92 Central European Journal of Urology ORIGINAL PAPER UROLOGICAL ONCOLOGY Association among the R.E.N.A.L. nephrometry score and clinical outcomes in patients with small renal masses treated with percutaneous contrast enhanced ultrasound radiofrequency ablation Cristian Konstantinidis1,2, Enrique Trilla1,2, Xavier Serres2,3, Carolina Montealegre3, David Lorente1,2, Rafael Castellón3, Juan Morote1,2 1 Department of Urology, Valld'Hebron University Hospital, Barcelona, Spain 2 Universitat Autònoma de Barcelona, Spain 3 Department of Radiology, Valld’Hebron University Hospital, Barcelona, Spain Citation: Konstantinidis C, Trilla E, Serres X, et al. Association among the R.E.N.A.L. nephrometry score and clinical outcomes in patients with small renal masses treated with percutaneous contrast enhanced ultrasound radiofrequency ablation. Cent European J Urol. 2019; 72: 92-99. Article history Introduction An association between the R.E.N.A.L. nephrometry score (RNS) and clinical outcomes Submitted: Dec. 16, 2018 in patients with a small renal mass (SRM) has been proposed. We analyzed clinical outcomes according Accepted: May 28, 2019 to the RNS in patients with a SRM treated with percutaneous contrast enhanced ultrasound (CEUS) Published online: June 4, 2019 radiofrequency ablation (RFA). Material and methods Patients with a SRM, who underwent RFA between January 2005 and March 2015, were retrospectively identified. The association between RNS and clinical outcomes was evaluated using parametric and non-parametric analysis. Results We analyzed 163 SRMs in 149 consecutive patients. The mean age was 71.7 years. Mean follow- up time was 33.3 months ±20.6 (2–102). The mean RNS was 5.6 ±1.52 (4–11). A total of 121 (74.2%) cases were of low complexity and 42 (25.8%) were medium complexity. We identified 11 cases of tumor persistence (6.7%). The mean RNS was 5.58 in the cases with no persistence and 5.73 in the cases with persistence (p = 0.788). We identified 15 (9.2%) cases of recurrence. The mean RNS was 5.57 ±0.1 (4–11) in the cases without recurrence and 5.73 ±0.4 (4–9) in recurrence cases (p = 0.804). Of the 76 biopsy proven RCC cases, 8 (10.5%) cases of recurrence were observed, 5 in the low complexity group and 3 in the medium complexity group (p = 0.690). A total of 9 (5.5%) cases of complications were observed, with 5 (4.3%) in the low complexity group and 4 cases in the medium complexity group (p = 0.23). Corresponding author The mean length of stay was 1.5 days with a significant difference between low and medium complexity Cristian Konstantinidis Universitat Autonoma groups (1.3 vs. 2.1 days, p = 0.02). The mean difference between preoperative eGFR and estimated eGFRat de Barcelona 12 months was -3.08 mL / min ±13.3 (-49.4–34.1) and was significant (p = 0.008).However, this variation Valld'Hebron University did not show significant differences between the low and medium complexity groups (p = 0.936). All- Hospital cause mortality was 11.7%, 14 cases (11.6%) in the low complexity group and 5 (11.9%) in the medium Department of Urology complexity group (p = 1.0). No cases of renal cell carcinoma (RCC) specific mortality were identified. 119 Passeig de la Valld'Hebron Conclusions The RNS was not associated with tumor persistence, recurrence, cancer specific mortality, 08035 Barcelona, Spain complications or renal function 12 months after the first treatment, showing significant difference only cristiank1979@yahoo.com in length of hospital stay between low and medium complexity groups. Key Words: contrast enhanced ultrasound, R.E.N.A.L. nephrometry score ‹› radiofrequency ablation ‹› renal cell carcinoma ‹› small renal masses Cent European J Urol. 2019; 72: 92-99 doi: 10.5173/ceju.2019.1833 93 Central European Journal of Urology INTRODUCTION Spain between January 2005 and March 2015 were prospectively enrolled in this study. Institutional re- The incidence of renal cell carcinoma (RCC) has in- view board ethics approval was obtained. Patients creased significantly in the last 50 years [1]. In Eu- were initially evaluated by a urologist to determine rope in 2008 there were 88 400 new cases and 39 300 and counsel about the best treatment strategy. If ab- kidney cancer-related deaths per year [2]. Nephron lation was decided upon, the patient was referred to sparing approaches (NSA) using minimally invasive an interventional radiologist for feasibility assess- techniques are highly precise procedures specialized ment using CEUS. Patients lacking digital images or for small renal masses (SRM), which are defined other relevant data were excluded. Unless obtained as incidentally detected, contrast-enhancing renal beforehand, a simultaneous renal mass biopsy was tumors ≤4 cm in diameter [3]. While partial nephrec- incorporated into routine practice, particularly tomy (PN) is the new gold standard of care for T1 in later years. The biopsy was obtained during the RCC, there is a group of patients unfit for surgery RFA ablation, thus, the final pathology report was given their short life expectancy, co-morbidities revealed afterwards. We used a 15 cm electrode- or denial. In response to the need for NSA in patients needle Cool-Tip TM RF ablation system under con- unfit for surgery, there has been an increasing inter- scious sedation plus local anesthesia. When a biopsy est in percutaneous ablation techniques such as ra- was performed, an 18 G needle was used. If required, diofrequency ablation (RFA) and cryoablation (CA). a bowel hydrodissection, transhepatic approach or RFA for the treatment of kidney tumors was initially a cold saline solution irrigation through an ureter- described by Zlotta et al. in 1997 [4] and consists of al tube were performed. The technique used in our transferring alternating monopolar radiofrequency center was described in detail by Trilla et al. in 2017 electrical currents through needle electrodes into [12]. Patients were evaluated in the urology clinic the target tissue, which results in ionic agitation, at 3, 6 and 12 months after treatment for the first heating, and eventual desiccation with sub-sequent year, then every 6 months for the following 4 years coagulative necrosis [5]. and yearly follow-ups thereafter, assessing clini- During recent years, our knowledge has expanded cal condition, renal function and imaging including regarding the influence of the tumor's anatomical a computed tomography (CT) scan and/or CEUS. complexity, rather than just the diameter, on clini- cal outcomes in terms of treatment for RCC by NSA Outcomes and definitions [6, 7]. In order to measure and standardize that com- plexity, Kutikov and Uzzo developed the R.E.N.A.L.  Tumor persistence was defined as the presence Nephrometry Score (RNS) in 2009 [8] which assigns of a contrast enhanced nodule or soft tissue in the points for size, location and depth of renal tumors, treated area at the first 3 month control. The treat- classifying complexity into low (4–6), medium (7–9) ment was considered successful with the absence and high (10–12). of these findings. Contrast enhanced ultrasound (CEUS) is a real-time  Oncological outcomes dynamic imaging technique that plays an important  Recurrence, defined as a contrast enhanced role in the management of patients treated with ab- nodule or soft tissue in the treated area after lation for malignant tumors. Characterization of re- a negative first control. nal masses and cyst lesions is a well-established in-  Metastasis dication for CEUS [9]. In patients undergoing renal  Cancer specific mortality (CSM) and all-cause percutaneous tumor ablation, CEUS may be used mortality (ACM). as a pre-treatment evaluation to improve lesion vi-  Complications, according to the Clavien–Dindo sualization in difficult cases, to guide the placement system and length of hospital stay. of ablation devices and to detect residual tumors, ei-  Functional results, using serum creatinine lev- ther immediately or later after ablation [10, 11]. els to calculate estimated glomerular filtration In the present study we analyzed the association rate (eGFR) according to the Modification of Diet between the RNS and clinical outcomes in patients in Renal Disease formula. Levels at pre-treatment with SRM treated with percutaneous RFA guided and at the 12 month follow-up were compared. by CEUS. Statistical analysis MATERIAL AND METHODS Clinicopathological data and outcomes were ana- Patients who underwent percutaneous CEUS guid- lyzed using descriptive statistics. Outcomes and ed RFA performed in a single hospital in Barcelona, R.E.N.A.L. nephrometry scores were compared us- 94 Central European Journal of Urology ing Fisher's test for categorical variables and Mann and 7.8 ±0.9 (7–11) in the medium complexity group Whitney's and Wilcoxon's test for quantitative vari- (p ≤0.001). Given that only one case was highly com- ables. Kaplan–Meier analyses was performed for plex as determined by the RNS, this single case was overall, cancer-specific and local recurrence-free included from the average complexity group. Thus, survival. Statistical significance was set at p ≤0.05. 121 cases were of low complexity and 42 of medium SPSS software version 20.0 was used. complexity. RESULTS Tumor persistence A total of 182 procedures were performed in a sam- We identified 11 cases of tumor persistence (6.7%). ple of 166 consecutive patients. We excluded 19 cases The mean size of the tumors in the non-persistent as we did not have the images necessary to calculate cases was 2.6 cm whereas in those with persistence the RNS, which could be obtained in the 163 cases it was 3.3 cm (p = 0.01). The mean RNS was 5.58 in (89.5%) in the 149 (89.8%) patients who were includ- the cases with no persistence and of 5.73 in the cases ed in the analysis. Cohort characteristics are sum- with persistence (p = 0.788). Of the 121 cases of low marized in Table 1. The mean age was 71.7 years complexity, 8 (6.6%) had tumor persistence, whereas and 69.1% were men. Mean follow-up time was 33.3 of the 42 cases of medium complexity, 3 (7.1%) had months ±20.6 (2–102). The mean RNS was 5.6 ±1.52 tumor persistence (p = 0.57) (Table 2). The 11 cases (4–11), 4.8 ±0.8 (4–6) in the low complexity group of persistence were submitted to a second treatment, Table 1. General characteristics of the whole cohort according to RNS Characteristc Whole cohort Low RNS Medium RNS p-value Patients1 149 (100) 108 (72.5) 41 (27.5) 71.4 ±11.3 72.5 ±9.0 Age (years)2 71.7 ±10.7 (36–92) 0.742 (36–92) (50–86) Male1 103 (69.1) 74 (68.5) 29 (70.7) 0.480 Female 1 46 (30.9) 34 (31.5) 12 (29.3) 66.1 ±0.9 65.5 ±24.5 70.1 ±27 Basal eGFR2 0.337 (3.7–159.8) (16–160) (15–114) 81 Right Kidney1 65 (53.7) 16 (38.1) (49.7) 0.167 81 Left Kidney1 55(45.5) 26 (61.9) (49.7) Renal graft1 1 (0.6) 1 (0.8) 0 121 42 Procedures 1 163 (100) (74.2) (25.8) 33.3 ±20.6 33.3 ±19.5 33.4 ±23.7 Follow–up (months)2 0.678 (2–102) (2–100) (2–102) Biopsy during procedure1 129 (79.1) 95 (73.6) 34 (26.4) 34 (26.4) Tumor characteristics 2.7 ±0.8 2.6 ±0.8 2.9 ±0.9 – Major diameter (cm)2 0.015 (1.2–4.9) (1.2–4.9) (1.5–4.9) – Benign1 46 (35.7) 36 (37.9) 10 (29.4) 0.208 – RCC 1 76 (58.9) 53 (55.8) 23 (69.7) 0.158 – Papillary1 20 (26,3) 16 (28,5) 4 (17,4) – Clear cell1 39 (51,3) 26 (49,1) 13 (56,5) – Chromophobe1 11 (14.5) 6 (11.3) 5 (21.7) 0.256 – Mucinous tubular 1 1 (1.3) 0 1 (4.3) – Indeterminate1 5 (6.6) 5 (9.4) 0 – Non–diagnostic biopsy 1 7 (5.4) 6 (6.3) 1 (2.8) 1 : n (%); 2: mean ±SD (min-max). RNS – RENAL nephroemtry score; eGFR – estimated glomerular filtration rate; RCC – Renal cell carcinoma 95 Central European Journal of Urology Table 2. Main outcomes of the whole cohort according to RNS Characteristc Whole cohort Low RNS Medium RNS p-value Complications 1 9 /163 (5.5) 5/121 (4.1) 4/42 (9.5) 0.230 1.5 ±1.9 1.3 ±0.6 2.1 ±3.5 Hospital stay (days)2 0.020 (1–23) (1–5) (1–23) 66.6 ±25.2 64.3 ±2.6 72.1 ±4.4 Basal eGFR2 0.298 (15.0–159.8) (15.8–159.8) (15.0–114.3) 63.4 ±25.9 61.2 ±2.6 69.2 ±4.6 12 months eGFR2 0.105 (8.6–138.8) (8.6–138.8) (8.6–119.8) -3.08 ±13.3 -3.1 ±1.3 -2.9 ±2.6 eGFR variation2 0.936 (-49.4–34.1) (-47.8–29.1) (-49.4–34.1) Persistence1 11/163 (6.7) 8/121 (6.6) 3/42 (7.1) 0.570 Recurrence1 15/163 (9.2) 10/121 (8.3) 5/42 (11.9) 0.530 Recurrence* 1 8/76 (10.5) 5 /53 (9.4) 3/23 (13) 0.690 ACM 11.7 % 11.6 % 11.9 % 1.000 1 n/total (%); mean ±DS (min-max); n (%); *only RCC biopsy proven 2 2 RNS – RENAL nephrometry score; eGFR – estimated glomerular filtration rate; ACM – all cause mortality 9 of them through a second RFA and 2 cases with re-treated with RN with final pathology diagnosis PN. 3 cases presented a relapse after re-treatment. of RCC-clear cell, one re-treated with RFA and 2 of them were treated with a new RFA while in one 2 not re-treated). No significant difference was ob- case a radical nephrectomy (RN) was performed. served in recurrence rates between these 3 groups (p = 0.344). Overall, 11 cases of recurrence were Tumor recurrence subjected to a second treatment, 10 RFA and 1 RN. In the remaining 4 cases, active surveillance was We identified 15 (9.2%) cases of tumor recurrence, chosen considering the patients’ general condition 8 biopsy proven RCCs (7 re-treated, with RFA), 3 ini- and life expectancy. The mean size of the tumors tially reported as benign (2 Oncocytomas, both re-re- in cases without recurrence was 2.6 cm ±0.1 (1.2–4.9) treated with RFA and one initially reported with no whereas in those with relapse it was 3.2 cm ±0.2 evidence, not re-treated) and 4 indeterminate (one (1.9–4.7) (p = 0.02). The mean RNS was 5.57 ±0.1 Figure 1. Recurrence-free survival (Kaplan-Meier) according to R.E.N.A.L nephrometry score. 96 Central European Journal of Urology Complications and length of stay A total of 9 (5.5%) cases of complications were ob- served, 5 cases of 121 (4.3%) in the low complexity group and 4 of 42 (9.5%) cases in the medium com- plexity group (Table 2) (p = 0.23). In the uncompli- cated group, the mean RNS was 5.5 ±0.12 (4–11), while in the group with complications the mean RNS was 6.33 ±0.5 (5–9) (p = 0.097). In the uncomplicat- ed group the mean tumor diameter was 2.7 cm ±0.1 (1.2–4.9) whereas in the group with complications the mean tumor diameter was 3.3 cm ±0.5 (1.6–4.9) (p = 0.071). 5 complications were Clavien 1, 3 were Clavien 2 and 1 case was Clavien 3a (Table 3). The mean length of stay was 1.5 days for the whole group, with a significant difference between low and medi- um complexity groups (1.3 vs. 2.1 days, p = 0.02). Renal function Figure 2. Overal survival according RNS. There were 8 patients who were on hemodialysis pri- or to ablation, so they were excluded from the analy- (4–11) in the cases without recurrence and 5.73 sis of renal function. During follow-up 7 patients un- ±0.4 (4–9) in cases with recurrence (p = 0.804). derwent renal replacement therapy (RRT), 6 of them Of the 121 cases of low complexity, 10 (8.3%) had tu- in a hemodialysis program while 1 patient received mor recurrence, whereas, of the 42 cases of medium a renal transplant. Only 1 patient required RRT complexity, 5 (11.9%) had recurrence (p = 0.53). during the first year of follow-up. The mean preop- Of the 76 biopsy proven RCC cases, 8 (10.5%) cases erative eGFR was 66.6 ±25.2 (15.0–159.8), in the of recurrence were observed, 5 in the low complex- low complexity group it was 64.3 ±2.6 (15.8–159.8) ity group and 3 in the medium complexity group and in the medium complexity group, 72.1 +4.4 (p = 0.690). No significant differences of recurrence (15.0–114.3) (p = 0.298), while eGFR at 12 months were observed among RCC subtypes (p = 0.927). post-ablation was 63.4 mL/min +25.9 (8.6–138.8), Overall recurrence-free survival (RFS) and biopsy in the low complexity group, 61.2 mL/min +2.6 proven RCC group RFS according to RNS are pre- (8.6–138.8) and in the medium complexity group, sented in Figure 1. 69.2 +4.6 (8.6–119.8) (p = 0.105). The mean dif- ference between preoperative eGFR and estimat- Metastasis ed eGFR at 12 months was -3.08 mL/min +13.3 (-49.4–34.1) which was significant, (p = 0.008) how- One case (1.3% of biopsy-proven RCC group) of nodal ever, this variation did not show significant differ- metastasis was identified at 12 months after the ini- ences between the low and medium complexity tial treatment in a patient with tumor persistence groups (p = 0.936) (Table 2). that had been re-treated by PN. The initial tumor was 2 cm with a RNS of 4. Biopsy of the tumor showed a clear cell RCC Fuhrman grade 2. Table 3. Description of complications according to the RNS and Clavien-Dindo System Mortality Clavien- Medium Low RNS Total -Dindo RNS In total there were 19 deaths (11.7%), 14 (11.6%) in Subcapsular Haematoma 1 3 2 5 the low complexity group and 5 (11.9%) in the medi- um complexity group (p = 1.0). No significant differ- Subcapsular Haematoma 2 0 2 2 ence was observed in mortality regarding the initial Abdominal collection 2 1 0 1 pathology report (7 RCC, 6 benign and 6 without bi- Skin burns 3a 1 0 1 opsy, p = 0.353). No cases of RCC-specific mortality Total 5 4 9 were identified. Overall survival according to RNS is presented in Figure 2. RNS – R.E.N.A.L. nephrometry score 97 Central European Journal of Urology DISCUSSION ly with CT guided percutaneous RFA reporting that maximum tumor diameter was the strongest predic- Since the first publication of the RNS, there have tor of local recurrence with a Harrell C index = 0.81 been many articles showing a significant association while RNS was found to be significantly predictive with several clinical outcomes [13] such as surgi- but showing poor performance with a Harrell C in- cal approach [14], surgical complications [15], renal dex = 0.68, limiting its overall utility in the authors’ functional outcome [16], ischemia time [17], histol- opinion [29]. Neither pathology report nor subtype ogy [18] and hospital stay, [19] however there is still of RCC were associated with recurrence nor mortal- little evidence regarding percutaneous ablative tech- ity, which is consistent with previous research, find- niques with contradictory results [20–23]. ing that 64–84% of SRM are indolent tumors. Con- We observed a 6.7% tumor persistence rate, which trarily, a significant proportion of patients with SRM is slightly higher than the 5.9% reported in the sys- who progress to metastatic cancer are not identified tematic review performed by Vollherbst et al. [24] by current pathological techniques. New technol- but lower than the 13% reported by Ptsuka et al. ogy in imaging and molecular analysis are currently [25]. We observed that tumor median size was sig- in development to address this issue [30]. nificantly higher in patients with persistence. Us- We had only one case of metastatic progression, how- ing a CT guide, Ianuccilli et al. studied 203 biopsy- ever, it was in a patient who had a small (2 cm), low proven, percutaneous RFA findings that tumor size RNS and low Fuhrman's grade tumor, which is con- ≥3.5 cm confers a significantly increased risk for cerning considering our current understanding that residual tumors [26]; whereas Wah et al. found, SRMs rarely provoke metastatic disease when sized in a multivariate, logistic regression analysis of 200 <3 cm [25]. Minardi et al. studied 48 patients with percutaneous RFA, that two independent predictors a pT1a RCC treated with PN finding that distant of successful RFA in a single setting were tumor size metastatic disease occurred in 2.4% of patients with (<3 cm) and exophytic location [27]. The RNS was tumors <3 cm versus 8.4% of patients with tumors higher in patients with tumor persistence but this between 3.1 cm and 4 cm, which is concordant with difference was not significant. Concordantly, the lo- our results [31]. cal failure ratio reported by Bhindi et al. using CA We observed an ACM of 11.7% without statistical dif- (defined as failure of the ablation ice ball to extend ference between low and medium RNS groups. beyond the tumor margin on monitoring CT imaging Our complication rate of 5.5% is within the range during the procedure) was also not associated to the of the 5.1–37% reported by the Vollherbst et al. Sys- RNS [23]. tematic review [24]. RNS and tumor diameter were We found a recurrence rate of 9.2% (10.5% in biopsy larger in the cases with complications, however proven cases) which is on the higher end of the in- no significant difference was found. Length of hos- terval observed in literature according to the Voll- pital stay was the only issue significantly associated herbst et al. systematic review [24]. Tumor size was with RNS. Tumor diameter or size has been con- significantly higher in patients with recurrence. The sidered a significant factor influencing the proce- RNS was higher in patients with recurrence but this dure's safety. In the Camacho et al. study, a diameter difference was not significant. These findings are >2 cm and a RNS >8 were significantly correlat- not concordant with the results of Camacho et al. ed with the presence of complications while in the who studied 101 biopsy proven SRMs treated with Schmit et al. study, the RNS was found to be signifi- CA (54%) or RFA (46%) and reported a significant cantly higher (8.1 vs. 6.8, p = 0.001) comparing pa- correlation between recurrence and a RNS >8 [28]. tients with and without major complications. Again, In another study performed by Schmit et al., 751 the lack of a high complexity group in our study renal tumors were treated using a percutaneous ap- could explain these differences. proach with CA (57%) or RFA (43%) and retrospec- We observed a slight but significant decrease of tively categorized regarding the RNS, finding that eGFR one year after the first RFA which reflects mean RNS was 7.6 versus 6.9 in patients with or with- the fragility of this population. No significant differ- out treatment failure respectively (p = 0.001). These ence was observed between RNS groups. Lucas et al. differences may be explained by the lack of a high studied renal function in patients with RCC, finding complexity group in our study whereas the Camacho that patients treated with RN were 34.3 times more et al. study had 61 low, 26 medium and 14 high pa- likely to develop stage 3 chronic renal disease than tients regarding the RNS and the Schmit et al. study patients treated with PN or percutaneous RFA [32]. had 351, 330 and 70 low, medium and high complex- In our study, one patient was successfully treated by ity cases respectively. On the other hand, Maxwell renal graft. Cool et al. studied outcomes and graft et al. studied 217 biopsy-proven SRMs treated main- viability after percutaneous RFA of 12 biopsy-proven 98 Central European Journal of Urology RCC developing within renal transplant allografts. we performed a retrospective analysis reflecting the The authors reported 100% technical success and no experiences within the first ten years of a single hos- recurrence nor progression after a mean follow-up pital. Only in 79% of our treatments was a biopsy of 54 months with no significant difference in eGFR sample obtained as this was not part of our protocol previous to and 6 months after the procedure [33]. in the beginning. Also, we had a lack of a high com- According to the European Federation of Societies plexity group according to the RNS which could have for Ultrasound in Medicine and Biology (EFSUMB) influenced our results; having a very homogeneous guidelines, the use of CEUS can be useful in the man- sample of patients could have prevented us from agement of RCC patients undergoing ablation proce- finding more significant outcomes. dures due to the improved visualization of ambigu- ous tumors, the assessment of therapeutic efficacy CONCLUSIONS within 24 h after ablation, the detection of unablated tumors and local tumor progression, and the ability In conclusion, percutaneous CEUS-RFA is a fea- to guide re-ablation of recurrent viable tissue [10]. sible technique with excellent functional and onco- In our study, all cases had a first evaluation by the logical outcomes and low rate of complications. The same radiologist who performed the procedure, as- RNS was not associated with tumor persistence, sessing the reliability of the treatment. During the recurrence, cancer specific mortality, complications procedure, CEUS was used to guide the needle and or renal function showing significant difference only to evaluate the ablation's success in difficult cases. in length of hospital stay between low and medium In our follow-up protocol CT scan and CEUS were complexity groups. used, however, we did not evaluate the concordance between CT and CEUS to detect recurrence. Conflicts of interest Our study has several limitations. First of all, The authors declare no conflicts of interest. References 1. Jemal A, Siegel R, Ward E, et al. Cancer ablation of renal cell carcinoma: part 1, 13. Konstantinidis C, Trilla E, Lorente D, statistics, 2008. CA Cancer J Clin. 2008; Indications, results, and role in patient Morote J. 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