Curr Bladder Dysfunct Rep (2011) 6:100–109 DOI 10.1007/s11884-011-0084-9

Bladder Neck Dysfunction in Spinal Cord Injury Hann-Chorng Kuo

Published online: 11 March 2011 # Springer Science+Business Media, LLC 2011

Abstract Spinal cord injury (SCI) impairs the voluntary and autonomic control of storage and emptying functions of the urinary bladder, leading to a marked remodulation of the micturition reflex. Autonomic dysreflexia (AD) is found in SCI patients with a lesion level above T6. The occurrence of AD in SCI patients may also result in bladder neck dysfunction, which is often associated with AD and may cause bladder neck obstruction or inhibit detrusor contractility. Patients with bladder neck dysfunction may present with normal or underactive detrusor contractility, resulting in inefficient bladder emptying and prolonged AD. Using videourodynamic study, bladder neck dysfunction can be clearly demonstrated as a narrow bladder neck associated with a narrow external urethral sphincter and normal detrusor contractility. Medical treatment with α-adrenergic agents is the first-line treatment for patients with bladder neck dysfunction. If medical treatment fails, transurethral incision of the bladder neck is indicated to relieve bladder outlet obstruction and to resume spontaneous detrusor contractility. Keywords Spinal cord injury . Sympathetic activity . Detrusor-sphincter dyssynergia . Urinary incontinence . Bladder outlet obstruction

Introduction Spinal cord injury (SCI) results in impairment of sensory and motor function of the limbs and visceral function. H.-C. Kuo (*) Department of Urology, Buddhist Tzu Chi General Hospital and Tzu Chi University, 707, Section 3, Chung Yang Road, Hualien, Taiwan e-mail: [email protected]

Patients with suprasacral cord SCI may develop detrusor hyperreflexia and dyscoordinated sphincter function (detrusorsphincter dyssynergia [DSD]). Patients with cords above the mid-thoracic level may have autonomic dysreflexia (AD) and bladder neck dyssynergia (dysfunction). Recent studies also revealed that failed urethral stent treatment of DSD may be caused by persistent bladder neck dysfunction, and patients with detrusor underactivity after the recovery period may resume detrusor contractility following transurethral bladder neck incision. This article reviews recent research on bladder neck dysfunction in SCI.

Normal Micturition Function The functions of the lower urinary tract are storage and periodic release of urine. These functions are dependent on complex neural control, which involves the brain, spinal cord, and peripheral ganglia [1]. Normal micturition also depends on the integration of autonomic and somatic efferent mechanisms within the lumbosacral spinal cord [2]. During urine storage, the bladder outlet is closed, including the bladder neck, urethral smooth muscle, and periurethral striated sphincter, and the detrusor muscle is quiescent; thus, the bladder can be filled gradually with urine, and a low intravesical pressure is maintained. During voiding, the bladder outlet is relaxed and the detrusor contracts, generating a sustained pressure that pushes the urine out of the bladder. Inadequate detrusor contractility, increased bladder neck resistance, prostatic urethral obstruction in men, as well as inadequate relaxation of the periurethral striated muscles will result in failure to empty. Overactive bladder, an incompetent bladder neck, or an incompetent urethral sphincter, on the other hand, may result in failure to store [3].

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Studies in animals have revealed that the micturition reflex is mediated by a spinobulbospinal pathway under a coordination center—the pontine micturition center—located in the rostral brainstem, and further modulated by a higher center in the cerebral cortex [4]. Bulbospinal pathways from the pons may be responsible for maintaining the normal reciprocal relationship between the bladder and urethral sphincter [5]. During bladder filling, the sympathetic system inhibits bladder activity and excites to increase urethral tone. The sympathetic reflex provides negative feedback to the bladder. Increased bladder pressure tends to increase the inhibitory input to the smooth muscle of the bladder and to increase sympathetic excitatory input to the bladder base and urethra. Thus, the bladder volume can be increased without it resulting in detrusor contraction or urinary incontinence [6]. Bladder sensation is mediated by small, myelinated A-δ afferents and unmyelinated C fibers. These sensory fibers convey signals received from receptors in the bladder muscle and urothelia to second-order neurons in the spinal cord [2]. When the bladder is filled to a certain volume, an individual can feel the sensation first of the bladder filling, followed by fullness, urge to void, or even pain at an extremely high volume. Under normal conditions, although the bladder is fully distended, detrusor contractions will not occur unless the micturition center commands to relax the urethral sphincter. The bulbospinal pathway from the pons is responsible for the relationship between the bladder and urethral-striated sphincter activity. The pathway functions as an on–off switch [4]. Activation of the bulbospinal pathway starts from a critical level of afferent activity of the bladder, followed by inhibition of the urethral sphincter activity. A study of rat urethral muscle revealed that coordinated external urethral sphincter function (bursting activity) in the male rat is dependent on supraspinal pathways, and that the urethral smooth muscle response during voiding is composed of a predominantly cholinergic, atropine-sensitive contraction, as well as a nitric oxidemediated relaxation [7].

Changes in Lower Urinary Tract Function After Spinal Cord Injury SCI impairs the voluntary and autonomic control of storage and emptying functions of the urinary bladder, leading to a marked remodulation of the micturition reflex. SCI at the level above the sacral cords (upper motor neuron type) initially leads to a spinal shock stage, followed by a recovery phase. During the spinal shock phase, the detrusor is in a state of flaccid paralysis. The detrusor activity reappears slowly after about 2 to 12 weeks. The bladder becomes hyperreflexic due to the emergence of a spinal micturition reflex pathway. The activities of urethral-striated and smooth muscles rapidly

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recover after SCI. Because the urethral tone is present and the detrusor contractility does not recover completely, patients usually have to urinate via intermittent catheterization of an indwelling Foley catheter [8]. After the recovery period, detrusor contractility increases and urinary incontinence may occur, depending on the urethral sphincteric tone. In patients with a suprasacral cord lesion, the bladder is partially emptied due to unsustained detrusor contractions and the development of simultaneous contraction of the urethral sphincter during voiding, so-called DSD [9]. DSD results in high intravesical pressure and bladder trabeculation, vesicoureteral reflux, urothelial damage that causes frequent urinary tract infection (UTI), as well as upper urinary tract dilatation and hydronephrosis [2, 8]. SCI at the cervical or thoracic levels disrupts voluntary voiding. The recovery of bladder function after SCI is dependent in part on the plasticity of bladder afferent pathways and the unmasking of reflexes triggered by unmyelinated, capsaicin-sensitive, C-fiber bladder afferent neurons. Plasticity is associated with morphologic, chemical, and electrical changes in bladder afferent neurons and appears to be mediated in part by neurotrophic factors released in the spinal cord and the peripheral target organs [10•]. AD is an acute syndrome characterized by inappropriate and massive autonomic response that occurs in patients with SCI above the T6 level. AD is characterized by hypertension, bradycardia, sweating, and flushing below the lesion level. In severe cases, cerebrovascular hemorrhage may also occur [8]. AD can be induced by stimuli below the SCI level, such as bladder distention, fecal impaction, or UTI. During urodynamic study, AD is frequently encountered and should be carefully managed to prevent inadvertent complications [11]. The relationship between urodynamic data and dysreflexia crisis shows that the presence of detrusor-uninhibited contractions and bladder distention can stimulate the AD crisis. SCI significantly impairs psychological and physical aspects of female sexual arousal. In addition, bladder and bowel incontinence and AD can negatively impact sexual activity and intercourse. SCI influences psychogenic as well as physical components of female sexual functioning [12].

Bladder Neck Dysfunction: Possible Neurological Alteration in Spinal Cord Injury Bladder neck dysfunction is defined as an incomplete opening of the bladder neck during voluntary or involuntary voiding. It also has been called internal sphincter dyssynergia, primary bladder neck obstruction, and dysfunctional bladder neck. Bladder neck dysfunction may be observed in non-neurogenic as well as neurogenic voiding

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dysfunction [13]. Neurohistochemical and electron microscopic techniques reveal that many cholinergic nerves supply the bladder neck and female proximal urethra. The male proximal urethra is supplied richly with noradrenergic nerves, indicating that the region is under direct sympathetic control and functions to prevent vesical reflux of ejaculate [14]. Because sympathetic innervation is mediated by αadrenergic receptors extending from the bladder neck to the external sphincter, it has been suggested that the sympathetically innervated smooth muscle exerts a certain activity along the whole length of the proximal urethra [15]. Sympathetic dyssynergia is believed to be closely associated with external striated sphincter dyssynergia, pharmacologic manipulation with an α-adrenolytic agent, or radical transurethral resection of the prostate, uniformly resulting in the relief of sympathetic dyssynergia [16]. AD is found in SCI patients with a lesion level above T6 [17]. It has been proposed that the bladder neck may be the origin of the sympathetic hyperactivity. The occurrence of AD in patients with SCI lesions above T6 may also point to the presence of bladder neck dysfunction [18]. Detrusor, bladder neck, and urethral sphincter dysfunction are usually characterized as motor neuron diseases corresponding to damage to the spinal cord [19]. DSD, or detrusor-bladder neck dyssynergia may result in SCIinduced voiding dysfunction with or without AD. The effect of SCI on lower urinary tract dysfunction depends on the level of cord lesion. The incidence of neurogenic bladder neck dysfunction is very similar to that of DSD. The incidence of DSD is highest in high thoracic SCI (67%) and second highest in low thoracic SCI (56%), followed by cervical SCI (43%), and finally lumbar SCI (20%). Incidence of bladder neck dysfunction is also highest in high thoracic SCI (27%), second highest in low thoracic SCI (22%), and followed by cervical SCI (7%). No bladder neck dysfunction is seen in lumbar SCI [20]. The influence of sympathetic and pudendal nerve hyperactivity on the detrusor nucleus in sacral cords may be enhanced after SCI, thereby inducing bladder dysfunction and DSD. Pudendal nerve stimulation evoked somatic responses in the external urethral sphincter and autonomic responses in the smooth muscle sphincter controlling the bladder neck. Somatic afferent fibers of the pudendal nerve are supposed to project on sympathetic thoracolumbar neurons to the bladder neck and modulate their function. Afferent fibers of the pudendal nerve are postulated to have a potential modulatory effect on sympathetic neurons controlling the bladder neck function in neurogenic or non-neurogenic bladder [21]. In patients with mixed pathology and an underactive detrusor during urodynamic study, residual urine is hypothesized to be the result of fading detrusor contractility. Incomplete activation of the micturition reflex

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resulting in incomplete stimulation of the detrusor and incomplete relaxation of the urethral closure mechanism are postulated [22]. SCI impairs the voluntary and autonomic control of the storage and emptying functions of the urinary bladder, leading to a marked remodulation of the micturition reflex [2]. Although detrusor contractility recovers gradually after the initial spinal shock phase, the activity of the external sphincter and bladder neck activity increase, resulting in DSD and bladder neck dyssynergia. The major bladder outlet resistance is at the level of the external urethral sphincter [23]. DSD is thought to represent interruption of suprasacral pathways connecting the pontine and sacral micturition centers in SCI. Patients with DSD are at risk of urologic complications because the intravesical pressure increases during bladder filling and voiding [24]. A previous study suggested that sympathetic innervation may play a role in the activation of the external urethral sphincter [25]. Increased sympathetic activity is always associated with DSD in high thoracic or cervical level SCI. However, in real life clinical practice, not all SCI patients with DSD have bladder neck dysfunction. We have observed a typical group of patients maintaining low detrusor contractility after SCI even though the somatic reflexes have returned. It is possible that the influence on the detrusor nucleus by the increased pudendal or sympathetic activity persists, and therefore, the efficient voiding cannot be achieved. Bladder neck dysfunction and bladder neck contracture are different disease entities. The latter is an organic fibrosis, and the former is an accentuated sympathetic nervous function, or detrusor bladder neck dyssynergia. It is not clear whether detrusor bladder neck dyssynergia is responsible for bladder neck contracture in patients without neurogenic bladder. In a study designed to determine (by means of video urodynamics) whether bladder neck contracture would be of the same nature as detrusor bladder neck dyssynergia in non-neurogenic bladder patients, detrusor bladder neck dyssynergia was not thought to be a major factor in voiding dysfunction in bladder neck contracture in non-neurogenic bladder patients [26]. The sympathetic hyperactivity may be further activated in patients with SCI above the sympathetic nucleus level (T10–L2) and results in bladder neck dysfunction.

Urodynamic Study of Bladder Neck Dysfunction in Spinal Cord Injury To assess vesicourethral dysfunction in SCI patients, videourodynamic study is considered the first choice of investigation [27]. Patients with DSD may have a dilated bladder neck and proximal urethra during detrusor contrac-

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tion. Significant disagreement has been found between needle electromyography and voiding cystourethrography regarding a positive diagnosis of DSD. A combination of electromyography and voiding cystourethrography may identify more cases of DSD than either modality alone [28]. Using videourodynamic study, bladder neck dysfunction can be clearly demonstrated as a narrow bladder neck associated with a narrow external urethral sphincter and normal detrusor contractility (Fig. 1). Detrusor bladder neck dyssynergia can be diagnosed as any detrusor contraction accompanied by a closed bladder neck on fluoroscopy, a bladder neck pressure of at least 5 cm H2O above the intravesical contraction pressure, and a simultaneous decrease in the external sphincter pressure using a triple lumen catheter. Bladder neck dyssynergia can also be diagnosed when the bladder neck is noted to be incompletely or intermittently open during voiding, and a voiding urethral pressure profile discloses a pressure difference of 10 cm H2O across the bladder neck. A significantly higher resting detrusor pressure differential was found among the patients with bladder neck dyssynergia, suggesting sympathetic dysfunction and poor accommodation secondary to adrenergic detrusor neoinnervation [20]. We investigated 22 patients with thoracic or cervical SCI using videourodynamics. All the patients with cervical SCI had AD, and 44.4% with thoracic SCI reported AD. Ten patients had a baseline detrusor pressure (Pdet) greater than 15 cm H2O, five had a Pdet less than 15 cm H2O, and seven showed detrusor underactivity. Cinefluoroscopy during the voiding phase revealed no flow in 16 patients, and a nonfunneling appearance of the bladder neck was noted in all patients with bladder neck dysfunction [29•]. Patients with bladder neck dysfunction may have a high detrusor pressure, a low detrusor pressure, or underactive detrusor

Fig. 1 Videourodynamic study in a patient with cervical spinal cord injury and detrusor-sphincter dyssynergia and bladder neck dysfunction. The bladder neck and external urethral sphincter remain narrow during detrusor hyperreflexic contractions

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(Fig. 2). This finding is comparable with that of a previous study, in which patients with thoracic SCI, although they displayed the highest overall incidence of dyssynergia, also displayed the lowest detrusor pressure [20]. Patients with high thoracic or cervical SCI typically have a hyperreflexic detrusor contraction during cystometry. However, detrusor areflexia has been found in a group of suprasacral SCI patients. In this group of patients who have an intact sacral reflex arc, detrusor contractility is likely to return after a mean of 16.6 months from the date of injury [30]. The reason for inadequate detrusor contractility or the delay in recovery of detrusor function is likely a parasympathetic inhibitory effect of the detrusor nucleus exerted via sympathetic hyperactivity [19]. To directly measure active closure of the bladder neck during bladder contraction that results in bladder neck dyssynergia and outflow obstruction, Schurch et al. [31] investigated 34 SCI patients with two microtransducer catheters in the urethrovesical and anorectal regions, respectively. The respective roles of the striated and smooth muscles on bladder neck activity were evaluated after pudendal nerve blocks and phentolamine injections. Pressures were higher in the bladder neck than in the bladder in 25 patients with bladder neck dyssynergia. Pudendal blocks abolished detrusor-sphincter, but not bladder neck dyssynergia. Additional phentolamine treatment abolished bladder neck dyssynergia associated with autonomic hyperreflexia [31]. In non-neurogenic bladder neck dysfunction, differential diagnosis of the bladder neck dyssynergia and contracture may not be easy. A bladder neck diameter smaller than 0.75 cm on voiding cystourethrography was regarded as having a bladder outlet obstruction localized at the bladder neck. Detrusor bladder neck dyssynergia was defined in

104 Fig. 2 Bladder neck dysfunction in high-level spinal cord injury patients, showing normal detrusor contractility (a), low detrusor contractility (b), and detrusor underactivity (c), is associated with a narrow bladder neck

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cases in which pressures were higher at the level of the bladder neck than in the bladder during detrusor contraction [26]. For patients with bladder neck contracture, endoscopic intervention to relieve the bladder neck obstruction (anatomic obstruction) is necessary, whereas α-blocker therapy may be adequate in abolishing bladder neck dyssynergia in patients with bladder neck dysfunction (functional obstruction). During videourodynamic study, detrusor bladder neck dyssynergia was found at the beginning and end of micturition, but not at the time of maximum flow. The condition of bladder neck dyssynergia may disappear following terazosin treatment.

Clinical Impact of Bladder Neck Dysfunction on Spinal Cord Injury Bladder neck dysfunction causes bladder outlet obstruction in patients with high thoracic or cervical SCI. Because bladder neck dysfunction is always associated with DSD, it may represent a more severe form of sympathetic hyperactivity. In SCI patients with bladder neck dysfunction, opening of the bladder neck during the start of micturition is delayed; therefore, patients may have prolonged autonomic hyperreflexia and more difficulty urinating. The postvoid residual urine volume increases, and patients need an α-adrenergic blocker to relieve their AD symptoms. Early identification of bladder neck dysfunction is important to prevent further urologic complications, such as UTI or upper urinary tract exacerbation.

Conservative Management of Bladder Neck Dysfunction in Spinal Cord Injury In treatment of bladder neck dysfunction, α-adrenergic blockers are effective in relieving sympathetic activity and decreasing the severity of AD. Phenoxybenzamine has been proven useful in reducing bladder outlet resistance after SCI, provided that detrusor bladder contractions were present. It is useful in controlling DSD and autonomic hyperreflexia. However, phenoxybenzamine was not useful in treatment of areflexic bladders [32]. Other α-adrenergic blockers, such as terazosin, also proved effective in treating voiding difficulty in patients with SCI. A total of 15 normotensive SCI patients with DSD were treated with terazosin (5 mg nightly) [33]. Voiding pressure before and during terazosin therapy showed no significant decrease. After subsequent external sphincterotomy or sphincter stent placement, however, voiding pressure was reduced significantly. Patients who improved with terazosin treatment were demonstrated to have obstruction only at the bladder neck,

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with no evidence of obstruction at the external sphincter. Patients who failed to improve were found to have an open bladder neck but obstruction at the external sphincter. Urethral stenting using the UroLume Wallstent (American Medical Systems, Minnetonka, MN) is effective in the management of DSD in patients with SCI and is an acceptable long-term (up to 20 years) alternative to sphincterotomy [34•]. After treatment of DSD with a temporary urethral sphincter stent, 70.7% of patients subsequently require a permanent urethral sphincter stent. This period of time allows for selection of patients unlikely to benefit from permanent urethral sphincter stent [35]. The failures manifest within the first few years and can be managed easily with stent removal without significant problems. However, after UroLume stenting for DSD, bladder neck dyssynergia remained a long-term problem still to be solved. Bladder neck incision usually can treat this condition successfully [34•]. In a series of 153 SCI patients with DSD who received UroLume insertion, a total of 13 patients (8.5%) required a subsequent operation for bladder neck obstruction [36].

Surgical Management of Bladder Neck Dysfunction in Spinal Cord Injury When medical treatment fails to improve AD or voiding difficulty, surgical intervention using transurethral incision of the bladder neck (TUI-BN) is mandatory. In patients with a severe form of DSD, external urethral sphincterotomy is indicated to decrease intravesical pressure and to allow spontaneous voiding. TUI-BN was performed with an adult resectoscope and diathermy electrode using a 110-W cutting current. Double incisions were made at the 5-o’clock and 7-o’clock positions of the bladder neck in an attempt to see the serosal layer. The external urethral sphincter was not targeted (Fig. 3). Patients were catheterized with a Foley catheter for 2 days after the procedure [29•]. After TUI-BN, bleeding is a potential complication. Careful hemostasis should be achieved using electrocauterization. AD during a TUI-BN procedure or after surgery is possible. Ideally, spinal anesthesia should be used to prevent the occurrence of AD. If not, general anesthesia with careful monitoring of cardiopulmonary function is mandatory. Nifedipine administered sublingually or orally 30 min before the procedure has been reported to prevent or alleviate AD in patients with sympathetic hyperreflexia [37]. TUI-BN is usually performed concurrently. However, normal detrusor contractility is necessary to yield a therapeutic effect after TUI-BN. Patients with areflexic detrusor have been reported to be unable to void spontaneously after TUIBN [20]. Lockhart et al. [38] investigated 15 SCI patients

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Fig. 3 Transurethral incision of the bladder neck. Double incisions were made at the 5-o’clock (a) and 7-o’clock (b) positions of the bladder neck in an attempt to see the serosal layer. The external urethral sphincter was not targeted

who failed with external urethral sphincterotomy. Failure was established when symptomatic UTIs and high postvoid residual persisted. Urodynamic findings demonstrated detrusor areflexia in ten patients (66%), DSD in 2 (13.2%), detrusor hyperreflexia with unsustained bladder contractions in 1 (6.6%), and detrusor hyperreflexia and bladder neck obstruction in 2 (13.2%). Among these failures, poor detrusor contractility predominated. TUI-BN may be necessary in these types of patients when an external sphincterotomy is performed [38]. Al-Ali and Haddad [39] reported the outcome of transurethral resection of the external sphincter and/or bladder neck in a retrospective analysis of 82 SCI patients, and a prospective study was conducted on the other 43 SCI patients. About 8% of SCI patients had an outlet obstruction that required endoscopic treatment. They demonstrated that patients with a complete SCI at any level, and those with a high incomplete lesion (above T9) have benefited from external sphincterotomy combined with TUI-BN. Patients with a low incomplete lesion (T9 and below) have benefited from bladder neck resection alone. Bladder neck (internal sphincter) obstruction or dyssynergia should be considered in the management of the neuropathic bladder resulting from suprasacral SCI [39]. A videourodynamic study is essential to make an accurate diagnosis of bladder neck obstruction in SCI patients with DSD [27]. Blind bladder neck resection without prior urodynamic evaluation has been found to be useless in achieving therapeutic effect in these patients [40].

Improvement in Detrusor Function After Transurethral Incision of the Bladder Neck for Bladder Neck Dysfunction in Spinal Cord Injury In a recent study, Ke and Kuo [29•] found that TUI-BN was effective in restoring spontaneous voiding, increasing maximum flow rate, and decreasing postvoid residual in

high-level SCI patients. TUI-BN also leads to reduction in bladder outlet resistance, reduction in occurrence of AD episodes, and improvement in quality of life [29•]. Among 22 SCI patients with videourodynamics-proven bladder neck dysfunction and TUI-BN, spontaneous voiding resumed immediately after catheter removal in nine patients (41%), recovered within 1 week in six patients (27%) and recovered within 1 month in four patients (18%). Urinary retention persisted in four patients (18%). In ten patients with Pdet greater than 15 cm H2O, Pdet and postvoid residual decreased and maximum flow rate increased significantly after TUIBN. In 12 patients with a baseline Pdet less than 15 cm H2O, Pdet and maximum flow rate increased and postvoid residual decreased after TUI-BN (Fig. 4). An open urethral sphincter during voiding was noted in 19 patients (86.4%) after TUIBN. Among them, the clinical signs of DSD resolved completely in six patients. Among the 17 patients with preoperative AD, the degree of AD during micturition became less severe or disappeared in 15 (88.2%). The pathophysiology that bladder neck can affect on detrusor contractility in SCI patients has not been fully elucidated. Interestingly, after TUI-BN, not only is the AD relieved, but so are the signs of DSD. It is possible that a urethra-to-bladder neck reflex pathway exists that coordinates the function between these two muscles. Patients with high thoracic level SCI may have sympathetic hyperactivity that not only induces bladder neck dysfunction but also a tight urethral sphincter [25]. Only under this condition can TUI-BN relieve bladder neck obstruction and urethral sphincter resistance and allow the patients to resume spontaneous voiding. The results of this study demonstrated that TUI-BN is effective for treating bladder neck dysfunction in patients with high-level SCI. Voiding efficiency and detrusor contractility can be improved significantly after TUI-BN. TUI-BN was not only beneficial in decreasing detrusor voiding pressure and increasing maximum flow rate in patients with bladder neck obstruction, but also in

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Fig. 4 Videourodynamic study in a patient with detrusor underactivity and closed bladder neck at baseline (a) and resumption of normal detrusor contractility and wide-open bladder neck after transurethral incision of the bladder neck (b)

improving detrusor contractility in SCI patients with underactive bladder. It has been proposed that the bladder neck—but not the external sphincter—may be the origin of sympathetic hyperactivity in patients with SCI above level T9. Sympathetic hyperactivity may inhibit detrusor contractility at the spinal cord level [19]. TUI-BN may be capable of interrupting the hyperactive sympathetic response through the afferent nerves that inhibit the parasympathetic activity at the ganglionic level or detrusor nucleus in the spinal cord. Animal studies using the bilateral section of the

hypogastric nerves, which provide the major sympathetic input to the urinary bladder neck/proximal urethra, could show improved voiding via the reduction of urethral resistance in conscious, female SCI rats 2 to 3 weeks after T7 to T9 transection of the spinal cord [41]. The inhibitory effect of sympathetic nerves on detrusor contractility has been proposed to account for the improvement in voiding efficiency after α-adrenergic blocker therapy. In SCI patients with a lesion above T9, the sympathetic activity abnormally increases, resulting in a strong inhibition of detrusor contractility. Previous studies

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also demonstrated patients with high thoracic SCI may have low detrusor pressure or underactive detrusor [20]. The recovery period is also prolonged [29•]. Therefore, for patients with high-level SCI who continue to demonstrate detrusor underactivity and bladder neck dysfunction, TUIBN is likely an effective procedure to help them resume earlier spontaneous voiding.

Conclusions Bladder neck dysfunction is a sign of sympathetic hyperactivity in patients with high-level SCI. It is often associated with AD and may cause bladder neck obstruction or inhibit detrusor contractility. The bladder neck obstruction results in difficult bladder emptying and severe AD during micturition. The inhibitory effect of sympathetic hyperactivity, on the other hand, may inhibit detrusor contractions and cause urinary retention. α-Adrenergic blockers or clean intermittent catheterization should be given as first-line treatment. If medical treatment fails, TUIBN is an effective surgical procedure for restoring spontaneous voiding and reducing the occurrence of AD episodes.

Disclosure No potential conflict of interest relevant to this article was reported.

References Papers of particular interest, published recently, have been highlighted as: • Of importance 1. de Groat WC. Mechanisms underlying the recovery of lower urinary tract function following spinal cord injury. Paraplegia. 1995;33:493–505. 2. Chancellor MB, Yoshimura N. Physiology and pharmacology of the bladder and urethra. In: Walsh PC, Retik AB, Vaughn ED, Wein AJ, editors. Campbell’s urology. Philadelphia: Saunders; 2002. p. 831–86. 3. Wein AJ. Pathophysiology ad categorization of voiding dysfunction. In: Walsh PC, Retik AB, Vaughn ED, Wein AJ, editors. Campbell’s urology. Philadelphia: Saunders; 2002. p. 887–99. 4. de Groat WC. Nervous control of the urinary bladder of the cat. Brain Res. 1975;87:201–11. 5. Holstege G, Griffiths D, deWall H, Dalm E. Anatomical and physiological observations on supraspinal control of bladder and urethral sphincter muscles in cats. J Comp Neurol. 1986;250:449. 6. de Groat WC, Lalley PM. Reflex firing in the lumbar sympathetic outflow to activation of vesical afferent fibers. J Physiol (London). 1972;226:289–309.

Curr Bladder Dysfunct Rep (2011) 6:100–109 7. Kakizaki H, Fraser MO, de Groat WC. Reflex pathways controlling urethral striated and smooth muscle function in the male rat. Am J Physiol. 1997;272:R1647–56. 8. Fam B, Yalla SV. Vesicourethral dysfunction in spinal cord injury and its management. Semin Neurol. 1988;8:150–5. 9. de Groat WC, Yoshimura N. Mechanisms underlying the recovery of lower urinary tract function following spinal cord injury. Prog Brain Res. 2006;152:59–84. 10. • de Groat WC, Yoshimura N. Changes in afferent activity after spinal cord injury. Neurourol Urodyn 2010;29:63–76. This article reviews the anatomic, immunohistochemical, and pharmacologic studies of normal and dysfunctional bladder afferent pathways. The plasticity of afferent nerves after SCI alters the bladder function. 11. Giannantoni A, Di Stasi SM, Scivoletto G, Mollo A, Silecchia A, Fuoco U, et al. Autonomic dysreflexia during urodynamics. Spinal Cord. 1998;36:756–60. 12. Anderson KD, Borisoff JF, Johnson RD, Stiens SA, Elliott SL. Spinal cord injury influences psychogenic as well as physical components of female sexual ability. Spinal Cord. 2007;45:349–59. 13. Blaivas JG, Norten LJ. Primary bladder neck obstruction. World J Urol. 1984;2:191–5. 14. Gosling JA, Dixon JS, Lendon RG. The autonomic innervation of the human male and female bladder neck and proximal urethra. J Urol. 1977;118:302–5. 15. Awad SA, Downie JW, Lywood DW, Young RA, Jarzylo SV. Sympathetic activity in the proximal urethra in patients with urinary obstruction. J Urol. 1976;115:545–7. 16. Koyanagi T, Arikado K, Takamatsu T, Tsuji I. Relevance of sympathetic dyssynergia in the region of external urethral sphincter: possible mechanism of voiding dysfunction in the absence of (somatic) sphincter dyssynergia. J Urol. 1982;127:277–82. 17. Awad SA, Downie JW. Sympathetic dyssynergia in the region of the external sphincter: a possible source of lower urinary tract obstruction. J Urol. 1977;118:636–40. 18. Fam BA, Sarkarati M, Yalla SV, et al. Spinal cord injury. In: Yalla SV, McGuire EJ, Elbadawi A, et al., editors. Neurourology and urodynamics. New York: Macmillan; 1988. p. 291–302. 19. de Groat WC, Booth AM. Inhibition and facilitation in parasympathetic ganglia of the urinary ladder. Fed Proc. 1980;39:2990–6. 20. Krongrad A, Sotolongo JR. Bladder neck dyssynergia in spinal cord injury. Am J Phys Med. 1996;75:204–7. 21. Reitz A, Schmid DM, Curt A, Knapp PA, Schurch B. Afferent fibers of the pudendal nerve modulate sympathetic neurons controlling the bladder neck. Neurourol Urodyn. 2003;22:597–601. 22. Giffiths DJ. Residual urine, underactive detrusor function, and the nature of detrusor sphincter dyssynergia. Neurourol Urodyn. 1983;2:289–94. 23. Blaivas JG, Sinha HP, Zayed AAH, et al. Detrusor-external sphincter dyssynergia: a detailed electromyographic stud. J Urol. 1980;125:545–8. 24. Elbadawi A, Schenk EA. A new theory of the innervation of bladder musculature. Part 4. Innervation of the urethrovesical junction and external urethral sphincter. J Urol. 1974;111:613–5. 25. Yalla B, Rosier AB, Fam BA. Functional contribution of autonomic innervation to urethral striated sphincter. Studies with parasympathomimetic, parasympatholytic and alpha-adrenergic blocking agents in spinal cord injury and control male subjects. J Urol. 1977;117:493–9. 26. Yamanishi T, Yasuda K, Sakakibara R, Hattori T, Tojo M, Ito H. The nature of detrusor bladder neck dyssynergia in non-neurogenic bladder dysfunction. J Auton Nerv Syst. 1997;66:163–8. 27. Virseda CM, Salinas CJ, Allona AA, et al. Involvement of bladder neck and periurethral sphincter in dyssynergia in patients with spinal cord injury. Arch Esp Urol. 2002;55:293–302. 28. De EJ, Patel CY, Tharian B, Westney OL, Graves DE, Hairston JC. Diagnostic discordance of electromyography (EMG) versus

Curr Bladder Dysfunct Rep (2011) 6:100–109

29.

30. 31. 32.

33.

34.

voiding cystourethrogram (VCUG) for detrusor-external sphincter dyssynergy (DESD). Neurourol Urodyn. 2005;24:616–21. • Ke QS, Kuo HC. Transurethral incision of the bladder neck to treat bladder neck dysfunction and voiding dysfunction in patients with high-level spinal cord injuries. Neurourol Urodyn 2010;29:748– 52. TUI-BN is effective in restoring spontaneous voiding and reducing the occurrence of autonomic dysreflexia in high-level SCI patients. Light JK, Faganel J, Beric A. Detrusor areflexia in suprasacral spinal cord injury. J Urol. 1985;134:295–7. Schurch B, Yasuda K, Rossier AB. Detrusor bladder neck dyssynergia revisited. J Urol. 1994;152:2066–70. Al-Ali M, Salman G, Rasheed A, Al-Ani G, Al-Rubaiy S, Alwan A, et al. Phenoxybenzamine in the management of neuropathic bladder following spinal cord injury. Aust N Z J Surg. 1999;69:660–3. Chancellor MB, Erhard MJ, Rivas DA. Clinical effect of alpha-1 antagonism by terazosin on external and internal urinary sphincter function. J Am Paraplegia Soc. 1993;16:207–14. • Abdul-Rahman A, Ismail S, Hamid R, Shah J. A 20-year follow-up of the mesh wallstent in the treatment of detrusor external sphincter dyssynergia in patients with spinal cord injury. BJU Int. 2010;106:1510–3. Patients who develop bladder neck dyssynergia

109

35.

36.

37.

38. 39.

40. 41.

after long-term urethral Wallstent placement for DSD can be successfully treated with bladder neck incision. Gamé X, Chartier-Kastler E, Ayoub N, Even-Schneider A, Richard F, Denys P. Outcome after treatment of detrusor-sphincter dyssynergia by temporary stent. Spinal Cord. 2008;46:74–7. Chancellor MB, Rivas DA, Linsenmeyer T, et al. Multicenter trial in North America of UroLume urinary sphincter prosthesis. J Urol. 1994;152:924–30. Krassioukov A, Warburton DE, Teasell R, Eng JJ, Spinal Cord Injury Rehabilitation Evidence Research Team. A systematic review of the management of autonomic dysreflexia after spinal cord injury. Arch Phys Med Rehabil. 2009;90:682–95. Lockhart JL, Vorstman B, Weinstein D, Politano VA. Sphincterotomy failure in neurogenic bladder disease. J Urol. 1986;135:86–9. Al-Ali M, Haddad L. A 10 year review of the endoscopic treatment of 125 spinal cord injured patients with vesical outlet obstruction: does bladder neck dyssynergia exist? Paraplegia. 1996;34:34–8. Derry F, Al-Rubeyi S. Audit of bladder neck resection in spinal cord injured patients. Spinal Cord. 1998;36:345–8. Yoshiyama M, de Groat WC. Effect of bilateral hypogastric nerve transection on voiding dysfunction in rats with spinal cord injury. Exp Neurol. 2002;175:191–7.