Abstract
Purpose:
Although robot-assisted laparoscopic ureter reimplantation (RALUR) is a recognized alternative to open and laparoscopic ureter reimplantation in treating distal ureteral obstruction, there are limited data on long-term efficacy and safety outcomes of non-antireflux RALUR. We assessed patients undergoing RALUR, evaluating operative, functional, and safety determinants.
Materials and Methods:
All consecutive patients undergoing non-antireflux RALUR between April 2015 and January 2020 were included in this retrospective cohort study. The primary outcome endpoint was recurrent distal ureteral obstruction.
Results:
Mean follow-up was 41.3 months (95% confidence interval, 33.3–49.2; range 2–82). Among the 26 included patients, none developed recurrent distal ureteral obstruction. Kidney function in terms of serum creatinine level (72.0 μmol/L vs 71.0 μmol/L, p = 0.988) and glomerular filtration rate (92.0 mL/min vs 91.0 mL/min, p = 0.831) was stable between the preoperative period and the last follow-up. Renal pelvis dilatation decreased significantly postoperatively, from grade 2 to grade 0 (p < 0.001). Most patients (73.1%) remained free from any clinical symptoms of reflux during the follow-up. No recurring urinary tract infections were reported. The rate of postoperative complications (Clavien–Dindo grade ≥II) was 23.1%. All complications resolved without sequelae.
Conclusions:
Non-antireflux RALUR appears to be safe and effective in the management of distal ureteral obstruction. There was no recurrent ureteral obstruction after RALUR in our cohort during a mean follow-up of more than 3 years. Non-antireflux reimplantation did not seem to have any notable impact on renal function during the follow-up period.
Introduction
Robot-assisted laparoscopic (RAL) surgery has been successfully used in urological procedures. In comparison to conventional laparoscopy and laparotomy, RAL provides improved visualization and a high degree of dexterity for the surgeon particularly for operations in the small pelvis. 1 –3 These factors are essential for complex reconstructive operations at the distal ureter, such as ureteral reimplantation for the treatment of a variety of pathologies that cause ureteral obstruction, 4,5 which can lead to significant morbidity. 6
The initial management of distal ureter obstruction is often endoscopic, but the long-term outcomes of these procedures are poor and often not permanent. 7 Definitive reconstruction of the ureter has traditionally been performed through laparotomy to provide adequate exposure in the small pelvis and retroperitoneal space. 8 To date, laparoscopic ureter reconstruction has been associated with less blood loss, shorter hospital stay, and decreased postoperative pain when compared with traditional laparotomy. However, a disadvantage of the laparoscopic procedure is the decreased dexterity of suturing. Robot-assisted laparoscopic ureteral reimplantation (RALUR) with or without Psoas Hitch (PH) or Boari Flap (BF) has overcome the limitations of both the open and laparoscopic approaches. In smaller case series, RALUR has shown good performance in perioperative outcomes. 9 –11 However, the interpretation of the results to date is limited by the short follow-up periods, sometimes of only a few months postoperatively. 10 Furthermore, there is little consensus on whether the ureter should be implanted into the bladder by an antireflux or non-antireflux technique.
Accordingly, the present study was conducted to assess the long-term efficacy and safety of non-antireflux RALUR in patients with distal ureteral obstruction, specifically focusing on clinical recurrence of distal ureteral stenosis and reoperation rate, along with renal function parameters.
Patients and Methods
Study design and setting
We performed a retrospective, cohort study at the Departments of Urology at University Hospital Basel and Cantonal Hospital Baselland, both Swiss tertiary-care centers. DaVinci Si robotic systems (Intuitive Surgery, CA, USA) were acquired by the University Hospital Basel in 2012 and by the Cantonal Hospital Baselland in 2013.
All RALUR procedures were performed in the same technique with the patient under general anesthesia in dorsal lithotomy position, and the robot was docked from the side. A 12-mm camera port was placed above the umbilicus with two 8-mm working ports at ∼6–8 cm lateral on each side of the camera. A third working port was placed about 2 cm cranial to the left anterior superior iliac spine and 3–4 cm lateral to the first working port. Following the transperitoneal access, the parietal peritoneum was opened above the external iliac vessels to identify the ureter, which was then dissected without additional imaging of microperfusion. Then, a laparoscopic clip (Hem-O-lok) was applied at the distal end of the ureter and the ureter was transected. In patients with ureteral stents, the ureter was transected first and then the distal end of the ureter was closed with a clip.
The ureter proximal to the transection site was then further released and mobilized toward the bladder dome and the Retzius space was opened to evaluate the possibility of primary simple non-antireflux ureter reimplantation or of reimplantation in combination with PH, BF, or both.
The psoas muscle and the bladder wall were approximated by using 3-0 Vicryl absorbable suture. The distally spatulated ureter was sutured to a 2-cm vertical incision in the anterior wall of the bladder by an absorbable running suture (Stratafix 3-0 or Monocryl 4-0). In patients not preoperatively stented, a Double-J stent was inserted before closing the anastomosis so that all patients were stented postoperatively. Lastly, the detrusor and the serosa of the bladder were adapted.
All procedures were conducted by three experienced and trained robotic surgeons using the same technique.
The Ethics Committee of Northwestern and Central Switzerland approved our study protocol, waiving individual informed consent (No. 2020-01725). The study has been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. We adhered to the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guideline when reporting our study results. 12
Patient selection
Records of all consecutive patients undergoing non-antireflux RALUR for benign distal ureteral obstruction at both institutions between April 2015 and January 2020 were eligible for inclusion in the analysis. Eligible patients had a primary nonureteral cancer-related distal ureteral obstruction, defined as an obstruction of the pelvic ureter distally to the Linea terminalis. Exclusion criteria were: (1) missing outcome data; (2) patient-declined participation in any clinical study project involving secondary use of his or her routine health care data.
Data collection and definitions
Two independent investigators (K.B. and R.S.) collected and reviewed all relevant pre-, peri-, and postoperative data obtained from the in-house electronic medical records or from article archives. In addition to clinical symptoms and altered renal retention parameters, distal ureteral obstruction was usually diagnosed by different imaging modalities depending to the different etiologies of the obstruction. Baseline patient characteristics retrieved from the routine preoperative assessments included: sex; age; body mass index (BMI); American Society of Anesthesiologists (ASA) score; etiology of distal ureteral obstruction; urinary outflow obstruction (i.e., <50% decrease in 30 minutes or decrease only after application of diuretics) and split renal function in 99mTC-MAG3 scintigraphy; preoperative serum creatinine level and glomerular filtration rate (estimated by Chronic Kidney Disease Epidemiology Collaboration [CKD-EPI] equation); and preoperative ureteral stenting and grade of renal pelvis dilatation at sonography. Dilatation of the renal pelvis was rated from 0 (i.e., no dilatation) to IV (i.e., grade III plus parenchymal thinning). 13
Operative and hospital parameters included in the analysis were: side, method, and duration of RALUR; estimated blood loss (EBL); length of hospital stay; days until postoperative cystogram; and duration of postoperative ureteral stenting. Postoperative 30-day complications were assessed according to the Clavien–Dindo classification. Postoperative stent removal was routinely performed at the first follow-up visit, ∼4 to 6 weeks after RALUR, and further routine clinical follow-up visits took place regularly after that, with a focus on evidence of recurrent ureteral obstruction or the development of symptomatic reflux (e.g., onset of flank pain). In case of symptoms of reflux, a cystogram was performed. Routine urine culture, determination of renal retention parameters and sonography of the kidneys with empty bladder (i.e., <50 mL bladder filling), and assessment of upper urinary tract infections (UTIs) (e.g., pyelonephritis) were performed.
The follow-up was defined from the date of the RALUR until the last consultation until January 2022 or death or loss to follow-up, whichever occurred first. If a second RALUR was required due to recurrence, the follow-up was continued until the reoperation and the secondary RALUR was recorded as reoperation for the primary RALUR case.
Data were entered into a predefined and piloted Microsoft Excel spreadsheet (Microsoft Excel; Microsoft Cooperation, Redmond, WA, USA).
Primary outcome
Our primary outcome measure was recurrence of clinical distal ureteral obstruction. 13 When increasing dilatation of the renal pelvis—determined by sonography with empty bladder—suggested recurrence of ureteral obstruction, the first choice for further evaluation was (diuretic) 99mTC-MAG3 scintigraphy to detect urinary outflow obstruction and evaluate split renal function. Secondarily, contrast-enhanced CT, including delayed phase imagining could be performed to further examine urinary outflow obstruction and its cause.
Statistical analyses
Descriptive statistics, including median; minimum, maximum, and first- and third quartiles (i.e., interquartile range [IQR]); mean and confidence interval (CI); or total number and percentage of total, are reported for all outcomes.
To identify differences between pairwise pre- and postoperative outcomes, Wilcoxon signed-rank tests were applied. All statistical analyses were performed in R (R Core Team;
Results
Patient selection and incidence of recurring urinary outflow obstruction
A total of 26 patients underwent RALUR during the study period and none was excluded. Sixteen RALURs were performed at the Department of Urology at the University Hospital of Basel and 10 at Cantonal Hospital Baselland.
Mean follow-up was 41.3 months (95% CI, 33.3–49.2, range 2–82). During follow-up, no case of either clinical or image-morphological recurrent distal ureteral obstruction was recorded.
Patient characteristics
More women than men underwent RALUR (57.7% vs 42.3%). The median age was 53 years (IQR, 36.5–62.75), median BMI was 24.5 kg/m2 (IQR, 22–28), and median ASA score was 2 (IQR, 2–3) (Table 1).
Characteristics of the Patient Population (N = 26)
All proportions are expressed as valid percentages.
ASA = American Society of Anesthesiologists; BMI = body mass index; IQR = interquartile range; RALUR = robotic-assisted laparoscopic ureter reimplantation.
The majority of distal ureteral obstructions were caused by ureterolithiasis or followed ureterolithiasis treatment (26.9%) or scar tissue formation from other surgical interventions (23.1%). No case of distal ureteral obstruction was caused by prior radiotherapy. Urinary outflow obstruction determined by preoperative 99mTC-MAG3 scintigraphy was present in most of the patients who received scintigraphy (83.3%) and the median split renal function of the affected kidney was reduced to 33% (IQR, 27–39). Kidney function, determined by the serum creatine level and the glomerular filtration rate, was slightly impaired, and most of the affected ureters had been stented (84.1%) for a median of 65 days (IQR, 10–113) (Table 1) preoperatively.
Operative outcomes
More RALURs were performed on the left ureter (65.4%), and in the majority of cases, the RALUR was combined with a PH (84.6%). Median duration of RALUR was 224 minutes (IQR, 177–250) and median EBL was 103 mL (IQR, 0–200). Patients were discharged from the hospital after a median of 7 days (IQR, 6–8). Postoperative cystogram was performed after a median of 5 days (IQR, 5–7) and no leakage was noted in any case. Ureteral stents were routinely removed at 30 days (median; IQR, 14–44) after RALUR without any further imaging (Table 2).
Operative, Functional, and Safety Outcomes
All proportions are expressed as valid percentages.
99mTC-MAG3 = Technetium-mercaptoacetyltriglycine3; BF = Boari Flap; PH = Psoas Hitch.
Not due to RALUR.
Postoperative complications
Among 26 patients, 65.4% had no postoperative complication (Clavien–Dindo grade 0). Clavien–Dindo grade I complication occurred in two cases (7.7%; hematoma, transient neurological symptoms). Clavien–Dindo grade II complications were recorded in six patients (23.1%) and included lower UTI in three cases and one case of pseudomembranous colitis, all requiring antimicrobial treatment, along with one case of gross hematuria requiring catheterization. One pulmonary embolism was treated with the applicable anticoagulant therapy. Finally, one patient had a Clavien–Dindo grade IIIb complication. This patient had originally undergone RAL for intestinal and ureteral endometriosis, during which the distal ureter was injured, and was then treated by RALUR. Five days after RALUR, a sigmovaginal fistula was diagnosed, which was mainly related to the endometriosis RAL than to the RALUR.
No sequelae had been recorded in relation to any of these complications at the time of data collection for this study.
During the long-term follow-up period, 73.1% of the patients in the cohort remained without clinical symptoms of reflux. Three patients (11.5%) described occasional reflux symptoms and four (15.4%) had regular symptoms; in both groups, the symptoms were related to excessive bladder filling. No patient had permanent reflux symptoms. Among nine patients, who had a cystogram during the follow-up period, seven showed a median grade 2 (IQR, 1–3) reflux and only two of these had reflux symptoms. None of the patients with reflux symptoms required additional treatment.
No pyelonephritis or recurrent UTI occurred among the study cohort during the last year of follow-up (Table 2).
Primary outcome
Overall, dilatation of the renal pelvis assessed by sonography with empty bladder was significantly decreased, from grade 2 (preoperative) to grade 0 (postoperative), after RALUR (p < 0.001) (Fig. 1A). Renal function in terms of both the serum creatinine level (72.0 μmol/L vs 71.0 μmol/L, p = 0.988) and the glomerular filtration rate (92.0 mL/min vs 91.0 mL/min, p = 0.831) was stable between the preoperative period and the last follow-up (Fig. 1B and C).

Boxplots and summary of pre- and postoperative renal pelvis dilatation
Among imaging studies, neither postoperative 99mTC-MAG3 scintigraphy nor CT could show urinary outflow obstruction, and there was no case of clinical or image-morphological recurrent distal ureteral obstruction reported during the study, or any reoperation—ureteral stenting or reconstructive surgery (Table 2).
Discussion
Our cohort of 26 patients who underwent RALUR had no clinical or image-morphological recurrent distal ureteral obstruction during a long-term follow-up of 41.3 months. To date, to our current knowledge, this is the largest and longest summary of RALUR operative, functional, and safety outcomes (Table 3).
Operative Outcome in Comparison to Current Literature
Mean, **Median.
EBL = estimated blood loss.
The incidence of distal ureteral obstruction in adults has increased in recent years in tandem with the increasing incidence of ureteral injuries associated with ureteroscopic laser surgeries for stone treatment and other emerging laparoscopic gynecological, urological, and gastroenterological procedures. 14,15 In line with this, in our study, 26.9% of the distal ureteral obstructions were related to ureterolithiasis, with the second most common indication for RALUR (23.1%) being obstruction caused by previous open or laparoscopic surgery for other causes.
During preceding decades, laparotomy was the preferred approach to ureteroneocystostomy. Packiam and colleagues 16 compared laparoscopic and open ureteroneocystostomy in more than 500 patients through the National Surgical Quality Improvement Program and found a shorter duration of hospitalization, lower transfusion rates, fewer UTIs, and fewer superficial wound infections in the laparoscopic cohort. The reoperation rate was higher in the laparoscopic group. A challenge of the laparoscopic approach is the decreased dexterity of suturing. With the introduction of the DaVinci robotic system and RAL, this challenge was eliminated. 17 In several small case series, the open approach was compared with the RALUR approach: Kozinn and coworkers 18 found a significant increase of EBL and length of hospital stay in the open approach (10 matched cases) compared with RALUR.
Another retrospective comparison of 25 RALURs and 41 open ureteroneocystostomies confirmed the increased EBL and length of hospital stay and reported change in hematocrit and narcotic requirement during the latter procedure, whereas the operative time was longer for RALUR during a follow-up period of 11 months. 19 Our own data were consistent with the results in literature considering the operative time, the length of hospital stay, and the recurrence rate (Table 3).
Considering long-term outcome with regard to recurrence, there is only little evidence from small cohort studies in open or laparoscopic reimplantation in distal benign ureteral obstruction. One study on open reimplantation described a success rate of 72.4% and an improvement in 22.2% after 5.7 years. 20 At a mean follow-up of24.1 months, success in laparoscopic reimplantation was 96%. 21 With a success rate of 100% after 41 months or nearly 3.5 years, our results are comparable with open and laparoscopic long-term outcomes if not even better.
The anastomosis between bladder and ureter can be performed with a non-antireflux or antireflux technique. In former years it has been believed that refluxing anastomosis would increase the risk of upper UTI and renal insufficiency due to vesicoureteral reflux. In renal transplantation, vesicoureteral reflux into the transplanted kidney occurs frequently. 22 However, more recent studies on renal transplantation have shown that vesicoureteral reflux has no negative impact on graft function, graft survival, rates of bacteriuria or infection, and renal function. 23 –25 In line with this, literature on open ureteroneocystostomy did not find any significant difference in renal function between non-antireflux and antireflux methods. 26 Similarly, in our study treating patients with non-antireflux RALUR only, kidney function was preserved, represented by stable levels of serum creatine and glomerular filtration rates pre- and postoperatively. Furthermore, no patient had recurrent upper UTI and especially no pyelonephritis episodes in addition to the nonoccurrence of recurrent stenosis and only minor symptoms of reflux.
Showing only minor reflux symptoms, stable kidney function and no clinical or image-morphological recurrent distal ureter obstruction, our study results support the efficacy and safety of non-antireflux RALUR for the treatment of distal ureter obstruction.
Our study has several limitations. First, it was conducted at two tertiary care hospitals only and may not be generalizable, and this might have caused a selection bias. Second, the study may bear limitations due to its sample size. Due to its retrospective nature, certain outcome parameters were not routinely assessed such as scintigraphy or CT. However, since the decision against and for additional imaging was made by experienced urologists based on clinical parameters such as renal pelvis dilatation, renal retention parameters, and pain, we believe that omitting routine imaging would only reveal recurrence of minor clinical significance. A further limitation is the lack of follow-up during this longitudinal study. However, 24 of 26 patients had a follow-up in the last 6 months until end of data assessment. Lack of a comparator such as open or laparoscopic ureter implantation further limits interpretation of this study. Prospective multicenter investigations will be necessary to integrate our findings into current clinical practice.
Conclusions
RALUR is classified as a minimally invasive procedure. It can be safe and effective in managing distal ureteral obstruction. In our study, no patient had recurrent ureteral obstruction after RALUR during a median follow-up period more than 3 years. Non-antireflux implantation seems to have no impact on renal function or UTI in the follow-up. Definite recommendation of RALUR in distal ureteral obstruction warrants further study in prospective randomized controlled trials.
Footnotes
Authors' Contributions
K.B.: Protocol/project development, methodology, data collection, article preparation (writing and editing); R.S.: Data collection and article editing; F.S.H.: Methodology, data analysis, and article review; S.S. and H.H.S.: Protocol/project development, and article review; A.F.: Protocol/project development, data collection, and article writing.
Availability of Data and Material
Raw data were generated at the Department of Urology, University Hospital Basel and Cantonal Hospital Baselland. Derived data supporting the findings of this study are available from the corresponding author (K.B.) on request.
Ethics Approval
The Ethics Committee of Northwestern and Central Switzerland approved our study protocol, waiving individual informed consent (No. 2021-00561). The study has been performed in accordance with the ethical standards established in the 1964 Declaration of Helsinki. Reporting of the study results is in adherence with the STROBE guideline.
Consent to Participate
Due to the retrospective nature of the study, patients were not asked for individual informed consent. At University Hospital Basel, patients are asked to sign a general informed consent form for the further use of health care data. If patients declined this general informed consent, they were withdrawn from study participation. This procedure was approved by the Ethics Committee of Northwestern and Central Switzerland (No. 2020-01725).
Author Disclosure Statement
No competing financial interests exist.
Funding Information
No funding was received for this article.
