Abstract
Aim:
To report the outcomes of robot-assisted radical cystectomy (RARC) with bilateral extended pelvic lymph node dissection (BEPLND) and intracorporeal Studer pouch formation for bladder cancer.
Materials and Methods:
Overall 98 patients (92 males, 6 females) were included. Patient demographics, operative and postoperative variables, pathological parameters, complications, and functional outcomes were evaluated.
Results:
Mean age and American Society of Anesthesiologists score and body mass index were 60.9 years, 1.7 and 26 kg/m2, respectively. Neoadjuvant chemotherapy was given to 18 patients. Mean operation time, intraoperative estimated blood loss, and mean lymph node (LN) yield were 8.22 hours, 314.6 mL, and 28.3, respectively. Mean hospitalization time was 13.6 days. There were one perioperative and one postoperative deaths, both due to cardiac arrest on postoperative 21st and 60th days. Drains were removed at a mean of 10 days. Surgical margins were positive in two patients. Postoperative pathological stages were reported as pT0 (n = 21), pTis (n = 7), pT1 (n = 7), pT2a (n = 14), pT2b (n = 14), pT3a (n = 15), pT3b (n = 11), and pT4a (n = 9). Positive LNs were found in 21 patients. Prostate cancer was incidentally detected in 23 patients. Twenty-five patients received adjuvant chemotherapy. At a mean follow-up period of 25.1 months, 13 patients died from metastatic disease and 7 from cardiac disease. According to the modified Clavien–Dindo system, 30 minor and 20 major complications were identified in the perioperative (0–30 days) period, and 6 minor and 7 major complications were detected in the postoperative (31–90 days) period. According to the available data of the 60 patients, 37 were fully continent, 14 had mild, 6 had moderate, and 4 had severe daytime incontinence.
Conclusions:
Due to our experience, RARC with BEPLND and intracorporeal Studer pouch reconstruction procedures are complex procedures with acceptable morbidity, excellent surgical and pathological outcomes, and satisfactory oncologic and functional results.
Introduction
Open radical cystectomy (ORC) and urinary diversion is the gold standard surgical approach for some patients with muscle-invasive or high-grade, recurrent, noninvasive bladder cancer. 1,2 Since it was defined in 2003, robot-assisted laparoscopic radical cystectomy (RARC) and intracorporeal urinary diversion (ICUD) have been increasingly used worldwide, but the number of centers performing ICUD after RARC is still limited. 3
We have recently reported our experience and technique related to neurovascular bundle (NVB)—sparing RARC and ICUD, including 12 and 27 cases, 4,5 and also retrospectively compared the outcomes of ORC (n = 42) vs RARC (n = 32) with intracorporeal Studer pouch reconsturciton. 6
Herein, we reported the outcomes of our most recent experience, including 98 patients who underwent RARC and intracorporeal Studer pouch reconstruction for bladder cancer.
Materials and Methods
Between December 2009 and August 2018, RARC with bilateral extended pelvic lymph node dissection (BEPLND) and intracorporeal Studer pouch reconstruction procedures for bladder cancer were performed in two centers by three robotic surgeons (M.D.B., A.F.A., and A.E.C.) by using Da Vinci four-arms, si and xi surgical robots (Figs. 1 and 2). The present study protocol was reviewed and approved by the Institutional Review Board of Ankara Yıldırım Beyazit University, School of Medicine, Ankara Ataturk Training and Research Hospital. Anterior pelvic exenteration was also performed in female patients. Data were collected on patient demographics, operative parameters, pathologic parameters, complications, oncologic, and functional outcomes (urinary continence and erectile function). Overall survival (OS) was defined as time from date of cystectomy to death due to any cause.

Anastomosis to be made between chimney (arrowhead) of the Studer pouch and Wallace type uretero-ureteral anastomosis (arrow). Please note inserted ureteral stents.

Distended intracorporeal Studer pouch with water-tight appearance (arrows).
Cancer-specific survival (CSS) was defined as the time to death due to bladder cancer, whereas recurrence-free survival (RFS) was defined as time from date of cystectomy to local and or metastatic recurrence, based on histologic or radiologic evidence. Two-year OS, CSS, and RFS were calculated. Patient demographics and preoperative, operative, and postoperative parameters are summarized in Tables 1 and 2. Deviations from the expected postoperative course were regarded as complications. Complications that occurred during the 0–30-day period and within 31–90 days of surgery were graded according to the modified Clavien–Dindo system. 7,8 We previously described our surgical technique in details elsewhere. 4 –6
Demographics of Patients who Underwent Robot-Assisted Radical Cystectomy with Intracorporeal Studer Pouch Reconstruction for Bladder Cancer
BMI = body mass index; BCG = Bacillus Calmette-Guérin; TURBT = transurethral resection of bladder tumor; ASA = American Society of Anesthesiologists; TURP = transurethral resection of prostate; IIEF = International index of erectile function; SD = standard deviation.
Operative and Postoperative Parameters of Robot-Assisted Radical Cystectomy with Intracorporeal Studer Pouch Reconstruction for Bladder Cancer
NVB = neurovascular bundle; APA = accessory pudendal artery.
Postoperative functional evaluation
Daytime and nighttime urinary incontinence (UI) were evaluated and presented at latest follow-up for each patient. The daytime UI was measured as none (0–1 security pad/day), mild (1–2 pads/day), moderate (3 pads/day), and severe (>3 pads/day) as described by Lantz et al. 9 Nighttime UI was measured as good (dry with no protection), fair (dry with one awakening), and poor (wet, leakage, and UI during sleep) as described by Kulkarni et al. 10
Erectile function was assessed by using the International index of erectile function (IIEF) scores described by Rosen and colleagues 11 as: severe erectile dysfunction (ED) (IIEF score <7), moderate ED (IIEF score 7–12), mild-to-moderate ED (IIEF score 13–18), mild ED (IIEF score 19–24), and no ED (IIEF score >25). All patients with preoperative erectile function (IIEF score >7) were instructed to use oral phosphodiesterase type 5 (PDE-5) inhibitors after removal of the urethral catheter.
Statistical analysis
Data are descriptively reported using mean, median, and range. The 2-year OS, CSS, and RFS were assessed using the Kaplan–Meier estimator.
Results
Outcomes were evaluated and presented retrospectively. The mean operative time was 8.22 ± 1.7 hours (range, 4.3–12.5 hours) and mean estimated blood loss (EBL) was 314.6 ± 208 mL (range, 50–800 mL). Overall, 63 patients (64.2%) had organ-confined disease and 35 patients (35.7%) had local extravesical disease. Mean lymph node (LN) yield was 28.3 ± 11.6 (range, 7–63). Positive surgical margin (SM) was detected in two patients whose pathologic stages were pT3b and pT4a. Operative, postoperative, and pathological variables are shown in Tables 2 and 3. Mean follow-up was 25.1 ± 26 (range, 4–99) months. Distant metastatic disease was detected in 14 patients (14.2%) during follow-up. There was one perioperative death due to cardiovascular disease. Overall, 13 patients died from metastatic disease and 7 from cardiac disease. Adjuvant chemotherapy was offered to patients who had pT3b–4 and/or LN metastasis and 31 patients agreed to receive postoperative chemotherapy.
Postoperative Pathologic Evalutaion of Patients with Robot-Assisted Radical Cystectomy and Intracorporeal Studer Pouch Reconstruction for Bladder Cancer
Concomitant carcinoma in situ was present in two patients.
Concomitant carcinoma in situ was present in one patient.
Concomitant carcinoma in situ was present in four patients.
Concomitant carcinoma in situ was present in three patients.
Minor complications (grades 1 and 2) were detected in 30 patients and 6 patients during the 0–30-day period and 31–90-day period, respectively. Major complications (grades 3–5) were detected in 20 patients and 7 patients during the 0–30-day period and 31–90-day period, respectively. Complications according to the modified Clavien system are presented in Table 4.
0–30-Day and 31–90-Day Complications of Patients in Patients with Robot-Assisted Radical Cystectomy and Intracorporeal Studer Pouch Reconstruction for Bladder Cancer
Right external iliac vein injury occurred during extended pelvic lymph node dissection that was repaired primarily.
Two patients had pain at the camera port site above the umbilicus and physical examination revealed port site hernia. Both patients had hernia repair postoperatively between 0–30 days and 30–90 days.
Patients had postoperative prolonged urine drainage from the abdominal drains. Drainage resolved conservatively in one patient (0–30 days). Bilateral nephrostomy were applied in two patients and prolonged drainage ceased thereafter (0–30 days). One patient received antegrade JJ stent application (30–90 days).
Intestinal discharge was identified at the surgical wound on postoperative 28th day in one patient and surgical exploration demonstrated ileocutaneous fistula formation due to suture material during closure of the incision. Surgical repair was done and postoperative follow-up was uneventful.
During 0–30 days, bilateral grade IV hydronephrosis was developed due to stricture formation between Wallace type ureteral anastomosis and chimney of the Studer pouch in three patients and antegrade JJ stents were inserted by the radiology department. Between 30 and 90 days similar situation was identified in two more patients who were treated with antegrade JJ stent insertion by the radiology department.
Postoperative fever developed in one patient and abdominal imaging demonstrated intra-abdominal abscess formation that was successfully resolved and treated with intravenous antibiotics.
One patient had postoperative ileus that required ileostomy on the 28th day.
We reported this interesting complication previously as delayed massive hemorrhage due to external iliac artery pseudoaneurysm and ureteroiliac artery fistula following RARC and intracorporeal Studer pouch reconstruction with endovascular management.
Laparotomy performed due to intra-abdominal bleeding that did not resolve with blood transfusion. A mesenteric bleeder was identified and cautery application successfully controlled the bleeding area.
po = postoperative; RARC = robot-assisted radical cystectomy.
Functional outcomes, including urinary continence and erectile function are given in Tables 5 and 6.
Postoperative Urinary Continence Outcomes of Male and Female Patients Who Have Completed Postoperative >24 Months Follow-Up of Neurovascular Bundle Sparing Robot-Assisted Radical Cystectomy with Intracorporeal Studer Pouch Formation
Postoperative Erectile Function Outcomes of Patients with Mild or no Preoperative Erectile Dysfunction Who Have Completed Postoperative >24 Months Follow-Up of Neurovascular Bundle—Sparing Robot-Assisted Radical Cystectomy with Intracorporeal Studer Pouch Formation
FU = follow-up; PDE5-I = phosphodiesterase type 5 inhibitor.
Patients' demographic data, operative and postoperative parameters, pathologic parameters, complications according to the modified Clavien classification, urinary continence, and erectile function are presented in Tables 1–6. The number of patients who underwent bilateral, unilateral, and non-NVB-sparing surgery was 89 (90.8%), 4 (4%), and 5 (5.1%), respectively (Table 2). Details of the metastatic sites developed of the patients are presented in Table 7.
Metastatic Sites of the Patients Developed During Follow-Up
Overall, 13 patients developed metastasis.
Pt Nr = patient number; pTN = pathology; SM = surgical margin.
Two-year CSS was 80.6%, OS was 73.1%, and RFS was 78.9%. Median time to cancer-specific and noncancer-specific death was 10 (6–34) and 11 (5–30) months, respectively. Mean follow-up time was 25.1 months.
Overall, 20 patients died during follow-up. Of those, 13 died due to bladder cancer and 7 died due to cardiac disease. Of the remaining patients, three had local and distant metastasis. First patient had pT3bN0 urothelial carcinoma pathology with clear SMs who developed cranial metastasis on postoperative 14th month. This patient refused postoperative chemotherapy. Second patient had pT2bN0 urothelial carcinoma with plasmocytoid variant and with clear SMs who developed recurrence in the pelvis on postoperative 10th month and who received postoperative chemotherapy. Third patient had pT4aN0 urothelial carcinoma with clear SMs who developed local recurrence on rectum on postoperative 20th month and who received postoperative chemotherapy.
Discussion
Radical cystectomy for muscle-invasive bladder cancer is considered as the gold standard treatment method. Oncological and technical results have been shown equivalent to open surgery by the advancing robotic technology. 12,13 While RARC is associated with favorable perioperative results, including decreased blood loss, hospital stay, and enhanced recovery; especially the ICUD approach that has a prolonged operation time resulting from the formation of a continent reservoir and the lack of tactile feedback were reported as negative aspects. 14
Our study included 98 patientswho underwent RARC and BEPLND with intracorporeal Studer pouch formation. In the literature, there are limited number of studies on intracorporeal orthotopic urinary diversion after RARC. Intracorporeal ileal conduit and orthotopic urinary diversion are presented together in most of the studies. To the best of our knowledge, the largest series of robotic intracorporeal orthotopic urinary diversion by two centers (Southern California and Karolinska Institute, from Sweden and United States of America) was reported including 132 patients. 15 In this aspect, our series might be the second largest series including two centers from the same country with RARC and intracorporeal Studer pouch reconstruction.
SMs and the number of LNs are important variables related to the surgical oncological efficiency of radical cystectomy. Recommended ratios for oncological competence in ORC are <10% for positive SMs 16,17 and >15 for number of LNs. 18,19 Hellenthal and colleagues 12 (513 patients), Ng and colleagues 8 (83 patients), Pruthi et al. 20 (100 patients), and Khan and colleagues 21 (50 patients) reported the SM ratios in their RARC series as 6.8%, 7.2%, 0%, and 2%, respectively. SM rates in patients who underwent RARC were reported by Pasadena Consensus Panel, 22 International Robotic Cystectomy Consortium (IRCC), 14 Memorial Sloan Kettering Cancer Center, 13 and randomized prospective RAZOR 23 study as 7%, 7%, 3.3%, and 10.6%, respectively. In addition, EAU Robotic Urology Section reported the positive SM ratio as 4.8% in a multicenter study, including 717 patients. 24 In our series, the SM ratio was found to be 2% and was lower than the most of the previously reported series.
We performed BEPLND in our patients to remove the maximum number of LNs. In our current series we found the mean (standard deviation [SD], range) LN number as 28.3 (±11.5, 7–63). Pruthi and colleagues 20 (100 patients), Parekh 23 (151 patients), and IRCC 14 (1094 patients) reported the LN counts as 19, 23, and 18, respectively, in their RARC groups.
In our current series, the mean (SD, range) operation time was 8.22 (±1.7, 4.3–12.5) hours and the mean EBL was 314.6 ± 208 (50–800) mL. On the other hand, the mean (SD, range) blood loss was 300 (105–500) mL and the operation time was 357 (297–420) minutes in IRCC report, 14 with the shorter operation time probably due to the larger number of ileal conduits in ICUDs. In literature, RARC and ileal neobladder diversion series were reported by Desai and colleagues 15 and Schwentner et al. 25 with the mean operation time and EBL as 456 minutes and 430 mL in 132 patients, 477 minutes and 385 mL in 62 patients, respectively. Porreca and colleagues compared the patients who underwent intracorporeal Studer pouch and ileal loop after RARC, and the mean operation time and EBL were 412 ± 19.0 minutes and 425 ± 61.3 mL in the Studer pouch group. 26
In our current study, the mean operation time was slightly longer and EBL was consistent with the previously reported series in the literature. Additionally, in our previous study published in 2015, we reported the mean operation time and EBL as 9.76 hours and 412 mL in patients who underwent intracorporeal Studer pouch following RARC. 6 Our most recent series included patients operated by three surgeons therefore learning curve of three surgeons were included that might have had an impact particularly on the slightly longer operation time. In addition, initial cases underwent superextended pelvic LN dissection above the level of inferior mesenteric artery that might also have an impact on longer operation time. However, the considerable decrease of the mean operation time down to 6–6.5 hours particularly in the last eight patients might be due to increased experience.
RARC was suggested to be advantageous compared with ORC with having lower complication rates. Ng and colleagues prospectively compared the 104 ORC patients with 83 RARC patients in terms of complication rates and found significantly higher rates in ORC, and they reported RARC as an independent predictor of major and general complications at postoperative 30–90 days. 8 Schwentner et al. reported the early (<30 days) complication rates in their RARC and intracorporeal Studer pouch series, including 62 patients as 24.2% and 25.8% in terms of minor (Grade 1–2) and major (Grade 3–5) complications, respectively. 25 In our previous study published in 2015 that included 32 patients who underwent RARC and intracorporeal Studer pouch formation, our minor and major complication rates were 62.5% and 19% in early period, and 15.6% and 6.3% in late period, respectively. 6
Collins and colleagues reported their minor and major complication rates as 17% and 27% in early period, and 11% and 19% in late period, respectively, in their series incluing 80 patients. 27 In our present series, 65% of the patients had any complication according to the Clavien–Dindo system.We observed minor and major complication rates as 31.2% and 20.8% in early period, and 6.2% and 7.2% in late period, respectively. The detailed data are given in Table 4.
We recommend performing intracorporeal diversion after RARC for some reasons. First of all, the incision is quite smaller compared with the open diversion technique that might enhance wound healing and wound dehiscence. Another remarkable advantage might be minimal intestinal mobilization and retraction leading to less edema and decreased fluid loss through the intestinal wall.
In our current RARC and intracorporeal Studer pouch report, time to regular diet and duration of hospital stay were longer than previously reported series. This might be due to not applying enhanced recovery after surgery (ERAS) program in our initial cases. However, as our experience increased, we started to apply ERAS protocols routinely and the regular diet and hospitalization time periods have been decreased down to 3 and 6 days, respectively.
Continent diversion aims to maintain day and night continence and to ensure permanent discharge of neobladder. 28 Functional outcomes based on continence and sexual results are important for evaluating the success of RARC and intracorporeal neobladder. 29 NVB sparing radical cystectomy is recommended in invasive bladder cancer as it contributes positively to the functional results of the patients. 30 Pruthi et al. 20 and Khan and associates 21 used NVB sparing technique in patients without preoperative ED (IIEF score >7). In our current series, we performed NVB sparing surgery bilaterally in 89 patients and unilaterally in 4 patients irrespective of the preoperative erectile function status. NVBs were separated by blunt and sharp dissection. In our general practice, we spare NVBs in preoperative severe ED (IIEF <7) because we believe that NVB sparing improves the results in terms of not only the postoperative ED, but also the urinary continance.
There are limited data in the literature on functional results of the RARC series. Desai et al. reported 1-year continence rates (0–1 pad/day) as 90% for daytime and 75% for nighttime in their RARC and intracorporeal neobladder series. 15 In their series, continence data were available for 73 patients who had completed at least 6 months follow-up. Continence was achieved in 62 patients (0–1 pad per day), whereas 11 required 2 or more pads for persistent incontinence. 15 They reported their potency rates as 81% in 41 NVB sparing patients. 15 Schwentner and colleagues found the continence ratios as 88% for daytime and 58.1% for nighttime, and potency ratios as 54% in their neobladder series, including 62 patients. 25 In our series, we had continence data of 61 cases, and of those patients 37 (60.6%) were full continent (0–1 security pad/day), 14 (22.9%) had mild UI (1–2 pads/day), 6 (9.8%) had moderate UI (3 pads/day), and 4 (6.5%) had severe UI (>3 pads/day) during the daytime (in Table 5, day and night continence rates in men, women, and total are shown separately). In our study, daytime UI was measured as none (0–1 security pad/day), mild (1–2 pads/day), moderate (3 pads/day), and severe (>3 pads/day) as described by Lantz and colleagues. 9
In our study, full continent (0–1 security pad/day) included patients with no pad usage or one safety pad usage that was dry. However, Desai et al. 15 described continence as 0–1 pad/day and 2 or more pads was accepted as incontinence. If we define continence as 0–1 pad/day like Desai et al. 15 did, then our continence rate will be 73.7% (n = 45). During nighttime, 25 (40.9%) had full continence, 26 (42.6%) had moderate UI, and 10 (16.3%) had severe UI. In terms of the potency status, not all patients received postoperative penile rehabilitation and we started postoperative PDE-5 inhibitors in 4 of 8 patients with preoperative mild ED (IIEF score of 19–24) and the mean IIEF score at >24 months follow-up was 11.1 ± 4.6, 5 –20 and we also started PDE-5 inhibitor in 6 of 23 patients without preoperative ED and the mean IIEF score was 20.6 ± 7.4. 8 –25 Remaining patients did not want to use any medication. Most of the patients also complained of postoperative decreased libido. We believe that the prevalent use of PDE-5 inhibitors and regular follow-up of the patients may improve the functional results.
In conclusion, NVB sparing RARC with BEPLND and intracorporeal Studer pouch formation is a complex procedure with acceptable morbidity, excellent surgical and pathological outcomes, and satisfactory oncologic and functional results.
Footnotes
Author Disclosure Statement
No competing financial interests exist.
