Prospective Study Comparing Two Techniques of Renal Clamping in Laparoscopic Partial Nephrectomy: Impact on Perioperative Parameters

Abstract

Purpose:

To compare en bloc and artery-only clamping techniques on renal function and perioperative outcomes after laparoscopic partial nephrectomy (LPN).

Patients and Methods:

From March 2003 to December 2008, 205 patients underwent LPN by one surgeon in a single institution. The first 103 LPNs were achieved with artery-only clamping (AO), and the last 102 LPNs were realized under control of the renal hilum (artery and vein [AV] clamping). Renal function was evaluated by creatinine changes, estimation of the glomerular filtration rate (eGFR), and assessment of split renal function using renal mercaptoacetyl triglycine-Lasix scintigraphy. Sixty-two of 205 patients had renal scintigraphy before and after surgery.

Results:

There was no significant difference between the two groups regarding demographic data and renal mass characteristics. Warm ischemia time (WIT) was higher in the AO group: 30.4±8.2 vs 23.3 minutes±10.0 (P<0.0001). The eGFR change was significantly lower in the AV group during the postoperative period: 10.2 mL/min vs 13.7 mL/min (P=0.0472). Operative blood loss, operative time, and complication rate were not statistically different between groups. Average loss of differential function of the operated kidney was 13.6±9.2% for the AO group and 14.3±12.3% for the AV group (P=0.8016). On multivariate analysis, clamping technique was not a predictive factor of renal function reduction.

Conclusion:

AV and AO techniques are associated with similar renal function outcomes in patients who were undergoing LPN. In our series, the AV technique was associated with a lower WIT, an important predictor of decrease in renal function.

Introduction

D uring the last decade, nephron-sparing surgeries (NSS), such as partial nephrectomy (PN), cryoablation, and radiofrequency ablation have gained in popularity. PN has become the gold standard for the treatment of patients with small renal tumors.^1,2 Laparoscopic partial nephrectomy (LPN) is now considered an alternative to the open approach. LPN is technically challenging and a number of modifications to the original technique have been developed to facilitate the surgery. To reduce acute kidney injury, urologists have described PN techniques such as “parenchymal,” “selective” renal artery clamping, on-demand clamping, early unclamping, and no clamping techniques.

Among the renal artery clamping techniques, the artery and vein clamping of the renal hilum (AV) prevents venous backflow during tumorectomy, allowing better visualization of the renal tumor margins and ensuring occlusion of secondary arteries.³ Despite its obvious technical advantages, AV control has not been widely accepted, because animal and a recent human study have shown that it might alter renal function.^4
–6 These studies, however, were limited by short-term follow-up and lack of a multivariate statistical analysis. Because acute renal injuries are often at least partially reversible, the permanent effects of the clamping technique remain unknown.

At our institution, we have modified our renal artery clamping technique during LPN, switching from a control of the artery alone (AO) to a complete en-bloc (AV) clamping of the renal hilum. In this study, we compared the effect of the two clamping techniques on short- and long-term renal function (RF) as well as on the renal differential function.

Materials and Methods

Data collection and patient selection

The ethical committee of our institution approved this project. Between March 2003 and December 2008, we identified 205 consecutive patients who underwent LPN by a single surgeon at our institution for organ-confined tumors on preoperative imaging. All procedures were performed by one surgeon in a single institution. The transperitoneal approach was generally used. The first 103 LPN were achieved with AO clamping with a bulldog clamp. The last 102 LPN were performed under renal hilum control (AV) with a Satinsky clamp. Selection criteria included all surgically eligible patients with localized enhancing renal masses. There were no absolute exclusions based on tumor size or location.

Clinical parameters such as patient age, sex, serum creatinine level, operative time, estimated blood loss, tumor size, histopathology, tumor grade, and imaging were collected prospectively. The presence of comorbidities was evaluated using the American Society of Anesthesiologists (ASA) scale. Chest radiography and CT were performed before the surgery in all patients to exclude metastasis. Tumor size was defined as the longest single dimension of the lesion measured on the CT scan. The localization of the tumor was defined as stage A, B, or C as proposed by Johnston and associates.⁷ The stages are: A stage, a mass that is exophytic involving less than 5 mm of renal parenchyma; B stage, a mass that penetrates more than 5 mm in the renal parenchyma, while a C stage mass is less than 5 mm from the renal sinus. Specimen volume was calculated according to the tumor size on pathologic specimen (volume=4/3IIabc). Postoperative complications were analyzed according to the modified Clavien classification.⁸

Preoperative preparation and surgical technique

All patients underwent standard preoperative medical optimization. Mechanical bowel preparation and prophylactic intravenous antibiotics were used. Preoperatively, intravenous fluids were administered to achieve an euvolemic state. For some patients, a ureteral catheter connected to a syringe filled with diluted methylene blue was placed cystoscopically in patients with tumors that abutted the collecting system on imaging.

The surgical techniques for transperitoneal and retroperitoneal LPN are detailed in a previous publication from our institution.^9,10 Briefly, initial dissection is directed toward defining the renal hilum. Renal vessels are meticulously dissected and prepared for cross-clamping. A 10 MHz, 1 cm ultrasound probe (B-K Medical, Herlev, Denmark) is used to help localize tumors, define the margins of parenchymal resection, and identify the adjacent vasculature. The resection margin on the renal capsule is marked with a bipolar electrode. After achieving diuresis with intravenous mannitol (12.5 g), the renal hilum is cross-clamped with a noncrushing laparoscopic bulldog clamps (Aesculap, Melsungen, Germany) or bluntly with a 5-mm Satinsky clamp (Aesculap, Melsungen, Germany).

Cold excision of the tumor is performed using 5-mm. In all cases, renal repair begins with a running 2-0 or 3-0 Maxon™ to close the collecting system and ligate or repair vascular defects. Parenchymal closure is achieved with a first layer of 2-0 Maxon running suture. The second layer is done with 2-0 Polysorb™ buttress sutures if necessary. The sutures are end-loaded with Hem-o-lok® clips (Teleflex Inc, Limerick, PA). Other Hem-o-lok clips are added after each running suture passage to avoid renal capsule shearing. FloSeal™ (Baxter, Deerfield, IL) is used to fill the deep portion of the parenchymal defect. Polyglactin mesh rolls (surgical) are placed to fill the parenchymal void and stabilize by tying down the buttress sutures. The kidney is then reperfused by removing the hilar clamps.

The tumor is removed using an Endo Catch™ bag (Covidien, Mansfield, MA). A perinephric Jackson-Pratt drain is placed through the most posterior or lateral port site. The ureteral catheter is generally removed 1 day postoperatively. The drain is removed when drainage decreases below 30 mL per 24 hours and after a renal scan has ruled out urine leak 7 to 10 days postoperatively. Patients are discharged to home when they are ambulatory and can tolerate a regular diet.

Follow-up

Serum creatinine was measured preoperatively and postoperatively at day 1, 3 months, and at the last follow-up. Routine follow-up includes a biannual serum creatinine measurement. Estimated glomerular filtration rate (eGFR) was calculated using the Modification of Diet in Renal Disease (MDRD) study equation (mL/min/1.73 m²). Finally, renal differential function was evaluated by assessing the split RF using renal mercaptoacetyl triglycine-Lasix scintigraphy. Sixty-two patients had renal scintigraphy before and after surgery (46 patients in the AO group and 16 patients in the AV group). CT or MRI was performed at 6-month or at 1-year intervals thereafter according to the tumor's pathology.

Statistical analysis

Both groups were compared for demographics, renal mass characteristics, operative and postoperative data, and RF. The statistical analysis was based on the Pearson chi-square test or the Fisher exact test for the qualitative values and on the Student t test for the quantitative values. Potential factors affecting RF were identified and analyzed in relation to the reduction in eGFR according to the MDRD equation and the renal scintigraphy. Multivariate regression was used for the determination of independent variable predictive of postoperative RF deterioration. The stepwise method was used. A P value of 0.05 or less was set for significance.

Results

Preoperative and perioperative patient characteristics of our cohorts

Data are summarized in Table 1. Preoperative data were not statistically different between AO and AV groups with the exception of the ASA score, which was higher in the AV group (58.5% vs 26.3%, P≤0.0001). AO and AV groups had, respectively, 44 and 15 months of median follow-up (P≤0.0001). Both groups had comparable characteristics regarding side, CT size, tumor volume, clinical stage, pathologic diagnosis, and Fuhrman grade. Of note, tumors of intrarenal stage C were more prevalent in the AV group, reaching almost the statistical significance (52.2% vs 36.0%, P=0.0712). Operative and perioperative characteristics are summarized in Table 2. Importantly, clamping time was significantly shorter in the AV group (23.3 min vs 30.4 min, P≤0.0001) despite a trend toward more endophytic and larger tumors than in the AO group. Also, postoperative general complications were equivalent in both groups (P=0.4545).

Table 1.

Preoperative Patient Characteristics

Variables	Artery only (AO) N=103	En-bloc (AV) N=102	All N=205	P value
Age (y)	59.9	59.4	59.6	0.7545
Min;max	32;83	24;87	24;87
Sex (%)
Female	50 (48.5)	44 (43.6)	94 (46.1)	0.4756
Male	53 (51.5)	57 (56.4)	110 (53.9)
ASA scale (%)
1	57 (57.6)	19 (23.2)	76 (42.0)	≤0.0001
2	26 (26.3)	48 (58.5)	74 (40.9)
3	16 (16.2)	15 (18.3)	31 (17.1)
Diabetes (%)
No	80 (83.3)	73 (79.4)	153 (81.4)	0.4828
Yes	16 (16.7)	19 (20.7)	35 (18.6)
BMI	28.5	29.4	28.9	0.2968
Min;max	17;45	17;58	17;58
Median follow-up (mos)	44	15	29	≤0.0001
Min;max	29;65	2;28	2;65
Side (%)
Right	48 (46.6)	57 (56.4)	105 (51.5)	0.1600
Left	55 (53.4)	44 (43.6)	99 (48.5)
Tumor location (%)
A (<5 mm incursion)	23 (23.0)	14 (15.2)	37 (19.3)	0.0712
B (>5 mm incursion)	41 (41.0)	30 (32.6)	71 (37.0)
C (w/in 5 mm sinus)	36 (36.0)	48 (52.2)	84 (43.8)
CT size (mm)	32.0	34.7	33.1	0.2444
Tumor volume (cm³)	23.6	38.8	30.2	0.2231
Clinical stage (%)				0.1639
PT_1a	72 (69.9)	73 (76.8)	145 (73.2)
PT_1b	16 (15.5)	12 (12.6)	28 (14.1)
PT₂	2 (1.9)	5 (5.3)	7 (3.5)
PT_3a	13 (12.6)	5 (5.3)	18 (9.1)
Pathologic diagnosis (%)
RCC	80 (78.4)	76 (78.4)	156 (78.4)	0.9889
Benign lesion	22 (21.6)	21 (21.7)	43 (21.6)
Fuhrman grade (%)
1–2	53 (73.6)	40 (76.9)	93 (75.0) 31	0.8365
3–4	19 (26.4)	12 (23.1)	(25.0)

ASA=American Society of Anesthesiologists; BMI=body mass index; CT=computed tomography; RCC=renal-cell carcinoma.

Table 2.

Perioperative Characteristics

Variables	Artery only (AO) N=103	En-bloc (AV) N=102	P value
Operative time (min)	126.7±32	122.4±37.5	0.4133
Clamping time (min)	30.4±8.2	23.3±10.0	≤0.0001
Blood loss (mL)	199.0±300.6	160.1±198.4	0.2816
Transfusion (%)	5.8	7.4	0.6902
Overall complications using Clavien classification (%)
I	5.8	6.0	0.4545
II	17.5	17.0
III	17.5	10.0
IV	1	0
V	0	0
Urine leak (%)	11.7	8.0	0.3829
Hospital stay (d)	4.5	3.9	0.1218

RF outcomes

Patients who underwent AV clamping had a lower change in serum creatinine (12.0 m/L vs 18.0 m/L, P=0.0168) and eGFR (71.0 mL/min vs 65.1 mL/min, P=0.0435) during the immediate postoperative period (Table 3). There was no significant difference at 3 months and at the time of the final follow-up, however. Loss of renal differential function (RDF) during the postoperative period was the same for both groups (13.6% vs 14.3%, P=0.8096) (Table 4). Overall, postoperative RDF of the operated kidney was 40%±13.5 for the AV group and 35%±11.0 for the AO group (P=0.2053).

Table 3.

Comparison of Renal Function Outcomes for Renal Artery Only or En-Bloc Hilar Clampings by Estimated Glomerular Filtration Rate and Creatinine Changes

	AO	AV	P value
Creatinine change (μmol/L)
Postoperative	18.0	12.0	0.0168
3 months	9.3	11.3	0.4401
Final	12.8	7.5	0.3859
MDRD change (cc/min/1.73 m²)
Postoperative	13.7	10.2	0.0472
3 months	8.1	10.0	0.4716
Final	7.2	3.3	0.3476

AO=artery only; AV=arteriovenous; MDRD=Modification of Diet in Renal Disease.

Table 4.

Comparison of Renal Function Outcomes for Renal Artery Only or En Bloc Hilar Clampings by Renal Scintigraphic Changes of the Operated Kidney

	AO (n=46)	AV (n=16)	P value
Postoperative (n=62)	13.6	14.3	0.8096

AO=artery only; AV=arteriovenous.

On univariate analysis, characteristics associated with loss of eGFR were sex (greater change of RF in men), warm ischemia time (WIT), and preoperative RF (Table 5). When looking at the eGFR changes at 3 months, preoperative RF and body mass index were the statistically associated factors. Loss of RDF on renal scintigraphy was associated with tumor location and WIT but not the clamping technique. On multivariate analysis, clamping technique was not a predictive factor of eGFR or scintigraphy changes (Table 6). Preoperative RF was predictive of eGFR change during the postoperative period (β=0.2273, P≤0.001) and at 3 months (β=0.2606, P≤0.001). WIT was significant for the postoperative eGFR change (β=0.2877, P=0.0018) and the loss of RDF (β=0.5959, P≤0.001). Finally, location of the tumor was a significant factor associated with loss of RDF (A vs C, β=−5.5829, P=0.03).

Table 5.

Predictive Factors of Renal Function Reduction After Laparoscopic Partial Nephrectomy: Univariate Analysis

	ΔΔMDRD (postoperative) P value	ΔΔMDRD (3 months) P value	ΔΔ Scintigraphy P value
Age	0.1192	0.2825	0.6599
Sex	0.0141	0.3040	0.3488
BMI	0.8487	0.0366	0.9363
Diabetes	0.5157	0.8793	0.1558
Tumor location	0.2340	0.3186	0.0115
CT size	0.5392	0.3119	0.0676
Warm ischemia time	0.0006	0.4330	≤0.0001
Technique (AO vs AV)	0.0472	0.4716	0.8096
Tumor volume	0.9296	0.9167	0.2704
Preoperative renal function	≤0.0001	≤0.0001	0.8165

MDRD=Modification of Diet in Renal Disease; BMI=body mass index; CT=computed tomography; AO=artery only; AV=arteriovenous.

Table 6.

Factors Associated with Loss of Renal Differential Function After Laparoscopic Partial Nephrectomy in Multivariate Analysis

	ΔMDRD (postoperative)			ΔMDRD (3 months)			ΔScintigraphy
Variables	Estimate	SD	P value	Estimate	SD	P value	Estimate	SD	P value
Warm ischemia time	0.2877	0.09	0.0018	NS		NS	0.5959	0.11	≤0.0001
Preoperative renal function	0.2273	0.04	≤0.0001	0.2606	0.05	≤0.0001	NS		NS
Tumor location (A vs C)	NS		NS	NS		NS	−5.5829	2.5	0.0300
Technique (AO vs AV)	NS		NS	NS		NS	NS		NS

MDRD=Modification of Diet in Renal Disease; SD=standard deviation; NS=not statistically significant; AO=artery only; AV=arteriovenous.

Discussion

The interest in nephron-sparing techniques has heightened in recent years, especially after the publication of Go and colleagues¹¹ who correlated cardiovascular events and overall survival with eGFR.¹¹ NSS has now emerged as the gold standard treatment for small renal masses achieving equivalent oncologic outcomes and superior RF when compared with radical nephrectomy (RN).^1,2,12
–14 Indeed, there is some evidence that NSS may be associated with a better overall survival in pT_1a renal masses compared with RN, possibly secondary to the decrease of long-term renal impairment.¹⁵ Therefore, identifying technical factors that can facilitate NSS or improve postoperative RF is of paramount importance.

In this series, we compared 103 patients who underwent LPN with artery-only clamping with 102 patients in which en-bloc clamping was used. We found that the clamping technique was not an independent predictive factor of postoperative RF deterioration. Moreover, we observed a significant reduction of 7 minutes of WIT in the AV group compared with the AO group.

The influence of clamping technique on RF outcomes remains unclear in the literature. Some studies performed in animals have demonstrated the benefit of AQ occlusion during open partial nephrectomy (OPN).^4,5 The physiologic explanation of this findings is that the AO technique allows retrograde venous blood flow and partial oxygenation of the parenchyma.^4,5 Only two studies, however, have looked at the effects of the clamping technique after LPN. Orvieto and coworkers¹⁶ compared AO vs AV clamping technique effects on RF during laparoscopic and OPN using a single-kidney porcine model. The open approach was associated with a lower serum creatinine change on postoperative day (POD) 1 and 3 in the AO group when compared with the AV group. This benefit, however, was not observed in the laparoscopic group. Moreover, the more important long-term effects were not reported. The authors postulated that during LPN, the pneumoperitoneum pressure may impair venous backflow, negating the benefits of clamping the artery alone. Subsequently, the same team compared RF outcomes between AO vs AV hilar clamping techniques during LPN in humans.⁶ Consistent with the porcine model, immediate POD 1 eGFR was not statistically different from the preoperative eGFR in the AO group while a significant change in the eGFR was seen in the AV group. Based on a univariate analysis, the authors concluded that AO occlusion may provide a superior RF after LPN. Unfortunately, no data regarding the intraparenchymal tumor depth, operated kidney RDF change, or long-term eGFR outcomes were provided, which limited the conclusions. Moreover, no statistically significant difference in eGFR was seen between AO and AV groups. These results, despite being interesting, did not completely address the question of the optimum hilar clamping technique to preserve RF.

In our series, despite increased study power, evaluation of the RDF on the operated kidney, and multivariate analysis, we did not observe significant deleterious effects of AV clamping on immediate and late RF. Unexpectedly, the AV technique was associated with improved RF in the immediate postoperative period and decreased blood loss. We believe that these results are explained in part by improved resection margin visualization during tumorectomy and reduced WIT for the AV group. The AV clamping technique creates a relatively bloodless field, which minimizes the amount of normal parenchyma that is removed, a factor known to be associated with postoperative RF.¹⁷ Moreover, the AV clamping technique allows a less extensive dissection of the artery and vein, decreasing the risk of vascular trauma and ensuring occlusion of polar arteries if there is. Finally, it has been shown that Satinsky vascular clamps generate stronger clamping than bulldog clamps.¹⁸ In our opinion, this characteristic allows a better vascular occlusion together with a better stability of the clamp on the renal vessels.

The impact of WIT on postoperative kidney function and on renal metabolism has been studied extensively during NSS.^19
–21 It is well established that WIT time is one of the strongest modifiable risk factors for renal impairment after PN.²² Based on this principle, some surgeons recommend reducing WIT to a minimum. This has prompted the development of a number of innovative clamping techniques such as “parenchymal,” “on-demand,” “early unclamping,” “no clamp,” and “selective renal clamping” for which the long-term results on RF are still maturing.^23,24 Moreover, some studies have shown a benefit on late RF associated with no vascular clamping compared with hilar clamping in OPN.^25

–28 These new approaches challenge the already complex debate regarding the best clamping technique during PN to preserve long-term RF. In our opinion, any clamping technique that could reduce WIT without increasing the surgical morbidity should be favored.

Recent advances in minimally invasive surgery have been done with the introduction of robot-assisted laparoscopic partial nephrectomy (RLPN) in which RF preservation and renal clamping technique remain important points of concern. Some studies have shown that RLPN could be associated with a shorter WIT when compared with LPN.^29,30 It is unknown, however, if this finding would still be observed if the PN would be performed by an experienced pure laparoscopic surgeon, keeping in mind that the main advantage of the robot is to facilitate tumorectomy and renal defect closure.

In addition to WIT, we identified other factors associated with a loss of RF in multivariate analysis. Of those, the preoperative RF was statistically associated with postoperative lost of eGFR in both the early postoperative period and at 3 months (P≤0.0001). This result confirms findings of other studies and reflects the inability of the contralateral kidney to compensate for the operated kidney renal mass loss when RF is already compromised.²² Furthermore, it suggests that eGFR is not a sensitive tool to assess the effect of surgical factors on the operated kidney in healthy patients, because the contralateral kidney can compensate and obscure damages to the operated kidney. This was shown indirectly on subset analysis of changes in the RDF of the operated kidney. When loss in RDF was used as an end point of RF, the contribution of the preoperative RF was lost statistically (P=0.81), whereas WIT remained independently associated as with loss in RDF (P≤0.0001).

Several limitations inherent to the retrospective design of this study are important to mention. Even if multivariate analysis has been performed to counteract some bias, the fact that this study was nonrandomized can limit the generalization of its conclusions. First, the AO group includes patients on whom surgery was performed earlier in the series. Despite this, we did not observed a statistically significant difference in perioperative characteristics between the two groups. We cannot exclude the impact of unmeasured technical skills gained with surgical experience that might explain some of the differences observed between the two groups. On the other hand, there was a trend toward larger and deeper tumors in the AV group, which should have increased WIT and normal parenchyma removed for these patients, two factors that would be expected to decrease RF on the operated kidney. It is also important to mention that the follow-up between the two groups was not equivalent. Therefore, our conclusions are based on the RF at 3 months postoperatively. Despite being too short to address RF decrease down to end-stage renal disease, there is evidence showing that this follow-up is sufficient to address the damage to the operated kidney.³¹ Using renal scintigraphy and split RF, Porpiglia and associates³¹ reported that most of the RDF recovery occurred between POD 5 and 3 months. In their study, the difference in RDF between a 3-month and a 12-month follow-up was only 1.2%. We therefore believe that the results obtained would be similar to those observed with a 1-year follow-up.

Conclusion

En-bloc clamping of the renal hilum is not associated with decreased RF impairment in patients who are undergoing LPN. In the current case series comparison, we observed that en-bloc clamping is associated with a shorter WIT, one important predictor of RF after LPN. We believe that en-bloc hilar clamping can be used safely during LPN without compromising RF.

Footnotes

Disclosure Statement

No competing financial interests exist.

Abbreviations Used

References

Novick

, Campbell

. Guideline for management of the clinical stage 1 renal mass. American Urological Association 2009. http://www.auanet.org/content/guidelines-and-quality-care/clinical-guidelines.cfm. 2011 June 13.

Gill

, Aron

, Gervais

, Jewett

. Clinical practice. Small renal mass. N Engl J Med, 2010; 362:624–634.

Haber

, Gill

. Laparoscopic partial nephrectomy: Contemporary technique and outcomes. Eur Urol, 2006; 49:660–665.

Neely

, Turner

. The effect of arterial, venous, and arteriovenous occlusion on renal blood flow. Surg Gynecol Obstet, 1959; 108:669–672.

Birkeland

, Vogt

, Krog

et al. Renal circulatory occlusion and local cooling. J Appl Physiol, 1959; 14:227–232.

Gong

, Zorn

, Orvieto

et al. Artery-only occlusion may provide superior renal preservation during laparoscopic partial nephrectomy. Urology, 2008; 72:843–846.

Johnston WK

III

, Montgomery

, Seifman

et al. Fibrin glue v sutured bolster: Lessons learned during 100 laparoscopic partial nephrectomies. J Urol, 2005; 174:47–52.

Rassweiler

, Teber

, Frede

. Complications of laparoscopic pyeloplasty. World J Urol, 2008; 26:539–547.

Pouliot

, Lebel

, Audet

, Dujardin

. Determination of success by objective scintigraphic criteria after laparoscopic pyeloplasty. J Endourol, 2010; 24:299–304.

10.

Pouliot

, Pantuck

, Imbeault

et al. Multivariate analysis of the factors involved in loss of renal differential function after laparoscopic partial nephrectomy: A role for warm ischemia time. Can Urol Assoc J, 2011; 5:89–95.

11.

, Chertow

, Fan

et al. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med, 2004; 351:1296–1305.

12.

Berger

, Crouzet

, Canes

et al. Minimally invasive nephron-sparing surgery. Curr Opin Urol, 2008; 18:462–466.

13.

Pahernik

, Roos

, Hampel

et al. Nephron sparing surgery for renal cell carcinoma with normal contralateral kidney: 25 years of experience. J Urol, 2006; 175:2027–2031.

14.

Lau

, Blute

, Weaver

et al. Matched comparison of radical nephrectomy vs nephron-sparing surgery in patients with unilateral renal cell carcinoma and a normal contralateral kidney. Mayo Clin Proc, 2000; 75:1236–1242.

15.

Thompson

, Boorjian

, Lohse

et al. Radical nephrectomy for pT1a renal masses may be associated with decreased overall survival compared with partial nephrectomy. J Urol, 2008; 179:468–473.

16.

Orvieto

, Zorn

, Mendiola

et al. Recovery of renal function after complete renal hilar versus artery alone clamping during open and laparoscopic surgery. J Urol, 2007; 177:2371–2374.

17.

Song

, Bang

, Park

, Ahn

. Factors influencing renal function reduction after partial nephrectomy. J Urol, 2009; 181:48–54.

18.

Lee

, Box

, Abraham

et al.

Laboratory evaluation of laparoscopic vascular clamps using a load-cell device—Are all clamps the same?

J Urol, 2008; 180:1267–1272.

19.

Desai

, Gill

, Ramani

et al. The impact of warm ischaemia on renal function after laparoscopic partial nephrectomy. BJU Int, 2005; 95:377–383.

20.

Simmons

, Schreiber

, Gill

. Surgical renal ischemia: A contemporary overview. J Urol, 2008; 180:19–30.

21.

Thompson

, Frank

, Lohse

et al. The impact of ischemia time during open nephron sparing surgery on solitary kidneys: A multi-institutional study. J Urol, 2007; 177:471–476.

22.

Lane

, Babineau

, Poggio

et al. Factors predicting renal functional outcome after partial nephrectomy. J Urol, 2008; 180:2363–2369.

23.

Benway

, Baca

, Bhayani

et al. Selective versus nonselective arterial clamping during laparoscopic partial nephrectomy: Impact upon renal function in the setting of a solitary kidney in a porcine model. J Endourol, 2009; 23:1127–1133.

24.

Bollens

, Rosenblatt

, Espinoza

et al. Laparoscopic partial nephrectomy with ‘‘on-demand’’ clamping reduces warm ischemia time. Eur Urol, 2007; 52:804–809.

25.

Smith

, Kenney

, Lee

, Libertino

. Non-clamped partial nephrectomy: Techniques and surgical outcomes. BJU Int, 2011; 107:1054–1058.

26.

Wszolek

, Kenney

, Lee

, Libertino

. Comparison of hilar clamping and non-hilar clamping partial nephrectomy for tumours involving a solitary kidney. BJU Int, 2011; 107:1886_1892.

27.

Thompson

, Lane

, Lohse

et al. Comparison of warm ischemia versus no ischemia during partial nephrectomy on a solitary kidney. Eur Urol, 2010; 58:331–336.

28.

Gill

, Eisenberg

, Aron

et al. ‘‘Zero ischemia’’ partial nephrectomy: Novel laparoscopic and robotic technique. Eur Urol, 2011; 59:128–134.

29.

Williams

, Kacker

, Alemozaffar

et al. Robotic partial nephrectomy versus laparoscopic partial nephrectomy: A single laparoscopic trained surgeon's experience in the development of a robotic partial nephrectomy program. World J Urol, 2011 Jan 29Epub ahead of print.

30.

Benway

, Bhayani

, Rogers

et al. Robot assisted partial nephrectomy versus laparoscopic partial nephrectomy for renal tumors: A multi-institutional analysis of perioperative outcomes. J Urol, 2009; 182:866–883.

31.

Porpiglia

, Renard

, Billia

et al. Is renal warm ischemia over 30 minutes during laparoscopic partial nephrectomy possible? One-year results of a prospective study. Eur Urol, 2007; 52:1170–1178.