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10.14440/bladder.2024.0012
Review Article
Bladder dysfunction following stroke: An updated review on diagnosis and management
Agapiou Eleni 1 2
Pyrgelis Efstratios-Stylianos 1 3 *
Mavridis Ioannis N. 1 4
Meliou Maria 1
Wimalachandra Welege Samantha Buddhika 1
1 C.N.S. Alliance Research Group, Athens, Greece
2 Department of Physical Medicine and Rehabilitation, “Asklipieion Voulas” General Hospital, Voula, Athens, Greece
3 First Department of Neurology, School of Medicine, National and Kapodistrian University of Athens, Eginition Hospital, Athens, Greece
4 Department of Neurosurgery, School of Medicine, Democritus University of Thrace, University General Hospital of Alexandroupolis, Alexandroupoli, Greece
*Corresponding author: Efstratios-Stylianos Pyrgelis (stratospyrg@yahoo.gr)
2024
23 8 2024
11 1 e2120000501 7 2024
28 7 2024
07 8 2024
© 2024 Bladder, All rights reserved.
2024
https://creativecommons.org/licenses/by-nc-sa/4.0/ This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License: http://creativecommons.org/licenses/by-nc-sa/4.0
Bladder dysfunction represents a frequent and important clinical problem in stroke patients. The aim of this narrative review was to explore the currently available information regarding the diagnosis and management of bladder dysfunction following stroke. The most common symptoms of bladder dysfunction following stroke are urinary incontinence, urgency, increased frequency, and difficulty voiding. Medical history, including voiding diary, physical examination, and urodynamic studies are useful in establishing diagnosis. Bladder pressure in stroke patients with detrusor overactivity is rarely high enough to damage the upper urinary tract. In neurogenic bladder, however, there is always a risk for transmission of intravesical pressure to the upper tract. In incontinent patients, urodynamic studies can reveal bladder hyper- or hyporeflexia, detrusor overactivity with impaired contractility or detrusor-sphincter dyssynergia, or even no abnormalities at all. With stroke patients with urinary dysfunction, establishing a proper diagnosis is of paramount importance to start appropriate treatment, prevent upper tract damage, maintain continence, and ensure complete emptying. After diagnosis, an individually tailored treatment plan is mandatory, including behavioral techniques, lifestyle interventions, and anticholinergic medication. Other therapeutic choices include alternative drugs, intradetrusor injection of botulinum toxin, and spinal neuromodulation. A bladder rehabilitation program is essential for improving post-stroke lower urinary symptoms and depends on the patient’s awareness, cooperation, and independence. Bladder dysfunction after stroke, as a strong prognostic factor of disability, exerts an enormous impact on health and economy. Therefore, every single effort toward a proper diagnosis and effective rehabilitation is crucial.

Keywords

Bladder dysfunction
Lower urinary tract dysfunction
Stroke
Urinary incontinence
Urodynamic studies
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pmc1. INTRODUCTION

Cerebral stroke is among the most common causes of death and disability worldwide [1-3]. Bladder dysfunction is a well-known complication in stroke patients [4-6] that severely affects quality of life (QoL) [2,7,8]. Urinary symptoms are reported in the majority of patients [9] and primarily include urinary incontinence (UI) and voiding difficulty [2]. UI is more frequent [4], affecting approximately 33% of patients with acute stroke [4,9-11] and persisting for up to 3 months after stroke [11-14]. Its frequency ranges between 28% and 79% [12,13,15-17], and several factors contribute to this issue [16].

The European Association of Urologists (EAU) has not formulated any specific guidelines for urinary dysfunction after a stroke. According to EAU, the pattern of urinary symptoms depends on the anatomical site of neurological lesions, namely supra-pontine, spinal, and sacral/infrasacral ones. Anatomical lesions in the brain are not so clearly classified (EAU Guidelines. Edn. presented at the EAU Annual Congress, Paris 2024, ISBN 978-94-92671-23-3) [18].

Clinically, post-stroke symptoms mainly involve nocturia, overactive bladder (OAB), urgency UI, neurogenic detrusor overactivity, and other less frequent patterns: (a) 57 – 83% of neuro-urological symptoms at 1-month post-stroke, (b) 71 – 80% spontaneous recovery at 6 months, and (c) persistence of UI that is correlated with poor prognosis.

Spasticity is a well-studied stroke complication, which can severely impair bladder control [19]. Neurogenic bladder [14,20] may coexist with the so-called “functional bladder,” which results from associated deficits (immobility, cognitive dysfunction, etc.) [14]. Pre-existing urological problems, such as benign prostatic hyperplasia (BPH), may worsen urinary symptoms in many cases. Stroke has a higher prevalence in the elderly and, as a result, comorbidities are common. BPH should always be kept in mind in dealing with aging men with stroke and need to be excluded to manage urinary symptoms properly. Specifically, the presence of detrusor–sphincter dyssynergia in elderly males with stroke should warn clinicians of possible prostatic urethra obstruction. The differential diagnosis is difficult and the presence of BPH needs to be confirmed by integrating clinical, imaging, and urodynamic assessment. Another example is diabetic patients in whom urinary problems may coexist due to peripheral neuropathy [21].

Bladder dysfunction, which is of prognostic importance, exerts social impact, and incurs a remarkable economic burden [22], is unfortunately often overlooked in these patients. Relevant literature data are also relatively scarce. In light of the impact of bladder problems on victims of cerebrovascular events, the primary purpose of this review article was to look into currently available data regarding the diagnosis and management of bladder dysfunction following stroke.

2. METHODOLOGY

Methodologically, a literature search was conducted in PubMed using the terms “bladder dysfunction” and “stroke,” and the search retrieved 272 related articles. The authors examined all articles published from the inception until March 2021 for potential eligibility. Publications in the English language, including those in foreign language publications with English abstracts, were included in this non-systematic review. Articles concerning bladder dysfunction after stroke, its diagnosis, and management were further analyzed. Our exclusion criteria were (1) articles irrelevant to our topic or them, (2) lesions not affecting the brain, and (3) non-stroke brain lesions. Eventually, a total of 62 articles remained and were used for this narrative review. Data were collected by five independent investigators and then synthesized in a narrative format for a thorough review.

3. CLINICAL FINDINGS

3.1. UI

UI is the predominant urinary symptom and may last for up to 1 year after stroke. Incontinence is correlated with large infarcts [9-11,16], aphasia, cognitive impairment, and functional disability [10,11]. Different types of UI have been described, including urge incontinence from detrusor overactivity, due to disruption of the neuro-micturition pathways (reduced supra-pontine micturition control) [23], overflow incontinence from detrusor underactivity, impaired awareness of incontinence [10,11,13], functional incontinence, exacerbation of pre-existing stress incontinence [11,13], incoordination/weakness of sphincter muscles, impaired bladder’s sensation [24], and transient incontinence due to potentially reversible causes, such as fecal impaction or medications [11]. Risk factors for UI include advanced age, female sex, depression, limited activity, large lesions [9,25], aphasia [25], and underlying medical conditions, such as diabetes or pelvic prolapse in women [9,11,13,25,26]. UI has been found in 73% of patients with hemorrhagic and 64% with ischemic stroke and urinary retention in 13% and 52%, respectively [27].

3.2. Other urinary symptoms

Apart from incontinence [4,9-11], other common post-stroke urinary complaints involve urgency [14,25,28], high frequency [14,25,28], nocturia [25,28], leakage of urine [28], and difficulty voiding [14]. Urgency and frequency of micturition along with urge UI consist of the so-called “Overactive Bladder” syndrome [14]. According to another study, nocturnal urinary frequency is the most common urinary problem, which is followed by incontinence [14]. The prevalence of both urgency and UI is closely associated with the infarction size [7]. Retention is much rarer [9,14,26] and has been associated with cortical strokes, diabetes, aphasia, and cognitive disorders [9]. Other bladder issues in chronic stroke patients include infections (10 – 27%) [4,26,29], asymptomatic (12%), and significant bacteriuria (39%) [29]. In one study, the patients were divided into two groups: those who had an infarction and those who had a hemorrhagic stroke with lower urinary tract dysfunction. Patients with ischemic stroke presented larger bladder capacity (250 mL) and larger post-void residual urine (PVR) volume (136 mL) than their counterparts with hemorrhagic stroke (195 mL and 30 mL, respectively), which may indicate a more severe bladder dysfunction [14].

The bladder-emptying method and residual (post-void) urine volume >50 mL are important risk factors for urinary infections and significant bacteriuria [26,29]. Lower urinary tract manifestations after stroke are sometimes more complicated to address. For instance, during urinary catheterization, which is often used to count urinary output and estimate fluid balance [30], trauma, or infection can result, in further deteriorating such symptoms [31]. Table 1 summarizes the most important locations of lesions and their relevant patterns of bladder dysfunction.

Table 1 The most usual locations of lesions related to bladder dysfunction, their pathophysiological pathways, and clinical consequences

Location of lesion	Pathophysiology	Clinical effect	References	
Frontal lobe	Disruption of frontal connections: overdrive of renal angiotensin system	Detrusor overactivity leads to urinary incontinence (predominantly) and retention	[14,17,26,32-34]	
Parietal lobe	Disruption of afferent pathways to the micturition center (reflex)	Reduced or absent urine sensation: leakage	[32,35]	
Insula	Unclear	Urinary retention	[36]	
Basal ganglia	Unclear	Detrusor areflexia	[37]	
Cerebellum	Unclear	Detrusor overactivity	[14,38,39]	
Pons	Disruption of the descending inhibitory fibers of the midbrain tegmentum	Increased bladder residual volume	[33,34,40]	
Damage to the pontine micturition center	Detrusor dyssynergia		
The lesion in the central pons	Detrusor underactivity leads to urinary retention		
Medulla oblongata	Disruption of the descending stimulatory fibers of the pontine micturition center	Detrusor overactivity	[41]	

3.3. Diagnostic evaluation

Bladder dysfunction after stroke is very common and should be primarily evaluated to better formulate treatment and follow-up plans. A thorough history taking should include past and present urinary symptoms, and also medications received and other concomitant diseases. Information about types of dysfunction, such as voiding or storage problems, that include frequency, voided volume, stress or urgency incontinence, and incontinence episodes, should also be collected or obtained.

Bladder diaries are considered a valuable diagnostic tool for the initial/preliminary assessment of neurogenic lower urinary tract dysfunction. They provide data on the number of voids (spontaneous or intermittent catheter), voided volume, stress/urgency/mixed UI episodes and facilitate the interpretation of urodynamic testing. Preferably, bladder diaries should be completed for 3 consecutive days [42].

Along with the voiding diary, a clinical examination is also necessary before any additional diagnostic investigation [41]. In early assessment of stroke severity, the NIH Stroke Scale/Score is the most well-established tool. However, it does not include any field concerning lower urinary symptoms. Moreover, in the acute phase after stroke, patients usually need to wear an indwelling catheter, depending on the level of consciousness, the clinical status of the patient, and his or her ability to urinate. In those with indwelling catheters, ideally, an urodynamic study should be performed a few days after decatheterization. In those without a catheter, residual urine should be measured after voiding with a bladder ultrasound repeatedly [43]. The bladder’s pathophysiology and functional status can evolve over time [13]. Consequently, urodynamic findings vary, depending on post-stroke phases [44]. Urinary obstruction due to non-neurologic causes also exists [45]. Urodynamic studies (cystometry and pelvic floor electromyography) are very useful in determining pathophysiological mechanisms of bladder dysfunction [11,13,16,19,20,43,46,47] and investigating the cause of incontinence. A standard urodynamic study involves non-invasive uroflowmetry, followed by invasive cystometry and a pressure-flow study, and may reveal a great deal about urinary flow, intravesical and abdominal pressure, urethral pressure profile, and PVR. Urodynamic testing in stroke patients can vary but can reveal uninhibited detrusor overactivity in up to 90% of patients [13]. The following patterns have been described in stroke patients: normal study meaning that there is no abnormal detrusor activity, normal bladder sensation, and normal voiding with complete bladder emptying, detrusor overactivity with involuntary detrusor contractions during the filling phase, detrusor overactivity with impaired contractility during filling phase accompanied by urine loss and terminal overactivity which results in incomplete emptying with large PVR, and detrusor underactivity where contractions are either weak or of short duration leading to prolonged and incomplete emptying [44].

Video-urodynamics, which is considered the gold-standard investigation for patients with neurogenic bladder, combines standard urodynamic testing with fluoroscopic imaging, with radiographic contrast used in bladder filling [10,43].

Bladder pressure in stroke patients with detrusor overactivity is rarely high enough to damage the upper urinary tract [46]. With neurogenic bladder, however, there is always a risk for the transmission of intravesical pressure to the upper tract [43]. In incontinent patients, urodynamic studies can reveal bladder hyper- or hyporeflexia [10,44], detrusor overactivity with impaired contractility [44], or detrusor-sphincter dyssynergia [10], or even no abnormalities at all (37%) [10,44]. Patients with hyporeflexic bladders are usually either diabetic or on anticholinergic medication [10]. Furthermore, urodynamic findings in patients with a disturbed perception of the need to void include terminal detrusor overactivity, incompetent urethral closure, or no abnormalities [23]. In possible neurogenic bladder cases, PVR should be measured since its volume is associated with infection, bladder stone formation, and impaired renal function [46].

3.4. Management and rehabilitation

In stroke patients with urinary dysfunction, an accurate diagnosis is of paramount importance to start an appropriate treatment, prevent upper tract damage, maintain continence, and ensure complete emptying. Treatment strategies should be individually tailored and structured [15]. Nursing care during the acute stroke phase is also important for early detection of bladder dysfunction [48].

Behavioral techniques should be applied as the first step. These include urination on a schedule with or without physical assistance (tapping over the bladder), bladder training, pelvic floor muscle training [11-13,15,16,26,46,49,50], “double voiding” (waiting and attempting to void again after voiding once) [26], and fluid management [11,12,26], along with other lifestyle interventions, such as reducing medications that exacerbate incontinence [11,13]. In fact, scheduled voiding or timed voiding has been shown to be superior to pharmacological treatment in many incontinence cases [10]. Some evidence proved that a voiding program starting at 12-week post-stroke is beneficial, mainly in patients with urge and stress incontinence [50]. Patients’ training that focuses on the bladder’s sensation, inhibition of its contractions, and improvement of the sphincter’s voluntary control, can also treat incontinence effectively [24]. Patients with disturbed awareness of their voiding need may benefit from early training and additional medication for bladder overactivity if needed [35].

The bladder rehabilitation program is essential in improving post-stroke lower urinary tract symptoms and depends on the patient’s awareness, cooperation, and independence. For cooperative patients with independent ambulation, but unaware of the status of their bladder experiencing either urinary retention or UI, timed voiding is a rational choice. For those with the same symptoms but aware of the bladder situation, prompted voiding is more appropriate. For independent patients with urge symptoms who are motivated to participate in a rehabilitation program, bladder training with urge suppression is a good choice. The best approach to improve post-stroke symptoms of the lower urinary tract is a combination of remedial approach and functionally oriented approach. The first uses neurodevelopmental techniques to improve impairment and the second aims to optimize function [51].

If these measures are not efficacious, then medication, primarily anticholinergics, should be considered [11,13,16,43,46,49,52]. Antimuscarinic drugs are considered the first-line medication choice for patients with neurogenic lower urinary tract dysfunction. Antimuscarinic agents reduce urge, stabilize detrusor contractility, and increase bladder capacity. Oxybutynin chloride, trospium chloride, tolterodine tartrate, and propiverine are established and effective antimuscarinic agents. Solifenacin is a new oral anti-cholinergic drug, with a high affinity for the M3 muscarinic receptor in the bladder, but data for its efficacy in neurogenic bladder are limited. Antimuscarinic drugs are generally well tolerated and safe, but adverse effects limit their use. The most common adverse reactions are dry mouth, blurred vision, and constipation. Less frequent are somnolence and impaired cognitive function [52]. The gold standard for patients with bladder overactivity after stroke is the combination of intermittent catheterization with anti-muscarinic drugs [42]. Pilot studies have shown that phosphodiesterase-5 inhibitors have worked effectively on detrusor overactivity and in the future, they may be used as adjuncts to antimuscarinic drugs [43]. Adverse events and limited efficacy, however, make alternative therapies desirable [13,52].

Other less-used drugs include adrenergic alpha-blockers [12,53] and beta-3 agonists [13]. Most alternative drugs act peripherally, primarily on neurotransmission or directly on the detrusor muscle. Just a few drugs with a well-defined central nervous system action can be used for treating micturition disorders, such as baclofen and duloxetine [52]. These treatment strategies are good choices for patients with overactive detrusor [13,16,46,49]. Some clinical data also mentioned the potential benefits of electroacupuncture in detrusor overactivity [54]. Patients with underactive detrusor muscles should be managed with intermittent catheterizations or an indwelling catheter to minimize PVR and prevent upper tract damage [13,16,46]. If these measures fail, intra-detrusor injection of botulinum toxin has shown promising results [12,46]. Most usual applied medications are summarized in Table 2. Of course, if UI persists, containment devices may be required [11].

Table 2 Medications for stroke-related bladder dysfunction, their action, and main adverse effects

Frequency of use	Medical agents	Actions	Adverse effects	References	
Frequently used	Antimuscarinic agents: oxybutynin chloride, trospium chloride, tolterodine tartrate and propiverine	Reduce urge, stabilize detrusor contractility, and increase bladder capacity	Frequent: dry mouth, blurred vision, and constipation. Less frequent: somnolence and cognitive impairment	[19,52]	
Less frequently used	Phosphodiesterase-5 Inhibitors	Effective on detrusor overactivity	Headache, flushing, nasal congestion, nasopharyngitis, and dyspepsia	[13,43,52]	
Adrenergic alpha-blockers and beta3 agonists	Effective on detrusor overactivity	Hypertension, nasopharyngitis, urinary tract infections, dry mouth, back pain, upper respiratory tract infections, sinusitis, headache and dizziness	[12,13,53]	
Intra-detrusor injection of botulinum toxin	Effectiveness on detrusor underactivity	Pain at the injection site, urinary tract infections, hematuria, and an increase in post-void residual volume	[12,46]	

Non-invasive neuromodulation may improve urinary dysfunction in selected patients [12,15,55,56]. Transcutaneous electrical nerve stimulation in combination with an exercise program has shown significant improvement in spasticity and bladder function [3]. Sacral nerve stimulation is a surgical treatment (invasive neuromodulation) of lower urinary dysfunction of non-neurogenic origin approved by the Food and Drug Administration and can benefit patients with neurogenic bladder as well [57]. In addition, electrical stimulation of the posterior tibialis nerve may improve OAB symptoms after stroke [58]. Another non-invasive treatment approach for the UI may be the combination of pelvic floor muscle exercise with biofeedback or/and pelvic floor electric stimulation. A meta-analysis and systematic review regarding this combination approach was beneficial to the recovery of UI after radical prostatectomy. Hence, this treatment option may also, to some extent, work on stroke patients [59].

3.5. Prognosis and impact

In stroke survivors, UI usually improves with time [7,12,13,49,60], with a frequency of 32 – 79% in the acute phase of stroke, 27% at the time of discharge, and 16% several months following stroke [7], reflecting some recovery of bladder control [60]. Other studies have shown an incontinence frequency of 19% at 3 months, 15% at 1 year, and 1% at 2 years [13]. Half of patients with urgency incontinence may become continent after 1 year, a common improvement for patients with disturbed perceptions of their need to void [35].

Although post-stroke recovery of urinary symptoms is possible, it remains a lingering problem for many patients. Problems associated with urinary dysfunction can significantly affect QoL [15,16,25]. Urgency incontinence and nocturia probably have the strongest impact on QoL [24]. UI is a strong predictor of long-term disability [9,13,55], depression [9,13,14,55], and prolonged institutionalization [4,9,11,13,16,25,55]. Moreover, incontinence is associated with stroke severity [9,11,24], poor functional [9,11,14,15] and cognitive status [9,14], urinary tract infection [9,16,25,61], skin breakdown [16,25], falls [14,25], and mortality [11,14,16]. Activities of daily living can also be affected by anxiety [4], low self-esteem, embarrassment, and a sense of fear, which may lead to decreased participation in the rehabilitation program [25]. As a result, bladder dysfunction can interfere with the rehabilitation process and delay the social integration of stroke patients [14,16,61].

Mobility independence after stroke accompanies independence of continence in most cases. This parallel recovery may be explained by common cortical/subcortical pathways of continence and motor function. Rehabilitation interventions also help urinary recovery in patients with functional or mixed UI through improvement of mobility independence [49]. Furthermore, the absence of severe bladder dysfunction is associated with home return from a rehabilitation center [62-64]. Thus, evaluation of urinary dysfunction and its consequences, as well as their treatment, is vital, and rehabilitation efforts should aim to promote recovery of urinary dysfunction [9,13,25,49].

4. CONCLUSION

The prevalence of stroke nowadays has been on the rise and bladder function after stroke is frequently impaired, affecting the QoL of stroke survivors. Despite rehabilitation efforts and the fact that bladder dysfunction usually improves over time, it remains a major issue substantially impacting both the patient and society. However, this problem is often overlooked and poorly managed. A thorough evaluation of the severity of lower urinary tract symptoms and an individualized treatment plan is crucial. The latter is associated with better prognosis and outcomes and should be included in the primary goals of all physicians treating stroke sufferers.

ACKNOWLEDGMENTS

None.

FUNDING

None.

CONFLICT OF INTEREST

The authors declare no competing interests.

AUTHOR CONTRIBUTIONS

Conceptualization: Eleni Agapiou, Efstratios-Stylianos Pyrgelis

Writing – original draft: All authors

Writing – review & editing: All authors

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

Not applicable.

CONSENT FOR PUBLICATION

Not applicable.

DATA AVAILABILITY

Not applicable.
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REFERENCES

1. Kim BR Lee J Sohn MK . Risk factors and functional impact of medical complications in stroke. Ann Rehabil Med 2017;41 (5 ):753–760. doi:10.5535/arm.2017.41.5.753 29201813
2. Liang CC Shaw SW Huang YH Lin YH Lee TH . Bladder transplantation of amniotic fluid stem cell may ameliorate bladder dysfunction after focal cerebral ischemia in rat. Stem Cells Transl Med 2017;6 (4 ):1227–1236. doi:10.1002/sctm.16-0212 28186672
3. Tekeoğlu Y Adak B Göksoy T . Effect of transcutaneous electrical nerve stimulation (TENS) on barthel activities of daily living (ADL) index score following stroke. Clin Rehabil 1998;12 (4 ):277–280. doi:10.1191/026921598672∢16 9744663
4. Kuptniratsaikul V Kovindha A Suethanapornkul S Manimmanakorn N Archongka Y . Complications during the rehabilitation period in Thai patients with stroke:A multicenter prospective study. Am J Phys Med Rehabil 2009;88 (2 ):92–99. doi:10.1097/PHM.0b013e3181909d5f 19077674
5. Lorish TR Sandin KJ Roth EJ Noll SF . Stroke rehabilitation. 3. Rehabilitation evaluation and management. Arch Phys Med Rehabil 1994;75 5 Spec No :S47–S51 7514395
6. Olai L Borgquist L Svärdsudd K . Health problems in elderly patients during the first post-stroke year. Ups J Med Sci 2012;117 (3 ):318–327. doi:10.3109/03009734.2012.674572 22554141
7. Yoo KH Lee SJ Chang SG . Predictive value of the ischemic stroke lesion to detrusor function. Neurourol Urodyn 2010;29 (7 ):1355–1356. doi:10.1002/nau.20885 20127838
8. Salehi-Pourmehr H Hajebrahimi S Rahbarghazi R . Stem cell therapy for neurogenic bladder dysfunction in rodent models:A systematic review. Int Neurourol J 2020;24 (3 ):241–257. doi:10.5213/inj.20040058.029 33017895
9. Akkoç Y Bardak AN Ersöz M . Post-stroke lower urinary system dysfunction and its relation with functional and mental status:A multicenter cross-sectional study. Top Stroke Rehabil 2019;26 (2 ):136–141. doi:10.1080/10749357.2018.1555389 30570391
10. Gelber DA Good DC Laven LJ Verhulst SJ . Causes of urinary incontinence after acute hemispheric stroke. Stroke 1993;24 (3 ):378–382. doi:10.1161/01.str.24.3.378 8446973
11. Mehdi Z Birns J Bhalla A . Post-stroke urinary incontinence. Int J Clin Pract 2013;67 (11 ):1128–1137. doi:10.1111/ijcp.12183 23834208
12. Guo GY Kang YG . Effectiveness of neuromuscular electrical stimulation therapy in patients with urinary incontinence after stroke:A randomized sham controlled trial. Medicine (Baltimore) 2018;97 (52 ):e13702. doi:10.1097/MD.0000000000013702 30593142
13. Panfili Z Metcalf M Griebling TL . Contemporary evaluation and treatment of poststroke lower urinary tract dysfunction. Urol Clin North Am 2017;44 (3 ):403–414. doi:10.1016/j.ucl.2017.04.007 28716321
14. Sakakibara R . Lower urinary tract dysfunction in patients with brain lesions. Handb Clin Neurol 2015;130 :269–287. doi:10.1016/B978-0-444-63247-0.00015-8 26003249
15. Kohler M Mayer H Battocletti M Kesselring J Saxer S . Wirksamkeit von nichtmedikamentösen interventionen zur förderung der urinkontinenz bei menschen nach einem cerebro-vaskulären insult - eine systematische literaturübersicht [Effectiveness of non-pharmacological interventions to promote urinary continence in stroke survivors - a systematic literature review. Pflege 2016;29 (5 ):235–245. [German doi:10.1024/1012-5302/a000493 27239745
16. McKenzie P Badlani GH . The incidence and etiology of overactive bladder in patients after cerebrovascular accident. Curr Urol Rep 2012;13 (5 ):402–406. doi:10.1007/s11934-012-0269-6 22836679
17. Miyazato M Kadekawa K Kitta T . New frontiers of basic science research in neurogenic lower urinary tract dysfunction. Urol Clin North Am 2017;44 (3 ):491–505. doi:10.1016/j.ucl.2017.04.014 28716328
18. European Association of Urology EAU Guidelines Edition. Presented at the EAU. Annual Congress Paris 2024
19. Satkunam LE . Rehabilitation medicine:3. Management of adult spasticity. CMAJ 2003;169 (11 ):1173–1179 14638654
20. Amarenco G . Troubles vésico-sphinctériens d'origine nerveuse [Vesico-sphincter disorders of nervous origin. Rev Prat 1995;45 (3 ):331–335. [French] 7725038
21. Chartier-Kastler E Mozer P Ayoub N Richard F Ruffion A . Hypertrophie bénigne de la prostate et neuro-urologie [Benign prostatic hyperplasia and neurourology. Prog Urol 2007;17 (3 ):529–534. [French]. doi:10.1016/s1166-7087(07)92363-5 17622085
22. Kasyan GR Dreval RO Krivoborodov GG . [Socio-economic aspects of neurogenic dysfunctions in urology]. Urologiia 2020;5 :127–132. [Russian].
23. Pehrson R Stenman E Andersson KE . Effects of tramadol on rat detrusor overactivity induced by experimental cerebral infarction. Eur Urol 2003;44 (4 ):495–499. doi:10.1016/s0302-2838(03)00353-1 14499688
24. Middaugh SJ Whitehead WE Burgio KL Engel BT . Biofeedback in treatment of urinary incontinence in stroke patients. Biofeedback Self Regul 1989;14 (1 ):3–19. doi:10.1007/BF00999338 2752058
25. Akkoç Y Yıldız N Bardak AN . The course of post-stroke bladder problems and their relation with functional and mental status and quality of life:A six-month, prospective, multicenter study. Turk J Phys Med Rehabil 2019;65 (4 ):335–342. doi:10.5606/tftrd.2019.3205 31893270
26. Smith CE Schneider MA . Assessing postvoid residual to identify risk for urinary complications post stroke. J Neurosci Nurs 2020;52 (5 ):219–223. doi:10.1097/JNN.0000000000000536 32694465
27. Ouyang M Billot L Song L . Prognostic significance of early urinary catheterization after acute stroke:Secondary analyses of the international HeadPoST trial. Int J Stroke. 2021;16 (2 ):200–206. doi:10.1177/1747493020908140 32075569
28. Liu HT Liu AB Chancellor MB Kuo HC . Urinary nerve growth factor level is correlated with the severity of neurological impairment in patients with cerebrovascular accident. BJU Int 2009;104 (8 ):1158–1162. doi:10.1111/j.1464-410X.2009.08533.x 19338537
29. Lee HS Choi JG Shin JH . Urological disturbance and its neuroanatomical correlate in patients with chronic brainstem stroke. Neurourol Urodyn 2017;36 (1 ):136–141. doi:10.1002/nau.22889 26397818
30. Shukla R Giri P Bhandari A Shankhwar SN . Pontine stroke and bladder dysfunction. BMJ Case Rep 2014;2014 :bcr2013200787. doi:10.1136/bcr-2013-200787
31. Yum KS Na SJ Lee KY . Pattern of voiding dysfunction after acute brainstem infarction. Eur Neurol 2013;70 5-6 :291–296. doi:10.1159/000352040 24052006
32. Tateno F Sakakibara R Aiba Y . Bladder autonomic dysfunction after a parietal stroke. J Stroke Cerebrovasc Dis 2020;29 (4 ):104620. doi:10.1016/j.jstrokecerebrovasdis.2019.104620 32033903
33. Wu MN Guo YC Lai CL Shen JT Liou LM . Poststroke detrusor hyporeflexia in a patient with left medial Pontine infarction. Neurologist 2012;18 (2 ):73–75. doi:10.1097/NRL.0b013e318247b9d9 22367833
34. Saint S Trautner BW Fowler KE . A multicenter study of patient-reported infectious and noninfectious complications associated with indwelling urethral catheters. JAMA Intern Med 2018;178 (8 ):1078–1085. doi:10.1001/jamainternmed.2018.2417 29971436
35. Pettersen R Stien R Wyller TB . Post-stroke urinary incontinence with impaired awareness of the need to void:Clinical and urodynamic features. BJU Int 2007;99 (5 ):1073–1077. doi:10.1111/j.1464-410X.2007.06754.x 17437440
36. Jeanson G Lebreton F . Corrélats neuroanatomiques entre lésions AVC et troubles urinaires:Une revue de la littérature [Neuroanatomical correlates between stroke lesions and urinary disorders:A narrative review]. Prog Urol 2019;29 (4 ):226–234. [French]. doi:10.1016/j.purol.2018.10.004 30527571
37. Burney TL Senapati M Desai S Choudhary ST Badlani GH . Acute cerebrovascular accident and lower urinary tract dysfunction:A prospective correlation of the site of brain injury with urodynamic findings. J Urol 1996;156 (5 ):1748–1750. doi:10.1016/s0022-5347(01)65498-3 8863586
38. Kreydin EI Gad P Gao B Liu CY Ginsberg DA Jann K . The effect of stroke on micturition associated brain activity:A pilot fMRI study. Neurourol Urodyn 2020;39 (8 ):2198–2205. doi:10.1002/nau.24473 32761953
39. Sakakibara R . Editorial comment to effect of dominant hemispheric stroke on detrusor function in patients with lower urinary tract symptoms. Int J Urol 2010;17 (7 ):660. doi:10.1111/j.1442-2042.2010.02549.x 20590950
40. Pelz JO Fischer MM Bungert-Kahl P Lindner D Fricke C Michalski D . Fluid balance variations during the early phase of large hemispheric stroke are associated with patients'functional outcome. Front Neurol 2019;10 :720. doi:10.3389/fneur.2019.00720 31333571
41. Ersoz M Ulusoy H Oktar MA Akyuz M . Urinary tract infection and bacteriurua in stroke patients:Frequencies, pathogen microorganisms, and risk factors. Am J Phys Med Rehabil 2007;86 (9 ):734–741. doi:10.1097/PHM.0b013e31813e5f96. Erratum in:Am J Phys Med Rehabil 2007;86(12):1038 17709997
42. Kovindha A Wattanapan P Dejpratham P Permsirivanich W Kuptniratsaikul V . Prevalence of incontinence in patients after stroke during rehabilitation:A multi-centre study. J Rehabil Med 2009;41 (6 ):489–491. doi:10.2340/16501977-0354 19479163
43. Liao L . Evaluation and management of neurogenic bladder:What is new in China?. Int J Mol Sci 2015;16 (8 ):18580–18600. doi:10.3390/ijms160818580 26266405
44. Pizzi A Falsini C Martini M Rossetti MA Verdesca S Tosto A . Urinary incontinence after ischemic stroke:Clinical and urodynamic studies. Neurourol Urodyn 2014;33 (4 ):420–425. doi:10.1002/nau.22420 23775804
45. Kodama K Yokoyama O Komatsu K Yotsuyanagi S Niikura S Namiki M . Contribution of cerebral nitric oxide to bladder overactivity after cerebral infarction in rats. J Urol 2002;167 (1 ):391–396 11743362
46. Yared JE Gormley EA . The role of urodynamics in elderly patients. Clin Geriatr Med 2015;31 (4 ):567–579. doi:10.1016/j.cger.2015.06.003 26476116
47. Nitti VW Adler H Combs AJ . The role of urodynamics in the evaluation of voiding dysfunction in men after cerebrovascular accident. J Urol 1996;155 (1 ):263–266 7490851
48. Wald ME . Cerebral thrombosis:Assessment and nursing management of the acute phase. J Neurosci Nurs 1986;18 (1 ):36–38. doi:10.1097/01376517-198602000-00010 2936842
49. Kushner DS Johnson-Greene D . Association of urinary incontinence with cognition, transfers and discharge destination in acute stroke inpatient rehabilitation. J Stroke Cerebrovasc Dis. 2018;27 (10 ):2677–2682. doi:10.1016/j.jstrokecerebrovasdis.2018.05.028 29941393
50. Thomas LH Watkins CL Sutton CJ . Identifying continence options after stroke (ICONS):A cluster randomised controlled feasibility trial. Trials 2014;15 :509. doi:10.1186/1745-6215-15-509 25539714
51. Dumoulin C Korner-Bitensky N Tannenbaum C . Urinary incontinence after stroke:Does rehabilitation make a difference?A systematic review of the effectiveness of behavioral therapy. Top Stroke Rehabil 2005;12 (3 ):66–76. doi:10.1310/ENMX-RUV5-15WL-VNA2 16110429
52. Andersson KE Pehrson R . CNS involvement in overactive bladder:Pathophysiology and opportunities for pharmacological intervention. Drugs 2003;63 (23 ):2595–2611. doi:10.2165/00003495-200363230-00003 14636079
53. Nakada Y Yokoyama O Komatsu K . Effects of aniracetam on bladder overactivity in rats with cerebral infarction. J Pharmacol Exp Ther 2000;293 (3 ):921–928 10869393
54. Shin S Lee J Yoo J Lim SM Lee E . Electroacupuncture versus sham electroacupuncture for urinary retention in poststroke patients:Study protocol for a multicenter, randomized controlled trial. Trials 2016;17 :197. doi:10.1186/s13063-016-1315-3 27072880
55. Kreydin E Zhong H Latack K Ye S Edgerton VR Gad P . Transcutaneous electrical spinal cord neuromodulator (TESCoN) improves symptoms of overactive bladder. Front Syst Neurosci 2020;14 :1. doi:10.3389/fnsys.2020.00001 32116576
56. Havton LA Christe KL Edgerton VR Gad PN . Noninvasive spinal neuromodulation to map and augment lower urinary tract function in rhesus macaques. Exp Neurol 2019;322 :113033. doi:10.1016/j.expneurol.2019.113033 31400304
57. Peters KM Kandagatla P Killinger KA Wolfert C Boura JA . Clinical outcomes of sacral neuromodulation in patients with neurologic conditions. Urology 2013;81 (4 ):738–743. doi:10.1016/j.urology.2012.11.073 23537757
58. Monteiro ÉS de Carvalho LB Fukujima MM Lora MI do Prado GF . Electrical stimulation of the posterior tibialis nerve improves symptoms of poststroke neurogenic overactive bladder in men:A randomized controlled trial. Urology 2014;84 (3 ):509–514. doi:10.1016/j.urology.2014.05.031 25168524
59. Sciarra A Viscuso P Arditi A . A biofeedback-guided programme or pelvic floor muscle electric stimulation can improve early recovery of urinary continence after radical prostatectomy:A meta-analysis and systematic review. Int J Clin Pract 2021;75 (10 ):e14208. doi:10.1111/ijcp.14208 33811418
60. Ersoz M Erhan B Akkoc Y . An evaluation of bladder emptying methods and the effect of demographic and clinical factors on spontaneous voiding frequency in stroke patients. Neurol Sci 2013;34 (5 ):729–734. doi:10.1007/s10072-012-1123-9 22684236
61. Freed MM Wainapel SF . Predictors of stroke outcome. Am Fam Physician 1983;28 (5 ):119–123
62. Loewen SC Anderson BA . Predictors of stroke outcome using objective measurement scales. Stroke 1990;21 (1 ):78–81. doi:10.1161/01.str.21.1.78 2300994
63. Massucci M Perdon L Agosti M . Prognostic factors of activity limitation and discharge destination after stroke rehabilitation. Am J Phys Med Rehabil 2006;85 (12 ):963–970. doi:10.1097/01.phm.0000242620.44924.1b 17033592
64. Mokler PJ Sandstrom R Griffin M Farris L Jones C . Predicting discharge destination for patients with severe motor stroke:Important functional tasks. Neurorehabil Neural Repair 2000;14 (3 ):181–185. doi:10.1177/154596830001400303 11272474
