Abstract
Objectives:
The aim of the present study was to compare the perioperative outcomes of extracorporeal (EXTRA) vs intracorporeal (INTRA) urinary diversion in patients undergoing robotic cystectomy and ileal conduit for neurogenic bladder.
Methods:
All consecutive patients who underwent robot-assisted cystectomy and ileal conduit for neurogenic bladder in six centers between 2011 and 2020 were included in a retrospective study. Four centers performed exclusively INTRA urinary diversion all over the study period, one center performed exclusively EXTRA urinary diversion, and the last center performed EXTRA urinary diversion during a first period and INTRA during the subsequent period.
Results:
Ninety-seven patients were included: 66 in the EXTRA group and 31 in the INTRA group. There were 11 major (Clavien grade ≥3) postoperative complications in the overall population (11.3%) with no statistically significant difference between both groups (EXTRA = 12.1% vs INTRA = 9.7%; p = 0.99). The mean length of stay did not differ significantly between INTRA and EXTRA (13.1 vs 14.1 days; p = 0.44). The mean times to oral feeding and to return of bowel function were similar in the two groups (3.9 vs 3.5 days; p = 0.28 and 4.1 vs 4.1 days; p = 0.51, respectively). There was no incisional hernia in the INTRA group vs five in the EXTRA group (0% vs 7.6%; p = 0.17).
Conclusion:
The perioperative morbidity of robotic cystectomy and ileal conduit for neurogenic bladder appears to be relatively limited compared with the historical open series. Possibly due to the relatively small sample size, no difference was found between INTRA and EXTRA urinary diversion in terms of perioperative outcomes.
Introduction
The two objectives of neurogenic bladder management are to prevent upper urinary tract deterioration and to improve patients' quality of life (QoL) by restoring or maintaining urinary continence. 1,2
The introduction of clean intermittent catheterization by Lapides in 19723 and the development of numerous conservative therapies over the past two decades (e.g., antimuscarinics, beta-3 agonists, intradetrusor botulinum toxin A) have revolutionized neurourology and have decreased tremendously the need for major surgical reconstruction of the lower urinary tract in neurourologic patients. 1,4 –6 However, incontinent urinary diversion remains necessary in some neurogenic bladder patients, especially those with detrusor sphincter dyssynergia or neurogenic detrusor acontractility unable to self-catheterize, those with a devastated outlet and/or an urethrocutaneous fistula, and those refractory to all other treatments. 1,6
Ileal conduit is an interesting alternative to suprapubic tube in this patient population, which has been reported to improve the patients' QoL 7 and avoids the need of foreign material and may therefore decrease the risk of urinary tract infections (UTIs) and urolithiasis. Concomitant cystectomy is often considered at the time of ileal conduit creation to avoid the relatively high risk of pyocystitis, pain, and cancer when the bladder is left in situ. 1,6 Owing to the significant perioperative morbidity of the open approach for cystectomy and ileal conduit in neurologic patients, with postoperative complications rate as high as 43%, 8 several teams started using minimally invasive approaches over the past decade. 9,10 However, only scant evidence is available on the outcomes of robotic cystectomy and ileal conduit. 6,10 Moreover, while the urologic oncology literature suggests that intracorporeal (INTRA) may decrease surgical morbidity compared with extracorporeal (EXTRA), 11 no such comparison exists in neurogenic bladder patients and INTRA ileal conduit has never been reported so far in this population.
The aim of the present study was to compare the perioperative outcomes of EXTRA vs INTRA cystectomy and ileal conduit in patients with neurogenic bladder.
Methods
Study design
After Institutional Review Board approval, all consecutive patients who underwent robot-assisted cystectomy and ileal conduit for neurogenic bladder at six academic departments of urology between 2011 and 2020 were included in a retrospective study. All patients were older than 18 years at the time of surgery. All patients who underwent cystectomy and ileal conduit for non-neurogenic benign condition such as bladder pain syndrome or radiation cystitis were excluded.
The indications for cystectomy and incontinent urinary diversion in neurologic patients were as follows: urinary retention with inability to self-catheterize vs urinary incontinence refractory to all other treatments vs urethrocutaneous fistula vs upper urinary tract deterioration. The indication of cystectomy and ileal conduit was discussed in a neurourology multidisciplinary team meeting for all patients. The neurologic conditions were categorized as follows: multiple sclerosis (MS), spina bifida, spinal cord injury, myelitis, and suprapontine disease. The study was approved by the local ethics committees and was conducted following the principles of the Helsinki Declaration.
Surgical techniques
The robotic approach was the only surgical approach used for cystectomy and ileal conduit in neurogenic bladder patients in three centers over the study period. In the three other centers, the purely laparoscopic approach was used as an alternative to the robotic approach in rare occasions when the surgical robot was not available due to being overwhelmed by urologic oncology procedures. Four centers performed exclusively INTRA urinary diversion all over the study period, one center performed exclusively EXTRA urinary diversion, and the last center performed EXTRA urinary diversion during the first period (2011–2018) and INTRA during the subsequent period (2019–2020).
Owing to the retrospective multicenter study design, the surgical techniques were not perfectly standardized. However, they followed broadly similar principles. The patient was placed in a deep Trendelenburg position (20°–30°) with spread legs. The procedure was performed using a transperitoneal approach. The procedure started by dissecting the left and right ureter after retracting the colon toward the midline. One of the main assets of the robotic approach lies in the ureterolysis as it allows careful and precise dissection aiming to preserve as much periureteral tissue as possible to optimize ureters' blood supply and minimize the risk of stricture. The ureters were dissected above the iliac bifurcation and down to the ureterovesical junction on both sides to allow adequate mobilization. The left ureter was crossed to the right side below the sigmoid mesentery.
Concomitant cystectomy was performed in all cases to minimize the risks of pyocystitis, pain, and bladder cancer. Genital sparing cystectomy was done in the vast majority of female patients. In male patients, the question of leaving the prostate in situ was discussed with all patients and decisional factors included patient's preference, age, and sexual function, existence of urethrocutaneous fistula or pressure ulcers, and suspicion of prostate cancer based on digital rectal examination and prostate specific antigen (PSA) assessment. Bladder was extracted using a retrieval bag. An ileal segment was identified 20 cm proximal to the ileocecal valve. At this step, the INTRA and EXTRA techniques differed.
In the EXTRA technique, the urinary diversion was done extracorporeally through a 5 cm incision extending from the supraumbilical camera port site. A 10 to 15 cm was harvested and the bowel continuity restored by manual anastomosis with two running sutures. The ureteroileal anastomosis was done over 6 to 10F ureteral stents using either the Wallace or the Bricker technique at the surgeon's discretion. The stents were then grasped to deliver the ileal conduit at the stoma site after a cruciate incision has been made in the rectus fascia and three Vicryl anchoring sutures have been taken in the fascia.
In the INTRA technique, the urinary diversion was done intracorporeally. The bowel segment was isolated using a 45-mm Endo-GIA stapler and the enteric anastomosis was done using a 60-mm Endo-GIA stapler (Covidien plc, Dublin, Ireland). The ureteroileal anastomosis was done over 6 to 10F ureteral stents using either the Wallace or the Bricker technique at the surgeon's discretion. Recently, most surgeons started using indocyanine green and Firefly™ to ensure that adequate blood supply to the ureter ends was present and ureters were cut more proximal when needed. The stents were then grasped to deliver the ileal conduit at the stoma site as done in the EXTRA technique.
Nine surgeons were involved in the present series, most of them having limited experience with both cystectomy and the robotic approach. The most experienced surgeon performed a large part of the EXTRA procedures. The surgeon's level of experience was categorized as moderate/high if the surgeon had performed at least 10 cystectomy and 10 robotic procedures before the case was included, and was otherwise categorized as low. We also created a time trend variable by splitting the cohort of each center into two equal consecutive halves categorizing it as “early years” for the first half and “late years” for the second half.
Outcomes
Complications occurring within the first 90 days postoperatively were graded according to the Clavien–Dindo classification 12 and were reported according to the European Association of Urology (EAU) guidelines. 13 Postoperative complications were categorized as minor (Clavien <3) and major complications (Clavien ≥3). The primary endpoint was the rate of major postoperative complications. The other outcomes of interest were operative time; estimated blood loss; perioperative blood transfusion; return of bowel function; time to oral feeding; length of hospital stay; and late (>90 days) postoperative complications including incisional hernias and ureteroenteric anastomotic stricture.
Statistical analyses
Means and standard deviations were reported for continuous variables and proportions for nominal variables. Comparisons between the INTRA and EXTRA groups were performed using the χ 2 test, Fisher exact test for discrete variables, and the Mann–Whitney test for continuous variables. Univariate logistic regression was used to assess the predictive factors of major postoperative complications. Statistical analyses were performed using JMP v.14.0 software (SAS Institute, Inc., Cary, NC). All tests were two-sided with a significance level at p < 0.05.
Results
Patients' characteristics
After exclusion of 10 patients who underwent robotic cystectomy and ileal conduit for other benign conditions, 97 patients were included in the present analysis: 66 in the EXTRA group and 31 in the INTRA group. The caseload per surgeon varied from 1 to 23 cases over the study period. The patients' characteristics are summarized in Table 1. The neurologic conditions were homogeneously distributed between both groups although the suprapontine disease tended to be more common in the INTRA group (25.8% vs 10.6%; p = 0.07).
Patients' Characteristics
For MS patients only.
For male patients only.
ASA = American Society of Anesthesiology; EDSS = Expanded Disability Status Scale; MS = multiple sclerosis.
They were more male patients in the EXTRA group, but this difference did not reach statistical significance (53% vs 35.5%; p = 0.11). The INTRA patients appeared to be more comorbid with tendencies toward a higher body mass index (27.3 vs 24.7; p = 0.07) and higher American Society of Anesthesiology (ASA) score (ASA score = 3: 90% vs 69.2%; p = 0.06) in the INTRA group. The Wallace ureteroileal anastomosis was more commonly used in the INTRA group (66.7% vs 45.5%; p = 0.05). The surgeon's level of experience was homogeneously distributed between the two groups (low experience: 45.2% vs 40.9%; p = 0.69). There were similar rates of “early years” procedures in the INTRA and EXTRA groups (58.1% vs 45.5%; p = 0.25).
Perioperative outcomes in the overall population
The perioperative outcomes observed in the overall population are shown in Table 2. There were 56 postoperative complications overall (57.7%) and 11 major postoperative complications (11.3%): 1 Clavien grade 3a (urinary fistula with CT-guided percutaneous drainage under local anesthesia), 9 Clavien grade 3b (6 urinary fistula with reoperation; 1 abdominal abscess with surgical drainage, and 2 obstructive pyelonephritis), and 1 Clavien grade 4 (urosepsis with septic shock and intensive care unit admission). After a mean follow-up of 7.1 months, there were five incisional hernias (5.1%) and eight ureteroileal anastomotic strictures (8.3%).
Comparison of Perioperative Outcomes
Comparison of perioperative outcomes
The perioperative outcomes in both groups are presented in Table 2. There was no statistically significant difference in terms of major postoperative complications between both groups (EXTRA = 12.1% vs INTRA = 9.7%; p = 0.99). The unadjusted relative risk of major postoperative complications for EXTRA vs INTRA was 1.25 (95% confidence interval: 0.19–3.15). The mean operative time was comparable between both groups (340.4 vs 351.1 minutes; p = 0.98), and the mean length of stay did not differ significantly between INTRA and EXTRA (13.1 vs 14.1 days; p = 0.44). The mean times to oral feeding and to return of bowel function were similar in the two groups (3.9 vs 3.5 days; p = 0.28 and 4.1 vs 4.1 days; p = 0.51, respectively).
There were 20 and 36 postoperative complications in the INTRA and EXTRA groups, respectively (64.5% vs 54.6%; p = 0.38). After a mean follow-up of 5 and 8.2 months (p = 0.73), the rates of ureteroileal anastomotic strictures were comparable in both groups (9.7% vs 7.6%; p = 0.71), but there was no incisional hernia in the INTRA group vs five in the EXTRA group (0% vs 7.6%; p = 0.17). The rates of ureteral stricture did not differ significantly between the Bricker and Wallace groups (6.5% vs 10%; p = 0.72). Overall, the rates of long-term complications were comparable in both groups (18.2% vs 19.4%; p = 0.89). In the subgroup of male patients, there was no statistically significant difference between the prostate-sparing and concomitant prostate excision groups in terms of perioperative outcomes (operative time; length of stay; rates of postoperative complications; major postoperative complication; or blood transfusion), except higher estimated blood loss in the prostate excision group (525.23 vs 236.36 mL; p = 0.02).
Predictors of major postoperative complications
The univariate assessment of major complication predictors is reported in Table 3. No statistically significant association was found between any of the patients' characteristics and the occurrence of a major postoperative complication. The only factor that approached statistical significance was MS (odds ratio = 3.21; p = 0.06).
Predictors of Major Postoperative Complications in Univariate Analysis
CI = confidence interval.
Discussion
The literature on cystectomy and ileal conduit for neurogenic bladder is scarce. 14 While the robotic approach has been widely adopted for cystectomy in general over the past decade, only one series has aimed to assess the value of the robotic approach for cystectomy and ileal conduit in neurogenic bladder. 10 To our knowledge, no study has ever reported the use of INTRA urinary diversion nor aimed to compare INTRA vs EXTRA urinary diversion in the neurogenic bladder population. In the present multicenter series, we found a relatively limited perioperative morbidity of robotic cystectomy and ileal conduit for neurogenic bladder with 11.3% of major postoperative complications compared with up to 54% in the urologic oncology literature. 15 No statistically significant difference was found for any perioperative outcomes between EXTRA and INTRA.
Intracorporeal urinary diversion may have several theoretical advantages over extracorporeal urinary diversion. 16 First, it avoids a supraumbilical incision that may result in wound complication and incisional hernia. Most importantly, it prevents to exteriorize temporarily to harvest the ileal conduit, which may favor prolonged ileus postoperatively. Bringing the ureter to the skin to make the ureteroenteric anastomosis for EXTRA urinary diversion may also be challenging, especially in obese patients, and traction on the ureter may affect its blood supply and favor ischemic ureteroenteric anastomotic stricture. Finally, because the skin incision is kept minimal for EXTRA urinary diversion, it is almost impossible to see how the conduit and ureteroenteric anastomosis will ultimately be positioned in the abdomen as the conduit is brought almost blindly from the median skin incision to the stomal orifice at the end of the procedure.
The existing literature on extracorporeal vs intracorporeal urinary diversion after cystectomy is entirely made up of a series, including bladder cancer patients undergoing radical cystectomy. 11,17 The present series is the first to address this issue in the neurogenic bladder population. Neurologic patients are extremely different from bladder cancer patients. They are typically much younger with less cardiovascular comorbidities, but with a weak abdominal wall due to their impaired innervation for those being paraplegic or quadriplegic. They also commonly have coexisting neurogenic bowel dysfunction. 18 Hence, they may represent the ideal target population susceptible to benefit from INTRA, which may minimize the risk of both incisional hernias and prolonged ileus. One of the main points of strength of the present study is that it focuses entirely on neurogenic bladder patients, excluding other benign conditions, to avoid diluting out the possible condition-specific benefits of the INTRA approach.
The present series is also the largest to report the outcomes of robotic cystectomy for neurogenic bladder in general (i.e., regardless of the approach for the urinary diversion). Several points deserve to be emphasized in that regard. The length of stay was longer in our series (13.8 days on average) than usually reported in an open series of cystectomy for neurogenic bladder and in a series of robotic radical cystectomy. 15,19, However, we believe this is more attributable to the specificity of the national health care system (national insurance covering all health care costs) than to the impact of the surgery itself. The mean operative time in our series was similar to the one reported in the robotic radical cystectomy series and, not surprisingly, longer than in most open series. 8,15,19 The estimated blood loss (308.6 mL on average) and the transfusion rate (18.6%) were broadly similar to the ones of robotic radical cystectomy series but lower than in open series. 8,15,19,20 Likewise, the rates of postoperative complications and major postoperative complications in our series (57.7% and 11.4% respectively) were slightly lower those reported in robotic radical cystectomy series. 8,15,19,20 There were seven urine leakages in our series (7.2%), which seems higher than in most series in the radical cystectomy literature. 21,22 We believe this may be due either to the learning curve or to the inflammatory nature of ureters often encountered in neurogenic patients, which may favor anastomotic leakage.
The role of ileal conduit in neurourology remains a matter of debate, some experts advocating to favor suprapubic tubes when incontinent urinary diversion is indicated because of the high risk of severe postoperative complications with ileal conduit in the frail neurologic population. 23 In the present series, we observed much lower rates of major postoperative complications and ureteroenteric anastomotic stricture than previously reported in open cohorts. 23 By decreasing the surgical morbidity, the robotic approach may encourage wider adoption of ileal conduit in neurologic patients unable to self-catheterize, with lower urinary tract dysfunction refractory to all other treatments, or those with devastated outlets. However, high level of evidence studies comparing ileal conduit with suprapubic tubes in these patients in terms of QoL, surgical morbidity, and long-term complications would be needed before ileal conduit could be unanimously recommended as the incontinent urinary diversion of choice in neurologic patients.
Although some elements meant to improve postoperative recovery were applied (e.g., early oral feeding, early mobilization, omission of drain placement), no real enhanced recovery after surgery (ERAS) protocols were used in the present series mostly due to the lack of any data and recommendations. Especially, no standardized analgesic and anesthetic regimens were used and nutritional optimization was rarely implemented. The role of ERAS care pathways in improving recovery after radical cystectomy has been largely demonstrated in the urologic oncology literature. 24 Optimization of recovery after abdominal surgery in neurologic patients remains an elusive question, but one may assume that the present study findings might have been influenced by the heterogeneous perioperative management and the lack of ERAS protocols.
The present article has several limitations that should be acknowledged. The main drawbacks are inherent to the retrospective and nonrandomized study design. Despite being restricted to neurogenic bladder patients, our study population remained extremely heterogeneous with various neurologic conditions, some differing between the two groups. This is a significant bias especially given the fact that statistical adjustment was not possible due to insufficient statistical power. However, none of the patients' characteristics, which differ between the two groups, was significantly associated with the primary endpoint.
The lack of standardization of the perioperative management may be a significant confounder that we could not adjust for and which may have influenced the perioperative outcomes. Another important shortcoming that is worth mentioning is the relatively small sample size that may have masked some differences between the two groups due to the inherent lack of statistical power (e.g., for incisional hernias). The median follow-up was short preventing to assess properly the late postoperative complication rate and especially the rate of ureteroileal anastomotic stricture, which is likely to increase with time.
The analysis was entirely focused on the perioperative morbidity, and the impact of urinary diversion on patients' QoL was not assessed, which could be regarded as an important limitation. However, one may postulate that the surgical approach for the urinary diversion (i.e., intracorporeal vs extracorporeal) was unlikely to have an impact on the postoperative QoL. The cost-effectiveness of robot-assisted radical cystectomy has been called into question. 25 No such data exist for robotic cystectomy for neurogenic bladder and it would have been interesting to explore the financial aspect of this procedure. Finally, as for any complex surgical procedures, we believe that surgical experience may have had a significant impact on the perioperative outcomes. However, it was extremely difficult to adjust the present analyses for that variable because surgeons involved in that series had extremely heterogeneous profiles and were at different steps in their learning curves.
What is even more challenging in our view is that three surgical learning curves have to be considered here: the one for robotic surgery in general, the one for cystectomy, and the one specifically for robotic cystectomy in neurogenic bladder patients. Only the latter can be clearly determined as all the cases included here represent each surgeon's learning curve for robotic cystectomy in neurogenic bladder patients (i.e., all the cases ever performed by each surgeon were included herein). The stage where each surgeon was in robotic surgery and cystectomy learning curves is much more challenging to establish. We strived to take the surgeon's factor in the best way we could by creating a binary surgeon's experience variable. However, we explored a possible time trend by dividing the early and late cases of each center.
Conclusion
The perioperative morbidity of robotic cystectomy and ileal conduit for neurogenic bladder appears to be relatively limited compared with the historical open series or the urologic oncology literature. Robot-assisted cystectomy for neurogenic bladder with INTRA urinary diversion may favor enhanced postoperative recovery and decrease the risk of incisional hernias compared with the EXTRA urinary diversion. However, due to the relatively small sample size in this series, the differences observed between INTRA and EXTRA did not reach statistical significance. Further studies are needed to evaluate the potential benefit of the INTRA urinary diversion in neurologic patients undergoing robotic cystectomy and ileal conduit.
Footnotes
Author Disclosure Statement
Gregory Verhoest and Franck Bruyere are proctors for Da Vinci. Other authors have nothing to disclose.
Funding Information
No funding was received for this study.
