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Neuropathic bladder as a cause of chronic renalfailure in children in developing countries Received: 23 September 2005 / Revised: 5 November 2005 / Accepted: 6 November 2005 / Published online: 2 March 2006 Abstract Neuropathic bladder is considered a threat to the kidneys if not managed appropriately. In this study, wereport our experience with neuropathic bladder at King Neuropathic bladder is considered a major risk factor for Abdulaziz University Hospital (KAUH) as a cause of chronic pyelonephritis and progressive renal damage [ chronic renal failure (CRF) in the pediatric age group. This There are numerous causes of neuropathic bladder retrospective study included all children diagnosed with including open and closed spina bifida, sacral agenesis, neuropathic bladder who presented with moderate or spinal cord tumor, trauma, transverse myelitis, and auto- severe CRF over a 4-year period from December 2000 to nomic neuropathy [Furthermore, no anatomical or December 2004 [glomerular filtration rate (GFR) at neurological defect could be found in a small group of presentation <50 ml/min per 1.73 m2]. Fifteen patients children who manifested signs of bladder sphincter inco- were diagnosed with neuropathic bladder; group A ordination and intravesical functional obstruction. The consisted of ten patients with spina bifida and one with latter condition is called nonneurogenic neurogenic bladder sacral agenesis and group B consisted of four patients with (NNNB) or occult neuropathic bladder (Hinman syn- nonneurogenic neurogenic bladders (NNNB). The mean drome) , ] and it carries the same risks to the kidneys age±SD at presentation was 6.2±3.8 years, GFR was 24.2± The usual presentation of NNNB is incontinence with 12.4 ml/min per 1.73 m2, and creatinine was 289.9± daytime wetting as a result of impaired bladder sensation 253.2 μmol/l. There were no differences in the age at and poor bladder emptying [or recurrent urinary tract presentation to a pediatric nephrologist or the degree of renal failure at presentation between the two groups. Clean The aim of the management of neuropathic bladder is to intermittent catheterization (CIC) was not started in all preserve renal function and to improve continence [ patients before presentation to KAUH, except in two The best way of preserving renal function is by keeping the children. Five children required dialysis as they were in bladder empty, at low pressure, and free of infection end-stage renal failure (ESRF). All except one received Clean intermittent catheterization (CIC) has made a peritoneal dialysis (PD). Their mean age at the start of tremendous difference to the management of such patients, dialysis was 10.8±1.7 years. Neuropathic bladder due to with an improvement in continence, reduction of renal spina bifida or NNNB is an important cause of CRF in problems, and UTI However, CIC has psychosocial developing countries. There was a considerable delay in the impact on the treated children and their families , diagnosis of NNNB and a significant delay in starting CIC and probably the rejection of this form of treatment is more common in Arab cultures like ours. With the recentmodalities of treatment, chronic renal failure (CRF) is Keywords Neuropathic bladder . Chronic renal failure .
rarely seen in children with neuropathic bladder; however, there is a risk that this may merely be postponed intoadulthood Spina bifida remains a problem in Saudi Arabia as the incidence of neural tube defects (NTD) appears to be non-declining over the years [, despite a recent folic acid food fortification. Furthermore, high prevalence of con- Paediatrics Department, King Abdulaziz University Hospital, sanguinity of the parents in Saudi Arabia was reported as a P.O. Box 80215, Jeddah 21589, Saudi Arabia significant risk factor for spina bifida. Consanguinity of the parents was found in 89% of the spina bifida parents and in only 67% of the controls (p<0.0005) ].
In this study we report our experience at King Abdulaziz was 1:4. Ten patients had spina bifida, one patient had University Hospital (KAUH) with children with neuro- sacral agenesis, and four had occult or nonneurogenic pathic bladder who presented with CRF. We discuss the possible causes of their presentation early in life with CRF.
At presentation to our pediatric nephrology clinic, their mean age±SD was 6.2±3.8 years (range: 1.5–13), GFR was24.2±12.4 ml/min per 1.73 m2 (range: 5–44), and creati- nine was 289.9±253.2 μmol/l (range: 69–925).
All children with spina bifida (except two) had hydro- This retrospective study covered all pediatric cases cephalus which required ventriculoperitoneal (VP) shunt.
diagnosed with neurogenic bladder who presented with Similarly, all of them were paraplegic except two who had chronic renal failure (CRF) to the pediatric nephrology minimal neurological involvement of their lower limbs and clinic over 4 years from December 2000 to December were able to walk. All of them had operations to close the 2004. Only children with glomerular filtration rate (GFR) spina bifida in the first 2 days except one who underwent of less than 50 ml/min per 1.73 m2 were included in the study. GFR was measured using diethylenetriaminepentaa- Table summarizes the clinical and radiological data of cetic acid (DTPA) scan or calculated using the Schwartz group A consisting of children with spina bifida or sacral agenesis and the clinical and radiological data of group B The patient’s notes were reviewed for demographic data, consisting of children with occult or nonneurogenic age at presentation to a pediatric nephrologist, clinical neurogenic bladder. There were no differences in the age presentation, radiological investigations, and laboratory at presentation to a pediatric nephrologist or the degree of renal failure at presentation between the two groups.
Results are expressed as mean+SD or median (range).
All children with NNNB in group B presented with The t-test assuming equal variance was used to compare recurrent urinary tract infection (UTI) and two of them were also reported as wet during the day (the other twowere young and in nappies).
The diagnosis of NNNB in group B was made on the bases of radiological investigations and urodynamicstudies. All of them had radiological and urodynamic Fifteen patients presented with a variable degree of CRF evidence of neuropathic bladder with no neurological [six moderate CRF (GFR 49–30 ml/min per 1.73 m2), four abnormalities. All of them had normal magnetic resonance severe CRF (GFR 29–15 ml/min per 1.73 m2), and five end-stage (GFR <15 ml/min per 1.73 m2)]. All were of CIC was started by the pediatric nephrologist in all Arab ethnic origin (67% Saudi) and the female:male ratio patients except two patients in group A, in whom it was Table 1 Clinical and radiological data of groups A and B. GFR glomerular filtration rate, MCUG micturating cystourethrogram, VUR vesicoureteral reflux, PUJ pelviureteric junction obstruction, MRI magnetic resonance imaging, CIC clean intermittent catheterization hydronephrosis and absent left kidney (1) Sacral agenesis (1), leptomeningeal cyst (1) started by urologists before their presentation. Five with a thickened wall is usually found. Urodynamic studies children required dialysis as they were in end-stage renal usually reveal detrusor sphincter dyssynergia. The etiology failure (ESRF), four in group A and one in group B. All of this voiding disturbance remains unclear; however, it except one received peritoneal dialysis (PD), two with results from functional urinary tract obstruction and can automated PD (APD) and two with continuous ambulatory initiate and perpetuate vesicoureteral reflux (VUR) as well peritoneal dialysis (CAPD). Their mean age at the start of as encourage UTI and renal damage [].
dialysis was 10.8±1.7 years. Two children with shunted NNNB has traditionally been believed to represent a hydrocephalus were dialyzed peritoneally. One of them had disorder of older children; however, recently it has been no infections or other complications for 1 year, while the recognized as a severe form of dysfunctional voiding that other one had peritonitis which was complicated by a staph may be present even in the neonatal period []. In our epidermis shunt infection. The latter was changed to series, the younger patient with NNNB was 1.5 years old.
hemodialysis and required externalization of the VP shunt The radiological and urodynamic investigations (Table for few weeks. Only one patient was started on hemodi- revealed similar results to those previously reported in alysis from the beginning because of social reasons. Three young children with NNNB []. These were thick-walled, patients continued on CIC, while two stopped it, as they poorly compliant bladders with incomplete bladder were continent and they felt that it was difficult to do both emptying causing significant upper tract pathology (VUR PD and CIC. All of them received anticholinergic agents and hydronephrosis). Boys with trisomy 21 may be at particular risk for NNNB However, none of our The patients on dialysis were advised to have renal patients with NNNB had Down syndrome.
transplantation after correcting their lower urinary tracts.
It is interesting to observe that all the patients with spina However, none of the patients had renal transplantation bifida had received attention to their neurological problems because of the unavailability of donors.
as all of them had operations for the myelomeningocele and The rest of the patients were managed with CIC, the hydrocephalus. In contrast, most of them were not anticholinergic drugs (oxybutynin), prophylactic antibio- advised about the risk to their kidneys from the associated tics, and conservative measures for CRF (phosphate neuropathic bladder. This delay in the management also binders, active vitamin D, erythropoietin, iron, folic acid, explains the high percentage of VUR in our cohort in both sodium bicarbonate, antihypertensive agents if needed, and groups (A and B), as regular emptying of the bladder was high calorie, low protein, low phosphate and potassium not commenced early and anticholinergic drugs were not diet). Two of them were lost to follow-up, one died from instituted to reduce intravesical pressure. Furthermore, the nonrenal causes (toxic shock syndrome), and the remaining lack of good medical follow-up and management including seven were followed up for 2.7±1.1 years. Five of them had early diagnosis and treatment of acute pyelonephritis could fairly stable kidney function while the last two showed a also have contributed to the bad outcome in these patients.
A multidisciplinary approach in a specialized spina bifidaclinic would help to reduce this observed delay incommencing the appropriate management to protect the One-third of our cohort required renal replacement All the patients in our study group presented with a therapy (RRT) at a rather young age. PD was the main considerable degree of CRF at an early age. This finding is modality of RRT as it is the dialysis of choice in the different from reports from Western countries [, majority of pediatric patients. However, the presence of VP Although renal complications were reported as the most shunt makes it more complicated as those children are frequent cause of long-term morbidity in children with prone to develop shunt infection as was the case in one of neuropathic bladder, CRF is rarely seen at an early age , our patients and has been reported by others More , This could be explained by the delay in the recent reports demonstrated that PD under close monitor- management as most of the children were not started on ing is not contraindicated in children with myelomeningo- CIC until presentation to pediatric nephrology or urology cele, regardless of the presence of VP shunt or any stoma clinics, which occurred after multiple scars and significant ]. However, if cerebrospinal fluid diversion is needed renal damage had already occurred. Similar reports of simultaneously or after starting PD, an extraperitoneal site neurogenic bladder causing CRF were reported from other would be a better choice than VP shunt. This may avoid the developing countries [], and this could be attributed to risk of intra- and postoperative infection in the PD catheter, the same lack of early awareness, early diagnosis, and secondary to surgical intervention for VP shunt insertion.
appropriate treatment of the problem, which are vital to Loss of peritoneal function is a potential late risk related to avoid chronic renal insufficiency in these patients.
exposure to cerebrospinal fluid and PD. Furthermore, spina NNNB was not reported as a cause of CRF in the bifida patients on PD present specific diagnostic challenges pediatric literature. Patients with NNNB present with due to overlapping symptoms (e.g., vomiting, abdominal symptoms similar to those with a neurogenic bladder, but tenderness, fever) secondary to PD- or VP shunt-related no neurological or anatomical lesions can be identified.
complications (e.g., peritonitis, visceral injury by devices) These children have diurnal wetting and recurrent urinary or primary disease (e.g., neurogenic bladder, pyelonephri- infections. Radiologically, a trabeculated, enlarged bladder tis) with potential risks of delaying adequate treatment.
Early evaluation by a pediatric surgeon and a neurosurgeon 4. Borzyskowski M (2003) Neuropathic bladder: identification, is required for effective management of complications and investigation, and management. In: Webb N, Postlethwaite R(eds) Clinical paediatric nephrology. Oxford University Press, selection of more efficient individualized therapeutic 5. Hinman F Jr (1986) Nonneurogenic neurogenic bladder (the Although renal transplantation is now considered the Hinman syndrome)—15 years later. J Urol 136:769–777 optimal treatment for ESRF in all age groups, doubts 6. Kaneti J, Sober I, Gradus D (1988) Fate of nonneurogenic bladder—end-stage renal failure. Eur Urol remain however about the risks of transplantation when the patient has an abnormal lower urinary tract, because it is 7. Wraige E, Borzyskowski M (2002) Investigation of daytime logical to assume that the bladder that contributed to the wetting: when is spinal cord imaging indicated? Arch Dis Child destruction of native kidneys would also threaten subse- quent renal allograft [Therefore, the general recom- 8. Johnston LB, Borzyskowski M (1998) Bladder dysfunction and neurological disability at presentation in closed spina bifida.
mendation is to correct inefficiencies and deficiencies of the lower urinary tracts of these patients before transplan- 9. Borzyskowski M, Mundy AR (1988) The management of the tation []. Recent data demonstrate the feasibility of renal neuropathic bladder in childhood. Pediatr Nephrol 2:56–66 transplantation in patients with spina bifida and ESRF , 10. Borzyskowski M, Mundy AR, Neville BG, Park L, Kinder CH, Joyce MR, Chantler C, Haycock GB (1982) Neuropathic ]. The current recommendation is that these patients vesicourethral dysfunction in children. A trial comparing clean should not be deprived of the benefits of renal transplan- intermittent catheterisation with manual expression combined tation [Similarly, renal transplantation in children with drug treatment. Br J Urol 54:641–644 with severe bladder dysfunction due to other causes can 11. Edwards M, Borzyskowski M, Cox A, Badcock J (2004) Neuropathic bladder and intermittent catheterization: social and achieve similar results to those obtained in the general psychological impact on children and adolescents. Dev Med population ]. Meticulous selection of patients and surgical reparative techniques ensuring voiding as well as 12. Borzyskowski M, Cox A, Edwards M, Owen A (2004) adequate control of urinary infections are mandatory.
Neuropathic bladder and intermittent catheterization: social Augmentation cystoplasty and intermittent catheterization and psychological impact on families. Dev Med Child Neurol46:160–167 are appropriate techniques currently used for achieving this 13. Asindi A, Az-Shehri A (2001) Neural tube defects in the Asir region of Saudi Arabia. Ann Saudi Med 21:26–29 14. Murshid WR (2000) Spina bifida in Saudi Arabia: is consan- guinity among the parents a risk factor? Pediatr Neurosurg32:10–12 15. Hamed RM (2002) The spectrum of chronic renal failure among Jordanian children. J Nephrol 15:130–135 Neuropathic bladder due to spina bifida or NNNB is an 16. Koff SA (1992) Relationship between dysfunctional voiding important cause of CRF in the developing countries. There 17. Jayanthi VR, Khoury AE, McLorie GA, Agarwal SK (1997) was a considerable delay in the diagnosis of NNNB and a The nonneurogenic neurogenic bladder of early infancy. J Urol significant delay in starting the appropriate management in all neuropathic patients. More awareness is required among 18. Handel LN, Barqawi A, Checa G, Furness PD III, Koyle MA pediatricians about NNNB and about the risk to the kidneys (2003) Males with Down’s syndrome and nonneurogenic caused by neuropathic bladder. Specialized spina bifida 19. Kazee MR, Jackson EC, Jenkins RD (1990) Management of a clinics with a multidisciplinary approach will help to child on CAPD with a ventriculoperitoneal shunt. Adv Perit reduce the observed delay in commencing appropriate 20. Grunberg J, Rebori A, Verocay MC (2003) Peritoneal dialysis in children with spina bifida and ventriculoperitoneal shunt:one center’s experience and review of the literature. Perit Dial 21. Power RE, O’Malley KJ, Little DM, Donovan MG, Creagh TA, Murphy DM, Hickey DP (2002) Long-term followup of 1. Brown S, Marshall D, Patterson D, Cunningham AM (1999) cadaveric renal transplantation in patients with spina bifida.
Chronic pyelonephritis in association with neuropathic bladder.
22. Hamdi M, Mohan P, Little DM, Hickey DP (2004) Successful 2. Muller T, Arbeiter K, Aufricht C (2002) Renal function in renal transplantation in children with spina bifida: long term meningomyelocele: risk factors, chronic renal failure, renal single center experience. Pediatr Transplant 8:167–170 replacement therapy and transplantation. Curr Opin Urol 23. Mendizabal S, Estornell F, Zamora I, Sabater A, Ibarra FG, Simon J (2005) Renal transplantation in children with severe 3. Schumacher S, Haferkamp A, Muller SC (2003) Bladder dysfunc- bladder dysfunction. J Urol 173:226–229 tion due to rare neurological disorders. Urologe A 42:1564–1568


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