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Operative Outcomes of Upper Pole Laparoscopic Partial Nephrectomy: Comparison of Lower Pole Laparoscopic and Upper Pole Open Partial Nephrectomy
Adult Urology Operative Outcomes of Upper Pole Laparoscopic Partial Nephrectomy: Comparison of Lower Pole Laparoscopic and Upper Pole Open Partial Nephrectomy Kevin C. Zorn, Edward M. Gong, Frederick P. Mendiola, Albert A. Mikhail, Marcelo A. Orvieto, Ofer N. Gofrit, Gary D. Steinberg, and Arieh L. Shalhav OBJECTIVES
METHODS
RESULTS
CONCLUSIONS
The intraoperative complexity of laparoscopic partial nephrectomy (LPN) for upper pole renal tumors is recognized. We report on the technical feasibility and operative outcomes of LPN for upper pole tumors (UPLPN) and lower pole tumors (LPLPN), and open partial nephrectomy (UPOPN) for upper pole tumors. We retrospectively reviewed our database of LPNs performed by a single surgeon from October 2002 to February 2006. All solitary, upper and lower pole tumors in patients with a normal contralateral kidney were included. The perioperative outcomes were assessed. UPOPNs performed in the same institution by a separate surgeon were analyzed and compared separately with the UPLPN group. Three groups, UPLPN (20 patients), LPLPN (33 patients), and UPOPN (24 patients), were analyzed. The UPLPN and LPLPN groups had similar perioperative outcomes. The intraoperative and postoperative major complications were also comparable between the UPLPN and LPLPN groups (17% versus 12%, P ⫽ 0.68 and 22% versus 6%, P ⫽ 0.07, respectively). The mean pathologic tumor size was larger (3.2 versus 2.3 cm, P ⫽ 0.05) and the mean operative time significantly shorter (187 versus 244 minutes, P ⫽ 0.02) in the UPOPN group than in the UPLPN group. The UPOPN group had a trend toward fewer intraoperative complications compared with the UPLPN group (4% versus 17%, P ⫽ 0.17). The final pathologic surgical margins were negative in all three groups. LPN for upper pole renal tumors is technically feasible and may have comparable outcomes to LPN for lower pole tumors. However, performing open nephron-sparing surgery is still the standard of care because it may offer fewer complications and reduce the risk of ischemic damage to the kidney. UROLOGY 70: 28 –34, 2007. © 2007 Elsevier Inc.
L
aparoscopic partial nephrectomy (LPN) is becoming an established therapeutic modality in the management of small renal masses.1 Despite the emergence of several minimally invasive ablative therapies, such as cryotherapy and radiofrequency ablation, LPN is still the most comparable and oncologically equivalent alternative to open partial nephrectomy (OPN) for small renal tumors.2 With increasing surgical experience and the advancement of laparoscopic instrumentation, the indications for nephron-sparing surgery (NSS) and LPN have expanded.3– 6 However, despite the growing experience, the inherent intraoperative techniFrom the Section of Urology, Department of Surgery, University of Chicago Pritzker School of Medicine, Chicago, Illinois Reprint requests: Kevin C. Zorn, M.D., Section of Urology, Department of Surgery, University of Chicago Pritzker School of Medicine, 5841 South Maryland Avenue, MC6038 J-653, Chicago, IL 60637. E-mail: [email protected] Submitted: September 18, 2006; accepted (with revisions): February 27, 2007
28
© 2007 Elsevier Inc. All Rights Reserved
cal complexity of this procedure has limited its acceptance as the standard of care in the general urologic community.7 Several institutions have described surgical techniques to simplify LPN and improve the surgical outcome.8,9 However, for a novice laparoscopist with less LPN experience, certain preoperative considerations might influence the decision to perform laparoscopic NSS. These include the tumor characteristics such as an upper or a hilar location, collecting system involvement, renal insufficiency, and tumor size. These factors can result in more technically demanding surgery, increase the warm ischemia time,10 and result in poorer outcomes. Several investigators have reported their LPN experiences with challenging tumor characteristics,3–5,11 such as a hilar location. To the best of our knowledge, no published studies have assessed the difficulty associated with upper pole renal tumors. We present our experience 0090-4295/07/$32.00 doi:10.1016/j.urology.2007.02.059
Figure 1. (a) Right kidney with upper pole, lateral, exophytic renal tumor (A). Traction suture (B) has been placed just superior to renal tumor at upper lateral aspect of kidney, but not yet passed through abdominal wall and tumor not in optimal position for excision. (b) Right renal tumor (arrow) after traction suture has been pulled and secured at skin level. Tumor in triangulation with surgical instruments and camera for optimal excision.
Table 1. Comparison of baseline demographic data on upper and lower pole LPN and OPN for renal tumor Characteristic Patient data Patients (n) Age (yr) Mean Range BMI (kg/m2) Mean Range ASA score Mean Range Sex Male Female Preoperative creatinine (mg/dL) Mean Range Previous abdominal surgery (n) Yes No Tumor data Radiographic tumor size (cm) Mean Range Laterality (n) Right Left Tumor location (n) Anterior Posterior Lateral Tumor depth (n) Exophytic Mesophytic Endophytic
Lower Pole LPN
P Value*
33
Upper Pole LPN 20
0.78 61.2 35–81 0.18
24 62.2 37–81 0.34
28.9 21.5–38.8 0.68
2.3 2–3
27.9 21.1–41.7 0.62
2.2 1–4 0.54
17 16
2.4 1–3 0.87
12 8 0.23
1.0 0.5–2.6
15 9 0.17
1.1 0.6–2.9 0.19
16 17
1.2 0.6–4.5 0.42
6 14 0.08
3.1 1.3–4.5
10 14 0.10
2.4 1–4 0.30
18 15
2.8 2–4.7 0.51
8 12 0.22
9 (27) 10 (30) 14 (43)
Upper Pole OPN
0.71 61.2 37–83
30.9 22.4–44.1
12 12 0.44
8 (40) 2 (10) 10 (50) 0.72
25 (76) 5 (15) 3 (9)
P Value†
11 (46) 5 (21) 8 (33) 0.72
17 (85) 2 (10) 1 (5)
18 (75) 4 (17) 2 (8)
LPN ⫽ laparoscopic partial nephrectomy; OPN ⫽ open partial nephrectomy; BMI ⫽ body mass index; ASA ⫽ American Society of Anesthesiologists. Data in parentheses are percentages. * Between lower pole and upper pole LPN. † Between upper pole LPN and upper pole OPN.
UROLOGY 70 (1), 2007
29
Table 2. Perioperative and pathologic outcomes among all groups Variable Surgical data OR time (min) Mean Range EBL (mL) Mean Range Ischemia time (min) Mean Range Collecting system injury and repair (n) Yes No Open conversions (n) Hospital stay (days) Mean Range Postoperative creatinine (mg/dL) Mean Range Transfusion rate (n) Intraoperative Postoperative Complications (n) Intraoperative Major Vascular hemorrhage Renal parenchymal Liver or spleen laceration Total Minor Subcutaneous emphysema Total Postoperative‡ Major Urine leak Hemorrhage Pulmonary embolism Pleural effusion/pneumothorax Total Minor Arrhythmia UTI Atelectasis Blurry vision Acute tubular necrosis Epididymitis Hip pain Muscle spasm Total Pathologic data‡ Tumor size (cm) Mean Range Positive surgical margin (n) Pathologic stage (n) pT0§ pT1a pT1b Histologic findings (n) Malignant Clear cell RCC Chromophobe RCC Papillary RCC
Lower Pole LPN (n ⫽ 33)
P Value*
Upper Pole LPN (n ⫽ 20)
0.70 236 122–396 0.55 0.91
0.48 0.98
2.7 1–7
1 1 (3) 0 1 (3) 1 0 2 (6) 0 1 0 0 0 0 1 1 3 (9)
0.63
5.8 4–9
0.04
0.68
0.17
0 0 1 1 (4)
0.45
0 0
0.94
0 0
0.07
0 3 (17) 1 0 4 (22)
0.21
0 0 1 1 1 1 0 0 4 (22)
0.08
0.37 0.97
0.24
1.4 0.7–5.9 1 (4) 0 1
1 (6) 1 1 3 (17)
6 (19) 24 (75) 2 (6)
0.06 0.83
1 (4) 1 (4) 0 4 (17) 6 (25)
0.40
2 0 1 0 0 0 0 0 3 (12)
0.17
0.05 2.3 0.9–4.1 1 (5)
0.45 0.89
3 (17) 14 (78) 1 (5) 0.85
26 (81) 20 3 3
— 0.002
21 (88) 3 (12) NA
0.21 1.2 0.8–2.1 5 (25) 2 3
0.06 2.9 0.8–4.6 0
23.5 15–38
2.8 1–14
0.05
306 100–800
0.50 13 (80) 7 (20) 2 (10)
0.72
3 (9) 1 0 4 (12)
⬍0.001
32.4 13–75 0.45
1.2 0.6–2.2 2 (6) 1 1
187 110–260 0.006
197 5–600
34.3 20–55
Upper Pole OPN (n ⫽ 24)
0.02 244 140–447
244 20–1700
18 (55) 15 (45) 1 (3)
P Value†
3.2 1.3–5 0 3 (13) 19 (79) 2 (8)
0.70 15 (83) 12 1 2
21 (87) 15 2 4 Continued
30
UROLOGY 70 (1), 2007
Table 2. Continued Variable Benign Oncocytoma Angiomyolipoma Benign cyst
Lower Pole LPN (n ⫽ 33) 6 (19) 2 3 1
P Value*
Upper Pole LPN (n ⫽ 20)
P Value†
Upper Pole OPN (n ⫽ 24)
3 (17) 0 0 3
3 (13) 0 1 2
OR ⫽ operating room; EBL ⫽ estimated blood loss; UTI ⫽ urinary tract infection; RCC ⫽ renal cell carcinoma; other abbreviations as in Table 1. Data in parentheses are percentages. * Between lower pole and upper pole LPN. † Between upper pole LPN and upper pole OPN. ‡ Excluding open conversions. § Pathologic benign disease.
with LPN in patients with upper pole renal tumors, describing the modifications in operative technique to address the technical considerations. We also retrospectively reviewed our results with LPN and compared cohorts of LPN of lower pole tumors and OPN of upper pole lesions.
MATERIAL AND METHODS A review of our database from October 2002 through February 2006 was performed after obtaining institutional review board approval. A total of 256 laparoscopic procedures for patients with renal tumors were performed at our institution by a single surgeon (A.L.S.), of which 166 were laparoscopic radical nephrectomy and 90 were LPN. Patients with a localized renal tumor with a normal contralateral kidney were included in the review. Patients with tumors involving the middle pole were excluded from the study. A total of 20 patients underwent LPN for upper pole lesions (UPLPN group) and 33 patients underwent LPN for lower pole lesions (LPLPN group). A “tumor size”-matched cohort of 24 patients who underwent OPN for upper pole tumors (UPOPN group) were randomly selected from our database of 186 OPNs performed from April 1995 to July 2005 by an open surgeon (G.D.S.). Preoperatively, the patients were evaluated with a medical history, physical examination, urinalysis, chest x-ray, laboratory studies, including serum creatinine determinations, and abdominal computed tomography to allow for intraoperative surgical planning. The tumors were characterized as described by Finley et al.12: tumor that extended less than 40%, 40% to 60%, and more than 60% off the natural surface of the kidney was defined as endophytic, mesophytic, and exophytic, respectively.
LPN Surgical Technique Our LPN technique has previously been reported.8,13–15 In brief, after hilar dissection, a laparoscopic ultrasonic probe was used to delineate the tumor extent. Vascular clamping was performed using endoscopic bulldog clamps (Klein Surgical, San Antonio, Tex). Tumor excision was performed with cold scissors, maintaining a safety margin of normal parenchyma of at least 0.5 cm. Argon beam coagulation of the tumor bed, followed by freehand suturing of the collecting system and major bleeding sites, anchored and secured with a LapraTy clip, was then completed. Defect closure was completed with individual parenchymal sutures, securely cinched with the LapraTy UROLOGY 70 (1), 2007
clip. FloSeal was then placed in the closed defect space to further secure hemostasis.
Upper Pole LPN: Triangulation Technique Our technical alterations for LPN have been previously described with modifications depending on the tumor location.8,16 In brief, after mobilizing the entire kidney, the perinephric fat was dissected off the capsule, except for the peritumoral fat, which was left over the tumor. Intraoperative ultrasonography was used to delineate the tumor margins. Depending on the exact tumor location, a suspensory traction system was used to optimize and stabilize the kidney position. This traction suture with a LapraTy clip on its end was passed as a figure-of-eight, 2 mm deep and 1.5 cm along the renal capsule, and then brought out through a preplanned site in the abdominal wall using a Carter-Thomason suture closure device. The suture location on the renal capsule, the direction of traction, and the abdominal placement of the suture all depend on the anteroposterior location of the tumor and whether it was a polar, medial, or lateral tumor. A hemostat held the suture extracorporeally at the level of the skin. The suspension created by the traction suture allowed the kidney to be positioned for optimal tumor visualization, excision, and suturing (triangulation between the two working laparoscopic instruments; Fig. 1). The sling was used for all upper pole tumors and only as needed (17%) for the lower pole tumors.
OPN Surgical Technique OPN was routinely performed through a transperitoneal approach. Intraoperative ultrasonography helped delineate the tumor margins. Unlike LPN, in which the ischemia time occurred in a warm environment, OPN was performed with ice cooling of the kidney. After cold scissor tumor excision with sufficient margins, argon beam coagulation of the renal defect was performed. Injury of the collecting system was then repaired with sutures, followed by meticulous oversewing of the individual blood vessels. Parenchymal closure was performed with individual sutures with Surgicel bolsters for tissue compression.
Statistical Analysis Statistical comparisons were made between cohorts using baseline demographic data and were compared using the chi-square test. Continuous variables are shown as mean values and compared using Student’s t tests and Fisher’s exact test, with correlation between variables performed using the Pearson’s cor31
relation coefficients, with P ⬍0.05 considered statistically significant.
RESULTS The baseline patient demographics are summarized in Table 1. Three groups (UPLPN, LPLPN, and UPOPN) were compared according to surgical approach and tumor location. Age, sex, body mass index, American Society of Anesthesiologist scores, and preoperative serum creatinine levels were similar between the UPLPN group and the other groups. The mean radiographic tumor size in the UPLPN group was comparable with that in the LPLPN group (2.4 versus 3.1 cm, P ⫽ 0.08). Similarly, no significant difference was noted in the tumor size between the UPLPN and UPOPN groups (2.4 versus 2.8 cm, P ⫽ 0.10). The tumors were mostly exophytic in all groups, with no significant differences in tumor depth among the groups. No differences were noted in tumor location (anterior, posterior, or lateral) or tumor literality between the UPLPN group and the other study groups. The intraoperative data are summarized in Table 2. The mean operative time, estimated blood loss, and ischemia time were not significantly different between the UPLPN and LPLPN groups. The UPOPN group, however had a significantly shorter mean operative time (187 versus 244 minutes, P ⫽ 0.02), shorter ischemia time (23.5 versus 32.4 minutes, P ⬍0.001), and higher estimated blood loss (306 versus 197 mL, P ⫽ 0.006) compared with the UPLPN group. All patients in the UPOPN group required collecting system repair compared with 65% and 55% in the LPLPN and UPLPN groups, respectively. One open conversion (3%) was required in the LPLPN group and two (10%) in the UPLPN group (P ⫽ 0.48). The LPLPN open conversion occurred because of persistent parenchymal bleeding on hilar unclamping. An attempt at laparoscopic resuturing was unsuccessful before a decision to convert to an open approach was made. Of the 2 patients requiring open conversion in the UPLPN group, 1 had brisk renal arterial bleeding after an injury to the renal artery and 1 had positive margins on frozen section analysis. As expected, the hospital stay was significantly longer for the UPOPN group than for the UPLPN group (P ⫽ 0.002). A similar hospital stay length was noted between the LPLPN and UPLPN groups. The incidence of major and minor intraoperative complications was similar among all groups (Table 2). The incidence of major postoperative complications was greater in the UPLPN group than in the LPLPN group (22% versus 6%, P ⫽ 0.07). Most such complications were hemorrhagic (17% versus 3%, P ⫽ 0.08). In the UPOPN group, 1 patient had a perinephric fluid collection secondary to a urine leak that eventually resolved after radiographic replacement of a Jackson-Pratt drain. The incidence of minor postoperative complications did not differ significantly among the three groups. 32
Renal cell carcinoma was confirmed in 83%, 81%, and 87% of the patients in the UPLPN, LPLPN, and UPOPN groups, respectively. The mean pathologic size was significantly larger in the UPOPN group than in the UPLPN group (3.2 versus 2.3 cm, P ⫽ 0.05). Other than the 1 patient in the UPLPN group with a positive surgical margin noted intraoperatively whose surgery was converted to an open approach for management, no other positive surgical margin was noted in all groups on final pathologic examination.
COMMENT OPN remains the established standard for NSS of renal tumors.16 Recently published series have stated that “elective” NSS provides optimal long-term oncologic efficacy in properly selected patients with localized renal cell carcinoma.18 With the expanding criteria for NSS and the advancement of laparoscopic instrumentation and pharmaceutical hemostatic agents, the indications for this procedure have expanded. Because of rib cage encasement, upper pole lesions represent a significant technical challenge for the open, and more so for the laparoscopic, approach. The limited visualization and compromised tumor positioning for rapid and efficient suturing of resected upper pole tumors are an impediment to the novice laparoscopist. This difficult anatomic tumor location is the reason many patients with a small renal tumor in the upper pole who might otherwise be a candidate for NSS are undergoing OPN or laparoscopic radical nephrectomy.19 In our series, we used techniques to facilitate renal positioning (using a suspension traction system and other modifications), thereby allowing better upper pole access for precise tumor excision and efficient hemostasis and renal reconstruction during the critical steps of LPN16 (Fig. 1). The principle of leaving a handle of fat on top of the tumor is very helpful in providing increased maneuverability after renal positioning by the traction system. Our data have demonstrated the similarity in operative outcomes in both LPN groups, which could be attributed to our surgical modifications. In their initial LPN experience, Ramani et al.20 reported that the most common complications were related to intraoperative hemorrhage. Our study demonstrated comparable intraoperative hemorrhage results with a similar incidence in the UPLPN and LPLPN groups (P ⫽ 0.63). The likely causes of persistent parenchymal bleeding were an unoccluded renal artery in the setting of multiple vessels or bulldog clamp malfunction, both of which were not associated with the primary location of the tumor. Our study did demonstrate that upper pole renal tumors, relative to lower pole tumors, were associated with a trend toward a greater incidence of postoperative hemorrhage after LPN, although statistical significance was not reached (17% versus 3%, P ⫽ 0.08). These complications occurred even though complete hemostasis on UROLOGY 70 (1), 2007
hilar unclamping had been noted in all cases. No obvious precipitating factor could be found in these cases, although inadequate parenchymal repair might be the most plausible explanation. Gill et al.21 emphasized that the best management of postresection parenchymal hemorrhage is preventive through well-functioning vascular instruments for hilar control and meticulous oversewing of transected vessels. Our results are similar to previously reported series by Gill et al.21 in that LPN, compared with OPN, required a longer warm ischemia time and resulted in less blood loss, shorter hospital stay, and more rapid convalescence. They also concluded that LPN was associated with a greater incidence of intraoperative and renal/urologic complications compared with those in the open group.21 In our study, despite the larger pathologic tumor size in the open group compared with the laparoscopic upper pole group, the latter had a greater incidence of intraoperative and postoperative hemorrhagic complications. No urinary leakage was observed in either LPN group, and 1 patient in the OPN group (5%) had a significant postoperative urine leak. This difference could have been related to the larger pathologic tumor size (requiring deeper resection) and greater need for collecting system repair in the OPN group. Other series have reported similar urinary leakage rates after OPN.22 Our data have reaffirmed that watertight suture repair of the collecting system can be accomplished with similar efficacy using the laparoscopic approach regardless of tumor location. This study had several limitations that warrant discussion. The retrospective nature of the study using data from a single institution, with small patient numbers, must be noted. Furthermore, the comparison between two surgeons’ experience also might have added an inherent weakness to the study. However, a cohort of patients with upper pole lesions of comparable radiologic tumor size was selected from the OPN database for comparison. A significant difference between the radiographic and pathologic tumor size was noted. Such a change could have been related to the three-dimensional tumor configuration, in that the largest radiographic measurement taken with standard axial imaging might not have been accurate, especially for the OPN group for whom the imaging was performed between 1995 and 2005. Ultimately, the UPOPN group had a significantly larger tumor size compared with those of the UPLPN group. Our study has highlighted the technical feasibility of LPN in upper pole tumors. The similarity in the operative outcomes between the UPLPN and LPLPN groups has proved that the difficulty associated with tumor location can be overcome with modifications in surgical technique. With regard to positive surgical margins, the results in our LPN groups were comparable with those of other OPN21,23,24 and LPN series.6,17,18,21,25 However, it is important to realize that this procedure is associated with a very steep learning curve.25,26 At present, OPN UROLOGY 70 (1), 2007
still offers lower complication rates compared with the laparoscopic approach. We believe that with continuous growth in experience and additional developments in technique and pharmacologic and hemostatic tools, achieving comparable results to OPN could be possible.
CONCLUSIONS LPN can be performed in patients with peripheral small renal tumors, regardless of location. We believe that with technical modifications, LPN for upper pole lesions can be performed with optimal tumor positioning for excision and repair, thereby replicating surgery for lower pole tumors. The decision to perform NSS laparoscopically will ultimately depend on the surgeon’s level of experience. Performing open NSS is still the standard of care because it seems to result in fewer complications and reduce the risk of ischemic damage to the kidney. References 1. Albqami N, and Janetschek G: Laparoscopic partial nephrectomy. Curr Opin Urol 15: 306 –311, 2005. 2. Finelli A, and Gill IS: Laparoscopic partial nephrectomy: contemporary technique and results. Urol Oncol 22: 139 –144, 2004. 3. Gill IS, Colombo JR Jr, Frank I, et al: Laparoscopic partial nephrectomy for hilar tumors. J Urol 174: 850 – 854, 2005. 4. Reisiger K, Venkatesh R, Figenshau RS, et al: Complex laparoscopic partial nephrectomy for renal hilar tumors. Urology 65: 888 – 891, 2005. 5. Finelli A, Gill IS, Desai MM, et al: Laparoscopic heminephrectomy for tumor. Urology 65: 473– 478, 2005. 6. Rassweiler JJ, Abbou C, Janetschek G, et al: Laparoscopic partial nephrectomy: the European experience. Urol Clin North Am 27: 721–736, 2000. 7. Gerber GS, and Stockton BR: Trends in endourologic practice: laparoscopic partial nephrectomy. J Endourol 19: 21–24, 2005. 8. Orvieto MA, Chien GW, Tolhurst SR, et al: Simplifying laparoscopic partial nephrectomy: technical considerations for reproducible outcomes. Urology 66: 976 –980, 2005. 9. Weld JW, Venkatesh R, Huang J, et al: Evolution of surgical technique and patient outcomes for laparoscopic partial nephrectomy. Urology 67: 502–507, 2006. 10. Desai MM, Gill IS, Ramani AP, et al: The impact of warm ischaemia on renal function after laparoscopic partial nephrectomy. BJU Int 95: 377–383, 2005. 11. Ramani AP, Abreu SC, Desai MM, et al: Laparoscopic upper pole nephrectomy with concomitant en bloc adrenalectomy. Urology 62: 223–226, 2003. 12. Finley DS, Lee DI, Eichel L, et al: Fibrin glue-oxidized cellulose sandwich for laparoscopic wedge resection of small renal lesions. J Urol 173: 1477–1481, 2005. 13. Orvieto MA, Chien GW, Laven B, et al: Eliminating knot tying during warm ischemia time for laparoscopic partial nephrectomy. J Urol 174: 2292–2295, 2004. 14. Orvieto MA, Chien GW, Tolhurst, et al: Simplifying laparoscopic partial nephrectomy: technical considerations for reproducible outcomes. Urology 66: 976 –980, 2005. 15. Shalhav AL, Orvieto MA, Chien GW, et al: Minimizing knot tying during reconstructive laparoscopic urology. Urology 63: 508 –513, 2006. 16. Chien GW, Orvieto MA, Chuang MS, et al: Use of suspension traction system for renal positioning during laparoscopic partial nephrectomy. J Endourol 19: 406 – 409, 2005. 17. Gill IS, Desai MM, Kaouk JH, et al: Laparoscopic partial nephrectomy for renal tumor: duplicating open surgical techniques. J Urol 167: 469 – 476, 2002.
33
18. Moinzadeh A, Gill IS, Finelli A, et al: Laparoscopic partial nephrectomy: 3 year followup. J Urol 175: 459 – 462, 2006. 19. Best S, Ercole B, Lee C, et al: Minimally invasive therapy for renal cell carcinoma: is there a new community standard? Urology 64: 22–25, 2004. 20. Ramani AP, Desai MM, Steinberg AP, et al: Complications of laparoscopic partial nephrectomy in 200 cases. J Urol 173: 52– 47, 2005. 21. Gill IS, Matin SF, Desai MM, et al: Comparative analysis of laparoscopic versus open partial nephrectomy for renal tumors in 200 patients. J Urol 170: 64 – 68, 2003. 22. Beasley KA, Al Omar M, Shaikh A, et al: Laparoscopic versus open partial nephrectomy. Urology 64: 458 – 461, 2004.
34
23. Thompson RH, Leibovich BC, Lohse CM, et al: Complications of contemporary open nephron sparing surgery: a single institution experience. J Urol 174: 855– 858, 2005. 24. Gerard C, Ballereau C, Leroy X, et al: Long-term oncological results after conservative surgery for unifocal renal cancer. Prog Urol 13: 14 –22, 2003. 25. Link RE, Bhayani SB, Allaf ME, et al: Exploring the learning curve, pathological outcomes and perioperative morbidity of laparoscopic partial nephrectomy performed for renal mass. J Urol 173: 64 – 68, 2003. 26. Sutherland SE, Resnick MI, Maclennan GT, et al: Does the size of surgical margin in partial nephrectomy for renal cell cancer really matter? J Urol 167: 61– 64, 2002.
UROLOGY 70 (1), 2007
METHODS
RESULTS
CONCLUSIONS
The intraoperative complexity of laparoscopic partial nephrectomy (LPN) for upper pole renal tumors is recognized. We report on the technical feasibility and operative outcomes of LPN for upper pole tumors (UPLPN) and lower pole tumors (LPLPN), and open partial nephrectomy (UPOPN) for upper pole tumors. We retrospectively reviewed our database of LPNs performed by a single surgeon from October 2002 to February 2006. All solitary, upper and lower pole tumors in patients with a normal contralateral kidney were included. The perioperative outcomes were assessed. UPOPNs performed in the same institution by a separate surgeon were analyzed and compared separately with the UPLPN group. Three groups, UPLPN (20 patients), LPLPN (33 patients), and UPOPN (24 patients), were analyzed. The UPLPN and LPLPN groups had similar perioperative outcomes. The intraoperative and postoperative major complications were also comparable between the UPLPN and LPLPN groups (17% versus 12%, P ⫽ 0.68 and 22% versus 6%, P ⫽ 0.07, respectively). The mean pathologic tumor size was larger (3.2 versus 2.3 cm, P ⫽ 0.05) and the mean operative time significantly shorter (187 versus 244 minutes, P ⫽ 0.02) in the UPOPN group than in the UPLPN group. The UPOPN group had a trend toward fewer intraoperative complications compared with the UPLPN group (4% versus 17%, P ⫽ 0.17). The final pathologic surgical margins were negative in all three groups. LPN for upper pole renal tumors is technically feasible and may have comparable outcomes to LPN for lower pole tumors. However, performing open nephron-sparing surgery is still the standard of care because it may offer fewer complications and reduce the risk of ischemic damage to the kidney. UROLOGY 70: 28 –34, 2007. © 2007 Elsevier Inc.
L
aparoscopic partial nephrectomy (LPN) is becoming an established therapeutic modality in the management of small renal masses.1 Despite the emergence of several minimally invasive ablative therapies, such as cryotherapy and radiofrequency ablation, LPN is still the most comparable and oncologically equivalent alternative to open partial nephrectomy (OPN) for small renal tumors.2 With increasing surgical experience and the advancement of laparoscopic instrumentation, the indications for nephron-sparing surgery (NSS) and LPN have expanded.3– 6 However, despite the growing experience, the inherent intraoperative techniFrom the Section of Urology, Department of Surgery, University of Chicago Pritzker School of Medicine, Chicago, Illinois Reprint requests: Kevin C. Zorn, M.D., Section of Urology, Department of Surgery, University of Chicago Pritzker School of Medicine, 5841 South Maryland Avenue, MC6038 J-653, Chicago, IL 60637. E-mail: [email protected] Submitted: September 18, 2006; accepted (with revisions): February 27, 2007
28
© 2007 Elsevier Inc. All Rights Reserved
cal complexity of this procedure has limited its acceptance as the standard of care in the general urologic community.7 Several institutions have described surgical techniques to simplify LPN and improve the surgical outcome.8,9 However, for a novice laparoscopist with less LPN experience, certain preoperative considerations might influence the decision to perform laparoscopic NSS. These include the tumor characteristics such as an upper or a hilar location, collecting system involvement, renal insufficiency, and tumor size. These factors can result in more technically demanding surgery, increase the warm ischemia time,10 and result in poorer outcomes. Several investigators have reported their LPN experiences with challenging tumor characteristics,3–5,11 such as a hilar location. To the best of our knowledge, no published studies have assessed the difficulty associated with upper pole renal tumors. We present our experience 0090-4295/07/$32.00 doi:10.1016/j.urology.2007.02.059
Figure 1. (a) Right kidney with upper pole, lateral, exophytic renal tumor (A). Traction suture (B) has been placed just superior to renal tumor at upper lateral aspect of kidney, but not yet passed through abdominal wall and tumor not in optimal position for excision. (b) Right renal tumor (arrow) after traction suture has been pulled and secured at skin level. Tumor in triangulation with surgical instruments and camera for optimal excision.
Table 1. Comparison of baseline demographic data on upper and lower pole LPN and OPN for renal tumor Characteristic Patient data Patients (n) Age (yr) Mean Range BMI (kg/m2) Mean Range ASA score Mean Range Sex Male Female Preoperative creatinine (mg/dL) Mean Range Previous abdominal surgery (n) Yes No Tumor data Radiographic tumor size (cm) Mean Range Laterality (n) Right Left Tumor location (n) Anterior Posterior Lateral Tumor depth (n) Exophytic Mesophytic Endophytic
Lower Pole LPN
P Value*
33
Upper Pole LPN 20
0.78 61.2 35–81 0.18
24 62.2 37–81 0.34
28.9 21.5–38.8 0.68
2.3 2–3
27.9 21.1–41.7 0.62
2.2 1–4 0.54
17 16
2.4 1–3 0.87
12 8 0.23
1.0 0.5–2.6
15 9 0.17
1.1 0.6–2.9 0.19
16 17
1.2 0.6–4.5 0.42
6 14 0.08
3.1 1.3–4.5
10 14 0.10
2.4 1–4 0.30
18 15
2.8 2–4.7 0.51
8 12 0.22
9 (27) 10 (30) 14 (43)
Upper Pole OPN
0.71 61.2 37–83
30.9 22.4–44.1
12 12 0.44
8 (40) 2 (10) 10 (50) 0.72
25 (76) 5 (15) 3 (9)
P Value†
11 (46) 5 (21) 8 (33) 0.72
17 (85) 2 (10) 1 (5)
18 (75) 4 (17) 2 (8)
LPN ⫽ laparoscopic partial nephrectomy; OPN ⫽ open partial nephrectomy; BMI ⫽ body mass index; ASA ⫽ American Society of Anesthesiologists. Data in parentheses are percentages. * Between lower pole and upper pole LPN. † Between upper pole LPN and upper pole OPN.
UROLOGY 70 (1), 2007
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Table 2. Perioperative and pathologic outcomes among all groups Variable Surgical data OR time (min) Mean Range EBL (mL) Mean Range Ischemia time (min) Mean Range Collecting system injury and repair (n) Yes No Open conversions (n) Hospital stay (days) Mean Range Postoperative creatinine (mg/dL) Mean Range Transfusion rate (n) Intraoperative Postoperative Complications (n) Intraoperative Major Vascular hemorrhage Renal parenchymal Liver or spleen laceration Total Minor Subcutaneous emphysema Total Postoperative‡ Major Urine leak Hemorrhage Pulmonary embolism Pleural effusion/pneumothorax Total Minor Arrhythmia UTI Atelectasis Blurry vision Acute tubular necrosis Epididymitis Hip pain Muscle spasm Total Pathologic data‡ Tumor size (cm) Mean Range Positive surgical margin (n) Pathologic stage (n) pT0§ pT1a pT1b Histologic findings (n) Malignant Clear cell RCC Chromophobe RCC Papillary RCC
Lower Pole LPN (n ⫽ 33)
P Value*
Upper Pole LPN (n ⫽ 20)
0.70 236 122–396 0.55 0.91
0.48 0.98
2.7 1–7
1 1 (3) 0 1 (3) 1 0 2 (6) 0 1 0 0 0 0 1 1 3 (9)
0.63
5.8 4–9
0.04
0.68
0.17
0 0 1 1 (4)
0.45
0 0
0.94
0 0
0.07
0 3 (17) 1 0 4 (22)
0.21
0 0 1 1 1 1 0 0 4 (22)
0.08
0.37 0.97
0.24
1.4 0.7–5.9 1 (4) 0 1
1 (6) 1 1 3 (17)
6 (19) 24 (75) 2 (6)
0.06 0.83
1 (4) 1 (4) 0 4 (17) 6 (25)
0.40
2 0 1 0 0 0 0 0 3 (12)
0.17
0.05 2.3 0.9–4.1 1 (5)
0.45 0.89
3 (17) 14 (78) 1 (5) 0.85
26 (81) 20 3 3
— 0.002
21 (88) 3 (12) NA
0.21 1.2 0.8–2.1 5 (25) 2 3
0.06 2.9 0.8–4.6 0
23.5 15–38
2.8 1–14
0.05
306 100–800
0.50 13 (80) 7 (20) 2 (10)
0.72
3 (9) 1 0 4 (12)
⬍0.001
32.4 13–75 0.45
1.2 0.6–2.2 2 (6) 1 1
187 110–260 0.006
197 5–600
34.3 20–55
Upper Pole OPN (n ⫽ 24)
0.02 244 140–447
244 20–1700
18 (55) 15 (45) 1 (3)
P Value†
3.2 1.3–5 0 3 (13) 19 (79) 2 (8)
0.70 15 (83) 12 1 2
21 (87) 15 2 4 Continued
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UROLOGY 70 (1), 2007
Table 2. Continued Variable Benign Oncocytoma Angiomyolipoma Benign cyst
Lower Pole LPN (n ⫽ 33) 6 (19) 2 3 1
P Value*
Upper Pole LPN (n ⫽ 20)
P Value†
Upper Pole OPN (n ⫽ 24)
3 (17) 0 0 3
3 (13) 0 1 2
OR ⫽ operating room; EBL ⫽ estimated blood loss; UTI ⫽ urinary tract infection; RCC ⫽ renal cell carcinoma; other abbreviations as in Table 1. Data in parentheses are percentages. * Between lower pole and upper pole LPN. † Between upper pole LPN and upper pole OPN. ‡ Excluding open conversions. § Pathologic benign disease.
with LPN in patients with upper pole renal tumors, describing the modifications in operative technique to address the technical considerations. We also retrospectively reviewed our results with LPN and compared cohorts of LPN of lower pole tumors and OPN of upper pole lesions.
MATERIAL AND METHODS A review of our database from October 2002 through February 2006 was performed after obtaining institutional review board approval. A total of 256 laparoscopic procedures for patients with renal tumors were performed at our institution by a single surgeon (A.L.S.), of which 166 were laparoscopic radical nephrectomy and 90 were LPN. Patients with a localized renal tumor with a normal contralateral kidney were included in the review. Patients with tumors involving the middle pole were excluded from the study. A total of 20 patients underwent LPN for upper pole lesions (UPLPN group) and 33 patients underwent LPN for lower pole lesions (LPLPN group). A “tumor size”-matched cohort of 24 patients who underwent OPN for upper pole tumors (UPOPN group) were randomly selected from our database of 186 OPNs performed from April 1995 to July 2005 by an open surgeon (G.D.S.). Preoperatively, the patients were evaluated with a medical history, physical examination, urinalysis, chest x-ray, laboratory studies, including serum creatinine determinations, and abdominal computed tomography to allow for intraoperative surgical planning. The tumors were characterized as described by Finley et al.12: tumor that extended less than 40%, 40% to 60%, and more than 60% off the natural surface of the kidney was defined as endophytic, mesophytic, and exophytic, respectively.
LPN Surgical Technique Our LPN technique has previously been reported.8,13–15 In brief, after hilar dissection, a laparoscopic ultrasonic probe was used to delineate the tumor extent. Vascular clamping was performed using endoscopic bulldog clamps (Klein Surgical, San Antonio, Tex). Tumor excision was performed with cold scissors, maintaining a safety margin of normal parenchyma of at least 0.5 cm. Argon beam coagulation of the tumor bed, followed by freehand suturing of the collecting system and major bleeding sites, anchored and secured with a LapraTy clip, was then completed. Defect closure was completed with individual parenchymal sutures, securely cinched with the LapraTy UROLOGY 70 (1), 2007
clip. FloSeal was then placed in the closed defect space to further secure hemostasis.
Upper Pole LPN: Triangulation Technique Our technical alterations for LPN have been previously described with modifications depending on the tumor location.8,16 In brief, after mobilizing the entire kidney, the perinephric fat was dissected off the capsule, except for the peritumoral fat, which was left over the tumor. Intraoperative ultrasonography was used to delineate the tumor margins. Depending on the exact tumor location, a suspensory traction system was used to optimize and stabilize the kidney position. This traction suture with a LapraTy clip on its end was passed as a figure-of-eight, 2 mm deep and 1.5 cm along the renal capsule, and then brought out through a preplanned site in the abdominal wall using a Carter-Thomason suture closure device. The suture location on the renal capsule, the direction of traction, and the abdominal placement of the suture all depend on the anteroposterior location of the tumor and whether it was a polar, medial, or lateral tumor. A hemostat held the suture extracorporeally at the level of the skin. The suspension created by the traction suture allowed the kidney to be positioned for optimal tumor visualization, excision, and suturing (triangulation between the two working laparoscopic instruments; Fig. 1). The sling was used for all upper pole tumors and only as needed (17%) for the lower pole tumors.
OPN Surgical Technique OPN was routinely performed through a transperitoneal approach. Intraoperative ultrasonography helped delineate the tumor margins. Unlike LPN, in which the ischemia time occurred in a warm environment, OPN was performed with ice cooling of the kidney. After cold scissor tumor excision with sufficient margins, argon beam coagulation of the renal defect was performed. Injury of the collecting system was then repaired with sutures, followed by meticulous oversewing of the individual blood vessels. Parenchymal closure was performed with individual sutures with Surgicel bolsters for tissue compression.
Statistical Analysis Statistical comparisons were made between cohorts using baseline demographic data and were compared using the chi-square test. Continuous variables are shown as mean values and compared using Student’s t tests and Fisher’s exact test, with correlation between variables performed using the Pearson’s cor31
relation coefficients, with P ⬍0.05 considered statistically significant.
RESULTS The baseline patient demographics are summarized in Table 1. Three groups (UPLPN, LPLPN, and UPOPN) were compared according to surgical approach and tumor location. Age, sex, body mass index, American Society of Anesthesiologist scores, and preoperative serum creatinine levels were similar between the UPLPN group and the other groups. The mean radiographic tumor size in the UPLPN group was comparable with that in the LPLPN group (2.4 versus 3.1 cm, P ⫽ 0.08). Similarly, no significant difference was noted in the tumor size between the UPLPN and UPOPN groups (2.4 versus 2.8 cm, P ⫽ 0.10). The tumors were mostly exophytic in all groups, with no significant differences in tumor depth among the groups. No differences were noted in tumor location (anterior, posterior, or lateral) or tumor literality between the UPLPN group and the other study groups. The intraoperative data are summarized in Table 2. The mean operative time, estimated blood loss, and ischemia time were not significantly different between the UPLPN and LPLPN groups. The UPOPN group, however had a significantly shorter mean operative time (187 versus 244 minutes, P ⫽ 0.02), shorter ischemia time (23.5 versus 32.4 minutes, P ⬍0.001), and higher estimated blood loss (306 versus 197 mL, P ⫽ 0.006) compared with the UPLPN group. All patients in the UPOPN group required collecting system repair compared with 65% and 55% in the LPLPN and UPLPN groups, respectively. One open conversion (3%) was required in the LPLPN group and two (10%) in the UPLPN group (P ⫽ 0.48). The LPLPN open conversion occurred because of persistent parenchymal bleeding on hilar unclamping. An attempt at laparoscopic resuturing was unsuccessful before a decision to convert to an open approach was made. Of the 2 patients requiring open conversion in the UPLPN group, 1 had brisk renal arterial bleeding after an injury to the renal artery and 1 had positive margins on frozen section analysis. As expected, the hospital stay was significantly longer for the UPOPN group than for the UPLPN group (P ⫽ 0.002). A similar hospital stay length was noted between the LPLPN and UPLPN groups. The incidence of major and minor intraoperative complications was similar among all groups (Table 2). The incidence of major postoperative complications was greater in the UPLPN group than in the LPLPN group (22% versus 6%, P ⫽ 0.07). Most such complications were hemorrhagic (17% versus 3%, P ⫽ 0.08). In the UPOPN group, 1 patient had a perinephric fluid collection secondary to a urine leak that eventually resolved after radiographic replacement of a Jackson-Pratt drain. The incidence of minor postoperative complications did not differ significantly among the three groups. 32
Renal cell carcinoma was confirmed in 83%, 81%, and 87% of the patients in the UPLPN, LPLPN, and UPOPN groups, respectively. The mean pathologic size was significantly larger in the UPOPN group than in the UPLPN group (3.2 versus 2.3 cm, P ⫽ 0.05). Other than the 1 patient in the UPLPN group with a positive surgical margin noted intraoperatively whose surgery was converted to an open approach for management, no other positive surgical margin was noted in all groups on final pathologic examination.
COMMENT OPN remains the established standard for NSS of renal tumors.16 Recently published series have stated that “elective” NSS provides optimal long-term oncologic efficacy in properly selected patients with localized renal cell carcinoma.18 With the expanding criteria for NSS and the advancement of laparoscopic instrumentation and pharmaceutical hemostatic agents, the indications for this procedure have expanded. Because of rib cage encasement, upper pole lesions represent a significant technical challenge for the open, and more so for the laparoscopic, approach. The limited visualization and compromised tumor positioning for rapid and efficient suturing of resected upper pole tumors are an impediment to the novice laparoscopist. This difficult anatomic tumor location is the reason many patients with a small renal tumor in the upper pole who might otherwise be a candidate for NSS are undergoing OPN or laparoscopic radical nephrectomy.19 In our series, we used techniques to facilitate renal positioning (using a suspension traction system and other modifications), thereby allowing better upper pole access for precise tumor excision and efficient hemostasis and renal reconstruction during the critical steps of LPN16 (Fig. 1). The principle of leaving a handle of fat on top of the tumor is very helpful in providing increased maneuverability after renal positioning by the traction system. Our data have demonstrated the similarity in operative outcomes in both LPN groups, which could be attributed to our surgical modifications. In their initial LPN experience, Ramani et al.20 reported that the most common complications were related to intraoperative hemorrhage. Our study demonstrated comparable intraoperative hemorrhage results with a similar incidence in the UPLPN and LPLPN groups (P ⫽ 0.63). The likely causes of persistent parenchymal bleeding were an unoccluded renal artery in the setting of multiple vessels or bulldog clamp malfunction, both of which were not associated with the primary location of the tumor. Our study did demonstrate that upper pole renal tumors, relative to lower pole tumors, were associated with a trend toward a greater incidence of postoperative hemorrhage after LPN, although statistical significance was not reached (17% versus 3%, P ⫽ 0.08). These complications occurred even though complete hemostasis on UROLOGY 70 (1), 2007
hilar unclamping had been noted in all cases. No obvious precipitating factor could be found in these cases, although inadequate parenchymal repair might be the most plausible explanation. Gill et al.21 emphasized that the best management of postresection parenchymal hemorrhage is preventive through well-functioning vascular instruments for hilar control and meticulous oversewing of transected vessels. Our results are similar to previously reported series by Gill et al.21 in that LPN, compared with OPN, required a longer warm ischemia time and resulted in less blood loss, shorter hospital stay, and more rapid convalescence. They also concluded that LPN was associated with a greater incidence of intraoperative and renal/urologic complications compared with those in the open group.21 In our study, despite the larger pathologic tumor size in the open group compared with the laparoscopic upper pole group, the latter had a greater incidence of intraoperative and postoperative hemorrhagic complications. No urinary leakage was observed in either LPN group, and 1 patient in the OPN group (5%) had a significant postoperative urine leak. This difference could have been related to the larger pathologic tumor size (requiring deeper resection) and greater need for collecting system repair in the OPN group. Other series have reported similar urinary leakage rates after OPN.22 Our data have reaffirmed that watertight suture repair of the collecting system can be accomplished with similar efficacy using the laparoscopic approach regardless of tumor location. This study had several limitations that warrant discussion. The retrospective nature of the study using data from a single institution, with small patient numbers, must be noted. Furthermore, the comparison between two surgeons’ experience also might have added an inherent weakness to the study. However, a cohort of patients with upper pole lesions of comparable radiologic tumor size was selected from the OPN database for comparison. A significant difference between the radiographic and pathologic tumor size was noted. Such a change could have been related to the three-dimensional tumor configuration, in that the largest radiographic measurement taken with standard axial imaging might not have been accurate, especially for the OPN group for whom the imaging was performed between 1995 and 2005. Ultimately, the UPOPN group had a significantly larger tumor size compared with those of the UPLPN group. Our study has highlighted the technical feasibility of LPN in upper pole tumors. The similarity in the operative outcomes between the UPLPN and LPLPN groups has proved that the difficulty associated with tumor location can be overcome with modifications in surgical technique. With regard to positive surgical margins, the results in our LPN groups were comparable with those of other OPN21,23,24 and LPN series.6,17,18,21,25 However, it is important to realize that this procedure is associated with a very steep learning curve.25,26 At present, OPN UROLOGY 70 (1), 2007
still offers lower complication rates compared with the laparoscopic approach. We believe that with continuous growth in experience and additional developments in technique and pharmacologic and hemostatic tools, achieving comparable results to OPN could be possible.
CONCLUSIONS LPN can be performed in patients with peripheral small renal tumors, regardless of location. We believe that with technical modifications, LPN for upper pole lesions can be performed with optimal tumor positioning for excision and repair, thereby replicating surgery for lower pole tumors. The decision to perform NSS laparoscopically will ultimately depend on the surgeon’s level of experience. Performing open NSS is still the standard of care because it seems to result in fewer complications and reduce the risk of ischemic damage to the kidney. References 1. Albqami N, and Janetschek G: Laparoscopic partial nephrectomy. Curr Opin Urol 15: 306 –311, 2005. 2. Finelli A, and Gill IS: Laparoscopic partial nephrectomy: contemporary technique and results. Urol Oncol 22: 139 –144, 2004. 3. Gill IS, Colombo JR Jr, Frank I, et al: Laparoscopic partial nephrectomy for hilar tumors. J Urol 174: 850 – 854, 2005. 4. Reisiger K, Venkatesh R, Figenshau RS, et al: Complex laparoscopic partial nephrectomy for renal hilar tumors. Urology 65: 888 – 891, 2005. 5. Finelli A, Gill IS, Desai MM, et al: Laparoscopic heminephrectomy for tumor. Urology 65: 473– 478, 2005. 6. Rassweiler JJ, Abbou C, Janetschek G, et al: Laparoscopic partial nephrectomy: the European experience. Urol Clin North Am 27: 721–736, 2000. 7. Gerber GS, and Stockton BR: Trends in endourologic practice: laparoscopic partial nephrectomy. J Endourol 19: 21–24, 2005. 8. Orvieto MA, Chien GW, Tolhurst SR, et al: Simplifying laparoscopic partial nephrectomy: technical considerations for reproducible outcomes. Urology 66: 976 –980, 2005. 9. Weld JW, Venkatesh R, Huang J, et al: Evolution of surgical technique and patient outcomes for laparoscopic partial nephrectomy. Urology 67: 502–507, 2006. 10. Desai MM, Gill IS, Ramani AP, et al: The impact of warm ischaemia on renal function after laparoscopic partial nephrectomy. BJU Int 95: 377–383, 2005. 11. Ramani AP, Abreu SC, Desai MM, et al: Laparoscopic upper pole nephrectomy with concomitant en bloc adrenalectomy. Urology 62: 223–226, 2003. 12. Finley DS, Lee DI, Eichel L, et al: Fibrin glue-oxidized cellulose sandwich for laparoscopic wedge resection of small renal lesions. J Urol 173: 1477–1481, 2005. 13. Orvieto MA, Chien GW, Laven B, et al: Eliminating knot tying during warm ischemia time for laparoscopic partial nephrectomy. J Urol 174: 2292–2295, 2004. 14. Orvieto MA, Chien GW, Tolhurst, et al: Simplifying laparoscopic partial nephrectomy: technical considerations for reproducible outcomes. Urology 66: 976 –980, 2005. 15. Shalhav AL, Orvieto MA, Chien GW, et al: Minimizing knot tying during reconstructive laparoscopic urology. Urology 63: 508 –513, 2006. 16. Chien GW, Orvieto MA, Chuang MS, et al: Use of suspension traction system for renal positioning during laparoscopic partial nephrectomy. J Endourol 19: 406 – 409, 2005. 17. Gill IS, Desai MM, Kaouk JH, et al: Laparoscopic partial nephrectomy for renal tumor: duplicating open surgical techniques. J Urol 167: 469 – 476, 2002.
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18. Moinzadeh A, Gill IS, Finelli A, et al: Laparoscopic partial nephrectomy: 3 year followup. J Urol 175: 459 – 462, 2006. 19. Best S, Ercole B, Lee C, et al: Minimally invasive therapy for renal cell carcinoma: is there a new community standard? Urology 64: 22–25, 2004. 20. Ramani AP, Desai MM, Steinberg AP, et al: Complications of laparoscopic partial nephrectomy in 200 cases. J Urol 173: 52– 47, 2005. 21. Gill IS, Matin SF, Desai MM, et al: Comparative analysis of laparoscopic versus open partial nephrectomy for renal tumors in 200 patients. J Urol 170: 64 – 68, 2003. 22. Beasley KA, Al Omar M, Shaikh A, et al: Laparoscopic versus open partial nephrectomy. Urology 64: 458 – 461, 2004.
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23. Thompson RH, Leibovich BC, Lohse CM, et al: Complications of contemporary open nephron sparing surgery: a single institution experience. J Urol 174: 855– 858, 2005. 24. Gerard C, Ballereau C, Leroy X, et al: Long-term oncological results after conservative surgery for unifocal renal cancer. Prog Urol 13: 14 –22, 2003. 25. Link RE, Bhayani SB, Allaf ME, et al: Exploring the learning curve, pathological outcomes and perioperative morbidity of laparoscopic partial nephrectomy performed for renal mass. J Urol 173: 64 – 68, 2003. 26. Sutherland SE, Resnick MI, Maclennan GT, et al: Does the size of surgical margin in partial nephrectomy for renal cell cancer really matter? J Urol 167: 61– 64, 2002.
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