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Renal Cancer

Outcomes of RoboticPartial Nephrectomy for RenalMasses With Nephrometry Score of >7Michael A. White, Georges-Pascal Haber, Riccardo Autorino, Rakesh Khanna,Adrian V. Hernandez, Sylvain Forest, Bo Yang, Fatih Altunrende, Robert J. Stein, andJihad H. Kaouk

OBJECTIVES To evaluate the safety and feasibility of robotic partial nephrectomy for patients with complexrenal masses.

METHODS We reviewed the data for 164 consecutive patients who had undergone transperitoneal robotic partialnephrectomy at a tertiary care center from February 2007 to June 2010. Of the 112 patients who hadavailable imaging studies to review, 67 were identified and classified as having a moderately or highlycomplex renal mass according to the R.E.N.A.L. nephrometry score (�7) (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.

ESULTS The median body mass index was 29.6 kg/m2 (range 19.9-44.8). Of the 67 patients, 32 were menand 35 were women, with 32 right-sided masses and 35 left-sided masses. The median tumor sizewas 3.7 cm (range 1.2-11), and the median operative time was 180 minutes (range 150-180). Themedian estimated blood loss was 200 mL (range 100-375), and the warm ischemia time was 19.0minutes (range 15-26). The median hospital stay was 3.0 days (range 3-4). The estimatedglomerular filtration rate was calculated at a median decrease of 11.1 mL/min/1.73 m2 (range9-1.3). According to the Clavien-Dindo classification of surgical complications, 2 grade 1, 12grade 2, and 1 grade 3 complication occurred. All margins were pathologically negative, exceptfor 1, and, after a mean follow-up of 10 months, no recurrences had developed.

CONCLUSIONS Robotic partial nephrectomy is a safe and feasible option for moderately or highly complex renal massesdetermined 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.

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The expansion of minimally invasive techniqueshas allowed laparoscopic partial nephrectomy tobe performed for small renal masses with onco-

logic and functional outcomes comparable to those ofopen partial nephrectomy.1,2

Robotic-assisted laparoscopy allows for improved dex-terity, increased visualization, tremor filtration, and anergonomic setting to enhance surgeon comfort. Experi-ence with robotic partial nephrectomy (RPN) continuesto grow, and �300 cases have been reported in 2009 and2010 alone.3-14 The indications for RPN have expandedo include the treatment of “complex” renal masses. The

G.-P. Haber is a speaker for Intuitive Surgical; R. J. Stein is a speaker for AppliedMedical; 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 Lapa-roscopic and Robotic Surgery, Glickman Urological and Kidney Institute, 9500 Euclid

Avenue, Q-10, Cleveland, OH 44195. E-mail: kaoukj@ccf.org

Submitted: October 8, 2010, accepted (with revisions): December 5, 2010

© 2011 Elsevier Inc.All Rights Reserved

vailable studies to date have had to rely solely on singleumor features to define masses as “complex,” including,or example, location (hilar), growth pattern (endo-hytic), and number of lesions (multiple).6,15,16

We report on our single-surgeon experience with RPNin patients with moderate and highly complex renalmasses. In an attempt to characterize the renal tumoranatomy in a reproducible and quantifiable manner, weelected to use the recently developed and externallyvalidated, R.E.N.A.L. nephrometry score to designaterenal masses as “complex” in nature.17-19 The scoringsystem considers the Radius (tumor size), Exophytic orendophytic (location and depth), Nearness to the renalsinus fat or collecting system, Anterior or posterior posi-tion, 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 809doi:10.1016/j.urology.2010.12.005

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institutional review board-approved RPN database. Of the 164patients, the films for 52 patients were not accessible eitherbecause of missing hard copies (returned to the patients) or aninability to access them from our electronic system. A total of112 patients had computed tomography scans available forreview, and 6 were excluded because of multiple masses in asingle renal unit. The patient demographic data for those whohad undergone RPN are summarized in Table 1. The R.E.N.A.L.nephrometry score was applied by 2 urology fellows indepen-dently and in consensus when differences occurred, and 67patients with a score of �7 were identified as having a moderater highly complex renal mass. The nephrometry score wasetermined by 5 reproducible and important features that char-cterize the renal tumor anatomic attributes as they apply tourgical resectability.17 Of the 5 components, 4 are scored from

1 to 3 points, and a cumulative total is assigned. The fifthcomponent is used to designate whether the renal mass isanteriorly or posteriorly located. Scores of 4-6 are representativeof low complexity masses and scores of 7-9 moderately complex,and scores of 10-12 highly complex. The nephrometry score andeach of its elements are detailed in Table 2.

The perioperative outcome data, including estimated bloodloss (EBL), operative time, warm ischemia time (WIT), lengthof stay (LOS), change in creatinine and estimated glomerularfiltration rate from preoperatively to postoperative day 3, com-plications, and conversion to open surgery were recorded. Ad-ditionally, a subset analysis was performed to evaluate theperioperative outcomes between patients with moderate andhighly complex masses and those with lower complexity masses.

Statistical AnalysisThe Statistical Package for Social Sciences (SPSS, Chicago, IL)was used to perform all statistical analyses. Statistical signifi-

Table 1. Patient demographic data

Variable Value

Patients (n) 67Tumors resected (n) 67Age (y)

Median 60.0Range 35-88

Sex (n)Male 32Female 35

Body mass index (kg/m2)Median 29.6Range 19.9-44.8

Preoperative serum creatinine (mg/dL)Median 0.92Range 0.51-2.58

Preoperative GFR (mL/min/1.73 m2)Median 75.3Range 26.6-148.9

Side of involvement (n)Right 32Left 35

R.E.N.A.L. score7-9 56�10 11

GFR, glomerular filtration rate; R.E.N.A.L., Radius (tumor size),Exophytic or endophytic (location and depth), Nearness to renalsinus fat or collecting system, Anterior or posterior position, andLocation (polar vs nonpolar).

cance was set at P � .5. Descriptive analyses were performed to

810

describe the characteristics of the patient sample (median,standard deviation, percentages, and frequencies). The Wil-coxon rank-sum test and Fisher’s exact test were used to com-pare the outcomes between the 2 subset analyses.

Surgical TechniquePositioning and Port Placement. The patient was positioned inthe modified flank position at approximately 60°. The table wasflexed and positioned in a slight Trendelenburg position. Theabdomen was insufflated to 15 mm Hg with a Veress needle atthe lateral border of the rectus muscle across from the twelfthrib and served as the site for a 12-mm port and the standardrobotic telescope. An 8-mm robotic port was placed at thelateral border of the ipsilateral rectus muscle, about 3 cm belowthe costal margin. A second 8-mm robotic port was placedabout 5-7 cm cephalad to the anterior superior iliac spine. Anassistant 12-mm port was placed along the lateral border of therectus muscle in the lower abdominal quadrant. If additionalretraction was needed on the right side to retract the liver, a5-mm port was placed in the subxiphoid area. The robot wasthen positioned over the patient’s shoulder, with the cameraoriented 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 En-dowrist Prograsp Grasper in the left hand. The peritoneum wassharply incised along the white line of Toldt. The bowel wasmobilized medially, developing a plane anterior to Gerota’sfascia and posterior to the mesocolon. Dissection continued

Table 2. Patient distribution according to R.E.N.A.L.nephrometry score parameters

Score ParametersPatients

(n)

R (maximal diameter; cm)�4 (1 point) 43�4 but �7 (2 points) 19�7 (3 points) 5

E (exophicity)�50% (1 point) 5�50% (2 points) 59Entirely endophytic (3 points) 3

N (nearness of tumor to collecting systemor sinus; mm)

�7 (1 point) 6�4 but �7 (2 points) 6�4 (3 points) 55

A (anterior vs posterior)Anterior 28Posterior 33Indeterminate 6

L (location relative to polar lines)Entirely above upper or below lower polar

line (1 point)18

Lesion crosses polar line (2 points) 16�50% of mass crosses polar line or axial

renal midline or is entirely betweenpolar lines (3 points)

33

Scores of 4-6 represent low complexity masses, scores of 7-9considered moderately complex, and scores of 10-12 highly com-plex.

cephalad to mobilize the spleen or liver.

UROLOGY 77 (4), 2011

Hilar Dissection and Control. Dissection proceeded along thepsoas muscle with anterior elevation of the ureter and/or go-nadal vein to identify the renal hilum. The hilum was clearedof all its attachments to allow for occlusion with either bulldogclamps or a satinsky clamp. The artery and vein should becompletely dissected to achieve adequate occlusion for thebulldog clamps. The hilum was clamped en bloc if a satinskyclamp was used.

Tumor Exposure and Ultrasound Identification. Gerota’s fas-cia was opened and dissection performed along the renal cap-sule until the mass was exposed. The fat was then clearedcircumferentially around the mass, allowing for visualization of�1-2 cm of normal parenchyma for future renal reconstruction.All attempts should be made to leave the overlying Gerota’sfascia atop the mass to assist in histopathologic staging and alsoto use as a handle for retraction. The laparoscopic ultrasoundprobe was used to plan the excision margins. The renal capsulewas scored to delineate the resection boundaries.

Vasculature Control and Tumor Excision. Before hilar occlu-sion, 12.5 g of mannitol was given intravenously. The hilumwas occluded and the tumor resected along the previouslyscored margin using cold scissors. The bedside assistant usedsuction to clear the resection bed and allow for improvedvisualization while applying slight counter retraction, asneeded.

Renal Reconstruction. An 8-in. 2-0 Vicryl suture on an SH-1needle (Ethicon Endosurgery, Johnson & Johnson, Cincinnati,OH) with a knot and Hem-o-Lok clip (Teleflex Medical, Re-search Triangle Park, NC), fixed to the opposite end was usedto place a running suture of the tumor excision bed to achievehemostasis and closure of the collecting system. The hilum wasunclamped, and the renal excision bed was inspected for he-mostasis. The renal parenchyma defect was approximated using0 Vicryl sutures on a CT-1 needle. These sutures were placed ina running horizontal mattress fashion and secured in place withHem-o-Lok clips in a sliding technique. The defect was coveredwith oxidized cellulose (Surgicel, Johnson & Johnson, Somer-ville, NJ) and a fibrin sealant (Evicel, Johnson & Johnson) or(Vitagel, Orthovita, Malvern, PA).

Specimen Extraction and Closure. The specimen was placed ina laparoscopic entrapment sac and removed from an extendedlower quadrant port site. Care must be taken to make theextraction incision large enough to avoid fracturing the speci-men, possibly preventing accurate histopathologic examinationfor margin status and staging. All 12-mm incisions were closedwith 0 Vicryl suture using the Carter Thomason device. A drainwas placed through a lower lateral port.

RESULTSA total of 67 patients who had undergone RPN formoderately or highly complex renal masses were includedin the present study. The median tumor size was 3.7 cm(range 1.2-11), with a median operative time of 180minutes (range 150-180). The median EBL was 200 mL(range 100-375), and the WIT was 19 minutes (range15-26). The median hospital stay was 3.0 days (range3-4). The overall results are detailed in Table 3. A total

of 15 complications occurred. These were graded using

UROLOGY 77 (4), 2011

the Clavien-Dindo classification of surgical complica-tions and included 1 grade 3 complication, 12 grade 2complications, and 2 grade 1 complications. One surgicalmargin was positive on final pathologic evaluation, butno evidence was found of recurrence during 8 months offollow-up.

The subset analysis comparing the perioperative out-comes between the groups demonstrated a statisticallysignificant reduction in EBL, operative time, and WIT, infavor of the lower and moderately complex groups overthe highly complex group. Statistically significant differ-ences in perioperative outcomes were not demonstratedbetween the lower and moderately complex groups. Thecomplete results are detailed in Table 4.

COMMENTGettman et al20 were the first to report the use of the daVinci surgical system (Intuitive Surgical) to assist inlaparoscopic partial nephrectomy. They performed 13procedures, and the mean size of the tumor resected was3.5 cm, with a mean operative time of 215 minutes and

Table 3. Summary of results

Variable Value

Operative time (min)Median 180IQR 150-180

WIT (min)Median 19IQR 15-26

EBL (mL)Median 200IQR 100-375

Hospital stay (d)Median 3.0IQR 3-4

Decrease in eGFR (mL/min/1.73 m2)Median �11.1IQR* �19 to �1.3

Resected mass (cm)Mean 3.7Range 1.2-11

Mass type (n)Clear cell renal cell carcinoma 45Papillary renal cell carcinoma 5Chromophobe renal cell carcinoma 2Unclassified renal cell carcinoma 3Oncocytoma 4Angiomyolipoma 3Benign cyst 4Metanephric adenoma 1

Pathologic stage (n)T1a 38T1b 11T2 2T3a 4Benign 12

IQR, interquartile range (25th to 75th percentile); WIT, warmischemia time; EBL, estimated blood loss; eGFR, estimated glo-merular filtration rate.* Between level at third postoperative day and preoperative level.

a WIT of 22 minutes. The mean EBL was 170 mL, and

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the mean LOS was 4.3 days. At 2-11 months of follow-up, no recurrence had been noted.

Since then, �24 reports have been published on theechnique and specific institutions’ experience, totalingpproximately 600 cases.3-16,20-29 Initially, the system was

recommended for small anterior exophytic masses; how-ever, as documentation regarding the safety and efficacywere amassed, the indications for using the da Vincisurgical system for partial nephrectomy were expanded.

Rogers et al15 described their technique and results forPN in 8 complex cases, including hilar tumors, endo-hytic tumors, and multiple tumors, with a total of 14umors resected. The mean tumor size resected was 3.6m, with a mean operative time of 192 minutes and a

IT of 31 minutes. The mean EBL was 230 mL, and theean LOS was 2.6 days. All patients had negative sur-

ical margins, and no tumor recurrence had been ob-erved at a follow-up of 3 months. The investigatorsoncluded that RPN is a safe and feasible approach forelect patients with complex renal tumors.15

Additionally, Rogers et al16 reported on a multi-insti-tutional analysis of RPN for renal hilar tumors. A total of11 RPN procedures were performed for renal hilar tu-mors, defined as tumors abutting the renal artery and/orrenal vein on preoperative imaging. The mean tumor sizeresected was 3.8 cm, with a mean operative time of 202minutes and a WIT of 28.9 minutes. The mean EBL was220 mL, and the mean LOS was 3 days.16

Recently, Gong et al6 reported on the outcomes of 29patients, who had undergone RPN for renal masses, in-cluding hilar, endophytic, and multiple tumors. Themean tumor size resected was 3.0 cm, with a mean oper-ative time of 197 minutes and a WIT of 25 minutes. Themean EBL was 220 mL, and the mean LOS was 2.5 days.All cases had negative surgical margins, and no recur-rence was evident at a mean follow-up of 15 months.6

Our results were comparable to these previously pub-lished reports detailing RPN for complex masses; how-ever, because these studies were performed before theR.E.N.A.L. nephrometry score was developed, exactcomparisons could not be drawn. Patients with moderateor highly complex renal masses constituted �50% of

Table 4. Comparative outcomes among mild/least complex (s

OutcomeMild

(Score 4-6; n � 39) (Sc

EBL (mL) 150 (100-300) 15Operative time (min) 180 (150-190) 17WIT (min) 14 (0-17) 1Hospital stay (d) 3 (3-4)Difference in creatinine 0.06 (�0.08 to 0.19) 0.0Difference in GFR NA �11.Any complication 8 (21) 1

NA, not applicable; other abbreviations as in Table 3.Data presented as median, with interquartile range in parentheP value for differences among 3 groups, tested using Krusk

complication).* Greater values for severe group vs other 2 groups.

our patient population according to the R.E.N.A.L. d

812

nephrometry score and was representative of our center’stertiary care status. The median renal mass diameter,operative time, and EBL were similar to those publishedby Rogers et al15,16 and Gong et al6; however, our serieshad a shorter WIT at 19.0 minutes compared with 31.0,28.9, and 25.0 minutes. The shorter WIT might haveresulted from the early unclamping technique used duringour initial deep layer renorrhaphy and described byNguyen et al30 for use during standard laparoscopy ormight have resulted from the sliding clip renorrhaphytechnique, which allows for faster reconstruction.12 Byperforming a precise and detailed reconstruction of thecollecting system and surrounding deep cortex, we wereable to release the vasculature occlusion device withoutencountering significant hemorrhage. Whether a reduc-tion in WIT will translate into long-term preservation ofrenal function has yet to be determined.

Our follow-up data demonstrated renal function pres-ervation and oncologic outcomes similar to those frompreviously published reports. The estimated glomerularfiltration rate in our study was calculated at a mediandecrease 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 etal.6 At a mean follow-up of 10 months, we have not hadevidence of tumor recurrence in any patient.

When the perioperative outcomes were analyzed amongthe lower, moderately, and highly complex masses, signifi-cant differences were found in the EBL, operative time, andWIT, favoring the lower and moderately complex groups.This was not surprising and supported the findings by Haynet al,19 regarding the application of the R.E.N.A.L.

ephrometry score to LPN specimens.A total of 15 complications occurred, including in 12

atients who required transfusions (Clavien grade 2) and 1ho eventually required thoracostomy tube placement be-ause of iatrogenic pneumothorax (Clavien grade 3b). Theneumothorax had occurred in 1 patient with a right-sidedpper pole mass and resulted from diaphragmatic injuryrom the locking grasper used for liver retraction. No pa-ients required angioembolization. One patient developed aontained urine leak that did not require intervention (Cla-ien grade 1), and one developed a prolonged ileus (4-7

4-6), moderate (score 7-9), and severe (score 10-12) groups

derate-9; n � 56)

Severe(Score 10-12; n � 11) P Value

0-300) 500 (300-525) .03*0-180) 200 (180-225) .02*-23) 27 (21-33) �.00001*

4) 4 (3-5) .102-0.20) 0.12 (0.02-0.31) .217.4 to �2.3) �11.7 (�20.7 to �0.8) —) 5 (45) .1

or numbers, with percentages in parentheses.llis test (continuous variables) or Fisher’s exact test (for any

core

Moore 7

0 (105 (157 (153 (2-9 (0.1 (�0 (18

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ays; Clavien grade 2) and was treated conservatively.

UROLOGY 77 (4), 2011

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Although the R.E.N.A.L. score can be helpful in evalu-ating the anatomic complexity of renal masses, it is impor-tant to acknowledge additional factors that can add to thedifficulty of RPN. Posteriorly located tumors require nearlycomplete mobilization of the kidney and thereby increasethe possibility of adjacent structural damage. Obese patients,especially those with a body mass index �35 kg/m2, increasethe difficulty of appropriate robotic setup and could limitthe range of motion available. Kidneys with multiple renalmasses can require longer WIT or portions of the procedureto be performed under normal renal perfusion. Tumorslocated at the upper pole, especially on the right side,increase the risk of pneumothorax and hepatic injury. Fi-nally, patients who have undergone previous surgery to theabdominal or renal vasculature could have extensive scarformation, limiting the ability to adequately occlude therenal hilum.

To our knowledge, the present study represents the larg-est report of RPN for complex masses as defined by theR.E.N.A.L. nephrometry score and has strengthened thegrowing evidence that RPN is feasible and can be performedsafely and adequately, even for challenging renal masses.Our surgical technique evolved during the study period. Weno longer use bolsters and instead prefer sliding clip renor-rhaphy in a horizontal mattress fashion. Additionally, weprefer to almost exclusively use bulldog clamps for hilarocclusion to avoid an additional laparoscopic port. We donot currently alter our surgical approach according to theR.E.N.A.L. nephrometry score; however, we are gatheringdata, with the ultimate goal of the construction of analgorithm that can be used for patient counseling and tai-lored treatment planning. We do recognize that complexrenal tumors that would require intracorporeal cooling re-quire open partial nephrectomy. The limitations of thepresent study included the small sample size, short follow-upperiod, and retrospective nature.

CONCLUSIONSRPN is safe and feasible for patients with moderate tohighly complex renal masses, as defined by a score of �7sing the R.E.N.A.L. nephrometry score. The risk ofdverse outcomes will be increased for patients with aephrometry score of �10. Larger studies and long-term

ollow-up are needed to determine efficacy of renal func-ion preservation and oncologic adequacy.

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