Objectives: To evaluate the etiology and diagnostic tools for ureteropelvic obstruction in kidney transplant recipients, we investigated the short-term and long-term outcomes of Foley Y-V pyeloplasty.
Materials and Methods: We retrospectively reviewed 10 patients who underwent kidney transplant followed by additional interventions to treat obstructive ureteral pathologies between 2016 and 2020. We enrolled 4 patients who had received intervention to treat ureteropelvic obstruction. For these 4 patients, serum creatinine and estimated glomerular filtration rate levels were recorded at baseline, during the symptomatic period, and long-term. In this single-center study, we investigated diagnostic tools and management strategies for ureteropelvic obstruction and assessed performance of Foley Y-V nondis-membered pyeloplasty in kidney transplant recipients.
Results: Among 4 patients, graft function (assessed by serum creatinine and estimated glomerular filtration rate) worsened significantly (P = .03) in the symptomatic period of ureteropelvic obstruction in all patients; however, graft function levels improved rapidly to levels similar to baseline (P = .07) after Y-V pyeloplasty. In addition, no statistically significant difference was detected between baseline and long-term graft functions after Y-V pyeloplasty in follow-up (P = .28).
Conclusions: Diagnosis and management of ureter-opelvic obstruction in kidney transplant recipients are challenging due to rarity and lack of an ideal management algorithm. There is no specific diagnostic tool to discriminate this pathology from other ureteral pathologies; therefore, a regimen of conventional imaging modalities and diuretic renogram combined with endoscopic evaluation is more reliable. Moreover, nondismembered Foley Y-V pyeloplasty is effective and safe for graft function in the short-term and long-term.

Key words : End-stage renal disease, Foley Y-V plasty, Kidney transplantation, Ureteropelvic junction

Introduction

Kidney transplant (KT) is the optimal treatment for patients with end-stage renal disease (ESRD), because KT reduces the risk of death and provides better quality of life and longer life expectancy than dialysis.^1,2 Despite KT being the most efficient treatment, many well-known factors and surgical complications may influence outcomes. To date, various studies have highlighted urological complica-tions such as ureteral stenosis, vesicoureteral reflux, urine leakage, and ureteropelvic obstruction (UPO) and appropriate treatment modalities to improve graft survival. Nevertheless, these complications may occur in 2.8% to 15.5% of KT recipients and cause significant morbidity and mortality.^3,4

According to the literature, UPO is a rare comp-lication in KT patients, with an incidence rate of 0.25%,⁵ and causes significant deterioration in graft functions. Although several studies have investigated the etiology and management strategies, the absence of a reliable diagnostic tool or precise treatment algorithm for UPO presents a persistent challenge for clinicians. Several potential causes have been identified in the literature, such as denervation of the graft due to surgery, severe fibrosis in the periureteric tissue, insufficient blood supply to the ureter, existence of prior asymptomatic UPO in the transplanted kidney, and improper anastomosis of the lower pole artery.^5-9 Although there are well-known open surgical interventions, such as Anderson-Hynes dismembered pyeloplasty, Foley Y-V pyeloplasty, and uretero-native pyeloureterostomy, that have demonstrated successful and long-lasting outcomes,^5,10,11 minimally invasive endoscopic inter-ventions have been described in recent years.^9,12,13

In the present study, we investigated the possible causes of UPO and its association with other ureteral pathologies, considered the absence of a specific diagnostic tool, and evaluated the performance of the Foley Y-V pyeloplasty in the short-term and long-term.

Materials and Methods

This study was conducted in accordance with the Declaration of Helsinki and approved by our institutional ethics committee (August 2, 2023; Decision No. 2012-KAEK-20). Written informed consent was obtained from participants.

We retrospectively reviewed 10 patients who had received KT for ESRD followed by additional interventions due to obstructive ureteral pathologies between 2016 and 2020. Four patients diagnosed with UPO and treated with additional surgery were enrolled in the present study. We collected data on age, sex, serum creatinine level, estimated glomerular filtration rate (eGFR), ultrasonography (USG) results, split kidney function with technetium-99m diethyle netriaminepentaacetic acid (DTPA) scans, and radiological and surgical interventions during follow-up. Patients with voiding dysfunction, graft rejection, or additional surgeries during the acute period were excluded.

For all recipients and the deceased donor, open surgery was preferred, and laparoscopic nephrec-tomy was performed in living donors by a highly experienced transplant team consisting of general surgeons and nephrologists. Ureterovesical (UV) anastomosis was created according to the modified Lich-Gregoir technique with a detrusor tunnel in at least a 3:1 ratio, and a double J stent was routinely placed and removed endoscopically in the posto-perative week 5 or 6. All patients were routinely monitored at the transplant clinic via clinical visits and referred to the urology clinic for the presence of any postrenal pathologies such as an increase in kidney function with hydronephrosis, recurrent urinary tract infections, and voiding dysfunction.

Patients suspected of having UPO were examined using USG scans and serum creatinine and eGFR values in the first-line evaluation. Additionally, for 2 patients who had no graft deterioration that would necessitate urgent intervention, DTPA or computed tomography (CT) scans were used to determine the certainty of the diagnosis. To anticipate concomitant UV anastomotic stricture or intrinsic obstructive abnormality, either antegrade nephrostogram or diagnostic ureterorenoscopy combined with retrograde pyelography (URS/RGP) via flexible devices was performed to assess the urinary system. Subsequent to definitive pyeloplasty, the double J stent was removed in week 6 or week 8, and patients were routinely followed-up with serum creatinine and serum eGFR assessments and additional USG scans. Detailed diagnostic evaluation processes were presented separately for each patient, to emphasize the diversity in clinical management.

Statistical analyses
Differences between values were checked with the Friedman test. The 2-way comparisons were performed with the Wilcoxon test. The SPSS software program (version 21) was used for statistical analyses. Statistical significance was set at P < .05.

Results

Of 10 patients, we examined 4 patients for this study. Data including patient age, sex, donor source, and ESRD etiology are summarized in Table 1.

Patient 1
A female patient, 23 years old, with congenital hypoplastic kidney disease underwent KT from a deceased donor in 2016. The donor had no history of urinary abnormalities on blood tests or radiological examination. The postoperative period was une-ventful, with a basal creatinine of 0.86 mg/dL and basal eGFR of 95.22 mL/min/1.73 m².

Patient 1 presented to the transplant clinic in month 9 after KT with deteriorated kidney functions (1.4 mg/dL serum creatinine, 50 mL/min/1.73 m2 eGFR). Although minimal hydronephrosis with 15 mm anteroposterior diameter (APD) was detected on USG scan, no abnormality was observed in DTPA. Two weeks later, a percutaneous nephrostomy catheter was placed, and serum creatinine level decreased from 2.6 to 0.9 mg/dL in 2 days. On antegrade pyelography, neither obvious UPO nor total UV anastomosis stricture was identified; thus, URS/RGP was planned to evaluate intrinsic obstructive pathologies. In diagnostic URS/RGP, no pathology was observed in the ureteropelvic junction (UPJ), whereas partial anastomotic stricture was seen in UV junction. Therefore, the patient was scheduled to undergo redo ureteroneocystostomy (redo-UNC) avoiding aggressive ureteral dissection according to the Paquin technique14 in month 12 after KT, and no additional complications were monitored intrao-peratively and postoperatively.

Serum creatinine levels were between 0.8 and 1.0 mg/dL for 2 years during follow-up. Twenty-five months after redo-UNC, the patient presented to the transplant clinic with an increase in serum creatinine to 2.1 mg/dL and isolated pelvicalyceal dilatation (without ureteral dilatation) on USG with APD of 22 mm; hence, a DTPA scan was performed. In the DTPA scan, partial blockage of urine flow through the ureter and a time to maximum relative enhan-cement (Tmax) value of 9 minutes were detected, which were suspicious for UPO. Therefore, diag-nostic URS/RGP was performed, and the results suggested a likely UPJ disruption (UPJD) but not a UV stricture (Figure 1A). Hence, pyeloplasty was planned for reconstruction.

In open surgery, severe fibrosis in periureteric tissue and angulation of the UPJ were observed, and pyeloplasty was performed according to the Foley Y-V pyeloplasty technique with double J ureteral stent placement.

Patient 2
A male patient, 48 years old, with ESRD of unknown etiology underwent KT from a living donor (patient’s spouse) in 2016. The donor had no prior urological pathologies on examination or USG, DTPA, and CT scans. Postoperative period was uneventful with 1.0 mg/dL baseline serum creatinine and 98 mL/min/1.73 m² baseline eGFR.

In month 5 after KT, the patient presented to the transplant clinic with deteriorated kidney functions with 2.2 mg/dL serum creatinine, 32 mL/min/1.73 m² eGFR, and 28 mm APD on USG scan. Therefore, DTPA and CT scans were performed, and a potential UPO was identified (Figure 1B). Subsequent to these analyses, diagnostic URS/RGP was performed to evaluate UV anastomosis and any intrinsic obstructive pathology. None of these was observed; however, RGP revealed a suspicious extrinsic obstruction in the UPJ. Therefore, a double J stent was placed, kidney function ranged within acceptable limits, and the patient was scheduled for pyeloplasty in month 7 after KT.

During surgery, angulation of the proximal ureter caused by severe fibrosis and medial rotation of the kidney in the transverse axis was observed; hence, the UPJ was dissected meticulously and recon-structed according to the Foley Y-V pyeloplasty technique with placement of a double J ureteral stent.

Patient 3
A male patient, 37 years old, with hypertension-related ESRD underwent KT from a living donor (patient’s mother) in 2022. The donor had no prior urological pathologies in the mentioned analysis. The postoperative period was uneventful with baseline serum creatinine of 1.4 mg/dL and baseline eGFR of 61 mL/min/1.73 m². In week 6 after KT, the double J stent inserted in KT was removed. Two days after stent removal, kidney function had deteriorated to 6.6 mg/dL serum creatinine, 10 mL/min/1.73 m² eGFR, and 20 mm APD on USG scan. Thus, URS/RGP was applied, which revealed no intrinsic obstruction in UV junction or UPJ. Following double J stent insertion, serum values improved to 1.2 mg/dL serum creatinine and 55 mL/min/1.73 m² eGFR, and the patient was monitored for 3 months. In month 3, the patient presented to the transplant clinic with elevated serum creatinine (4.5 mg/dL) and 27 mm APD on USG scan; thus, percutaneous nephrostomy was placed, and the ureteral double J stent was removed. After the patient showed improved kidney function, antegrade pyelography was performed and was compatible with UPJD (Figure 1C); hence, the patient was scheduled for pyeloplasty. During surgery, severe fibrosis causing angulation of UPJ was eliminated meticulously, and reconstruction was performed according to Foley Y-V pyeloplasty in the same manner.

Patient 4
A male patient, 68 years old, with ESRD related to autosomal dominant polycystic kidney disease underwent KT from a living donor (patient’s spouse) in 2021. The postoperative period was uneventful with 1.3 mg/dL baseline serum creatinine and 61 mL/min/1.73 m² baseline eGFR. Twenty-four hours after the removal of double J stent in week 6 after KT, the patient presented with anuria and 10 mm APD on USG scan and deteriorated graft functions (3.7 mg/dL serum creatinine, 13 mL/min/1.73 m² eGFR). A double J stent insertion was performed urgently; subsequently, graft functions returned to baseline levels within 2 days. Preoperative medical records revealed that the donor had no symptoms prior to nephrectomy. However, the donor had grade 1 pelvicalyceal dilatation on USG scan, minimal disrupted urine flow to the ureter with a Tmax of 18.5 minutes and 53% split function in DTPA scan, and the accessory artery to the lower pole on CT scan. In addition, transplant surgery records revealed that the main renal artery was anastomosed to the common iliac artery, and the accessory lower pole artery was anastomosed to the external iliac artery.

In the diagnostic process, URS/RPG was prefer-red and revealed a suspected extrinsic obstruction in the UPJ but no stricture in the UV junction (Figure 1D). Therefore, a double J stent was reinserted, and the patient was scheduled for open reconstruction. During open surgery, the renal pelvis was dilated and the proximal ureter was crossed by the lower pole accessory, which caused extrinsic obstruction in the UPJ. The ureter was dissected and transected from the UV level and placed above the lower pole artery. The Y-V pyeloplasty and redo-UNC were performed according to the Paquin technique (Figure 2).

Analyses of patient data
Clinical data during preoperative and postoperative periods are summarized in Table 2. Although graft function (serum creatinine and serum eGFR) worsened significantly (P = .03) in the symptomatic period of UPO in all patients, it improved rapidly to levels similar to baseline (P = .07) after Y-V pyeloplasty. Moreover, we detected no statistically significant difference between baseline and long-term graft function in any patients (P = .28).

Complications
In the follow-up period, no complication required radiological or surgical interventions. Patient 3 and patient 4 developed urinary tract infections after Y-V pyeloplasty (Clavien-Dindo grade 2), which were treated with antibiotherapy.

Discussion

Currently, the diagnosis of UPO remains challenging because of its rarity and lack of an ideal diagnostic tool. Especially in transplanted kidneys, diagnosis and management of UPO are complex and require meticulous evaluation. To date, few potential causes have been described, such as denervation of the graft, severe fibrosis, prior subclinical UPO in donor kidney, and extrinsic obstruction via a crossing vessel. Additionally, the type of donor nephrectomy (open and laparoscopic approach) has been charged for ureteral complications at the beginning of laparoscopic era; however, recent studies have concluded that the laparoscopic approach preserves the vasculature and thereby reduces subsequent ureteral pathologies with increasing experience.^3,15,16 Nevertheless, a precise diagnostic tool or a treatment algorithm has not been established.^7,8,12 In the present study, we aimed to present the potential causes and clinical variations in diagnosis of UPO and investigate the short-term and long-term outcomes of Foley Y-V pyeloplasty.

Many studies and reported cases have inves-tigated the possible causes and duration between KT and UPO in graft kidneys. Shoskes and colleagues⁹ stated that ureteral obstruction occurs most often within 3 months of KT and reported a case with a lower pole vessel that caused a UPO in the early period, which was treated with division of the vessel. In contrast, George and colleagues¹⁷ and Doehn and colleagues18 have published case studies that revealed late occurrence of UPJD (6 months and 2129 days, respectively) caused by severe fibrosis. In addition, Shabtai and colleagues7 have presented a case of Y-V pyeloplasty that was suspected to be UPO prior to KT and revealed progression in 6 months. On the other hand, a recent study has shown that prior UPO of the renal allograft had a negligible effect on graft functions.¹⁹

In the present study, patient 1 was diagnosed with UPO in month 37 after KT due to severe fibrosis in periureteral tissue. Patient 2 was diagnosed in month 5 after KT and underwent open reconstruction, which revealed severe fibrosis and angulation of UPJ due to medially rotated graft in transverse axis. We assume that rotation of the graft caused kinking and/or angulation in the UPJ, which may have aggravated the obstruction in the UPJ, especially in combination with severe fibrosis.

To the best of our knowledge, no study has highlighted the effect of graft placement on UPO. Patient 3 and patient 4 were identified as having early occurrence of UPO due to rapid graft dete-rioration subsequent to stent removal. Although a crossing vessel causing extrinsic obstruction and subclinical UPO in the donor kidney were detected in patient 4, fibrosis and other potential causes such as denervation and insufficient blood supply were identified in patient 3. To date, studies have not identified a reliable etiological factor to predict late or immediate onset of UPO. While an external crossing vessel or local ischemia may cause immediate onset of UPO, fibrotic differentiation may reveal late onset of UPO in immunocompromised individuals. However, there are many unclear factors, such as denervation and existence of prior subclinical UPO, that could cause obstruction in the short-term or long-term. According to our experience, multiple factors may trigger the process, and it remains difficult to determine the exact etiology in such cases.

Diagnosis of UPO remains difficult for clinicians due to rare prevalence and absence of a precise diagnostic tool. For many years, conventional imaging techniques, such as USG, CT, and intravenous pyelography, have been used; however, the diuretic renogram has been introduced in recent years as a game changer. Despite its popularity, discrepancies in repeated scans and equivocal results of 15% to 17% in patients has undermined the reliability of such tools.⁷ In our study, the diagnostic process for patient 1 and patient 2 included DTPA scans. However, patient 3 and patient 4 had rapid deterioration in graft function, which led to urgent intervention; therefore, URS/RGP or antegrade pyelography through percutaneous nephrostomy to allow urgent stenting was preferred. In addition, these inter-ventions may enable the evaluation and discri-mination of potential ureteral pathologies and UPJ obstruction, which may cause deceptive results in DTPA scans.

Although well-established surgical procedures such as Anderson-Hynes dismembered pyeloplasty, Foley Y-V pyeloplasty, and uretero-native pyelo-ureterostomy have been described and used for several years, none of these has been recommended as a superior technique. Additionally, in recent years, minimally invasive endoscopic interventions, such as balloon dilation and UPJ incision with a hooked knife or with a laser, have demonstrated promising results.^9,12,13 In contrast, Krajewski and colleagues11 and Shoskes and colleagues⁹ reported cases of open reconstruction following failed endoscopic procedures.

In our series, open reconstruction was preferred over endoscopic procedures due to potential severe fibrosis in periureteric tissue causing angulation of UPJ and/or crossing vessel obstructing the UPJ. Thus, improvements in graft function have been achieved rapidly, and additional interventions have been avoided. Moreover, no conclusions have been made regarding the advantages or potential risks of pyeloplasty techniques in the literature. Branches of renal artery that supply the renal pelvis have been shown to also supply the adjacent part of the proximal ureter and the UPJ with the adventitial vascular plexus and descending branches.²⁰ Hence, excessive dis-section of the UPJ and adjacent structures, the so-called “golden triangle”, may damage the blood supply.²¹ In addition, revascularization of the ureter seems quite difficult in such immunocompromised patients. Therefore, in kidney transplants, the transection of the ureter during the dismembered technique seems more likely to damage the vasculature and carries very high risk for insufficient blood supply to the UPJ. To avoid such risks, the nondismembered Foley Y-V pyeloplasty technique, which allows preser-vation of vascular structures around UPJ with minimal dissection, was preferred over the dismembered technique, even though it required redo-UNC (patient 4).

The main limitations of our study are the retrospective design, the small group of patients due to rarity of UPO in grafts, and the absence of patients who had undergone endoscopic intervention and dismembered pyeloplasty. Therefore, we were not able to properly compare the mentioned techniques. In addition, follow-up periods subsequent to definitive surgery were relatively brief in 2 cases, which may have influenced the strength of the present study significantly. Furthermore, the specific mechanism to determine late or immediate onset of UPO was not identified in all cases, although whole potential etiological factors have been evaluated.

Conclusions

Diagnosis and management of UPJD in kidney transplants are extremely challenging due to rare prevalence, lack of an ideal diagnostic tool, and the invasive nature of treatment options. The diagnostic process should include evaluation of concomitant ureteral pathologies, and no imaging modality is reliable and discriminative for UPJD solely. Nondismembered Foley Y-V pyeloplasty is safe for graft functions in the short-term and long-term, and it is the proper pyeloplasty technique in graft kidneys. More comprehensive and prospective studies are needed to address proper management algorithms.

References:

1. Purnell TS, Auguste P, Crews DC, et al. Comparison of life participation activities among adults treated by hemodialysis, peritoneal dialysis, and kidney transplantation: a systematic review. Am J Kidney Dis. 2013;62(5):953-973. doi:10.1053/j.ajkd.2013.03.022
   CrossRef - PubMed
2. Wolfe RA, Ashby VB, Milford EL, et al. Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. N Engl J Med. 1999;341(23):1725-1730. doi:10.1056/NEJM199912023412303
   CrossRef - PubMed
3. Davari HR, Yarmohammadi H, Malekhosseini SA, Salahi H, Bahador A, Salehipour M. Urological complications in 980 consecutive patients with renal transplantation. Int J Urol. 2006;13(10):1271-1275. doi:10.1111/j.1442-2042.2006.01539.x
   CrossRef - PubMed
4. Praz V, Leisinger HJ, Pascual M, Jichlinski P. Urological complications in renal transplantation from cadaveric donor grafts: a retrospective analysis of 20 years. Urol Int. 2005;75(2):144-149. doi:10.1159/000087169
   CrossRef - PubMed
5. Whang M, Benson M, Salama G, et al. Urologic complications in 4000 kidney transplants performed at the Saint Barnabas health care system. Transplant Proc. 2020;52(1):186-190. doi:10.1016/j.transproceed.2019.10.008
   CrossRef - PubMed
6. Krol R, Ziaja J, Chudek J, et al. Surgical treatment of urological complications after kidney transplantation. Transplant Proc. 2006;38(1):127-130. doi:10.1016/j.transproceed.2005.12.100
   CrossRef - PubMed
7. Shabtai M, Nativ O, Dreznik Z, Jacob ET. Decompensated ureteropelvic junction obstruction in renal allograft. J Urol. 1988;139(3):578-579. doi:10.1016/s0022-5347(17)42532-8
   CrossRef - PubMed
8. Venkatramani V, Mukha RP, Kekre NS. Equivocal pelvi-ureteric junction obstruction manifesting in a renal transplant recipient. Indian J Urol. 2012;28(3):350-352. doi:10.4103/0970-1591.102727
   CrossRef - PubMed
9. Shoskes DA, Hanbury D, Cranston D, Morris PJ. Urological complications in 1000 consecutive renal transplant recipients. J Urol. 1995;153(1):18-21. doi:10.1097/00005392-199501000-00008
   CrossRef - PubMed
10. Ho TP, El-Sheikh MF, Talbot D. Case report: living related renal transplantation with a donor kidney with pelviureteric junction obstruction using an Anderson-Hynes pyeloplasty. Transplant Proc. 2002;34(4):1193-1194. doi:10.1016/s0041-1345(02)02633-7
    CrossRef - PubMed
11. Krajewski W, Dembowski J, Kolodziej A, et al. Urological complications after renal transplantation: a single centre experience. Cent European J Urol. 2016;69(3):306-311. doi:10.5173/ceju.2016.833
    CrossRef - PubMed
12. Schumacher M, Studer UE, Danuser H. Antegrade endopyelotomy for treatment of ureteropelvic junction obstruction in transplanted kidneys. J Endourol. 2006;20(5):305-308. doi:10.1089/end.2006.20.305
    CrossRef - PubMed
13. Yildirim UM. Double-puncture technique for management of severe ureteropelvic obstruction in kidney transplant. Exp Clin Transplant. 2022;20(10):950-953. doi:10.6002/ect.2020.0184
    CrossRef - PubMed
14. Paquin AJ Jr. Ureterovesical anastomosis: the description and evaluation of a technique. J Urol. 1959;82:573-583. doi:10.1016/S0022-5347(17)65934-2
    CrossRef - PubMed
15. Altinel M, Acikgoz O. Standardization of laparoscopic donor nephrectomy technique in minimizing ureteral complications in renal transplant recipients: 10-year experience of a single center. Transplant Proc. 2023;55(5):1116-1120. doi:10.1016/j.transproceed.2023.02.065
    CrossRef - PubMed
16. Lind MY, Hazebroek EJ, Kirkels WJ, Hop WC, Weimar W, Ijzermans JN. Laparoscopic versus open donor nephrectomy: ureteral complications in recipients. Urology. 2004;63(1):36-39. doi:10.1016/j.urology.2003.07.025
    CrossRef - PubMed
17. George K, Gopalakrishnan G, Al-Mamari SA, Viswaroop SB. Late occurrence of pelvi-ureteric junction obstruction in renal allograft and live-related kidney donor. Saudi J Kidney Dis Transpl. 2019;30(6):1464-1469. doi:10.4103/1319-2442.275495
    CrossRef - PubMed
18. Doehn C, Bose N, Meyer AJ, Jocham D. Results of secondary ureteral implantation after kidney transplantation. Int Urol Nephrol. 2011;43(3):669-674. doi:10.1007/s11255-010-9893-6
    CrossRef - PubMed
19. Tisljar M, Ali H, Gledhill-Flynn C, Garreus M, Ponnusamy A, Ahmed A. The outcome of kidney transplant from living donors with pelvi-ureteric junction dysfunction. Int Urol Nephrol. 2020;52(10):1863-1868. doi:10.1007/s11255-020-02522-x
    CrossRef - PubMed
20. Frober R. Surgical anatomy of the ureter. BJU Int. 2007;100(4):949-965. doi:10.1111/j.1464-410X.2007.07207.x
    CrossRef - PubMed
21. Keller H, Noldge G, Wilms H, Kirste G. Incidence, diagnosis, and treatment of ureteric stenosis in 1298 renal transplant patients. Transpl Int. 1994;7(4):253-257. doi:10.1007/BF00327152
    CrossRef - PubMed