Systematic Review and Meta-Analysis of Comparative Studies Reporting Perioperative Outcomes of Robot-Assisted Partial Nephrectomy Versus Open Partial Nephrectomy

Abstract

Background:

Robot-assisted partial nephrectomy (RAPN) is increasingly being used for the surgical management of renal masses. The comparison of RAPN with open partial nephrectomy (OPN) has not yet led to a unified conclusion with regard to perioperative outcomes.

Purpose:

To conduct a systematic review and meta-analysis of the literature on the perioperative outcomes of RAPN compared with OPN.

Methods:

We searched PubMed and EMBASE through January 31, 2016, to identify randomized controlled trials (RCTs) and observational comparative studies assessing the comparison of the two approaches (RAPN vs OPN). Primary outcomes were intraoperative complication rate and postoperative complication rate (including minor and major). Secondary outcomes were perioperative transfusion rate, positive surgical margin (PSM) rate, operative time (OT), warm ischemia time (WIT), estimated blood loss (EBL), length of hospital stay (LOS), and estimated glomerular filtration rate (eGFR) change.

Results:

A total of 19 cohort studies with at least 3551 patients (RAPN, 1216; OPN, 2335) were included. Compared with OPN, RAPN had the advantages of (a) lower rates of postoperative complication (risk ratio [RR] = 0.60, 95% confidence interval [CI] = 0.46, 0.78, p = 0.0002), postoperative minor complication (RR = 0.73, 95% CI = 0.56, 0.96, p = 0.02), and postoperative major complication (RR = 0.50, 95% CI = 0.30, 0.84, p = 0.01); (b) lower need for transfusion (RR = 0.64, 95% CI = 0.41, 0.98, p = 0.04); (c) less EBL (weighted mean difference [WMD] = −98.82, 95% CI = −125.64, −72.01, p < 0.00001); and (d) shorter LOS (WMD = −2.64, 95% CI = −3.27, −2.00, p < 0.00001). Sensitivity analyses excluding studies with obvious selection bias based on tumor complexity confirmed all these advantages. RAPN had longer OT (WMD = 18.56, 95% CI = 2.13, 35.00, p = 0.03) and WIT (WMD = 3.65, 95% CI = 0.75, 6.56, p = 0.01) in the primary analyses. Sensitivity analyses, however, showed no differences between RAPN and OPN regarding OT and WIT. Intraoperative complication rate (RR = 0.61, 95% CI = 0.29, 1.27, p = 0.19), PSM rate (RR = 0.87, 95% CI = 0.56, 1.34, p = 0.52), and short-term eGFR change, including absolute eGFR change (WMD = −1.56, 95% CI = −3.41, 0.28, p = 0.10) and percentage eGFR change (WMD = 0.99, 95% CI = −0.52, 2.50), did not differ between the two approaches.

Conclusions:

Compared with OPN, RAPN appears to have lower morbidity and achieves similar short-term functional outcomes. However, evidence is limited regarding the long-term oncologic outcomes even though the PSM rate is similar between the two groups. Well-designed RCTs with large sample sizes and long-term follow-up are needed to confirm and update the findings of our study.

Introduction

Partial nephrectomy (PN) is currently the “gold standard” for the surgical management of localized T1 (<7 cm) renal-cell carcinomas.¹ However, PN is still underutilized compared with radical nephrectomy (RN).^2

–5 One possible reason accounting for underutilization is patients' and surgeons' preference toward minimally invasive procedures. Laparoscopic radical nephrectomy, which is widely used by surgeons, is a mature technique, has a shorter learning curve, and is associated with less perioperative complications.⁶ On the contrary, laparoscopic partial nephrectomy (LPN) is a challenging procedure with a steep learning curve, which has limited its adoption among some urologists.^7,8 For the past decade, robot-assisted partial nephrectomy (RAPN) has gained popularity because the Da Vinci platform offers significant advantages and has substantially decreased the learning curve associated with minimally invasive PN.^9
–11

Previous large comparative studies and meta-analyses have already confirmed the significant advantages of RAPN over LPN.^9,10,12 So, as Mottrie et al.¹¹ have suggested, the real gold standard reference for RAPN outcome comparisons should be open partial nephrectomy (OPN), not LPN. For the past several years, a number of studies comparing perioperative outcomes between RAPN and OPN have been published with various results.^{13

–31} With this in mind, we conducted a meta-analysis and systematically review the perioperative outcomes of RAPN vs OPN.

Methods

Search strategy

This systematic review and meta-analysis were conducted and reported in adherence to Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) statement (Supplementary Table S1; Supplementary Data are available online at www.liebertpub.com/end).³² We used the search terms combination [“robot” OR “robotic” OR “robot-assisted” OR “robotic-assisted” OR “da Vinci” AND “partial nephrectomy”] and restricted language to English for both PubMed and EMBASE. For EMBASE, we also excluded publication types of conference abstract, conference article, and conference review. The last updated literature search was performed on January 31, 2016. We also reviewed the full-text articles designated for inclusion and manually checked the references of the retrieved articles and previous reviews and/or meta-analyses to identify additional eligible studies.

Selection criteria

Inclusion criteria were as follows: (a) studies comparing RAPN with OPN; (b) studies focusing on adult populations; (c) randomized controlled trials (RCTs) or observational cohort studies; (d) having, at least, one of the outcomes of interest. When two or more studies were reported by the same institutions and/or authors, or when two or more studies clearly had the duplicate patient population, the study with the largest sample size was included. However, if multiple studies with the same patient population had different outcomes of interest, they can be included for analysis separately.

Exclusion criteria were as follows: (a) RAPN/OPN only for benign tumors or bilateral tumors; (b) RAPN/OPN only in patients with solitary kidney; (c) single-port RAPN; (d) entirely zero-ischemia RAPN; (e) review articles, editorials, comments, letters to the editor, case reports, and conference abstracts; and (f) population-based studies.

Data extraction

Data extraction was performed by two reviewers and discrepancies were resolved by discussion. The following information was extracted from each study: authors; publication year; region; time period of RAPN/OPN; institutions; number of surgeons; number of patients; surgical approach; clamping method; study design; age; gender; body mass index (BMI); tumor size; tumor side; tumor location (upper/interpolar/lower); tumor depth (exophytic/mesophytic/endophytic); number of solitary kidney; number of malignant tumor; R.E.N.A.L score, preoperative aspects and dimensions used for an anatomical (PADUA) score, and outcomes of interest.

Total events, means, and standard deviations (SDs) were extracted from each study. Zero event studies were included. For studies presenting continuous data as median and/or range and/or interquartile range, the means and SDs were calculated using the methodology described by mathematicians and in the Cochrane handbook.^33
–35

Outcomes of interest

The primary outcomes were the intraoperative complication rate, overall postoperative complication rate, postoperative minor (Clavien–Dindo grades 1–2) complication rate, and postoperative major (Clavien–Dindo grades 3–4) complication rate. We defined major complication as Clavien–Dindo grades 3–4 since the perioperative mortality rate (Clavien–Dindo grade 5) of RAPN/OPN is rare.

The secondary outcomes were perioperative transfusion rate, positive surgical margin (PSM) rate, operative time (OT), warm ischemia time (WIT), estimated blood loss (EBL), length of hospital stay (LOS), and estimated glomerular filtration rate (eGFR) change.

Quality assessment

Quality assessment was performed by two reviewers and discrepancies were resolved by discussion. Cochrane risk of bias tool was used to assess the risk of bias for RCTs.³³ Observational studies were evaluated using the Newcastle–Ottawa Scale (NOS).³⁶ The NOS evaluates the quality of studies by examining three aspects of the study design: patient selection, comparability of the study groups, and assessment of outcomes. A score of 0–9 may be given to individual studies. Observational studies achieving a score of 6 or more indicate a high quality.

Statistical analysis

Meta-analysis

To be more conservative, the weighted mean difference (WMD) and risk ratio (RR) were used to compare continuous and dichotomous variables, respectively. The Mantel–Haenszel method with random-effects model was used to calculate pooled RRs and 95% confidence intervals (CIs). The inverse variance method with random-effects model was used to calculate pooled WMDs and 95% CIs. p < 0.05 was considered statistically significant.

Statistical heterogeneity

Statistical heterogeneity between studies was assessed using the chi-square (χ ²) test with significance set at p < 0.10. Heterogeneity was also quantified using the I ² statistic. I ², which is ranging from 0% to 100%, measures the degree of inconsistency across studies in a meta-analysis.³⁷ I ² values of 25%, 50%, and 75% were deemed as low, moderate, and high heterogeneity.³⁷ Usually, I ² value greater than 50% suggests significant heterogeneity in the reported effect sizes.³⁸

Sensitivity analysis

Due to the fact that RAPNs were usually performed for less complex tumors compared with OPN, we excluded the studies in which obvious selection bias existed for the sensitivity analysis. The R.E.N.A.L score and PADUA score are two commonly used tools classifying tumor complexity.^39,40 Obvious selection bias was defined as having unmatched R.E.N.A.L score or PADUA score between RAPN and OPN groups. If neither the R.E.N.A.L score nor PADUA score was reported, obvious selection bias was defined as having unmatched tumor size between RAPN and OPN groups. Remaining studies were included for sensitivity analysis.

Subgroup analyses

We chose postoperative complication rate for subgroup analyses since it has a decent number of included studies and has relatively more clinical significance. Subgroup analyses were conducted according to study design (prospective vs retrospective), setting (single center vs multicenter), sample size (≥200 vs <200), and region (Asia vs Europe vs the United States).

Publication bias

Publication bias was assessed by visually inspecting a funnel plot in which the logRRs or WMDs were plotted against their standard errors. The presence of publication bias was also evaluated by Begg's and Egger's tests. p < 0.05 was considered statistically significant.

Software

Excel 2013 (Microsoft Corporation), Review Manager 5.3 (Cochrane Collaboration), and STATA 14.0 (StataCorp LP).

Results

Literature search

The PRISMA flow diagram is shown in Figure 1. A total of 1491 studies were identified from the initial database search. Five hundred thirty-eight were excluded for duplication. The remaining 953 records were screened based on titles and abstracts. After exclusion of 903 studies from screening, 43 potentially eligible studies were reviewed based on full-text. In this process, another 24 studies were excluded for not meeting our inclusion criteria or falling into exclusion criteria. Finally, 19 studies were included in the meta-analysis.^{13

–31}

FIG. 1.

Flow diagram of studies identified, included, and excluded. RAPN = robot-assisted partial nephrectomy; LPN = laparoscopic partial nephrectomy.

Study characteristics

The main characteristics of the included studies are shown in Table 1. These studies were published between 2011 and 2015. The sample size ranged from 31 to 501. Two studies^15,18 and another two studies^24,27 shared some duplicate patient populations and had different outcomes of interest. After excluding the potential maximum overlapping patients, the total patient number was 3551 (RAPN group, 1216; OPN group, 2335). All studies were observational cohort studies, eight of them were prospective and 11 were retrospective. Five studies were multicenter studies. Among the 19 studies, eight of them were conducted in the United States, six in Europe, five in Asia. Some of the outcomes in the study of Simhan and colleagues²⁸ had to be pooled into two separate groups because the comparisons in the original study were stratified by a moderately and highly complex group (labeled as Simhan M and Simhan C, respectively) based on the R.E.N.A.L score.

Table 1.

Characteristics of the Included Studies

						No. of patients			No. of no clamping
First author	Year	Region	Time period	No. of institutions	No. of surgeons	RAPN	OPN	Surgical approach for RAPN	RAPN	OPN	Study design	Quality scores ^a	Conflict of interest stated
Alemozaffar et al.¹³	2013	United States of America	11/2008 to 09/2010	1	RAPN-1; OPN-5	25	25	Unclear	/	/	Retrospective	9	Yes
Boylu et al.¹⁴	2015	Turkey	2009 to 2013	1	Unclear	46	20	Transperitoneal	1	1	Prospective	8	No
Ficarra et al.¹⁵	2014	Italy, Belgium, United States of America	RAPN-09/2008 to 09/2010; OPN-01/2009 and 01/2011	RAPN-4; OPN-19	RAPN-4; OPN-unclear	200	200	Transperitoneal	20	62	Retrospective	9	Yes
Han et al.¹⁶	2014	Korea	07/2011 to 04/2014	1	Unclear	147	354	Transperitoneal	1	21	Retrospective	9	Yes
Laydner et al.¹⁷	2013	United States of America	01/2009 to 12/2010	1	4	145	133	Unclear	/	/	Prospective	8	Yes
Lee et al.¹⁸	2011	Korea	05/2003 to 12/2010	1	3	69	234	Unclear	0	2	Retrospective	9	Yes
Lucas et al.¹⁹	2012	United States of America	2004 to 2010	1	RAPN-1; OPN-unclear	27	54	Unclear	/	/	Retrospective	9	No
Mano et al.²⁰	2015	United States of America	2011	1	RAPN-2; OPN-8	63	190	Unclear	/	/	Retrospective	9	Yes
Masson-Lecomte et al.²¹	2013	France	2008 to 2010	1	RAPN-1; OPN-1	42	58	Transperitoneal	/	/	Prospective	8	No
Minervini et al.²²	2014	Italy	01/2010 to 12/2011	6	Unclear	105	198	Transperitoneal	40	103	Prospective	9	Yes
Miyake et al.²³	2015	Japan	01/2012 to 05/2014	1	RAPN-1; OPN-1	16	15	Transperitoneal and retroperitoneal	/	/	Retrospective	9	Yes
Oh et al.²⁴	2014	Korea	05/2003 to 05/2013	1	1	100	100	Unclear		/	Retrospective	9	Yes
Patton et al.²⁵	2015	United States of America	11/1999 to 07/2013	1	Unclear	55	37	Unclear	/	/	Prospective	7	Yes
Pignot et al.²⁶	2014	France	06/2010–12/2010.	56	Unclear	89	359	Unclear	8	126	Prospective	8	Yes
Porpiglia et al.²⁷	2015	Italy	01/2009 to 12/2012	22	Unclear	95	133	Transperitoneal and retroperitoneal	13	26	Prospective	9	Yes
Simhan et al.²⁸	2012	United States of America	2007 to 2010	1	Unclear	91	190	Unclear	/	/	Prospective	6	Yes
Stroup et al.²⁹	2012	United States of America	03/2003 to 05/2011	3	RAPN-3; OPN-3	31	153	Transperitoneal and retroperitoneal	/	/	Retrospective	8	Yes
Webb et al.³⁰	2015	United States of America	2005 to 2011	1	Unclear	14	21	Unclear	1	4	Retrospective	7	No
Wu et al.³¹	2014	China	2009 to 2013	1	4	51	94	Unclear	0	0	Retrospective	9	Yes

RAPN = robot-assisted partial nephrectomy; OPN = open partial nephrectomy; / = not available.

Based on the Newcastle–Ottawa Scale (details in Supplementary Table S2).

Patient and tumor characteristics of the included studies are shown in Table 2. Mean/median patient age of the RAPN group ranged from 52.5 to 63.3 years old (OPN, 52–65 years old). Mean/median patient BMI of the RAPN group ranged from 24.8 to 31.4 kg/m² (OPN, 24.4–30.1 kg/m²). Mean/median tumor size of the RAPN group ranged from 20 to 50 mm (OPN, 23–54 mm).

Table 2.

Patient Demographics and Tumor Characteristics of the Included Studies

	No. of patients		Age (years)		No. of male		BMI (kg/m²)		Tumor size (mm)		No. of left side tumor		No. of exophytic tumor		No. of solitary kidney		No. of malignant tumor		R.E.N.A.L score
First author	RAPN	OPN	RAPN	OPN	RAPN	OPN	RAPN	OPN	RAPN	OPN	RAPN	OPN	RAPN	OPN	RAPN	OPN	RAPN	OPN	RAPN	OPN	Match factors
Alemozaffar et al.¹³	25	25	55.9	61.9	15	19	27.5	30.1	25	33	13	8	/	/	/	/	/	/	6.08	7	3, 4, 6, 10
Boylu et al.¹⁴	46	20	54	56	29	14	28.7	27.5	35.6	40.4	28	8	38	16	0	0	37	14	5.35	6.35	1, 3, 5, 6, 12, 13, 15, 16
Ficarra et al.¹⁵	200	200	62.4	62.4	121	131	/	/	28	30	/	/	142	135	/	/	158	163	/	/	1, 2, 6, 8, 9, 15, 16
Han et al.¹⁶	147	354	52.5	55.3	108	270	25.6	24.5	25.8	28	68	177	68	143	1	10	/	/	6.58	6.72	1, 2, 3, 6, 7, 8, 9, 10, 13, 14, 15
Laydner et al.¹⁷	145	133	59	61	83	96	30	28	26	40	73	61	/	/	/	/	/	/	/	/	1, 3, 7, 15
Lee et al.¹⁸	69	234	53.5	54.4	50	164	25.5	24.5	23.7	25.8	41	127	20	63	0	0	64	215	/	/	1, 2, 6, 7, 9, 13, 15, 16
Lucas et al.¹⁹	27	54	62.1	57.6	19	38	31.4	29.6	24	23	/	/	/	/	0	0	17	44	6	6	1, 2, 3, 6, 10, 13, 15
Mano et al.²⁰	63	190	57	59	46	132	29.1	29	26	30	37	100	/	/	/	/	55	169	/	/	1, 2, 3, 6, 7, 10
Masson-Lecomte et al.²¹	42	58	61.7	60.8	22	40	26.9	26.5	28	31	/	/	/	/	/	/	34	52	/	/	1, 2, 3, 4, 6, 8, 15, 16
Minervini et al.²²	105	198	62.3	63.8	69	123	25.7	26.2	28	35	/	/	/	/	/	/	91	156	/	/	1, 2, 3, 5, 11, 15, 16
Miyake et al.²³	16	15	63.3	64.2	14	10	24.9	24.4	30	32	6	7	/	/	0	0	/	/	/	/	1, 2, 3, 4, 6, 7, 9, 10, 13, 15, 16
Oh et al.²⁴	100	100	54.3	54.6	70	69	25.5	25.1	25.2	25.9	54	48	31	26	0	0	94	94	7	7	1, 2, 3, 4, 6, 7, 9, 10, 13, 15, 16
Patton et al.²⁵	55	37	63	65	58	9	29	29	/	/	/	/	/	/	0	0	/	/	/	/	1, 2, 3, 4, 13, 14
Pignot et al.²⁶	89	359	60	61	60	212	26.1	25.5	30	35	/	/	/	/	/	/	/	/	/	/	1, 2, 3, 4, 16
Porpiglia et al.²⁷	95	133	57.3	62.3	42	87	25.8	26	50	50	54	68	51	91	/	/	/	/	/	/	2, 3, 6, 7, 8, 9, 15, 16
Simhan et al.²⁸	91	190	/	/	/	/	/	/	/	/	/	/	/	/	/	/	/	/	/	/	1, 2, 3, 4
Stroup et al.²⁹	31	153	61	56	19	12	27.7	28.9	20	42	/	/	13	53	/	/	23	119	6.4	8	1, 2, 3
Webb et al.³⁰	14	21	60.5	53.6	6	14	/	/	29.9	42.2	7	16	13	11	/	/	12	19	/	/	1, 2, 6, 7, 16
Wu et al.³¹	51	94	53	52	35	62	24.8	25.1	/	/	/	/	/	/	0	0	/	/	/	/	1, 2, 3, 4, 5, 15

Continuous variables were reported as mean or median.

Match factors (details in Supplementary Table S3): 1 = age; 2 = gender; 3 = BMI; 4 = American Society of Anesthesiology (ASA) score; 5 = Charlson Comorbidity Index (CCI); 6 = tumor size; 7 = tumor laterality (left/right); 8 = tumor location (upper/interpolar/lower pole); 9 = tumor depth (exophytic/mesophytic/endophytic); 10 = R.E.N.A.L score; 11 = PADUA score; 12 = clamping method; 13 = solitary kidney; 14 = previous abdominal surgery; 15 = preoperative estimated glomerular filtration rate (eGFR); 16 = preoperative creatinine.

BMI = body mass index; PADUA = preoperative aspects and dimensions used for an anatomical; / = not available.

Quality assessment

Quality assessments of included studies are shown in Table 1 and Supplementary Table S2. Based on the NOS to assess the risk of bias of the cohort studies, one study was rated as a total score of 6, two studies as a score of 7, five studies as a score of 8, and 11 studies as a score of 9. So, all observational studies had a score of ≥6 and were considered high quality.

Primary outcomes

Meta-analyses of primary outcomes are shown in Table 3 and Figure 2.

FIG. 2.

Forest plots of primary and secondary outcomes: (1) intraoperative complication; (2) postoperative complication; (3) postoperative minor (Clavien–Dindo grades 1–2) complication; (4) postoperative major (Clavien–Dindo grades 3–4) complication; (5) perioperative transfusion; (6) positive surgical margin; (7) operative time; (8) warm ischemia time; (9) estimated blood loss; (10) length of hospital stay; (11) absolute eGFR decline; (12) percentage eGFR decline. eGFR = estimated glomerular filtration rate.

Table 3.

Primary and Secondary Outcomes Comparing Robot-Assisted Partial Nephrectomy with Open Partial Nephrectomy

			No. of patients				Study heterogeneity				Publication bias
Outcomes studied	No. of studies	Reference of studies	RAPN	OPN	RR/WMD ^a [95% CI]^*	p Value^*	χ²	df	p Value^*	I ² (%)	Begg's test^*	Egger's test^*
Intraoperative complication	9	14,15,19,22 –24,27,30,31	654	835	0.61 [0.29, 1.27]	0.19	3.51	5	0.62	0	1.000	0.756
Postoperative complication	13	15,16,18 –23,25,27,29 –31	915	1741	0.60 [0.46, 0.78]	0.0002	14.86	11	0.19	26	0.945	0.804
Minor complication	13	15,16,18 –23,25,27,29 –31	915	1741	0.73 [0.56, 0.96]	0.02	8.22	11	0.69	0	0.304	0.881
Major complication	13	15,16,18 –23,25,27,29 –31	915	1741	0.50 [0.30, 0.84]	0.01	11.48	11	0.4	4	0.631	0.220
Perioperative transfusion	12	14 –16,20 –26,30,31	928	1646	0.64 [0.41, 0.98]	0.04	11.61	9	0.24	22	0.721	0.366
Positive surgical margin	15	14 –16,19,21 –24,26 –31	1012	1912	0.87 [0.56, 1.34]	0.52	6.82	11	0.81	0	0.837	0.936
Operative time, minutes	16	13 –16,19 –29,31	1173	2126	18.56 ^a [2.13, 35.00]	0.03	296.88	15	<0.00001	95	0.392	0.037
Warm ischemia time, minutes	8	14,15,19,21,22,24,26,27	620	766	3.65 ^a [0.75, 6.56]	0.01	97.79	7	<0.00001	93	0.386	0.635
Estimated blood loss, mL	16	13 –15,19 –31	1040	1793	−98.82 ^a [−125.64, −72.01]	<0.00001	54.71	15	<0.00001	73	0.043	0.048
Length of hospital stay, days	16	13 –17,20 –26,28,30,31	1189	1994	−2.64 ^a [−3.27, −2.00]	<0.00001	311.13	15	<0.00001	95	0.079	0.012
Absolute eGFR decline, mL/minute	5	15,16,18,25,27	566	958	−1.56^a [−3.41, 0.28]	0.10	7.79	4	0.10	49	1.000	0.995
Percentage eGFR decline, %	3	23,24,31	167	209	0.99^a [−0.52, 2.50]	0.20	1.37	2	0.50	0	0.296	0.302

WMD.

Statistically significant results are shown in bold.

RR = risk ratio; WMD = weighted mean difference; CI = confidence interval; minor = Clavien–Dindo grades 1–2; major = Clavien–Dindo grades 3–4; eGFR = estimated glomerular filtration rate.

Intraoperative complications

Pooling data from nine studies^{14,15,19,22
–24,27,30,31} that assessed intraoperative complications in 1489 patients showed no significant difference between the RAPN and OPN groups (RR [95% CI]: 0.61 [0.29, 1.27], p = 0.19).

Postoperative complications

A total of 13 studies^{15,16,18

–23,25,27,29
–31} provided the data of overall postoperative complication, but the time frame of the postoperative complications varied. Three studies^20,26,29 defined it as complications that happened within 30 days of the date of surgery, one¹⁵ as within 90 days of the date of surgery, and another one³¹ as during hospital stay. Eight studies^{16,18,19,21,22,25,27} did not specify the time frame of the postoperative complication. Pooling data from the 13 studies^{15,16,18

–23,25,27,29
–31} that assessed postoperative complications in 2656 patients showed a significantly lower rate of postoperative complication in the RAPN vs OPN groups (RR [95% CI]: 0.60 [0.46, 0.78], p = 0.0002).

Overall postoperative complications were further divided into minor and major complications in the original 13 studies.^{15,16,18

–23,25,27,29
–31} There was a significantly lower minor complication rate (RR [95% CI]: 0.73 [0.56, 0.96], p = 0.02) and a significantly lower major complication rate (RR [95% CI]: 0.50 [0.30, 0.84], p = 0.01) in the RAPN vs OPN groups.

Secondary outcomes

Meta-analyses of secondary outcomes are shown in Table 3 and Figure 2.

Perioperative transfusion

Pooling data from 12 studies^{14
–16,20

–26,30,31} that assessed perioperative transfusions in 2574 patients showed a significantly lower rate of perioperative transfusion in the RAPN vs OPN groups (RR [95% CI]: 0.64 [0.41, 0.98], p = 0.04).

Positive surgical margin

Pooling data from 15 studies^{14
–16,19,21

–24,26

–31} that assessed PSMs in 2924 patients showed no significant difference between the RAPN and OPN groups (RR [95% CI]: 0.87 [0.56, 1.34], p = 0.52).

Operative time

Pooling data from 16 studies^{13

–16,19

–29,31} that assessed OTs in 3299 patients showed significantly longer OT in the RAPN vs OPN groups (WMD [95% CI]: 18.56 [2.13, 35.00], p = 0.03).

Warm ischemia time

For WIT, patients who underwent cold ischemia and/or off-clamp techniques in the RAPN and OPN groups were excluded. Studies in which cold ischemia was used in the OPN group were excluded. Pooling data from eight studies^{14,15,19,21,22,24,26,27} that assessed WITs in 1386 patients showed significantly longer WIT in the RAPN vs OPN groups (WMD [95% CI]: 3.65 [0.75, 6.56], p = 0.01).

Estimated blood loss

Pooling data from 16 studies^{13
–15,19

–31} that assessed EBL in 2833 patients showed a significantly lower EBL in the RAPN vs OPN groups (WMD [95% CI]: −98.82 [−125.64, −72.01], p < 0.00001).

Length of hospital stay

Pooling data from 16 studies^{13

–17,20

–26,28,30,31} that assessed LOSs in 2783 patients showed significantly shorter LOS in the RAPN vs OPN groups (WMD [95% CI]: −2.64 [−3.27, −2.00], p < 0.00001).

eGFR change

Five studies^{15,16,18,25,27} reported postoperative absolute eGFR decline and another three studies^23,24,31 reported percentage eGFR decline with extractable data. The postoperative eGFRs were assessed at postoperative 1 month in three studies,^18,23,27 3 months in two studies,^15,31 and 6 months in one study.²⁴ In another two studies,^16,25 assessment time of postoperative eGFRs was not clear.

Pooling data from five studies^{15,16,18,25,27} that assessed absolute eGFR decline showed no significant difference between the RAPN and OPN groups (WMD [95% CI]: −1.56 [−3.41, 0.28], p = 0.10).

Pooling data from three studies^23,24,31 that assessed percentage eGFR decline showed no significant difference between the RAPN and OPN groups (WMD [95% CI]: 0.99 [−0.52, 2.50], p = 0.20).

Sensitivity analyses

Sensitivity analyses of all the primary and secondary outcomes are shown in Table 4 and Supplementary Figure S1. Sensitivity analyses included 13 studies^{13,15,16,18
–20,22

–25,27,30,31} after excluding studies^{14,17,21,26,28,29} with obvious selection bias. Of the excluded studies, three of them^14,21,29 had unmatched R.E.N.A.L score and another three^17,26,28 had unmatched tumor size between the RAPN and OPN groups. p-Value of OT changed from 0.03 to 0.15 (compared with primary meta-analysis), which indicated no significant difference between the RAPN and OPN groups. p-Value of WIT changed from 0.01 to 0.06 (compared with primary meta-analysis), which indicated no significant difference between the RAPN and OPN groups. p-Values of other outcomes of interest remain significant (<0.05) or nonsignificant (≥0.05) after sensitivity analyses.

Table 4.

Sensitivity Analysis—Excluding Studies with Obvious Selection Bias Based on Tumor Complexity

			No. of patients				Study heterogeneity				Publication bias
Outcomes studied	No. of studies	Reference of studies	RAPN	OPN	RR/WMD ^a [95% CI]^*	p Value^*	χ²	df	p Value^*	I² (%)	Begg's test^*	Egger's test^*
Intraoperative complication	8	15,19,22 –24,27,30,31	608	815	0.61 [0.29, 1.27]	0.19	3.51	5	0.62	0	1.000	0.756
Postoperative complication	11	15,16,18 –20,22,23,25,27,30,31	842	1530	0.58 [0.42, 0.80]	0.0008	14.65	9	0.10	39	0.858	0.703
Minor complication	11	15,16,18 –20,22,23,25,27,30,31	842	1530	0.72 [0.54, 0.96]	0.02	8.06	9	0.53	0	0.592	0.983
Major complication	11	15,16,18 –20,22,23,25,27,30,31	842	1530	0.44 [0.24, 0.82]	0.01	10.38	9	0.32	13	0.858	0.297
Perioperative transfusion	9	15,16,20,22 –25,30,31	751	1209	0.55 [0.31, 0.98]	0.04	10.66	6	0.10	44	0.548	0.205
Positive surgical margin	9	15,16,19,22 –24,27,30,31	713	1132	0.82 [0.47, 1.43]	0.48	2.79	5	0.73	0	0.260	0.333
Operative time, minutes	11	13,15,16,19,20,22 –25,27,31	884	1400	15.52^a [−5.57, 36.61]	0.15	232.99	10	<0.00001	96	0.533	0.116
Warm ischemia time, minutes	5	15,19,22,24,27	452	456	4.08^a [−0.18, 8.34]	0.06	89.93	4	<0.00001	96	0.806	0.853
Estimated blood loss, mL	11	13,15,19,20,22 –25,27,30,31	751	1067	−92.18 ^a [−120.82, −63.54]	<0.00001	35.89	10	<0.00001	72	0.087	0.058
Length of hospital stay, d	10	13,15,16,20,22 –25,30,31	776	1234	−1.74 ^a [−2.21, −1.28]	<0.00001	88.75	9	<0.00001	90	0.474	0.265
Absolute eGFR decline, mL/minute	5	15,16,18,25,27	566	958	−1.56^a [−3.41, 0.28]	0.10	7.79	4	0.10	49	1.000	0.995
Percentage eGFR decline, %	3	23,24,31	167	209	0.99^a [−0.52, 2.50]	0.20	1.37	2	0.50	0	0.296	0.302

WMD.

Statistically significant results are shown in bold.

Minor = Clavien–Dindo grades 1–2; major = Clavien–Dindo grades 3–4.

Subgroup analyses

Subgroup analyses of overall postoperative complication rate are shown in Table 5 and Supplementary Figure S2. The findings of lower postoperative complication rate were consistent in all subgroup analyses except for the single-center, sample size <200, Asian, and US subgroups. Subgroup differences were found in study design and sample size.

Table 5.

Subgroup Analysis for Postoperative Complication

			No. of patients				Study heterogeneity				Test for subgroup differences
Stratification	No. of studies	Reference of studies	RAPN	OPN	RR [95% CI]^*	p Value^*	χ²	df	p Value^*	I² (%)	p Value^*	I² (%)
All studies	13	15,16,18 –23,25,27,29 –31	915	1741	0.60 [0.46, 0.78]	0.0002	14.86	11	0.19	26
Study design											0.04	76.9
Prospective	4	21,22,25,27	297	426	0.43 [0.29, 0.62]	<0.0001	2.13	3	0.55	0
Retrospective	9	15,16,18 –20,23,29 –31	618	1315	0.72 [0.53, 0.97]	0.03	7.92	7	0.34	12
Setting											0.15	51.3
Multicenter	4	15,22,27,29	431	684	0.49 [0.34, 0.72]	0.0002	4.27	3	0.23	30
Single center	9	16,18 –21,23,25,30,31	484	1057	0.72 [0.51, 1.03]	0.07	7.94	7	0.34	12
Sample size											0.01	84.6
≥200	6	15,16,18,20,22,27	679	1309	0.49 [0.37, 0.64]	<0.00001	3.85	5	0.57	0
<200	7	19,21,23,25,29 –31	236	432	0.90 [0.62, 1.32]	0.60	4.36	5	0.50	0
Region											0.48	0
Asia	4	16,18,23,31	283	697	0.69 [0.34, 1.39]	0.30	6.4	3	0.09	53
Europe	4	16,21,22,27	442	589	0.49 [0.33, 0.71]	0.0001	4.01	3	0.26	25
United States of America	5	19,20,25,29,30	190	455	0.67 [0.42, 1.09]	0.11	1.34	3	0.72	0

Statistically significant results are shown in bold.

Publication bias

All the funnel plots are shown in Figure 3. All the Begg's and Egger's tests are shown in Tables 3 and 4. The funnel plots and Begg's and Egger's tests showed no evidence of significant publication bias for intraoperative complication, postoperative complication, minor postoperative complication, major postoperative complication, transfusion, PSM, WIT, absolute eGFR decline, and percentage eGFR decline. Potential publication biases were seen in OT, EBL, and LOS.

FIG. 3.

Funnel plots of primary and secondary outcomes: (1) intraoperative complication; (2) postoperative complication; (3) postoperative minor (Clavien–Dindo grades 1–2) complication; (4) postoperative major (Clavien–Dindo grades 3–4) complication; (5) perioperative transfusion; (6) positive surgical margin; (7) operative time; (8) warm ischemia time; (9) estimated blood loss; (10) length of hospital stay; (11) absolute eGFR decline; (12) percentage eGFR decline.

Discussion

Main findings

The present systematic review and meta-analysis identified 19 studies comparing RAPN with OPN in terms of perioperative outcomes. The primary meta-analyses (Table 3; Fig. 2) showed that compared with OPN, RAPN had the following advantages: (a) lower rates of intraoperative complication, overall postoperative complication, postoperative minor and major complication; (b) lower transfusion rate; (c) less EBL; and (d) shorter LOS. However, the OPN group had a significantly shorter OT and WIT. No significant difference was found regarding PSM and eGFR decline between the two groups. After excluding studies with obvious selection bias based on tumor complexity, sensitivity analyses showed the same results for all the outcomes of interest except OT and WIT, both of which became nonsignificant (Table 4).

Comparison with one previous systematic review and meta-analysis

One previous meta-analysis on this topic, which included eight studies with a total of 3418 patients, was published in 2014.⁴¹ There was one major flaw in their meta-analysis even though the sample size was almost the same as ours.⁴¹ It is noticeable that more than half of their patient sample came from one population-based study (2022 patients).^41,42 In contrast, included in our meta-analysis were entirely single-center or multicenter studies. We excluded the population-based study because single-center or multicenter studies can provide more precise or detailed clinical information. Also, population-based studies themselves can be considered as heterogeneous factors, which can affect the results.^43,44 After the publication of the previous meta-analysis, several high-quality observational studies comparing RAPN with OPN were published.^{15,24

–27,31} Therefore, our meta-analysis can provide the most updated and comprehensive evidence on this topic.

Implications for clinical practice

Although there were more studies comparing RAPN with LPN than RAPN with OPN, using OPN as the reference of RAPN might have more clinical significance.¹¹ Like Mottrie et al.¹¹commented, traditional laparoscopy might not be the real competitor of RAPN. Large comparative studies and meta-analyses have demonstrated that compared with LPN, RAPN had the advantages of lower complication rate, less EBL, and shorter WIT.^9,10,12,45 Therefore, except for the cosmetic advantage, whether RAPN has other benefits over OPN is a topic worth clarifying.

Two facts need to be addressed before interpreting the clinical significance of our study. First, most of the outcomes of interest were procedure related, which can only provide early safety and efficacy evaluations. Second, match factors were reported in our results (Table 2 and Supplementary Table S3) and it was clear that selection bias existed. Although we excluded the obvious selection bias in the sensitivity analysis (Table 4), it was not possible to entirely eliminate the effects of selection bias considering all included studies were observational.

Optimal PN has three objectives: (a) minimalizing perioperative complications; (b) completely removing the tumor; and (c) maximally preserving remaining renal function. Previously proposed “trifecta,” “MIC,” or other combined outcomes were all based on these three objectives.^46

–50 Although we did not have enough studies to directly compare the “trifecta” or “MIC” achievements between RAPN and OPN, most of the individual outcomes were reported in our meta-analysis. In our meta-analysis, safety outcome was reported as intraoperative complication, postoperative complication, transfusion, and EBL; cancer control outcome was reported as PSM; and renal function outcome was reported as WIT and eGFR decline. Although PSM and WIT cannot truly reflect the cancer control and renal function preservation, respectively, they are generally used as the surrogates and long-term follow-up data are still not available. So, we believe our meta-analyses have enough outcomes of interest to assess the performance difference between RAPN and OPN.

Fewer postoperative complications were seen in the RAPN group than OPN group. Furthermore, both postoperative minor and major complications were more frequently seen in the OPN group. However, there was no difference regarding intraoperative complication between the two groups. The possible reason is that intraoperative complication was much rarer than postoperative complication and the absolute difference might be diluted. Compared with OPN, RAPN also had the advantages of less EBL and fewer transfusions. Based on the current evidence, it appears that RAPN offers more than not just cosmetic benefits but also lower morbidity.

As for cancer control, no direct comparison of RAPN vs OPN in terms of long-term outcomes (overall survival, cancer-specific survival, and recurrence) has been reported in the literature to date. Our meta-analysis only showed a similar PSM rate between RAPN and OPN groups. Although the impact of PSM on the long-term oncologic outcomes of patients with kidney cancer remains debatable, complete removal of the tumor and achieving a negative margin is undoubtedly one critical goal of PN.^51
–53 Andrade and colleagues⁵⁴ recently reported the longest follow-up data on RAPN and the 5-year overall survival, cancer-free survival, and cancer-specific survival were 91.1%, 97.8%, and 97.8%, respectively. Another two studies with intermediate-term follow-up also showed that recurrence and survival outcomes of RAPN were similar to those reported for OPN and LPN.^55,56 Also, one previous meta-analysis revealed that there was no significant difference in survival outcome between LPN and OPN for the treatment of localized kidney cancer.⁵⁷ RAPN is nothing but more advanced LPN, so based on all these studies combined with our results, it is safe to say that RAPN, at least, has noninferior oncologic outcomes compared with OPN.

Our primary analysis showed that OPN had the shorter WIT compared with RAPN. However, the sensitivity analysis showed no significant difference. Furthermore, there was no difference between the two groups regarding postoperative eGFR decline. Although WIT is an important predictor of postoperative renal function, it certainly is not the only factor.^58

–61 In fact, one major advantage of RAPN compared with LPN is WIT according to previous studies.^10,62
–64 The WIT of RAPN is generally brief because of the improved ability to suture with RAPN compared with LPN. In experienced hands and appropriate patient selection, the WIT of RAPN can be controlled to less than 20 minutes.^{9,15,21,27,48} So, the marginal difference of WIT between RAPN and OPN may not have much clinical significance for patients with adequate renal reserve. Also, off-clamp or selective artery clamp RAPN can be applied to limit the renal function loss for patients with compromised renal function even though the benefit from those techniques is still controversial.^65

–68 However, in patients with marginal renal function or where a complex renal reconstruction may be anticipated, OPN may still remain the procedure of choice. For all comers, however, functional outcomes are generally comparable between the RAPN and OPN groups.

In our primary meta-analysis, OT was longer in the RAPN group, which is understandable considering the docking time was included in most of the studies. The different result demonstrated by the sensitivity analysis could simply be explained by the fact that heterogeneity between studies was large. The shorter LOS in our results can be considered as another benefit of RAPN, which could be possibly explained by the less invasive approach and lower postoperative complication rate. Also, the shorter LOS of LPN has already been reported in the comparison of OPN.^7,69 The shorter LOS has the potential to lower cost of hospitalization, which may offset the higher operating room costs of RAPN.^13,17,20 In other words, the advantages of RAPN may enable cost equivalence between RAPN and OPN.^13,17

One hidden point from our meta-analysis and included studies is that robotic technology has expanded the indications of minimally invasive PN.^{23,25,27
–29} More complex renal masses are being managed with RAPN instead of OPN and the robot platform can help narrow the gap that has long existed between PN and RN.^25,70,71 Furthermore, even for complex renal masses, RAPN can still offer significant lower morbidity and simultaneously achieve oncologic and functional outcomes comparable to OPN.^23,25,27,28

Strengths and limitations

Major strengths of our meta-analysis included the compliance with the PRISMA guideline, extended search, critical assessment, substantial analyses, including sensitivity analyses accounting for the tumor complexity, all of which made it the most comprehensive evidence regarding RAPN vs OPN to date. Since there are still no RCTs comparing RAPN and OPN, our meta-analysis might contribute to the literature in a meaningful way.

However, there are several limitations in the current meta-analysis that must be acknowledged. First, the protocol for this meta-analysis was not registered before. Second, selection biases were inevitable considering all included studies were observational and only 8 of them were claimed prospective. We conducted a sensitivity analysis to limit the bias from tumor complexity, but other selection biases were not explored. Third, the learning curve of the surgeons, especially in RAPN, was not accounted for before conducting the analyses, which could further skew our results. Worth mentioning, most of the studies did declare that the surgeons in their series were beyond the learning curve. Fourth, heterogeneities among the studies for OT, WIT, EBL, and LOS were relatively high (Table 3). The possible explanation is that all of them are continuous variables and it is also relatively harder to document them in a unified method. On the contrary, categorical variables tend to have low heterogeneities.

Conclusions

This meta-analysis indicates that compared with OPN, RAPN appears to be associated with fewer postoperative complications (including both minor and major complications), lower need for transfusion, less EBL, and shorter LOS. Although OPN has shorter WIT, short-term postoperative GFR decline is comparable between RAPN and OPN. There is no difference between the RAPN and OPN in terms of PSM. Well-designed RCTs with large sample size and long-term follow-up are still needed to confirm and update the findings of our study.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

Abbreviations Used

References

Ljungberg

, Bensalah

, Canfield

, et al. EAU guidelines on renal cell carcinoma: 2014 update. Eur Urol, 2015; 67:913–924.

Woldrich

, Palazzi

, Stroup

, et al. Trends in the surgical management of localized renal masses: Thermal ablation, partial and radical nephrectomy in the USA, 1998–2008. BJU Int, 2013; 111:1261–1268.

Liss

, Wang

, Palazzi

, et al. Evaluation of national trends in the utilization of partial nephrectomy in relation to the publication of the American Urologic Association guidelines for the management of clinical T1 renal masses. BMC Urol, 2014; 14:101.

Liu

, Leppert

, Maxwell

, Panousis

, Chung

. Trends and perioperative outcomes for laparoscopic and robotic nephrectomy using the National Surgical Quality Improvement Program (NSQIP) database. Urol Oncol, 2014; 32:473–479.

Bjurlin

, Walter

, Taksler

, et al. National trends in the utilization of partial nephrectomy before and after the establishment of AUA guidelines for the management of renal masses. Urology, 2013; 82:1283–1289.

Pareek

, Hedican

, Gee

, Bruskewitz

, Nakada

. Meta-analysis of the complications of laparoscopic renal surgery: Comparison of procedures and techniques. J Urol, 2006; 175:1208–1213.

Porpiglia

, Volpe

, Billia

, Scarpa

. Laparoscopic versus open partial nephrectomy: Analysis of the current literature. Eur Urol, 2008; 53:732–742; discussion 742–743.

Link

, Bhayani

, Allaf

, et al. Exploring the learning curve, pathological outcomes and perioperative morbidity of laparoscopic partial nephrectomy performed for renal mass. J Urol, 2005; 173:1690–1694.

Zargar

, Allaf

, Bhayani

, et al. Trifecta and optimal perioperative outcomes of robotic and laparoscopic partial nephrectomy in surgical treatment of small renal masses: A multi-institutional study. BJU Int, 2015; 116:407–414.

10.

Choi

, You

, Kim

, Rha

, Lee

. Comparison of perioperative outcomes between robotic and laparoscopic partial nephrectomy: A systematic review and meta-analysis. Eur Urol, 2015; 67:891–901.

11.

Mottrie

, Borghesi

, Ficarra

. Is traditional laparoscopy the real competitor of robot-assisted partial nephrectomy?. Eur Urol, 2012; 62:1034–1036; discussion 1038–1039.

12.

, Li

, Song

, et al. Propensity-score matched analysis comparing robot-assisted with laparoscopic partial nephrectomy. BJU Int, 2015; 115:437–445.

13.

Alemozaffar

, Chang

, Kacker

, Sun

, DeWolf

, Wagner

. Comparing costs of robotic, laparoscopic, and open partial nephrectomy. J Endourol, 2013; 27:560–565.

14.

Boylu

, Basatac

, Yildirim

, Onol

, Gumus

. Comparison of surgical, functional, and oncological outcomes of open and robot-assisted partial nephrectomy. J Minim Access Surg, 2015; 11:72–77.

15.

Ficarra

, Minervini

, Antonelli

, et al. A multicentre matched-pair analysis comparing robot-assisted versus open partial nephrectomy. BJU Int, 2014; 113:936–941.

16.

Han

, Song

, You

, et al. Comparison of hand-assisted laparoscopic versus robot-assisted laparoscopic versus open partial nephrectomy in patients with T1 renal masses. J Endourol, 2014. [Epub ahead of print]; DOI: 10.1089/end.2014.0517.

17.

Laydner

, Isac

, Autorino

, et al. Single institutional cost analysis of 325 robotic, laparoscopic, and open partial nephrectomies. Urology, 2013; 81:533–538.

18.

Lee

, Oh

, Hong

, Lee

, Byun

. Open versus robot-assisted partial nephrectomy: Effect on clinical outcome. J Endourol, 2011; 25:1181–1185.

19.

Lucas

, Mellon

, Erntsberger

, Sundaram

. A comparison of robotic, laparoscopic and open partial nephrectomy. JSLS, 2012; 16:581–587.

20.

Mano

, Schulman

, Hakimi

, et al. Cost comparison of open and robotic partial nephrectomy using a short postoperative pathway. Urology, 2015; 85:596–603.

21.

Masson-Lecomte

, Yates

, Hupertan

, et al. A prospective comparison of the pathologic and surgical outcomes obtained after elective treatment of renal cell carcinoma by open or robot-assisted partial nephrectomy. Urol Oncol, 2013; 31:924–929.

22.

Minervini

, Vittori

, Antonelli

, et al. Open versus robotic-assisted partial nephrectomy: A multicenter comparison study of perioperative results and complications. World J Urol, 2014; 32:287–293.

23.

Miyake

, Hinata

, Imai

, Furukawa

, Tanaka

, Fujisawa

. Partial nephrectomy for hilar tumors: Comparison of conventional open and robot-assisted approaches. Int J Clin Oncol, 2015; 20:808–813.

24.

, Byun

, Hong

, Jeong

, Lee

. Comparison of robotic and open partial nephrectomy: Single-surgeon matched cohort study. Can Urol Assoc J, 2014; 8:E471–E475.

25.

Patton

, Salevitz

, Tyson

2nd , et al. Robot-assisted partial nephrectomy for complex renal masses. J Robot Surg, 2016; 10:27–31.

26.

Pignot

, Mejean

, Bernhard

, et al. The use of partial nephrectomy: Results from a contemporary national prospective multicenter study. World J Urol, 2015; 33:33–40.

27.

Porpiglia

, Mari

, Bertolo

, et al. Partial nephrectomy in clinical T1b renal tumors: Multicentre comparative study of open, laparoscopic and robot-assisted approach (the RECORd Project). Urology, 2016; 89:45–53.

28.

Simhan

, Smaldone

, Tsai

, et al. Perioperative outcomes of robotic and open partial nephrectomy for moderately and highly complex renal lesions. J Urol, 2012; 187:2000–2004.

29.

Stroup

, Palazzi

, Kopp

, et al. RENAL nephrometry score is associated with operative approach for partial nephrectomy and urine leak. Urology, 2012; 80:151–156.

30.

Webb

, Kamel

, Eltahawy

, et al. A comparative study of open, laparoscopic and robotic partial nephrectomy in obese patients. Urol Ann, 2015; 7:231–234.

31.

, Li

, Qu

, et al. A propensity-score matched comparison of perioperative and early renal functional outcomes of robotic versus open partial nephrectomy. PLoS One, 2014; 9:e94195.

32.

Moher

, Liberati

, Tetzlaff

, Altman

, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med, 2009; 6:e1000097.

33.

Higgins

JPT

, Green

. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.cochrane-handbook.org Accessed March 2, 2016 .

34.

Hozo

, Djulbegovic

, Hozo

. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol, 2005; 5:13.

35.

Wan

, Wang

, Liu

, Tong

. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol, 2014; 14:135.

36.

Wells

, Shea

, O'Connell

, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality if nonrandomized studies in meta-analyses. Ottawa Hospital Research Institute. Web site: www.ohri.ca/programs/clinical_epidemiology/oxford.asp Accessed March 2, 2016 .

37.

Higgins

, Thompson

, Deeks

, Altman

. Measuring inconsistency in meta-analyses. BMJ, 2003; 327:557–560.

38.

Phan

, Tian

, Cao

, Black

, Yan

. Systematic review and meta-analysis: Techniques and a guide for the academic surgeon. Ann Cardiothorac Surg, 2015; 4:112–122.

39.

Ficarra

, Novara

, Secco

, et al. Preoperative aspects and dimensions used for an anatomical (PADUA) classification of renal tumours in patients who are candidates for nephron-sparing surgery. Eur Urol, 2009; 56:786–793.

40.

Kutikov

, Uzzo

. The R.E.N.A.L. nephrometry score: A comprehensive standardized system for quantitating renal tumor size, location and depth. J Urol, 2009; 182:844–853.

41.

, Li

, Liu

, et al. Robotic versus open partial nephrectomy: A systematic review and meta-analysis. PLoS One, 2014; 9:e94878.

42.

, Hevelone

, Lipsitz

, Kowalczyk

, Hu

. Use, costs and comparative effectiveness of robotic assisted, laparoscopic and open urological surgery. J Urol, 2012; 187:1392–1398.

43.

Novara

, Catto

, Wilson

, et al. Systematic review and cumulative analysis of perioperative outcomes and complications after robot-assisted radical cystectomy. Eur Urol, 2015; 67:376–401.

44.

Yuh

, Wilson

, Bochner

, et al. Systematic review and cumulative analysis of oncologic and functional outcomes after robot-assisted radical cystectomy. Eur Urol, 2015; 67:402–422.

45.

Wang

, Ma

, Huang

, et al. Comparison of robot-assisted and laparoscopic partial nephrectomy for complex renal tumours with a RENAL nephrometry score ≥7: Peri-operative and oncological outcomes. BJU Int, 2016; 117:126–130.

46.

Hung

, Cai

, Simmons

, Gill

. “Trifecta” in partial nephrectomy. J Urol, 2013; 189:36–42.

47.

Zargar

, Autorino

, Akca

, Brandao

, Laydner

, Kaouk

. Minimally invasive partial nephrectomy in the age of the “trifecta”. BJU Int, 2015; 116:505–506.

48.

Khalifeh

, Autorino

, Hillyer

, et al. Comparative outcomes and assessment of trifecta in 500 robotic and laparoscopic partial nephrectomy cases: A single surgeon experience. J Urol, 2013; 189:1236–1242.

49.

Buffi

, Lista

, Larcher

, et al. Margin, ischemia, and complications (MIC) score in partial nephrectomy: A new system for evaluating achievement of optimal outcomes in nephron-sparing surgery. Eur Urol, 2012; 62:617–618.

50.

Minervini

, Siena

, Antonelli

, et al. Open versus laparoscopic partial nephrectomy for clinical T1a renal masses: A matched-pair comparison of 280 patients with TRIFECTA outcomes (RECORd Project). World J Urol, 2014; 32:257–263.

51.

Bensalah

, Pantuck

, Rioux-Leclercq

, et al. Positive surgical margin appears to have negligible impact on survival of renal cell carcinomas treated by nephron-sparing surgery. Eur Urol, 2010; 57:466–471.

52.

Borghesi

, Brunocilla

, Schiavina

, Martorana

. Positive surgical margins after nephron-sparing surgery for renal cell carcinoma: Incidence, clinical impact, and management. Clin Genitourin Cancer, 2013; 11:5–9.

53.

Marszalek

, Carini

, Chlosta

, et al. Positive surgical margins after nephron-sparing surgery. Eur Urol, 2012; 61:757–763.

54.

Andrade

, Zargar

, Caputo

, et al. Five-year oncologic outcomes after transperitoneal robotic partial nephrectomy for renal cell carcinoma. Eur Urol, 2016; 69:1149–1154.

55.

Khalifeh

, Autorino

, Eyraud

, et al. Three-year oncologic and renal functional outcomes after robot-assisted partial nephrectomy. Eur Urol, 2013; 64:744–750.

56.

Kyllo

, Tanagho

, Kaouk

, et al. Prospective multi-center study of oncologic outcomes of robot-assisted partial nephrectomy for pT1 renal cell carcinoma. BMC Urol, 2012; 12:11.

57.

Zheng

, Zhang

, Geng

, et al. Long-term oncologic outcomes of laparoscopic versus open partial nephrectomy. Chin Med J (Engl), 2013; 126:2938–2942.

58.

Mir

, Ercole

, Takagi

, et al. Decline in renal function after partial nephrectomy: Etiology and prevention. J Urol, 2015; 193:1889–1898.

59.

Thompson

, Lane

, Lohse

, et al. Every minute counts when the renal hilum is clamped during partial nephrectomy. Eur Urol, 2010; 58:340–345.

60.

Volpe

, Blute

, Ficarra

, et al. Renal ischemia and function after partial nephrectomy: A collaborative review of the literature. Eur Urol, 2015; 68:61–74.

61.

Zhang

, Zhao

, Dong

, et al. Acute kidney injury after partial nephrectomy: Role of parenchymal mass reduction and ischemia and impact on subsequent functional recovery. Eur Urol, 2016; 69:745–752.

62.

Aboumarzouk

, Stein

, Eyraud

, et al. Robotic versus laparoscopic partial nephrectomy: A systematic review and meta-analysis. Eur Urol, 2012; 62:1023–1033.

63.

Froghi

, Ahmed

, Khan

, Dasgupta

, Challacombe

. Evaluation of robotic and laparoscopic partial nephrectomy for small renal tumours (T1a). BJU Int, 2013; 112:E322–E333.

64.

Zhang

, Shen

, Zhong

, Zhu

, Wang

, Xu

. Comparison of peri-operative outcomes of robot-assisted vs laparoscopic partial nephrectomy: A meta-analysis. BJU Int, 2013; 112:1133–1142.

65.

Gill

, Eisenberg

, Aron

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

66.

Kaczmarek

, Tanagho

, Hillyer

, et al. Off-clamp robot-assisted partial nephrectomy preserves renal function: A multi-institutional propensity score analysis. Eur Urol, 2013; 64:988–993.

67.

, Gill

, Patil

, et al. Anatomic renal artery branch microdissection to facilitate zero-ischemia partial nephrectomy. Eur Urol, 2012; 61:67–74.

68.

Komninos

, Shin

, Tuliao

, et al. Renal function is the same 6 months after robot-assisted partial nephrectomy regardless of clamp technique: Analysis of outcomes for off-clamp, selective arterial clamp and main artery clamp techniques, with a minimum follow-up of 1 year. BJU Int, 2015; 115:921–928.

69.

Gill

, Kavoussi

, Lane

, et al. Comparison of 1,800 laparoscopic and open partial nephrectomies for single renal tumors. J Urol, 2007; 178:41–46.

70.

Ghani

, Sukumar

, Sammon

, Rogers

, Trinh

, Menon

. Practice patterns and outcomes of open and minimally invasive partial nephrectomy since the introduction of robotic partial nephrectomy: Results from the nationwide inpatient sample. J Urol, 2014; 191:907–912.

71.

Patel

, Mullins

, Pierorazio

, et al. Trends in renal surgery: Robotic technology is associated with increased use of partial nephrectomy. J Urol, 2013; 189:1229–1235.

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