UROLOGICAL ONCOLOGY Comparison of Non-Hilar Clamping Simple Enucleation and Enucleo-Re- section of Exophytic Renal Tumors Mehmet Balasar,1* Emrullah Durmuş,2 Mehmet Mesut Pişkin,1 Giray Karalezli,1 Recai Gürbüz,1 Mehmet Kilinç1 Purpose: To retrospectively evaluate our institutional experience with non-hilar-clamping simple enucleation (SE) and enucleoresection (ER) for the treatment of exophytic renal tumors regarding their oncological outcomes. Materials and Methods: We retrospectively evaluated patients treated between 2006 and 2013 for clinical exo- phytic T1-T2a renal tumors using open nephron-sparing surgery. Results: A total of 33 patients underwent SE and 39 underwent ER. The mean tumor size was 38.7 mm. None of the patients had positive surgical margins. No local recurrences were observed during the postoperative follow-up period (mean 40.7 ± 23.4 months); however, ipsilateral adrenal and contralateral kidney metastasis was detected in one of the patients. There was no statistically significant difference in the R.E.N.A.L Nephrometry Score, op- erative time, or intraoperative blood loss in the non-hilar-clamping SE and ER groups (P > .05). During the third postoperative month, the estimated glomerular filtration rate (eGFR) levels in the SE group were significantly reduced compared with the preoperative eGFR levels (P = .046). Conclusion: SE and ER with non-hilar clamping are safe, acceptable approaches for treating exophytic renal tumors. Keywords: carcinoma, renal cell; surgery; follow-up studies; kidney neoplasms; mortality; nephrectomy; adverse effects; organ sparing treatments; methods; glomerular filtration rate. INTRODUCTION During recent decades, modern imaging techniques have facilitated the use of nephron-sparing surgery (NSS) to protect intact tissue when treating small renal tumors, with oncological outcomes similar to those ac- complished with radical nephrectomy.(1,2) The current gold standard for addressing renal tumors is NSS that includes enucleoresection (ER). With this procedure, the tumor is removed, along with an adequate safety margin of healthy parenchyma.(3) As reported in various studies, a minimal tumor-free surgical margin is con- sidered sufficient to avoid the risk of local recurrence and allow the possible use of simple enucleation (SE), a nephron-sparing procedure with oncological effective- ness.(4) The aims of NSS are total resection of the tumor with as little intraoperative hemorrhage as possible and leav- ing as much intact functional parenchyma as possible. Minimal hemorrhage is achieved by clamping the hi- lar vessels in either a warm or cold ischemia condition. The maximum warm ischemia time during NSS without leading to permanent damage in the kidney is reported to be 30 minutes.(5) However, recent studies have de- creased this time to 20 minutes. Various studies have claimed that every minute during ischemia, even if it is less than 20 minutes, damages kidney function.(6) The aim of the present study was to analyze the pa- tients’ preoperative, intraoperative, and postoperative conditions; positive surgical margins; and the patholog- ical outcome data of 72 patients who underwent non-hi- lar clamping SE or ER. MATERIALS AND METHODS A total of 72 patients who underwent SE and ER from 2006 to 2013 due to exophytic T1-T2a renal tumors were included in this retrospective study. Two surgical teams performed the operations. One team exclusive- ly performed SE, and the other team exclusively per- formed ER. The preoperative evaluation of all patients included ultrasonography of the kidney, ureter, and bladder, abdominal computed tomography with contrast enhancement, and chest radiography. To determine the location of the tumor in the kidney, we calculated the R.E.N.A.L Nephrometry Score (radius, exophytic or endophytic nearness to the collecting system or sinus, and anterior or posterior location relative to polar lines). 1 Department of Urology, Necmettin Erbakan University, Meram Medical School, Konya, Turkey. 2 Department of Urology, Bulanık State Hospital, Muş, Turkey. *Correspondence: Department of Urology, Necmettin Erbakan University, Meram Medical School, Konya 42080, Turkey. Tel: +90 532 5174613. Fax: +90 332 2236522. E-mail: drbalasar@gmail.com. Received February 2015 & Accepted November 2015 Vol 12 No 06 November-December 2015 2410 Urological Oncology 2411 (7) The E-score of the R.E.N.A.L nephrometry was 1 point for all patients recruited to the study. All patients were considered to be free from distant metastases prior to surgery. Technique The participants provided written consent before the surgical intervention. An anterior subcostal approach was used in all patients. A direct approach to the kidney was preferred before the kidney was totally separated from the perirenal fat to extricate the exophytic renal tumor that had been detected earlier by imaging. For safety reasons, the renal pedicle was carefully iso- lated and then suspended with umbilical tape but not clamped. In the patients who underwent SE, the renal capsule at the edges of the mass was denoted using electrocautery. The natural cleavage was opened using clamps. The natural cleavage plane between the tumor and normal parenchyma enabled a 360° turn with the index finger. The mass was totally excised without tu- mor bed ablation. For hemostasis, the renal parenchyma around the enucleation site was compressed using the thumb and index finger. The renal parenchymal defect was closed with hemostatic material and parenchymal horizontal mattress sutures. In the ER group, using Gyrus open forceps (Gyrus Medical PK System Seal; Gyrus International, Berk- shire, UK), the mass was resected along with 1 to 5 mm of intact parenchyma around the tumor (Figures Table 1. Patient and event characteristics. Variables Group SE (Simple Enucleation) Group ER (Enucleo-Resection) P Value Patients, no 33 39 Age, years, mean ±SD 55.5 ± 11.0 54.6 ± 12.9 .76 Gender, no (%) .85 Male 21 (63.6) 24 (61.5) Female 12 (36.4) 15 (38.5) Tumor side, no (%) .83 Right 17 (51.5) 18 (46.1) Left 16 (48.5) 21 (53.9) Tumor localization, no (%) .67 Upper pole 8 (24.2) 13 (33.3) Mid-kidney 4 (12.1) 5 (12.8) Lower pole 21 (63.7) 21 (53.9) Tumor size, mm, mean ±SD 36.8 ± 13.3 40.4 ± 15.2 .17 R.E.N.A.L nephrometry score, mean ± SD 4.55 ± 0.87 4.64 ± 0.78 .39 PT stage, no (%) pT1a 21 (63.6) 23 (58.9) pT1b 11 (33.4) 15 (38.5) pT2a 1 (3) 1 (2.6) RCC grade, no (%) G1 2 (6.9) 1 (2.5) G2 16 (55.1) 18 (46.1) G3 10 (34.5) 18 (46.1) G4 1 (3.5) 2 (5.2) Operative time (min), mean ± SD 100.0 ± 13.2 106.7 ± 14.1 .61 Estimated blood loss (mL), mean ± SD 286.7 ± 143.1 313.8 ± 169.7 .47 Hb drop (g/dL), mean ± SD 1.55 ± 1.20 1.07 ± 1.58 1.19 Follow-up (months), mean ± SD 40.5 ± 21.5 41.5 ± 24.3 .6 Local recurrences / metastasis 0/0 0/1 Abbreviations: SD, standard deviation; RCC, Renal Cell Carcinoma; Hb, Hemoglobin Renal Tumor and Nephron Sparing Surgery-Balasar et al. 1-3). The renal parenchymal defect was closed with he- mostatic material and parenchymal horizontal mattress sutures. We observed no parenchymal hemorrhage that necessitated digital compression of the parenchyma due to the thermal effect of the Gyrus open forceps. In both groups, the operation was conducted without clamping the renal artery. The operation time, intraoperative blood loss, preoper- ative and postoperative hemoglobin (Hb) levels, serum creatinine levels, estimated glomerular filtration rate (eGFR), and R.E.N.A.L Nephrometry Score were eval- uated in all patients undergoing the NSS techniques (SE and ER). Glomerular filtration speed was calculated us- ing the Chronic Kidney Disease Epidemiology Collab- oration formula.(8) Pathological tumor size, 2010 TNM (tumor, node, metastasis) stage, the surgical margin in the specimens, and histological subtypes according to the World Health Organization (WHO) classifications were recorded. During the postoperative follow-up, all patients underwent radiological reevaluations for local recurrence and metastasis. The study was presented to the local ethics committee. This study followed the Declaration of Helsinki statement on medical protocol and ethics. Statistical Analysis The Statistical Package for the Social Science (SPSS Inc, Chicago, Illinois, USA) version 18.0 was used for statistical analysis. The data are recorded as the mean ± standard deviation (SD) and percentage values. For the parameters with a normal distribution, Student’s t-test was used to compare the two groups. Comparisons of categorical data were made using a χ² test. Variant anal- yses were used to test the difference in the GFR and cre- atinine levels in repetitive measurements. Bonferroni’s correction was used to determine differences between the groups. P = .05 was considered to indicate statistical significance. RESULTS Patient Characteristics The data obtained from 72 patients were evaluated. When the two groups (SE and ER) were compared, the mean ages of the patients were 55.5 ± 11.0 and 54.6 ± 12.9 years, respectively (P = .76). The male/female ra- tios were 21 (63.6%) and 24 (61.5%) for males and 12 (36.4%) and 15 (38.5%) for females in the SE and ER groups, respectively (P = .85; Table 1). Event Characteristics The mean tumor size was 36.8 ± 13.3 mm in the SE group and 40.4 ± 15.2 mm in the ER group (P = .17). The mean R.E.N.A.L Nephrometry Score was 4.55 ± 0.87 (range 4-6 points) in the SE group and 4.64 ± 0.78 (range 4-6 points) in the ER group (P = .39). In terms of localization of the mass in the kidneys, 17 (51.5%) and 18 (46.1%) lesions were on the right side in the SE and ER groups, respectively, whereas 16 (48.5%) and 21 (53.9%) lesions were on the left side in the SE and ER groups, respectively (P = .83). The numbers of histological types of tumors (clear cell renal cell carcinoma [RCC], papillary RCC, chromo- phobe RCC, other RCC, non-RCC) were 16 (48.5%), 8 (24.3%), 2 (6%), 3 (9.1%), and 4 (12.1%), respectively, in the SE group and 25 (64.1%), 7 (18%), 5 (12.8%), 2 (5.1%), and 0, respectively, in the RE group. In the SE group, four non-RCC tumors were noted, two of which were angiolipomas and two were oncocytomas. The histopathological analysis of the surgical specimens re- vealed negative surgical margins in all specimens. The TNM 2010 classifications (pT1a, pT1b, and pT2a) Table 2. Preoperative and postoperative renal function results. Variables Preoperative eGFR (mL/min/1.73 m²) Postoperative 3rd Month eGFR (mL/min/1.73 m²) P Value Group SE 103.6 ± 24.1 96.0 ± 23.8 .046 Group ER 89.5 ± 26.4 85.6 ± 30.5 .636 Abbreviations: eGFR, estimated glomerular filtration rate; SE, simple Enucleation; ER, enucleo-resection Figure 1. Exophytic tumor located at the lower pole of the kidney. Renal Tumor and Nephron Sparing Surgery-Balasar et al. Vol 12 No 06 November-December 2015 2412 were assigned to the lesions as follows: 21 (63.6%), 11 (33.4%), and 1 (3%), respectively, in the SE group and 23 (58.9%), 15 (38.5%), and 1 (2.6%), respectively, in the RE group. The average operation durations for the SE and ER groups were 100.0 ± 13.2 and 106.7 ± 14.1 minutes (P = .61), respectively. The average blood loss volumes were 286.7 ± 143.1 and 313.8 ± 169.7 mL (P = .47), re- spectively, and the average Hb drop measurements were 1.55 ± 1.20 and 1.07 ± 1.58 mg/dL (P = 1.19), respec- tively. The intraoperative blood loss ranged between 50 and 750 mL. Blood transfusion was performed in three patients in whom the preoperative Hb level of 10 mg/ dL decreased postoperatively to 8 mg/dL (two in the SE group and one in the ER group). The preoperative and 3-month postoperative eGFR values in the SE group were 103.6 ± 24.1 and 96.0 ± 23.8 mL/min/1.73 m2, respectively (P = .046). The cor- responding eGFR values in the ER group were 89.5 ± 26.4 and 85.6 ± 30.5 mL/min/1.73 m2 (P = .636). Sig- nificant differences were noted between the preopera- tive and 3-month eGFR values in the SE group (Table 2). The drains were removed on the third postoperative day. Prolonged urinary drainage (6 days) was observed in one patient in the ER group. One patient in the SE group had gross hematuria for 7 days that resolved spontane- ously during the follow-up. The mean follow-up was 40.5 ± 21.5 months after SE and 41.5 ± 24.3 months after ER (P = .6). The median follow-up was 19 months (2-80 months) for the SE group and 41 months (1-95 months) for the ER group. The patients were re-evaluated during the postoperative follow-up period for local recurrence and metastasis. Two years after the operation, ipsilateral adrenal and probable contralateral kidney metastases were detected in one patient in the ER group who had a history of histologically diagnosed papillary RCC. No local recur- rence or metastasis was observed in any other patients. DISCUSSION Czerny first described NSS for treating renal tumors in 1890.(9) In 1950, Vermooten proposed that peripheral encapsulated renal neoplasms could be excised local- ly by leaving a margin of normal parenchyma around the tumor.(9,10) Although radical nephrectomy (RN) has been a proven effective treatment modality since the 1950s, NSS has only limited applications. Many re- searchers have published their results after kidney-pre- serving surgical interventions and have demonstrated the validity of this approach in cases in which RN could not be conducted. Moreover, various retrospective stud- ies have demonstrated that survival is enhanced with NSS due to preserved renal function.(11) The European Organization for Research and Treatment of Cancer randomized trial 30904 demonstrated that NSS has a reduced overall survival rate compared with RN. The study also demonstrated that NSS reduced the incidence of moderate renal failure.(12,13) In line with the recent in- crease in incidental tumor diagnosis, the focus on NSS has also increased. Today, according to European As- sociation of Urology guidelines, NSS has become the standard treatment modality for tumors < 4 cm.(14) The aim of NSS is total resection of the renal tumor while retaining as much functional parenchyma as pos- sible.(15) Several tumor-related factors, i.e., renal tumor Urological Oncology 2413 Figure 2. Enucleated tumor. Figure 3. The tumor bed after resection. Renal Tumor and Nephron Sparing Surgery-Balasar et al. size, location, and depth, are visible on preoperative imaging and can affect the tumor resection technique. Hence, various NSS techniques are available. The most common NSS technique is clamping the renal artery with or without the renal vein and sharply excising the renal mass. The time frame during which a vessel is clamped is called the “warm ischemia time.” A safe warm ischemia time is still under discussion; however, it is generally accepted to be 20 to 30 minutes.(6,16) Re- moving a 1-cm margin of normal parenchyma may lead to complications, such as increased hemorrhage risk, potential renal hilum injury, collecting system injury, the need for renal vessel clamping, and prolonged is- chemia time.(17) When the concept of an NSS surgical technique was in- itiated, it involved excising a 1-cm margin of peritumor normal renal parenchyma to ensure a negative surgical margin. In recent decades, however, various authors have demonstrated that intact parenchyma surrounding the tumor can be limited to a few millimeters while pre- serving the oncological safety of NSS.(18) Despite the fact that the mean thickness of the safety margin sur- rounding the tumor ranges from 2.5 to 5.0 mm, various studies have demonstrated that the minimum thickness of the safety margin is 0 to 1 mm, which is most impor- tant at the bottom of the tumor. Various recent studies have assumed no association between margin size dur- ing NSS of small renal masses and the recurrence of RCC.(2) With NSS, especially in single, small (< 4 cm) tumors limited to the kidney, oncological outcomes are simi- lar to those of RN outcomes, whereas renal function is better preserved. This finding is especially important for patients with a solitary functioning kidney. Most of these patients had pre-existing renal insufficiency. Thus, their quality of life, i.e., having dialysis-free and tumor-free renal function, is positively affected.(19) The 5-year disease-specific survival rates can increase up to 97%, differentiating NSS from RN.(20) Although the up- per tumor size limit for elective NSS is defined as 4 cm, tumors up to 7 cm might be appropriate for treatment using NSS in cautiously selected patients.(14,21,22) Following these developments, SE and ER techniques have been used.(14,21) Small RCCs may frequently be well bordered and have a pseudocapsule. These are not true capsules, however, and might be invaded by the tumor. Therefore, if a small portion of the healthy pa- renchyma surrounding the renal tumor is not excised, it may lead to incomplete resection because of microscop- ically sized residual tumors. Therefore, in the case of simple tumor enucleation, frozen section analysis from the resection borders and the coagulation of the tumor bed is suggested.(23) Alternatively, as with the ER tech- nique, the mass is debulked with a cautery dissection 1 to 5 mm away from the peritumoral capsule. With SE, the tumor is excised with blunt dissection following the natural cleavage plane between the peri- tumoral capsule and the renal parenchyma, leaving be- hind a visible border of healthy renal tissue. Evaluations of progression-free and cancer-specific survival (CSS) data revealed that renal tumor enucleation is a more on- cologically sound procedure than NSS.(24) Lapini and colleagues reported on the results of enucle- ation of small RCCs (median 2.5 cm) combined with tumor bed coagulation with diathermy spray coagula- tion or an argon beam. The 107 patients were followed for a mean of 88.3 months. The authors reported 99% 5-year and 97.8% 10-year CSS rates for this patient se- ries. The 5- and 10-year progression-free survival rates were 98.1% and 94.7%, respectively.(25) However, re- cent data suggested that enucleation of RCCs without tumor bed ablation may produce similar oncological outcomes. Minervini and colleagues reported the results of a series of consecutive patients undergoing enucleation without ablation of the renal tumor surgical bed. According to their report, all of the patients had positive surgical mar- gins, but only 3 of the 164 patients (1.8%) developed a local recurrence, of which only one (0.6%) was a true local recurrence in the enucleation bed. To date, this study is the largest consecutive series of RCCs treated with enucleation with no ablation of the surgical bed.(24) In the present study, only 1 of the 72 patients who un- derwent either SE or ER had a positive surgical margin and developed metastasis and/or local recurrence dur- ing the mean 40.7-month follow-up. Two years after the operation, ipsilateral adrenal and contralateral kidney metastases were detected in this patient, who was in the ER group and was formerly diagnosed with histologi- cally diagnosed papillary RCC. Despite the fact that our mean postoperative follow-up period was short (40.7 months), neither of the surgical techniques was superior to the other in terms of survival rates. Three anatomical classification and scoring systems are used to identify the predictive characteristics of renal tumors and can be used to identify the risk of a pro- longed warm ischemia time or surgical complications: the R.E.N.A.L Nephrometry Score, Padua score, and C (centrality) index.(16) R.E.N.A.L nephrometry scores impact the preoperative approaches to kidney tumors. According to one retrospective study, this scoring sys- tem is a useful tool when using NSS to remove a cT1 Renal Tumor and Nephron Sparing Surgery-Balasar et al. Vol 12 No 06 November-December 2015 2414 renal cancer.(26) In another study on the predictive val- ue of the R.E.N.A.L Nephrometry Score in regard to performing robotic partial nephrectomy, a strong pos- itive relation was observed between the R.E.N.A.L Nephrometry Score and the warm ischemia time.(27) To decrease hemorrhage during NSS, the renal pedicle is frequently clamped. However, recent studies have claimed that warm ischemia of > 20 minutes might lead to serious kidney damage. The increased popularity of laparoscopic NSS with a prolonged operation time among NSS procedures exposes the kidney to more is- chemia, leading to long-lasting harm. Thompson and colleagues. demonstrated that a prolonged ischemia time in patients with solitary kidneys has undesirable long-term effects on renal function.(28) Despite the fact that the use of NSS has been described with open, laparoscopic, and robotic methods, the most important point for the patient is to preserve renal func- tion.(29) Marszalek and colleagues reported that when open NSS (ONSS) is compared to laparoscopic surgery the warm ischemia time is shorter with ONSS, although the hemorrhage levels are the same.(30) Lucas and col- leagues, in a study of 96 patients with kidney tumors with a mean size of 2.3 cm and a Nephrometry Score of 6, reported that renal function preservation, complica- tion rates, and surgical margin positivity were compa- rable for all three methods.(31) The mean operation time was 147 minutes in the ONSS group, which included a significantly shorter (12 minutes) warm ischemia time. However, the hemorrhage amount was > 250 mL. In the same study, a decrease of > 10% in the eGFR levels of 44 patients was significant. In the 72 NSS cases in this study, the mean tumor size was 36.8 mm in the SE group and 40.4 mm in the ER group, respectively. The R.E.N.A.L Nephrometry Scores were 4.55 ± 0.87 and 4.64 ± 0.78, respectively. The mean hemorrhage amount during the intervention was 301.4 ± 157.5 mL, which is consistent with the findings in the literature. The pedicle was not clamped in any of the patients during the operation, and the kid- ney was not exposed to warm ischemia. During the SE procedure, while the tumor was enucleated and the pa- renchyma sutured, the enucleation site and surrounding parenchyma were compressed between the thumb and index finger for homeostasis. During the ER procedure, Gyrus open forceps were used, and some intact tissue was excised together with the tumor. There was some concern that the Gyrus open forceps might affect the eGFR by its thermal energy. We did not observe any eGFR change at the 3-month follow-up evaluation in the ER group (P = .636). However, we identified a sig- nificant change in the SE group from the preoperative eGFR level (P = .046). Although the compression time and compression force applied to the parenchyma were not clear, we thought that the decrease in the eGFR scores at the 3-month follow-up might be attributed to the renal parenchymal compression that was achieved using the thumb and index finger, perhaps causing me- chanical or ischemic stress. The small sample size, short follow-up period, and ret- rospective nature of the study design are the limitations of this study. Hence, there is need for well-designed prospective studies. CONCLUSIONS Non-hilar clamping SE and ER are safe, acceptable approaches for treating exophytic renal tumors. No statistically significant differences were noted in the R.E.N.A.L Nephrometry Scores, operative times, or intraoperative blood loss in the non-hilar clamping SE and ER groups. CONFLICT OF INTEREST None declared. REFERENCES 1. Haddad RL, Patel MI, Vladica P, Kassouf W, Bladou F, Anidjar M. Percutaneous radiofrequency ablation of small renal tumors using CT-guidance: a review and its current role. Urol J. 2012;9:629-38. 2. Ficarra V, Galfano A, Cavalleri S. Is simple enucleation a minimal partial nephrectomy responding to the EAU guidelines’ recommendations? Eur Urol. 2009;55:1315-8. 3. Uzzo RG, Novick AC. Nephron sparing surgery for renal tumors: indications, techniques and outcomes. J Urol. 2001;166:6- 18. 4. Minervini A, Rosaria Raspollini M, Tuccio A, et al. Pathological characteristics and prognostic effect of peritumoral capsule penetration in renal cell carcinoma after tumor enucleation. Urol Oncol. 2014;32:50.e15-22 5. Margreiter M, Marberger M. Current status of open partial nephrectomy. Curr Opin Urol. 2010;20:361-4. 6. Shikanov S, Lifshitz D, Chan AA, et al. Impact of ischemia on renal function after laparoscopic partial nephrectomy: a multicenter study. J Urol. 2010;183:1714-8. 7. Kutikov A, Uzzo RG. The R.E.N.A.L. nephrometry score: a comprehensive standardized system for quantitating renal tumor size, location and depth. J Urol. 2009;182:844-53. 8. Levey AS, Stevens LA, Schmid CH, et al. A new equation to estimate glomerular filtration Urological Oncology 2415 Renal Tumor and Nephron Sparing Surgery-Balasar et al. rate. Ann Intern Med. 2009;150:604-12. 9. Czerny HE. Cited by Herczele: Ueber Nierenexstirpation. Beitr Z Klin. 1890;6:484- 6. 10. Vermooten V. Indications for conservative surgery in certain renal tumors: a study based on the growth pattern of the cell carcinoma. J Urol. 1950;64:200-8. 11. Weight CJ, Lieser G, Larson BT, et al. Partial nephrectomy is associated with improved overall survival compared to radical nephrectomy in patients with unanticipated benign renal tumours. Eur Urol. 2010;58:293- 8. 12. Van Poppel H, Da Pozzo L, Albrecht W, et al. A prospective, randomised EORTC inter group phase 3 study comparing the oncologic outcome of elective nephron-sparing surgery and radical nephrectomy for low-stage renal cell carcinoma. Eur Urol. 2011;59:543-52. 13. Scosyrev E, Messing EM, Sylvester R, Campbell S, Van Poppel H. Renal function after nephron-sparing surgery versus radical nephrectomy: results from EORTC randomized trial 30904. Eur Urol. 2014;65:372-7. 14. Ljungberg B, Cowan NC, Hanbury DC, et al. EAU guidelines on renal cell carcinoma: the 2010 update. Eur Urol. 2010;58:398-406. 15. Miyamoto K, Inoue S, Kajiwara M, Teishima J, Matsubara A. Comparison of renal function after partial nephrectomy and radical nephrectomy for renal cell carcinoma. Urol Int. 2012;89:227-32. 16. Krebs RK, Andreoni C, Ortiz V. Impact of radical and partial nephrectomy on renal function in patients with renal cancer. Urol Int. 2014;92:449-54. 17. Li QL, Guan HW, Zhang QP, Zhang LZ, Wang FP, Liu YJ. Optimal margin in nephron sparing surgery for renal cell carcinoma 4 cm or less. Eur Urol. 2003;44:448-51. 18. Sutherland SE, Resnick MI, Maclennan GT, Goldman HB. Does the size of the surgical margin in partial nephrectomy for renal cell cancer really matter? J Urol. 2002;167:61-4. 19. Fergany AF, Hafez KS, Novick AC. Long- term results of nephron sparing surgery for localized renal cell carcinoma: 10-year follow- up. J Urol. 2000;163:442-5. 20. Patard JJ, Shvarts O, Lam JS, et al. Safety and efficacy of partial nephrectomy for all T1 tumors based on an international multicenter experience. J Urol. 2004;171:2181-5. 21. Canda AE, Kirkali Z. Current management of renal cell carcinoma and targeted therapy. Urol J. 2006;3:1-14. 22. Bayrak O, Seckiner I, Erturhan S, Cil G, Erbagci A, Yagci F. Comparison of the complications and the cost of open and laparoscopic radical nephrectomy in renal tumors larger than 7 centimeters. Urol J. 2014;11:1222-7. 23. Steinbach F, Stöckle M, Hohenfellner R. Current controversies in nephron-sparing surgery for renal-cell carcinoma. World J Urol. 1995;13:163-5. 24. Minervini A, Serni S, Tuccio A, et al. Local recurrence after tumour enucleation for renal cell carcinoma with no ablation of the tumour bed: results of a prospective single-centre study. BJU Int. 2011;107:1394-9. 25. Lapini L, Serni S, Minervini A, Masieri L, Carini M. Progression and long-term survival after simple enucleation for the elective treatment of renal cell carcinoma: experience in 107 patients. J Urol. 2005;174:57-60. 26. Yasuda Y, Yuasa T, Yamamoto S, et al. Evaluation of the RENAL nephrometry scoring system in adopting nephron-sparing surgery for cT1 renal cancer. Urol Int. 2013;90:179-83. 27. Boylu U, Güzel R, Turan T, Lee BR, Thomas R, Gumus E. Predictive value of R.E.N.A.L. nephrometry score in robotic assisted partial nephrectomy. Turk J Urol. 2011;37:81-5. 28. Thompson RH, Lane BR, Lohse CM, et al. Comparison of warm ischemia versus no ischemia during partial nephrectomy on a solitary kidney. Eur Urol. 2010;58:331-6. 29. Leslie S, Goh AC, Gill IS. Partial nephrectomy- contemporary indications, techniques and outcomes. Nat Rev Urol. 2013;10:275-83. 30. Marszalek M, Meixl H, Polajnar M, Rauchenwald M, Jeschke K, Madersbacher S. Laparoscopic and open partial nephrectomy: a matched-pair comparison of 200 patients. Eur Urol. 2009;55:1171-8. 31. Lucas SM, Mellon MJ, Erntsberger L, Sundaram CP. A comparison of robotic, laparoscopic and open partial nephrectomy. JSLS. 2012;16:581-7. Renal Tumor and Nephron Sparing Surgery-Balasar et al. Vol 12 No 06 November-December 2015 2416