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The Role of Laparoscopic and Robotic Cystectomy in the Management of Muscle-Invasive Bladder Cancer With Special Emphasis on Cancer Control and Complications

Abstract

Context

Minimally invasive radical cystectomy (MIRC) techniques for the treatment of muscle-invasive bladder cancer (BCa) are being increasingly applied. MIRC offers the potential benefits of a minimally invasive approach in terms of reduced blood loss and analgesic requirements whilst striving to provide similar oncologic efficacy to open radical cystectomy (ORC). Whether quicker recovery, shorter hospital stay, and a reduction in complications are routinely achieved with MIRC remains to be proved in prospective comparisons.

Objective

To explore both laparoscopic radical cystectomy (LRC) and robot-assisted radical cystectomy (RRC), focusing specifically on the oncologic parameters and comorbidity of the procedures. Reported complications from major centres are identified and categorised via the Clavien system. Positive margins rates, local recurrence, and both cancer-specific survival (CSS) and overall survival rates are assessed.

Evidence acquisition

A comprehensive electronic literature search was conducted in November 2010 using the Medline database to identify publications relating to laparoscopic, robotic, or minimally invasive radical cystectomy.

Evidence synthesis

There are encouraging short- to medium-term results for both LRC and RRC in terms of postoperative morbidity and oncologic outcomes. It seems possible in experienced hands to perform a satisfactory minimally invasive lymphadenectomy regarding lymph node counts and levels of dissection. Positive soft-tissue margins are similar to large open series for T2/T3 disease but inferior for bulky T4 disease. Local recurrence rates and CSS rates seem equivalent to ORC at up to 3 yr of follow-up; however, mature outcome data still need to be presented before definitive comparisons can be made.

Conclusions

Robotic and laparoscopic cystectomy has a growing role in the management of muscle-invasive BCa. Long-term oncologic results are awaited, and there are concerns over the ability of MIRC to treat bulky and locally advanced disease, making careful patient selection vital. Forthcoming randomised trials in this area will more fully address these issues.

Take Home Message

Minimally invasive radical cystectomy (MIRC) is rapidly becoming part of mainstream urology as an attractive option for skilled surgeons. Proper dissection can be achieved, but dedication is required to optimise outcomes. Bulky advanced tumours should be avoided, limiting MIRC to selected patients until oncologic evidence matures.

Keywords: Laparoscopic radical cystectomy, Robotic radical cystectomy, Bladder cancer.

1. Introduction

Although open radical cystectomy (ORC) remains the gold standard treatment for muscle-invasive, organ-confined bladder carcinoma, there is increasing interest in both laparoscopic radical cystectomy (LRC) and robot-assisted radical cystectomy (RRC). Minimally invasive radical cystectomy (MIRC) for muscle-invasive bladder cancer (BCa) has been one of the final frontiers of urologic oncology to be addressed by emerging pure laparoscopic and, more recently, robot-assisted techniques. Some pioneers of these new techniques believe that LRC and RRC lead to faster recovery, shorter hospital stay, and more rapid return to daily activities compared with ORC while offering the same functional and oncologic results. As these laparoscopic and robotic approaches evolve, there remains significant scepticism of the true benefits of MIRC because of the lack of adequate comparative data and sufficient follow-up to demonstrate similar oncologic outcomes in comparison to traditional ORC, where at specialised centres, the 5-yr survival for select patients with organ-confined, muscle-invasive, lymph node–negative disease approaches 89% [1] . Despite aggressive surgical treatment, 50% of all patients undergoing radical cystectomy (RC) for locally advanced cancers (≥T3) experience tumour recurrence, and many subsequently die from the disease [1] . Although some potential advantages may be provided in terms of blood loss, analgesic requirements, reduced scarring, and recovery, the key question is whether MIRC approaches are a clear forward step in terms of oncologic outcomes and morbidity. These issues still need to be fully evaluated. There may be postoperative complications specifically related to minimally invasive approaches, and many are concerned that case-selection issues dominate the literature in this area. Many patients requiring RC are deemed unsuitable (because of clinical characteristics or pathologic features) for MIRC, which leads to selection bias in many comparative studies.

There is increasing indication that an extended pelvic lymphadenectomy (PLND) at the time of the cystectomy can also improve survival [2] and [3]. Larger centres have proposed optimum standards for this procedure, such as ≤10% positive surgical margin (PSM) rate overall and 15% in patients with T3 and T4 tumours. The median number of lymph nodes undergoing pathologic examination should generally be at least 10–14, although it is the level of dissection itself that is of primary importance, as focusing on node counts alone is not the goal [3] and [4]. Although ORC has become safer in expert hands, it remains a formidable procedure, with a complication rate of around 40–65% [5] . Excessive bowel handling, fluid loss, and opiates can lead to prolonged ileus. In spite of improvements in surgical techniques, blood loss during ORC is often significant, requiring transfusion in up to 66% of cases [5] .

LRC is an advanced laparoscopic procedure that places significant demands on the patient and the surgeon alike. Taking place within the confines of the true pelvis in a highly morbid population, LRC represents a formidable challenge to urologic laparoscopists. It is a prolonged procedure that includes several technical steps and requires highly developed laparoscopic skills, including intracorporeal suturing. RRC is similarly a complex and demanding procedure that may benefit from the enhanced optical and ergonomic features of the da Vinci Surgical System (Intuitive Surgical, Sunnyvale, CA, USA). Generally, both LRC and RRC mimic the standard ORC procedure with small technical modifications resulting from their minimally invasive nature. The procedures involve initial ureteric identification and ligation, posterior dissection between the rectum and prostate, followed by control of the lateral pedicles to the bladder and, finally, anterior dissection and PLND. In women, the vagina is reconstructed with a running intracorporeal suture.

2. Evidence acquisition

A comprehensive electronic literature search was conducted in November 2010 using the Medline database to identify publications relating to laparoscopic, robotic, or minimally invasive RC.

3. Evidence synthesis

3.1. Brief evolution and history of laparoscopic and robot-assisted radical cystectomy

Laparoscopy for definitive oncologic treatment has progressed slowly compared to other areas secondary to the hypothetical risks of tumour dissemination or port site implantation. LRC was first performed by Parra in 1992 for pyocystis after a supravesicle urinary diversion a few months earlier [6] . This procedure was closely followed by the first LRC and extracorporeal ileal conduit for an invasive bladder tumour performed on a female patient by a group from Malaga [7] . Puppo et al. then described anterior pelvic exenteration in five females through a combined transvaginal and laparoscopic approach in 1995 [8] . It was soon shown that the entire procedure could be completed intracorporeally with an ileal conduit [9] , ileal neobladder [10] , or continent reconstruction via a rectosigmoid pouch [11] and [12]. Several series from major institutions gradually appeared, showing good early oncologic results over the initial 2–3 yr (and some patients up to 5 yr) with low morbidity [13], [14], and [15], although reoperation rates were initially high at up to 29% [16] . The largest series of LRC is currently from China, where 171 patients had an orthotopic ileal neobladder reconstruction with a median follow-up of 37 mo (maximum: 7 yr) [17] . Clearly, longer median follow-up periods are required to determine clear LRC survival probabilities.

With the arrival of the da Vinci system in 2001, many units with access to a robotic system switched form LRC to RRC after the publication of the initial cases of RRC and the increasing availability of the robotic platform. It is generally felt that there is a decreased learning curve in RRC for surgeons without prior experience in laparoscopic surgery. The da Vinci system has the potential to overcome some of the technical difficulties of LRC, including fatigue, tremor, and intracorporeal suturing. The first RRC was reported in 16 Egyptian patients by Menon et al. in 2003 [18] , followed soon after by a single case report of RRC with intracorporeal neobladder from Germany [19] . Following this, Menon and colleagues described the initial series of RRC in both men and women [20] , and other units subsequently confirmed proof of concept and short-term oncologic efficacy [21], [22], and [23].

3.1.1. Selection criteria for laparoscopic and robot-assisted radical cystectomy

One difficulty in comparing nonrandomised cohort studies in this area is the real possibility for a selection bias. As novel techniques commence, it is only natural and appropriate to select favourable patients to try and ensure patient safety and optimal outcomes. Many programmes offering MIRC tend to select patients with less advanced disease and a good comorbidity profile early in their series and typically offer the procedure to patients with organ-confined, nonbulky BCa, as determined by preoperative clinical and radiographic findings [22] . The presence of bulky lymphadenopathy, locally advanced disease (T4), uncorrected coagulopathy, and morbid obesity (body mass index [BMI] >35) are strong contraindications to MIRC. These favourable selection criteria would also include those patients most likely to recover more quickly from ORC with a lower risk of requiring a transfusion and a high probability of cure. In contrast, some institutions are offering LRC or RRC to all patients requiring—and fit for—cystectomy [13] and no longer perform ORC. Consequently, there is no selection bias in these groups; however, this policy may be responsible for early reports from these centres showing higher PSM and more T3/4 disease stages in the initial learning curve [21] .

All patients need to be able to withstand a pneumoperitoneum with a significant degree of Trendelenberg angulation. Some groups have regarded severe cardiorespiratory compromise as a relative contraindication to RRC because of the operative position. The cohort of patients requiring RC is amongst the most comorbid of all urologic subgroups. Respiratory compromise, cardiovascular disease, and renal impairment are common with many series, having >50% of patients with an American Society of Anaesthesiologists (ASA) score ≥3 and 50% with a BMI >30. In addition, specifically for MIRC, patients with significant prior abdominal surgery and/or prior radiation therapy (RT) are often avoided because of concerns about prolonged laparoscopic adhesiolysis and the consequent risks of bowel injury and poor anastomotic healing. It has been shown that these patients can have higher complication rates and an inferior lymphadenectomy [24] .

3.2. Lymphadenectomy

Radical cystectomy is defined as the removal of the bladder, prostate, and seminal vesicles in the male and of the uterus, ovaries, and fallopian tubes in the female combined with the surrounding perivesical tissues and pelvic lymph nodes. Thus, LRC and RRC must be able to replicate the standardised lymphadenectomy possible with open surgery [4] to be established as alternative techniques. There were initial concerns that the manoeuvrability of the standard da Vinci system may not permit an adequate extended lymphadenectomy that is increasingly being seen as the standard of care.

An extensive regional lymphadenectomy at the time of RC has been shown to aid oncologic control, with node-positive patients having up to a 36% survival at 5 yr [25] and [26] in several other confirmatory studies. There is strong evidence that the more nodes removed at cystectomy, the better the chance of long-term survival [27] and [28]. The extent of the lymphadenectomy and the number of nodes removed has been viewed as an indirect surrogate of the indicator of the quality of the surgery and may contribute to a more thorough removal of microscopic tumour within the perivesical soft tissues in the pelvis [29] .

Lymphadenectomy during LRC requires high-level laparoscopic skills. However, it would seem that experienced surgeons are capable of performing a laparoscopic lymphadenectomy with node counts equivalent to these major series of ORC. In Huang's recent large series of LRC [16] , a median of 16 nodes (range: 5–46) were excised, although an extended lymphadenectomy to the aortic bifurcation was only performed in higher-risk patients (≥T3, abnormal nodes on preoperative computed tomography scan). The mean BMI is this series was 21.3, which is reflective of the local population and significantly lower than most other centres, perhaps aiding the node dissection.

There have been concerns that RRC does not permit the same extent and quality of lymphadenectomy as is possible with ORC, particularly using the initial da Vinci model, but the improved range of movement possible with the da Vinci S and Si systems has alleviated many of these concerns. Acceptable lymph node yields have been reported in RRC [30] , with mean node counts up to 18 (range: 6–43), and with this stage of the procedure lasting around 44 min with little comorbidity. A nonrandomised comparative study has also shown equivalence between ORC and RRC lymph node yields (15 vs 16) [31] using the same bilateral template for node dissections, with boundaries of the aortic bifurcation proximally, genitofemoral nerve laterally, circumflex iliac vein and node of Cloquet distally/caudally, and hypogastric vessels and iliacus muscle posteriorly. A small randomised, prospective trial comparing RRC and ORC showed equivalence in node counts [32] , with a mean of 18 nodes removed in the open group and 19 nodes removed in the robotic group. In this study, the lymphadenectomy template included removal of the obturator, external iliac, hypogastric, and common iliac lymph node chains but did not include a para-aortic dissection.

A prospectively maintained but retrospectively analysed database held by the International Robotic Cystectomy Consortium (IRCC) recorded lymph nodes yields for 527 patients who underwent RRC for urothelial carcinoma (UC) by 22 surgeons at 15 institutions worldwide [33] . In this large cohort, a median of 17 lymph nodes per RRC were examined (range: 0–68), with high yields associated with tumour stage (pT4), sequential case number, institution volume, and individual surgeon volume. Encouragingly, 83% of cases in this database had a formal lymph node dissection (≥10 nodes) at RRC, with only seven patients having no nodes removed. We can conclude from these studies that the extensiveness of lymphadenectomy now advocated for RC is certainly possible with RRC and that the number of nodes excised at RRC is similar to ORC series. In addition, robotic surgeons appear to be incorporating at least PLND into their standard technique, although the IRCC comprises a group of highly motivated minimally invasive surgeons. There appears to be a learning curve associated with the performance of lymphadenectomy at RRC, as surgeons excised more nodes as their series grew. Similarly, high-volume surgeons and institutions were more likely to perform lymphadenectomy at RRC than their low-volume counterparts. It remains to be seen whether MIRC lymphadenectomy can consistently reach the high node counts (25–30 nodes) seen in the highest-volume ORC centres, and future randomised studies must strive to compare MIRC with the optimum ORC lymphadenectomy standards.

3.3. Complications after laparoscopic and robot-assisted radical cystectomy

ORC remains a highly morbid procedure, with a historical published rate of postoperative complications of between 30% and 60% from large pelvic oncology centres [1], [5], and [34]. In recent years, the method of complication reporting has received deserved focus, with most contemporary series using the Clavien system or a modification version thereof [35] . Importantly, this change extends the period of reporting from 30 to 90 d. Prior to this, the disparity in the quality of complication reporting after RC made it impossible to compare the morbidity of new surgical techniques. As this new system has been disseminated throughout urologic reporting and surgery in general, it has shown increased rates of complications compared with previous studies because of more rigorous prospective reporting and the standardised methodology, making comparisons with earlier open series more difficult to interpret. Shabsigh and colleagues have shown the Clavien-Dindo system to be highly relevant in defining the morbidity of RC [5] . They reported that 64% (735 of 1142) of ORC patients experienced a complication within 90 d of surgery, with 13% having a grade 3–5 complication and a mortality of 1.5%. Important predictors of serious (grade 3–4) complications included patient increased age, prior abdominal/pelvic surgery, and ASA score >2, which are patient variables potentially avoided early in minimally invasive RC series. It should be remembered in this series that although the overall rate of complications using a prospective, rigorous collection technique appears higher than previously published, 85% of these reported complications were low grade (1–2), and serious complication rates (3–4) remained relatively low (13%).

The reported rates of complications in LRC fall between 8% and 42% in the recent major LRC series [11], [12], [13], [14], [36], and [37], with some institutions reporting at least one patient death ( Table 1 ). Many series do not define blood transfusion as a complication; however, the Clavien system indicates that it should be counted as such [35] . Although the only randomised controlled trial (RCT) of RRC was designed as a noninferiority study regarding lymphadenectomy node retrieval, it also reported no difference in complications between the two small groups (n = 20) [32] , although in this study, this end point was underpowered to clearly define this relationship.

Table 1 Complications of laparoscopic and robot-assisted radical cystectomy, including the larger series

Series; type Sample, no. Age, yr, mean (range) BMI kg/m2, mean (range) ASA grade ≥3, no. (%) Overall complication, no. (%) Transfusions, no. (%) Clavien grade 1–2, no. (%) Clavien grade 3–4, no. (%)
Haber and Gill, 2007 [13] ; LRC 37 66 (37–81) 26 (17.4–34.6) 24% 9 (25) 1 of 37 (3) 5 of 37 (14) 4 of 37 (11)
Haber et al, 2008 [36] ; LRC 572 65 26 NR 35%

Intraoperatively: 33 (7)

Postoperatively: 139 (28)
Blood loss: 556 ml NR NR
Castillo et al, 2006 [37] ; LRC 59 NR NR NR 25 (42)

2 deaths
12 (20) 19 (32) 6 (10)
Cathelineau et al, 2005 [14] ; LRC 84 61 (36–79) NR 17% 15 (8) 5% 14 1
Hemal et al, 2008 [15] ; LRC 48 59 25 (21–33) 14 (27) 13 (27)

1 death
21 (44) 8 of 48 5 of 48 (10.4)
Huang et al, 2010 [17] ; LRC 171 63 (27–84) 21.3 (15.0–26.4) Excluded from LRC 67 (39) 17% 44 (26) 23 (13)
Ng et al, 2009 [39] ; RRC 83 70.9 26.3 43% 37 (48.1) 6 (7.2) 24 of 83 (29) 13 of 83 (17)
Khan et al, 2011 [38] ; RRC [38] 50 66 (38–79) 28.7 ± 4.1 9 of 50 (18) 17 of 50 (34) 4% 12 of 50 (24) 5 of 50 (10)
Guru et al, 2007 [21] ; RRC 20 70 (56–90 26 (17.3–36) 6 of 20 (30) 4 of 20 (20)

1 conversion
0% 2 of 20 (10) 2 of 20 (10)

1 death

BMI = body mass index; ASA = American Society of Anaesthesiologists; LRC = laparoscopic radical cystectomy; NR = not reported; RRC = robot-assisted radical cystectomy.

There have been concerns that LRC and RRC may generate higher rates of some complications because of the minimally invasive approach. One example is anastomotic stricture and/or urinary leak at the uretero-ileal anastomosis, which occurs up to 8% of the time after RRC. This was certainly evident early in some series and may have been to the result of poor mobilisation of the left ureter or ureteric kinking as it was passed beneath the mesocolon [38] and [39]. Further problems may become evident with longer follow-up periods. Despite initial concerns, there does not seem to be a high number of complications specific to the minimally invasive approaches. It should be remembered that most units have case selected early in their series, whilst only a few have taken on all patients requiring minimally invasive RC [21] . Ng's group has suggested a decrease in the rate of high-grade complications compared to ORC [39] , with a 17% major complication rate in 83 patients undergoing RRC compared to a 31% high-grade complication rate observed in 104 ORC patients. The authors concluded that RRC is associated with a lower major complication risk; however, as noted in prior large ORC series, the high-grade complication rate for ORC should be in the range of 13% [5] . Series reporting an increased risk of major complications in their open population compared to other centres suggest either a difference in experience between surgical techniques or a mismatched patient population. Though arguably reduced in comparison to some ORC series [5] , urologists should be in no doubt that RC remains a formidable operation on highly comorbid patients, whatever technique is used.

Some of the reported series give insufficient data on the patient population undergoing RC, which limits the ability to compare these reports to other contemporary series. Martin and colleagues have made clear recommendations for the standardised reporting of surgical complications [40] , and these recommendations should be used routinely in the RC literature and throughout urologic oncology to permit the reliable comparison of outcomes among different centres, surgeons, or techniques [41] . These criteria include recording data on the methods of data acquisition, the duration of follow-up, whether outpatient complication data are included, mortality rates and cause of death, morbidity rates (number of patients, total number of complications recorded), an indication of procedure-specific complications, the use of a grading system to clarify severity of complications, the median or mean length of stay, and an indication of the methodology used to assess patient risk stratification (eg, Charlson-Romano index, ASA scoring).

3.4. Oncologic outcomes

To maintain the enthusiasm for MIRC, the oncologic outcomes must be rigorously assessed and maintained. Parity with ORC is the minimum requirement because, above all else, surgical quality may determine outcome. Incomplete surgery cannot be salvaged by current systemic therapies, and local recurrences are invariably associated with a fatal outcome. MIRC must adhere to all the oncologic principles previously established from the ORC experience.

3.4.1. Surgical margins

We know clearly that a PSM in the perivesical soft tissues after RC for BCa is an independent predictor of metastatic progression and leads to an increased probability of disease-specific death [42] . In this landmark study, the soft tissue surgical margin rate for ORC was 4.2% overall and 7% for extravesical disease, and a PSM more than doubled the risk of metastatic progression (74% vs 32%) and almost doubled the risk of subsequent BCa death. We also know that in expert hands. there should be no PSM in tumours that are organ confined. Positive margins seen in ORC as the presence of tumour at the surgical margin is usually not a surgical mistake (cutting through the tumour bulk) but rather is associated with infiltration of the soft-tissue boundaries of the bladder. However, the observation that only 9% of the locally advanced tumours were associated with a positive margin suggests that negative margins can be achieved in high-risk cases by wide dissection of the perivesical soft tissues. PSM at the urethra and ureters are usually considered less important than if the tumour has been cut through at any other location. In several of the MIRC studies to date, it is not clear whether this subgroup of positive margin patients have been differentiated from others. The International Laparoscopic Cystectomy Registry (ILCR) has been established, and in this international registry for LRC, the PSM rate was only 2% (9 of 574 patients) [36] .

The IRCC has also evaluated this issue in RRC [43] and found that 35 of 513 patients (6.8%) undergoing RRC had PSM. This study evaluated 21 surgeons at 14 institutions and showed that increasing age, increasing pathologic T stage, and lymph node positivity were predictive factors for a positive margin, while gender, case number, and institutional volume were not. The rates of margin-positive disease at RRC were 6.8% overall (1.6% for patients with ≤pT2 disease, 8.6% for pT3 disease, and 40% for pT4 disease). These PSM rates for RRC (particularly pT1–2 disease) from this large, multi-institutional, prospective cohort are similar to the 1–10% in seen large ORC series [1] and [42] and equivalent to other RRC reports [44] and [45]. Presently, the IRCC collects data based on pathology (using reports), not clinical staging, which is likely to skew their results. It is unclear how many of their patients had a palpable mass, hydronephrosis, or other signs of advanced disease. As a result, current enthusiasm for approaching locally advanced tumours by the RRC technique should be tempered, as there remains a concern that positive margin rates for T3 and T4 tumours are higher than the rates reported in ORC (7.6% of pT3 and 24% of pT4 cases) [46] . It may be that in patients with these more locally advanced tumours, the lack of tactile feedback to determine the surgical planes coupled with the relative inexperience of the minimally invasive approach negatively influences the margin rates. It is also possible that some of the increased rates of surgical margins seen in RRC are the result of excessive robotic manipulation of the specimen rather than incomplete resection, and only long-term recurrence rates will determine whether all of these margins are as meaningful as those seen in ORC. As nearly 50% of all RC specimens demonstrate extravesical disease, careful patient selection should be recommended until further data clarify the ability of RRC to adequately excise more advanced lesions.

3.4.2. Local and distant recurrence

In Dotan's study looking at the influence of positive margins on local recurrence rates, these rates were increased for the patients with PSM compared to the negative margins group (21% vs 6% at 5 yr after cystectomy) [42] . In addition, metastatic disease developed in the majority of patients, with local recurrence at a mean of 6 mo following the detection of local recurrence.

The rates of local recurrence after ORC are generally around 7–10% [1] . At the present time, with limited follow-up, this rate appears equivalent or lower in the LRC and RRC groups ( Table 2 ), with several institutions reporting low local recurrence rates even though there was a slightly higher margin rate, possibly because of more favourable patient selection. Overall survival (OS) in the LRC cohorts was 90–100% at 1–2 yr and 63–79% at 2–3 yr. Publications reporting RRC demonstrated a 90–96% OS rate in 1–2 yr of follow-up. These figures should be compared to large series of ORC, showing a 62–68% recurrence-free survival (RFS) at 5 yr and 50–60% rate at 10 yr, with OS rates of 59–66% at 5 yr and 37–43% at 10 yr [47] . Kauffman's recent series of 85 cases of RRC has shown that at a mean follow-up of 18 mo, 20 patients (24%) developed recurrent disease, but only 3 patients (4%) had recurred locally, offering some short-term reassurance of the oncologic efficacy of RRC [48] .

Table 2 Oncologic outcomes of larger series of laparoscopic and robot-assisted radical cystectomy

Series No. and type Age, med/mean yr (range: 27–84) Follow-up, mo, median/mean (range) Lymph node yield, mean (range) PSM, no. (%) Recurrence: local and distant Mortality: RFS, CSS, OS
Stein et al, 2001 [1] 1054 ORC 66 (22–93) 122 (0–28 yr) Pelvic iliac template

Numbers NR
NR Local: 7.3%

Distant: 22.2%
RFS: 68% 5 yr

OS: 66% 5 yr

RFS: 60% 10 yr

OS: 43% 10 yr
Haber and Gill, 2007 [13] 37 LRC 66 31 (1–66) 14.8 2 (5) Distant: 5.4% CSS: 92%

OS: 63%
Haber et al, 2008 [36] 392 LRC 65 18 (0.5–72) 13 (0–36) 2 (9) Local: 27 (5%)

Distant: 39 (8%)
CSS: 80%

OS: 65%
Hemal et al, 2008 [15] 48 LRC 59 (24–80) 38 (10–72) 14 (4–24) 1 (2) urethral Local: 1

Distant: 8
RFS: 73%

OS: 79%
Cathelineau et al, 2005 [14] 84 LRC 61 (36–79) 18 (1–44) NR 0 Local: 5 (6%)

Distant: 3 (4%)
RFS: 83%

OS: 100%
Huang et al, 2010 [17] 171 LRC 63 37 (3–83) 16 (5–46) 0 Local: 11 (6.4%)

Distant: 25 (14.6%)
RFS: 72.6%

CSS: 81.3%

OS: 73.7%
Menon et al, 2003 [18] 17 RRC NR NR (4–27)

1 positive
0 NR NR
Guru et al, 2010 [21] 20 RRC 70 NR 13 (6–26) 1 (5) NR NR
Dasgupta et al, 2008 [63] 17 RRC 66 (38–77) 23 (7–44) 16 (6–28) 0 RFS: 90% CSS: 95%

OS: NR
Kauffman et al, 2011 [48] 85 RRC 73.5 18 (1–40) 19.1 5 (6) Local: 3 (4%)

Distant: 20 (24%)
CSS: 85%

OS: 79%
Pruthi et al, 2010 [44] 100 RRC 65.5 (33–86) 21 19 (8–40) 0 15% any recurrence CSS: 94%

OS: 90%

PSM = positive surgical margin; RFS = recurrence-free survival; CSS = cancer-specific survival; OS = overall survival; ORC = open radical cystectomy; NR = not reported; LRC = laparoscopic radical cystectomy; RRC = robot-assisted radical cystectomy.

A lack of long-term follow-up clearly positively slants the data for MIRC, and a significant selection bias is also likely to skew many series, as most authors describe avoiding bulky and possible T4 tumours early in their series. Bearing this in mind, the reported results for MIRC do not seem to suggest unusual recurrence rates or patterns in patients undergoing robotic cystectomy at the current time. Concerns regarding peritoneal seedling resulting from the pneumoperitoneum have not been realised thus far. Port-site recurrence seems rare with current techniques for intra-abdominal placement of the specimens into laparoscopic bags, with only one case reported for a muscle-invasive, high-grade bladder tumour after RRC [49] .

Overall, the data for the long-term oncologic outcomes of LRC and RRC is lacking. The majority of published series have inadequate follow-up periods, with few series reporting follow-up to 5 yr. Most minimally invasive surgery (MIS) series report median or mean follow-up <2 yr ( Table 2 ). Based on the relatively small number of reported cases in the MIS series and their lack of adequate follow-up, and despite the huge enthusiasm for these techniques, true oncologic effectiveness has not been established. Few series have follow-up to 5 yr, let alone 10 yr. Thus, equivalency or noninferiority will only be determined in the context of adequately powered randomised clinical trials.

3.5. Discussion

Despite significant enthusiasm for both LRC and RRC in many centres worldwide, there remains concern over pathologic and long-term oncologic results, particularly in patients with more advanced disease [50] . Guru's group has identified this issue of potentially higher PSM rates in high-stage bladder tumours treated with RRC [51] . The selection bias present in many early series may have falsely elevated our expectations for MIRC, and it is evidently sensible for surgeons considering these approaches to select healthier patients with more favourable tumour characteristics for their initial experience.

These outcomes clearly need to be verified in an appropriately powered RCTs, with composite complication rates and oncologic outcomes as the primary outcome measures. Many reports to date have been from single institutions and contained small numbers of patients, and most are not randomised or even compared to equivalent ORC groups. Future comparisons of MIRC should be directly compared to contemporary ORC series from the same institution, ideally in a randomised fashion. The time to conduct a large RCT in robot-assisted radical prostatectomy (RARP) has already passed, but for both LRC and RRC, now is the moment, and several studies (the UK's CORAL [52] and BOLERO studies, and the Memorial Sloan-Kettering Cancer Centre study) are already underway. Comprehensive data that includes the extent of lymphadenectomy, lymph node counts, PSM, local and distant recurrence, and longer-term survival (disease-specific and overall) should be the standard of reporting. In the current financial climate, a detailed health economic evaluation of expensive new technologies is also vital.

The issue over whether it is possible to perform an adequate lymphadenectomy during MIRC seems to have been adequately answered by experienced minimally invasive surgeons from the large institutions. It is becoming clear that the PLND within MIRC is feasible, safe, and equivalent to the open lymph node dissection technique seen in most centres, within the same anatomic boundaries up to the aortic bifurcation [53] . Whether the highest node counts seen in quaternary centres performing lymphadenectomy up to the inferior mesenteric artery is possible in MIRC awaits confirmation.

Complications have been reported as reduced when using either LRC or RRC compared to ORC; however, patient selection bias clearly makes a definitive statement regarding complications difficult. There is often a wide difference in complication rates in the various published series despite using standardised reporting systems, confirming the difficulties faced when studying complications. There remains a high risk of underreporting, and differences between series probably reflect variations in reporting. Reassuringly, it does not seem that there are an elevated number of complications specifically related to the minimally invasive approach at this stage. Whether longer-term follow-up will reveal increased numbers of MIRC-related issues, such as left ureteric strictures, needs close observation. This review also seems to indicate that in patients with UC of the bladder that is ≤pT2, LRC and RRC achieve comparable, acceptable PSM to ORC. Of concern, however, in those with higher-stage disease (pT4) and perhaps in those with pT3 disease, PSM rates are higher, and the loss of tactile feedback or inexperience with the technique may contribute to this rise. Multiple factors other than surgeon expertise and the type of procedure performed may influence the incidence of positive margins. Those with significant comorbidity and >80 yr of age may benefit from a quicker open procedure than a more prolonged MIRC with the additional affects of laparoscopy [42] and [54]. In addition, data on the outcome of patients managed with LRC or RRC who have undergone prior pelvic surgery and exposure to pelvic RT is lacking and should likely be avoided. There are few patients who are not fit for ORC in high-volume institutions, but the same is probably not true for MIRC.

The outcomes data from the multi-institutional collaborative series for both LRC and RRC probably provide the strongest current data for the morbidity and oncologic efficacy of MIRC. These group efforts are the only papers with sufficient numbers of cases to make meaningful analysis of the outcomes for different subgroups, as the largest cohort from a single institution is 171 [17] . Standardised prospective data collection and adherence to detailed established complication classifications should be included in future multicentre studies to provide the highest-quality data possible for comparison to previously published ORC data. The IRCC has also been able to make useful statements regarding training in RRC and the role of previous robotic prostatectomy experience [55] . The learning curve for the procedure is thought to be around 30 cases in terms of lymph node yield and PSM status [56] , although Guru has shown continued improvements in operative times and lymph node yields up to case 100 [57] ; as with RARP, improvements might be expected to continue as experience grows [55] .

Certainly as operative times for LRC and RRC continue to decrease, there appears to be renewed interest in intracorporeal reconstruction, with totally robotic procedures witnessing a resurgence [58] and [59]. Minimally invasive cystectomists should be aiming to improve on the current rates of reconstruction, with neobladder rates approaching the 30–40% seen in contemporary ORC series [60] rather than the 10% seen in many MIRC series. Initially, total operative times for intracorporeal reconstruction appeared excessive, but a recent nonrandomised comparison between extra- and intracorporeal reconstruction (n = 13) showed no difference in operative times within a single-institution series [61] , although early Clavien grade 3 complications remain an important issue [62] . Clearly, further randomised trials addressing this area are awaited from the major proponents of totally intracorporeal techniques. It should be appreciated that most papers on LRC and RRC involve the initial learning curves for the respective techniques, whereas the significant ORC series are almost exclusively from centres of excellence with long experience and large volumes.

4. Conclusions

It is generally believed that the quality of RC and thus oncologic outcomes depends primarily on several variables, such as surgeon experience and the ability to completely remove the tumour, with wide perivesical soft tissue and a thorough PLND. Whether minimally invasive approaches can achieve this across the broad range of patients with BCa currently seems unlikely, although the IRCC has shown that people with large experience and small numbers can achieve satisfactory results. Single-institution experiences from around the world have reported favourable short-term and intermediate [63] oncologic outcomes, but long-term data from larger cohorts are lacking, resulting in continued controversy over long-term oncologic results.

MIRC is certainly an attractive option, with a good morbidity profile for patients with muscle-invasive BCa, particularly those without bulky disease and significant comorbidity, and it is perhaps these patients who will ultimately best be served by such an approach that minimises the morbidity and convalescence associated with cystectomy. However, these more favourable patients are also most likely to do well with ORC, which highlights the need for a proper comparison in randomised trials.

It remains vital to firmly adhere to the fundamental principles of oncologic surgery, whatever the surgical approach: Do not transgress the tumour boundaries, ensure adequate margins during the resection, and perform a thorough PLND. It is likely that some patients are more suited for MIRC and others still require an open operation. We should await larger numbers as well as longer-term disease-specific survival and RFS data on patients with pT3 and pT4 disease before universally accepting MIRC as equivalent to ORC. Indeed, RARC outside of RCTs or in inexperienced centres may be unjustified until oncologic outcomes are better defined. To move forward scientifically, centres offering MIRC must use standardised data collection and rigorous complication classifications as well as a robust health economic evaluation to allow adequate and meaningful comparison with ORC.


Author contributions: Ben J. Challacombe had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Challacombe, Dasgupta.

Acquisition of data: Challacombe.

Analysis and interpretation of data: Challacombe.

Drafting of the manuscript: Challacombe, Dasgupta.

Critical revision of the manuscript for important intellectual content: Bochner, Gill, Guru, Herr, Mottrie, Pruthi, Palou Redorta, Wiklund.

Statistical analysis: Challacombe.

Obtaining funding: None.

Administrative, technical, or material support: None.

Supervision: Challacombe.

Other (specify): None.

Financial disclosures: I certify that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None. Prokar Dasgupta received financial support from the Department of Health via the National Institute for Health Research comprehensive Biomedical Research Centre award to Guy's & St Thomas’ NHS Foundation Trust in partnership with KCL and KCH NHS Foundation Trust. He also acknowledges the support of the MRC Centre for Transplantation.

Funding/Support and role of the sponsor: None.

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Footnotes

a The Urology Centre, Guy's and Thomas’ NHS Foundation Trust and KCL, London, United Kingdom

b Department of Urology, Memorial Sloan-Kettering Cancer Centre, New York, NY, USA

c Medical Research Council (MRC) Centre for Transplantation, KCL, King's Health Partners, Guy's Hospital, UK

d USC Institute of Urology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA

e Department of Urology, Roswell Park Cancer Institute, Buffalo, NY, USA

f Department of Urology, Onze Lieve Vrouw (O.L.V.) Clinic Aalst, Aalst, Belgium

g Division of Urologic Surgery, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

h Department of Urological Oncology, Fundació Puigvert, University Autónoma of Barcelona, Barcelona, Spain

i Department of Molecular Medicine and Surgery, Division of Urology, Karolinska Institute, Stockholm, Sweden

lowast Corresponding author. Urology Centre, 1st Floor Southwark Wing, Guy's Hospital, London, SE1 9RT, UK. Tel. +44 207 188 6797; Fax: +44 207 188 6797.