Objectives: A ureteric stent is routinely placed to minimize urological complications during kidney transplant. However, some complications may occur in association with the ureteric stent, such as urinary tract infections, and the optimal duration for stent placement is unclear. We reviewed the outcomes following early simultaneous removal of the ureteric stent with the urethral catheter in pediatric kidney transplant recipients.

Materials and Methods: We reviewed all kidney transplants from January 2009 to January 2019. The data we collated included demographics, donor and recipient characteristics, and perioperative details, including urological complications, stent-related complications, and kidney graft function. The financial cost of late stent removal was calculated. The early stent removal group was defined as 5 days, and the late removal group was about 4 to 6 weeks. The median follow-up time was 60 months (interquartile range, 31.5-91 months).

Results: There were 32 transplants in 31 patients during the study period (early vs late group = 23:9). No urine leak occurred in either group. One patient in the early group developed distal ureteric stenosis, and this condition was managed with interventional balloon dilatation. The median time for stent removal was 6 days in the early group and 39 days in the late group. There were 5 episodes of symptomatic urinary tract infections in 3 patients in the early group and 10 episodes of symptomatic urinary tract infections in 3 patients in the late group. The mean estimated glomerular filtration rate at 12 months was comparable between the 2 groups (84 ± 54 vs 64 ± 21 L/min/1.73 m²; P = .3). The average cost for each early removal was A$772.65 compared with the late group.

Conclusions: Early simultaneous removal of the ureteric stent with the urethral catheter in pediatric kidney transplant recipients is feasible, safe, and cost-effective.

Key words : Indwelling urethral catheter, Pediatric kidney transplant, Simultaneous removal, Ureteric stent

Introduction

Kidney transplant is the optimal treatment for patients with end-stage kidney disease. Long-term outcomes of kidney transplant have improved steadily as a result of improvements in surgical techniques, better diagnostic tools, and advances in immunosuppression. However, urological complica­tions such as urine leak and ureteric stenosis remain common complications with incidence rates of 0% to 2% and 5% to 8%, respectively, which may lead to graft loss or mortality.^1-4

Placement of a ureteric stent at ureteroneocys­tostomy has been proven to reduce major urological complications significantly.^1,2,5-7 The stent is usually removed by cystoscopy around 4 to 6 weeks after transplant,8 and the timing for ureteric stent removal is balanced between the time for anastomotic healing and the avoidance of stent-related complications.^1,9 In pediatric kidney transplant recipients, cystoscopy and removal of the ureteric stent requires a general anesthetic.¹ The longer the stent remains in place, the greater the risk to the patient for complications such as urinary tract infections (UTI). A randomized controlled trial (the Transplant Ureteric Stent Trial) showed a significant reduction of stent-associated complications by early removal of the ureteric stent on day 5.8 Moreover, some studies have found an association between ureteric stent placement and BK virus infection and nephropathy.^9-12

Evidence for early removal of the ureteric stent in pediatric transplant recipients remains sparse.^1,6,7,9 The aims of this study were to evaluate (1) the safety and feasibility of early removal of ureteric stents in pediatric transplant recipients, (2) the complications associated with early ureteric stent removal, and (3) the cost-effectiveness associated with early removal of the ureteric stent.

Materials and Methods

This study was approved by the hospital human research ethics committee as a quality improvement project (QI 23721) and was conducted in accordance with Declaration of Istanbul.¹³ Using a prospective hospital register, we conducted a retrospective review of all cases of pediatric kidney transplant performed between January 2009 to January 2019 at Perth Children’s Hospital (formerly Princess Margaret Hospital for Children). Perth Children’s Hospital is the sole pediatric transplant center for the state of Western Australia. Pediatric recipients were defined as those aged 18 years old or less at transplant. The patients were divided into 2 groups, ie, early ureteric stent removal and late ureteric stent removal, defined according to the timing of stent removal. The early group (EG) was defined as the simultaneous removal of the ureteric stent with the indwelling urethral catheter (IDC) on day 5 posttransplant prior to hospital discharge. The late group (LG) was defined as removal of the ureteric stent at 4 to 6 weeks posttransplant under general anesthesia by cystoscopy as a day procedure, asynchronous to the previous removal of the IDC.

Surgical technique and perioperative care
All kidney transplants were performed by conven­tional open surgery. For recipients weighing over 20 kg, the renal artery was anastomosed in end-to-side fashion to the common/external iliac artery, and the renal vein was anastomosed in an end-to-side fashion to the external iliac vein. For recipients weighing less than 20 kg, the renal vein was anastomosed to the distal part of inferior vena cava, and the renal artery was anastomosed to the side of distal part of aorta. A modified Lich-Gregoir technique was used for ureteroneocystostomy.¹⁴ A ureteric stent (4.8-6F, 12 cm long; Cook Medical) was routinely placed during kidney transplant. In EG, the ureteric stent was connected to the tip of the IDC by a 4-0 polydioxanone suture string during kidney transplant (Figure 1); as such, the stent removal was simultaneous with IDC removal on day 5 posttransplant. In contrast, in the LG the ureteric stent was not connected to the IDC; therefore, for the LG the IDC was routinely removed on day 5 posttransplant, whereas the stent was removed around 4 to 6 weeks posttransplant by cystoscopy under general anesthesia. Doppler ultrasonography of the kidney graft was performed on day 1 posttransplant and was repeated when there was a deterioration in kidney graft function.

Data collection, analyses, and definitions
Data collection included basic demographics, primary cause of renal failure, type of renal replacement therapy (hemodialysis vs peritoneal dialysis), donor characteristics, date of transplant, intraoperative and postoperative variables, timing of ureteric stent removal, episodes of UTI and its associated hospital admissions, number of episodes of BK viremia/nephropathy with its management, and follow-up biochemistry and imaging results. All recipients were followed up per hospital transplant protocol.

The diagnosis of UTI was made if the patient presented with any symptoms of dysuria, frequency, and urgency with midstream urine bacterial cultures of > 106 colony-forming units per liter.8 Data on urine cultures were collected up to 3 months posttransplant.

The BK virus screening was performed using quantitative nucleic acid testing in plasma by commercially available assays. This occurred weekly for the first 3 months after transplant, then monthly thereafter. BK viremia was defined as > 104 copies/mL. All patients with a concurrent rise in serum creatinine also underwent transplant biopsy, and BK nephro­pathy was diagnosed and graded according to the Banff criteria.¹¹

Graft function was monitored by periodic measurement of serum creatinine. The estimated glomerular filtration rate was calculated at 12 months according to the modified Schwartz equation.¹⁵

The finance department of the hospital calculated the financial costs for the following items, according to the policies of the Independent Hospital Pricing Authority: cystoscopy with removal of ureteric stent, general anesthesia, and a day admission.

Statistical analyses
Continuous variables were expressed as median values with interquartile ranges (IQR). Categorical variables were expressed as count and proportion. Between-group differences were tested for statistical significance by the chi-square test for categorical variables or the Mann-Whitney test for continuous variables. A 2-sided P value of < .05 was considered significant. SPSS version 16.0 was used for statistical analyses.

Results

From January 2009 to January 2019, a total of 31 patients underwent 32 kidney transplants. The median follow-up time was 60 months (IQR, 31.5-91 months).

There were 23 patients (18 males, 5 females) in the EG and 9 patients (9 males, 0 females) in the LG. The median age was 10 years in the EG (IQR, 5-15 years) and 12 years in the LG (IQR, 6-15.5 years). In the EG, 10 patients received deceased donor transplants and 13 patients received living related donor transplants (first degree); in the LG, there were 3 patients with deceased donors and 6 patients with living related donors (first degree) (Table 1). The primary cause of renal failure in both groups is summarized in Table 2. Five patients had a previous vesicotomy, and 2 patients had a previous Mitrofanoff procedure (Table 1). In the EG, 4 patients received hemodialysis, 10 received peritoneal dialysis, and 9 received a preemptive kidney transplant. In the LG, 1 patient received hemodialysis, 4 received peritoneal dialysis, and 4 received a preemptive kidney transplant.

Postoperative urological complications
No urine leak occurred in either group. One patient in the EG (11-year-old male) developed distal ureteric stenosis. The ureteric stent was removed on day 5 posttransplant. The serum creatinine was elevated (from 41 to 61 μmol/L) on day 14, and Doppler ultrasonography showed hydronephrosis on day 16 after ureteric stent removal. Percutaneous nephrog­raphy confirmed a distal ureteric stenosis (6 mm in length on fluoroscopy). Interventional balloon dilatation (5-mm × 2-cm balloon) was performed, and a ureteric stent (4.8F) was placed by antegrade approach. The ureteric stent was then removed 6 weeks later. The serum creatinine rebounded to 107 μmol/L at 2 days after the removal of the second stent, which required repeat percutaneous nephrog­raphy and interventional balloon dilatation (8-mm × 2-cm cutting balloon) with antegrade placement of a ureteric stent (4.8F). The ureteric stent remained in situ for 3 months before removal. The kidney graft function remained stable after that time, with serum creatinine at 70 μmol/L for 24 months of follow-up and no signs of hydronephrosis on repeat ultrasonography.

Timing of stent removal and stent-related complications
The median time of stent removal in the EG was 6 days after placement (IQR, 3-11 days) versus 39 days in the LG (IQR, 18-49 days). The ureteric stent and the IDC were successfully and simultaneously removed on the ward in 23 patients (85%). In the LG cases, 5 patients had planned late stent removal with peritoneal dialysis catheter and 4 patients had unsuccessful early removal due to protracted hematuria (n = 1) or difficulty with removal due to complaint of pain (n = 3). In these 4 cases, the suture string was divided and the ureteric stent was left in situ at the time of IDC removal.

The ureteric stent was removed later (in 4-6 weeks) by cystoscopy under general anesthesia. There were no other stent-related complications in either group.

Urinary tract infection within 3 months posttransplant and BK infection posttransplant
There were 5 episodes of symptomatic UTI in 3 EG patients, and all 5 episodes required hospital admissions. There were 10 episodes of symptomatic UTI in 3 LG patients, and all 10 episodes required hospital admissions. Two of the 3 EG patients with UTI tested positive for a single microorganism (Enterococcus faecalis or Proteus mirabilis), and the third patient tested positive for 2 microorganisms (Klebsiella oxytoca and coagulase-negative Staphylococcus). Two of the 3 LG patients with UTI tested positive for a single microorganism (Enterococcus faecalis or Escherichia coli), and the third patient tested positive for multiple micro­organisms (Enterobacter sp, Pseudomonas sp, and Enterococcus sp). None of the patients required removal of the ureteric stent to mitigate UTIs.

In each group, 2 patients developed BK viremia (8.7% for EG and 22.2% for LG; P = .557). Two EG patients developed biopsy-proven BK nephropathy at 6 and 8 months posttransplant; both of these patients were treated with intravenous human immunoglobulin and a reduction in immunosup­pression to good effect, with clearance of plasma BK and resolution of nephropathy on biopsy. Two LG patients developed BK viremia and were monitored closely and did not develop BK nephropathy on renal biopsy, and follow-up blood tests were negative for BK virus.

Long-term graft function
The median estimated glomerular filtration rate at 12 months was 72 mL/min/1.73 m² in the EG patients (IQR, 50-112 mL/min/1.73 m²) compared with 58 mL/min/1.73 m2 in the LG patients (IQR, 46-79 mL/min/1.73 m²) (P = .35).

During follow-up, 1 patient died with a func­tioning graft 2 years after transplant, from cerebral venous thrombosis. One patient had graft loss due to renal vein thrombosis and underwent the second kidney transplant without further complications during the study period.

Financial cost for ureteric stent removal in the late group
In the EG patients the ureteric stent removal on the ward was simultaneous with the IDC removal. In the LG patients the average cost for each case was calculated to be A$772.65, which consisted of the costs of cystoscopy and removal of the ureteric stent, general anesthesia, and day admission (Table 3).

Discussion

This 10-year retrospective review indicates that early simultaneous removal of the ureteric stent with the IDC at day 5 after kidney transplant is feasible and safe without an increase in the major urological complications in pediatric recipients. Most importantly, this approach is cost-effective because there is no need for the additional procedure of cystoscopy and general anesthesia with a day admission.

The best practice for the timing of ureteric stent removal after kidney transplant remains contro­versial. In most transplant units, the stent is removed about 4 to 6 weeks posttransplant. Three methods for early removal have been described in the literature. In 1998, Morris-Stiff and colleagues described a simple method for early removal of the ureteric stent by suturing the tip of the stent to the tip of IDC so that the stent and the IDC could be removed simultaneously in a single procedure.¹⁶ In their study, 15 recipients were included with a median age of 48 years (IQR, 18-68 years). The stent and IDC were simultaneously removed at 6 to 10 days (median 8 days) posttransplant. There were no indications of urinary sepsis or urological complications. This technique has also been adopted by other centers with satisfactory results (incidence of UTI was 7.6% vs 24.6%; P = .004; and urine leak and/or ureteric stenosis was 3.75% vs 0.8%; P = .36).⁸ Another method was also described, in which the string was tethered to the distal end of the ureteric stent and remained in situ in the bladder; later, the ureteric stent could be removed in an outpatient setting when the string was seen at the external meatus.¹⁷ However, this method is unreliable, with high risk of accidental dislodgement while bathing or voiding, with incidence reported up to 15% and with higher risk in females (25%).¹⁷ The third method was described Insall and colleagues as external drainage stent,¹⁸ for which the ureterovesicular stent remained in place to drain percutaneously.¹⁸ In a study by Simpson and colleagues, they found significantly greater risk of ureteral obstruction (up to 33.3%) with the external drainage stent compared with the first method; therefore, they switched to the first method and observed a significant reduction in ureteral obstruction (6.25%).⁷ Vogel and colleagues also showed higher rates of urine leak (14%), ureteric stenosis (7%), and ureteric necrosis (2.33%) in the external drainage group compared with none in the other group with conventional ureteric stent.19 The external drainage method also has a theoretical increased risk of UTIs because the stent exit acts as an entry point for microorganisms. However, no significant difference in rate of UTI incidence was observed in the 2 studies.^7,19

The optimal duration for ureteric stent placement remains controversial. It is understood that the ureteric stent should be removed as early as possible to reduce the risk of stent-related complications including infection, encrustation, and irritation, as well as the possible risk of forgetfulness regarding the presence of the ureteric stent (and subsequently retention of the stent for a longer duration than planned).^2,4,7 However, the definition of “early” with regard to ureteric stent removal is not well-documented in the literature and varies between 5 days to 3 weeks, dependent on the method of removal.^1,4,8,11 The IDC is routinely placed for kidney transplant to provide distension of the bladder for ureteroneocystostomy and capability to monitor urine output during the immediate posttransplant period. The duration of IDC varies among transplant units and ranges between 3 and 7 days prior to discharge. This situation represents an opportunity to simultaneously remove the ureteric stent with the IDC. In our present study, the early removal of the stent was intended at day 5 posttransplant, to be simultaneous with the removal of the IDC. There were cases for which the procedure was delayed because of weekends/public holidays. Another cause for unplanned delayed removal of the ureteric stent, asynchronous to the early removal of the IDC, was due to the pain as the ureteric stent was caught up with the string. This situation could be resolved by cutting the suture string to leave the ureteric stent in place during the IDC removal. In such cases, the ureteric stent could be removed by cystoscopy at a later time, as a separate procedure.

Recently, some studies have evaluated the timing of ureteric stent removal to discover the earliest appropriate opportunity that would best avoid risk for major urological complications, such as urine leak and ureteric stenosis, which were reported to be 0% to 2% and 5% to 8%, respectively.^3,4,20 One study that investigated the safety of early ureteric stent removal (mean time 10 days) versus later removal of the ureteric stent showed significantly lower rates of urine leak in early removal (0.3% vs 2.6%; P < .001) but no significant difference in ureteric stenosis (1.5% vs 1.2%).²¹ In our cohort, there were minimal urological complications in both groups of patients (EG and LG). The only case of distal ureteric stenosis resolved satisfactorily after radiological intervention. It was shown that symptomatic UTI was more common (15.1% vs 2.5%) in the late removal of the ureteric stent (median 42 days).8 A study of 129 pediatric recipients demonstrated that the placement of a ureteric stent was associated with higher incidence of UTI (83.3% vs 52.9%; P = .0399), whereas the major urological complications (urine leak and ureteric stenosis) were reduced in the ureteric stent group (1.55%) compared with the group where the ureteric stent was not used for kidney transplant (54.2%).9 On the contrary, another study showed no correlation between the occurrence of UTI and duration of the ureteric stent.⁷ However, those studies were limited by the small numbers of cases and a different definition of UTI. In our study, late removal of the ureteric stent was associated with a tendency toward symptomatic UTI hospital presen­tations versus early removal, although there was no difference in hospital admissions. The overall incidence of symptomatic UTI was 18.75%, which is in the lower range in comparison with the literature (18% to 38.7%).²² This would potentially improve long-term graft survival because UTIs among hospitalized patients are associated with higher risk for graft loss.^23,24 In addition, late removal of the ureteric stent could predispose pediatric recipients to higher risk for potential stent-related complications such as pain, hematuria, and stent encrustation.^1,3,5,8

The early removal of the ureteric stent may potentially reduce the risk of BK virus infection.¹⁰ It has been proposed that pathogenesis of BK nephropathy may be related to urothelial injury due to placement of a ureteric stent and administration of immunosuppression that may lead to reactivation and replication of BK virus.^10-12 Pediatric recipients are more susceptible to these risks than are adults because children are less likely to have acquired prior immunity.⁹ Hence, early removal of the ureteric stent may reduce the risk of BK virus reactivation. However, we cannot conclude that a correlation exists between early removal of ureteric stent and BK infection from this study because of the small cohort size and the low incidence of BK infection.

Our present study was retrospective in nature, and the usual caveats apply. The sample size was small, and thus the analyses presented here are mainly descriptive in nature.

Our findings support the implementation of early removal of the ureteric stent at day 5 posttransplant in pediatric recipients. This method is feasible, safe, and easily adopted. Early removal is also cost-effective because it avoids a day admission for a procedure of cystoscopy and removal of ureteric stent under general anesthesia, which has potential risk for negative effects on neurodevelopment.²⁵

Conclusions

Early simultaneous removal of the ureteric stent with the IDC at day 5 is feasible and safe in pediatric kidney transplant recipients without higher risk of major urological complications. It is also cost-effective because the early removal approach does not require the additional procedure of cystoscopy under general anesthesia.

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