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Scandinavian Journal of Surgery 100: 256–263, 2011

Neurogenic bladder in children: basic principles, new therapeutic trends J. M. Guys, G. Hery, M. Haddad, C. Borrionne Pole Medico Chirurgical Pédiatrique, Hôpital d’enfants de la Timone, Marseille, France

ABSTRACT

Diagnosis of neurogenic bladder is straightforward in children with myelomeningocele. However, recognition is more difficult in patients with occult dysraphism or central nervous system disorders since clinico-anatomical correlations are poor. Careful clinical examination and urodynamic exploration are mandatory for diagnosis and follow-up. Even if urinary leak is the first symptom, the main goal of the pediatric surgeon must be to preserve the upper urinary tract. The ideal protection strategy consists of ensuring that micturition is voluntary and complete and that the bladder capacity is sufficient with adequate compliance and sphincter outlet resistances. Balancing these functions requires a combination of medical and surgical treatment. A variety of techniques can be used depending on gender and age of the patient and social environment. In most cases, intermittent bladder catheterization is necessary to obtain complete evacuation of the bladder. Bladder capacity can be increased by anticholinergic drugs, injection of botulinum toxin into the bladder, and augmentation cystoplasty. Augmentation of bladder outlet resistances requires endoscopic injection of bulking agents, surgical bladder neck reconstruction and urethral lengthening, bladder neck suspension, and artificial urinary sphincter. In difficult cases, continent cystostomy with closure of the bladder neck can achieve definitive continence. At the beginning endoscopic treatment combining anti reflux procedure, injection of the bladder neck and botulinum toxin can be considered as a “total endoscopic management” and should be our first line. Other techniques are under evaluation. Sacral neuromodulation has given promising results. Artificial tissue engineering will probably be used in the next future. Management of neurogenic bladder is not limited to urological considerations. Orthopedic, digestive, and sexual problems must also be taken into account in order to obtain an “acceptable quality of life”. Key words: Urinary incontinence; pediatric neurogenic bladder; spinal dysraphism; bladder sphincter dyssynergy; total endoscopic management; sacral neuromodulation

Correspondence: Jean Michel Guys, M.D. Service de Chirurgie Pédiatrique Hôpital d’Enfants de la Timone 13 385 Marseille Cedex 5 France Email: jean-michel.guys@ ap-hm.fr

Neurogenic bladder, new trends

INTRODUCTION To ensure adequate treatment of neurogenic bladder in children, management must be proactive rather than reactive. Decision-making must take into account prognostic factors anticipating the consistently unfavorable natural course of neurogenic bladder. The purpose of this article is to show the importance of the circumstances surrounding diagnosis and/or paraclinical findings in determining the functional urologic grade of disease as a basis for selecting the­ rapeutic modalities. The last part of this article presents a quick update of current therapeutic indications that have advanced in recent years. Etiologies and diagnostic features Congenital causes

Myelomeningocele (spina bifida) For a long time, myelomeningocele, was the main etiology of neurogenic bladder in children (1,2,3). With the advent of prenatal diagnosis, the frequency of this cause has dropped since, in many countries including France, this in utero finding often leads to termination of pregnancy. In a recent randomized trial of prenatal versus postnatal repair of myelomeningocele, Adzick et al reported that prenatal repair reduced the need for shunting and improved motor outcome at 30 months but was associated with a non negligible maternal and fetal risks (4). This finding prompts the question: do the potential benefits of prenatal coverage of hindbrain herniation, shunt-dependent hydrocephalus, and leg function justify the associated risks for mother and child (5)? Occult spinal dysraphism This malformation is currently the most common cause of neurogenic bladder (1). It can be suspected based on the presence of characteristic lumbosacral cutaneous stigmata and confirmed by spinal ultrasound in the first two months of life. In many cases, diagnosis is made later upon presentation of micturitional disturbances and motor or sensory deficits involving the lower extremities and perineal region. These manifestations frequently occur around the time of puberty when growth causes increased traction on the spinal cord. Dysraphism includes tethered spinal cord associated or not with imperforate anus, cloacal malformation, diastematomyelia, and sacral hypoplasia or agenesis (3). Acquired neurogenic bladder

In addition to being less common than in adults, spinal cord injuries in children are intrinsically different owing to a number of factors including mechanism of injury. Tumor-related spinal compression is not uncommon in children. Irreversible changes in bladder enervation can occur as complication after pelvic surgery in patients with urologic malformations rang-

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ing from ectopic ureter to exstrophy as well as after treatment for Hirschsprung disease, upper anorectal malformation, sacral coccygeal teratoma, etc. Transient or permanent neurogenic bladder can also be observed in association with myelitis and radiculoneuritis. Neonatal cerebral anoxia and central nervous system abnormalities including spastic diplegia (cerebral palsy) and learning disabilities, severe infectious syndrome (meningitis) can be observed (7). Diagnostic features

Neurogenic bladder can also be diagnosed in cases involving a more or less long history of micturitional disturbances considered as benign and treated medically and even surgically. In most of the cases, the possibility of a neurological background is raised only after repeated therapeutic failure. Neurogenic bladder may be suspected during diagnostic work-up for other symptoms associated or not with micturitional disturbances, e.g., severe constipation or psychological disorders with encopresia. In this setting, it should be pointed out that Hinman syndrome involves bladder dysfunction that closely mimics organic neurogenic bladder even if no organic defect can be found (8). The psychological context of these children is special and abuse can be identified as a possible cause in numerous cases. Only after completing an exhaustive work-up, it will be possible to speak of «non-neurogenic elimination disorders » that have been indifferently designated under a number of names including “neurogenic non-neurogenic bladder”, “occult neurogenic bladder”, “lazy bladder”. All of these names clearly reflect the paucity of our current knowledge in this domain. Pathophysiology and work up Natural course

Regardless of etiology of neurogenic bladder, the natural course almost always involves altered storage function and vesicosphincteric dyssynergia. Overactivity of the detrusor muscle often due to loss of inhibition from the pontine and suprapontine centers leads to high intravesicular pressure. As a result, the striated ureteral sphincter exhibits spasticity (1,6). These changes explain that neurogenic bladder presenting mainly as urinary incontinence actually corresponds to an obstructive disorder of the lower tract due to high-grade vesicosphrincteric dyssynergia. Strategy

In this setting, the use of the conventional neurological categories, i.e., central, peripheral or mixed has little bearing on therapeutic decision-making. Strategy must simply be aimed at achieving ideal micturition characterized by voluntary control, low pressure, and complete voiding. Accordingly, assessment must focus on the three main bladder functions, i.e., retention, storage and discharge. Capacity must be sufficient for low-pressure retention and storage with

So : no sphincterian resistances S+- : variable sphincter V- : “big” bladder 258

J. M. Guys, G. Hery, M. Haddad, C. Borrionne

Abbreviations: R : kidney V : “normal” bladder (capacity) V 0 : “small” bladder S 0 : no sphincterian resistances S+ – : variable sphincter V– : “big” bladder

tients with congenital neurogenic bladder. Functional exploration (uro-MRI and isotopic examination) becomes mandatory if pyelonephritic renal scaring is suspected. Bladder exploration The essential examination for bladder exploration is cystography coupled with urodynamic investigation. This combination allows complete morphological, functional, and dynamic assessment of the lower urinary tract. Cystography

Fig. 1. Urinary incontinence: one symptom, numerous causes.

adequate sphincter resistances and emptying control. In our view, functional urologic assessment (Wein) provides the soundest basis for therapeutic planning (1, 4). Urinary incontinence can be caused by a variety of factors (Fig. 1) including: 1. true sphincter-related incontinence (a) with a “normal” bladder (uncommon). 2. undersize bladder resulting in limited retention time and need for frequent voiding that is incompatible with a normal social life (b). 3. oversize hypotonic bladder that empties by overflowing (c). Any of these bladder conditions can occur in combination with sphincter-related incontinence that can range from obstructive hypertonia to a total lack of resistance. All these disorders lead to the same clinical finding, i.e., leakage. For this reason, a careful work-up is necessary to determine the exact underlying mechanism. Work-up

Radiological and urodynamic examination must provide a precise idea of the morphological and functional condition of the upper tract and of lower tract function with regard to storage, discharge and synergy with sphincteric resistance (1). Exploration of the upper urinary tract In the early stages of disease, the upper urinary tract can be studied by ultrasound since the kidneys are generally unaffected. This is particularly true in pa-

Cystography is usually performed by retrograde catherization. Catheter diameter must allow micturition. Bladder features are key findings for diagnosis of neurogenic bladder: verticalization of the long axis, thickening of the wall, diverticulas. Vesico-ureteral reflux, even if only minor, can be evidence of high bladder pressure. The bladder neck may open spontaneously with opacification of the posterior uretra, since the external sphincter is often hypertonic (9). In case of particularly low sphincter resistance, it may be necessary to perform this examination using an occlusive catheter at the level of the bladder neck. Characteristic urodynamic data for diagnosis neurogenic bladder include maximum detrusor pressure, reflex volume, maximum cystometric capacity, leak point pressure, and detrusor activity. Detrusor overactivity is defined as any short-lived pressure rise > 15 cm H2O over baseline before capacity is reached (10, 11). Dynamic electromyography of the striated ureteral sphincter can be the only way to demonstrate vesicosphincterian dyssynergy. However, like study of evoked somesthesic sensory and motor potentials, dynamic electromyography is not performed systematically in children since these examinations are interesting only if the neurological background is uncertain (12). Risk factors and follow-up The essential goal of workup is to evaluate risk factors for the upper tract deterioration and to follow-up the treatment. For this reason, leak point pressure is one of the main urodynamic prognostic factors. The estimated critical threshold is at 40 cm H2O. Beyond this point, upper tract damage appears in 70% of cases (11). A similar adverse relationship is observed between bladder overactivity and pressure peaks again reaching 40 cm H2O on a regular basis. While there is not always a direct link between high bladder pressure and appearance of reflux, this finding should be considered as a high-risk signal of imminent upper tract deterioration (13). 23 facIn summary, the most detrimental urodynamic tor is elevated bladder pressure regardless of whether this occurs throughout the micturition cycle (“bladder hypertonia”), transiently (“bladder overactivity”), or even only in the pre-micturition phase. Early detection and treatment of this condition is mandatory. In association with elevated pressure, inadequate

Neurogenic bladder, new trends

emptying whether due to dyssynergy or to sphincter hypertonicity aggravates the effect of the “high-pressure syndrome”. Chronic retention of urine in the bladder is the most important clinical prognostic factor. Urinary incontinence is of limited prognostic value since it is just a “symptom” of an unbalanced relationship between the different bladder functions. Treatment In all cases, treatment of micturition disturbances associated with neurogenic bladder must be guided by the notion of protecting the upper urinary tract (1). In older children, management of incontinence is necessary to ensure a normal social life. Continence depends on urinary storage, complete voiding, and sufficient sphincter resistances. Ideally the goal should be to achieve voluntary control of the micturition via the natural passages. Socially compatible continence is generally defined as the ability to hold urine for four hours without leakage. Management of neurogenic bladder should therefore focus on: 1. ensuring bladder emptying; 2. improving bladder capacity; 3. increasing sphincter resistances. Ensuring bladder emptying

Therapeutic modality The simplest therapeutic modality use expression voiding methods such as the Crede and Valsalva maneuvers. However Crede voiding is frequently inadequate in older children because most have intact motor function above L1 and any augmentation in abdominal pressure can lead to a reflexive increase in urethral sphincter activity, thus producing an increase in bladder outlet resistance (3). Intermittent catheterization Intermittent catheterization performed 4 to 5 times a day is the easiest-to-use instrumental bladder management technique (14). Current devices have benefited from numerous technological improvements (e.g. self-lubricating catheters and built-in drainage receptacle). By allowing the bladder to be emptied at low pressure and removing residues that can be harmful for the upper tract, intermittent catheterization is the mainstay of management for neurogenic bladder. Catheterization allows complete voiding through the natural passages in a manner that can be considered as voluntary. There is no age limit for beginning intermittent catheterization that is proposed to young children by many groups (15). Pharmacological treatment Pharmacological treatment in order to facilitate bladder emptying is not widely used in patients with neurogenic bladder. Alpha-adrenergic blockers and

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smooth muscle relaxants may be useful in some cases involving hypertonia but indications are limited due to adverse effects (cardiac) and poor clinical efficacy. Neurotomy and sphrincterotomy Neurotomy and sphincterotomy have been used to permanently suppress peripheral resistance. However, this definitive solution has been largely abandoned due to severe side effects (impotence) and too definitive incontinence. Improving bladder capacity

Pharmacological treatment Anticholinergic agents are most commonly used medication to improve bladder capacity. Oxybutinin chloride is currently the most active agent. Detrusitol® (tolteridine) seems to be best tolerated. Ceris® (trospium chloride) is used in adult patients and appears to have fewer side effects but has not been approved for children. In theory more than in practice, diazepam is thought to have a relaxant effect on the detrusor muscle and tonic effect on the sphincter. Impramine is hazardous at effective doses. Betamimetics (Isoprenaline) also have a relaxant activity on the detrusor muscle but their use is greatly limited by undesirable systemic effects. Botulinum toxin Botulinum toxin has been proposed for management of neurological detrusor hyperactivity. The first description of this technique was published in 2000 by Schurch et al (16) who administered botulinum toxin (Botox®, Allergan®) by endoscopic injection and observed a significant increase in maximal bladder capacity and a decrease in maximal detrusor pressure and number of incontinence episodes. Since 2002, prospective studies have confirmed the efficacy of botulinum toxin in children with a neurogenic detrusor overactivity (17–20) with continence rates ranging from 60 to 83%. In our center, patients undergoing intermittent catheterization for urinary incontinence associated with poorly compliant and overactive bladder that fails to respond to anticholinergic agents are included in a ongoing prospective trial after informed consent. The treatment protocol calls for injection of 12 U/kg of Botox (maximum 300U) into the detrusor and 2 to 3 cc of polydimethylsolixane into the bladder neck. Response is evaluated on the basis of urinary diary data and urodynamic testing at 2 and 6 months after the 1st injection and 4 months after subsequent injections. Ten patients (7 boys and 3 girls) with a mean age of 9.36 years (range, 5.6–16) have been included. All but two presented spina bifida. The number of injections was 1 in 3 patients, 2 in 5, and 3 in 2. From a clinical standpoint, 8 patients reported a decrease in leak episodes and 2 reported no response. No patient achieved continence even after 3 injections. Clinical effects were observed at a mean interval of 3.13 ± 3.98 days after injection and lasted for a mean

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duration of 2.87 ± 1.27 months. Follow-up at 2 and 6 months showed increased bladder compliance (p < 0.01). A positive effect (not statistically significant) was also observed on maximal bladder capacity and maximal detrusor pressure. The same results were noted after repeated injections.

Few series describing percutaneous tibial nerve stimulation in children have been published, but existing data suggest that improvement in continence was significantly greater for patients with non-neurogenic than neurogenic disease (30).

Bladder autoaugmentation

The effectiveness of parasacral transcutaneous electrical nerve stimulation for treatment of overactive bladder in children was recently evaluated in a prospective trial in which 25 girls and 12 boys were randomized into a test and sham group. Thirteen of the 16 patients who underwent parasacral transcutaneous electrical nerve stimulation were cured. Again none of these patients presented neurogenic bladder (31).

If performed early, auto-augmentation that consists of anteroposterior section of the detrusor muscle fibers can be sufficient to increase bladder capacity. Some evidence indicates that instrumental bladder dilation using an intravesicular balloon is necessary to ensureat least short term success of this procedure (21). Bladder enlargement Bladder enlargement can be performed using various materials including segments from the colon, ileum, stomach, or dilated ureter. The ileum is the most commonly used tissue reported in the literature (22). Enlargement is always achieved using the detubularized patch technique to avoid residual hyperactivity due to intrinsic intestinal peristalsis. Results after removal of the digestive mucosa are controversial but some investigators have reported excellent clinical outcomes (23). As a prerequisite for bladder enlargement, it is mandatory for the patient to be able to perform effective emptying of the new bladder (1, 3). In particular, the patient must accept and understand the need for intermittent catheterization and his/her ability to use the device must be tested before undertaking bladder enlargement. Disadvantages include mucus production, recurrent urinary infection, electrolyte imbalance, stone formation and the risk for the late occurrence of cancer in the augmented segment (25). In the future, it is likely that tissue culture will provide a new source of material for bladder enlargement (26).

Parasacral transcutaneous electrical nerve stimulation

Direct stimulation of the S3 and S4 nerve roots

Direct stimulation of the S3 and S4 nerve roots i.e., sacral neuromodulation (SNM: “Interstim therapy”) is performed not only to reinforce the sphincter tone by stimulating contraction of all the muscles of the perineal floor but also to improve bladder compliance by reactivating certain efferent and afferent nerves (32). The efficacy of this treatment in children was assessed in a multicenter, open label, randomized, crossover study including children older than 5 years in France. The positive response rate was more than 75% overall, 81% for urinary incontinence and (78%) for bowel incontinence. Crossover analysis indicated that SNM is more effective than conservative treatment for both types of incontinence (p = 0.001) (33). Various radiculotomy procedures

Various selective radiculotomy procedures (S2 or S3) have been used in adults. The goal of these procedures is to suppress detrusor contraction and increase bladder capacity. Continuous intraoperative monitoring of the bladder pressure is necessary to ensure precise selection of the targeted nerve roots. No information is available about the long-term outcome of these procedures.

Electrical stimulation Electrical stimulation has been used in adults for more than 25 years. Transuretral electrical bladder stimulation

Kaplan was the main proponent of the technique of transurethral electrical bladder stimulation in children and reported a series of 372 patients with a mean age of 5.5 years and mean follow-up 6.6 years. In 76.9% of these patients, the increase in bladder capacity was 20% or greater (27). Despite these results, few groups have adopted this technique. Stimulation of the posterior tibial nerve

Some investigators have reported statistically significant symptomatic improvement after percutaneous tibial nerve stimulation in adult patients with overactive bladder. Twelve weekly procedures achieved some short term success results for 12 months (28). This technique is considered as safe and effective (29).

Increasing sphincter resistances

Pharmacodynamic treatment Cholinergic and alpha-stimulating agents exhibit weak action and have undesirable side effects. Surgery of the bladder neck Surgery of the bladder neck such as anterior wedge reinforcement type Young Dees, bladder neck suspension (rectus facial sling) (Goebbel-Stœckel) or simple urethropexy (Marshall-Marchetti) are well known and have been used for years (34). In a recent 51-case Spanish study using the rectus fascial sling technique, good continence was achieved in 88% of patients with a mean follow-up of 4.16 years (35). Bladder neck reconstruction using the Kropp and Pippi Salle techniques appeared to be promising. The short-term success rate was 61% in girls but few longterm data have been reported (36).

Neurogenic bladder, new trends

Combined techniques, e.g. fascial wrap and urethral lengthening, appear to give the best results (37). In one 19-case series using this approach, complete continence was achieved in 15 patients with a mean ± SD follow-up of 35.5 ± 29.1 months (38). Artificial urinary sphincter The only model now used is the totally implantable Scott device (AS800). In children, the cuff is placed at the level of the bladder neck. Short- and middle-term results are often good (80% continence) but technical problems require a mean number of 3 re-operations per patient (39). One review in the literature showed that long-term results of artificial urinary sphincter placement were better and more reproducible in terms of continence, preservation of voluntary voiding including CIC (Clean Intermittent Catheterization) and avoidance of bladder augmentation (34). Placement of an artificial sphincter does not rule out intermittent catheterization (39). Injection of bulking agents Injection of bulking agents at the level of the bladder neck increase passive resistance to urinary flow. The current popularity of injection (for the authors) is based on the materials used and the minimal invasiveness of the technique that can be carried out endoscopically. The most common materials now in use are Macroplastic® and Deflux®. Used alone or in combination with other techniques, these materials have a 30% success rate (40,41). Urinary diversion and continent cystotomy Urinary diversion and continent cystotomy is ultimate procedure for reinforcement of resistance since the bladder neck is divided. This technique has undergone many technical improvements according to the Mitrofanoff principle to allow creation of a catheterizable urinary stoma by anti-reflux reimplantation of the appendix or of a tubularized bowel segment (Monti) or a ureter. This procedure was initially used in patients in whom self-catheterization of the urethra was difficult due to obesity, poor eye–hand coordination or caretaker issues surrounding genital organ privacy. In a recent review of their continent stomas, Pippi Salle et al reported surgical revision in 39% of patients, including stomal revision in 18%, redo in 8%, bulking agent injection in 8% and prolapse correction in 4%. No statistically significant differences in complication rates were noted between appendix and tubularized bowel or different stoma locations (42). External urinary diversion External urinary diversion, once considered as an effective method to protect the upper tract, is now used only in special cases involving infants and young children that develop high intravesicular pressure syndrome (> 40 cm H2O during filling phase). The adverse effects of high pressure requires temporary

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but rapid decompression. The only other indications for external urinary diversion are in extreme situations and usually for social reasons (1, 3). Therapeutic indications

A succinct description of therapeutic strategies is difficult because incontinence can be compounded by a host of other problems associated with the underlying disease: digestive, sexual and orthopedic disorders. Emptying of the bladder and protection of the upper urinary tract The first step is to ensure adequate bladder emptying and to protect the upper urinary tract. In baby, the Crede or Vasalva method or, in case of reflux in small children, intermittent catheterization can be proposed. In cases strictly limited to vesicosphincteric dyssynergy, biofeedback training can be tried in the older patient. Surgical treatment of reflux more likely involves a Cohen crossed trigonal ureteral reimplantation more than the Leadbetter technique. Bilateral treatment of the reflux is performed in all cases. Subureteral injections (Teflon, collagen, or silicone gel) must be used as an alternative to surgery in young children or as a bridge therapy if a bladder surgery is planned at a later time. Improving bladder capacity The second phase consists of improving bladder capacity once complete bladder emptying has been enabled. If pharmacological treatment using anticholinergic agents fails, botulinum toxin followed in case of failure by bladder enlargement is mandatory. In our opinion, the preferred method is sigmoid plasty. We only use the stomach in association with the bowel in case of low-grade kidney insufficiency to alleviate ionic reabsorption problems. Necessary sphincter resistance If only a slight increase of the sphincter resistances is needed, our approach consists of injecting silicone gel in the bladder neck. If reinforcement is required during a bladder procedure (anti-reflux or cystoplasty), we prefer the Young-Dees or Pippi Salles procedure in boys in association with suspension of the bladder neck in girls. Once again endoscopic injection can enhance results in terms of residual continence. In our hands, the artificial sphincter remains an excellent tool especially in boys and more as the first line. Continent cystostomy is proposed to patients in whom micturition by natural passages is not easy, e.g., patients who are in wheelchairs or obese. Definitive closure of the bladder neck is performed only if bladder catheterization through the Mitrofanoff canal is fully functional. Optimizing the patient´s wellbeing Decision-making at each step of treatment must take into account the cooperation of the patient, his au-

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tonomy and the family situation. The adolescent period is even more difficult to manage and requires a global approach to digestive, sexual and orthopedic problems. Close cooperation between the different specialties is necessary to optimize the quality of the patient’s social life. Conclusion Management of neurogenic bladder in children is wrought with endless servitude for the patient and challenge without real victory for the paediatric surgeon. However, technology and techniques have improved and it is now possible to give a hopeful message to these patients and their families. Endoscopic management is the first option nowadays: we can treat vesico renal reflux, improve bladder compliance (botulinum toxin), and increase sphincterian resistances (neck injection) at the same operation. Instead of definitive surgery, electrical neuro stimulation (and particularly sacral nerve stimulation) became a valuable option. In 2011, therapy of urinary incontinence in neurogenic bladder can be considered as successful in more than 90% of our patients. REFERENCES 01. Guys JM, Aubert D: La vessie neurologique de l’enfant. Eds Sauramps Medical (Montpellier) 1998: 280 p 02. Genitori L, Caulheiro S, Lena G, et al: Spina bifida, myelo­ meningocele. Encycl Med Chir (Paris) Pediatrie 1993;4096 D 10 03. Stuart B: Neurogenic bladder: etiology and assessment. Bauer Pediatr Nephrol 2008;23:541–551 04. Adzick NS, Thom EA, Spong CY, et al: A randomized trial of prenatal versus postnatal repair of myelomeningocele. N Engl J Med 2011;364:993–1004 05. Mayer S, Weisser M, Till H, et al: Congenital myelomeningocele – do we have to change our management? Cerebrospinal Fluid Res 2010;7:17. Published online 2010 October 14;7:17 06. Guys JM, Simeoni-Alias J, Fakhro A, et al: Use of polydimethylsiloxane for endoscopic treatment of neurogenic urinary incontinence in children. J Urol 1999;162:2133–2135 07. Kuban KC, Leviton: A cerebral palsy. N Engl J Med 1994;330: 188–195 08. Guys JM, Fakhro A, Louis Borrione C, et al: Endoscopic treatment of urinary incontinence: long term evaluation of the results. J Urol 2001;165:389–392 09. Mitrofanoff P: Cystostomie continente trans-appendiculaire dans le traitement des vessies neurologiques. Chir Pediatr 1980;21:297–302 10. Bauer SB, Labib KB, Dieppa RA, et al: Urodynamic evaluation in a boy with myelodysplasia and incontinence. Urology 1977; 10:354–362 11. Wan J, Mc Guire EJ, Bloom DA, et al: Stress leak point pressure: a diagnostic tool for incontinent children. J Urol 1993;150: 700–702 12. Torre M, Planche D, Louis Borrione C, et al: Value of electrophysiological assessment after surgical treatment of spinal dysraphism. J Urol 2002:168:1759–1763 13. Torre M, Guida E, Bisio G, et al: Risk factors for renal function impairment in a series of 502 patients born with spinal dysraphisms. J Pediatr Urol 2011;7:39–43 14. Wyndaile JJ, Maes D: Clean intermittent self catheterization: a 12 years follow up. J Urol 1990;143:906–915 15. Edelstein RA, Bauer SB, Kelly MD, et al: The long-term urologic response of neonates with myelodysplasia treated proactively with intermittent catheterization and anticholinergic therapy. J Urol 1995;154:1500–1504

16. Schurch B, Stohrer M, Kramer G, et al: Botulinum-A toxin for treating detrusor hyperreflexia in spinal cord injured patients: a new alternative to anticholinergic drugs? Preliminary results. J Urol 2000;164:692–697 17. Riccabona M, Koen M, Schindler M, et al: Botulinum-A toxin injection into the detrusor : a safe alternative in the treatment of children with myelomeningocele with detrusor hyper­ reflexia. J Urol 2004;171:845–848 18. Altaweel W, Jednack R, Bilodeau C, Corcos J: Repeated intradetrusor botulinum toxin type A in children with neurogenic bladder due to myelomeningocele. J Urol 2006;175:1102–1105 19. Hoebeke P, De Caestecker K, Vande, Walle J, et al: The effect of botulinum-A toxin in incontinent children. J Urol 2006:176; 328–330 20. Do Ngog Thanh C, Audry G, Forin V: Botulinum toxin type A for neurogenic detrusor overactivity due to spinal cord lesions in children: a retrospective study of seven cases. J Pediatr Urol 2009; Dec 5 (6):430–436 21. Alova I, Margaryan M, Verkarre V, et al: Outcome of continence procedures after failed endoscopic treatment with dextranomerbases implants (Deflux®). J Pediatr Urol 2011 Jan 28 (Epub ahead of print) 22. Guys JM, Faure F, Kreitmann B, et al: L’entérocystoplastie dans les vessies neurologiques : peut-on améliorer les résultats? Chir Pediatr 1986;27:124–127 23. González R, Ludwikowski B, Horst M: Determinants of success and failure of seromuscular colocystoplasty lined with urothelium. J Urol 2009;182:1781–1784 24. Lima SV, Araujo LA, Vilar Fde O, Lima RS, Lima RF: Nonsecretory intestinocystoplasty: a 15-year prospective study of 183 patients. J Urol 2008;179:1113–1116 25. Metcalfe PD, Rink RC: Bladder augmentation: complications in the pediatric population. Curr Urol Rep 2007;8:152–156 26. Atala A: Tissue engineering of human bladder. Br Med Bull 2011;97:81–104 27. Hagerty JA, Richards I, Kaplan WE: Intravesical electrotherapy for neurogenic bladder dysfunction: a 22-year experience. J Urol 2007;178:1680–1683 28. MacDiarmid SA, Peters KM, Shobeiri SA, Wooldridge LS, et al: Long-term durability of percutaneous tibial nerve stimulation for the treatment of overactive bladder. J Urol 2010;183: 234–240 29. Peters KM, Macdiarmid SA, Wooldridge LS, et al: Randomized trial of percutaneous tibial nerve stimulation versus extendedrelease tolterodine: results from the overactive bladder innovative therapy trial. J Urol 2009;182:1055–1061 30. Capitanucci ML, Camanni D, Demelas F, et al: Long-term efficacy of percutaneous tibial nerve stimulation for different types of lower urinary tract dysfunction in children. J Urol 2009;182:2056–2061 31. Lordêlo P, Teles A, Veiga ML, et al: Transcutaneous electrical nerve stimulation in children with overactive bladder: a randomized clinical trial. J Urol 2010;184:683–689 32. Guys JM, Haddad M, Planche D, et al: J. Sacral neuromodulation for neurogenic bladder dysfunction in children. J Urol 2004;172:1673–1676 33. Haddad M, Besson R, Aubert D, et al: Sacral neuromodulation in children with urinary and fecal incontinence: a multicenter, open label, randomized, crossover study. J Urol 2010;184:696– 701 34. Kryger JV, Gonzalez R, Spencer Barthold J: Surgical management of urinary incontinence in children with neurogenic sphincteric incompetence. J Urol 2000;163:256–263 35. Castellan M, Gosalbez R, Labbie A, et al: Bladder neck sling for treatment of neurogenic incontinence in children with augmentation cystoplasty: long-term follow-up. J Urol 2005;173: 2128–2131 36. Hayes MC, Bulusu A, Terry T, Mouriquand PD, Malone PS: The Pippi Salle urethral lengthening procedure; experience and outcome from three United Kingdom centers. BJU Int 1999;84:701–705 37. Snodgrass W, Barber T: Comparison of bladder outlet procedures without augmentation in children with neurogenic incontinence. J Urol 2010;184:1775–1780 38. Churchill BM, Bergman J, Kristo B, Gore JL: Improved continence in patients with neurogenic sphincteric incompetence with combination tubularized posterior urethroplasty and fascial wrap: the lengthening, narrowing and tightening procedure. J Urol 2010;184:1763–1767

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Received: July 30, 2011