Surgical Techniques Robotic Versus Laparoscopic Partial Nephrectomy: Single-surgeon Matched Cohort Study of 150 Patients Georges-Pascal Haber, Wesley M. White, Sebastien Crouzet, Michael A. White, Sylvain Forest, Riccardo Autorino, and Jihad H. Kaouk OBJECTIVES
To present comparative outcomes among matched patients who underwent robotic partial nephrectomy (RPN) or laparoscopic partial nephrectomy (LPN) by a single surgeon at a single institution. Between March 2002 and August 2009, a retrospective review of 261 consecutive patients who underwent LPN (n ⫽ 186) or RPN (n ⫽ 75) by a single surgeon was performed. Patients were matched for age, gender, body mass index (BMI), American Society of Anesthesiologists (ASA) score, and tumor size, side, and location. Perioperative outcomes were compared. A matched cohort of 150 patients who underwent RPN (n ⫽ 75) or LPN (n ⫽ 75) were compared. There was no significant difference between the 2 cohorts with respect to patient age (P ⫽ .17), BMI (P ⫽ .68), ASA score (P ⫽ .96), preoperative estimated glomerulofiltration rate (eGFR; P ⫽ .54), or tumor size (P ⫽ .17). Mean operative time for RPN was 200 vs 197 minutes for LPN (P ⫽ .75). Mean estimated blood loss (EBL) was higher in the RPN cohort (323 vs 222 mL, P ⫽ .01). There was no significant difference with respect to warm ischemia time (18.2 minutes vs 20.3 minutes, P ⫽ .27), length of hospitalization (P ⫽ .84), percent change in eGFR (P ⫽ .80), or adverse events (P ⫽ .52). All surgical margins were negative. Although initial surgical experience with RPN was included in this study and compared with a vast experience in LPN by the same surgeon, RPN offers at least comparable outcomes to LPN. UROLOGY 76: 754 –758, 2010. © 2010 Elsevier Inc.
revalent use of cross-sectional imaging has led to a manifest increase in the number of newly diagnosed, radiographically enhancing small renal masses.1 This migration toward smaller, localized lesions has allowed urologists to pursue nephron-sparing approaches to treatment, including partial nephrectomy and targeted in situ ablation.2 Currently, open partial nephrectomy (OPN) is considered the “gold standard” treatment for small renal masses, as it offers equivalent disease-specific survival and superior renal functional outcomes compared with radical nephrectomy.3,4 Laparoscopic partial nephrectomy (LPN) similarly offers equivalent disease-specific outcomes but with shortened convalescence compared with OPN.5 However, LPN is a technically challenging procedure that requires advanced laparoscopic skills and, in the vast majority of cases, the
Competing interests: Jihad H. Kaouk is a speaker for Intuitive Surgical (Sunnyvale, CA). From the Section of Laparoscopic and Robotic Urologic Surgery, Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, Ohio Reprint requests: Jihad H. Kaouk, M.D., Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute, Cleveland Clinic, 9500 Euclid Avenue, Suite Q10-1, Cleveland, OH 44195. E-mail: [email protected]
Submitted: January 5, 2010, accepted (with revisions): March 21, 2010
© 2010 Elsevier Inc. All Rights Reserved
need for renal hilar occlusion.5,6 In an attempt to shorten the considerable learning curve associated with LPN, to ease surgeon fatigue, and to further expand indications set for LPN, robotic partial nephrectomy (RPN) has been introduced. Outcomes of early experience reports have thus far have been favorable.7,8 However, few comparative studies have been performed to evaluate the merit of RPN compared with either OPN or LPN. We present here a single-surgeon comparative study of LPN and RPN in 150 matched patients.
MATERIAL AND METHODS Study Population Between March 2002 and August 2009, a retrospective cohort study was performed to evaluate perioperative outcomes among patients who underwent RPN and to compare these results with those of a matched cohort of patients who underwent LPN. The medical charts of 261 consecutive LPN (n ⫽ 186) or RPN (n ⫽ 75) performed by a single surgeon (J.H.K.) were reviewed. All data were obtained from our prospectively maintained, Institutional Review Board–approved database. A total of 75 consecutive RPN patients were matched with 75 LPN patients who were similar for age, body mass index (BMI), American Society of Anesthesiologists (ASA) score, laterality of the tumor, tumor 0090-4295/10/$34.00 doi:10.1016/j.urology.2010.03.058
Table 1. Demographic characteristics of study patients Characteristic Male/female Age (y) Body mass index ASA score CCI Side (right/left) Tumor size (cm) Inter/lower/upper pole Preoperative eGFR* Early/conventional/unclamped
Laparoscopic Partial Nephrectomy
Robotic Partial Nephrectomy
40/35 60 29.7 2.4 0.90 43/32 2.5 18/26/31 81 48/17/10
44/31 62.6 30.1 2.4 1.02 36/39 2.75 25/24/26 83.1 51/12/12
.43 .17 .68 .96 .48 .25 .17 .39 .54 .20
ASA ⫽ American Society of Anesthesiologists; CCI ⫽ creatinine clearance index; eGFR ⫽ estimated glomerular filtration rate. * mL/min/1.73 m2.
size, tumor location, creatinine clearance index (CCI), and preoperative estimated glomerular filtration rate (eGFR). The Modification of Diet in Renal Disease formula was used to calculate eGFR.
0 Vicryl sutures were placed through the renal capsule and tied over a Surgicel bolster (capsular sutures). A topical hemostatic agent was applied over the bolster and at the base of the bed of resection. A Jackson-Pratt drain was placed in all patients. All lesions were sent to pathology for frozen section analysis.
Surgical Technique The technique of LPN has been previously described.9 For RPN, patients were positioned in the flank position after induction and secured to the table with adhesive tape. Pneumoperitoneum was established using a Veress needle. The abdomen was insufflated with CO2 gas to a maximum pressure of 15 mm Hg. Two 8-mm robotic ports and two 12-mm ports were placed as follows: an 8-mm port placed at the junction of the costal margin and the lateral edge of ipsilateral rectus muscle, a 12-mm port camera port placed at the paraumbilical area along the line of the 12th rib, an 8-mm port placed in the ipsilateral flank area, as lateral as possible, and a 12-mm assistant port placed in the infraumbilical area along the lateral edge of ipsilateral rectus muscle. The robot was positioned with a cephalad angulation with respect to patient’s table at the level of the 12th rib. The robotic camera was docked through the “middle” port. Robotic arms 1 and 3 were docked through the “upper” and “lateral” ports. The second robotic arm was not used. The remaining 12-mm port was used by the bedside assistant to provide suction/irrigation and to introduce and retrieve sutures during renal reconstruction. The colon was reflected medially away from the kidney. The ureter and gonadal vein were identified and preserved. The renal vessels were identified in all patients in preparation for temporary hilar occlusion, if necessary. Hilar occlusion was dependent on the size and location of the lesion and was at the discretion of the operating surgeon. Following hilar preparation, the kidney was mobilized within Gerota’s fascia and the lesion identified. Intraoperative renal ultrasonography (BK Medical, Denmark) was performed to confirm the nature, size, and depth of the lesion. If hilar occlusion was planned, 12.5 g of mannitol were administered intravenously to the patient before clamping. A laparoscopic Satinsky clamp was employed for all clamped renal vessels in both cohorts. Cold robotic shears or Harmonic scalpel (Ethicon Endo-surgery, Cincinnati, OH) were used for tumor excision in the clamped and unclamped hilum, respectively. The renal reconstruction was performed using a 2-0 Vicryl suture placed through the capsule of the kidney and sequentially through the parenchyma of the operative bed (parenchymal sutures). Preplaced Hem-O-Lok clips (Weck Closure Systems, Research Triangle Park, NC) were used to secure the entry and exit sites of the suture at the renal capsule. Additional UROLOGY 76 (3), 2010
Data Analysis Pertinent intraoperative data were accrued for all patients. Patients were followed postoperatively for evidence of immediate and delayed adverse events. Surgical complications were defined according to the Clavien classification system.10 Pathology was reviewed by a dedicated genitourinary pathologist for tumor subtype and margin status. Serum creatinine levels were obtained at 3 months after surgery, and the eGFR and percent change in eGFR were calculated. The Statistical Package for the Social Sciences (SPSS Inc., Chicago, IL) was used to perform all statistical analyses. Descriptive analyses were performed to describe the characteristics of the patient sample (mean, standard deviation, percentages, and frequencies). Statistical significance was set at P ⱕ .05.
RESULTS A total of 75 consecutive patients who underwent RPN were reviewed and matched to a contemporary cohort of 75 patients who underwent LPN by the same surgeon. Demographic data are summarized in Table 1. There was no significant difference between the 2 cohorts with respect to age, gender, BMI, ASA score, CCI, tumor laterality, tumor size, tumor location, preoperative eGFR, or the type of renal hilar occlusion (clamped, unclamped, early unclamping). Operative outcomes were likewise comparable between the 2 cohorts (Table 2). Mean operative time was similar at approximately 3 hours 20 minutes. Mean warm ischemia time (WIT) was shorter in the RPN cohort (18.2 vs 20.3 minutes) but the difference was not significant. Estimated blood loss (EBL) was significantly less in the LPN cohort (P ⫽ .01), but the rate of transfusion was less in the RPN cohort (4% vs 5.3%). Three patients in the RPN cohort required conversion to standard laparoscopy because of failure of progression. In our early experience, 1 patient in the LPN cohort required conversion to open partial neprectomy secondary to significant bleeding. 755
Table 2. Operative outcomes in study patients
Table 3. Final pathology
Laparoscopic Robotic Partial Partial Nephrectomy Nephrectomy P (n ⫽ 75) (n ⫽ 75) Value OR time (min) EBL (mL) WIT (min) Length of stay (days) Intraoperative complications Kidney loss Conversion Conversion to laparoscopy Conversion to open Postoperative complications
197 222 20.3 4.1
200 323 18.2 4.2
.75 .01 .27 .84
1* 1* —
0 3 3
.23 .3 —
EBL ⫽ estimated blood loss; WIT ⫽ warm ischemia time. * Represents the patient converted to open radical nephrectomy for persistent bleeding.
Adverse events occurred in 10 LPN patients (13.3%) and 12 RPN patients (16%) (P ⫽ .64). Complications in the LPN cohort included 2 Clavien grade I complications (prolonged postoperative ileus), 7 Clavien grade II complications, including 4 patients who required a blood transfusion, 1 patient who developed atrial fibrillation, and 2 patients who developed a deep venous thrombosis (DVT). One patient in the LPN cohort required angioembolization (Clavien grade IIIb) for persistent postoperative bleeding. Adverse events in the RPN cohort included 2 patients with a prolonged ileus (Clavien grade I), 1 patient who experienced a transient syncopal episode (Clavien grade I), 3 patients who required a blood transfusion (Clavien grade II), 1 patient who developed atrial fibrillation requiring pharmacotherapy (Clavien grade II), 2 patients who developed a DVT (Clavien grade II), 1 patient who developed a urinoma that did not require intervention (Clavien grade II), and 2 patients who required angioembolization for persistent postoperative bleeding (Clavien grade IIIb). One patient in the laparoscopic group was converted to open radical nephrectomy after persistent bleeding from the partial nephrectomy bed, and 3 conversions to laparoscopic partial nephrectomy in the robotic group (failure to progress, n ⫽ 1; robotic camera malfunction, n ⫽ 1; and intraoperative positive margin on frozen section that necessitated a deeper parenchymal resection, n ⫽1). All conversion cases in the robotic group occurred among the first 20 cases. In the LPN cohort, pathologic findings demonstrated American Joint Committee on Cancer (AJCC) stage T1a in 54 patients, stage T1b RCC in 5 patients, and benign tumors in 16 patients. In the RPN cohort, pathology demonstrated AJCC stage T1a in 52 patients, stage T1b in 7 patients, and benign tumors in 16 patients. All surgical margins were negative in both cohorts (Table 3). 756
Laparoscopic Robotic Partial Partial Nephrectomy Nephrectomy Total
Clear-cell RCC Papillary RCC Oncocytoma Angiomyolipoma Chromophobe RCC Other benign Unclassified RCC Benign cyst Neuroendocrine carcinoma (carcinoid) Positive frozen section** Positive surgical margin
32 18 5 6 6 4 2 1 1
39 14 8 5 4 2 2 1 0
71 32 13 11 10 6 4 2 1
RCC ⫽ renal cell carcinoma. * P ⫽ 0.85; ** P ⫽ 0.99. ‡ Deeper parenchymal resection, second frozen section, and final margin negative.
Table 4. Postoperative serum creatinine (Cr) in LPN and RPN cohorts
Preoperative serum Cr Postoperative serum Cr* % Serum Cr change Preoperative eGFR** Postoperative eGFR** % eGFR change
0.93 1.05 11.93% 81 72.7 ⫺9.9%
0.97 1.06 11.38% 83 74.8 ⫺9.3%
.45 .78 .85 .54 .56 .80
LPN ⫽ laparoscopic partial nephrectomy; RPN ⫽ robotic partial nephrectomy. * mg/dL. ** mL/min/1.73 m2.
Postoperative serum creatinine (mg/dL) was similar between the LPN (1.05) and RPN (1.06) cohorts (P ⫽ .78) (Table 4). Likewise, there was no significant difference in % change in creatinine between the LPN and RPN cohorts (11.93% vs 11.38%, P ⫽ .85). There was no significant difference in postoperative eGFR (72.7 vs 74.8 mL/min, P ⫽ .56) or percent change in eGFR (⫺9.95% vs ⫺9.34%, P ⫽ .80) between the LPN and RPN cohorts, respectively.
COMMENT Historically, patients with small renal masses concerning for malignancy underwent definitive extirpative surgery in the form of open or laparoscopic radical nephrectomy.1– 4 Nephron-sparing surgery (NSS) was largely reserved for patients at risk for end-stage renal disease after treatment with radical nephrectomy.2 Subsequent studies have demonstrated that OPN offers equivalent disease-specific survival compared with radical nephrectomy with superior long-term renal functional outcomes, overall survival, and quality of life with the former.6,11 Moreover, NSS avoids overtreatment of patients with benign or UROLOGY 76 (3), 2010
indolent tumors.1,11 However, OPN is associated with significant morbidity and prolonged convalescence. To minimize morbidity associated with OPN, LPN was developed and refined.5,9 LPN offers comparable diseasespecific outcomes but with less pain, superior cosmesis, and a shortened length of hospitalization. However, LPN is associated with increased operative complications and the need for advanced laparoscopic skills.5 Furthermore the vast majority of renal lesions necessitate hilar occlusion during tumor excision and renorrhaphy so that directed renal reconstruction may be obtained in a clear and bloodless field.12 Because in situ renal hypothermia during LPN has been largely unsuccessful, the kidney is placed at considerable risk for postischemic injury if WIT is carried beyond 30 minutes.13,14 Even in expert hands, the mean WIT during LPN approaches or exceeds this threshold.5 The introduction and FDA approval of robotics in 2000 revolutionized urological surgery by offering the advantages of laparoscopy with a considerably shorter learning curve. Although initially used exclusively for radical prostatectomy by most urologists, its application and advantages in the field of extirpative and reconstructive renal and pelvic surgery is now being realized.8,15 The robotic platform is ideally suited for reconstructive procedures given its superior optics, its capacity to filter tremor, and its ability to operate freely, precisely, and rapidly in a confined field. Moreover, a myriad of studies have successfully demonstrated that robotic reconstructive procedures can be performed with confidence and safety even among surgeons with little to no formal laparoscopic experience.16,17 Given these advantages, it would appear that use of the robotic operating platform may help to overcome many of the aforementioned limitations of LPN. RPN has been well described in the literature.7,8,18,19 Multicenter outcomes have been favorable, with excellent oncological and renal functional outcomes. Published comparative studies to LPN are preliminary but demonstrate comparable or superior outcomes in patients treated with RPN.8,19 However, several of these series evaluated strikingly dissimilar patient cohorts that introduced considerable selection bias and/or were multi-institutional and therefore invoked concerns regarding surgeon variability. To our knowledge, this study represents the only single-surgeon series in which RPN outcomes were compared with a “control” group of LPN patients operated on by the same surgeon. The results of our matched, cohort study support the role of RPN in the management of small, radiographically enhancing renal masses. Both cohorts demonstrated excellent renal functional and oncological outcomes. Adverse events were comparable between the 2 groups and consistent with the published literature. Operative outcomes were nearly identical. The only significant difference between the 2 cohorts was less intraoperative blood loss in the LPN cohort (222 vs 323 mL); however UROLOGY 76 (3), 2010
fewer patients in the RPN cohort required a blood transfusion. This may be due to the significant difference in surgeon learning curve for RPN compared with LPN. Initial RPN cases included more blood loss with the surgeon away from the patient side and coordinating surgical steps with the bed side assistant. The issue of warm ischemia and postischemic renal injury during LPN and RPN is of particular importance. No significant difference in WIT was detected in our study. Nevertheless it is important to place our findings in the context of surgeon’s overall experience. The laparoscopic cases had been performed by the surgeon when he was well beyond his learning curve for this approach. The primary limitation of our study was its retrospective nature. Selection bias and patient confounders were minimized by matching the RPN cohort to demographically similar LPN patients. Surgical confounders were minimized by using the outcomes of a single surgeon. Ultimately, a randomized controlled trial is needed to confirm our results. Finally, we recognize that objective measures of tumor complexity, such as the RENAL nephrometry score, might currently represent an important tool for meaningful data comparisons in nephron-sparing surgery.20 Nevertheless we were unable to provide such an assessment, given the retrospective nature of this study, which made it impossible to retrieve the required information needed for our LPN cases and partially for our RPN cases.
CONCLUSIONS Outcomes of this study support RPN as an effective and safe alternative to LPN, given the translational capacity of the robotic operating platform coupled with its superior optics and flexibility. Further prospective comparative studies are awaited to confirm these encouraging findings and to further define the current role of robotics in nephron-sparing surgery. References 1. Kunkle DA, Egleston BL, Uzzo RG. Excise, ablate, or observe: the small renal mass dilemma—a meta-analysis and review. J Urol. 2008;179:1227-1233. 2. Uzzo RG, Novick AC. Nephron sparing surgery for renal tumors: indications, techniques and outcomes. J Urol. 2001;166:6-18. 3. Mabjeesh NJ, Avidor Y, Matzkin H. Emerging nephron sparing treatments for kidney tumors: A continuum of modalities from energy ablation to laparoscopic partial nephrectomy. J Urol. 2004; 171:553-560. 4. Fergany AF, Hafez KS, Novick AC. Long-term results of nephronsparing surgery for localized renal cell carcinoma: 10-year followup. J Urol. 2000;163:442-445. 5. Gill IS, Kavoussi LR, Lane BR, et al. Comparison of 1,800 laparoscopic and open partial nephrectomies for single renal tumors. J Urol. 2007;78:41-46. 6. Riggs SB, Larochelle JC, Belldegrun AS. Partial nephrectomy: a contemporary review regarding outcomes and different techniques. Cancer J. 2008;14:302-307. 7. Gettman MT, Blute ML, Chow GK, et al. Robotic-assisted laparoscopic partial nephrectomy: technique and initial clinical experience with DaVinci robotic system. Urology. 2004;64:914-918.
8. 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. 9. Nguyen MM, Gill IS. Halving ischemia time during laparoscopic partial nephrectomy. J Urol. 2008;179:627-632. 10. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205-213. 11. Zini L, Perrotte P, Capitanio U, et al. Radical versus partial nephrectomy: effect on overall and noncancer mortality. Cancer. 2009;115:1465-1471. 12. Aron M, Haber GP, Gill IS. Laparoscopic partial nephrectomy. BJU Int. 2007;99:1258-1263. 13. Gill IS, Abreu SC, Desai MM, et al. Laparoscopic ice slush renal hypothermia for partial nephrectomy: the initial experience. J Urol. 2003;170:52-56. 14. Webster TM, Moeckel GW, Herrell SD. Second prize: simple method for achieving renal parenchymal hypothermia for pure laparoscopic partial nephrectomy. J Endourol. 2005;19:1075-1081.
15. Hyams ES, Mufarrij PW, Stifelman MD. Robotic renal and upper tract reconstruction. Curr Opin Urol. 2008;18:557563. 16. Yohannes P, Rotariu P, Pinto P, et al. Comparison of robotic versus laparoscopic skills: is there a difference in the learning curve? Urology. 2002;60:39-45. 17. Bentas W, Wolfram M, Brautigam R, et al. DaVinci robot assisted Anderson-Hynes dismembered pyeloplasty: technique and 1-year follow-up. World J Urol. 2003;21:133-138. 18. 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. 19. Aron M, Koenig P, Kaouk JH, et al. Robotic and laparoscopic partial nephrectomy: a matched-pair comparison from a highvolume centre. BJU Int. 2008;102:86-92. 20. Kutikov A, Uzzo RG, The RENAL. nephrometry score: a comprehensive standardized system for quantitating renal tumor size, location and depth. J Urol. 2009;182:844-853.
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