Stesura Seveso 41Archivio Italiano di Urologia e Andrologia 2015; 87, 1 ORIGINAL PAPER Comparing robotic, laparoscopic and open cystectomy: A systematic review and meta-analysis Thomas Fonseka 1, Kamran Ahmed 2, Saied Froghi 2, Shahid A Khan 3, Prokar Dasgupta 2, Mohammad Shamim Khan 2 1 King’s College London School of Medicine, London, UK; 2 MRC Centre for Transplantation, King's College London, King’s Health Partners, Department of Urology, Guy’s Hospital, London, UK; 3 Surrey and Sussex Healthcare NHS Hospital, Redhill, UK. Objective: To conduct a systematic review and meta-analysis comparing outcomes between Open Radical Cystectomy (ORC), Laparoscopic Radical Cystectomy (LRC) and Robot-assisted Radical Cystectomy (RARC). RARC is to be compared to LRC and ORC and LRC compared to ORC. Material and methods: A systematic review of the litera- ture was conducted, collating studies comparing RARC, LRC and ORC. Surgical and oncological outcome data were extracted and a meta-analysis was performed. Results: Twenty-four studies were selected with total of 2,104 cases analyzed. RARC had a longer operative time (OPT) compared to LRC with no statistical difference between length of stay (LOS) and estimated blood loss (EBL). RARC had a significantly shorter LOS, reduced EBL, lower complication rate and longer OPT compared to ORC. There were no significant differences regarding lymph node yield (LNY) and positive surgical margins (PSM.) LRC had a reduced EBL, shorter LOS and increased OPT compared to ORC. There was no significant difference regarding LNY. Conclusion: RARC is comparable to LRC with better surgi- cal results than ORC. LRC has better surgical outcomes than ORC. With the unique technological features of the robotic surgical system and increasing trend of intra-corpo- real reconstruction it is likely that RARC will become the surgical option of choice. KEY WORDS: Radical cystectomy; Robotic assisted radical cystec- tomy; Laparoscopic radical cystectomy; Open radical cystectomy; Bladder cancer. Submitted 22 December 2014; Accepted 31 December 2014 Summary No conflict of interest declared. my (RARC) has since emerged as a viable alternative. RARC has been reported to be associated with fewer com- plications compared to LRC (2) and the appeal of the robotic surgical system has led to the adoption of the pro- cedure worldwide. However the production of high-qual- ity evidence that measures the relative merits of ORC, LRC and RARC is lacking with surgeons having to rely on sys- tematic review. This article aims to compare surgical and oncological outcomes of ORC, LRC and RARC. METHODS Eligibility criteria Data were collected on all patients over the age of 60 with muscle-invasive bladder cancer undergoing RARC, LRC or ORC. Surgical outcomes were; operative time (OPT), esti- mated blood loss (EBL), length of stay (LOS) and compli- cation rate 90 days post-operatively. Oncological out- comes were; lymph node yield (LNY) and positive surgi- cal margins (PSM). Comparisons were made between RARC, LRC and ORC and the outcomes of interest meas- ured included both surgical and oncological outcomes. The studies forming the current meta-analysis include comparative studies, either retrospective or prospective, as well as randomized control trials. For a study to be included in our analysis it had to fulfill the following criteria. The study had to: – Compare outcome measures of two or all three surgi- cal techniques (ORC, LRC and RARC). – Use quantitative data for at least one outcome measure. – Be a high quality study. If it was one of two studies that were produced by the same institution, it was ensured the data were mutually exclusive. Studies were excluded if they: – Lacked reporting of the desired outcome measures list- ed above or presented the data in such a way that it was not possible to carry out an analysis for the study. – Reported on only one of the techniques of ORC, LRC and RARC. – Were written in non-English language. DOI: 10.4081/aiua.2015.1.41 INTRODUCTION Open Radical Cystectomy (ORC) is currently regarded as the gold standard surgical treatment for muscle-invasive and non-muscle invasive high-grade recurrent bladder cancer (1). However, the procedure is associated with high morbidity including increased blood loss, pro- longed hospital stay and slower recovery. Laparoscopic Radical Cystectomy (LRC) was developed around two decades but Robot-assisted Radical Cystecto - Fonseka_Stesura Seveso 02/04/15 10:21 Pagina 41 Archivio Italiano di Urologia e Andrologia 2015; 87, 1 T. Fonseka, K. Ahmed, S. Froghi, S.A. Khan, P. Dasgupta, M. Shamim Khan 42 Information sources A systematic review of the literature was conducted using the following databases; PubMed, Medline, the Cochrane Library and EMBASE. The reference lists of reviews were also cross-referenced. The last search was conducted on 11/12/2014. Search The following search terms were used: “Open cystectomy”, “Open radical cystectomy”, “Laparoscopic cystectomy”, “Laparoscopic assisted cystectomy”, “Laparoscopic radical cys- tectomy”, “Laparoscopic assisted radical cystectomy”, “Robotic cystectomy”, “Robot* assisted cystectomy”, “Robotic radical cystectomy”, “Robot* assisted radical cystectomy”, “Robot* assisted laparoscopic cystectomy”, “Robot* assisted laparoscop- ic radical cystectomy”, “Minimally invasive”, “Bladder cancer”. The search terms were combined to ensure as many studies as possible that compared ORC, LRC and RARC, or any combination were included. Study selection Studies were selected by two reviewers (T.F and S.F), independently. Where the decision was split and agree- ment could not be made, the study was included so as to include as many studies as possible. Data items After selection of the studies, the following data were extracted; primary author of the study, year of publica- tion, country of study, study design, study exclusion cri- teria (if mentioned), total number of patients undergoing ORC, LRC and RARC, study population characteristics (mean age, mean BMI, mean American Society of Anesthesiologists (ASA) grade, Charlson’s Co-morbidity Index, gender, and pathological stage). For each tech- nique (ORC, LRC and RARC), the following data were recorded: primary author of the study, year of publica- tion, total number of patients undergoing each urinary diversion type (conduit or neo-bladder), total number of patients requiring blood transfusion, surgical outcomes (as previously listed) and oncological outcomes (as pre- viously listed). Complications were assessed using the Clavien-Dindo grading system (3). Risk of bias in individual studies The Newcastle-Ottawa Quality Assessment Scale (4) was used to assess the quality of the studies. It was tailored to suit the analysis of the studies included in this evalua- tion. Areas analyzed for quality were patient selection, including representativeness of the exposed cohort, com- parability of cohorts, and assessment of outcomes. Studies which were rated with five or more stars were deemed to be high-quality. The entire analysis was con- ducted using Review Manager Version 5 (The Cochrane Collaboration, Software Update, Oxford). Summary measures To assess whether there was a statistically significant dif- ference between data of a dichotomous nature, the odds ratio (OR) was calculated. The OR is a measure of the probability of an event occurring in an RARC patient group compared to either ORC or LRC patient groups or LRC compared to ORC. When comparing adverse events, where an OR value was less than one it implied that RARC was favored. In order for the point estimate of the OR to be considered statistically significant at the P < 0.05 level, the 95% CI must not have included the value of one. When handling continuous data the mean weighted difference (MWD) was used instead of the OR. A negative MWD value indicated RARC was favored. Synthesis of results Guidance was sought from the Cochrane Collaboration as well as information from the QUORUM guidelines (5) to provide the framework of the statistical analysis. When studies reported of medians, ranges or confidence intervals for continuous variables, statistical algorithms were used to derive the appropriate means and standard deviations. The OR for continuous variables could be cal- culated using the Mantle-Haenszel Chi square method with the ‘random effects’ meta-analytical technique. The ‘ran- dom effects’ model is particularly useful when conducting surgical research. This is because it takes into account the almost inevitable natural variation inherent between stud- ies. Subsequently a more conservative OR is produced. For both OR and MWD, corresponding 95% CI’s were calcu- lated. Regarding the Forest plots produced, a square repre- sents the point estimate of the treatment effect, that is the OR or MWD, with a horizontal bar going through the square showing the 95% CI. The summary measure of the pooled studies with 95% CI’s is represented by a diamond. RESULTS Study selection The initial literature search identified 598 papers, which matched the search criteria. Of these, 486 papers were eliminated due to broad incoherency with the aims of this study. Of the 112 remaining, a further 83 papers were excluded based on the exclusion criteria as outlined above. On more in depth examination of the 29 remain- Figure 1. Fonseka_Stesura Seveso 02/04/15 10:21 Pagina 42 43Archivio Italiano di Urologia e Andrologia 2015; 87, 1 Robotic cystectomy: A meta-analysis ing papers, a subsequent 5 were removed for not meet- ing the requirements of the inclusion criteria. Thus 24 studies were included in the final quantitative and qual- itative analysis (Figure 1) (6-29). Study characteristics Characteristics of all 24 studies included in the analysis are summarized in Table 1 (6-29). There were three random- ized control trials with the remaining 21 made up of ret- rospective and prospective studies. Each study was either 2-arm or 3-arm. For the purposes of the statistics RARC was always regarded as experimental. LRC was also con- sidered experimental except when being compared to RARC, in which case it was used as control. All of the stud- ies included were fairly recent with the oldest published in 2006. The two reviewers who selected the studies were in complete agreement (100%) about data extraction. A total of 2,104 cases were analyzed, with 1,100 (52.3%) undergoing ORC, 276 (13.1%) LRC and 728 (34.6%) RARC. Approximately 65% of patients were male. With regards to the pathological stage of the tumors, the average percentage of tumors that were non-organ confined (pT3- 4) was similar in both RARC and ORC groups. On average 30.1% of patients reported in the RARC studies had non- organ confined tumors compared with 29.5% in ORC group and 14.5% in the LRC group. On average 28% of patients undergoing RARC developed complications 90 days post-operatively. Major complications were defined as Table 1. Study characteristics. Matching: 1 - Age; 2 - BMI; 3 - ASA; 4 - Charlson; 5 - Gender; 6 - Pathological stage; 7 - Urinary diversion type. Study type: RCT - Randomized control trial; R - Retrospective, P - Prospective. Study Study type Cases Matching Mean age, yaers Exclusion criteria Study quality Country ORC LRC RARC ORC LRC RARC Abaza 2012 R 120 NR 35 1,2,6 69.8 NR 67.3 Undergoing lesser *** USA node dissection due to a history of radiation, aortoiliac grafting or significant comorbidity Abraham 2007 P NR 20 14 1,2,3,5,7 NR 77.6 76.5 NR **** USA Gan 2013 P 20 19 20 NR NR NR NR NR **** UK Galich 2006 P 24 NR 13 1,2,3,6 63.03 NR 66.2 Morbid obesity (generally **** USA body mass index _ 35), prior pelvic radiation, or significant medical comorbidities including pulmonary obstructive airway disease Gondo 2012 P 15 NR 11 1,2,4,5,6,7 69.7 NR 68.9 NR **** Japan Guillotreau 2009 P 30 38 1,2,3,5,6,7 64.9 (12.3) 67.9 (9.0) ******* France Ha 2010 R 34 36 1,2,5,6 55.9 (9.8) 67.5 (8.9) ***** Korea Haber 2008 R 50 50 1,2 67 66 *** USA Kader 2013 R 100 NR 103 1,2,3,5,6,7 66 NR 67 NR ***** USA Khan 2012 P 52 58 48 1,2,3,5,6,7 65 69.8 66.5 NR **** UK Knox 2013 R 84 NR 58 1,2,3,5,6,7 67.07 (1.2) NR 65.9 (1.2) NR **** USA Lin 2014 RCT 35 35 1,2,3,5,6 63.6 (8.9) 63.2 (9.1) ******* China Martin 2010 P 14 NR 19 1,2,3,5,6 68 NR 74 NR **** USA Musch 2014 P 42 100 1,2,3,4,5,6,7 69.0 (11.5) 71.4 (9.4) ******* Germany Nepple 2013 R 29 NR 36 1,2,5,6,7 67 NR 72 Contraindication ***** USA to robotic surgery Ng 2010 P 104 NR 83 1,2,3,5,6,7 67.2 NR 70.9 NR ***** USA Nix 2010 RCT 20 NR 21 1,2,3,5,6,7 69.2 NR 67.4 1) not surgical candidates, **** USA 2) not allowing randomization 3) those with preference for specific surgical modality Parekh 2013 RCT 19 NR 20 1,2,3,5,6 69.5 NR 69.5 1) Inability to give informed ***** USA consent, 2) unsafe for robotic approach, 3) clinical T4 bladder cancer, 4) clinical lymph node positive bladder cancer with grossly enlarged pelvic or retroperitoneal lymph nodes, 5) age younger than 30 or older than 90 years and 6) pregnancy. Porpiglia 2007 P 22 20 NR 1,2,3,5,6,7 71 63.5 NR NR ***** Italy Pruthi 2007 R 24 NR 20 1,6,7 68.2 NR 62.3 NR *** USA Rhee 2006 P 23 7 1,2,3,5,6 67 (13) 60 (9) ******* USA Richards 2010 R 35 NR 35 1,2,3,5,6,7 66 NR 65 NR **** USA Styn 2012 P 100 NR 50 1,2,3,4,5,6,7 65.6 NR 66.6 NR ***** USA Sung 2012 R 104 NR 35 1,2,3,5,6 65.9 NR 62.2 Had undergone radiotherapy **** Korea before operation or for whom palliative treatment was the primary aim Fonseka_Stesura Seveso 02/04/15 10:21 Pagina 43 Archivio Italiano di Urologia e Andrologia 2015; 87, 1 T. Fonseka, K. Ahmed, S. Froghi, S.A. Khan, P. Dasgupta, M. Shamim Khan 44 complications above Clavien grade 3, including return to operating room (OR) within 30 days post-operatively and death within 90 days post-operatively. 8.51% of patients undergoing RARC had major complications with 3 deaths (0.412%) within 90 days post-operatively. In the LRC stud- ies, 72.1% of patients developed complications with 3 deaths (1.087%) within 90 days post-operatively. The over- all complication rate in ORC was 47.2% with an average of 8.5% of patients having major complication. There were 7 deaths (0.64%) within 90 days post-operatively. The type of urinary diversion created with each technique was broadly classified into either conduit or bladder substitu- tion (neo-bladder). On average 17.4% of RARC patients had a bladder substitution compared to 13.04% in LRC and 12.4% in the ORC groups and the remaining had an ileal conduit urinary diversion. Synthesis of results RARC versus LRC As shown in Figure 2, OPT was significantly longer in RARC when compared to LRC (P = 0.02; mean weighted difference (MWD) was 47.61 with 95% confidence interval (CI) of 8.83 to 86.40). There was no statistically significant difference concerning LOS (P = 0.63; MWD = -1.95, 95% CI = -9.88 to 5.97) (Figure 3). There was also no statistical significance observed when comparing EBL (P = 0.17; MWD = -167.52, 95% CI = -408.48 to 73.44) (Figure 4). RARC versus ORC OPT was significantly longer in RARC when compared to ORC (P = < 0.00001; MWD = 60.78, 95% CI = 49.64 to 71.92) (Figure 5). Comparing other parameters of EBL, LOS and complications the analysis showed that there was significant reduction in EBL (P = < 0.00001; MWD = -638.24, 95% CI = -850.26 to -426.21) (Figure 6), LOS after RARC (P = 0.004; MWD = -1.75, 95% CI = -2.94 to -0.56) (Figure 7) and complications in the RARC group (P = < 0.0001; MWD = 0.53, 95% CI = 0.40 to 0.71) (Figure 8). There was no statistical difference in LNY (P = 0.87; MWD = -0.22, 95% CI = -2.83 to 2.39) (Figure 9) or PSM (P = 0.42; MWD = 0.80, 95% CI = 0.47 to 1.37) (Figure 10). Figure 2. Figure 3. Figure 4. Figure 5. Fonseka_Stesura Seveso 02/04/15 10:21 Pagina 44 LRC versus ORC Comparing LRC to ORC operative time was significantly longer using LRC (P = 0.002; MWD = 34.93, 95% CI = 12.76 to 57.10) (Figure 11). EBL was significantly reduced in the LRC group (P = 0.0009; MWD = -480.96, 95% CI = -765.04 to -196.88) (Figure 12). Likewise LOS was signif- 45Archivio Italiano di Urologia e Andrologia 2015; 87, 1 Robotic cystectomy: A meta-analysis Figure 6. Figure 7. Figure 8. Figure 9. Fonseka_Stesura Seveso 02/04/15 10:21 Pagina 45 Archivio Italiano di Urologia e Andrologia 2015; 87, 1 T. Fonseka, K. Ahmed, S. Froghi, S.A. Khan, P. Dasgupta, M. Shamim Khan 46 icantly shorter in the LRC group (P = 0.001; MWD = -2.54, 95% CI = -4.08 to -0.99) (Figure 13). There was no statis- tical difference in LNY (P = 0.99; MWD = 0.01, 95% CI = -1.11 to 1.13) (Figure 14). DISCUSSION Comparing RARC to LRC, the results show that there is no statistical difference in LOS or EBL but the operating time is significantly longer. More data is needed to see Figure 10. Figure 11. Figure 12. Figure 13. Figure 14. Fonseka_Stesura Seveso 02/04/15 10:21 Pagina 46 whether complication rate is significantly reduced when comparing RARC to LRC. RARC takes longer to do than ORC but produces better surgical outcomes with reduced EBL, shorter LOS and fewer complications. There are equivalent oncological outcomes (LNY and PSM.) When comparing LRC to ORC, LNY is equivalent but there is an increase in OPT, reduction in EBL and short- er LOS using the laparoscopic approach. The results therefore are in favor of using LRC in preference to ORC. It may be that it is when the robotic technique is used with intracorporeal urinary diversion, as opposed to extracorporeal, that it is superior to LRC. Most studies included used extracorporeal urinary diversion. Intracorporeal urinary diversion has been demonstrated to be technically feasible with good oncological out- comes (13,30). More data is needed to assess long-term outcomes. The difficulty in obtaining data on complications results from a lack of consistency in reporting complications. In this paper the Clavien-Dindo system was used and it is broadly accepted as the better current standard for reporting of surgical complications. All future trials assessing the complications in radical cystectomy should use this system to facilitate universal comparison (31). One outcome in which data was lacking was PSM. A study using data from the International Robotic Cystectomy Consortium (IRCC) (32) found that the rate of PSM was similar between RARC and ORC, consistent with the results of this meta-analysis. Variables associat- ed with increased probability of PSM using RARC included older age, higher pathological T stage and lymph node positivity. A similar study by the IRCC reviewed the outcomes of extended lymph node dissection, an essential part of rad- ical cystectomy (33). Similar lymph node yields were obtained in RARC and ORC, which were found to be the case in this study. The study also identified that high vol- ume institutions (≥ 100 cases) had 3.46-times increased probability of carrying out extended lymph node dissec- tion (LND). It is crucial that survival data is reported in the studies of different surgical techniques to see if technology is hav- ing an influence on the survival of these patients. This would only be possible with longer follow up after surgical procedures. Kaplan-Meier plots to compare sur- vival rates between the three operative techniques would prove valuable in assessing the evidence for RARC. Guru et al. (34) have shown that surgical and oncological outcomes constantly improve with each RARC case the surgeon performs. The learning curve for RARC was defined by results from the IRCC. Using proxy measure- ments for RARC quality such as OPT, EBL, LNY and mar- gin positivity it was found that acceptable proficiency in the procedure was attained by the 30th case. The cost of RARC is estimated to be about $20,000 per case and is an important factor to consider when evaluat- ing the use of RARC. Lee et al. (35) have found that RARC is less expensive than ORC when ileal conduit or conti- nent cutaneous diversion is performed. The main driver of cost was LOS and though material cost was higher with RARC, in high-volume centres RARC can be more cost- effective particularly with ileal conduit urinary diversion. The true benefit of RARC may lie in the improved ergonomics of the robotic system. The more comfortable operating system may cause less fatigue to the surgeon as compared to laparoscopic methods, thereby leading to fewer errors. This was shown by Elhage et al. (36) where time taken to perform a suturing task was not only short- er compared to laparoscopic and open, but there were also fewer errors made when compared to the laparoscopic method. The major limitation of this study is the possi- bility of bias. When evaluating surgical procedures there is always a lack of blinding and natural variation in both the skill of the surgeon pathology of different cases. This is reflected in the significant heterogeneity found in the forest plots of this study. Inclusion criteria varied among studies as well as there being different systems of follow- up with differing outcome definitions. Publication bias is also a possibility that was not factored into this study. CONCLUSIONS The results of this meta-analysis shows that LRC pro- vides better outcomes than ORC but that RARC provides similar outcomes to LRC, only with longer OPT. More randomised control trials are required to provide conclu- sive evidence to show whether or not RARC is in fact a better alternative to ORC or LRC. These studies must use a unified system for the classification of complications and assess both surgical and oncological outcomes. More data is also needed on the ergonomics, learning curve, cost-effectiveness and patient-perspectives of RARC. ACKNOWLEDGEMENTS P.D. acknowledges financial support from the National Institute for Health Research (NIHR) Biomedical Research Centre based at Guy’s and St Thomas’ NHS Foundation Trust and King’s College London. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health. P.D. also acknowledges the support of the MRC Centre for Transplantation, London Deanery, London School of Surgery and Olympus. P.D., S.K. and K.A. acknowledge funding for the SIMULATE project from the Urology Foundation (TUF) and the BAUS. 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Correspondence Thomas Fonseka (BSc) King’s College London School of Medicine, London, UK Kamran Ahmed, MRCS, PhD (Correspondent Author) kamran.ahmed@kcl.ac.uk Saied Froghi, MBBS Prokar Dasgupta, MSC, MD, FEBU, FRCS Urol Mohammad Shamim Khan, OBE, FEBU, FRCS Urol NIHR Academic Clinical Lecturer /Specialist Registrar in Urology MRC Centre for Transplantation, Guys Hospital St Thomas Street, London SE1 9RT, UK Shahid A Khan, FRCS Urol Surrey and Sussex Healthcare NHS Hospital, Redhill, UK Fonseka_Stesura Seveso 02/04/15 10:21 Pagina 48