Long-term Outcomes of Robot-assisted Radical Cystectomy for Bladder Cancer

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1 EUROPEAN UROLOGY 64 (2013) available at journal homepage: Platinum Priority Bladder Cancer Editorial by Bernard H. Bochner on pp of this issue Long-term Outcomes of Robot-assisted Radical Cystectomy for Bladder Cancer Muhammad Shamim Khan a, Oussama Elhage a, Benjamin Challacombe a, Declan Murphy a, Bola Coker a, Peter Rimington b, Tithy O Brien a, Prokar Dasgupta c, * a The Urology Centre, Guy s & St Thomas NHS Foundation Trust, Great Maze Pond, London SE1 9RT, United Kingdom; b The Urology Department, Eastbourne District General Hospital, Kings Drive, East Sussex, BN21 2UD, United Kingdom; c Medical Research Council (MRC) Centre for Transplantation & National Institute for Health Research (NIHR) Comprehensive Biomedical Research Centre, King s College London, King s Health Partners, Guy s Hospital, London, SE1 9RT, United Kingdom Article info Article history: Accepted January 6, 2013 Published online ahead of print on January 11, 2013 Keywords: Bladder cancer Cystectomy Robotics Outcome measures Survival Abstract Background: Long-term oncologic and functional outcomes after robot-assisted radical cystectomy (RARC) for bladder cancer (BCa) are lacking. Objective: To report oncologic and functional outcomes in a cohort of patients who have completed a minimum of 5 yr and a maximum of 8 yr of follow-up after RARC and extracorporeal urinary diversion. Design, setting, and participants: In this paper, we report on the experience from one of the first European urology centres to introduce RARC. Only patients between 2004 and 2006 were included to ensure follow-up of 5 yr. We report on an analysis of oncologic outcomes in 14 patients (11 males and 3 females) with muscle-invasive/high-grade non muscle-invasive or bacillus Calmette-Guérin refractory carcinoma in situ who opted to have RARC. Intervention: RARC with pelvic lymphadenectomy was performed using the three-arm standard da Vinci Surgical System (Intuitive Surgical, CA, USA). Urinary diversion, either ileal conduit (n = 12) or orthotopic neobladder (n = 2), was constructed extracorporeally. Outcome measurements: Parameters were recorded in a prospectively maintained database including assessment of renal function, overall survival, disease-specific survival, development of metastases, and functional outcomes. Statistical analysis: Results were analysed using descriptive statistical analysis. Survival data were analysed and presented using the Kaplan-Meier survival curve. Results and limitations: Five of the 14 patients have died. Three patients died of metastatic disease, and two died of unrelated causes. Two other patients are alive with metastases, and another has developed primary lung cancer. Six patients are alive and disease-free. These results show overall survival of 64%, disease-specific survival of 75%, and disease-free survival of 50%. None of the patients had deterioration of renal function necessitating renal replacement therapy. Three of four previously potent patients having nerve-sparing RARC recovered erectile function. The study is limited by the relatively small number of highly selected patients undergoing RARC, which was a novel technique 8 yr ago. The standard da Vinci Surgical System made extended lymphadenectomy difficult. Conclusions: Within limitations, in our experience RARC achieved excellent control of local disease, but the outcomes in patients with metastatic disease seem to be equivalent to the outcomes of open radical cystectomy. # 2013 European Association of Urology. Published by Elsevier B.V. All rights reserved. * Corresponding author. MRC Centre for Transplantation, 5th Floor, Tower Wing, Guy s Hospital, Great Pond Maze, London, SE1 9RT, UK. Tel ; Fax: addresses: oussama.elhage@kcl.ac.uk (O. Elhage), prokarurol@gmail.com (P. Dasgupta) /$ see back matter # 2013 European Association of Urology. Published by Elsevier B.V. All rights reserved.

2 220 EUROPEAN UROLOGY 64 (2013) Introduction Since its initial description in 1949, open radical cystectomy (ORC) for bladder cancer (BCa) [1] has remained the mainstay of surgical treatment of muscle-invasive and high-risk non muscle-invasive BCa. In spite of a reduction in rtality, the complication rate of this procedure remains high even in the best centres in the world. In addition to the generally high corbidity in BCa patients, these complications are related to the longer incisions, higher blood and tissue fluid losses, and excessive bowel manipulation leading to prolonged ileus. The combination of these factors results in slower recovery and a longer hospital stay [2]. The high complication rate of ORC has been the main catalyst for embracing laparoscopy and robotics in the expectation that the advantages of these procedures may translate into decreased rbidity. The combination of pneuperitoneum and the smaller incisions required for surgical access results in lower blood and tissue fluid losses, reduced trauma to the abdominal musculature, and lower postoperative analgesic requirements [3]. These characteristics, in combination with minimal bowel manipulation, can facilitate earlier bowel function and quicker recovery. With the wider availability of robotic technology, many surgeons have preferentially adopted robot-assisted radical cystectomy (RARC) over laparoscopic radical cystectomy (LRC). Robotics offers the advantages of three-dimensional vision, enhanced magnification, higher degrees of freedom of vement, and superior ergonomics. However, any important scientific advance is initially accompanied by disinterest, then scepticism, and finally enthusiastic acceptance. RARC is going through a similar evolutionary cycle because of a paucity of randomised trials. The method has attracted scepticism for bias in patient selection, extent of lymphadenectomy, lack of long-term oncologic/functional outcomes, and cost effectiveness. At present there is a paucity of such data. We report longer-term oncologic and functional outcomes in a series of patients undergoing RARC and extracorporeal urinary diversion who have completed 5 yr of follow-up. robotic radical prostatectomy. However, the team had a laparoscopic surgeon who had performed >50 LRCs and an open surgeon who had performed >200 ORCs. Thus, this consecutive series of patients had surgery during the learning phase of the operating surgeon. Our surgical technique for RARC has previously been published [4]. Pelvic lymphadenectomy was performed with the limits of dissection being the genitoferal nerve laterally, the bifurcation of the comn iliac artery proximally, and the node of Cloquet distally. The lymph node packets were placed in separately marked laparoscopic sacks. Two patients did not undergo formal lymphadenectomy because they were deemed during their operations to be not medically fit to experience the additional anaesthetic time beyond that for radical cystectomy alone. Bilateral nerve sparing was performed in four male patients who had normal erectile function (potency defined as Sexual Health Inventory for Men [SHIM] >21) at presentation and desired preservation of sexual function. Other male patients had erectile dysfunction (SHIM <10) and hence did not undergo nerve sparing. Urinary diversion, either ileal conduit (n = 12) or orthotopic neobladder (n = 2), was performed extracorporeally. The nasogastric tube was reved the next rning and oral liquids started as tolerated. Early bilisation and chest physiotherapy were encouraged. Most patients were discharged with their pelvic drains and ureteric catheters in situ, which were reved at 2 3 wk. All specimens were examined by a team of uropathologists who reported on the local extent of the disease (T stage), margin status (urethral, ureteric, and perivesical), and number of lymph nodes reved and their status. Patients were followed up in a multidisciplinary BCa clinic at which assessment at each visit included physical examination, full blood count, and renal profile. Patients had computed tography scans of the chest, abdomen, and pelvis at 4 and then annually. Additional imaging was performed if clinically indicated. A prospective institutional review board approved database was maintained. 3. Results A total of 41 patients underwent radical cystectomy in our institution during the reported time frame, of whom 14 patients underwent RARC (Table 1). Of these patients, 5 (36%) have died; 3 patients died because of metastatic BCa, and 2 patients died of unrelated causes. The latter 2. Materials and methods All patients with proven BCa presenting to our unit between June 2004 and June 2006 who needed radical cystectomy and were considered suitable for RARC were offered a robot-assisted procedure with the extracorporeal urinary diversion of their choice. Selection was nonrandomised and subject to informed consent to undergo surgery using this newly introduced surgical technique. Exclusion criteria were radiologically or clinically advanced (pt4)/metastatic disease, history of multiple abdominal or pelvic operations, pelvic radiotherapy, severe cardiopulnary dysfunction, uncorrectable coagulopathy, or unwillingness to undergo RARC. The preference for a particular type of urinary diversion was not affected if patients opted to have RARC. Neoadjuvant chetherapy was offered to patients with proven muscle-invasive disease. Our criteria for offering adjuvant therapy are locally advanced disease (>pt3b), particularly with lymphovascular invasion or evidence of lymph node metastases on final histology. All procedures were performed by a single surgeon (P.G.), who had no previous experience with robotic cystectomy and had performed one Table 1 Degraphic and perioperative data Characteristic Outcome Comment Patients, no male, 3 female Age, yr, mean SD ASA 1, no 3 ASA 2, no. 9 ASA 3, no. 2 Urinary diversion type, no. Ileal conduit 12 Studer pouch 2 Operative time, min, mean SD Estimated blood loss, ml, mean SD Hospital stay, d, mean SD Transfusions, no. (%) 1 (7.1) 2 U Complication rate, % 28.6 Conversion to open None SD = standard deviation; ASA = American Society of Anesthesiologists score.

3 [(Fig._1)TD$FIG] EUROPEAN UROLOGY 64 (2013) Proportion Surviving Overall survival () Survival Function Censored Fig. 1 The Kaplan-Meier curve for overall survival of patients who had robotic cystectomy. Mean time of survival was (95% confidence interval, ). Data analysis was done using SPSS v.17. group included delayed bowel infarction (n = 1) and cancer of the pancreas (n = 1). Two patients are alive with metastatic BCa, and another patient has developed primary lung cancer. Six patients are alive with no evidence of either local recurrence or metastatic spread. The Kaplan-Meier curve shows the overall survival in the current series (Fig. 1). Four patients received neoadjuvant chetherapy consisting of three cycles of gemcitabine and cisplatin. Two patients received adjuvant chetherapy. One of these patients received six courses of cisplatin and gemcitabine after radical cystectomy for residual pt3b disease with lymphovascular invasion. The other patient received six courses of gemcitabine and carboplatin after developing lung metastasis. Of the 14 patients who underwent RARC, 4 patients had locally advanced disease on final histology. Three patients had pt3 transitional cell cancer, and 1 patient had a pt4 tuur (Table 2). Surgical margins were clear in all patients. None of the patients developed local or port-site recurrence during follow-up. Three patients who died of BCa had cystectomy for bacillus Calmette-Guérin resistant carcinoma in situ (CIS) or CIS with other-stage tuurs (G3pTa, G3pT3b), highlighting the high-risk nature of this disease entity. Two patients are alive with metastatic disease. In one patient, metastases developed in the liver 60 after surgery. This patient had G3pT2 with CIS. He received only two cycles of neoadjuvant chetherapy because of poor tolerability but subsequently had four cycles of adjuvant chetherapy, which he tolerated reasonably well. The other patient, who developed pulnary metastases after 29 of disease-free survival, had no residual tuur in the cystectomy specimen (T0). A third patient has no evidence of metastases from BCa at 77 but has been diagnosed with primary lung cancer. He remains alive 13 after the diagnosis of lung cancer, for which he received appropriate chetherapy. Six patients (43%) are alive and disease-free, with median disease-free survival of 84. Indications for RARC in this group included refractory CIS (n = 1), G3pT1 plus CIS (n = 1), G3pT2 plus CIS (n = 1), G3pT2 (n = 2), and G3pT4a (n = 1). Two of these patients received neoadjuvant chetherapy. The average number of nodes reved was 11 (range: 6 25) using the template described. An analysis of these results yields an overall survival of 64%, disease-specific survival of 75%, and disease-free survival of 50%. The complication rate in this cohort is 28.6% according to Clavien classification [5]. The details of complications in our Table 2 Results for patients undergoing robot-assisted radical cystectomy Age, yr (gender) Initial stage Final stage Lymph nodes, pos/all Follow-up, Recurrence, Disease-free, Death, Chetherapy Cause of death 73 (M) G3pT2 + CIS G3pTa + CIS 0/ Neoadjuvant Distant mets 77 (M) CIS CIS 0/ Distant mets 59 (M) G3pT1 + CIS G3pT3b + CIS Distant mets 71 (F) G3pT2 G3T3a 0/ Bowel infarction 62 (M) G2pT1 G2pT1 + CIS 0/ Pancreatic carcinoma 61 (M) G3pT2 + CIS G3pT1 + CIS 0/ (kidney UC pt3, liver mets) 61 (M) G3pT1 + CIS pt0 0/ (lung mets) 65 (M) CIS G3pT2a + CIS 0/ (primary lung carcinoma) 60 (F) pt3 urethral adenocarcinoma pt3b urethral adenocarcinoma Neoadjuvant and adjuvant Adjuvant 0/ (M) G3pT2 G3pT4a 0/ Neoadjuvant 59 (F) CIS CIS (M) G3pT1 + CIS G3T1 + CIS 0/ (M) G3pT2 + CIS G3pT2b + CIS 0/ Neoadjuvant 72 (M) G3pT2 G3pT2 0/ M = male; F = female; mets = metastasis; CIS = carcinoma in situ; UC = urothelial carcinoma; pos/all = positive/overall number, = nth.

4 222 EUROPEAN UROLOGY 64 (2013) robotic series have been published elsewhere [6]. One patient developed incisional and parastomal hernias requiring surgical repair. Another developed stricture of the anastosis between the neobladder and urethra, requiring a single urethral dilatation. Both patients who underwent orthotopic bladder substitution were fully continent day and night. The mean preoperative creatinine level was ml/l, and at long-term follow-up was ml/l. The difference was not statistically significant ( p = 0.1, student t test, 95% confidence interval). We did not routinely check renal function using other techniquesifthepatient screatinine levelremained stable and there were no changes in the dimension of renal ieties on follow-up scan. The length of hospital stay in our cohort is acceptable but slightly longer than in other series reported from North America. Length of hospital stay is influenced by many factors, including limited community support for stoma care in certain rural areas. Other factors include a cautious approach early in our series, patient tivation, and significant corbidities [7]. Three of the four patients with penile rehabilitation, which included oral tadalafil (5 mg once a day) after nervesparing RARC, recovered their erections (SHIM >20) after 6 of surgery, and they remain potent. 4. Discussion Radical cystectomy and an appropriate form of urinary diversion make up the standard treatment of muscleinvasive and high-risk non muscle-invasive BCa. There has been a surge of robot-assisted surgical procedures over the last decade. Although not regarded as a gold standard, robotic procedures are being increasingly used for prostate, kidney, and bladder surgery. Well re than 1000 RARCs have been reported by the International Robotic Cystectomy Consortium (pers. comm., K. Guru, New York, NY, USA, 2012) [8]. With increasing experience, many centres have adopted intracorporeal reconstruction after RARC [9]. Whether this transition will translate into additional benefits needs further investigation [10]. We embraced robotic technology in treating patients with BCa requiring radical cystectomy as an alternative to ORC, which is known to have high rbidity and significant rtality [11 13]. Being the first centre in the United Kingdom, we adopted a cautious approach in selecting patients for RARC. We offered RARC to patients with localised disease and satisfactory general health as assessed by American Society of Anesthesiologists grading to reduce the risk of complications and ensure patients safety. Lack of previous adequate robotic surgery experience may have contributed to the relatively longer operating time. However, our complication rate was acceptable [6], and immediate surgical and oncologic outcomes were on par with published outcomes [14 16]. This result helped us to sustain our programme, which has now matured and has enabled us to report on eagerly awaited longer-term oncologic outcomes. Pelvic lymphadenectomy is considered an integral part of radical cystectomy. There is ongoing debate about many aspects of lymphadenectomy, including the optimal level (standard compared with extended), the number of lymph nodes reved, the lymph node density, and whether it is simply the count or meticulous clearance of the zones that is important [17,18]. Nodal yield is not necessarily the marker of extent of lymphadenectomy but varies with lymph node package size, interest of the pathologist, and effort of the surgeon [19,20]. The number of nodes varies considerably even when the same template is used for lymphadenectomy [21]. RARC has been the focus of major scepticism because of a perception that adequate lymphadenectomy cannot be performed based on previouslyreported nodal yields. Patients in this series were operated on using the first-generation da Vinci Surgical System, which has a shorter instrument length and restricted manoeuvrability compared with the newer versions, which emulate all steps of ORC in RARC, including extended lymphadenectomy [22,23]. Whether relatively limited (standard compared with extended) lymphadenectomy had any influence on the oncologic outcomes is open to speculation. Limitations in studies caused by technological evolution will continue to pose challenges for future generations. Assessment of oncologic outcomes is confounded somewhat by the technological advances that occur at a faster pace than does accrual of the follow-up data. An analysis of our results yields overall survival of 64%, disease-specific survival of 75%, and disease-free survival of 50%. These figures are comparable to the outcomes from st open series [11,24,25]. In patients with BCa, there is a high prevalence of deaths from other competing causes, approaching 25% at 5 yr [26]. In this series, 2 of the 14 patients died of unrelated causes, while another patient has developed lung cancer. RARC appears to be effective in local disease control [27,28]. Metastasis is a function of the biology of the cancer, and this idea is reflected in this series. Some of the patients had advanced disease and yet are still alive, while others with less advanced disease have died of distant metastasis. Most patients after RARC have good functional outcomes and maintain their renal function, and some patients can recover their erections with nerve sparing, along with dedicated penile rehabilitation thereafter. It is unlikely that improvements in outcomes of invasive BCa treatment will occur merely from improvements in surgical techniques or technology. Such improvements will re likely result from better understanding of the disease, a rational approach to its detection and treatment, and multidal therapy in particular, re effective systemic treatment [29]. Several studies have been published comparing the cost of RARC with ORC. Most of these studies suggest higher costs for RARC because of increased material cost; however, when complications, length of stay, and operating time are taken into consideration, RARC appears to be re cost-effective [10,30,31]. In our centre it costs 2500 (s2990) extra to have RARC instead of ORC, but the shorter hospital stay and fewer complications offset st of this additional cost. 5. Conclusions Within the limitations of our study, RARC in our experience achieved excellent control of local disease, but the outcome

5 EUROPEAN UROLOGY 64 (2013) in metastatic disease seems to be equivalent to ORC [20 22]. Author contributions: Prokar Dasgupta 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: Khan, Dasgupta. Acquisition of data: Khan, Dasgupta, Rimington, O Brien. Analysis and interpretation of data: Khan, Elhage, Challacombe, Dasgupta. Drafting of the manuscript: Khan, Elhage, Challacombe. Critical revision of the manuscript for important intellectual content: Dasgupta. Statistical analysis: Coker, Dasgupta. Obtaining funding: Dasgupta. Administrative, technical, or material support: Rimington, O Brien. Supervision: Dasgupta. Other (specify): None. Financial disclosures: Prokar Dasgupta certifies 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 testiny, royalties, or patents filed, received, or pending), are the following: None. Funding/Support and role of the sponsor: Prokar Dasgupta acknowledges financial support from the Department of Health via the National Institute for Health Research (NIHR) Comprehensive Biomedical Research Centre at Guy s & St Thomas National Health Service (NHS) Foundation Trust in partnership with King s College London and King s College Hospital NHS Foundation Trust. He also acknowledges the support of the MRC Centre for Transplantation. This project was supported by grants from the Guy s and St Thomas Charity and The Urology Foundation. 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