosurgical ablation of the prostate was would incur at the freeze-zone margin during <0.5 ng/mL and <1.0 ng/mL. In 2002, Bahn removed from the investigative therapies list cryosurgery [20]. et al. [26] reported 7-year actuarial bDFS (1997

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American Society of Therapeutic Radiology criteria) patients was 86%, 67% and 51%, and Oncology (ASTRO) criteria [27]) using respectively. For individuals with an initial PSA similar definitions of biochemical failure of level after cryoablation of ≥0.6 ng/mL, the 0.5 ng/mL and 1.0 ng/mL . In 2002, Donnelly 24-month biochemical failure rate was 29.5% et al. [28] reported the 5-year bDFS in a cohort regardless of risk stratification. The referenced of 87 patients using two PSA threshold points, end-point in this study, a PSA level after <0.3 ng/mL and <1.0 ng/mL. Also, in 2002 Ellis cryoablation of < 0.6 ng/mL, was not intended [29] reported outcome data on 93 patients to represent a measure of treatment success. who underwent primary cryoablation of the Rather the value represents a favourable initial prostate, 84% of whom achieved a nadir PSA reading, and an evidence-based component level of ≤0.4 ng/mL, which was used as a of treatment outcomes that will be benchmark of treatment outcome. In 2008, incorporated into a developing definition Jones et al. [30] reported an analysis of a risk- of treatment success that will develop from stratified cohort of 1198 patients from the ongoing and future collaborative studies Cryo On-Line Data (COLD) Registry for whom of primary whole gland cryoablation biochemical success was defined in two populations. manners. The authors utilized the 1997 ASTRO definition [27] and the 2006 Phoenix definition Prognostic factors for favourable PSA of bDFS (D’Amico criteria [31]). Based on the outcomes based on the above mentioned Phoenix definition, mean (SD) bDFS rates for identified benchmark of <0.6 ng/mL have low-, intermediate- and high-risk patients in been reported and are related to the relative this series was 91.1 (2.9)%, 78.5 (3.6)% and disease burden in the gland [37]. In an 62.2 (4.9)%, respectively. More recently, Cohen institutional cohort of 122 patients treated by et al. [32] reported primary whole gland cryoablation at the 10-year outcomes Cleveland Clinic, 16.4% (20 of 122) patients ‘In the late 1990s cryosurgery of the data on 204 patients had unfavourable (≥0.6 ng/mL) PSA levels who underwent after cryoablation. The single most prostate was utilized predominantly as primary statistically significant predictor of favourable a salvage procedure for patients with cryoablation of the PSA outcome (<0.6 ng/mL) was the number of recurrent disease after radiation therapy’ prostate using both positive cores (P = 0.010, multivariate). the 1997 ASTRO Additionally, on multivariate analysis, the definition [27] and maximum percentage of any given core the 2006 nadir plus two revision [22], as means involved with disease (P = 0.034) and the ratio of assessing treatment response. In this report, of number of positive cores to prostate gland based on the Phoenix definition, the 10-year volume (mL) (P = 0.023) were predictive for bDFS rates were 80.56%, 74.16% and 45.54% favourable PSA outcomes. No other for, low-, intermediate- and high-risk patients, demographic or clinicopathological factors respectively (D’Amico criteria [31]). Thus, were predictive of achievement of a PSA level several reports have been published on after cryoablation of <0.6 ng/mL. The outcomes after cryosurgical ablation of the conclusion of the study was that relative prostate, yet to date there is no standard disease burden as evidenced by the number of PSA endpoint by which outcomes can be positive cores, maximum percentage of core assessed. Studies have also been reported positive and the ratio of percentage core that support the concept that the lower the positive to prostate gland volume (mL) yield PSA level after cryoablation of the prostate significant prognostic information for the higher the likelihood of a negative biopsy achievement of a favourable (<0.6 ng/mL) and stable PSA levels during follow-up PSA level after primary whole gland prostate [33–35]. cryoablation.

A recent report from the COLD Registry The most robust data on complications come described the correlation of initial PSA levels from the COLD Registry report. Urinary after cryoablation with ongoing bDFS in a retention was reported in 43/1198 patients cohort of 2427 treatment naïve patients who (3.6%). This was managed with further underwent primary whole gland cryoablation catheterization until resolution in 18 of the 43 [36]. The data analysis showed that 80.2% of patients. The remaining 25 (2.1%) underwent the study cohort achieved an initial PSA level TURP to remove sloughed tissue. The rectal after cryoablation of <0.6 ng/mL. Based on the ﬁstula rate was 0.4%, and incontinence was Phoenix deﬁnition, the 60 month bDFS for 4.8% with a pad rate of 2.9%. Of the 354 low-, intermediate- and high-risk (D’Amico patients potent at the time of therapy

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25.2% had returned to intercourse but only respectively; P = 0.02) for individuals with undergoing this type of therapy as well as 8.8% were able to do so without any lower (<10 ng/mL) vs higher (≥10 ng/mL) PSA continued efforts at arriving at an evidence- pharmaceutical or device assistance. levels before salvage cryotherapy. A PSA level based definition of treatment success for of >10 ng/mL (P = 0.002) before cryotherapy this unique subset of the prostate cancer Table 1 [14,25,26,28,30,32,36,38–40] and shorter (≤16 months) PSA-doubling time population. represents 10 contemporary series of (P = 0.06) after cryotherapy were indicators of cryosurgical outcomes with associated means eventual biochemical failure as defined by the Table 2 [12,13,15,36,39,51] represents of measure of outcomes with regard to Phoenix definition. contemporary salvage cryosurgical series with ASTRO/Phoenix criteria, as well as PSA ranges bDFS rates and follow-up periods. used for assessment of the study populations. At the 2009 annual meeting of the AUA a Ongoing studies in the primary whole study detailing 5-year bDFS in 471 patients gland cryoablation population are underway who underwent salvage cryotherapy from the Focal cryoablation in an effort to arrive at an evidenced National COLD Registry was reported [50]. based definition of treatment success Patients were studied in the absence of Subtotal prostate cryoablation is based upon and to better delineate the role of this hormonal influence, for bDFS based upon the premise of accurate identification of therapeutic regimen in the prostate cancer nadir + 2 criteria. The data analysis showed a the extent of disease within the gland. population. 36-month 75.9% bDFS for individuals with The published prostate cancer pathology initial post-salvage cryoablation PSA levels literature shows that a percentage of patients <0.6 ng/mL, and a 12-month biochemical diagnosed with the disease have single focus Salvage cryoablation failure rate of 45% for individuals with initial prostate cancer and many additional patients post-salvage cryolablation PSA levels of have secondary foci that may not be clinically In the late 1990s cryosurgery of the prostate ≥0.6 ng/mL. The conclusion of the study was significant [52–54]. As there are no available was utilized predominantly as a salvage that initial post-salvage cryoablation PSA imaging methods that reliably identify the procedure for patients with recurrent disease level is prognostic of bDFS based on the true extent of disease within the prostate, after radiation therapy [12,13,15]. Patients are Phoenix definition. focal therapy remains reliant on a sufficient typically deemed radiation failures based number of biopsies to guide the surgeon in upon achievement of threshold PSA levels A comparative outcomes study of salvage carrying out the treatment in an efficient after radiation therapy. In the late 1990s, the cryotherapy vs salvage radical prostatectomy manner. Furthermore, most reports of focal ASTRO criteria were the main component of was recently published using two measures of therapy do not specify how much of the gland such an assessment and this definition was biochemical treatment success, a PSA level is ablated, making comparisons difficult. Ward revised in 2006 at the Radiation Therapy thresholdof 0.4 ng/mL and two increases and Jones [55] have recently published a Oncology Group-ASTRO Phoenix Consensus above nadir PSA [44]. The data showed categorization scheme that may eliminate the Conference in the form of the nadir plus two superior 5-years bDFS based upon both limitation in the future. definition [22]. definitions, 21% salvage cryotherapy vs 61% salvage prostatectomy (P = 0.001) for the In 2002, Onik et al. [56] published the first Numerous studies detail outcomes after 0.4 ng/mL definition, and 42% salvage proof of principal report of focal prostate salvage therapy for recurrent prostate cancer cryotherapy vs 66% salvage prostatectomy cryoablation performed on 11 patients, nine from both the radiation and surgical literature (P = 0.002) for the two rises above nadir. The of whom had stable PSA levels during follow- [41–46]. For the cryosurgical publications, conclusion was that based on the chosen up. Subsequently in 2006, Bahn et al. [57] outcomes have been reported using various endpoints, salvage cryotherapy outcomes reported on 31 patients that underwent initial endpoints. In 2001, short-term bDFS of 86% were inferior to salvage prostatectomy and 6–8 core prostate needle biopsy and colour and 74% at 12 and 24 months, respectively, younger individuals may have greater benefit Doppler ultrasonography (US) with additional were reported from a cohort of 38 patients from surgical extirpation, although the biopsies as indicated in an effort to eliminate treated at Columbia [44]. In 2001, Izawa et al. authors did not consider the additional bilateral disease. Focal cryoablation was [47] reported the impact of initial stage of morbidity of salvage prostatectomy. Notably, carried out and the patients were followed disease and the pre-cryotherapy PSA level on the complications in the COLD Registry with serial PSA determinations every biopsy proven salvage cryotherapy failure in a salvage report were markedly less 3 months for 1 year, and every 6 months cohort of 145 patients treated at the MD common than those reported for salvage thereafter. Biopsies were performed at Anderson Cancer Center. Using the Phoenix prostatectomy. The incontinence rate 6 months, 1, 2 and 5 years after treatment definition, Izawa et al. [48] subsequently (requiring pad use) was 4.4% for patients and for cause based on biochemical evidence reported 5-year bDFS rates of 57% and 23% undergoing salvage cryotherapy. The rectal of failure as defined by the ASTRO definition. for patients with pretreatment PSA levels of fistula rate was 1.2% and 3.2% underwent The investigators reported bDFS of 92.8% (26/ ≤10 ng/mL and ≥10 ng/mL, respectively, and TURP to remove sloughed tissue. 28 patients) and a negative biopsy rate of 90% and 69% for individuals with pre- 96% (24/25 patients) at a mean follow-up of radiation clinical T1/T2 and T3/T4 disease, Salvage cryoablation has been used 70 months. In 2007, Ellis et al. [58] reported respectively, who underwent salvage for over a decade and technological 60 patients treated with focal cryoablation. cryotherapy. In 2006, Spiess et al. [49] reported advancements have markedly improved the In this study 80.4% of treated patients a statistically significant difference in PSA- procedure-related morbidity. Prognostic maintained bDFS (ASTRO) at a median (SD) doubling times (12.3 months vs 5.6 months, studies are underway for individuals follow up of 15.2 (7.4) months. However, 35

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TABLE 1 Contemporary cryosurgical series with respective PSA thresholds and bDFS results

Reference, year Cohort, n Agent PSA range, ng/mL Reported bDFS risk, %† Follow-up, months Levy et al. [36], 2009 2427 Argon Phoenix <0.1 Low, 91.8 60 Intermediate, 76 High, 71 <0.5 Low, 86 Intermediate, 67 High, 51 ≥0.6 Low, 70.5 24 Intermediate, 56 High, 47 Cohen et al. [32] 2008 204 Nitrogen/argon Phoenix Low, 81 120 Intermediate, 74 High, 46 Jones et al. [30] 2008 1198 Argon ASTRO Low, 85 60 Intermediate, 73 High, 75 Phoenix Low, 91 Intermediate, 79 High, 62 Prepelica et al. [38] 2005 65 Argon ASTRO High, 82 72 <0.4 High, 50 <1.0 High, 35 Han et al. [39] 2003 122 Argon ≤0.4 Low, 76 12

Donnelly et al. [28] 2002 76 Nitrogen <0.1 Low, 75 60 Intermediate, 89 High, 76 <0.3 Low, 60 Intermediate, 77 High, 48 Bahn et al. [26] 2002 590 Nitrogen/argon ASTRO Low, 92 84 Intermediate, 89 High, 89 <0.1 Low, 87 Intermediate, 79 High, 71 <0.3 Low, 61 Intermediate, 68 High, 61 Long et al. [25] 2001* 975 Nitrogen/argon <0.1 Low, 76 60 Intermediate, 71 High, 61 <0.5 Low, 60 Intermediate, 61 High, 36 De la Taille et al. [14] 2000 35 Argon <0.1 Low, 86 9 70% all patients Koppie et al. [40] 1999 176 Nitrogen <0.5 ng/mL Low, 69 36 High, 45

*Review of multi-institutional series; †bDFS risk based on D’Amico et al. [31] risk stratiﬁcation criteria.

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the disease [61–63]. Over the past 15 years, TABLE 2 Contemporary salvage cryosurgical series with respective PSA thresholds and bDFS results nephron-sparing surgery (NSS) has been proven effective based on long-term disease- Cohort, PSA levelrange, Reported Follow-up, specific survival outcomes that parallel those Reference, year n Agent ng/mL bDFSrate, % months of traditional radical nephrectomy [64–67]. Pisters et al. [12] 1997 150 Nitrogen <0.2 31 17 Based upon these data and the technological Chin et al. [15] 2001 118 Argon 0.5 34 18 advances in minimally invasive surgical Ghafar et al. [13] 2001 43 Argon 0.3 74 20 techniques, cryoablation has recently gained Han et al. [39] 2003 29 Argon 0.4 75 12 interest as an alternative option for the Donnelly et al. [51] 2005 46 Argon <0.3 51 20 treatment of localized RCC. Levy et al. [36] 2009 471 Argon Phoenix ≤ 0.5 75 36 Most renal tumours are discovered incidentally during unrelated imaging procedures. Identified lesions are typically small, and are amenable to minimally invasive NSS approaches including laparoscopic or robotic-assisted partial nephrectomy (PN) or patients underwent prostate biopsy after cryoablation [68,69]. Based upon tumour focal cryotherapy, 14 of whom failed at a Comment location, renal cryoablation can be delivered median of 3.5 months. In all, 40% of these Technological advances have significantly laparoscopically or percutaneously under individuals (14 of 30) had biopsy evidence of reduced procedure-related morbidity for radiographic imaging, which affords disease and 13 of these specimens came from patients undergoing primary or salvage the patient more rapid convalescence the non-treated side of the prostate. In all, prostate cryoablation. While this is a [61,71]. 27.5% (14 of 51) of this study cohort with relatively new therapeutic approach, sufficient follow up had prostate cancer available data indicate similar efficacy to As in prostate cryoablation, renal cryoablation after focal cryoablation. It appears as alternative curative approaches to the involves delivery of pressurized argon gas to though the pretreatment biopsy data were disease. To date, there are no data that achieve lethal tissue temperatures of −40 °C. misleading in this study cohort, and support an evidence-based definition of Early in the renal cryosurgical experience, the underscores the likelihood that patients treatment success for any type of therapeutic goal was extension of the ice ball harbour greater disease burden than biopsy cryoablative technique directed at prostate to ≥0.5 cm beyond the periphery of the often indicates. cancer. Developing such a definition is now targeted renal tumour. This was primarily a major objective. While many studies have based on studies by Chosy et al. [72] which In 2007, Lambert et al. [59] reported a bDFS been published on prostate cryoablation, reported that a temperature of −19.4 °C was rate of 36% (nine of 25 patients) after focal the implementation of various PSA levels required for renal tissue treatment. While the cryoablation. One criterion was an arbitrary as endpoints by which outcomes have been work of Campbell et al. [73] reaffirmed these PSA threshold of 1.0 ng/mL yielding a 36% assessed confounds the true efficacy of data, efforts to minimize the risk of under bDFS. A second criterion of outcome was a this therapy. Adoption of one evidence- treatment resulted in the designation of nadir PSA level of >50% of the total PSA at based PSA level as a means to assess achievement of a threshold temperature of time of diagnosis, which yielded an 84% bDFS outcomes would forward the effort. In the −40 °C with an ice ball extension to 1 cm rate. The lack of a definition of treatment absence of large scale prostate biopsy data outside the margins of the lesion as the success affects the interpretation of these studies after cryoablation that show accepted standard in clinical practice. data. eradication of disease as well as studies that address metastasis-free survival or Proof of principle In 2008, Onik et al. [60] reported 2-year disease-specific survival, the true efficacy follow-up data on 48 patients treated with of this therapy cannot be delineated. For The first application of renal cryosurgery was focal cryoablation between 1995 and 2004. focal cryoablation, the lack of a reliable reported by Uchida et al. [74] in a combined in In this study a proportion of the cohort, means of accurately assessing disease vitro/in vivo study. Two renal units containing those treated after 1 March 2001 underwent burden within the prostate precludes the large hypervascular tumours were treated in transperineal three-dimensional mapping of implementation of focal cryotherapy as a vitro and four patients with metastatic RCC the prostate with 5-mm step biopsies to standard of care. underwent primary tumour cryoablation in a better delineate the true extent of disease in proof-of-principal setting. At the time of the gland. In all, 45 of 48 patients (94%) autopsy extensive parenchymal necrosis and a had stable PSA levels after treatment decrease in tumour size were reported. with a mean PSA level of 2.19 ng/mL after cryoablation. Of these individuals, RENAL CRYOABLATION In 1996, Delworth et al. [75] reported a 24 had routine biopsies at 1 year after feasibility study in which two patients with treatment, all of whom had no evidence of The incidence of RCC continues to rise based solitary kidneys were treated with renal disease on the treated as well as on the widespread use of cross-sectional cryoablation via an open surgical technique at contralateral side. imaging as well as an increased prevalence of the MD Anderson Cancer Center.

The first clinical application of the technique the efficacy and safety of this approach. was reported by the Cleveland Clinic in 1998 During laparoscopic surgery, needle biopsy [76]. Ten patients with 11 renal lesions under direct visualization through existing ranging in size from 1.5 cm to 3 cm were laparoscopic ports can be carried out, thus treated laparoscopically with the aid of minimizing the risk of seeding the biopsy laparoscopic US treatment monitoring. In a tract. Kramer et al. [80] reported that multiple subsequent study from the Cleveland Clinic biopsies of a given renal lesion increased the [77], 23 of 32 patients underwent CT-guided diagnostic yield, and can confirm malignancy. needle biopsy after cryoablation of the previously treated renal lesions at 6 months Renal cryoablation does not require hilar follow-up, all of which were negative for clamping, and the lack of renal ischaemia is a evidence of disease. The authors subsequently potential advantage when compared with PN. reported no local recurrence or port-site Carvalhal et al. [81] reported preservation of metastasis at a short-term follow-up of renal function after cryoablation in a cohort 16 months. of 22 patients, three of whom had a solitary kidney. At a mean follow up of 20.6 months, In 2001, Shingleton and Sewell [78] reported there was no statistically significant the initial series of percutaneous image- difference between the mean serum guided renal cryoablation; 20 patients with creatinine level before (1.13 mg/dL) and after radiographically documented small renal (0.91 mg/dL) cryoablation. Additionally, there tumours of ≤4 cm were treated with three was no difference in creatinine clearance freeze-thaw cycles using MRI guidance. (P < 0.05). Similarly, Bourne et al. [82] reported on a cohort of 123 cryoablation Current approaches to renal lesions patients, 14 of whom had chronic renal insufficiency. No difference was identified A double freeze/thaw cycle with a period of between the mean serum creatinine level active or passive thawing is widely used. A before (2.39 mg/dL) and after (2.24 mg/dL) 10 min freezing time results in achievement cryoablation (P = 0.05). In this study, of maximal negative temperatures and creatinine clearance rates before and after maximal ice ball extension. There have been cryoablation were also similar, at 32.3 mL/ no studies that delineate whether active or min/1.73m2 and 35.2 mL/min/1.73m2, passive thawing provides enhanced tumour respectively (P = 0.034). necrosis.

Renal cryoablation can be performed Follow-up regimens laparoscopically through a transabdominal or retroperitoneal approach or percutaneously The absence of a surgical specimen mandates under radiographic imaging. The serial imaging as one component of long- transabdominal approach can be applied to term surveillance regimens. In the early post- any tumour location but may require cryoablation setting, imaging studies often extensive mobilization of the kidney. This reflect an increase in the size of the treated technique affords a larger working area renal lesion, which may be attributed to compared with the retroperitoneal approach. oedema [83]. Data show that a curvilinear Laparoscopic techniques provide for direct area of hypoattenuation or a thin rim of visualization of tumour margins; however, the peripheral enhancement may be seen during use of intraoperative real-time US may the early postoperative course in 19.7% of enhance delineation of tumour extent, treated lesions [84,85]. A wedge-shaped confirmation of which is mandatory for defect may also be seen, similar in appearance proper cryoprobe selection to afford maximal to renal infarction [83]. A decrease in treated tumour kill based upon known isotherm data lesion size can be expected over time. Imaging and to minimize the affect on normal renal at 1, 3, 6 and 12 months may reflect decreases parenchyma. In cases of intraparenchymal in discernable lesion size of: 61.5%, 78.7%, tumour location, US may be the only means 83.5%, and 94.2%, respectively. By of identification of tumour boundaries. 36 months, 38% may be undetectable by MRI Meticulous comparison with preoperative [86]. imaging studies is imperative [79]. A lack of involution does not necessarily imply The role of needle biopsy of renal lesions has treatment failure. While imaging criteria of a been controversial despite studies reporting lack of vascular enhancement is consistent

with an inactive disease status, biopsies of cardiovascular complications, have been reveal lower local recurrence-free survival such lesions have revealed viable neoplastic reported [90]. rates for cryoablated lesions compared with cells. Thus, any lesion with a ≥ 10 Hounsfield those treated with PN, 90.6% vs 98.4%, units enhancement (CT criteria), increasing The incidence of conversion to open renal respectively. The conclusion of the expert size, or increasing signal intensity on MRI cryosurgery or open radical nephrectomy is panel for the role of ‘thermal ablation warrants further evaluation including biopsy 3.5%. The most common related factors (cryoablation or radiofrequency ablation)’ was to delineate the presence of recurrent are; impaired access/adhesions, bleeding, that thermal ablation is an option for the disease. An enlarging lesion will often be respiratory distress, preponderance of high-risk surgical patient as long as the characteristic of treatment failure at the base perirenal fat, or renal hilar involvement [91]. patient is counselled regarding; the necessity of the original tumour [85]. of long-term surveillance imaging, increased Although severe complications including risk of local recurrence, possible need for re- In 2008, Cleveland Clinic reported the largest haemothorax, colorenal fistula, and acute treatment and or biopsy of the treated lesion, series of follow-up data on a cohort of 176 renal failure, have been reported, the overall lack of well proven radiographic parameters patients with 192 lesions treated with complication rate is low in comparison to for success, potential for difficult surgical laparoscopic renal cryoablation [87]. In all, 60 laparoscopic PN series [92–94]. salvage and the substantial limitations of the of 176 (34%) patients with no evidence of available thermal ablation literature. enhancement on imaging studies underwent Renin mediated hypertension as a result CT-guided biopsy of the treated site at of renal cryoablation has been hypothesized 6 months after cryoablation, all of whom had but to date no data indicate such a negative results. Two of 26 patients with phenomenon. Comment imaging evidence of peripheral enhancement Minimally invasive surgical approaches to had biopsy evidence of persistent disease. In renal tumours are the current standard of 11 patients there was central enhancement, Disease-specific survival care in the USA. One component of this and of these four had biopsy proven type of approach is cryoablation. Currently persistence of disease. Thus, imaging and Long-term follow-up data reflect cancer- there are insufficient long-term DFS and pathological findings seem to correlate specific survival rates at 5- and 10-year disease-specific survival data to adequately. However, given the slow growth intervals of 93% and 81%, respectively [95]. substantiate this type of approach as an rate of small renal masses, and the lack of Most published reports are single-institution equivalent option to PN in the patient long-term data, continued surveillance and a studies with limited numbers of patients. with a normal contralateral renal unit and low-threshold for biopsy would seem Meta-analyses have been performed to no associated comorbid disease, although reasonable as some recurrences may develop further elucidate the findings. Kunkle and ongoing patient experience may change late. Uzzo [96] reported on 47 series consisting of that limitation. Renal cryoablation is 1375 renal lesions treated with cryoablation suitable for individuals with compromised Should biopsy or imaging reveal persistent or or radiofrequency ablation. The mean patient Eastern Cooperative Oncology Group recurrent tumour, several options are age and tumour size of the study population status, impaired renal function or who available. Repeat cryoablation has been used was 67.2 years and 2.64 cm, respectively. For would otherwise be considered as poor [42]. For lesions not amenable to repeat the subset of 600 lesions treated with surgical candidates for more invasive cryosurgery, salvage surgical therapy may be cryoablation, the mean patient age and therapy. necessary. Although salvage NSS may be tumour size were 76.2 years and 2.64 cm, considered, post-cryoablation perinephric respectively. Within this subset of cryoablated fibrosis or adhesions between recurrent lesions, 62.6% of patients underwent a biopsy tumour and adjacent structures can make before cryosurgery. Patients were treated CONFLICT OF INTEREST either open or laparoscopic PN treacherous laparoscopically (64.8%), percutaneously [88]. (23.2%), or via open cryoablation technique None declared. (12%). Overall, local tumour progression developed in 31 of 600 patients after Procedure-related morbidity cryoablation (5.2%) with six of 600 (1%) REFERENCES progressing to metastatic disease. Laparoscopic renal cryoablation is typically 1 Thompson I, Thrasher JB, Aus G et al. associated with less blood loss and a shorter Guideline for the management of hospitalization when compared with Best practice guidelines clinically localized prostate cancer: 2007 laparoscopic PN [87,89]. With renal update. 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