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| REVIEW ARTICLE |
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| Year : 2019 | Volume
: 30
| Issue : 1 | Page : 8-13 |
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Stroke and lower urinary tract symptoms: A neurosurgical view
Yu-Cheng Chou1, Yuan-Hong Jiang2, Tomor Harnod2, Hsu-Tung Lee3, Hann-Chorng Kuo2
1 Department of Neurosurgery, Neurological Institute, Taichung Veterans General Hospital, Taichung; Department of Neurological Surgery, Tri-Service General Hospital, National Defense Medical Center, Taipei; Rong Hsing Research Center for Translational Medicine, National Chung Hsing University, Taichung, Taiwan
2 Department of Urology, Buddhist Tzu Chi General Hospital and Tzu Chi University, Hualien, Taiwan
3 Department of Neurosurgery, Neurological Institute, Taichung Veterans General Hospital, Taichung; Graduate Institute of Medical Sciences, National Defense Medical Center, Taipei, Taiwan
| Date of Web Publication | 2-Jan-2019 |
Correspondence Address:
Hann-Chorng Kuo
Department of Urology, Buddhist Tzu Chi General Hospital, No. 707, Section 3, Chung-Yang Road, Hualien 970
Taiwan
 Source of Support: None, Conflict of Interest: None  | 5 |
DOI: 10.4103/UROS.UROS_82_18
Lower urinary tract symptoms (LUTSs) are common neurological sequelae of stroke, which negatively impact the mortality of patients with stroke and the quality of life of both patients and their caregivers. There are three hierarchical micturition centers: the sacral spinal center, subconscious structures, and conscious structures. Several brain imaging modalities for micturition studies on humans and animals and neuroanatomical studies on animals have facilitated a better understanding of LUTSs. The urodynamic findings in patients with stroke may vary and tend to evolve with time; the identification of the underlying cause of poststroke voiding dysfunction helps optimize the management of these patients. For patients with stroke with overactive bladders, the first-line treatments include behavioral therapies and the second-line therapies include the use of drugs. Intermittent or indwelling catheterization can be used for patients with stroke with detrusor underactivity. In this article, we discuss the current consensus, relevant assessment modalities, and management of LUTSs in patients with stroke. Keywords: Lower urinary tract symptoms, neurogenic voiding, neuroimaging, urodynamic detrusor overactivity
How to cite this article:
Chou YC, Jiang YH, Harnod T, Lee HT, Kuo HC. Stroke and lower urinary tract symptoms: A neurosurgical view. Urol Sci 2019;30:8-13 |
| Introduction | |  |
Lower urinary tract symptoms (LUTSs) are common neurological sequelae of stroke.[1],[2],[3] Neurogenic voiding dysfunction negatively impacts the mortality of patients with stroke and the quality of life of patients as well as their caregivers. Two-year stroke survival, disability, and institutionalization rates are adversely affected by poststroke incontinence.[3] The bladder and emptying function may change at the different stages of poststroke recovery and sequelae period.[4] Accurate assessment and management of LUTSs at different stages of recovery are a key element of poststroke care. In this article, we discuss the current consensus and review the recent developments in various aspects of evaluation and management of LUTSs in patients with stroke.
| Neuroanatomy and Neurophysiology | | |
There are three hierarchical micturition centers: (i) the sacral spinal center, which is regulated by the pontine center, under the control of multiple; (ii) subconscious structures (the cerebellum, the striate nucleus, and the hypothalamus); and (iii) conscious structures (limbic cortex, frontal ascending, and parietal ascending circumduction).[5] The central nervous system mediates chronic bladder pain and the brain integrates the sensory and the affective components of bladder pain.[6]
Prefrontal cortex
The forebrain influences the voluntary control of the human micturition switch and the maintenance of continence.[7] The role of the frontal lobes in the control of micturition was elucidated >50 years ago.[8] The prefrontal cortex (PFC) receives inputs pertaining to external and internal variables and is a region of multimodal convergence of information about the external environment.[7] The orbital prefrontal network serves as a “viscerosensory” system of the PFC that receives most of the sensory input, whereas the medial network serves as a “visceromotor” system that relays major cortical output to the hypothalamus and periaqueductal gray (PAG) in the midbrain. Neuroimaging studies have demonstrated the activation and deactivation of the medial PFC under different conditions of bladder filling. Real-time measurement of changes in oxyhemoglobin (oxy-Hb) levels in the frontal micturition area using functional near-infrared spectroscopy (fNIRS) has demonstrated the activation of the frontal micturition area during natural bladder filling and voiding.[9]
Thalamus
The thalamus gates almost all sensory information except olfaction. Functional imaging studies have demonstrated thalamic activation on bladder filling.[7] This is one of the first supraspinal sites involved in the processing of bladder pain as the termination point of the spinothalamic tract. Peripheral C-fiber input was shown to partially mediate thalamic activation resulting from cyclophosphamide-induced cystitis.
Hypothalamus
The hypothalamus, like the amygdala, is involved in neuroendocrinal responses to bladder pain because of its role as the head of the hypothalamic–pituitary–adrenal axis. Oxytocin, a hormone that is synthesized by the hypothalamus, was shown to decrease bladder pain-like responses and to exhibit an anxiolytic and analgesic effect.[7]
Limbic system and amygdala
The limbic system consists of cingulate and parahippocampal gyri, the hippocampus, septal nuclei, and the amygdala and is involved in the processing and regulation of emotions, memory, and sexual arousal.[7] Topical application of capsaicin to the bladder and urinary bladder distension in an animal model was shown to induce cortical desynchronization and cortical arousal.[10] Increased limbic activity is indicated by amygdala-mediated defense responses when presented with a visceral threat in patients with interstitial cystitis/bladder pain syndrome.[11]
Basal ganglia
The basal ganglia contains the striatum (caudate and putamen), globus pallidus, substantia nigra, and the subthalamic nucleus (STN). Patients with Parkinson's disease have an increased bladder volume at first sensation and at capacity during STN deep brain stimulation.[12],[13],[14] Activation of basal ganglia nuclei was observed in some bladder filling functional imaging experiments.[7]
Brain stem
In the brain stem, the PAG in the midbrain integrates somatic, autonomic, and sensory components of emotional behavior, which modulates the reactions to stress.[15],[16] It is a member of the descending modulatory pain nexus. The arc of the spinal cord/PAG/pontine micturition center (PMC) is responsible for the suppression of PAG and directs the urethral sphincter and bladder wall muscle activity to maintain bladder control, leading to the attenuation of these processes.[17] The presumed PMC, a separate dorsal pontine region, was shown to be active during the initiation of voluntary voiding in positron emission tomography (PET) functional brain imaging experiments on humans.[18],[19] The rostral ventromedial medulla (RVM) in the brain stem is associated with the modulation of descending pain, akin to its anatomically connected partner and PAG. RVM plays an important role in modulating bladder pain. Lesions of the RVM were shown to exacerbate visceromotor responses in rats with inflamed bladders.[20] In feline experiments, the nucleus locus subcoeruleus and the nucleus reticularis pontis oralis were shown to play a role in the neuronal mechanism for urine storage, by receiving inputs that enhance or inhibit micturition from an extended area between the cerebral cortex and the sacral spinal cord.[21] Neural circuitry transmits afferent impulses from the bladder to midbrain PAG and efferent signals from the PMC to the sacral cord.[22] This mechanism allows the spinobulbospinal voiding reflex pathway to function as a binary switch, “off” (storage) and “on” (voiding).
Lower urinary tract functions are involved in the filling and storage of urine and emptying or voiding.[23],[24] Intact voluntary (somatic) and involuntary (autonomic) nervous systems are necessary to maintain this function.[25] There are three sets of the peripheral nerves that innervate the bladder and the urethra: (i) pelvic parasympathetic nerves from sacral spinal cord segments S2–S4 induce the contraction of the detrusor muscle of the bladder, (ii) thoracic and lumbar sympathetic nerves T10–L2 control the bladder neck and urethra, and (iii) the pudendal nerve stimulates the external urethral sphincter and the pelvic floor muscles.[26],[27],[28] The PMC in the brain stem controls the coordinated relaxation of the urethral sphincter and contraction of the detrusor muscle by receiving inputs from the higher centers, including the frontal lobe and the hypothalamus.[24] Studies conducted on a rat model suggested that overactivity in the bladder is caused by an impaired balance between excitatory glutamatergic neurons and inhibitory γ-aminobutyric acid (GABA) ergic or glycinergic neurons after cerebral infarction.[29] Urethral continence may be impaired by stroke affecting the ascending and descending pathways through the raphe nuclei and the locus coeruleus, the major sources of spinal serotonergic and noradrenergic pathways.
| Neuroimaging | | |
Besides the neuroanatomical studies on animals, there are several brain imaging tools related to micturition in humans. These tools contribute to our understanding of LUTSs with some limitations. Molecular imaging techniques are essential for the study of brain diseases. Moreover, the development of molecular probes specific to biochemical markers has helped provide valuable insights into the organization of the brain and the relationship of structures and functions.[30] In the last two decades, the supraspinal control of LUTs has been studied using PET and functional magnetic resonance imaging (fMRI) of the brain.[31] The fMRI detects the changes in the proportions of oxygenated and deoxygenated hemoglobin in the activated brain areas, whereas PET entails the injection of a radioactive isotope that accumulates in metabolically active brain regions. Both imaging modalities provide complementary functional information about the brain [Table 1]. | Table 1: Summary of functional brain imaging studies for neural control of the lower urinary tract
Click here to view |
Functional magnetic resonance imaging
fMRI is a powerful noninvasive tool for brain functional mapping and study of connectivity.[32],[40] It acts on the changes in the signal intensity from the alterations in the local transverse relaxation times (T2 and T2*) associated with regional changes in the cerebral deoxyhemoglobin concentration on the basis of blood-oxygen-level-dependent contrast. It also provides an outstanding temporal and spatial resolution but requires several runs of the same event to increase the signal-to-noise ratio.[30] The involvement of the medial PFC, basal ganglia, and cerebellum in the control of micturition was confirmed by high-field fMRI in humans.[32]
PAG was shown to be activated during bladder filling by fMRI in humans;[33] this phenomenon was also detected by fMRI in rats.[33] In an fMRI study, the deactivation of the parahippocampal gyrus during bladder filling in women with an overactive bladder was demonstrated. In addition, in another fMRI study, hippocampal activation during bladder contractions in rats was demonstrated.[34],[35] Brain networks were analyzed longitudinally in adult patients with stroke by means of resting-state fMRI.[41] The potential importance of normalization of large-scale modular brain systems during stroke recovery may be established from this work (e.g., long-distance connections recovered over different periods after stroke). Urinary retention was shown to be more strongly associated with stroke in the dominant hemisphere and dominant insula.[36] The insular cortex was shown to be activated during the storage phase in PET and fMRI studies; therefore, the insular cortex might be related to the transition between the storage phase and the onset of micturition.
Positron emission tomography
PET can detect rapid changes in the brain metabolism and is very sensitive to changes in the neural activity.[31] Activation of the PAG during bladder filling in humans was demonstrated by fMRI as well as PET.[33],[37] The activation of the insula during bladder filling was observed in both PET and fMRI studies.[38],[39] An18 F-Fluorodeoxyglucose PET study revealed metabolic changes in different brain regions associated with sensory and cognitive functions in patients with central poststroke pain following thalamic intracerebral hemorrhage.[42]
Functional near-infrared spectroscopy
Cortical activation and the changes in cortical oxygenation have been assessed by near-infrared light since the early 1990s.[9] fNIRS can detect changes in the concentrations of oxygenated hemoglobin (HbO2) and deoxygenated hemoglobin (HHb) in the target cerebral cortices to measure the neuronal activity owing to neurovascular coupling.[43] This system has the advantage of less physical restriction for the patients, and it has been widely utilized in rehabilitation studies for stroke.[44] The frontal micturition area was shown to be activated during natural bladder filling and voiding by means of fNIRS [Table 1].[9] There is potential for further development of fNIRS techniques for imaging of patients with stroke with LUTSs in the future.
| Urinary Incontinence and Stroke Stages | | |
Urinary incontinence is a common problem after stroke, and it occurs in 35%–40% of patients at 7–10 days after acute stroke.[45] In a study on 95 patients with incontinence, 7-10 days after stroke, incontinence persisted at 3 months, 1 year, and 2 years in 36%, 24%, and 13% of the patients, respectively.[3] The initial incontinence was associated with age above 75 years, dysphagia, visual field defect, and motor weakness. Two-year stroke survival, disability, and institutionalization rates were adversely affected by poststroke incontinence. In a large cohort of 935 consecutive patients with acute stroke in Denmark, 36%, 11%, and 53% of the patients had full urinary incontinence, partial urinary incontinence, and no urinary incontinence at admission, respectively; the corresponding figures at 6-month follow-up were 8%, 11%, and 81%, respectively.[46] Older age, stroke severity, diabetes, and other disabling diseases were associated with a higher risk of urinary incontinence. The proportion of stroke patients with urinary incontinence tends to decline with time; this phenomenon is consistent with the gradual recovery of long-distance connections over different periods after stroke as demonstrated by resting-state fMRI.[41]
| Urodynamic Findings in Patients with Stroke | | |
Locations
In the first prospective study of urinary complaints and bladder physiology following acute stroke, no relationship was observed between the location of the infarct and the urinary symptoms.[1],[47] In a retrospective, cross-sectional study of 40 patients, no significant correlation was observed between the urodynamic study findings and the sites of the lesions.[48] In a prospective study of 60 patients with stroke, detrusor areflexia showed a correlation with cerebellar and hemorrhagic infarction.[49]
Patterns and timing
In a prospective study, urodynamic tests with electromyography were performed within 72 h of stroke onset in 60 patients with acute stroke; 47% of the patients had urinary retention principally because of detrusor areflexia (75%), whereas all six patients with cerebellar infarction had detrusor areflexia.[49] Detrusor areflexia within 3 days of stroke occurred in about 35% of these patients: 17 out of 20 patients (85%) with hemorrhagic infarction and 4 out of 40 patients (10%) with ischemic infarction. The initial detrusor areflexia and the increase in the bladder tone over time were likely attributable to the neurophysiological changes caused by cerebral shock.[50]
The urodynamic studies performed on 106 patients at 6–44 (mean: 22) days after ischemic stroke revealed normal findings in 15%, detrusor overactivity (DO) in 56%, DO with impaired contractility (DOIC) in 14%, and detrusor underactivity (DU) in 15% of the patients.[51] Repeat urodynamic studies in 63 patients 1 month later showed normal findings in 30%, DO in 48%, DOIC in 6%, and DU in 16%.
Detrusor hyperreflexia is the most frequent urodynamic finding after stroke and is likely attributable to the loss of inhibitory input from higher neurologic centers.[49] Detrusor hyperreflexia occurs in about half of all stroke patients during recovery from the shock stage and persists in around 20% of patients with chronic stroke.[49],[52],[53] It causes urinary urgency, frequency, and urge incontinence. In a retrospective study of 84 patients with stroke, DO was significantly more prevalent in patients with ischemic stroke as compared to patients with hemorrhagic stroke.[54] In our video urodynamic study, DO was observed in 75% of patients with ischemic cerebellar stroke and in 28.6% of patients with hemorrhagic cerebellar stroke.[55] Most of our patients with cerebellar stroke developed DO and dyssynergic urethral sphincter beyond 2 months after stroke.
During the recovery phase, 4–10 months after stroke, about 10% of the patients had urethral sphincter pseudodyssynergia, which caused incomplete bladder emptying and excessive residual urine.[56],[57] Patients with chronic stroke may have DO, which causes urinary incontinence.[57] On the contrary, DU is manifested more frequently in patients with chronic pontine stroke over 3 months.[58] The urodynamic findings in patients with stroke may vary and change with time. Urodynamic studies are a useful tool to identify the underlying cause of poststroke voiding dysfunction, which facilitates the management of these complex patients.[59]
| Management | | |
Bladder and urethral dysfunction alter with time in patients with stroke and other causes of neurogenic lower urinary tract dysfunction.[57] Transurethral resection of the prostate should be avoided within 6–12 months after stroke because of the changes in the voiding dysfunction over time during the recovery period.[59] For patients with stroke with overactive bladders, the first-line treatments are behavioral therapies, including bladder training, urge suppression, pelvic floor muscle training, and fluid management. The second-line therapies include medications such as antimuscarinic agents and beta-3 agonists. Urinary incontinence and intravesical pressure can be alleviated by long-term antimuscarinic therapy. Intravesical injection of botulinum toxin-A (BoNT-A, Botox) is effective in the restoration of urinary continence from 3 months to 9 months and may replace the demand for bladder augmentation.[60] Urethral sphincter injection of BoNT-A benefits patients with urethral sphincter pseudodyssynergia after stroke.[53] There are preliminary and promising data about percutaneous tibial nerve stimulation, a minimally invasive therapy, for overactive bladder symptoms of patients with stroke.[59] Intermittent or indwelling catheterization can be used for patients with stroke with DU. Appropriate treatments can be chosen according to the urodynamic findings. The clinical guidelines of the Taiwanese Continence Society recommend the least invasive surgery or reversible procedure first if a surgical intervention is needed.[57]
| Conclusion | | |
Evidence from animal studies, neuroanatomical and neurophysiological studies, clinical observations, and functional brain imaging indicates complex communicating networks among the brain, spinal cord, and lower urinary tract. Several fMRI and PET studies have contributed to our understanding of the pathophysiology of LUTSs in patients with stroke. In addition, fNIRS, which requires less physical restriction for the patients, has been applied in the studies on LUTSs. Further, fNIRS research in patients with stroke with LUTSs can be developed. Appropriate treatments for LUTSs can be selected on the basis of the changes in the urodynamic findings over time in patients with stroke.
Acknowledgment
The authors would like to thank Enago (www.enago.tw) for the English language review.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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