Renal failure was an important cause of mortality in the past decades1 for patients suffering from a lower urinary tract malformation (LUTM). Despite the first report of a renal transplantation on an ileal urinary diversion by Kelly in 1966,2 patients with a congenital LUTM were excluded from renal transplantation programs because of bladder dysfunction and the infectious risk for the graft. Improvements on primary bladder rehabilitation and surgical repair of the bladder expanded access to transplantation for such patients. Only few studies have described renal transplantation in LUTM, with conflicting results.
The aim of this study was to analyze technical aspects and results of renal transplantation in patients with LUTM.
MATERIALS AND METHODS
We conducted a descriptive, retrospective multicenter study in 3 French renal transplantation centers (Montpellier, Lyon, and Nantes). From January 1, 1996, to September 1, 2016, 123 renal transplantations were performed on 112 patients with LUTM.
We included patients with spina bifida (21), bladder exstrophy (14), urogenital sinus (4), posterior urethral valves (PUV) (49), Eagle-Barrett syndrome (prune belly) (12), central neurogenic bladders (13), Hinman syndromes (6), and acquired neurologic bladders (4).
We excluded upper urinary tract malformations.
Data were collected from a French multicenter DIVAT (Données Informatisées et VAlidées en Transplantation) database, after approval from the regional ethics committee (DC-2011-1939). A preliminary consent from patients regarding collection and data processing was obtained and anonymous data exploitation was done. Data were protected by French Information Commissioner’s Office for data privacy declaration (Commission nationale de l'informatique et des libertés [CNIL] No. 891735).
For the statistical analysis, we pooled patients in groups depending on their urinary rehabilitation. Group 1 contained bowel or ureteral bladder augmentations, group 2 contained continent diversions, group 3 contained incontinent diversions, and group 4 contained native bladders.
The main objective of the study was to analyze graft and patient survival. We defined renal transplant loss by return to dialysis or new preemptive transplantation. Secondary objectives were infectious, urological, vascular, parietal, and metabolic complications.
Quantitative data were analyzed by unilateral Student’s t test. Qualitative data were analyzed by a χ2 test. A P value of <0.05 was considered as significant. Graft survival was measured from the time of transplantation to event occurrence. Any patient death was considered as an event. Patients without an event were considered well until last known date. Graft and patient survival curves were built using a Kaplan-Meier model.
Mean age at transplantation was 32.1 years old (y/o) (±11.2). Twenty-six transplantations were preemptive (21.1%). Mean time of dialysis was 43.3 months (±57.1). A first transplantation was performed in 69.9% of cases, a second in 23.6% of cases, and a third in 6.5% of cases. There was an HLA-immunization or hyperimmunization in 37.4% of cases. Residual diuresis (>300 cc/24 h) was present in 50.4% of cases (Table 1).
Group 1 included 14 transplantations in 13 ileal or colic cystoplasties and 1 ureteroplasty. Group 2 included 15 transplantations into a continent diversion. Group 3 included 29 transplantations into an incontinent diversion. Group 4 included 65 transplantations into a native bladder.
Seven patients had a urological surgery during transplantation (5.6%) (6 incontinent diversions and 1 ileal bladder augmentation). Mean delay between surgery and transplantation was 14 years. A urodynamic evaluation before transplantation was performed on 39 patients (31.7%). Postvoid residual urine was not evaluated in 56.7% cases, it was nonsignificant (<150 cc) in 27.1% of cases and significant (>150 cc) in 16.1% of cases. Fifteen patients were on clear self intermittent catheterization (12.1%). Four patients used anticholinergic drugs (3.2%).
Most grafts came from deceased donors (79.7%). Donors’ mean age was 36.2 y/o (±15.3). Mean serum creatinine level was 84.9 μmol/L (±40.4). There were multiple kidney arteries in 24.2% of cases. There were 13 cardiac arrests (11.3%) with a mean low-flow time of 23 minutes (±15.3).
Technical Transplantation Aspect
A para-rectal Gibson incision was made in most cases (71.4%), and a median approach for continent or incontinent derivation and for third transplantation. Mean cold ischemia time was 17.7 hours (±11.1) and mean vascular anastomosis time was 34.0 minutes (±10.8).
Concerning urinary continuity, a ureteral graft implantation into the native bladder (even in the case of bladder augmentation) was done in 53.3% of casess. Uretero-neobladder anastomosis on bowel segment was done in 8.3% of cases. An uretero-ureteral anastomosis was done in 19.2% of cases. For ileal incontinent derivation (16.7%), a non-antireflux anastomosis with direct ureteral implantation in the bowel segment was done in all cases.
Concerning the antireflux technique on the bladder or neo-bladder anastomosis (61.6%), 50.4% were a Lich-Gregoir anastomosis, 5% were a Leadbetter-Politano anastomosis, and 2.5% were a Paquin technique. In 3.4% of cases the technique was not described.
There was an immediate diuresis without posttransplantation dialysis in 71.1% of cases. For others, there was a mean number of dialysis of 1.8.
The immunosuppressive treatment was tacrolimus in 89 patients (75.4%), Cyclosporine in 24 patients (20.3%), and mTOR inhibitors in 5 patients (4.2%).
The mean follow-up time after transplantation was 7.21 years. Of the total 123 transplants, 93 were still functional (75.6%). There were 22 graft losses for chronic reject (18,7%), 2 for urological complications (stenosis and trauma) (1,6%), and 5 for vascular complications (4.1%) (thrombosis and stenosis).
Overall Graft Survival
With a mean follow-up time of 7.21 years, graft survival at 1, 5, 10, 15, and 20 years was of 96.65%, 87.62%, 77.31%, 60.63%, and 36.43%, respectively. The median graft survival was 16.03 years.
The most recent mean creatinine level was 247 μmol/L (mean glomerular filtration rate [GFR] 46.2 mL/min/1.73 m2) for the 93 transplants that were still functional (75.6%) (Figure 1).
In a univariate analysis, absence of Clear Self Intermittent Catheterization (CSIC) (P = 0.038), expanded criteria donor (ECD) (P < 0,01), and surgical bladder management before the transplantation (P = 0.045) were influential factors of graft survival. In a multivariate analysis, CSIC was a protective factor of graft survival (hazard ratio, 0.334 [0.114–0.975]; P = 0.045; Table 2).
Overall Patient Survival
Twelve deaths were reported in this study, none considered being of surgical cause. There were 6 deaths for nonurological cancers, 2 vascular cerebral strokes, 1 digestive bleeding, and 3 indeterminate causes.
Overall patient survival at 1, 5, 10, and 15 years was of 97.48%, 93.01%, 89.39%, and 80.04%, respectively.
Results for Each Bladder Management
Group 1 included 14 transplantations on 14 patients with enterocystoplasty or ureterocystoplasty. With a mean follow up of 7.2 years, graft survival at 1, 5, 10, 15, and 20 years was of 100%, 89%, 74%, 74%, and 49.3%, respectively.
Group 2 included 15 transplantations on 14 patients with continent urinary diversion. With a mean follow up of 9 years, graft survival at 1, 5, 10, 15, and 20 years was of 100%, 100%, 83%, 75%, and 75%, respectively.
Group 3 included 29 transplantations on 28 patients with incontinent urinary diversion. With a mean follow up of 7.9 years, graft survival at 1, 5, 10, 15, and 20 years was of 100%, 89%, 74%, 74%, and 49.3%, respectively.
Group 4 included 65 transplantations on 57 patients on their native bladder. Before transplantation, 22 patients (33.8%) had a urodynamic study, 5 (7.6%) had a significant postvoiding volume, 9 (13.8%) were on self-catheterization, and 4 (6.1%) took anticholinergic drugs. With a mean follow up of 6.6 years, graft survival at 1, 5, 10, 15, and 20 years was of 96.76%, 84.07%, 69.97%, 51.38%, and 24.35%, respectively.
The Clavien-Dindo classification was used for postoperative complications. Postoperative dialysis requirement was not classified as a grade 4a complication. There were no complications for 64.3% of cases, grade 1 complications for 29.7% of cases, grade 2 complications (blood transfusion) for 4.9% of cases, grade 3b complications (surgical revision) for 16.8% of cases, and grade 4b complications (needed resuscitation care) for 2.9% of cases.
Acute Graft Pyelonephritis
Mean hospitalization for acute graft pyelonephritis was 2.15 stays for group 1, 2.13 stays for group 2, 0.84 stays for group 3, and 0.81 stays for group 4. Enterocystoplasty and continent urinary diversions exposed grafts to more frequent acute pyelonephritis with a significant P value (P = 0.02). In a multivariate analysis, the absence of a postvoiding residual volume was the only good prognostic factor of pyelonephritis occurrence with hazard ratio of 0.118 (−1.05 to 0.751; P = 0.047; Table 3).
Despite incidence of acute graft pyelonephritis, there was no statistical difference on graft survival when transplantation was performed in enterocystoplasty or continent urinary diversion compared with a native bladder (P = 0.06; Figure 2).
There were 5 urinary fistulas (4,1%), including 3 that needed a surgical revision. Eleven urinary stenoses (8.9%) appeared with a mean delay of 12.8 months (±25.6). Five stenoses needed a surgical revision and 6 were treated by endoscopy. There was no statistical difference in stenosis occurence between groups.
There were 2 venous thromboses (1.62%) and 2 arterial thromboses (1.62%). Four arterial stenoses (3.27%) appeared with a mean delay of 34 months (±42.4) after transplantation. Five grafts were lost because of a vascular complication. There was no statistical difference between groups.
There was 1 digestive fistula (0.8%) and 1 peritonitis (0.8%). We reported 2 abdominal eviscerations (1.6%) and 5 abdominal eventrations (4.0%). There were 6 abdominal wall abscesses (4.8%) with 1 needing a surgical evacuation.
We reported no cases of urological cancer or enterocystoplasty oncological transformation. Concerning metabolic disorders, there were 7 hyperchloremic acidosis (14.5%), most of them concerning continent ileal derivation.
Six patients had pouch stones (4.8%), and in 4 cases, Kock pouch urinary diversion was treated by an endoscopic procedure.
Results for Each Urological Malformation
Posterior Urethral Valves
We reported 49 transplantations in 43 patients with PUV. Mean age at transplantation was 29.6 y/o (±11.2). Only 1 patient had enterocystoplasty. A urodynamic study before transplantation was conducted in only 30.6% of cases. Three patients had a significant (>150 cc) postvoiding residual volume (6.1%), and 3 patients had an anticholinergic treatment (6.1%).
Mean time on dialysis was 3.8 years (±5.1) and 16 transplantations were preemptive (32.6%). Initial transplantation was the case for 28 patients (57.1%), a second for 15 patients (30.6%), and a third for 6 patients (12.2%).
With a mean follow-up of 7.3 years, graft survival at 1, 5, 10, and 15 years was of 95.50%, 84.63%, 72.52%, and 56.79%, respectively. Mean creatinine level was 279 μmol/L (mean GFR 46.98 mL/min/1.73 m2).
We included 21 transplantations in 18 patients with Spina bifida. Mean age at transplantation was 35.4 y/o (±11.2). Initial transplantation was the case for 17 patients (80.9%), a second for 3 patients (14.2%), and a third for 1 patient (4.7%). Three patients had a native bladder, 1 had a colonic enterocystoplasty, 1 had an ileal enterocystoplasty, 1 had an ileo-colic cystoplasty, 1 had a continent ileal diversion, 1 had a continent colic diversion, and 2 had an ileo-colic continent diversion. The other 10 had an incontinent ileal diversion.
Mean time on dialysis was 3.9 years (±4.7) and 3 were preemptive transplantations (14.2%).
With a mean follow-up of 6.9 years, graft survival at 1, 5, 10, and 15 years was of 95.20%, 87.3%, 87.3%, and 37.4%, respectively. Mean creatinine level was 226.2 μmol/L (mean GFR 42.2 mL/min/1.73 m2).
We included 13 transplantations in 12 patients with central neurogenic bladder. Neurogenic bladder is not considered to be a LTUM but the bladder dysfunction is similar to spina bifida. Mean age at transplantation was 34.6 y/o (±11.4). Initial transplantation was the case for 11 patients (84.6%) and a second for 2 patients (15.3%).
There were 2 ileal enterocystoplasties, 1 ileo-colic enterocystoplasty, 1 ileal continent derivation, 2 appendico-vesicostomies, and 6 incontinent urinary diversions.
Mean time on dialysis was 5.1 years (±4.9) and 1 was a preemptive transplantation (7.6%).
With a mean follow up of 7.6 years, graft survival at 1, 5, 10, and 15 years was of 100%, 100%, 80%, and 53.3%, respectively. Mean creatinine level was 211 μmol/L (mean GFR 49.3 mL/min/1.73 m2).
Prune Belly Syndrome
We reported 12 transplantations in 10 patients with prune belly syndrome. Mean age at transplantation was 25.0 y/o (±11.6). Initial transplantation was the case for 6 patients (50%), a second for 5 patients (41.6%), and a third for 1 patient (8.3%). There were no preemptive transplantations. Ten patients had a native bladder, 1 had an appendico-vesicostomy on native bladder, and 1 had an incontinent ileal diversion.
Mean time on dialysis was 2.7 years (±5.0). With a mean follow up of 6.2 years, graft survival at 1, 5, 10, and 15 years was of 91.60%, 80.2%, 66.8%, and 22.2%, respectively. Mean creatinine level was 336.5 μmol/L (mean GFR 35.7 mL/min/1.73 m2).
There were 14 transplantations in 14 patients with bladder exstrophy. Mean age at transplantation was 42.8 y/o (±11.1). Initial transplantation was the case for 12 patients (85.7%) and a second for 2 patients (14.2%). Two patients have been transplanted on their reconstructed native bladder, 8 had an incontinent urinary diversion, 1 had an ureterocystoplasty, and 3 had a continent urinary diversion.
Mean time on dialysis was 2.9 years (±4.7) and 2 were preemptive transplantations (14.2%).
With a mean follow-up of 8.2 years, graft survival at 1, 5, 10, and 15 years were of 100%, 93.3%, 93.3% and 93.3%, respectively.
We reported 4 transplantations in 4 patients with a urogenital sinus malformation. Two patients had a bladder reconstruction with ileal augmentation, a bladder neck closure, and a continent Monti diversion. One patient had a continent ileal diversion by a Koch pouch, and 1 patient had an incontinent diversion. Mean age at transplantation was 21.5 y/o (±10.9). Initial transplantation was the case for 3 patients (75%) and a second for 1 patient (25%).
Mean time on dialysis was 2.3 years (±4.9) and there were no preemptive transplantations.
With a mean follow-up of 6.2 years, 4 transplants were still functioning. Mean creatinine level was 140 μmol/L (mean GFR 68.2 mL/min/1.73 m2).
We included 6 transplantations in 6 patients with a nonneurogenic neurogenic bladder. Mean age at transplantation was 26.6 y/o (±11.2). Initial transplantation was the case for 5 patients (83.3%) and a second for 1 patient (16.6%). In our series, 3 patients had a native bladder and 3 had an ileal augmentation cystoplasty. Self-urethral catheterization was done in 83.3% (5/6). A urodynamic study was done in 4 cases (66.6%) before transplantation.
Mean time on dialysis was 2.1 years (±4.1) and 3 were preemptive transplantations (50%).
With a mean follow up of 4.6 years, 100% of grafts were still functional at 15 years. Mean creatinine level was 186 μmol/L (mean GFR 60.5 mL/min/1.73 m2).
For a long time, LUTM were excluded from kidney transplantation programs.3 Only few studies have been published about this subject and we report, to our knowledge, the largest series concerning renal transplantation in LUTM.
Bladder rehabilitation is the key to preventing chronic renal failure. McGuire demonstrated the relationship between bladder pressure and renal insufficiency.4 According to the literature in pediatric transplantation, children with clean intermittent catheterization and/or detrusor relaxant therapy showed better courses than those who underwent augmentation/diversion.5,6 For Bagga, this management also shifts toward older age at initial renal transplantation.7
What We Have Learned for Pretransplant Management?
Native Bladder Management
Despite initial treatment and bladder rehabilitation, >50% of patients still have a bladder dysfunction.8 For Chmura et al, all potential kidney recipients should undergo proper evaluation of the lower urinary tract before being qualified for kidney transplantation.9 Biologic tests, imagery, urodynamic study, and urethro-cystography are necessary. Barry also suggests a self-administered health questionnaire.10 If bladder pressure is >40 cm H2O, a bladder augmentation should be performed.11 For defunctionalized bladders, it is now well known that capacity should recover after transplantation.12 A special attention must be paid to postvoid residual volume; which is, according to our series, an independent factor for graft pyelonephritis. In 1986, this was the first report of a transplantation into a neurogenic bladder with CSIC.13 In our series, we found that CSIC is a prognostic factor of graft survival. In our data collection, we regret the lack of a functional evaluation before transplantation.
If a bladder augmentation is necessary, most transplant teams prefer to conduct the surgery before transplantation.14 Arguments for managing patients in this order are a graft risk in a high-pressure bladder and a slow wound healing during immunosuppressive induction treatment. In our univariate analysis, the surgical management of bladder before transplantation, instead of during or after, is a prognostic factor of graft survival. Nahas proved that, when an augmentation cystoplasty had been done, bladder capacity and compliance markedly improved after transplantation despite a dry period.15 Also, a weekly bladder wash with saline during dialysis procedure could be useful to maintain bladder capacity and prevent mucus accumulation.
Concerning ureteral implantation, effectiveness of antireflux depended on which intestinal segment was used.10 It is always better to implant ureters in a native bladder portion despite the thick muscular wall. If an ileo-colic augmentation has been performed, ureteral implantation can be done on tenia colic stripes with an easier antireflux anastomosis.16 If only ileum is available, antireflux technique can be difficult and a Camey-Leduc technique is a good alternative.17
In many cases, incontinent derivation is performed before transplantation. Surrange et al suggests a delay of 3 months before transplantation.18 Transplantation could be performed using an extraperitoneal approach, the kidney is thus put in an upside down position on the right side, and a peritoneal window is done for uretero-ileal anastomosis. Confection of a derivation could also be done during transplantation.
Posterior Urethral Valves
This LUTM has been well studied and our results are similar to those in the literature. Some studies have compared PUV and non-PUV results without a significant difference in graft survival.8,19,20 Authors suggest that bladder dysfunction is a prognostic factor of graft dysfunction underlying the importance of a pretransplant urodynamic study. Table 4.
Bladder augmentation in PUV before transplantation is still debated and no recommendations can be made.21 Bartsch et al showed that graft function was significantly better in the PUV group with limited intervention and without bladder augmentation.22 Bladder pressure evaluation before transplantation is important. If bladder augmentation is necessary, most transplant teams prefer to do it before transplantation.14 CSIC is a protective factor for graft function and should be encouraged.
Prune Belly Syndrome
There are only short series of transplantations in prune belly syndrome, and we report the largest to our knowledge. Fontaine23 and Kamel24 reported a comparative study versus non-LUTM and did not find a statistical difference (Table 5). Intraoperative abdominoplasty to prevent graft torsion is still controversial.
This population has been well studied.25-27 Heterogeneity in the management of neurogenic bladder made it hard to extrapolate. A special attention has to be paid for transplantation in native bladder. Bladder dysfunction depends on the level of lesion, and CSIC should be encouraged in hypotonic bladder dysfunction (Table 6).
According to our knowledge, we reported the first series concerning renal transplantation in bladder exstrophy. Our results are good but cannot be extrapolated because of the heterogeneity in bladder reconstruction techniques. Nowadays, urinary diversions are less frequent than conserving native reconstructed bladder in infancy.
There are no reports of renal transplantation for urogenital sinus. We included 4 cases and results are good, but too small to be analyzed. A larger multicenter study is needed.
We specifically focused on infectious complications, because it was a strong argument for excluding LUTM from renal transplantation programs. Basiri et al proved that augmented cystoplasty increased graft pyelonephritis risk by 10-fold.28 Gastroplasty seems to be the best type of augmentation regarding the prevention of the infectious risk because of acid secretion and easier antireflux ureteral implantation.29 However, it is not performed becauseof the important malignant risk. According to Muller et al, urinary tract infection is an important risk factor for the onset of chronic rejection.30 Despite this ascertainment, acute graft pyelonephritis did not independently contribute to poor graft or patient survival in the study by Kamath et al, which is also our conclusion.31 A low-pressure reservoir using cystoplasty and CSIC, combined with an antireflux ureteral implantation, is the best way to prevent graft pyelonephritis. We did not find the impact of an antibiotic prophylactic treatment to prevent graft pyelonephritis but a bias could be that antibiotics were given to high infectious–risk patients.
Urological complications seem to be comparable to renal transplantations without LUTM. In this series, we found 4.1% of urinary fistulas, which is comparable to the literature.32,33 Ureteral stenosis (8.1%) was slightly more frequent in our series than in the literature.34,35 Stenoses are more frequent in the PUV population36; modifications in the connective tissue in the bladder wall37 and an augmented intramural wall pressure in poorly compliant bladders38 could explain such differences. Nowadays, there is no urodynamic data to prevent urologic stenosis risk.
Patients with lower urinary tract malformations should be considered for renal transplantation as any other cause of end-stage renal disease. Even if enterocystoplasty and continent urinary diversions exposed grafts to more frequent acute pyelonephritis, patient and graft survival rates at 10 years were similar to other kidney transplantations on native bladder. Attention should be drawn to postvoiding residual volume and promotion of clear intermittent catheterization.
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38. Nguyen MT, Pavlock CL, Zderic SA, et al. Overnight catheter drainage in children with poorly compliant bladders improves post-obstructive diuresis and urinary incontinence. J Urol. 2005; 174:1633–6. discussion 1636