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Robotic-assisted Laparoscopic Radical Cystectomy with Extracorporeal Urinary Diversion: Initial Experience
European Urology, 3, 54, pages 570 - 580
The use of robotic technology for laparoscopic prostatectomy is now well established. The same cannot yet be said of robotic-assisted laparoscopic radical cystectomy (RARC), which is performed in just a few centres worldwide.
We present our technique and experience of this procedure using the da Vinci surgical system.
Design, setting, and participants
From 2004 to 2007, 23 patients underwent RARC and urinary diversion at our institution.
We report the development of our technique for RARC, which involves posterior dissection, lateral pedicle control, anterior dissection, and lymphadenectomy prior to either ileal conduit urinary diversion or Studer pouch reconstruction performed extracorporeally.
Demographic and perioperative data were recorded prospectively. Oncologic and functional outcomes were assessed at 3- to 6-mo intervals.
Results and limitations
To date, 23 patients have undergone this procedure at our institution. Of those, 19 had ileal loop urinary diversion and 4 were suitable for Studer pouch reconstruction. Mean total operative time plus or minus (±) standard deviation (SD) was 397 ± 83.8 min. Mean blood loss ± SD was 278 ± 229 ml with one patient requiring a blood transfusion. Surgical margins were clear in all patients with a median ± SD of 16 ± 8.9 lymph nodes retrieved. The complication rate was 26%. At a mean follow-up ± SD of 17 ± 13 (range 4–40) mo, one patient had died of metastatic disease and one other is alive with metastases. The remaining 21 patients are alive without recurrence.
RARC remains a procedure in evolution in the small number of centres carrying out this type of surgery. Our initial experience confirms that it is feasible with acceptable morbidity and good short-term oncologic results.
Keywords: Bladder cancer, da Vinci, Laparoscopic, Radical cystectomy, Robotic, Technique, Urinary diversion.
Open radical cystectomy with pelvic lymph node dissection remains the gold standard for muscle-invasive or high-risk non-muscle-invasive bladder cancer in patients fit for surgery  and . Significant morbidity is associated with this procedure in 20% to 50% of patients  and , and hospital stay in the United Kingdom averages 18.7 d  .
Urologists are exploring minimally invasive options to reduce this morbidity. Laparoscopic radical cystectomy (LRC) has been reported in over 500 patients, and evidence suggests that the laparoscopic approach may allow less blood loss, decreased postoperative pain, and quicker recovery compared to open surgery  and . Despite these benefits, LRC has not yet enjoyed widespread popularity largely because of the technical difficulty involved and the lack of long-term oncologic outcomes.
The introduction of robotic assistance using the da Vinci® surgical system (Intuitive Surgical Inc., Mountain View, CA) offers technical advantages that may be of use during LRC  .
We installed a three-arm da Vinci surgical system in 2004 and established a programme to develop robotic-assisted laparoscopic radical cystectomy (RARC) at our hospital. A programme of LRC had already been established by two of the authors (PR and PD), who had completed 30 LRCs prior to our first RARC. The objectives of this study are to report our technique and initial experience of RARC for the management of muscle-invasive and high-risk non-muscle-invasive bladder cancer.
2. Patients and methods
2.1. Patient selection and preparation
Between June 2004 and October 2007, all patients with muscle-invasive or high-risk noninvasive bladder cancer and no evidence of locally advanced disease or metastases were considered for RARC. The selection process included preoperative investigations to ensure fitness for surgery as well as specific counselling regarding robotic technology in the context of bladder cancer and other urological procedures. Those who had undergone radiotherapy or had extensive previous abdominal surgery were not considered for RARC in this initial series. Potency was assessed using the sexual health inventory for men (SHIM) questionnaire, with potency defined as a SHIM score > 21. Options for urinary diversion were discussed and orthotopic neobladder offered to those deemed suitable.
A prospective database was maintained by a research team responsible for the evaluation of robotic technology at our hospital. Postoperatively, patients were reviewed by a urologist at 6 wk, 3 mo, and every 6 mo thereafter. Blood tests and clinical examination were performed at each visit, and a CT scan was performed at 6-mo intervals.
Mechanical bowel preparation (using an osmotic laxative) was reserved for those patients scheduled for Studer pouch urinary diversion. All patients received a phosphate enema 2 h prior to surgery. Intravenous antibiotics were administered at induction of general anaesthesia.
3. Technique of RARC
3.1. Patient positioning and port placement
A pneumatic leg compression system is used for prophylaxis of deep vein thrombosis. In men, a disposable sigmoidoscope is inserted in the rectum to aid in subsequent identification. In women, a methylene blue-soaked swab stick is placed in the vagina. The bladder is catheterised, and the patient's legs are secured in modified lithotomy position. All pressure points are carefully padded, and the patient is secured to the table using heavy elastic tape. The table is placed in 45° Trendelenburg position (see Fig. 1 ).
A six-port transperitoneal approach is used (see Fig. 2 ). The first 12-mm port is placed in the midline 2 cm above the umbilicus, and pneumoperitoneum is established at a pressure of 14 mm Hg. Subsequent ports are placed under vision. The 8-mm robotic ports are placed 10 cm from the midline camera port. Two 12-mm assistant ports are placed on the right side of the abdomen with a further 5-mm assistant port on the left side. The robot is then docked.
3.2. Posterior dissection
The ureters are mobilised and divided 1–2 cm from the bladder. The ends are clipped using Hem-o-lok clips (Weck Closure Systems, Research Triangle Park, NC), and the distal margin is sent for frozen section analysis. A transverse peritoneotomy is made in the Pouch of Douglas, and Denonvillier's fascia is incised in the midline (see Fig. 3 ). The plane between prostate (or vagina) and rectum is developed using blunt and sharp dissection.
In females, the posterior vaginal fornix is opened, revealing the methylene blue-soaked swab stick. The lateral vaginal walls are transected using a combination of monopolar cautery and ultrasonic energy with the ACE Harmonic scalpel (Ethicon Endosurgery, Livingston, UK). The vagina is then closed longitudinally by continuous intracorporeal suturing with 2-0 polyglactin on a CT-1 needle.
3.3. Lateral dissection
The bladder is mobilized laterally by entering the space of Retzius on both sides. Dissection is continued medial to the external iliac veins to preserve the obturator nerves and expose the lateral pelvic wall. The lateral pedicles to the bladder (and uterus in females) are thereby delineated. The ACE Harmonic scalpel is used by the right-side assistant to ligate the vascular pedicles to the bladder (see Fig. 4 ). The Harmonic scalpel is not used in patients undergoing a nerve-sparing procedure, who instead undergo ligation of the pedicles using Hem-o-lok clips or a linear stapler.
3.4. Anterior dissection
The bladder is filled with 200 ml of formol-saline and mobilised off the anterior abdominal wall by an inverted-U incision to include the urachus. The endopelvic fascia is opened and the dorsal vein ligated using a 1/0 polyglactin suture on a CT-1 needle. An athermal nerve-sparing technique is used in appropriate candidates to dissect the neurovascular bundle off the prostate. This procedure utilizes the Maryland forceps and scissors without diathermy and Hem-o-lok clips for the pedicles. The dorsal vein complex and urethra are divided. The bladder neck is sealed with a Hem-o-lok clip to prevent contamination. The distal urethral margin is sent for frozen section analysis. The cysto-prostatectomy specimen is secured in a 15-mm EndoCatch II bag (Tyco Healthcare, Hampshire, UK) for later retrieval.
3.5. Lymphadenectomy and transposition of left ureter
Standard lymphadenectomy is performed in all patients (see Fig. 5 )  . Our margins for lymphadenectomy are the genitofemoral nerve laterally, the bifurcation of the common iliac artery proximally, the obturator nerve inferiorly, and the node of Cloquet distally. The lymph node specimens are placed in separately marked EndoCatch bags. An Endoloop (Ethicon Endo-surgery, Livingston, UK) is applied on the distal end of the left ureter, which is then transposed under the sigmoid mesocolon by pulling the Endoloop through.
3.6. Urinary diversion
The incision for specimen removal depends on the type of urinary reconstruction planned. All diversions are performed extracorporeally using a Deaver retractor to aid exposure.
For ileal conduits, a 5- to 7-cm muscle-splitting incision in the right iliac fossa, incorporating a port site, allows for extraction of the specimens and extracorporeal fashioning of the urinary diversion. In obese patients (body mass index [BMI] > 30 kg/m2), a lower midline incision may be used for easier access to the left ureter. Uretero-ileal anastomosis using 4/0 monocryl is performed over 8Fr ureteric stents using a Wallace I or Bricker technique. The distal end of the conduit is fashioned as a stoma at a previously marked site on the abdominal wall.
Orthotopic neobladders are fashioned through a 5- to 7-cm lower midline incision as described by Studer  . The more posterior urethral sutures are placed laparoscopically prior to undocking the da Vinci. The remaining urethral and neobladder sutures are placed using an open surgery approach through the lower midline incision. The pouch is then “parachuted” down to the urethra over an 18Fr urethral catheter. Further management of urinary catheters is as described by Studer.
The port sites and wounds are closed with absorbable sutures (see Fig. 6 ).
3.7. Postoperative care
These patients are managed using the Enhanced Recovery After Surgery (ERAS) programme coordinated by our anaesthetic team  . Regional anaesthesia is used as appropriate, high inspired oxygen concentrations are used intraoperatively, and early postoperative feeding and mobilisation are encouraged. Typically, patients start oral fluids on day 1 postoperatively, with semisolids on day 2 and solids on day 3.
4.1. Perioperative parameters
RARC was scheduled in 25 patients, but at laparoscopy, two cases were noted to have advanced disease and were converted to open surgery prior to docking of the robot. Those cases are excluded from this analysis. Of the remaining 23 patients, there were 20 males and three females. The mean age plus or minus (±) standard deviation (SD) was 64.8 ± 9.4 yr. Five patients received neo-adjuvant chemotherapy.
Of the 23 patients, 19 had ileal conduit urinary diversions and four opted for Studer pouch reconstruction. There were no conversions to open surgery. A nerve-sparing technique was used in four previously potent patients (potency defined as SHIM score > 21), none of whom had prostate cancer on final histopathology.
Perioperative details are summarized in Table 1 . Mean total operative time ± SD for the entire series was 397 ± 83.8 min (see Fig. 7 ). This period was the time from first skin incision to closure of the final incision. The mean duration ± SD of laparoscopic surgery (ie, from first port insertion until undocking of robot) was 234 ± 48.2 min. The mean total operative time ± SD for the ileal loop and Studer pouch groups was 368 ± 59 min and 517 ± 66.5 min, respectively.
|n||23||20 male; 3 female|
|Mean age ± SD||64.8 ± 9.3 yr|
|Mean BMI ± SD||28.9 kg/m2 ± 3.5|
|Mean ASA score ± SD||2.2 ± 0.6|
|Urinary diversion type||Ileal conduit: 19||All diversions performed extracorporeally|
|Studer pouch: 4|
|Mean total operative time ± SD||397 ± 83.8 min|
|Ileal conduit group||368 ± 59 min|
|Studer pouch group||517 ± 66 min|
|Mean estimated blood loss ± SD||278 ± 229 ml||1 blood transfusion: 2 units (4.4%)|
|Mean hospital stay ± SD||11.6 ± 3.8 d|
|Complication rate||26%||No mortality|
SD = standard deviation; BMI = body mass index; ASA = American Society of Anesthesiologists.
Mean blood loss ± SD was 278 ± 229.4 ml with one patient requiring a blood transfusion for a port-site haemorrhage. Mean hospital stay ± SD was 11.6 ± 3.8 d.
4.2. Histopathologic results
The final histopathologic results are summarized in Table 2 . Twenty-two of 23 patients had transitional cell carcinoma (TCC), and one female patient had adenocarcinoma of the urethra. Surgical margins were clear in all patients with a median ± SD of 16 ± 8.9 lymph nodes retrieved. Lymph node metastases were detected in two patients. One patient had Gleason 3+3 prostate cancer incidentally noted. Three patients with metastatic lymph node involvement or vascular invasion were offered adjuvant chemotherapy.
|Positive surgical margins||0|
|Median lymph node retrieval ± SD||16 ± 8.9|
|Incidental prostate cancer||1|
The complication rate was 26%. Complications are summarized in Table 3 . They include a female patient with T3 urethral cancer who suffered a rectal injury requiring a colostomy. A 50-yr-old man with pT1 G3 TCC underwent a straightforward RARC and ileal conduit and was discharged on postoperative day 5; however, he was readmitted with abdominal discomfort and found to have a leak from the left mid ureter requiring a nephrostomy and a stent. We have not identified the cause of this complication though it may have been related to the ureteric catheter.
|5||Rectal injury (T3 urethral cancer)||Required colostomy|
|6||Port-site bleed||Required transfusion|
|10||Anastomotic stricture (Studer pouch)||Required dilatation|
|17||Left ureteric leak||Resolved with stent|
|19||Anastomotic leak—left ureter||Nephro-ureterectomy—no TCC|
|22||Bilateral femoral neuropraxia||Resolved spontaneously|
One of our Studer pouches developed an anastomotic stricture at 3 mo postoperatively and required dilatation. An obese patient with a BMI of 40 kg/m2 developed temporary bilateral femoral neuropraxia despite careful attention to the protection of pressure points during patient positioning. This problem resolved completely within a few weeks. One patient with an ileal conduit urinary diversion developed hydronephrosis and poor function in his left kidney secondary to an anastomotic stricture. He subsequently underwent nephro-ureterectomy. There was no evidence of malignancy in the ureteric stricture.
There have been no port-site metastases in the series.
4.4. Oncologic and functional follow-up
Thirteen of our patients have completed 12-mo follow-up, of which seven have completed 2-yr follow-up and three have completed 3-yr follow-up. At a mean follow-up ± SD of 17 ± 13 (range 4–40) mo, one patient has died of metastatic disease and one other is alive with lung metastases. The remaining 21 patients are alive with no evidence of disease. The disease-free survival rate at a mean follow-up of 17 mo is 91%.
Three of the four patients who underwent a nerve-sparing technique were potent (SHIM score > 21) with the assistance of tadalafil at 6-mo follow-up.
Apart from the anastomotic stricture detailed above, the Studer pouches have all worked well. All four patients are fully continent during the day. Three of the four patients are continent at night with one patient wearing a pad.
Minimally invasive approaches may reduce some of the morbidity associated with radical cystectomy though the key goal must be to at least replicate the oncologic outcomes of open surgery.
LRC is increasing in popularity, and despite some concerns  , early series demonstrate oncologic outcomes comparable to those of open surgery  and . Nonrandomised studies have compared laparoscopic to open radical cystectomy and suggest that the laparoscopic group may have fewer analgesia requirements and quicker return to bowel function  and ; however, operative times remain long and the complication rates remain similar  .
Menon et al first reported the feasibility of RARC using the da Vinci surgical system in 2003  . The operative times ranged from 260–308 min depending on whether an ileal conduit or orthotopic neobladder was formed. Blood loss was < 150 ml and surgical margins were clear in all cases.
Since then, a number of other small series have been reported (see Table 4 ). Rhee et al compared seven RARCs to 23 open radical cystectomies (ORC)  . They utilized a midline incision to extract the specimen and fashion the ileal conduit and also performed pelvic lymphadenectomy through this incision. The mean operative duration was 638 min and 507 min for RARC and open radical cystectomy, respectively, and hospital stay averaged 11 d and 13 d, respectively.
|Author [Ref]||n||Urinary diversion||Mean operative time (min)||Mean estimated blood loss (ml)||Complications|
|Menon ||17||Ileal conduit (3)||260||150||1 patient explored for postoperative bleeding|
|Rhee ||7||Ileal conduit||638||479||57% blood transfusion|
|Guru ||20||Ileal conduit (18)||442 (series)||555||Mortality 5%|
|Pruthi ||20||Ileal conduit (10)||366 (series)||313||10% reoperation rate|
|Wang ||33||Ileal conduit (17)||390 (series)||400||1 open conversion|
|Neobladder (12)||1 enterocutaneous fistula|
|Indiana pouch (3)|
|Current series||23||Ileal conduit (19)||368||278||23% complication rate|
|Studer pouch (4)||517|
All urinary diversions performed extracorporeally in these series.
Guru et al reported their experience with RARC and extracorporeal urinary diversion in 20 patients  . The mean total operative time for the series was 442 min, including 133 min for urinary diversion. There was one postoperative death of a patient who developed bowel obstruction and septic shock despite surgery to correct an internal hernia.
Pruthi and Wallen also reported a series of 20 patients who underwent RARC with extracorporeal urinary diversion  . Mean total operative time for this series was 366 min. The complication rate was 30%, which included one rectal injury (repaired intraoperatively), one postoperative haemorrhage requiring laparotomy, and one parastomal hernia requiring repair.
Wang et al compared their series of 33 RARC with 21 ORC  . Operative times were longer (390 min versus 300 min), but blood loss was less (400 ml versus 750 ml) and hospital stay was shorter (5 d versus 8 d) in the RARC group. Complication rates were similar.
Though RARC with completely intracorporeal urinary diversion has been reported  and , long operating times have prevented widespread adoption of this approach and most units prefer an extracorporeal approach for urinary diversion  and .
Our initial experience adds further support to the feasibility of RARC using the da Vinci surgical system. Our mean total operative time ± SD was 397 ± 83 min (see Fig. 7 ). There does not appear to be a reduction in operative times to date, which is partly explained by the introduction of two additional surgeons on the console after case 15. Though these times remain long, especially when an orthotopic neobladder is used for urinary diversion, there appear to be benefits for the patient with use of a minimally invasive approach. Mean estimated blood loss is acceptable at 278 ml with only one blood transfusion in our series (4.4%) for a patient who suffered a port-site bleed. The mean hospital stay in this group is 11.6 d. This statistic compares favourably with the mean hospital stay for open radical cystectomy in the United Kingdom, which is 18.7 d  . We agree with others that factors contributing to a shorter hospital stay include decreased analgesia requirements and quicker return of bowel function  and . We acknowledge that randomised studies are required to quantify the advantage, if any, conferred by minimally invasive approaches. Our complication rate is 26%, which serves to remind that radical cystectomy by whichever approach remains a formidable procedure.
The obvious goal of LRC and RARC must be to maintain the oncologic standards of ORC while reducing the associated morbidity. It is not clear whether pneumoperitoneum has an effect on TCC spread or recurrence in the medium to long term. It is interesting to note a report of port-site metastasis following RARC for a pT3b G3 TCC of the bladder  , though hopefully this outcome will be the very rare phenomenon it appears to be with other types of laparoscopic surgery  .
The technical advantages offered by robotic assistance are well documented and may have some specific advantages for LRC. Apart from superior visualization and articulated instrumentation, the improved ergonomic position offered at the robotic console benefits the surgeon during prolonged procedures  . A potential disadvantage of robotic assistance is the difficulty in performing a more cranial lymph node dissection, though the new da Vinci S system appears to offer better multiquadrant access.
Our early experience with RARC suggests that it is a safe procedure with acceptable morbidity and good oncologic results at 1 yr. Hospital stay and blood transfusion requirements are reduced when compared to historic series of ORC. Extracorporeal urinary diversion is straightforward to achieve through a right iliac fossa or lower midline incision. Randomised studies with long-term follow-up are required to compare RARC with LRC or ORC.
Author contributions: Declan G. Murphy 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: Declan Murphy, Prokar Dasgupta.
Acquisition of data: Ben Challacombe, Oussama Elhage, Declan Murphy.
Analysis and interpretation of data: Declan Murphy.
Drafting of the manuscript: Declan Murphy.
Critical revision of the manuscript for important intellectual content: Prokar Dasgupta, Peter Rimington, MS Khan, Tim O’Brien.
Statistical analysis: Declan Murphy.
Obtaining funding: None.
Administrative, technical, or material support: None.
Supervision: Prokar Dsagupta.
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.
Funding/Support and role of the sponsor: No companies had a role or input into the current study.
Acknowledgement statement: The robotics programme at Guy's Hospital is supported by the Guy's & St Thomas’ Charity and the British Urological Foundation. Declan Murphy is supported by the Ellison-Cliffe Fellowship of the Royal Society of Medicine, the Prostate UK Travelling Fellowship, and the Ethicon Fellowship of the Royal College of Surgeons, Ireland.
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a Department of Urology, Guy's & St Thomas’ NHS Foundation Trust, London, United Kingdom
b Department of Urology, Eastbourne General Hospital, Eastbourne, United Kingdom
© 2008 European Association of Urology, Published by Elsevier B.V.