Robotic Partial Nephrectomy Versus Laparoscopic Cryoablation for the Small Renal Mass

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1 EUROPEAN UROLOGY 61 (2012) available at journal homepage: Platinum Priority Kidney Cancer Editorial by Jose A. Karam and Christopher G. Wood on pp of this issue Robotic Partial Nephrectomy Versus Laparoscopic Cryoablation for the Small Renal Mass Julien Guillotreau a, Georges-Pascal Haber a, *, Riccardo Autorino a, Ranko Miocinovic a, Shahab Hillyer a, Adrian Hernandez b, Humberto Laydner a, Rachid Yakoubi a, Wahib Isac a, Jean-Alexandre Long a, Robert J. Stein a, Jihad H. Kaouk a a Center for Laparoscopic and Robotic Surgery, Cleveland Clinic, Cleveland, OH, USA; b Health Outcomes and Clinical Epidemiology, Department Quantitative Health Sciences, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, USA Article info Article history: Accepted January 5, 2012 Published online ahead of print on January 14, 2012 Keywords: Kidney cancer Laparoscopic cryoablation Robotic partial nephrectomy Small renal tumor Please visit europeanurology to read and answer questions on-line. The EU-ACME credits will then be attributed automatically. Abstract Background: Open partial nephrectomy (OPN) remains the gold standard for treatment of small renal masses (SRMs). Laparoscopic cryoablation (LCA) has provided encouraging outcomes. Robotic partial nephrectomy (RPN) represents a new promising option but is still under evaluation. Objective: Compare the outcomes of RPN and LCA in the treatment of patients with SRMs. Design, setting, and participants: We retrospectively analyzed the medical charts of patients with SRMs (4 cm) who underwent minimally invasive nephron-sparing surgery (RPN or LCA) in our institution from January 1998 to December Intervention: RPN and LCA. Measurements: Perioperative complications and functional and oncologic outcomes were analyzed. Results and limitations: A total of 446 SRMs were identified in 436 patients (RPN, n = 210; LCA, n = 226). Patients undergoing RPN were younger ( p < ), had a lower American Society of Anesthesiologists score ( p < 0.001), and higher baseline preoperative estimated glomerular filtration rate (egfr) ( p < ). Mean tumor size was smaller in the LCA group (2.2 vs 2.4 cm; p = 0.004). RPN was associated with longer operative time (180 vs 165 min; p = 0.01), increased estimated blood loss (200 vs 75 ml; p < ), longer hospital stay (72 vs 48 h; p < ), and higher morbidity rate (20% vs 12%, p = 0.015). Mean follow-ups for RPN and LCA were 4.8 mo and 44.5 mo, respectively ( p < ). Local recurrence rates for RPN and LCA were 0% and 11%, respectively ( p < ). Mean egfr decrease after RPN and LCA was insignificant at 1 mo, at 6 mo after surgery, and during last follow-up. Limitations include retrospective study design, length of follow-up, and selection bias. Conclusions: Both techniques remain viable treatment options in the management of SRMs. A higher incidence of perioperative complications was found in patients undergoing RPN. However, the technique was not predictive of the occurrence of postoperative complications. Early oncologic outcomes are promising for RPN, which also seems to be associated with better preservation of renal function. Long-term follow-up and well-designed prospective comparative studies are awaited to corroborate these findings. # 2012 European Association of Urology. Published by Elsevier B.V. All rights reserved. * Corresponding author. Glickman Urological and Kidney Institute, Cleveland Clinic, 9500 Euclid Avenue, Cleveland, OH 44195, USA. Tel address: haberg2@ccf.org (G.-P. Haber) /$ see back matter # 2012 European Association of Urology. Published by Elsevier B.V. All rights reserved. doi: /j.eururo

2 900 EUROPEAN UROLOGY 61 (2012) Introduction Most small renal masses (SRMs) are incidentally diagnosed today because of improvement and increased use of abdominal imaging techniques [1]. Open partial nephrectomy (OPN) remains the gold standard for treatment of SRMs because of excellent long-term oncologic outcomes and optimal renal functional outcomes [2 6]. Several minimally invasive nephron-sparing techniques have emerged as viable treatment options offering outcomes comparable to OPN with the potential for reduced morbidity [4,6]. Laparoscopic partial nephrectomy (LPN) has similar results to open surgery [7,8] but continues to be performed only in selected centers. Ablative therapies represent an attractive option in patients with significant comorbidities [9 11]. Cryoablation can be performed either with a percutaneous or a laparoscopic approach. Percutaneous cryoablation (PCA) is less invasive than laparoscopic cryoablation (LCA) and equally effective, but LCA allows treatment of renal masses by displacing overlying structures (bowel) not accessible by percutaneous access, placement of bigger probes, and application of a hemostatic agent. Robotic partial nephrectomy (RPN) is gaining popularity over LPN by facilitating intracorporeal suturing and offering excellent early outcomes [12]. Despite a higher local recurrence rate, LCA is associated with low complication rates and good functional outcomes as compared to PN [13 15]. When focusing on minimally invasive nephronsurgery options, studies comparing RPN and LCA have not been reported so far. The aim of the present study is to compare perioperative, functional, and oncologic outcomes of LCA to RPN for patients with SRMs. 2. Material and methods 2.1. Study population Our prospectively maintained, internal review board approved, minimally invasive nephron-sparing surgery database was queried to identify patients with SRMs (4 cm) who were treated from January 1998 to December 2010 with RPN or LCA at our institution. Series were concurrent and selection for each treatment (LCA or RPN) was not randomized and was left at discretion of the surgeon. RPN was offered to healthy young patients who were elected for nephron-sparing surgery. LCA was proposed (1) to patients with comorbidities, with baseline renal dysfunction, and/or who were at high surgical risk and who were willing to accept an active treatment and (2) to those with renal masses after a previous ipsilateral kidney surgery Operative technique Our operative techniques for RPN [12] and LCA [16] have been previously described. Intraoperative ultrasonography was performed in all patients to guide tumor ablation or excision. Tumor biopsy was performed in all patients prior to LCA Outcome measures The following preoperative parameters were studied: age, body mass index (BMI), gender, American Society of Anesthesiologists (ASA) score, tumor size and location, serum creatinine, and estimated glomerular filtration rate (egfr). Intraoperative data included total operative time, intraoperative estimated blood loss (EBL), number and type of intraoperative complications, and transfusion rate. Postoperative data were duration of hospital stay, complications, and transfusion rate. Complications were defined according to the Clavien classification system [17]. Minor complications were defined as grade 1 and 2, and major complications included grades 3 5. Serum creatinine level was obtained on postoperative day 1, then at 3, 6, and 12 mo after surgery. Estimated GFR was calculated using the abbreviated Modification of Diet in Renal Disease study equation GFR [18]. Chronic kidney disease (CKD) staging was defined according to the US National Kidney Foundation [19]. Renal insufficiency was defined as an egfr <60 ml/min per 1.73 m 2 (CKD stage III or worse). Local recurrence for LCA was defined as an enlarging or persistently enhanced treatment site on follow-up imaging, according to Working Group on Image-guided Tumor Ablation criteria [20,21] Surveillance Follow-up after LCA consisted of magnetic resonance imaging or computed tomography (CT) scan at day 1 and at 3, 6, and 12 mo, and yearly thereafter. A CT-guided percutaneous needle biopsy of the lesion was scheduled at 6 mo postoperatively. Follow-up of patients who underwent RPN with a confirmed malignant lesion consisted of a CT scan done at 6 mo postoperatively and yearly thereafter Statistical analysis For continuous variables, student t test was used for those variables reportedasmean (plus orminus standarddeviation [SD]) and thewilcoxon rank-sum test for the variables reported as median with interquartile ranges (IQRs). For categorical variables, the chi-square test was used. Factors independently related to postoperative complications and to the latest postoperative egfr were established through multivariable models. Variables entered into the model for the postoperative complications were treatment modality, age, gender, BMI, ASA score, preoperative egfr, and EBL. Variables entered into the model for the latest egfr were treatment modality, age, gender, BMI, ASA score, preoperative egfr, EBL, and occurrence of postoperative complication. Differences were considered to be statistically significant if p < Results 3.1. Demographic and tumor characteristics A total of 446 SRMs were identified in 436 patients and were included in the analysis (Table 1). Patients undergoing RPN (n = 210) were significantly younger (mean age: 57.8 vs 67.4 yr; p < ), had a lower ASA (percentage of ASA >2: 51% vs 80%; p < 0.001), a lower baseline preoperative serum creatinine (mean: 0.94 vs 1.34 mg/dl; p < ), and a higher egfr (mean: 86.3 vs 65.8; p < ) compared to those undergoing LCA (n = 226). Mean tumor size was smaller in the LCA group (2.2 vs 2.4 cm; p = 0.004) Perioperative data Perioperative data are presented in Table 2. Median warm ischemia time during RPN was 17 min (IQR: 13 22). RPN

3 EUROPEAN UROLOGY 61 (2012) Table 1 Baseline patient demographics and tumor characteristics Variables RPN * LCA * p value Age, yr, mean (SD) 57.8 (11.8) 67.4 (11.3) < Male patients, no. (%) 123 (58) 167 (71) ASA score, no. (%) (49) 42 (20) < (51) 170 (80) BMI, kg/m 2, mean (SD) 30.1 (6.4) 29.3 (6.2) 0.2 Preoperative serum creatinine, mg/dl, mean (SD) 0.94 (0.28) 1.34 (0.71) < Preoperative egfr, ml/min, mean (SD) 86.3 (36.0) 65.8 (28.6) < CKD stage, no. (%) 1 78 (36.8) 43 (18.4) < (50.9) 87 (37.2) 3 24 (11.3) 79 (33.8) 4 2 (1.0) 22 (9.4) 5 0 (0) 3 (1.2) Tumor size, cm, mean (SD) 2.4 (0.8) 2.2 (0.9) Right-side tumor, no. (%) 108 (51) 119 (51) 0.9 Tumor position, no. (%) Upper pole 47 (27) 21 (33) 0.7 Middle pole 69 (39) 26 (41) Lower pole 58 (33) 17 (27) Tumor location, no. (%) Anterior 87 (41) 98 (42) < Posterior 67 (32) 53 (23) Lateral 18 (8) 63 (27) Not available 40 (19) 20 (8) RPN = robotic partial nephrectomy; LCA = laparoscopic cryoablation; SD = standard deviation; ASA = American Society of Anesthesiologists; BMI = body mass index; egfr = estimated glomerular filtration rate; CKD = chronic kidney disease. * Two hundred and ten patients underwent 212 RPN procedures, and 220 patients underwent 234 LCA procedures. was associated with longer operative time (median: 180 vs 165 min; p = 0.01), increased EBL (median: 200 vs 75 ml; p < ), longer hospital stay (median: 72 vs 48 h; p < ), and more intraoperative complications than LCA (proportion: 3% vs 0%; p = 0.005). The intraoperative complication rate was 3.3% (n = 7) in the RPN group. A total of four (1.9%) patients from the RPN group had conversion to LPN or OPN (robotic malfunction: n = 2; severe hypercapnia: n = 1; severe adhesions: n = 1). One patient (0.5%) had a radical nephrectomy due to renal vessel injury, one patient (0.5%) had an injury to the epigastric artery, and one (0.5%) sustained a splenic laceration. No conversions and no intraoperative complications were noted in the LCA group. The overall postoperative complication rate was 15.5% (n = 69). The postoperative complication rate was significantly higher in the RPN group than in the LCA group (respectively, 20% vs 12%; p = 0.015). LCA was associated with lower minor-complication rates (8% vs 17%; p = 0.004). The major-complication rate was 3% (n =14) with no difference between the two groups (3% vs 3%; p =0.94). Table 2 Perioperative outcomes Variables RPN * LCA * p value EBL, ml, median (IQR) 200 ( ) 75 (50 100) < Warm ischemia time, min, median (IQR) 17 (13 22) NA Operative time, min, median (IQR) 180 ( ) 165 ( ) 0.01 Hospital stay, h, median (IQR) 72 (72 96) 48 (24 72) < Conversions, no. (%) 4 (2) 0 (0) Intraoperative complications, no. (%) 7 (3) 0 (0) Postoperative complications, no. (%) 42 (20) 27 (12) Minor, Clavien 1 2, no. (%) 36 (17) 19 (8) Major, Clavien 3 5, no. (%) 6 (3) 8 (3) 0.71 Pathologic diagnosis, no. (%) RCC 156 (74) 181 (77) Benign 56 (26) 12 (5) Inconclusive 0 (0) 41 (18) RPN = robotic partial nephrectomy; LCA = laparoscopic cryoablation; IQR = interquartile range; EBL = estimated blood loss; NA = not applicable; RCC = renal cell carcinoma. * Two hundred and ten patients underwent 212 RPN procedures, and 220 patients underwent 234 LCA procedures.

4 902 EUROPEAN UROLOGY 61 (2012) Table 3 Oncologic outcomes Variables RPN * LCA * p value Follow-up, mo, median (IQR) 4.8 (1 7.9) 44.5 ( ) <0.001 Positive margins, no. (%) 3 (1.9) NA Recurrence, no. (%) 0 25 (11) < Metastasis, no. (%) 1 (0.5) 13 (5.6) RPN = robotic partial nephrectomy; LCA = laparoscopic cryoablation; IQR = interquartile range; NA = not applicable. * Two hundred and ten patients underwent 212 RPN procedures, and 220 patients underwent 234 LCA procedures Oncologic outcomes The LCA group had a longer follow-up in comparison to the RPN group (median: 44.5 vs 4.8 mo; p < ) (Table 3). In the RPN group, 74% and 26% of the lesions were malignant and benign, respectively. There were significantly fewer lesions without a pathologic diagnosis in the RPN group compared to the LCA group (0% vs 18%; p = 0.001). Three (1.9%) patients who underwent RPN for malignant tumor had positive surgical margins (Table 3). The rates of local recurrence for the RPN and LCA groups were 0% and 11%, respectively ( p < ). Recurrence after LCA developed after a median follow-up of 11.5 mo (range: mo). Twenty-five patients in the LCA group had a recurrence on imaging. Thirteen (52%) patients had a biopsy, with confirmed recurrence in nine cases and inconclusive findings in four cases. Recurrences were subsequently managed by surveillance (nine cases), percutaneous radiofrequency (four cases), cryoablation (six cases), LCA (two cases), and radical nephrectomy (four cases). Only one patient (0.6%) who underwent RPN developed metastatic disease; 13 patients (5.6%) from the LCA group ( p < ) developed metastases. Pathologic data and oncologic outcomes are shown in Tables 2 and Renal function outcomes The RPN group presented initially with a lower baseline serum creatinine (mean: 0.94 vs 1.34 mg/dl; p < ) and a higher baseline egfr (mean: 86.3 vs 65.8; p < ) than the LCA group (Table 4). Patients who underwent RPN Table 5 Multivariable logistic regression model to evaluate the association of all predictors and complications (any grade) Variable Multivariable OR (95% CI) p value RPN vs LCA 1.8 ( ) 0.1 Age, per 5-yr increase 1.1 ( ) 0.4 Male vs female 1.1 ( ) 0.8 BMI, per 5 kg/m 2 increase 1.1 ( ) 0.5 ASA >2 vs ASA ( ) 0.2 Preoperative GFR, per 1.0 ( ) 0.7 increase in 10 ml/min per 1.73 m 2 EBL, per increase in 100 ml 1.2 ( ) OR = odds ratio; CI = confidence interval; RPN = robotic partial nephrectomy; LCA = laparoscopic cryoablation; BMI = body mass index; ASA = American Society of Anesthesiologists; GFR = glomerular filtration rate; EBL = estimated blood loss. had a significant percent decrease in egfr on postoperative day 1 in comparison to LCA patients (percent change: 10.1 vs +4.6; p < ). However, percent egfr decrease after RPN and LCA was similar at 1 mo ( 6.5% vs 5.1; p = 0.8) and 6 mo ( 11.2% vs 8.9; p = 0.7) after surgery, or at the time of the latest follow-up ( 6.8% vs 4.6%; p = 0.5). New-onset CKD occurred more frequently in the LCA group than in the RPN group (18.2% vs 12.2%; p = ). End-stage CKD (egfr <15 ml/min) occurred more frequently in the LCA group than in the RPN group (4.7% vs 0%; p = ) Multivariable logistic regression model An increase of 100 ml in EBL was the only significant predictor for the occurrence of postoperative complications in any grade (odds ratio [OR]: 1.2; 95% confidence interval [CI], ; p = 0.005). When looking at factors predicting postoperative renal function, treatment modality (RPN vs LCA; p = ) and preoperative egfr ( p < ) were statistically significant (Tables 5 and 6). 4. Discussion The optimal treatment of SMRs should provide acceptable functional and oncologic outcomes with minimal morbidity [4 6,10]. Open nephron-sparing surgery remains the gold Table 4 Functional outcomes Time point Variables RPN * LCA * p value Day 1 Mean egfr, ml/min (%) 73.8 (22.0) 65.2 (32.0) Mean change in egfr (%) 10.1 (21.3) +4.6 (39.9) < Month 1 Mean egfr, ml/min (%) 77.6 (30.5) 53.7 (29.7) Mean change egfr (%) 6.5 (24.9) 5.1 (47.0) 0.8 Month 6 Mean egfr, ml/min (%) 76.0 (21.2) 60.1 (31.4) 0.4 Mean change egfr (%) 11.2 (14.2) 8.9 (36.7) 0.7 Last follow-up New-onset CKD y, no. (%) 26 (12.2) 38 (16.2) End-stage kidney disease z, no. (%) 0 (0) 11 (4.7) RPN = robotic partial nephrectomy; LCA = laparoscopic cryoablation; egfr = estimated glomerular filtration rate; CKD = chronic kidney disease. * Two hundred and ten patients underwent 212 RPN procedures, and 220 patients underwent 234 LCA procedures. y z egfr <60 ml/min. egfr <15 ml/min.

5 EUROPEAN UROLOGY 61 (2012) Table 6 Multivariable logistic regression model to evaluate the association of all predictors and latest postoperative estimated glomerular filtration rate Variable Estimate (standard error) p value Intercept 84.8 (12.1) < RPN vs LCA 14.8 (3.8) Age, per 5-yr increase 0.5 (0.6) 0.4 Male vs female 1.0 (2.7) 0.7 BMI per 5 kg/m 2 increase 1.1 (1.0) 0.3 ASA >2 vs ASA (2.7) 0.3 Preoperative GFR per increase 3.2 (0.4) < in 10 ml/min per 1.73 m 2 EBL per increase in 100 ml 0.3 (0.9) 0.7 Complications vs 6.2 (3.5) 0.1 no complications Follow-up, per yr 0.5 (0.6) 0.4 RPN = robotic partial nephrectomy; LCA = laparoscopic cryoablation; EBL = estimated blood loss; GFR = glomerular filtration rate. standard for the management of SRMs due to established long-term outcomes [2 6,9,10,21]. In experienced hands, LPN can offer similar results [7,8]. RPN represents a relatively recent application of the da Vinci platform (Intuitive Surgical, Inc., Sunnyvale, CA, USA) in urologic surgery and is being currently evaluated [6,12,22]. Ablative therapies are emerging as an attractive option, particularly in patients with significant comorbidities [4,9,10,23,24]. Active surveillance may also be offered as an acceptable option for management of SRMs, especially in patients with reduced life expectancy and who are presumably unfit for nephron-sparing therapies [4,6,25]. Among different ablative therapies, cryoablation can be performed through a percutaneous or laparoscopic approach. Posterior tumors are most often managed percutaneously and LCA allows treatment of anterior and medial masses by displacing overlying structures. Both approaches provided encouraging results in terms of complication rates and oncologic outcomes [11,13 15,21]. To our knowledge, herein we report the first study comparing perioperative, functional, and oncologic outcomes of LCA versus RPN in the management of SRMs. The incidence of perioperative complications in our study for RPN and LCA was 20% and 12%, respectively. Those rates are comparable to major series of RPN [26,27] and LCA [7,15,16,24]. More important, most of the postoperative complications were minor and classified as Clavien grade 1 or 2. Thus, in our experience, both techniques proved to be safe in the management of SRMs. However, RPN can be associated with significantly increased EBL and a higher overall complication rate compared to LPN series [11,13,14]. Nevertheless, in contrast to previous reports on LPN and OPN [11], our data did not show that RPN was associated with higher risk of major complications compared to LCA. Interestingly, EBL was the only significant predictor for the occurrence of postoperative complications at any grade (OR: 1.2; 95% CI, ; p = 0.005). In terms of oncologic outcomes, local recurrence rates in the LCA literature range from 0% to 17.7%. In the LPN and OPN series, local recurrence rates range from 0% to 4.8% [7,11]. Our data showed a higher rate of local recurrence with LCA in comparison to the RPN group (11% vs 0%, respectively; p < ). Klatte et al. reported similar findings with LCA in comparison to OPN and LPN [11]. In addition, local recurrence occurred after 11.5 mo, similar to other reports [11,13,14,21,28]. RPN seems to confer excellent cancer control based on our low positive surgical-margin rate of 1.9%. The findings are in accordance with those described in open and laparoscopic series [7,8,11,13,14]. However, the relatively short follow-up precludes any definite conclusions regarding the long-term oncologic outcomes of the procedure. One of the main goals of nephron-sparing surgery is to accomplish preservation of renal function [4]. In our study, RPN and LCA were both effective in preserving renal function, which was confirmed by a minimal postoperative decrease in egfr. Compared to the LCA group, no patients from the RPN group required hemodialysis. This may be explained by a shorter follow-up of the RPN cohort in our study. When looking at factors predicting postoperative renal function, treatment modality (RPN vs LCA; p = ) and preoperative egfr ( p < ) were statistically significant. Even though very few previous reports have evaluated functional outcomes in LCA compared to OPN and LPN, our data showed similar outcomes [11,13,14]. Our findings are subject to the limitations of a single institution, retrospective study design. A patient-selection bias may have affected the outcomes in this study population. Moreover, we recognize that objective measures of tumor complexity, such as the RENAL or the PADUA scores, currently represent important tools for meaningful data comparisons in nephron-sparing surgery [29,30]. Nevertheless, we were unable to provide such an assessment given the retrospective nature of this study, which did not allow us to retrieve the required information needed for our entire study population. Finally, a longer follow-up is awaited to confirm the long-term oncologic efficacy of these minimally invasive techniques. 5. Conclusions Both minimally invasive nephron-sparing surgery techniques remain viable options in the management of SRMs. RPN was offered to a younger and healthier patient population. A higher incidence of perioperative complications was found in patients undergoing RPN. However, the technique was not predictive of the occurrence of postoperative complications. Early oncologic outcomes are promising for RPN, which also seems to be associated with a better preservation of renal function. LCA should be reserved for patients with comorbidities who desire an active treatment. Long-term follow-up and well-designed prospective comparative study are awaited to corroborate these findings. Author contributions: Georges-Pascal Haber had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Haber. Acquisition of data: Guillotreau, Hillyer.

6 904 EUROPEAN UROLOGY 61 (2012) Analysis and interpretation of data: Guillotreau, Haber, Kaouk. Drafting of the manuscript: Guillotreau. Critical revision of the manuscript for important intellectual content: Haber, Autorino, Miocinovic. Statistical analysis: Hernandez. Obtaining funding: None. Administrative, technical, or material support: Stein, Laydner, Long, Yakoubi, Hillyer, Isac. Supervision: Haber, Kaouk. Other (specify): None. Financial disclosures: I certify that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: Georges-Pascal Haber has served as a consultant for Intuitive Surgical. Jihad H. 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