- Email: [email protected]
Outcomes of Robotic Partial Nephrectomy for Renal Masses With Nephrometry Score of ≥7
Renal Cancer Outcomes of Robotic Partial Nephrectomy for Renal Masses With Nephrometry Score of >7 Michael A. White, Georges-Pascal Haber, Riccardo Autorino, Rakesh Khanna, Adrian V. Hernandez, Sylvain Forest, Bo Yang, Fatih Altunrende, Robert J. Stein, and Jihad H. Kaouk OBJECTIVES METHODS
RESULTS
CONCLUSIONS
To evaluate the safety and feasibility of robotic partial nephrectomy for patients with complex renal masses. We reviewed the data for 164 consecutive patients who had undergone transperitoneal robotic partial nephrectomy at a tertiary care center from February 2007 to June 2010. Of the 112 patients who had available imaging studies to review, 67 were identified and classified as having a moderately or highly complex renal mass according to the R.E.N.A.L. nephrometry score (ⱖ7) (tumor size—[R]adius, location and depth—[E]xophytic or endophytic; nearness to the renal sinus fat or collecting system [N]; anterior or posterior position [A], and polar vs non-polar location [L]). The preoperative, perioperative, pathologic, and functional outcomes data were analyzed. The median body mass index was 29.6 kg/m2 (range 19.9-44.8). Of the 67 patients, 32 were men and 35 were women, with 32 right-sided masses and 35 left-sided masses. The median tumor size was 3.7 cm (range 1.2-11), and the median operative time was 180 minutes (range 150-180). The median estimated blood loss was 200 mL (range 100-375), and the warm ischemia time was 19.0 minutes (range 15-26). The median hospital stay was 3.0 days (range 3-4). The estimated glomerular filtration rate was calculated at a median decrease of 11.1 mL/min/1.73 m2 (range 9-1.3). According to the Clavien-Dindo classification of surgical complications, 2 grade 1, 12 grade 2, and 1 grade 3 complication occurred. All margins were pathologically negative, except for 1, and, after a mean follow-up of 10 months, no recurrences had developed. Robotic partial nephrectomy is a safe and feasible option for moderately or highly complex renal masses determined by the R.E.N.A.L. nephrometry score. The warm ischemia time, blood loss, and complications were increased with highly complex masses. UROLOGY 77: 809 – 813, 2011. © 2011 Elsevier Inc.
T
he expansion of minimally invasive techniques has allowed laparoscopic partial nephrectomy to be performed for small renal masses with oncologic and functional outcomes comparable to those of open partial nephrectomy.1,2 Robotic-assisted laparoscopy allows for improved dexterity, increased visualization, tremor filtration, and an ergonomic setting to enhance surgeon comfort. Experience with robotic partial nephrectomy (RPN) continues to grow, and ⬎300 cases have been reported in 2009 and 2010 alone.3-14 The indications for RPN have expanded to include the treatment of “complex” renal masses. The
G.-P. Haber is a speaker for Intuitive Surgical; R. J. Stein is a speaker for Applied Medical; and J. H. Kaouk is a speaker for Intuitive Surgical and Covidien. From the Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio Reprint requests: Jihad H Kaouk, M.D., Department of Surgery, Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute, 9500 Euclid Avenue, Q-10, Cleveland, OH 44195. E-mail: [email protected] Submitted: October 8, 2010, accepted (with revisions): December 5, 2010
© 2011 Elsevier Inc. All Rights Reserved
available studies to date have had to rely solely on single tumor features to define masses as “complex,” including, for example, location (hilar), growth pattern (endophytic), and number of lesions (multiple).6,15,16 We report on our single-surgeon experience with RPN in patients with moderate and highly complex renal masses. In an attempt to characterize the renal tumor anatomy in a reproducible and quantifiable manner, we elected to use the recently developed and externally validated, R.E.N.A.L. nephrometry score to designate renal masses as “complex” in nature.17-19 The scoring system considers the Radius (tumor size), Exophytic or endophytic (location and depth), Nearness to the renal sinus fat or collecting system, Anterior or posterior position, and Location (polar vs nonpolar).
MATERIAL AND METHODS From February 2007 to June 2010, 164 patients had undergone RPN. The patient data were entered prospectively into our 0090-4295/11/$36.00 doi:10.1016/j.urology.2010.12.005
809
Table 1. Patient demographic data Variable
Value
Patients (n) Tumors resected (n) Age (y) Median Range Sex (n) Male Female Body mass index (kg/m2) Median Range Preoperative serum creatinine (mg/dL) Median Range Preoperative GFR (mL/min/1.73 m2) Median Range Side of involvement (n) Right Left R.E.N.A.L. score 7-9 ⱖ10
67 67 60.0 35-88 32 35 29.6 19.9-44.8 0.92 0.51-2.58 75.3 26.6-148.9 32 35 56 11
GFR, glomerular filtration rate; R.E.N.A.L., Radius (tumor size), Exophytic or endophytic (location and depth), Nearness to renal sinus fat or collecting system, Anterior or posterior position, and Location (polar vs nonpolar).
institutional review board-approved RPN database. Of the 164 patients, the films for 52 patients were not accessible either because of missing hard copies (returned to the patients) or an inability to access them from our electronic system. A total of 112 patients had computed tomography scans available for review, and 6 were excluded because of multiple masses in a single renal unit. The patient demographic data for those who had undergone RPN are summarized in Table 1. The R.E.N.A.L. nephrometry score was applied by 2 urology fellows independently and in consensus when differences occurred, and 67 patients with a score of ⱖ7 were identified as having a moderate or highly complex renal mass. The nephrometry score was determined by 5 reproducible and important features that characterize the renal tumor anatomic attributes as they apply to surgical resectability.17 Of the 5 components, 4 are scored from 1 to 3 points, and a cumulative total is assigned. The fifth component is used to designate whether the renal mass is anteriorly or posteriorly located. Scores of 4-6 are representative of low complexity masses and scores of 7-9 moderately complex, and scores of 10-12 highly complex. The nephrometry score and each of its elements are detailed in Table 2. The perioperative outcome data, including estimated blood loss (EBL), operative time, warm ischemia time (WIT), length of stay (LOS), change in creatinine and estimated glomerular filtration rate from preoperatively to postoperative day 3, complications, and conversion to open surgery were recorded. Additionally, a subset analysis was performed to evaluate the perioperative outcomes between patients with moderate and highly complex masses and those with lower complexity masses.
Statistical Analysis The Statistical Package for Social Sciences (SPSS, Chicago, IL) was used to perform all statistical analyses. Statistical significance was set at P ⱕ .5. Descriptive analyses were performed to 810
Table 2. Patient distribution according to R.E.N.A.L. nephrometry score parameters Patients (n)
Score Parameters R (maximal diameter; cm) ⱕ4 (1 point) ⬎4 but ⬍7 (2 points) ⱖ7 (3 points) E (exophicity) ⱖ50% (1 point) ⬍50% (2 points) Entirely endophytic (3 points) N (nearness of tumor to collecting system or sinus; mm) ⱖ7 (1 point) ⬎4 but ⬍7 (2 points) ⱕ4 (3 points) A (anterior vs posterior) Anterior Posterior Indeterminate L (location relative to polar lines) Entirely above upper or below lower polar line (1 point) Lesion crosses polar line (2 points) ⬎50% of mass crosses polar line or axial renal midline or is entirely between polar lines (3 points)
43 19 5 5 59 3 6 6 55 28 33 6 18 16 33
Scores of 4-6 represent low complexity masses, scores of 7-9 considered moderately complex, and scores of 10-12 highly complex.
describe the characteristics of the patient sample (median, standard deviation, percentages, and frequencies). The Wilcoxon rank-sum test and Fisher’s exact test were used to compare the outcomes between the 2 subset analyses.
Surgical Technique Positioning and Port Placement. The patient was positioned in the modified flank position at approximately 60°. The table was flexed and positioned in a slight Trendelenburg position. The abdomen was insufflated to 15 mm Hg with a Veress needle at the lateral border of the rectus muscle across from the twelfth rib and served as the site for a 12-mm port and the standard robotic telescope. An 8-mm robotic port was placed at the lateral border of the ipsilateral rectus muscle, about 3 cm below the costal margin. A second 8-mm robotic port was placed about 5-7 cm cephalad to the anterior superior iliac spine. An assistant 12-mm port was placed along the lateral border of the rectus muscle in the lower abdominal quadrant. If additional retraction was needed on the right side to retract the liver, a 5-mm port was placed in the subxiphoid area. The robot was then positioned over the patient’s shoulder, with the camera oriented in line with the kidney. Bowel Mobilization. A 30° scope facing downward was used, along with the 8-mm Endowrist (Intuitive Surgical, Sunnyvale, CA) monopolar shears in the right hand and the 8-mm Endowrist Prograsp Grasper in the left hand. The peritoneum was sharply incised along the white line of Toldt. The bowel was mobilized medially, developing a plane anterior to Gerota’s fascia and posterior to the mesocolon. Dissection continued cephalad to mobilize the spleen or liver. UROLOGY 77 (4), 2011
Hilar Dissection and Control. Dissection proceeded along the psoas muscle with anterior elevation of the ureter and/or gonadal vein to identify the renal hilum. The hilum was cleared of all its attachments to allow for occlusion with either bulldog clamps or a satinsky clamp. The artery and vein should be completely dissected to achieve adequate occlusion for the bulldog clamps. The hilum was clamped en bloc if a satinsky clamp was used. Tumor Exposure and Ultrasound Identification. Gerota’s fascia was opened and dissection performed along the renal capsule until the mass was exposed. The fat was then cleared circumferentially around the mass, allowing for visualization of ⱖ1-2 cm of normal parenchyma for future renal reconstruction. All attempts should be made to leave the overlying Gerota’s fascia atop the mass to assist in histopathologic staging and also to use as a handle for retraction. The laparoscopic ultrasound probe was used to plan the excision margins. The renal capsule was scored to delineate the resection boundaries. Vasculature Control and Tumor Excision. Before hilar occlusion, 12.5 g of mannitol was given intravenously. The hilum was occluded and the tumor resected along the previously scored margin using cold scissors. The bedside assistant used suction to clear the resection bed and allow for improved visualization while applying slight counter retraction, as needed. Renal Reconstruction. An 8-in. 2-0 Vicryl suture on an SH-1 needle (Ethicon Endosurgery, Johnson & Johnson, Cincinnati, OH) with a knot and Hem-o-Lok clip (Teleflex Medical, Research Triangle Park, NC), fixed to the opposite end was used to place a running suture of the tumor excision bed to achieve hemostasis and closure of the collecting system. The hilum was unclamped, and the renal excision bed was inspected for hemostasis. The renal parenchyma defect was approximated using 0 Vicryl sutures on a CT-1 needle. These sutures were placed in a running horizontal mattress fashion and secured in place with Hem-o-Lok clips in a sliding technique. The defect was covered with oxidized cellulose (Surgicel, Johnson & Johnson, Somerville, NJ) and a fibrin sealant (Evicel, Johnson & Johnson) or (Vitagel, Orthovita, Malvern, PA). Specimen Extraction and Closure. The specimen was placed in a laparoscopic entrapment sac and removed from an extended lower quadrant port site. Care must be taken to make the extraction incision large enough to avoid fracturing the specimen, possibly preventing accurate histopathologic examination for margin status and staging. All 12-mm incisions were closed with 0 Vicryl suture using the Carter Thomason device. A drain was placed through a lower lateral port.
RESULTS A total of 67 patients who had undergone RPN for moderately or highly complex renal masses were included in the present study. The median tumor size was 3.7 cm (range 1.2-11), with a median operative time of 180 minutes (range 150-180). The median EBL was 200 mL (range 100-375), and the WIT was 19 minutes (range 15-26). The median hospital stay was 3.0 days (range 3-4). The overall results are detailed in Table 3. A total of 15 complications occurred. These were graded using UROLOGY 77 (4), 2011
Table 3. Summary of results Variable Operative time (min) Median IQR WIT (min) Median IQR EBL (mL) Median IQR Hospital stay (d) Median IQR Decrease in eGFR (mL/min/1.73 m2) Median IQR* Resected mass (cm) Mean Range Mass type (n) Clear cell renal cell carcinoma Papillary renal cell carcinoma Chromophobe renal cell carcinoma Unclassified renal cell carcinoma Oncocytoma Angiomyolipoma Benign cyst Metanephric adenoma Pathologic stage (n) T1a T1b T2 T3a Benign
Value 180 150-180 19 15-26 200 100-375 3.0 3-4 ⫺11.1 ⫺19 to ⫺1.3 3.7 1.2-11 45 5 2 3 4 3 4 1 38 11 2 4 12
IQR, interquartile range (25th to 75th percentile); WIT, warm ischemia time; EBL, estimated blood loss; eGFR, estimated glomerular filtration rate. * Between level at third postoperative day and preoperative level.
the Clavien-Dindo classification of surgical complications and included 1 grade 3 complication, 12 grade 2 complications, and 2 grade 1 complications. One surgical margin was positive on final pathologic evaluation, but no evidence was found of recurrence during 8 months of follow-up. The subset analysis comparing the perioperative outcomes between the groups demonstrated a statistically significant reduction in EBL, operative time, and WIT, in favor of the lower and moderately complex groups over the highly complex group. Statistically significant differences in perioperative outcomes were not demonstrated between the lower and moderately complex groups. The complete results are detailed in Table 4.
COMMENT Gettman et al20 were the first to report the use of the da Vinci surgical system (Intuitive Surgical) to assist in laparoscopic partial nephrectomy. They performed 13 procedures, and the mean size of the tumor resected was 3.5 cm, with a mean operative time of 215 minutes and a WIT of 22 minutes. The mean EBL was 170 mL, and 811
Table 4. Comparative outcomes among mild/least complex (score 4-6), moderate (score 7-9), and severe (score 10-12) groups Outcome EBL (mL) Operative time (min) WIT (min) Hospital stay (d) Difference in creatinine Difference in GFR Any complication
Mild (Score 4-6; n ⫽ 39)
Moderate (Score 7-9; n ⫽ 56)
Severe (Score 10-12; n ⫽ 11)
P Value
150 (100-300) 180 (150-190) 14 (0-17) 3 (3-4) 0.06 (⫺0.08 to 0.19) NA 8 (21)
150 (100-300) 175 (150-180) 17 (15-23) 3 (2-4) 0.09 (0.02-0.20) ⫺11.1 (⫺17.4 to ⫺2.3) 10 (18)
500 (300-525) 200 (180-225) 27 (21-33) 4 (3-5) 0.12 (0.02-0.31) ⫺11.7 (⫺20.7 to ⫺0.8) 5 (45)
.03* .02* ⬍.00001* .1 .2 — .1
NA, not applicable; other abbreviations as in Table 3. Data presented as median, with interquartile range in parentheses, or numbers, with percentages in parentheses. P value for differences among 3 groups, tested using Kruskal-Wallis test (continuous variables) or Fisher’s exact test (for any complication). * Greater values for severe group vs other 2 groups.
the mean LOS was 4.3 days. At 2-11 months of followup, no recurrence had been noted. Since then, ⬎24 reports have been published on the technique and specific institutions’ experience, totaling approximately 600 cases.3-16,20-29 Initially, the system was recommended for small anterior exophytic masses; however, as documentation regarding the safety and efficacy were amassed, the indications for using the da Vinci surgical system for partial nephrectomy were expanded. Rogers et al15 described their technique and results for RPN in 8 complex cases, including hilar tumors, endophytic tumors, and multiple tumors, with a total of 14 tumors resected. The mean tumor size resected was 3.6 cm, with a mean operative time of 192 minutes and a WIT of 31 minutes. The mean EBL was 230 mL, and the mean LOS was 2.6 days. All patients had negative surgical margins, and no tumor recurrence had been observed at a follow-up of 3 months. The investigators concluded that RPN is a safe and feasible approach for select patients with complex renal tumors.15 Additionally, Rogers et al16 reported on a multi-institutional analysis of RPN for renal hilar tumors. A total of 11 RPN procedures were performed for renal hilar tumors, defined as tumors abutting the renal artery and/or renal vein on preoperative imaging. The mean tumor size resected was 3.8 cm, with a mean operative time of 202 minutes and a WIT of 28.9 minutes. The mean EBL was 220 mL, and the mean LOS was 3 days.16 Recently, Gong et al6 reported on the outcomes of 29 patients, who had undergone RPN for renal masses, including hilar, endophytic, and multiple tumors. The mean tumor size resected was 3.0 cm, with a mean operative time of 197 minutes and a WIT of 25 minutes. The mean EBL was 220 mL, and the mean LOS was 2.5 days. All cases had negative surgical margins, and no recurrence was evident at a mean follow-up of 15 months.6 Our results were comparable to these previously published reports detailing RPN for complex masses; however, because these studies were performed before the R.E.N.A.L. nephrometry score was developed, exact comparisons could not be drawn. Patients with moderate or highly complex renal masses constituted ⬎50% of our patient population according to the R.E.N.A.L. 812
nephrometry score and was representative of our center’s tertiary care status. The median renal mass diameter, operative time, and EBL were similar to those published by Rogers et al15,16 and Gong et al6; however, our series had a shorter WIT at 19.0 minutes compared with 31.0, 28.9, and 25.0 minutes. The shorter WIT might have resulted from the early unclamping technique used during our initial deep layer renorrhaphy and described by Nguyen et al30 for use during standard laparoscopy or might have resulted from the sliding clip renorrhaphy technique, which allows for faster reconstruction.12 By performing a precise and detailed reconstruction of the collecting system and surrounding deep cortex, we were able to release the vasculature occlusion device without encountering significant hemorrhage. Whether a reduction in WIT will translate into long-term preservation of renal function has yet to be determined. Our follow-up data demonstrated renal function preservation and oncologic outcomes similar to those from previously published reports. The estimated glomerular filtration rate in our study was calculated at a median decrease of 11.1 mL/min/1.73 m2 compared with 5.6, 8.0, and 4.5 as documented by Rogers et al15,16 and Gong et al.6 At a mean follow-up of 10 months, we have not had evidence of tumor recurrence in any patient. When the perioperative outcomes were analyzed among the lower, moderately, and highly complex masses, significant differences were found in the EBL, operative time, and WIT, favoring the lower and moderately complex groups. This was not surprising and supported the findings by Hayn et al,19 regarding the application of the R.E.N.A.L. nephrometry score to LPN specimens. A total of 15 complications occurred, including in 12 patients who required transfusions (Clavien grade 2) and 1 who eventually required thoracostomy tube placement because of iatrogenic pneumothorax (Clavien grade 3b). The pneumothorax had occurred in 1 patient with a right-sided upper pole mass and resulted from diaphragmatic injury from the locking grasper used for liver retraction. No patients required angioembolization. One patient developed a contained urine leak that did not require intervention (Clavien grade 1), and one developed a prolonged ileus (4-7 days; Clavien grade 2) and was treated conservatively. UROLOGY 77 (4), 2011
Although the R.E.N.A.L. score can be helpful in evaluating the anatomic complexity of renal masses, it is important to acknowledge additional factors that can add to the difficulty of RPN. Posteriorly located tumors require nearly complete mobilization of the kidney and thereby increase the possibility of adjacent structural damage. Obese patients, especially those with a body mass index ⬎35 kg/m2, increase the difficulty of appropriate robotic setup and could limit the range of motion available. Kidneys with multiple renal masses can require longer WIT or portions of the procedure to be performed under normal renal perfusion. Tumors located at the upper pole, especially on the right side, increase the risk of pneumothorax and hepatic injury. Finally, patients who have undergone previous surgery to the abdominal or renal vasculature could have extensive scar formation, limiting the ability to adequately occlude the renal hilum. To our knowledge, the present study represents the largest report of RPN for complex masses as defined by the R.E.N.A.L. nephrometry score and has strengthened the growing evidence that RPN is feasible and can be performed safely and adequately, even for challenging renal masses. Our surgical technique evolved during the study period. We no longer use bolsters and instead prefer sliding clip renorrhaphy in a horizontal mattress fashion. Additionally, we prefer to almost exclusively use bulldog clamps for hilar occlusion to avoid an additional laparoscopic port. We do not currently alter our surgical approach according to the R.E.N.A.L. nephrometry score; however, we are gathering data, with the ultimate goal of the construction of an algorithm that can be used for patient counseling and tailored treatment planning. We do recognize that complex renal tumors that would require intracorporeal cooling require open partial nephrectomy. The limitations of the present study included the small sample size, short follow-up period, and retrospective nature.
CONCLUSIONS RPN is safe and feasible for patients with moderate to highly complex renal masses, as defined by a score of ⱖ7 using the R.E.N.A.L. nephrometry score. The risk of adverse outcomes will be increased for patients with a nephrometry score of ⱖ10. Larger studies and long-term follow-up are needed to determine efficacy of renal function preservation and oncologic adequacy. References 1. Uzzo RG, Novick AC. Nephron sparing surgery for renal tumors: indications, techniques and outcomes. J Urol. 2001;166:6-18. 2. Gill IS, Kavoussi LR, Lane BR, et al. Comparison of 1800 laparoscopic and open partial nephrectomies for single renal tumors. J Urol. 2007;178:41-46. 3. Ho H, Schwentner C, Neururer R, et al. Robotic-assisted laparoscopic partial nephrectomy: surgical technique and clinical outcomes at 1 year. BJU Int. 2009;103:663-668. 4. Michli EE, Parra RO. Robotic-assisted laparoscopic partial nephrectomy: initial clinical experience. Urology. 2009;73:302-305.
UROLOGY 77 (4), 2011
5. Wang AJ, Bhayani SB. Robotic partial nephrectomy versus laparoscopic partial nephrectomy for renal cell carcinoma: single-surgeon analysis of ⬎100 consecutive procedures. Urology. 2009;73:306-310. 6. Gong Y, Du C, Josephson DY, et al. Four-arm robotic partial nephrectomy for complex renal cell carcinoma. World J Urol. 2010;28:111-115. 7. Mottrie A, Koliakos N, DeNaeyer G, et al. Tumor enucleoresection in robot-assisted partial nephrectomy. J Robotic Surg. 2009;3:65-69. 8. Patel MN, Kaul SA, Laungani R, et al. Retroperitoneal robotic renal surgery: technique and early results. J Robotic Surg. 2009;3:1-5. 9. Kaouk JH, Goel RK. Single-port laparoscopic and robotic partial nephrectomy. Eur Urol. 2009;55:1163-1170. 10. Stein RJ, White WM, Goel RK, et al. Robotic laparoendoscopic single-site surgery using GelPort as the access platform. Eur Urol. 2010;57:132-137. 11. Nadler RB, Perry K, Smith N. Hybrid laparoscopic and robotic ultrasound-guided radiofrequency ablation-assisted clampless partial nephrectomy. Urology. 2009;74:202-205. 12. Benway BM, Wang AJ, Cabello JM, et al. Robotic partial nephrectomy with sliding-clip renorrhaphy: technique and outcomes. Eur Urol. 2009;55:592-599. 13. Benway BM, Bhayani SB, Rogers CG, et al. Robot assisted partial nephrectomy versus laparoscopic partial nephrectomy for renal tumors: a multi-institutional analysis of perioperative outcomes. J Urol. 2009;182:866-872. 14. Patel MN, Krane LS, Bhandari A, et al. Robotic partial nephrectomy for renal tumors larger than 4cm. Eur Urol. 2010;57:310-316. 15. Rogers CG, Singh A, Blatt AM, et al. Robotic partial nephrectomy for complex renal tumors: surgical technique. Eur Urol. 2008;53:514-523. 16. Rogers CG, Metwalli A, Blatt AM, et al. Robotic partial nephrectomy for renal hilar tumors: a multi-institutional analysis. J Urol. 2008;180:2353-2356. 17. 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;182:844-853. 18. Kenney P, Kozinn S, Wszolek M, et al. Interobserver reliability of the RENAL nephrometry scoring system. J Urol. 2010;183:e205-e206. 19. Hayn M, Schwaab T, Underwood W, et al. Application of the R.E.N.A.L. nephrometry score to laparoscopic partial nephrectomy. J Urol. 2010;183:e245. 20. Gettman MT, Blute ML, Chow GK, et al. Robotic-assisted laparoscopic partial nephrectomy: technique and initial clinical experience with da Vinci robotic system. Urology. 2004;64:914-918. 21. Phillips CK, Taneja SS, Stifelman MD. Robot-assisted laparoscopic partial nephrectomy: the NYU technique. J Endourol. 2005;19:441-445. 22. Kaul S, Laungani R, Sarle R, et al. da Vinci-assisted robotic partial nephrectomy: technique and results at a mean of 15 months of follow-up. Eur Urol. 2007;51:186-192. 23. Caruso RP, Phillips CK, Kau E, et al. Robot assisted laparoscopic partial nephrectomy: initial experience. J Urol. 2006;176:36-39. 24. Rogers CG, Menon M, Weise ES, et al. Robotic partial nephrectomy: a multi-institutional analysis. J Robotic Surg. 2008;2:141-143. 25. Bhayani SB, Das N. Robotic assisted laparoscopic partial nephrectomy for suspected renal cell carcinoma: retrospective review of surgical outcomes of 35 cases. BMC Surg. 2008;8:16-19. 26. Aron M, Koenig P, Kaouk J, et al. Robotic and laparoscopic partial nephrectomy: a matched-pair comparison from a high-volume centre. BJU Int. 2008;102:86-92. 27. Ho H, Peschel R, Neururer R, et al. Another novel application of Hem-o-Lok clips for transient vascular occlusion in robot-assisted laparoscopic partial nephrectomy: an alternative to laparoscopic bulldog and satinsky clamps. J Endourol. 2008;22:1677-1680. 28. Deane LA, Lee H, Box G, et al. Robotic versus standard laparoscopic partial/wedge nephrectomy: a comparison of intraoperative and perioperative results from a single institution. J Endourol. 2008;22:947-952. 29. Park SY, Ham WS, Jung HJ, et al. Robot-assisted laparoscopic partial nephrectomy during pregnancy. J Robotic Surg. 2008;2:193-195. 30. Nguyen MM, Gill IS. Halving ischemia time during laparoscopic partial nephrectomy. J Urol. 2008;179:627-632.
813
RESULTS
CONCLUSIONS
To evaluate the safety and feasibility of robotic partial nephrectomy for patients with complex renal masses. We reviewed the data for 164 consecutive patients who had undergone transperitoneal robotic partial nephrectomy at a tertiary care center from February 2007 to June 2010. Of the 112 patients who had available imaging studies to review, 67 were identified and classified as having a moderately or highly complex renal mass according to the R.E.N.A.L. nephrometry score (ⱖ7) (tumor size—[R]adius, location and depth—[E]xophytic or endophytic; nearness to the renal sinus fat or collecting system [N]; anterior or posterior position [A], and polar vs non-polar location [L]). The preoperative, perioperative, pathologic, and functional outcomes data were analyzed. The median body mass index was 29.6 kg/m2 (range 19.9-44.8). Of the 67 patients, 32 were men and 35 were women, with 32 right-sided masses and 35 left-sided masses. The median tumor size was 3.7 cm (range 1.2-11), and the median operative time was 180 minutes (range 150-180). The median estimated blood loss was 200 mL (range 100-375), and the warm ischemia time was 19.0 minutes (range 15-26). The median hospital stay was 3.0 days (range 3-4). The estimated glomerular filtration rate was calculated at a median decrease of 11.1 mL/min/1.73 m2 (range 9-1.3). According to the Clavien-Dindo classification of surgical complications, 2 grade 1, 12 grade 2, and 1 grade 3 complication occurred. All margins were pathologically negative, except for 1, and, after a mean follow-up of 10 months, no recurrences had developed. Robotic partial nephrectomy is a safe and feasible option for moderately or highly complex renal masses determined by the R.E.N.A.L. nephrometry score. The warm ischemia time, blood loss, and complications were increased with highly complex masses. UROLOGY 77: 809 – 813, 2011. © 2011 Elsevier Inc.
T
he expansion of minimally invasive techniques has allowed laparoscopic partial nephrectomy to be performed for small renal masses with oncologic and functional outcomes comparable to those of open partial nephrectomy.1,2 Robotic-assisted laparoscopy allows for improved dexterity, increased visualization, tremor filtration, and an ergonomic setting to enhance surgeon comfort. Experience with robotic partial nephrectomy (RPN) continues to grow, and ⬎300 cases have been reported in 2009 and 2010 alone.3-14 The indications for RPN have expanded to include the treatment of “complex” renal masses. The
G.-P. Haber is a speaker for Intuitive Surgical; R. J. Stein is a speaker for Applied Medical; and J. H. Kaouk is a speaker for Intuitive Surgical and Covidien. From the Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio Reprint requests: Jihad H Kaouk, M.D., Department of Surgery, Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute, 9500 Euclid Avenue, Q-10, Cleveland, OH 44195. E-mail: [email protected] Submitted: October 8, 2010, accepted (with revisions): December 5, 2010
© 2011 Elsevier Inc. All Rights Reserved
available studies to date have had to rely solely on single tumor features to define masses as “complex,” including, for example, location (hilar), growth pattern (endophytic), and number of lesions (multiple).6,15,16 We report on our single-surgeon experience with RPN in patients with moderate and highly complex renal masses. In an attempt to characterize the renal tumor anatomy in a reproducible and quantifiable manner, we elected to use the recently developed and externally validated, R.E.N.A.L. nephrometry score to designate renal masses as “complex” in nature.17-19 The scoring system considers the Radius (tumor size), Exophytic or endophytic (location and depth), Nearness to the renal sinus fat or collecting system, Anterior or posterior position, and Location (polar vs nonpolar).
MATERIAL AND METHODS From February 2007 to June 2010, 164 patients had undergone RPN. The patient data were entered prospectively into our 0090-4295/11/$36.00 doi:10.1016/j.urology.2010.12.005
809
Table 1. Patient demographic data Variable
Value
Patients (n) Tumors resected (n) Age (y) Median Range Sex (n) Male Female Body mass index (kg/m2) Median Range Preoperative serum creatinine (mg/dL) Median Range Preoperative GFR (mL/min/1.73 m2) Median Range Side of involvement (n) Right Left R.E.N.A.L. score 7-9 ⱖ10
67 67 60.0 35-88 32 35 29.6 19.9-44.8 0.92 0.51-2.58 75.3 26.6-148.9 32 35 56 11
GFR, glomerular filtration rate; R.E.N.A.L., Radius (tumor size), Exophytic or endophytic (location and depth), Nearness to renal sinus fat or collecting system, Anterior or posterior position, and Location (polar vs nonpolar).
institutional review board-approved RPN database. Of the 164 patients, the films for 52 patients were not accessible either because of missing hard copies (returned to the patients) or an inability to access them from our electronic system. A total of 112 patients had computed tomography scans available for review, and 6 were excluded because of multiple masses in a single renal unit. The patient demographic data for those who had undergone RPN are summarized in Table 1. The R.E.N.A.L. nephrometry score was applied by 2 urology fellows independently and in consensus when differences occurred, and 67 patients with a score of ⱖ7 were identified as having a moderate or highly complex renal mass. The nephrometry score was determined by 5 reproducible and important features that characterize the renal tumor anatomic attributes as they apply to surgical resectability.17 Of the 5 components, 4 are scored from 1 to 3 points, and a cumulative total is assigned. The fifth component is used to designate whether the renal mass is anteriorly or posteriorly located. Scores of 4-6 are representative of low complexity masses and scores of 7-9 moderately complex, and scores of 10-12 highly complex. The nephrometry score and each of its elements are detailed in Table 2. The perioperative outcome data, including estimated blood loss (EBL), operative time, warm ischemia time (WIT), length of stay (LOS), change in creatinine and estimated glomerular filtration rate from preoperatively to postoperative day 3, complications, and conversion to open surgery were recorded. Additionally, a subset analysis was performed to evaluate the perioperative outcomes between patients with moderate and highly complex masses and those with lower complexity masses.
Statistical Analysis The Statistical Package for Social Sciences (SPSS, Chicago, IL) was used to perform all statistical analyses. Statistical significance was set at P ⱕ .5. Descriptive analyses were performed to 810
Table 2. Patient distribution according to R.E.N.A.L. nephrometry score parameters Patients (n)
Score Parameters R (maximal diameter; cm) ⱕ4 (1 point) ⬎4 but ⬍7 (2 points) ⱖ7 (3 points) E (exophicity) ⱖ50% (1 point) ⬍50% (2 points) Entirely endophytic (3 points) N (nearness of tumor to collecting system or sinus; mm) ⱖ7 (1 point) ⬎4 but ⬍7 (2 points) ⱕ4 (3 points) A (anterior vs posterior) Anterior Posterior Indeterminate L (location relative to polar lines) Entirely above upper or below lower polar line (1 point) Lesion crosses polar line (2 points) ⬎50% of mass crosses polar line or axial renal midline or is entirely between polar lines (3 points)
43 19 5 5 59 3 6 6 55 28 33 6 18 16 33
Scores of 4-6 represent low complexity masses, scores of 7-9 considered moderately complex, and scores of 10-12 highly complex.
describe the characteristics of the patient sample (median, standard deviation, percentages, and frequencies). The Wilcoxon rank-sum test and Fisher’s exact test were used to compare the outcomes between the 2 subset analyses.
Surgical Technique Positioning and Port Placement. The patient was positioned in the modified flank position at approximately 60°. The table was flexed and positioned in a slight Trendelenburg position. The abdomen was insufflated to 15 mm Hg with a Veress needle at the lateral border of the rectus muscle across from the twelfth rib and served as the site for a 12-mm port and the standard robotic telescope. An 8-mm robotic port was placed at the lateral border of the ipsilateral rectus muscle, about 3 cm below the costal margin. A second 8-mm robotic port was placed about 5-7 cm cephalad to the anterior superior iliac spine. An assistant 12-mm port was placed along the lateral border of the rectus muscle in the lower abdominal quadrant. If additional retraction was needed on the right side to retract the liver, a 5-mm port was placed in the subxiphoid area. The robot was then positioned over the patient’s shoulder, with the camera oriented in line with the kidney. Bowel Mobilization. A 30° scope facing downward was used, along with the 8-mm Endowrist (Intuitive Surgical, Sunnyvale, CA) monopolar shears in the right hand and the 8-mm Endowrist Prograsp Grasper in the left hand. The peritoneum was sharply incised along the white line of Toldt. The bowel was mobilized medially, developing a plane anterior to Gerota’s fascia and posterior to the mesocolon. Dissection continued cephalad to mobilize the spleen or liver. UROLOGY 77 (4), 2011
Hilar Dissection and Control. Dissection proceeded along the psoas muscle with anterior elevation of the ureter and/or gonadal vein to identify the renal hilum. The hilum was cleared of all its attachments to allow for occlusion with either bulldog clamps or a satinsky clamp. The artery and vein should be completely dissected to achieve adequate occlusion for the bulldog clamps. The hilum was clamped en bloc if a satinsky clamp was used. Tumor Exposure and Ultrasound Identification. Gerota’s fascia was opened and dissection performed along the renal capsule until the mass was exposed. The fat was then cleared circumferentially around the mass, allowing for visualization of ⱖ1-2 cm of normal parenchyma for future renal reconstruction. All attempts should be made to leave the overlying Gerota’s fascia atop the mass to assist in histopathologic staging and also to use as a handle for retraction. The laparoscopic ultrasound probe was used to plan the excision margins. The renal capsule was scored to delineate the resection boundaries. Vasculature Control and Tumor Excision. Before hilar occlusion, 12.5 g of mannitol was given intravenously. The hilum was occluded and the tumor resected along the previously scored margin using cold scissors. The bedside assistant used suction to clear the resection bed and allow for improved visualization while applying slight counter retraction, as needed. Renal Reconstruction. An 8-in. 2-0 Vicryl suture on an SH-1 needle (Ethicon Endosurgery, Johnson & Johnson, Cincinnati, OH) with a knot and Hem-o-Lok clip (Teleflex Medical, Research Triangle Park, NC), fixed to the opposite end was used to place a running suture of the tumor excision bed to achieve hemostasis and closure of the collecting system. The hilum was unclamped, and the renal excision bed was inspected for hemostasis. The renal parenchyma defect was approximated using 0 Vicryl sutures on a CT-1 needle. These sutures were placed in a running horizontal mattress fashion and secured in place with Hem-o-Lok clips in a sliding technique. The defect was covered with oxidized cellulose (Surgicel, Johnson & Johnson, Somerville, NJ) and a fibrin sealant (Evicel, Johnson & Johnson) or (Vitagel, Orthovita, Malvern, PA). Specimen Extraction and Closure. The specimen was placed in a laparoscopic entrapment sac and removed from an extended lower quadrant port site. Care must be taken to make the extraction incision large enough to avoid fracturing the specimen, possibly preventing accurate histopathologic examination for margin status and staging. All 12-mm incisions were closed with 0 Vicryl suture using the Carter Thomason device. A drain was placed through a lower lateral port.
RESULTS A total of 67 patients who had undergone RPN for moderately or highly complex renal masses were included in the present study. The median tumor size was 3.7 cm (range 1.2-11), with a median operative time of 180 minutes (range 150-180). The median EBL was 200 mL (range 100-375), and the WIT was 19 minutes (range 15-26). The median hospital stay was 3.0 days (range 3-4). The overall results are detailed in Table 3. A total of 15 complications occurred. These were graded using UROLOGY 77 (4), 2011
Table 3. Summary of results Variable Operative time (min) Median IQR WIT (min) Median IQR EBL (mL) Median IQR Hospital stay (d) Median IQR Decrease in eGFR (mL/min/1.73 m2) Median IQR* Resected mass (cm) Mean Range Mass type (n) Clear cell renal cell carcinoma Papillary renal cell carcinoma Chromophobe renal cell carcinoma Unclassified renal cell carcinoma Oncocytoma Angiomyolipoma Benign cyst Metanephric adenoma Pathologic stage (n) T1a T1b T2 T3a Benign
Value 180 150-180 19 15-26 200 100-375 3.0 3-4 ⫺11.1 ⫺19 to ⫺1.3 3.7 1.2-11 45 5 2 3 4 3 4 1 38 11 2 4 12
IQR, interquartile range (25th to 75th percentile); WIT, warm ischemia time; EBL, estimated blood loss; eGFR, estimated glomerular filtration rate. * Between level at third postoperative day and preoperative level.
the Clavien-Dindo classification of surgical complications and included 1 grade 3 complication, 12 grade 2 complications, and 2 grade 1 complications. One surgical margin was positive on final pathologic evaluation, but no evidence was found of recurrence during 8 months of follow-up. The subset analysis comparing the perioperative outcomes between the groups demonstrated a statistically significant reduction in EBL, operative time, and WIT, in favor of the lower and moderately complex groups over the highly complex group. Statistically significant differences in perioperative outcomes were not demonstrated between the lower and moderately complex groups. The complete results are detailed in Table 4.
COMMENT Gettman et al20 were the first to report the use of the da Vinci surgical system (Intuitive Surgical) to assist in laparoscopic partial nephrectomy. They performed 13 procedures, and the mean size of the tumor resected was 3.5 cm, with a mean operative time of 215 minutes and a WIT of 22 minutes. The mean EBL was 170 mL, and 811
Table 4. Comparative outcomes among mild/least complex (score 4-6), moderate (score 7-9), and severe (score 10-12) groups Outcome EBL (mL) Operative time (min) WIT (min) Hospital stay (d) Difference in creatinine Difference in GFR Any complication
Mild (Score 4-6; n ⫽ 39)
Moderate (Score 7-9; n ⫽ 56)
Severe (Score 10-12; n ⫽ 11)
P Value
150 (100-300) 180 (150-190) 14 (0-17) 3 (3-4) 0.06 (⫺0.08 to 0.19) NA 8 (21)
150 (100-300) 175 (150-180) 17 (15-23) 3 (2-4) 0.09 (0.02-0.20) ⫺11.1 (⫺17.4 to ⫺2.3) 10 (18)
500 (300-525) 200 (180-225) 27 (21-33) 4 (3-5) 0.12 (0.02-0.31) ⫺11.7 (⫺20.7 to ⫺0.8) 5 (45)
.03* .02* ⬍.00001* .1 .2 — .1
NA, not applicable; other abbreviations as in Table 3. Data presented as median, with interquartile range in parentheses, or numbers, with percentages in parentheses. P value for differences among 3 groups, tested using Kruskal-Wallis test (continuous variables) or Fisher’s exact test (for any complication). * Greater values for severe group vs other 2 groups.
the mean LOS was 4.3 days. At 2-11 months of followup, no recurrence had been noted. Since then, ⬎24 reports have been published on the technique and specific institutions’ experience, totaling approximately 600 cases.3-16,20-29 Initially, the system was recommended for small anterior exophytic masses; however, as documentation regarding the safety and efficacy were amassed, the indications for using the da Vinci surgical system for partial nephrectomy were expanded. Rogers et al15 described their technique and results for RPN in 8 complex cases, including hilar tumors, endophytic tumors, and multiple tumors, with a total of 14 tumors resected. The mean tumor size resected was 3.6 cm, with a mean operative time of 192 minutes and a WIT of 31 minutes. The mean EBL was 230 mL, and the mean LOS was 2.6 days. All patients had negative surgical margins, and no tumor recurrence had been observed at a follow-up of 3 months. The investigators concluded that RPN is a safe and feasible approach for select patients with complex renal tumors.15 Additionally, Rogers et al16 reported on a multi-institutional analysis of RPN for renal hilar tumors. A total of 11 RPN procedures were performed for renal hilar tumors, defined as tumors abutting the renal artery and/or renal vein on preoperative imaging. The mean tumor size resected was 3.8 cm, with a mean operative time of 202 minutes and a WIT of 28.9 minutes. The mean EBL was 220 mL, and the mean LOS was 3 days.16 Recently, Gong et al6 reported on the outcomes of 29 patients, who had undergone RPN for renal masses, including hilar, endophytic, and multiple tumors. The mean tumor size resected was 3.0 cm, with a mean operative time of 197 minutes and a WIT of 25 minutes. The mean EBL was 220 mL, and the mean LOS was 2.5 days. All cases had negative surgical margins, and no recurrence was evident at a mean follow-up of 15 months.6 Our results were comparable to these previously published reports detailing RPN for complex masses; however, because these studies were performed before the R.E.N.A.L. nephrometry score was developed, exact comparisons could not be drawn. Patients with moderate or highly complex renal masses constituted ⬎50% of our patient population according to the R.E.N.A.L. 812
nephrometry score and was representative of our center’s tertiary care status. The median renal mass diameter, operative time, and EBL were similar to those published by Rogers et al15,16 and Gong et al6; however, our series had a shorter WIT at 19.0 minutes compared with 31.0, 28.9, and 25.0 minutes. The shorter WIT might have resulted from the early unclamping technique used during our initial deep layer renorrhaphy and described by Nguyen et al30 for use during standard laparoscopy or might have resulted from the sliding clip renorrhaphy technique, which allows for faster reconstruction.12 By performing a precise and detailed reconstruction of the collecting system and surrounding deep cortex, we were able to release the vasculature occlusion device without encountering significant hemorrhage. Whether a reduction in WIT will translate into long-term preservation of renal function has yet to be determined. Our follow-up data demonstrated renal function preservation and oncologic outcomes similar to those from previously published reports. The estimated glomerular filtration rate in our study was calculated at a median decrease of 11.1 mL/min/1.73 m2 compared with 5.6, 8.0, and 4.5 as documented by Rogers et al15,16 and Gong et al.6 At a mean follow-up of 10 months, we have not had evidence of tumor recurrence in any patient. When the perioperative outcomes were analyzed among the lower, moderately, and highly complex masses, significant differences were found in the EBL, operative time, and WIT, favoring the lower and moderately complex groups. This was not surprising and supported the findings by Hayn et al,19 regarding the application of the R.E.N.A.L. nephrometry score to LPN specimens. A total of 15 complications occurred, including in 12 patients who required transfusions (Clavien grade 2) and 1 who eventually required thoracostomy tube placement because of iatrogenic pneumothorax (Clavien grade 3b). The pneumothorax had occurred in 1 patient with a right-sided upper pole mass and resulted from diaphragmatic injury from the locking grasper used for liver retraction. No patients required angioembolization. One patient developed a contained urine leak that did not require intervention (Clavien grade 1), and one developed a prolonged ileus (4-7 days; Clavien grade 2) and was treated conservatively. UROLOGY 77 (4), 2011
Although the R.E.N.A.L. score can be helpful in evaluating the anatomic complexity of renal masses, it is important to acknowledge additional factors that can add to the difficulty of RPN. Posteriorly located tumors require nearly complete mobilization of the kidney and thereby increase the possibility of adjacent structural damage. Obese patients, especially those with a body mass index ⬎35 kg/m2, increase the difficulty of appropriate robotic setup and could limit the range of motion available. Kidneys with multiple renal masses can require longer WIT or portions of the procedure to be performed under normal renal perfusion. Tumors located at the upper pole, especially on the right side, increase the risk of pneumothorax and hepatic injury. Finally, patients who have undergone previous surgery to the abdominal or renal vasculature could have extensive scar formation, limiting the ability to adequately occlude the renal hilum. To our knowledge, the present study represents the largest report of RPN for complex masses as defined by the R.E.N.A.L. nephrometry score and has strengthened the growing evidence that RPN is feasible and can be performed safely and adequately, even for challenging renal masses. Our surgical technique evolved during the study period. We no longer use bolsters and instead prefer sliding clip renorrhaphy in a horizontal mattress fashion. Additionally, we prefer to almost exclusively use bulldog clamps for hilar occlusion to avoid an additional laparoscopic port. We do not currently alter our surgical approach according to the R.E.N.A.L. nephrometry score; however, we are gathering data, with the ultimate goal of the construction of an algorithm that can be used for patient counseling and tailored treatment planning. We do recognize that complex renal tumors that would require intracorporeal cooling require open partial nephrectomy. The limitations of the present study included the small sample size, short follow-up period, and retrospective nature.
CONCLUSIONS RPN is safe and feasible for patients with moderate to highly complex renal masses, as defined by a score of ⱖ7 using the R.E.N.A.L. nephrometry score. The risk of adverse outcomes will be increased for patients with a nephrometry score of ⱖ10. Larger studies and long-term follow-up are needed to determine efficacy of renal function preservation and oncologic adequacy. References 1. Uzzo RG, Novick AC. Nephron sparing surgery for renal tumors: indications, techniques and outcomes. J Urol. 2001;166:6-18. 2. Gill IS, Kavoussi LR, Lane BR, et al. Comparison of 1800 laparoscopic and open partial nephrectomies for single renal tumors. J Urol. 2007;178:41-46. 3. Ho H, Schwentner C, Neururer R, et al. Robotic-assisted laparoscopic partial nephrectomy: surgical technique and clinical outcomes at 1 year. BJU Int. 2009;103:663-668. 4. Michli EE, Parra RO. Robotic-assisted laparoscopic partial nephrectomy: initial clinical experience. Urology. 2009;73:302-305.
UROLOGY 77 (4), 2011
5. Wang AJ, Bhayani SB. Robotic partial nephrectomy versus laparoscopic partial nephrectomy for renal cell carcinoma: single-surgeon analysis of ⬎100 consecutive procedures. Urology. 2009;73:306-310. 6. Gong Y, Du C, Josephson DY, et al. Four-arm robotic partial nephrectomy for complex renal cell carcinoma. World J Urol. 2010;28:111-115. 7. Mottrie A, Koliakos N, DeNaeyer G, et al. Tumor enucleoresection in robot-assisted partial nephrectomy. J Robotic Surg. 2009;3:65-69. 8. Patel MN, Kaul SA, Laungani R, et al. Retroperitoneal robotic renal surgery: technique and early results. J Robotic Surg. 2009;3:1-5. 9. Kaouk JH, Goel RK. Single-port laparoscopic and robotic partial nephrectomy. Eur Urol. 2009;55:1163-1170. 10. Stein RJ, White WM, Goel RK, et al. Robotic laparoendoscopic single-site surgery using GelPort as the access platform. Eur Urol. 2010;57:132-137. 11. Nadler RB, Perry K, Smith N. Hybrid laparoscopic and robotic ultrasound-guided radiofrequency ablation-assisted clampless partial nephrectomy. Urology. 2009;74:202-205. 12. Benway BM, Wang AJ, Cabello JM, et al. Robotic partial nephrectomy with sliding-clip renorrhaphy: technique and outcomes. Eur Urol. 2009;55:592-599. 13. Benway BM, Bhayani SB, Rogers CG, et al. Robot assisted partial nephrectomy versus laparoscopic partial nephrectomy for renal tumors: a multi-institutional analysis of perioperative outcomes. J Urol. 2009;182:866-872. 14. Patel MN, Krane LS, Bhandari A, et al. Robotic partial nephrectomy for renal tumors larger than 4cm. Eur Urol. 2010;57:310-316. 15. Rogers CG, Singh A, Blatt AM, et al. Robotic partial nephrectomy for complex renal tumors: surgical technique. Eur Urol. 2008;53:514-523. 16. Rogers CG, Metwalli A, Blatt AM, et al. Robotic partial nephrectomy for renal hilar tumors: a multi-institutional analysis. J Urol. 2008;180:2353-2356. 17. 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;182:844-853. 18. Kenney P, Kozinn S, Wszolek M, et al. Interobserver reliability of the RENAL nephrometry scoring system. J Urol. 2010;183:e205-e206. 19. Hayn M, Schwaab T, Underwood W, et al. Application of the R.E.N.A.L. nephrometry score to laparoscopic partial nephrectomy. J Urol. 2010;183:e245. 20. Gettman MT, Blute ML, Chow GK, et al. Robotic-assisted laparoscopic partial nephrectomy: technique and initial clinical experience with da Vinci robotic system. Urology. 2004;64:914-918. 21. Phillips CK, Taneja SS, Stifelman MD. Robot-assisted laparoscopic partial nephrectomy: the NYU technique. J Endourol. 2005;19:441-445. 22. Kaul S, Laungani R, Sarle R, et al. da Vinci-assisted robotic partial nephrectomy: technique and results at a mean of 15 months of follow-up. Eur Urol. 2007;51:186-192. 23. Caruso RP, Phillips CK, Kau E, et al. Robot assisted laparoscopic partial nephrectomy: initial experience. J Urol. 2006;176:36-39. 24. Rogers CG, Menon M, Weise ES, et al. Robotic partial nephrectomy: a multi-institutional analysis. J Robotic Surg. 2008;2:141-143. 25. Bhayani SB, Das N. Robotic assisted laparoscopic partial nephrectomy for suspected renal cell carcinoma: retrospective review of surgical outcomes of 35 cases. BMC Surg. 2008;8:16-19. 26. Aron M, Koenig P, Kaouk J, et al. Robotic and laparoscopic partial nephrectomy: a matched-pair comparison from a high-volume centre. BJU Int. 2008;102:86-92. 27. Ho H, Peschel R, Neururer R, et al. Another novel application of Hem-o-Lok clips for transient vascular occlusion in robot-assisted laparoscopic partial nephrectomy: an alternative to laparoscopic bulldog and satinsky clamps. J Endourol. 2008;22:1677-1680. 28. Deane LA, Lee H, Box G, et al. Robotic versus standard laparoscopic partial/wedge nephrectomy: a comparison of intraoperative and perioperative results from a single institution. J Endourol. 2008;22:947-952. 29. Park SY, Ham WS, Jung HJ, et al. Robot-assisted laparoscopic partial nephrectomy during pregnancy. J Robotic Surg. 2008;2:193-195. 30. Nguyen MM, Gill IS. Halving ischemia time during laparoscopic partial nephrectomy. J Urol. 2008;179:627-632.
813