Meta-analysis of Transperitoneal Versus Extraperitoneal Robot-Assisted Radical Prostatectomy for Prostate Cancer

Abstract

Objective:

To conduct a meta-analysis of studies that compared transperitoneal (TP) and extraperitoneal (EP) robot-assisted radical prostatectomy (RARP).

Materials and Methods:

PubMed, the Cochrane Library, and EMBASE online databases were searched for studies released prior to June 2012. References were manually reviewed, and two researchers independently extracted the data. To assess the quality of the studies, the Scottish Intercollegiate Guidelines Network Methodology Checklist for case-control and cohort studies was applied.

Results:

One randomized controlled trial and five case-control studies were identified that met the inclusion criteria. Within these studies, 530 patients underwent EP-RARP, and 312 patients underwent TP-RARP. Operating room (OR) time for EP was shorter than for TP (mean difference, −25.551; 95% confidence interval [CI] −41.668 to −9.434; P=.002). For estimated blood loss, there was no significant difference between EP and TP (mean difference, −12.111; 95% CI −44.087 to 19.865; P=.458). There was a statistical difference in length of stay (LOS) between EP and TP patients (mean difference, −0.488; 95% CI −0.964 to −0.012; P=.044). There was no significant difference in margin positivity between EP and TP (odds ratio=1.023; 95% CI 0.656–1.573; P=.918). In complications including grade 2 or more than 2, there was also no difference between EP and TP (odds ratio=0.610; 95% CI 0.341–1.089; P=.094).

Conclusions:

This meta-analysis suggests that perioperative parameters, including OR time and LOS, may be more favorable for EP-RARP than for TP-RARP. However, the oncologic outcome of margin positivity did not demonstrate a significant difference between the EP and TP approaches.

Introduction

Since Rassweiler et al.¹ suggested using robot-assisted radical prostatectomy (RARP) for treating prostate cancer in 2001, numerous studies have shown its safety and efficacy, with decreased operative time, hospitalization stay, catheterization duration, and margin positivity compared with open retropubic radical prostatectomy (RRP). The advantages of RARP include increased precision, elimination of surgical tremor, enhanced dexterity for advanced reconstruction, three-dimensional vision, and the potential for remote and telerobotic surgery.² Short-term follow-ups have shown that continence, potency, and oncological results are comparable to those observed with open RRP and laparoscopic radical prostatectomy.^3,4

Gettman et al.⁵ reported the first clinical cases of extraperitoneal (EP) RARP (EP-RARP) in 2003, and several studies have compared the oncological outcomes and complications of transperitoneal (TP) RARP (TP-RARP) versus EP-RARP. Atug et al.⁶ showed that EP-RARP is comparable to TP-RARP and also produces favorable outcomes. Madi et al.⁷ also reported that EP-RARP offers similar clinical outcomes to TP-RARP but that EP-RARP avoids potential bowel injury or complications related to an intraperitoneal urine leak. Lee et al.⁸ suggested that EP-RARP may be the best alternative in robotic radical prostatectomy, considering the potential risk of bowel injury with TP-RARP and the reduced peritoneal irritation with EP-RARP. Recently, Davis et al.⁹ suggested that potential indications for EP-RARP may be patients with histories of previous abdominal surgery, symptomatic inguinal hernia needing mesh repair, or cardiac disease with inserted drug-eluting stents.

Some studies have reported that EP-RARP may be similar or superior to TP-RARP in terms of perioperative outcomes¹⁰; however, a systematic review or meta-analysis comparing EP-RARP and TP-RARP has not been published. Thus, we conducted a meta-analysis of studies that compared the TP versus the EP approach in RARP.

Materials and Methods

Inclusion criteria

Randomized controlled trials (RCTs) or case-control trials that met the following criteria were included: (1) a study design that included comparison of the TP and EP approaches in RARP for prostate cancer; (2) the study provided accurate perioperative data that could be analyzed, including the total number of subjects and the values of each index; and (3) the full text of the study could be accessed.

Search strategy

A comprehensive computer literature search for abstracts was performed to identify articles that compared the TP versus the EP approach in RARP. A systematic review of original articles that analyzed perioperative outcomes between TP- and EP-RARP and were published between 2001 and June 2012 was conducted. A literature search of PubMed, the Cochrane Library, and EMBASE online databases was performed using the key words “prostatectomy,” “robot,” and “extraperitoneal.” The searches were restricted to English language publications.

Data extraction

One researcher (J.Y.L.) screened the titles and abstracts identified by the search strategy. The other two researchers (K.S.C. and R.R.D.) independently assessed the full text of the articles for meeting of the inclusion criteria. The database was designed to ensure the most relevant data with respect to author, year of publication, demographics of the patients, tumor characteristics, geographic location, period of recruitment, study design, and inclusion of a reference standard. The data extracted from articles included perioperative data presented as the mean value with P values, including operating room (OR) time and estimated blood loss (EBL), and standard deviations were obtained according to the method of the Cochrane Handbook for Systematic Reviews of Interventions (http://handbook.cochrane.org/).¹¹ Complications in each study were recategorized according to the Clavien–Dindo classification.¹² Disagreements were resolved by discussion until a consensus was arrived at, or by arbitration using another researcher (Y.D.C.).

Study quality assessment

Once the final group of articles was agreed upon, two researchers (J.Y.L. and R.R.D.) independently examined the quality of each article using the Scottish Intercollegiate Guidelines Network (SIGN) as a quality assessment tool for observational studies.¹³ This system is internationally accepted and is used by guideline developers. Flay et al.¹⁴ for the Society for Prevention Research and Kumpfer and Alvarado¹⁵ have published similar rating scales, which require an even higher level of evidence (when such evidence comes from RCTs or case-control trials performed by multiple independent research groups) and stricter criteria for assessing the quality of the research.¹⁶ For quality assessment, four categories were used to categorize the design quality of a study: “low” (score of 0–14); “modest” (score of 14.5–19); “good” (score of 19.5–24); or “very good” (score of 24.5–30).

Heterogeneity test

Heterogeneity among the studies was explored using the Q statistic and Higgins' I² statistic.^17,18 Higgins' I² measures across studies for the percentage of total variation due to heterogeneity rather than chance. Higgins' I² is calculated as follows: \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*} I^2 = \frac {Q - df}{Q} \times 100\% \end{align*} \end{document}

where Q is Cochran's heterogeneity statistic and df is the statistical degrees of freedom.

An I² of >50% is considered to represent substantial heterogeneity. For the Q statistic, heterogeneity was deemed to be significant for P<.10.¹⁹ When there was evidence of heterogeneity, data were analyzed using a random-effects model to obtain a summary estimate for the test sensitivity with 95% confidence intervals (CIs) after the secondary examination of heterogeneity in the random-effects model using a radial plot.²⁰ Studies in which positive results were confirmed were conducted using a pooled specificity with 95% CIs.

Statistical analyses

When a significant Q test indicated heterogeneity across studies (P<.10 or I²>50%), the random-effects model was used for the meta-analysis; otherwise, the fixed-effects model was used.²¹ The data for heterogeneity were verified again using the radial plot by the method of Galbraith²⁰ after selection of each model for parameters. The Begg–Mazumdar rank-correlation test and Egger's regression intercept test were used to provide evidence of publication bias,^22,23 which was shown as a funnel plot (P<.05 was considered a significant publication bias). The meta-analysis of comparable data was carried out using R software (R version 2.15.3; R Foundation for Statistical Computing, Vienna, Austria) (www.r-project.org) and its metafor package for meta-analyses.

Results

Eligible studies and quality assessment

The database search found 45 articles that could potentially have been included in the meta-analysis. Based on the inclusion and exclusion criteria, 39 articles were excluded after a simple reading of the titles and abstracts of the articles, including two that lacked a full text version. In total, six articles were included in the analysis (Fig. 1).^6,7,24–27 The six eligible studies included 530 patients who had undergone EP-RARP and 312 who had undergone TP-RARP. The publication year of the studies ranged from 2006 to 2012. Four studies were conducted in the United States,^6,7,24,26 one was conducted in Korea,²⁵ and one was conducted in Switzerland.²⁷ Only one RCT²⁴ and five case-control trials were selected (Table 1). Of the six enrolled articles, the final assessment results quality was deemed to be “low” in two articles^6,7 and “modest” in four articles,^24–27 according to the SIGN checklists.

FIG. 1.

Flow diagram of the study selection.

Table 1.

Main Characteristics of the Studies Included in Our Extraperitoneal Versus Transperitoneal Robot-Assisted Radical Prostatectomy Meta-analysis

			Patients
Reference	Year	Country	RARP	n	Age (years)	BMI (kg/m²)	PSA (ng/mL)	Volume (mL)	OR time (minutes)	EBL (mL)	Catheter (days)	LOS (days)	Complication rate (%)	SMR (%)
Atug et al.⁶	2006	United States	TP	40	60.3	27.4	7.2	48.9	236.23	250	NA	1.1	12.5	17.5
			EP	40	60.4	27.8	7.4	52.7	229.15	221	NA	1.2	12.5	20
Capello et al.²⁴	2007	United States	TP	31	59	29.8	6.1	48	191	163	NA	NA	NA	0
			EP	31	56	26.5	7.8	53	118	199	NA	NA	NA	3.2
Madi et al.⁷	2007	United States	TP	21	59	NA	NA	37.3	241	150	NA	NA	0	19
			EP	34	48.5	NA	NA	41.1	214	124	NA	NA	6.25	23.5
Chung et al.²⁵	2011	Korea	TP	105	66.3	23.5	14.7	31.0	162.1	361.7	7.3	6.2	19.0	33.3
			EP	155	65.8	24.0	16.2	34.8	150.3	350.8	7.7	5.1	7.1	16.8
Jacobs et al.²⁶	2011	United States	TP	48	62.8	NA	7.5	NA	310	188	NA	1.5	NA	13.8
			EP	167	61.2	NA	6.3	NA	209	125	NA	1.1	NA	10.4
Horstmann et al.²⁷	2012	Switzerland	TP	67	65.6	26.3	12.2	55.8	224	281	6.5	8.8	7	NA
			EP	103	64.4	26.5	7.0	51.8	192	276	6.2	7.8	12	NA

BMI, body mass index; EBL, estimated blood loss; LOS, length of stay; NA, not available; OR, operating room; PSA, prostate-specific antigen; RARP, robot-assisted radical prostatectomy; SMR, surgical margin rate.

Heterogeneity assessment

A heterogeneity test of OR time, EBL, hospitalization length of stay (LOS), complication rate, and surgical margin rate (SMR) showed the following: for OR time, chi-squared=13.468 with 5 df (P=.013) and I²=65.44%; for EBL, chi-squared=11.083 with 5 df (P=.050) and I²=54.89%; for LOS, chi-squared=16.001 with 3 df (P=.001) and I²=81.25%; for SMR, chi-squared=1.234 with 4 df (P=.872) and I²=0%; and for rate of complications including grade 2 or more than 2, chi-squared=0.550 with 3 df (P=0.908) and I²=0%. Notable heterogeneities were detected in OR time, EBL, and LOS; thus random-effect models were used to further assess these three variables. In radial plots, no variable demonstrated heterogeneity after selection of effect models for each variable (Fig. 2).

FIG. 2.

Radial plots demonstrated that no variable demonstrated heterogeneity after selection of effect models: (A) operating room time, (B) estimated blood loss, (C) length of stay, (D) margin positivity, and (E) rate of complications including grade 2 and more than 2 according to the Clavien–Dindo classification.

Publication bias assessment

The Begg–Mazumdar rank-correlation test showed no evidence of publication bias in the present meta-analysis for OR time (P=.452), EBL (P=0.452), LOS (P=1.000), SMR (P=.221), and complication rate (P=.750). Egger's regression intercept test also revealed no evidence of publication bias in OR time (P=.614), EBL (P=.352), LOS (P=.861), SMR (P=.112), and complication rate (P=.960). Funnel plots detailing these results, including OR time, EBL, LOS, SMR, and complication rate, are shown in Figure 3.

FIG. 3.

Funnel plots for publication bias for (A) operating room (OR) time, (B) estimated blood loss (EBL), (C) length of stay (LOS), (D) margin positivity, and (E) complication including grade 2 and more than 2 according to the Clavien–Dindo classification.

Comparison of TP and EP approaches in RARP

Forest plots for OR time, EBL, LOS, SMR, and complications rate are given in Figure 4. OR time for EP was relatively shorter than for TP (mean difference, −25.551; 95% CI −41.668 to −9.434; P=.002; Fig. 4A). For EBL, there was no significant difference between EP and TP (mean difference, −12.111; 95% CI −44.087 to 19.865; P=.458; Fig. 4B). LOS for EP was also relatively shorter than for TP (mean difference, −0.488; 95% CI −0.964 to −0.012; P=.044; Fig. 4C). For SMR, the meta-analysis revealed an odds ratio of 1.023 (95% CI 0.656–1.573; P=.918; Fig. 4D). In rate of complications including grade 2 or more than 2, there was also no difference between EP and TP (odds ratio=0.610; 95% CI=0.341–1.089; P=.094; Fig. 4E).

FIG. 4.

Meta-analysis forest map of risk ratio between the extraperitoneal and transperitoneal approaches in robot-assisted radical prostatectomy for (A) operating room (OR) time, (B) estimated blood loss (EBL), (C) length of stay (LOS), (D) margin positivity, and (E) complication including grade 2 and more than 2 according to the Clavien–Dindo classification. OR time and LOS for the extraperitoneal approach were shorter than for the transperitoneal approach. There was no statistical difference in EBL, margin positivity, and complication rate. CI, confidence interval; FE, fixed-effects; RE, random-effects.

Discussion

The use of RARP has increased substantially in both the United States and Europe, and it is estimated that more than 75% of radical prostatectomies are performed using the da Vinci^® Surgical System platform (Intuitive Surgical Inc., Sunnyvale, CA).^28,29 RARP is generally superior to RRP with regard to functional outcomes.³⁰ Advantages of RARP include the 10 times magnified binocular, three-dimensional visualization, motion scaling with tremor filtration, improved surgical ergonomics, and miniature articulating instruments with seven degrees of freedom. These capabilities provide improved precision and comfort versus manual approaches and thus facilitate dissection of tissue planes and meticulous suturing.

Previous studies have shown that EP-RARP and TP-RARP have equal oncological and functional outcomes. Although comparative shortcomings of EP-RARP include limited working space and time-to-port installation, the EP approach may have advantages over TP-RARP, including less OR time and EBL and shorter hospital LOS and recovery times. Our study is the first systematic review and meta-analysis comparing EP- and TP-RARP. Our meta-analysis quantitatively assessed the results of prior studies that had compared the perioperative outcomes of the TP and EP surgical approaches.

We found that OR time was shorter with EP-RARP than with TP-RARP. Despite the slightly longer time-to-port installation with the EP approach, a significantly shorter overall surgical time using EP-RARP was described in the literature and was confirmed by our meta-analysis. This shorter overall surgical time was mainly achieved by a shorter console time in EP-RARP due to the fact that no further mobilization of the peritoneum and the bladder was necessary.²⁷ In the six studies that were included in our meta-analysis, the skill level of the surgeons performing the TP-RARP and EP-RARP was detailed. Therefore, a possible confounding factor may be the factor of the experience level of the surgeon and/or assistant who performed EP-RARP compared with TP-RARP. For EBL, there was no statistical difference using random-effects models. Only two of the six selected articles showed that EBL in EP-RARP was significantly less than for TP-RARP, and four articles found no difference in EBL between the EP and TP approaches. Data concerning LOS were extracted from four studies: the two studies from the United States^6,26 averaged only 1 day, but in one study each from Korea²⁵ and Switzerland,²⁷ LOS was longer (range, 5.1–8.8 days).

The complications following EP-RARP and TP-RARP are shown in Table 2 according to the Clavien–Dindo classification.¹² In fact, one of the most important advantages of EP-RARP is using the peritoneum as a natural barrier. The peritoneum during and after the EP procedure still functions as a natural barrier, minimizing the likelihood of persistent ileus occurrence because the bowel is minimally manipulated and there is no leakage of intraperitoneal fluids.³¹ Additionally, the EP approach is associated with a reduced number of accidental thermal injuries to the intestines, due to peritoneal sequestering of the bowels outside of the operating field. Moreover, bowel injuries that infrequently occur during trocar insertion and dorsal dissection of the overlying rectum prostatic apex are considered a less severe complication with EP access versus the TP approach because the risk of generalized peritonitis is diminished.³² However, the studies included in our meta-analysis were assessed as modest or low grade in SIGN checklists and used quite different categories to evaluate complications in each. There were some difficulties in analyzing comparisons of complications between TP and EP. For grade 1 complications, including postoperative ileus, EP may be superior to TP, pointing to one advantage of EP-RARP over TP-RARP. However, grade 2 or more than 2 complications did not demonstrate a significant difference between TP and EP. The complications arising from each procedure showed little difference except for complications that might result from procedural injury or underlying disease.

Table 2.

Comparison of Complications Between Transperitoneal and Extraperitoneal Robot-Assisted Radical Prostatectomy in Previous Studies According to the Clavien–Dindo Classification

	TP				EP
	1	2	3	4	1	2	3	4
Atug et al.⁶	3	1	1	0	1	1	1	1
Madi et al.⁷	0	0	0	0	0	1	0	0
Chung et al.²⁵	7	4	9	0	0	10	4	0
Horstmann et al.²⁷	4	4	3	2	1	5	2	1

Data are number of cases.

EP, extraperitoneal; TP, transperitoneal.

Considering surgical margin positivity, there were no significant differences between TP and EP. Previous studies revealed that open and laparoscopic approaches had similar oncological outcomes.³³ Surgical margin positivity is a unique marker of oncologic outcome that can be extracted from previous series. Postsurgical functional analysis should include oncologic outcomes, as well as recovery of continence and potency, when comparing TP and EP approaches in RARP.

There were some limitations in our meta-analysis. Although all cases and controls from each study were well defined with similar inclusion criteria, there may be potential factors that were not taken into account that may have influenced our study selection for inclusion in a meta-analysis. Second, data on oncologic and functional outcomes were not available in the original articles. In particular, pathologic stage, biochemical recurrence, and recovery of potency and of continence were not included, and confounding factors might have introduced bias.

Conclusions

Considering operative outcomes extracted from previous studies, OR time and LOS were relatively shorter and complication rates were lower when EP-RARP was used rather than the TP approach. However, EBL, surgical margin positivity, and complication rate did not show significant differences. Further RCTs comparing the TP and EP approaches should be conducted in larger patient populations to definitively assess potential differences in perioperative parameters and postoperative outcomes.

Footnotes

Acknowledgments

This study was supported by grant A084120 from the Korea Healthcare Technology R&D Project, Ministry for Health, Welfare & Family Affairs, Republic of Korea, and grant CB-2011-04-02 from the Korean Foundation for Cancer Research.

Disclosure Statement

No competing financial interests exist.

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