Robot-Assisted Repair of Ureteroenteric Strictures After Cystectomy with Urinary Diversion: Technique Description and Outcomes from the European Robotic Urology Section Scientific Working Group

Abstract

Background:

Robot-assisted repair of benign ureteroenteric anastomotic strictures (UAS) provides an alternative to the open approach. We aimed to report short-, medium-, and long-term outcomes for robotic repair of benign UAS, and to provide a detailed video demonstration of critical operative techniques in performing this procedure robotically.

Materials and Methods:

Between January 2013 and September 2022, 31 patients from seven institutions who previously underwent radical cystectomy and subsequently developed UAS underwent robotic repair of UAS. Perioperative variables were prospectively collected, and postoperative outcomes were assessed. The surgery starts with a lysis of adhesions after previous surgery. Ureters are dissected, and the level of the stricture is identified. The ureter is then divided, and the stricture is resected. Finally, the ureter is spatulated and reimplanted with Nesbit technique after stenting with Double-J stents. In cases where both ureters show strictures, Wallace technique for reimplantation can be applied.

Results:

After robotic or open cystectomy, 31 patients had a total of 43 UAS at a median (interquartile range) follow-up of 21 (9–43) months. Median stricture length was 2.0 (1.0–3.25) cm, operative duration was 141 (121–232) minutes, estimated blood loss was 100 (50–150) mL, and length of hospital stay was 5 (3–9) days. One (3.2%) case was converted to open and one (3.2%) intraoperative complication occurred. Seven (22.6%) patients experienced postoperative complications, including four (12.9%) Clavien–Dindo grade 3 complications. No Clavien–Dindo grade 4 or 5 complications occurred. Stricture recurrence occurred in 2 (6.5%) patients.

Conclusions:

These results demonstrate that robotic repair of UAS is feasible and effective approach with outcomes in line with prior open series.

Patient Consent Statement:

Authors have received and archived patient consent for video recording and publication in advance of video recording of procedure.

Introduction

Radical cystectomy (RC) with urinary diversion is the standard treatment for patients with muscle invasive bladder cancer and an option for high-risk non-muscle-invasive bladder cancer.^1,2 The incidence of benign ureteroenteric anastomotic stricture (UAS) after urinary diversion is between 3% and 15%, although it has been reported to be as high as 19% 5 years postoperatively.^3

–9 This wide range may be attributable to heterogeneity in data capture, inconsistent postoperative imaging frequency, differences in stent usage and surgical technique, and variability in follow-up practices.^6,9 The specific etiology of benign UAS is not entirely clear, but the origin is likely fibrosis and scarring secondary to ischemia from poor distal ureteral neovascularization or urine leakage at the anastomosis.^3,10
–12

Consequences of benign UAS stem from obstruction. Patients may present with recurrent urinary tract infection, acute kidney injury, flank pain, or upper urinary tract stones requiring urgent treatment.¹³ Alternatively, many strictures are clinically silent and only are discovered incidentally when imaging obtained for other indications reveals hydronephrosis.¹³ Initial management of UAS often consists of decompression with retrograde stenting or percutaneous nephrostomy tube placement.

However, these approaches are short-term solutions that overwhelmingly require more permanent treatments in patients suitable for surgery.^13,14 Definitive treatment options for UAS include endoscopic management or surgical repair. Although surgery for UAS is the gold standard in achieving more durable results, endoscopic procedures such as balloon dilation provide an advantage in terms of lower blood loss, morbidity, cost, and shorter hospital length of stay (LOS).^15

–18

Classically, the standard surgical repair of UAS was an open ureteral reimplant. Although robotic ureteral reimplant was first described in 2012, there is scarce information on this procedure with mostly small single-center series and a few recently published multicenter series.^19

–23 In this study, we analyze a multi-institutional series of patients who underwent robotic repair of UAS, highlighting the operative technique for this approach.

Patients and Methods

Between January 2013 and September 2022, 31 patients who underwent robotic repair of a UAS from our multi-institutional collaborative cohort within the European Robotic Urology Section (ERUS) Working Group were included. This study was approved by the institutional review board of each center. All patients previously underwent either open or robotic RC and were found to have a stricture during follow-up. The institutions included in this study performed an average of 490 cystectomies for the 10-year study period.

Indications for surgery included infection or impaired kidney function. The surgeries were performed at seven institutions using the da Vinci system (Intuitive Surgical, Sunnyvale, CA). This study includes only high-volume robotic surgeons. During the study period, virtually all patients who underwent repair of UAS were treated through the robotic approach. The patients' demographics and perioperative results were prospectively collected at all institutions. Stricture length was measured by preoperative radiographic evaluation and intraoperative findings.

Preoperative preparation

Patients underwent imaging using CT scan or nephrostogram to locate, measure, and anatomically characterize the stricture. The urinary tract was decompressed with either stents or nephrostomy at the clinician's discretion. No preoperative bowel preparation was used at any center. Antibiotic prophylaxis was given according to the respective center's guidelines.

Surgical technique

Port placement

Patients are positioned in Trendelenburg position. The locations of the ports are shown in Figure 1. For a right-handed surgeon, right-sided ports may go medial or lateral to the stoma depending on the position of the stoma. If the stoma is medially positioned, it may be best to have the right-sided robotic ports lateral to the stoma, and if the stoma is more laterally positioned, it may be best to have the right-sided robotic ports medial to the stoma.

FIG. 1.

Port placement. Port placement for robotic reimplantation. Please note that the right-sided robotic port may be placed lateral (a) or medial (b) to the stoma based on patient anatomy. Color images are available online.

Lysis of adhesions

All procedural steps are shown in the accompanying video (Supplementary Fig. S1). Based on the degree of previous surgery, the extent of adhesions will vary. It is important to release all adhesions to allow robotic instruments to enter the abdomen without bowel injury. In addition, adhesiolysis will facilitate improved observation of the ureter and its insertion into the urinary diversion. In general, adhesions will be more extensive after open RC. Otherwise, no specific aspect of the procedure is necessarily more difficult after open RC compared with robotic.

Dissection of ureter and identification of stricture

Depending on the location of the stricture (typically distal ureter), the appropriate length of the distal ureter must be dissected. For short strictures, it is usually enough to dissect 3 to 4 cm, but this may be adjusted depending on stricture location. The corresponding ileal conduit (IC)/neobladder segments are mobilized and dissected at the ureteroenteric anastomosis, and the level of the stricture is identified.

A no-touch technique should be used by avoiding grasping the ureter to minimize tissue damage. Sharp dissection is necessary to mobilize the ureter from the surrounding vessels, minimizing devascularization. After the ureter is identified, the stricture is resected. In our series, indocyanine green (ICG) was used to identify the stricture location and to assess blood supply to the distal ureter in 6 (19%) patients. Preoperative retrograde stenting can also be utilized to identify the ureter.

Anastomosis

The distal end of the ureter is spatulated and reimplanted through the Nesbit technique after stenting (Fig. 2). A 6.0F by 24 cm closed Double-J ureteral stent was used in neobladders, and single-J ureteral stents were used in ICs. The ureter is sutured to the side of the conduit using 4.0 monofilament suture. Passing the ureter through the intestinal serosa may reduce the risk of stricture recurrence. The ureter is implanted at a different site of the conduit or chimney than the prior anastomosis.

FIG. 2.

Spatulation of distal end of ureter. After resection of the stricture, the next step is spatulation of the distal end of the ureter. Shown is the spatulation of the right ureter. Color images are available online.

The Nesbit technique, alternatively described as Bricker or direct anastomosis, was utilized most often (Fig. 3), and is the technique shown in our accompanying video (Supplementary Fig. S1). In cases where both ureters show strictures, Wallace technique for reimplantation can be applied (Fig. 3). In shorter ureters that do not allow for Wallace type 1, Wallace type 2 may be utilized (Fig. 3). Stents are then placed in the reimplanted ureter and the anastomosis is completed using 4.0 monofilament sutures. The conduit/neobladder is then filled with fluid to check for leakage.

FIG. 3.

Techniques used for ureteroenteric anastomosis. Shown are three techniques that can be utilized for ureteroenteric anastomosis. Wallace type 1 uses a side-to-side anastomosis of the medial walls, whereas Wallace type 2 uses a head-to-tail technique that can be used in case of shorter ureters. Nesbit is a direct end-to-side anastomosis. Color images are available online. Illustration by Jill Gregory. Used with Permission of @ Mount Sinai Health System.

Postoperative treatment and follow-up

Depending on the degree of adhesiolysis, the patient may spend from a few days to a week in the hospital. Stents should be removed after 3 weeks, and patency of the new anastomosis should be assessed by following the patient's serum creatinine and with a CT Urogram at 12 weeks after surgery. Any additional follow-up was done according to the patient's regular oncologic interval follow-up after cystectomy.

Results

Baseline characteristics of the cohort are shown in Table 1. Twenty-nine (93.5%) male and 2 (6.5%) female patients underwent robotic ureteral reimplant, and median age was 67 (60–71.5). Five (16.1%) patients had a history of abdominal radiation. Details on index cystectomy and anastomosis type are presented in Table 2. Twenty-three (74.2%) patients underwent urinary diversion utilizing the intracorporeal approach. Twelve (54.8%) had an IC urinary diversion. Nesbit (Fig. 3) anastomosis was used in 26 (83.9%) patients and Wallace (Fig. 3) anastomosis was used in 5 (16.1%) at the time of initial cystectomy.

Table 1.

Baseline Patient Characteristics

n	31
Sex, n (%)
Male	29 (93.5)
Female	2 (6.5)
Age, median (IQR)	67 (60–71.5)
BMI (kg/m²), median (IQR)	28 (23–31)
Previous abdominal radiation, n (%)	5 (16.1)
ASA score, n (%)
1	3 (10.2)
2	9 (29.0)
3	19 (61.2)
4–6	0 (0)
Charlson comorbidity index, median (IQR)	4 (3–5)
Baseline creatinine in mg/dL, median (IQR)	0.99 (0.88–1.15)
Intravesical chemotherapy (BCG or gemcitabine), n (%)	12 (38.7)
Neoadjuvant chemotherapy, n (%)	6 (19.4)
Pathologic stage at cystectomy, n (%)
pT0	6 (19.4)
pTa/PTis	7 (22.6)
pT1	3 (9.7)
pT2	8 (25.8)
pT3	3 (9.7)
pT4	4 (12.9)

ASA = American Society of Anesthesiology; BMI = body mass index; BCG = bacille Calmette-Guerin; IQR = interquartile range; pT = pathologic tumor stage.

Table 2.

Index Cystectomy Characteristics

n	31
Surgical approach
Robotic	23 (74.2)
Open	8 (25.8)
Diversion type, n (%)
lleal conduit	17 (54.8)
Neobladder	13 (41.9)
Indiana pouch	1 (3.2)
Anastomosis type
Nesbit	26 (83.9)
Wallace	5 (16.1)
Adjuvant chemotherapy, n (%)	4 (12.9)

After cystectomy, patients were followed for a median and interquartile range (IQR) of 40 (22.5–62.5) months and 3 patients (9.7%) experienced a postoperative urinary leak. Forty-three benign strictures were detected with a median (IQR) of 146 (96–319) days after cystectomy. Thirteen (42.9%), 6 (19.4%), and 12 (38.7%) patients had left-sided, right-sided, and bilateral strictures, respectively. Stricture characteristics are presented in Table 3. Before robotic ureteral reimplant, nine (29.0%) patients underwent endoscopic balloon dilation for attempted stricture management (Table 3).

Table 3.

Reimplantation Preoperative and Perioperative Characteristics

n	31
Months of follow-up postcystectomy, median (IQR)	40 (22.5–62.5)
Postcystectomy urinary leak, n (%)	3 (9.7)
Days to stricture detection, median (IQR)	146 (96–318.5)
Stricture laterality, n (%)
Left	13 (41.9)
Right	6 (19.4)
Bilateral	12 (38.7)
Total number of strictures, n	43
Stricture length (cm), median (IQR)	2 (1.0–3.25)
Preoperative creatinine in mg/dL, median (IQR)	1.27 (1.10–1.55)
Pre-reimplant retrograde stent placement	13 (41.9)
Pre-reimplant PCN	9 (29.0)
Pre-reimplant balloon dilation, n (%)	9 (29.0)
Days after index surgery to reimplant, median (IQR)	378 (226–514)
Reimplant type, n (%)
Wallace I	2 (6.5)
Wallace II	2 (6.5)
Nesbit	27 (87.0)
Indocyanine green use, n (%)	6 (19.4)
Operative time (minutes), median (IQR)	141 (121–232)
Estimated blood loss (mL), median (IQR)	100 (50–150)
Intraoperative complications, n (%)	1 (3.2)
Conversion to open, n (%)	1 (3.2)
Hospital length of stay (days), median (IQR)	5 (3–9)

PCN = percutaneous nephrostomy tube.

Perioperative information is presented in Table 3. During robotic ureteral reimplant, ICG was used in six (19.4%) patients. One (3.2%) patient experienced an injury to the iliac vein requiring vascular repair. One (3.2%) case was converted from robotic to open. No patient was found to have a malignant stricture.

Postoperative complication and recurrence information is presented in Table 4. All complications except for two (6.5%) stricture recurrences occurred in the first 30 days. Overall, 30-day complication rate was 22.6% and four (12.9%) patients experienced a Clavien grade 3 complication.²⁴ No patient experienced a postoperative urinary leak. Patients have been followed for a median of 21 (9–43) months post-reimplant surgery.

Table 4.

Postoperative Complications and Recurrence

n	31
Months of follow-up post-reimplant, median (IQR)	21 (9–43)
0–30 Day complications, n (%)	7 (22.6)
Clavien grade I	2 (6.5)
Clavien grade II	1 (3.2)
Clavien grade IIIa	1 (3.2)
Clavien grade IIIb	3 (9.7)
Clavien grade ≥IV	0 (0)
30–90 Day complications, n (%)	0 (0)
Stricture recurrence, n (%)	2 (6.5)
Days to stricture recurrence, n = 2	278, 574

Discussion

In this multicenter collaborative study of robotic ureteral reimplant after UAS, we report detailed surgical technique with video demonstration, perioperative outcomes, complication rates, and risk of stricture recurrence at a median follow-up of 21 months. The results suggest that the Nesbit technique is preferred for robotic ureteral reimplants after stricture even when prior anastomosis was done through the Wallace technique. The stricture recurrence rate was 6.5% and complication rates compared well with published series.

This study reports competitive perioperative outcomes compared with prior series (Table 5). Using robotic technique, median operative time was 141 minutes, estimated blood loss (EBL) was 100 mL, LOS was 5 days, with one (3.2%) intraoperative complication and one (3.2%) conversion to open. Packiam et al. published one of the largest open anastomotic stricture revision series of 124 patients, reporting a median operative time of 162 minutes, EBL of 187 mL, LOS of 6 days, and 17 (13.7%) intraoperative complications.²⁵

Table 5.

Studies on Robotic Ureteral Reimplant After Cystectomy

Study	Number of patients	Repair technique	90-Day complication rate, %	90-Day Clavien ≥3 complication rate, %	Anastomotic technique reported	Stricture recurrence rate, %
Present study	31	Robotic	22.6	12.4	Yes	6.5
Dangle and Abaza²¹	2	Robotic	0	0	No	0
Tobis et al.¹⁹	4	Robotic	0	0	No	0
Gin et al.²⁶	375	Open Robotic	41 0	2.7 0	No No	Unknown Unknown
Tuderti et al.³⁰	10	Robotic	30	10	No	10
Lee et al.²⁷	8	Robotic	62.5	25	Yes	20
Scherzer et al.²⁰	75	Open Robotic	14.20	14.2 0	No No	Unknown Unknown
Carrion et al.²³	61	Robotic	36.5	5	No	16
Ghodoussipour et al.²²	46	Robotic	15.3	8.7	No	8.6

In 2012, Dangle and Abaza et al. reported the first robotic ureteral reimplant series with operative times of 173 and 178 minutes, EBLs of 10 and 25 mL, and no complications in two patients.²¹ Afterward, Tobis et al. reporting a mean operative time of 30 minutes, EBL of 87 mL, and LOS of 5.75 days without any intraoperative complications or conversions to open in a four patient robotic series.¹⁹ Direct comparisons of open and robotic approaches are limited, but Gin et al. first included both robotic and open surgeries in their 42-patient series of 37 open and 5 robotic ureteral reimplants after stricture, reporting an overall operative time of 218.5 minutes, EBL of 75 mL, and LOS of 6 days.²⁶

For robotic revisions, the median operative time was 285 minutes, EBL was 50 mL, and LOS was 3 days. Scherzer et al. included five open and seven robotic UAS repairs in their study.²⁰ The open group had a higher median LOS (8 days vs 4 days) and complication rate (60% vs 0%) compared with the robotic group. Median EBL and operative time was comparable between groups. One (16.7%) robotic case was converted to open because of significant adhesions. Recently, Ghodoussipour et al. published a 46-patient series on robotic ureteral reimplant after stricture.²² Median operative time was 188 and 273 minutes for unilateral and bilateral repair, respectively.

Median LOS was 2 days and EBL was 50 mL, with three (6.5%) intraoperative complications, and the study did not report on conversions to open. Carrion et al. reported a median operative time of 195 minutes and LOS of 3 days with no intraoperative complications or conversions to open in their 61 patient robotic series.²³ Importantly, our median LOS of 5 days is longer than the LOS seen in these contemporary robotic series. The likely reason for this is that our study includes patients predominantly treated in European centers where patterns of discharge are often more conservative than those in the United States. Overall, in the context of prior open and robotic series, our study maintains competitive perioperative outcomes.

In this study, the Nesbit anastomosis is the preferred reimplant technique, with 27 (87.1%) cases utilizing the Nesbit technique for anastomosis. Since only one ureter is affected in most cases it is logical to utilize the Nesbit technique. This is true even when prior anastomosis was done through the Wallace technique. Unfortunately, few prior series discussing ureteral reimplant reported the type of reimplant technique used, which makes comparison with other trials difficult. Only Lee et al. included this information in their eight-patient series with use of Nesbit technique in 62.5% of cases.²⁷

In addition, consistent with prior analyses of ureteral reimplant for stricture, the majority of strictures were left sided.^22,25 The reason for this discrepancy is thought to be to due stretching of left ureter as it is brought under the sigmoid colon, as well as the necessity of keeping the left ureter longer to reach the level of the anastomosis, all of which lead to increased risk of ischemia in the distal ureter.¹⁰ In patients with bilateral strictures, it is possible to perform the Wallace technique. However, most patients will have relatively short ureters, and the Wallace type 2 anastomosis is preferable (Fig. 3).

This study also reports low postoperative complications and stricture recurrence rates compared with prior robotic series at a median of 21 months follow-up. Our study reports a 22.6% overall complication rate with four (12.9%) patients experiencing Clavien 3 complications, with no patient experiencing a Clavien ≥4 complication. In addition, the stricture recurrence rate was 6.5%. Packiam et al. reported an overall complication rate of 48.4%, high-grade complication rate of 12%, and stricture recurrence rate of 6.5% in their large open series.²⁵

Scherzer et al. reported one (14.2%) postoperative complication in their seven patient open group and zero postoperative complications in their five patient robotic group.²⁰ Gin et al. reported a 41% complication rate in their 37 patient open group and no complications in their 5 patient robotic group.²⁶ Carrion et al. reported a 36.5% complication rate and a stricture recurrence rate of 16% at 19-month median follow-up in their robotic series.²³ Ghodoussipour et al. reported a 15.3% overall complication rate and 8.7% Clavien ≥3 complication rate, as well as an 8.6% stricture recurrence rate at a median follow-up of 18 months in their robotic series.²²

They utilized ICG to identify stricture vascularity in 19 (41.3%) of their patients, with zero stricture recurrences in this subgroup. In our study, ICG fluorescent angiography was used in six (19.4%) patients to assess stricture vascularity, all of which have had no stricture recurrence at follow-up. ICG use to assess for distal ureteral vascularity has been suggested to reduce the risk of UAS after robotic RC.^22,27,28 Future studies should focus on the potential benefits of ICG for preventing stricture development and recurrence, but regardless, even without universal use of this tool, the present technique was effective in preventing stricture recurrences.

To our knowledge, this study is the largest series to date describing outcomes and technique with educational videos for a robotic ureteral reimplant after stricture. In addition, we have included detailed visual descriptions and video of the latest management approaches and surgical techniques from surgeons in the ERUS Scientific working group. The multi-institutional nature of our study design is a strength of our study.

However, this study was not without limitations. First, although data were prospectively collected, the retrospective nature of our analysis limits the conclusions we can draw. Second, our relatively small sample size compared with prior open series limit direct comparison, and future larger studies will allow for comparisons that may yield specific variables associated with success of this procedure. Furthermore, as complication rate often depends on surgeons' skill and experience, this study may underestimate complication rates by only including highly skilled and experienced surgeons, limiting the generalizability of this technique and results to all settings. Longer follow-up may be beneficial; however, most strictures will be detected within 2 years of index surgery.²⁹

Conclusions

We report detailed technique with educational video description, intraoperative outcomes, complications, and stricture recurrence rates in robot-assisted ureteral reimplant after index cystectomy. We also describe anastomotic technique preferences in an experienced cohort of robotic surgeons. Robotic ureteral reimplant appears effective and feasible with durable results based on this multi-institutional experience. This study can reassure surgeons that ureteral reimplant after stricture can be performed through a minimally invasive robotic approach.

Footnotes

Acknowledgment

The authors would like to thank the Menon Family Foundation for the support of the research of author J.M.R.

Authors' Contributions

Formal analysis, writing—original draft, review and editing, and video editing by J.M.R. Writing—review and editing, and video editing by N.T. Writing—review and editing, and methodology by R.G. Writing—review and editing by D.B. and A.H. Writing—review and editing, and data retrieval by R.A. Writing—review and editing, and resources by A.B., S.B., F.D'H., U.F., R.M., A.M., A.M., J.S., J.P., and C.W. Supervision, conceptualization, methodology, and writing—review and editing by P.W. Supervision, conceptualization, resources, and writing—review and editing by H.J.

Author Disclosure Statement

No competing financial interests exist regarding the material discussed in this article.

Funding Information

No funding was received for this article.

Supplementary Material

Supplementary Figure S1

Abbreviations Used

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