World Journal of Urology (2023) 41:1951–1957 https://doi.org/10.1007/s00345-023-04455-3 ORIGINAL ARTICLE Effectiveness of endourological management of ureteral stenosis in kidney transplant patients: EAU‑YAU kidney transplantation working group collaboration Angelo Territo1 · Alejandra Bravo‑Balado1 · Iulia Andras2 · Riccardo Campi3,4 · Alessio Pecoraro3 · Vital Hevia5 · Thomas Prudhomme6 · Michael Baboudjian1,7 · Andrea Gallioli1 · Paolo Verri1 · Mathieu Charbonnier7 · Romain Boissier7 · Alberto Breda1 Received: 12 November 2022 / Accepted: 22 May 2023 / Published online: 20 June 2023 © The Author(s) 2023 Abstract Purpose Ureteral stenosis (US) in kidney transplant (KT) recipients is associated with poorer long-term graft survival. Surgical repair is the standard of care, and endoscopic treatment represents an alternative for stenosis < 3 cm. We aimed to determine the effectiveness and safety of endourological management of US in KT patients and predictors of failure. Methods A retrospective multicenter study was conducted in four European referral centers, including all KT patients with US managed endoscopically between 2009 and 2021. Clinical success was defined as the absence of upper urinary tract catheterization, surgical repair or transplantectomy during follow-up. Results A total of 44 patients were included. The median time to US onset was 3.5 months (IQR 1.9–10.8), the median length of stricture was 10 mm (IQR 7–20). Management of US involved balloon dilation and laser incision in 34 (79.1%) and 6 (13.9%) cases, respectively, while 2 (4.7%) received both. Clavien–Dindo complications were infrequent (10%); only one Clavien ≥ III complication was reported. Clinical success was 61% at last follow-up visit (median = 44.6 months). In the bivariate analysis, duckbill-shaped stenosis (vs. flat/concave) was associated with treatment success (RR = 0.39, p = 0.04, 95% CI 0.12–0.76), while late-onset stenosis (> 3 months post KT) with treatment failure (RR = 2.00, p = 0.02, 95% CI 1.01–3.95). Conclusions Considering the acceptable long-term results and the safety of these procedures, we believe that the endoscopic treatment should be offered as a first-line therapy for selected KT patients with US. Those with a short and duckbill-shaped stenosis diagnosed within 3 months of KT seem to be the best candidates. Keywords Endourology · Kidney transplantation · Ureteral stenosis Abbreviations EAU European association of urology Angelo Territo and Alejandra Bravo-Balado have equally IQR Interquartile range contributed to this manuscript as first authors. KT Kidney transplant US Ureteral stenosis Romain Boissier and Alberto Breda equally contributed to senior URS Ureterorenoscopy authorship. 4 * Alejandra Bravo‑Balado Department of Experimental and Clinical Medicine, alejandra.bravo146@gmail.com University of Florence, Florence, Italy 5 1 Hospital Universitario Ramón y Cajal. Alcalá Department of Urology, Fundació Puigvert and Autonomous University. Instituto Ramón y Cajal de Investigación University of Barcelona, Carrer de Cartagena 340, Fundació Sanitaria (IRYCIS), Madrid, Spain Puigvert, 08025 Barcelona, Spain 6 2 Department of Urology and Kidney Transplantation, Urology Department, Iuliu Hatieganu University of Medicine Toulouse University Hospital, Toulouse, France and Pharmacy, Cluj‑Napoca‑Napoca, Romania 7 3 Department of Urology and Kidney Transplantation, APHM, Unit of Urologic Robotic, Minimally‑Invasive Surgery CHU de La Conception Hospital, 146, Boulevard Baille, and Renal Transplantation, Careggi University Hospital, 13005 Marseille, France Florence, Italy 13 Vol.:(0123456789) 1952 World Journal of Urology (2023) 41:1951–1957 Introduction endoscopically between 2009 and 2021. Patients with missing variables required to analyze outcomes were The incidence of ureteral stenosis (US) in kidney trans- excluded. The decision to perform endoscopic manage- plant (KT) patients is around 5%, and goes up to 10% at ment was left to the clinical judgment of the treating phy- 5 years [1], representing the most common long-term uro- sician after discussion with each patient regarding the logical complication [2]. It is negatively correlated with potential benefits and side effects of all available treatment long-term renal graft survival [4]; consequently, timely modalities for the management of US after KT. diagnosis and treatment are mandatory. Ureteral stenosis We reviewed donor and recipient baseline characteristics, typically becomes evident within the first 3 months after allograft description (number of arteries, veins, ureters, lat- KT and is primarily caused by ureteral ischemia: loss of erality), KT surgery variables, ureteral stenosis description distal ureteral perfusion through graft explantation in the (clinical presentation, initial management, length, shape, situation of an ureterovesical anastomosis or loss of the location, and onset time) and endourological management proximal perfusion of the native ureter in case of pyelo- variables (the use of balloon and/or laser and complications). ureteral anastomosis. Late stenosis is rare, and less com- The postoperative outcomes were reviewed at 6 and mon causes should be explored, such as vascular disease, 12 months and at the last follow-up visit and included creati- fibrosis, infection, reactivation of BK virus or allograft nine values and estimated glomerular filtration rate (eGFR). rejection [5, 6]. Historically, the open surgical approach Clinical failure was defined as the need for upper urinary has been the main treatment option for these patients, tract catheterization, surgical repair or transplantectomy especially in cases of complex, mid-third or proximal US at 6, 12 and last follow-up visit. Follow-up duration was [7, 8], given its association with increased renal graft sur- defined as the time between endoscopic procedure and the vival [8]. Although the surgical reconstruction has gained last follow-up visit. new insights due to the possibility of robot-assisted US The statistical analysis was performed using Prism soft- repair, even minimally invasive reconstructive approaches ware; descriptive statistics using central tendency and fre- may have associated complications that are not negligible quencies for continuous and categorical variables, respec- [9]. Given recent advances in endourological instrumenta- tively, were used. Inferential statistics were employed for the tion, an endoscopic approach, using either percutaneous evaluation of potential predictive factors for failure, using balloon dilatation or flexible antegrade ureteroscopy and Chi2 test and presented as risk ratios; p values < 0.05 were holmium laser incision, has been proposed as a reason- considered as statistically significant. able alternative for stenosis < 3 cm. To date, data on endo- scopic treatment of US after KT are scarce and come from a limited number of single-center series. Factors that may Results predict outcomes of the endoscopic management are also not known, although they could improve patient selection A total of 44 KT recipients were included. Table 1 shows for optimal results. Our objective was to determine the the patients’ baseline characteristics. Twenty-nine (75%) effectiveness and safety of the endourological management KT were obtained from deceased donors, and the median of US in KT patients in four European institutions and to age in the overall cohort was 52 years (IQR 35–63). Eight determine predictive factors of clinical failure. (18.2%) patients had a pyelo-ureteral anastomosis, while the rest (81.8%) had an ureterovesical anastomosis. The clinical presentation of US was as acute renal fail- ure in 31 (79.5%) cases. The median time to US onset Materials and methods was 3.5 months (IQR 1.9–10.8) and was ≤ 3 months in 24 (56.8%) patients. The initial drainage consisted in a nephros- This retrospective, multicenter study was conducted in tomy tube in 37 (84.1%) patients, while 7 (16.7%) had a dou- accordance with the principles of Good Clinical Practice ble-J stent. The median length of US assessed by antegrade and the Declaration of Helsinki. Patients were recruited pyelogram was 10 mm (IQR 7–20). In 47.7% (n = 21) of from four referral centers in Spain (Barcelona), France cases the endoscopic approach was through antegrade ure- (Marseille and Toulouse), Italy (Florence). All data were terorenoscopy (URS), followed by retrograde URS (n = 19, de-identified and ethical approval was waived by the 43.2%), and in 9.1% (n = 4) a combined approach was used. local Ethics Committee of our institution in view of the The use of balloon dilation only was reported in 79.1% retrospective nature of the study and all the procedures (n = 34) and laser incision only in 13.9% (n = 6) of cases, being performed as part of the routine care. The cohort while 2 (4.7%) cases had both procedures. Intraoperative included KT patients aged ≥ 18 years with US managed double-J catheter insertion was registered in 80% (n = 35) of patients. 13 World Journal of Urology (2023) 41:1951–1957 1953 Table 1  Baseline characteristics Table 2  Ureteral stenosis description and management N = 44 % N = 44 %* Donor Clinical presentation Type of donor Incidentally at US or CT scan 8 18.2 Living donor unrelated 4 9.1 Acute renal injury 35 79.5 Living donor related 7 15.9 Acute pyelonephritis 1 2.6 Deceased donor 33 75.0 Onset time Sex Early (< 3 months) 25 56.8 Male 24 54.5 Late (> 3 months) 19 43.2 Female 20 45.5 Initial management Recipient Double-J stent 7 16.7 Sex Nephrostomy tube 37 84.1 Male 27 61.4 Location of the stricture Female 17 38.6 Pyelo-ureteral 7 15.9 Obesity 9 20.4 Proximal 3 7.7 BMI (median, IQR) 24.1 21.7–26.9 Middle 3 7.7 Hypertension 38 86.4 Distal/ureterovesical 31 70.5 Diabetes mellitus 10 22.7 Length (in mm) (median, IQR) 10 7–20 Charlson score (median, IQR) 5 3–5 Shape Numer of kidney transplants Flat/concave 13 29.5 1 40 90.9 Sharp 31 70.5 2 2 4.5 Pass of contrast at initial management 32 72.7 3 2 4.5 Endoscopic approach Numer of arteries Retrograde 19 43.2 1 36 85.7 Antegrade 21 47.7 2 5 11.9 Antegrade + retrograde 4 9.1 3 1 2.4 Use of balloon only 34 79.1 Number of veins Use of laser only 6 13.9 1 41 97.6 Balloon + laser 2 4.7 2 1 2.4 Passage of a Couvelaire catheter 1 2.3 Number of ureters Intraoperative double-J stent insertion 1 41 97.6 No passing of stent 1 2.5 2 1 2.4 Conventional double J 35 80.0 Transplantation side UniJ 1 2.5 Right 23 57.5 Memokath 6 15.0 Left 17 42.5 Clavien–Dindo complications Ureteral anastomosis II 3 7.5 Campos-Freire 3 7.3 IIIa 1 2.5 Lich-Gregoir 26 63.4 * Valid percentages due to missing data Politano-Leadbetter 2 4.5 Pyelo-ureteral 8 18.2 Taguchi-Alferez 2 4.5 Delayed graft function 8 18.2 Nadir eGFR (Me, IQR) 41.9 (30.5–49) BK virus infection 7 15.9 Table 3  Postoperative outcomes 6 months 12 months Last follow-up visit Clavien–Dindo II complications occurred in 7.5% (n = 3) of cases, and 1 patient had a IIIb (descended double-J stent Creatinine level 154 (106– 162 (99.5– 154 (95.4–202) 178.5) 200.5) that required reinsertion) (Table 2). After a median follow- eGFR 37 (28–48) 40 (23–52) 35 (17.5–45) up of 44.6 months (IQR 30.1–100.2), clinical success was Success rate (%) 28 (64) 29 (66) 27 (61) maintained in 61% (n = 27) of patients (Table 3). Salvage 13 1954 World Journal of Urology (2023) 41:1951–1957 therapies included a permanent double-J catheter for peri- success rate of endoscopic management according to the odic replacement in 6 patients (13.6%), ureteral reimplanta- shape of US. There were no differences in treatment success tion in 7 patients (15.9%) and transplantectomy in 4 cases regarding the location of the stenosis (p = 0.61). Figure 2 (9.1%). shows two antegrade pyelograms of both US morphologies. Concerning the factors associated with treatment failure, in the bivariate analysis, having a duckbill-shaped steno- sis (vs. flat/concave) was associated with treatment success Discussion (RR 0.38, p = 0.046, 95% CI 0.12–0.76, p = 0.04), while late-onset stenosis was associated with treatment failure Nowadays, choosing the optimal treatment for US in KT (RR 2.00, p = 0.023, 95% CI 1.01–3.95). Figure 1 shows the patients is still a matter of debate. Although minimally inva- sive approaches have been used for this condition for over 30 years [10], their interest has resumed with the appearance 80.0 of new technologies, including the use of the different lasers available for endourology [4]. 70.0 In our study, we reported a success rate of the endoscopic 60.0 management of US in KT patients of 64%, 66% and 61% at 6, 12 and last follow-up visit, respectively. These rates 50.0 are lower compared to the results published by Kristo et al. Percentage [2], who found a 100% success rate at a median follow-up 40.0 of 24 months; however, they only included short US with a mean length of 2.8 mm while we included longer US with a 30.0 median of 10 mm. Our results are similar to those of Kwong 20.0 et al. [11] who reported a success rate of the endourological approach of 64.3%. 10.0 In contrast, the success rates for surgical reconstruction have been reported in previous studies to be 77% [5], which 0.0 Flat, 28.6 Sharp, 73.3 is not far from the success achieved by the endoscopic man- agement but involves more complex strictures and cases that Fig. 1  Success rate according to the shape of ureteral stenosis Fig. 2  Antegrade pyelogram of ureteral stenosis. A. Sharp or duckbill shape. B. Flat or concave shape 13 World Journal of Urology (2023) 41:1951–1957 1955 have failed endoscopic management (in this study, more than stricture. The results of these studies are similar with our find- half of them had previously failed balloon dilation). ings: early-onset stenosis (< 3 months) was associated with A recent systematic review including 34 studies and 385 endoscopic management success. patients with distal ureteral strictures after KT found suc- Currently, the EAU guidelines on KT provide recommenda- cess rates for surgical reconstruction as high as 85.4% in tions on the management of US based on the timing, anatomy patients receiving this approach as primary treatment and of the stricture (i.e., length and location), patients’ character- as high as 93.1% as a secondary treatment, after a failed istics, and surgeon’s preferences [19]; however, no reference endoscopic treatment. In the same study, the endourological has yet been made to the shape of the stenosis and its possible approach had a success rate of 64.3% and 75.5% for primary implication in the success rate of endoscopically treated US. and secondary treatments, respectively, which is consistent There is a rationale from a previous study published by with our results. Gaya et al. [20] in 2023, who found that ureteroenteric anas- On the other hand, we included 6 patients who received tomotic strictures were more likely to be successful with a permanent double-J catheter, with no need for other treat- endoscopic management when these were < 1 cm (16.8% ments afterwards apart from periodic replacement; this vs 4.4%, p < 0.001) and had a duckbill-shaped (16, 7% vs approach is considered as acceptable, especially for unfit 3.1%, p < 0.001). patients or those who do not wish to undergo surgery, with Similarly, in our study, we found that a duckbill-shaped success rates that goes over 90% [12, 13]. Although some US was associated with treatment success. This finding may controversy still remains, according to previous studies, have an impact on patient selection that could potentially there seems to be no association between permanent ure- improve postoperative outcomes. We believe further stud- teral stenting in KT patients and the development of com- ies focusing on this aspect should be carried out to confirm plicated urinary tract infection [14–16]; therefore, we agree our findings. with other authors that this could be a reasonable solution We reported few Clavien–Dindo complications (only one in selected cases. IIIb and 3 II cases), with no reports of Clavien–Dindo > III, Other studies have also inquired about possible risk fac- which is consistent with previous published series [18]. tors associated with the success of US endoscopic manage- The present study has several limitations that should be ment. Gil-Sousa et al. [7] published in 2017 a single-center acknowledged. The main limitation lies in its retrospec- 10-year experience of US stenosis after KT, including both tive design. The size of the cohort was also modest, even reconstructive and endoscopic treatments; they found no dif- after including patients over a long period of time from four ferences according to length of stenosis, time between trans- dedicated European KT centers, underscoring the need to plant and stenosis or stenosis location; however, there was a increase the evidence for this management strategy to allow clear trend towards a higher success rate in stenosis < 1.5 cm for greater dissemination. Having a modest sample size may and early management < 3 months, particularly with the use confer low statistical power, which could explain why a mul- of balloon dilatation, which corresponds with our results. tivariate analysis was not feasible in our study. In addition, In line with these findings, regarding the length of the the patients included were probably considered good candi- stenosis [7], He et al. [17] published a classification of US dates for these treatments beforehand, which could overes- consisting of 3 grades: (1) graft function deterioration and timate the success rates. Moreover, our study lacks data on hydronephrosis on ultrasound but no obvious stricture iden- the duration of balloon dilation and the pressure used, which tified on a pyelogram; (2) focal (< 1 cm) distal ureteral ste- could potentially have implications for treatment outcomes. nosis at the ureteral anastomotic site, and (3) long segment In addition, there is a need for more data on the use of laser (> 1 cm) distal ureteral stenosis extending to proximal ureter in these procedures. or pelvis. Taking this classification into account, they suc- Regardless of these limitations, we present a European cessfully treated 1 case as grade 1 with ureteral stent reinser- multicenter study that represents one of largest series of tion for 6 weeks; 6 as grade 2 using balloon dilation/ureterot- endoscopic management of US in KT patients, including omy; and 5 as grade 3 with open surgery reconstruction after new evidence that could improve patient selection for these an initial attempt with endoscopic treatment. Their findings techniques, potentially reducing failed treatments, surgical suggest that there may be an association between the length complications, disease burden and costs. of the stenosis and the success of the endoscopic treatment. Interestingly, we did not find a statistically significant differ- ence regarding the length of the US, probably because our Conclusions sample of patients had a relatively short stenosis. Another study published by Juaneda et al. [18] found that According to our study, around two-thirds of KT patients a short time to diagnosis after KT and previous acute rejec- with US have a successful endoscopic management. Con- tion episode predicted the endourological success of a ureteral sidering the acceptable long-term results and the safety of 13 1956 World Journal of Urology (2023) 41:1951–1957 these procedures, we believe that the endoscopic treatment correction. J Urol 133:17–20. https://​doi.​org/​10.​1016/​S0022-​ should be offered as a first-line therapy for selected KT 5347(17)​48766-0 2. Kristo B, Phelan MW, Gritsch HA, Schulam PG (2003) Treat- patients with US. Those with a short and duckbill-shaped ment of renal transplant ureterovesical anastomotic strictures stenosis diagnosed within 3 months of KT seem to be the using antegrade balloon dilation with or without holmium:YAG best candidates. laser endoureterotomy. Urology 62:831–834. https://​doi.​org/​10.​ 1016/​S0090-​4295(03)​00655-1 Acknowledgements None. 3. Praz V, Leisinger HJ, Pascual M, Jichlinski P (2005) Urologi- cal complications in renal transplantation from cadaveric donor Author contributions AT: protocol and project development, data grafts: A retrospective analysis of 20 years. Urol Int 75:144– collection and management, and manuscript writing/editing. AB-B: 149. https://​doi.​org/​10.​1159/​00008​7169 protocol and project development, data collection and management, 4. Deininger S, Nadalin S, Amend B, Guthoff M, Heyne N, König- data analysis, and manuscript writing/editing. IA: protocol and project srainer A et al (2021) Minimal-invasive management of urologi- development, data collection and management, and manuscript writing/ cal complications after kidney transplantation. Int Urol Nephrol editing. 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