Surgical outcomes and perioperative complications of robot-assisted radical cystectomy with intracorporeal ileal neobladder: a narrative review

Introduction

Background

Bladder cancer (BC) is associated with a high mortality rate, with 85% of untreated patients with muscle-invasive BC (MIBC) dying within 5 years of diagnosis (1). According to several guidelines, radical cystectomy (RC) combined with pelvic lymph node dissection (PLND) and neoadjuvant/adjuvant therapy is recommended as one of the current standards of care for patients with MIBC and selected cases of high-risk non-MIBC (2-4). Despite the inherent technical difficulties, minimally invasive surgery has been rapidly adopted in the last decade, particularly robot-assisted RC (RARC), which has become a widespread surgical procedure for MIBC (5,6). However, this highly complex surgical operation is associated with significant post-operative complications. In the RAZOR trial, RARC and PLND followed by urinary diversion (UD) were shown to have oncologic efficacy comparable to that of open RC (ORC) (7). Early-to-intermediate perioperative and oncologic outcomes of RARC with UD appear to be equivalent to those of ORC; however, its feasibility in early experience remains debatable (8-10).

Complete intracorporeal UD (ICUD) aims to maximize the advantages of UD as a minimally invasive procedure following RARC, including reduced blood loss, early correction of fluid imbalance, reduced pain, and early improvement of bowel function (11-13). A recently published multicenter randomized controlled trial comparing RARC with ICUD to ORC showed a statistically significant increase in postoperative 90-day survival and reduced hospital stay (14). Although external UD is performed using an ileal conduit and continent UD using a neobladder (NB), the introduction of ICUD into clinical practice has been slow owing to the complexity of its surgical technique (15). Previous studies have indicated that NB reconstruction with ICUD (IC-NB) is a complex surgical procedure characterized by longer operative times and higher complication rates compared to ileal conduits, which has hindered its widespread adoption (11,14,16). Specifically, it has been suggested that mastering the surgical techniques for IC-NB and achieving favorable outcomes may require surgeons to perform 25–250 cases (11,16,17).

Rationale and knowledge gap

One of the important advantages of bowel detubularization and refolding is that it interferes with peristalsis of the bowel wall to reduce nocturnal incontinence. These facts apply to open and intracorporeal techniques and have been very clearly detailed in previous studies (18,19). Despite its challenging nature and steep learning curve, IC-NB is preferred for its ability to minimize evaporative peritoneal water loss, limit ureteral dissection, and potentially reduce postoperative complications (20). Several surgical techniques for IC-NB have been reported over the past few decades, including the Pauda ileal NB (17), Vesica Patavina (Ves. Pa.) procedure which is a modification of the Padua ileal NB method (21), Shell NB reconstruction (22), Florence robotic IC-NB (FloRIN) (23), cross-folded U-configuration IC-NB (24), Pyramid NB (25), Karolinska technique (26), and Studer pouch (27); however, no studies have investigated the surgical outcomes and complications of these techniques.

Objective

This narrative review aimed to identify various studies in patients with BC who underwent RARC with ICUD, particularly those who underwent RARC with IC-NB, and to introduce the different methods of NB reconstruction, surgical outcomes, and perioperative complications in the current state of the art. We present this article in accordance with the Narrative Review reporting checklist (available at https://jovs.amegroups.com/article/view/10.21037/jovs-24-15/rc).

Methods

For this narrative review, the online databases PubMed and Scopus were used to search for relevant literature. The eligible references included peer-reviewed English-language articles published from August 2009 to May 2024 containing the following Medical Subject Heading terms: “radical cystectomy, robotic surgery, intracorporeal neobladder, outcome, and complications”. Meeting abstracts, case reports, studies with insufficient data, including those with ≤19 cases, and duplicate records were excluded. Two authors (T.E. and T.K.) independently screened the literature, extracted data, and assessed article quality. After comparing the results of the paper selection, if the results were inconsistent, the final decision on the acceptance of the paper was made through consultation between T.E. and T.K. A total of 130 references were found on the surgical procedures for IC-NB, surgical outcomes, and NB-related complications, of which 22 were selected for full-text availability in English. The search strategy summary can be seen in Table 1.

Surgical procedures for IC-NB, surgical outcomes, and NB-related perioperative complications

Surgical procedures

Table 2 summarizes seven primary methods used to create IC-NB based on the literature where ≥20 perioperative outcomes have been reported. With respect to the methods of making NBs described in the cited references, the list is as follows: Yuvaraja et al. (14), Lavallee et al. (26), Hosseini et al. (28), Sim et al. (29) and Collins et al. (30) with the Karolinska technique, Tuderti et al. (17,31), Mastroianni et al. (32), and Simone et al. (33) with the Padua technique, Dal Moro et al. (21) with the Ves. Pa. technique (modified Padua technique), Bianchi et al. (22) with the shell technique, Minervini et al. (23) with the FloRIN technique, Koie et al. (24) with the U-neobladder technique, and Tan et al. (25) with the pyramid technique. Translated with www.DeepL.com/Translator (free version). In all the procedures, an isolated ileum was created approximately 20 cm from the ileocecal valve. For urethral anastomosis, five IC-NB methods were performed using the Van Velthoven technique (17,21,23,25,26), while two methods involved looping the isolated ileum around the urethra (22,24). In terms of ureteral anastomosis, five IC-NB creation methods directly anastomose to the NB (17,21-24), whereas two use the Bricker or Wallace technique to anastomose to the afferent limb (25,26). We have detailed the main points of each IC-NB creation method.

The Padua NB creation and Ves. Pa. techniques require familiarity because of the relatively difficult placement of the ileum (17). The key point in creating a modified Padua NB [as presented in (17)] are as follows: (I) selection of approximately 42 cm of the free ileum; (II) detubularization of the right horn (8 cm) and incision of the left horn to insert the stapler; (III) configuration of the NB neck using the stapler; (IV) incision and detubularization of 25 cm of the proximal ileum; (V) creation of two segments of approximately 8–10 cm as the first folding of the proximal ileum; (VI) second folding to create the posterior wall; (VII) closing of the anterior wall of the NB and completion of the modified Padua NB. In the Ves. Pa. technique, which is another modification of the original Padua NB, a 40-cm isolated ileal loop and the urethra are initially anastomosed using the Van Velthoven technique, and a urethral catheter is then placed. The isolated ileal loop is detubularized along the antimesenteric border (21). The inner edges are then aligned at 40 and 20 cm, the first ileal folding is performed, and running sutures are placed. A second folding is subsequently performed, the inner margins are aligned at 30 and 0 cm, and running sutures are performed again. After direct anastomosis of the ureter to the NB, the anterior wall of the NB is continuously sutured to complete the procedure. As these two methods require a large number of ileal folds and may cause intraoperative disorientation, it is important to place the free ileum precisely using guide strings.

The Karolinska technique uses simple anastomosis of the bilateral ureters to a single chimney, although the folding of the ileum is more complicated (26). Initially, the left ureter is moved under the sigmoid mesentery toward the right in preparation for the ureteral anastomosis. Subsequently, the Denonvillier’s fascia, posterior urethral rhabdosphincter, and posterior aspect of the ileum are sutured to provide posterior reinforcement for the IC-NB. The planned urethral anastomosis site is incised and the urethra and isolated ileum are anastomosed with a running suture using the Van Velthoven technique. The isolated ileum for NB reconstruction is incised at the antimesenteric border, leaving 10 cm of the ileum on the proximal side for the chimney. Subsequently, the isolated ileum is folded to form a spherical NB. Anastomosis of the ureter and IC-NB is performed using the Wallace method on the chimney.

The other four IC-NB creation methods involve forming the posterior wall by suturing a series of detubularized isolated ileal plates. The Shell NB achieves an almost spherical shell-like shape by suturing the posterior wall, anterior wall with a 10-cm suture, and anterior plate (22). The FloRIN method is characterized by an L-shaped reconfiguration of the posterior wall of the NB (23). The anterior plate is closed with an inverted V-shaped suture to form a NB. In the Pyramid NB, no 10-cm incision is made at either end when detubularization of the isolated ileum is performed (25). The anterior plate is closed 10 cm cephalad to the urethroileal anastomosis. The folded segment is then closed using a running suture from the outside to the inside of the coronal plane (26). In the cross-folded U-shaped IC-NB, the ends of the detubularized ileum are sutured to create a U-shaped plate (25). After anastomosing the urethra and ureter to the NB, the U-shaped plate is folded and running sutures are placed outward from the center to create an anterior wall.

Surgical outcomes

The clinical outcomes of the enrolled patients are listed in Table 3. While the time required for IC-NB creation warrants discussion, few studies have detailed specific operative times for ICUD alone and the chronological changes in NB capacity and voiding status. Therefore, we examined the total operation time, estimated blood loss (EBL), length of hospital stay (LOS), blood transfusion, clean intermittent catheterization and the status of surgical margins of the resected specimen assess surgical quality. Several institutions have adopted the Karolinska technique for the surgical procedure of IC-NB.

The entire operative time was approximately 5–7 h, EBL was approximately 350 mL, transfusion rate was <5%, and LOS was approximately 1–2 weeks, indicating that the entire operative time and LOS are similar and EBL tended to be less compared to those of ORC (15,32). In the literature describing IC-NB-only operative times, Sim et al. (29) reported a mean of 178.4 min; Pellegrino et al. (35), a median of 166 min; Nakane et al. (36), a median of 182 min; and Koie et al. (24), a median of 156 min. The IC-NB procedure varies among institutions; however, approximately 3 h are expected to be required to create an IC-NB using any of these methods.

Changes in IC-NB volume and urinary function over time have been extensively reported in detail by Koie et al. (24). Comparing 6 and 12 months postoperatively, the median NB capacity increased from 276 to 285 mL, median NB pressure remained almost unchanged at 19.0 and 26.5 cmH₂O, and median residual urine volume was stable at 40 and 29 mL, respectively (24). The maximum urine flow rate was 12.7 mL/s 3 months postoperatively and remained essentially unchanged thereafter, indicating a good outcome (24). Yuvaraja et al. (14) reported a mean NB capacity of 550 mL, storage NB pressure of 32 cmH₂O, and mean residual urine volume of 115 mL in six patients whose urinary function was studied in a urodynamic study. It was suggested that the use of the ileum in IC-NB could maintain sufficient NB capacity and low pressure in the NB.

The recovery rates of postoperative urinary continence are presented in Table 4. During the daytime, the proportion of patients who used one or fewer pads was approximately ≥75%, indicating a relatively good recovery, whereas during the nighttime, the proportion was only 60–70% (22,23,25,27). Additionally, considering the fact that a small number of patients require clean intermittent catheterization, as presented in Table 3, it may be necessary to cooperate with nurses not only in the creation methods of IC-NB but also in postoperative urinary voiding education.

Although epidemiologic and genetic studies have shown that many factors are associated with the development of BC and that sex differences are recognized, evidence-based recommendations for the sex-specific management of BC are lacking (37). Female patients who undergo RC have significantly longer LOS and operative time, significantly more blood loss, as well as higher 90-day mortality and perioperative complication rates (37). The maximum postoperative change in serum creatinine in the acute phase after RC tended to be greater in men (14.0%) than in women (9.7%); however, the difference was not significant (P=0.141) (38). In addition, acute kidney injury developed in 10.2% of male patients, whereas there was no incidence in female patients (P=0.016) (38). The literature reviewed for this study did not identify any data on surgical outcomes, perioperative complications, or oncological outcomes according to gender. However, the daytime incontinence rate at 1 year postoperatively was reported to be 84.4% for male patients and 46.1% for female and nighttime incontinence rate was 62.5% for male and 38.5% for female in the study regarding postoperative urinary incontinence (33). Among patients who underwent NB, female patients had significantly worse daytime urinary incontinence rates than male patients (31). Therefore, NB may be chosen less frequently as a UD for female patients with BC than for male patients (37).

Based on the systematic review and meta-analysis performed by Cella and colleagues (39), the median follow-up period in this review was 27.5–86.6 months (28,29,31,34,40,41). The 3-year cancer-specific survival (CSS) and overall survival (OS) rates were 73.9–80.2% and 68.4–74%, respectively (29,34,41,42), and 5-year CSS and OS rates were 65.4–72.0% and 61.5–71.0%, respectively (28,31,40). Postoperative local recurrence was found in 1.4–6.9% and distant metastasis in 13.0–21.9% of cases (28,29,34). Tuderti et al. (31) reported that pT stage ≥3 and pathologic lymph node metastasis were independent negative predictors for CSS, OS, and disease-free survival. With regard to oncological outcomes, all NB methods were comparable, and no statistically significant differences were found when compared to ORC.

The European Organization for Research and Treatment of Cancer (EORTC) Quality of Life Questionnaire Core 30 (EORCT QLQ-C30) was used as a measure of postoperative quality of life (QOL) (15,16). This questionnaire is a tool that scores each domain on a scale from 0 to 100, with the higher the score indicating a better QOL. The EORTC QOL-C30 was used to assess the QOL of patients who underwent RARC, and the overall mean QOL scores were 78–87.6 preoperatively, 77–86.1 at 3 months and 76–87.1 at 6 months postoperatively (15,16). In general, postoperative recovery of bowel function is assessed by time to oral intake, flatus, and defecation. Postoperatively, the median time to oral intake was 2–4 days, median time to normal food intake was 3–5 days, median time to flatus was 2–3 days, and median time to defecation was 4–6 days (14,21,25,32,33). Although the EORTC QLQ-C30 scores for constipation and diarrhea worsened at 3 months postoperatively, they recovered to preoperative levels at 6 months postoperatively. This suggests that it may take time for bowel function to recover to the same level as prior to surgery even though it tends to recover in the early postoperative period.

IC-NB related postoperative complications

Readmission rates within 30 and 90 days of hospital discharge ranged from 11–22.5% and 27–46.5%, respectively (15,32). The incidence of postoperative complications classified as Clavien-Dindo grade ≥ III ranged from 5.1–27.4% and 10.1–40% within 30 and 90 days, respectively (11,15,28,29,32,33). In a report by the Robotic Urology Section Scientific Working Group of the European Association of Urology, one patient died within 1 month postoperatively due to sepsis, two had thromboembolic events, and one died of sepsis between 2 and 3 months postoperatively (35). Overall, 514 patients (60%) developed at least one complication within 3 months, of which 223 (26%) experienced at least one serious complication (35). Urinary tract infection (UTI) was the most common complication, occurring in 20% of the early and 10% of the late phases (35). Although UTI occurred most frequently, it was not severe in most cases (35). The next most common early complications were paralytic ileus (10%) and anastomotic leak (9%), while the late complications included ureteral stricture (3%) and anastomotic leak (2%) (35). This information is useful for the postoperative management of patients undergoing IC-NB and suggests that careful follow-up should continue after surgery (35).

Learning curve

Although favorable perioperative outcomes have been demonstrated for IC-NB, several urologists still consider it a challenging procedure, necessitating the transfer of technical skills to the next generation. Here, we discuss some studies that reports on the learning curve of IC-NB.

The learning curve was evaluated using the following five criteria, defined as “RC-pentafecta”: (I) operative time of <5 h; (II) 24-h hemoglobin (Hb) drop <2 g/dL; (III) severe complications according to the Clavien-Dindo classification of <30%; (IV) positive surgical margin (PSM) rates of <5%; and (V) lymph node dissection defined as >16 nodes (16). In RARC, a minimum of 20 cases was required, with at least three consecutive cases achieving a surgical time of <300 min (16). The Hb level decline, PSM rate, and number of lymph nodes removed showed almost no change as the number of experienced cases increased; thus, no learning curve was determined for these items (16). A quartile analysis of the five outcomes benchmarked by the Pasadena Consensus concluded that 60 cases of experience were needed to reach a plateau in RARC with IC-NB outcomes (16). A report from Karolinska University compared the surgical outcomes of two surgeons who operated on 47 and 20 patients, respectively (30). The overall operative time was significantly shortened from a median of 565 min in the first 10 cases to a median of 345 min in the last group (P<0.001) (30). Although the overall complications decreased with an advancing learning curve from 70% in the first group to 30% in the latter group (P<0.05), major complications were not statistically different (30). The mean EBL, pathological stage, mean number of lymph nodes removed, and number of positive margins did not change across all cases (30). The study concluded that an experienced robotics team and mentors significantly influence the learning curve of new surgeons, resulting in shorter operative times and lower complication rates from the beginning of the procedure (30). Noh et al. (11) compared the surgical outcomes in 203 patients who underwent IC-NB in groups of 10 patients according to the order of surgery, for a total of 20 groups. The mean console time ± standard deviation was 362.59±82.62 min, and the operating time for RARC with IC-NB improved continuously up to 80 cases and then stabilized (11). The achievement rate of RC-pentafecta in the third group (31st to 40th patients) was not significantly different from that in all patient groups (40.0% vs. 53.7%, P=0.369), and the treatment outcomes reached a plateau thereafter (11).

When performing RARC with IC-NB, we suggest that the surgical skills of surgeons, anesthesiologists, operating room nurses, clinical engineering technicians, and other surgical staff, as well as the proficiency of the institution, may help stabilize surgical outcomes (36).

Strengths and limitations

This narrative review has several limitations. First, this document is a narrative review. Therefore, the consistency of the results and the quality of the evidence cannot be guaranteed because no meta-analysis or other statistical analysis has been performed. Second, this narrative review did not conduct a literature search based on the Preferred Reporting Items for Systematic review and Meta-Analysis methodology, nor did it strictly screen the extracted articles. Furthermore, data extraction and integration, subgroup analysis, and sensitivity analysis were not performed on the selected papers. Third, this review did not examine preoperative variables or tumor characteristics and the differences in surgeons’ and institutional experience with IC-NB in patients who underwent RARC with IC-NB. Finally, it is difficult to conclude which surgical method is appropriate for patients undergoing IC-NB because of potential bias due to the different methods used to create IC-NB at different institutions.

Conclusions

This narrative review presents various IC-NB techniques, surgical outcomes, NB-related complications, and learning curves. Because of the relatively high technical difficulty of robotic IC-NB, both the surgeon’s skill and institution’s proficiency in robotic surgery are crucial. However, regardless of the chosen IC-NB surgical technique, surgical outcomes were stable after a certain number of surgeries. This review highlights that mastering IC-NB can be expedited with guidance from experienced instructors. We hope that this narrative review will be helpful in introducing IC-NB in patients with BC.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://jovs.amegroups.com/article/view/10.21037/jovs-24-15/rc

Peer Review File: Available at https://jovs.amegroups.com/article/view/10.21037/jovs-24-15/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jovs.amegroups.com/article/view/10.21037/jovs-24-15/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

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