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Bladder Autonomic Dysfunction after a Parietal Stroke
ARTICLE IN PRESS
Case Report
Bladder Autonomic Dysfunction after a Parietal Stroke Fuyuki Tateno, MD,* Ryuji Sakakibara, MD, PhD,* Yosuke Aiba, MD,* Osamu Takahashi, BSci,† Ayami Shimizu, BSci,† Megumi Sugiyama, BSci,† Tsuyoshi Ogata, MSc,* and Nobuo Takada, MD, PhD†
We describe a case of a 57-year-old man who, immediately after a right parietal ischemic stroke, showed urodynamically determined bladder sensory decrement during filling and an underactive detrusor during voiding, both of which were ameliorated during the course of his treatment. The lower urinary tract symptom (LUTS) occurs in stroke in up to 60% of patients, when it involves the frontal and insular cortices. In addition, LUTS does occur in parietal stroke as seen in our patient, presumably by sensory deafferentiation within the brain that is relevant to the central regulation of the micturition reflex. Key Words: Stroke—parietal lobe—deep sensation—bladder sensation—detrusor underactivity © 2019 Elsevier Inc. All rights reserved.
Introduction The brain has significant impact on the bladder. Studies have shown that the prefrontal cortex, anterior and middle cingulate cortex, supplementary motor area, insular cortex (ie, mainly anterior brain), basal ganglia, and hypothalamus are the supratentorial structures relevant to the higher control of micturition.1 3 It is also known that bladder afferent information transmits to the parietal sensory cortex in experimental animals4 and humans.5 7 However, it is not known whether a parietal lesion might cause bladder dysfunction in humans, except for a study by Petersen et al.8 We recently had a case of a man who, immediately after a parietal stroke, showed transient bladder autonomic dysfunction.
From the *Neurology, Internal Medicine, Sakura Medical Center, Toho University, Sakura, Japan; and †Clinical Physiology Unit, Sakura Medical Center, Toho University, Sakura, Japan. Received July 9, 2019; revision received December 9, 2019; accepted December 22, 2019. Address correspondence to Ryuji Sakakibara, MD, PhD, Neurology, Internal Medicine, Sakura Medical Center, Toho University, 564-1 Shimoshizu, Sakura, 285-8741, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter © 2019 Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jstrokecerebrovasdis.2019.104620
Case Report A 57-year-old man whose dyslipidemia and ulcerative colitis were being treated by his general physician suddenly developed staggering gait and numbness on the left side of his body, which brought him to our hospital on the same day he was referred. Upon his arrival, he was alert and cooperative. His motor function (manual muscle test, deep tendon reflexes) was normal, though he had felt some weakness before referral in his left-side extremities. However, superficial sensations, ie, pin prick and crude touch, were decreased to 3 out of 10 on his left-side face, arm, and leg (Fig 1). The perineal area was not examined. Deep sensations for thumb localizing test,9 2-point discrimination, and joint position were decreased in his left-side arm and leg. He had mild sensory ataxia in his left-side arm and leg, and a mild staggering gait, which was exacerbated when his eyes closed. He also had bladder dysfunction, which was not detected by the International Prostate Symptom Score of 2 out of 35 and an overactive bladder symptom score of 1 out of 15. He had begun to notice that he could store more urine than usual, so he had started to use time cueing (every 2 hours) rather than sensation for toileting. Likewise, he could hear the sound of his urine stream, but could not sense his urination otherwise. The results of his blood test showed dyslipidemia (increased neutral
Journal of Stroke and Cerebrovascular Diseases, Vol. &&, No. && (&&), 2019: 104620
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F. TATENO ET AL.
Figure 1. Brain imaging and area of decreased sensation of the patient. (A) Diffusion-weighted axial images of brain MRI. The lesion was located at the right postcentral cortex and the subcortical white matter and posterior insular cortex. (B) MR angiography. Rami of right middle cerebral artery is occluded. (C) Cerebral blood flow SPECT imaging using ECD. The area of hypoperfusion area was located diffusely throughout the right parietal cortex. (D) Area of decreased sensation of the patient. Both superficial and deep sensations were decreased in the left-side face, arm and leg. Abbreviations: ECD, 99m-Tc ethylcysteinate dimer; MRI, magnetic resonance imaging; SPECT, single-photon emission computed tomography.
lipid of 424 mg/dL, decreased low-density lipoprotein cholesterol of 52 mg/dL), and no inflammatory markers. He had no diabetes or atrial fibrillation. Brain magnetic resonance images of the patient taken on admission day showed high-signal lesions at the right postcentral cortex and the subcortical white matter and posterior insular cortex (Fig 1). MR angiography showed occlusion of rami of right middle cerebral artery. Brain single-photon emission computed tomography using 99m-Tc ethylcysteinate dimer showed areas of decreased blood flow at the right parietal cortex wider than the lesions detected in the magnetic resonance images scan. Somatosensory evoked potentials revealed no laterality by medial nerve stimulation, but a slight delay in the right-side evoked cortical P38 (right 40.7 milliseconds, left 38.9 milliseconds) by
tibial nerve stimulation. He was diagnosed with parietal stroke, and started on 10 mg/day intravenous argatrovan, an anticoagulant, and 60 mg/day intravenous edaravon, a free radical scavenger. We performed a urodynamic study with his informed consent.
Urodynamic Study Results (the Next Day after Disease Onset) The methods and definitions used for the urodynamic study and sphincter electromyography conformed to the standards proposed by the International Continence Society.10,11 He had normal motor unit potentials by sphincter electromyography. Prostate echography showed a prostate volume of 23 mL (normal <20 mL, symptomatic >30 mL).
ARTICLE IN PRESS BLADDER AUTONOMIC DYSFUNCTION AFTER A PARIETAL STROKE
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Figure 2. Urodynamic recording of the patient. Prostate echography showed a prostate volume of 23 mL (normal <20 mL, symptomatic >30 mL). A free flow could not be obtained. One hour after voluntary void in the ward, 320 mL of postvoid residual (PVR) was catheterized. During slow filling (50 mL/min), he showed delayed first sensation at 337 mL, normal desire to void at 450 mL, and maximum desire to void (bladder capacity) at 623 mL (based on the sum of voluntary-voided volume soon afterwards and final-catheterized residual volume), but no uninhibited sphincter relaxation, and we stopped infusing saline into the bladder in order to avoid overdistension bladder injury. He had no detrusor overactivity or low compliance. We then asked him to void voluntarily. However, voiding did not begin for several minutes, and he showed poor urinary flow (voided volume 88 mL). Pressure-flow analysis of this flow showed a low maximum urinary flow rate (4.5 mL/s, normal >10), low average urinary flow rate (3.1 mL/s, normal >10); no obstruction (Abrams unobstructed; Schafer 0 [normal <2]); underactive detrusor (Schafer very weak, Watts factor 10.7 watts/m2); no detrusor-sphincter dyssynergia; and a large post-void residual (PVR) volume (535 mL). Abbreviations: EMG, electromyography; Flow, urinary flow; Pabd, abdominal (rectal) pressure; Pdiff, differential detrusor pressure = Pves Pabd; Pves, vesical (bladder) pressure.
ARTICLE IN PRESS F. TATENO ET AL.
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A free flow could not be obtained. Catheterization yielded a 320-mL postvoid residual (PVR). Urethral sensation seemed preserved when catheterized. During slow filling (50 mL/min), he showed a delayed first sensation at 337 mL, normal desire to void at 450 mL, and maximum desire to void (bladder capacity) at 623 mL (based on the sum of voluntary-voided volume soon afterwards and final-catheterized residual volume), no uninhibited sphincter relaxation, and we stopped infusing saline into the bladder in order to avoid overdistension bladder injury. (Fig 2) He had no detrusor overactivity or low compliance. We then asked him to void voluntarily. However, voiding did not begin for several minutes, and he showed poor urinary flow (voided volume 88 mL). Pressure-flow analysis of this flow showed a low maximum urinary flow rate (4.5 mL/s, normal >10), low average urinary flow rate (3.1 mL/s, normal >10); no obstruction (Abrams unobstructed; Schafer 0 [normal <2]); underactive detrusor (Schafer very weak, Watts factor 10.7 watts/m2); no detrusor-sphincter dyssynergia; and a large PVR volume (535 mL). In order to ameliorate his bladder condition, we first taught him to perform clean, intermittent self-catheterization twice a day in order to avoid overdistension bladder injury. On the following 2 days, PVR spontaneously decreased to less than 100 mL and clean, intermittent selfcatheterization was stopped. After that, repeated ultrasound measurement of PVR in the ward showed a PVR less than 50 mL. Although we did not repeat urodynamics, his bladder and somatic sensation soon gradually recovered to normal before discharge at the 11th admission day.
Discussion Stroke causes bladder dysfunction in up to 60% of patients.2,12,13 Most of the lower urinary tract symptoms due to stroke are overactive bladder (urinary urgency and frequency), but in the acute phase, up to 5% of patients may show transient urinary retention.12 In addition, stroke at the brainstem or infratentorial lesions tend to show large PVRs and/or urinary retention.2 Both the right and left hemisphere are involved in bladder dysfunction. Studies have shown that the prefrontal cortex, anterior and middle cingulate cortex, supplementary motor area and insular cortex (ie, anterior half of the brain) are structures relevant to the higher control of micturition.1 3 This is also true in stroke cases, since patients with sensory aphasia (Wernicke’s aphasia, temporal lobe lesion) or those with hemianopsia (occipital lobe lesion) seldom have bladder dysfunction.2,12,13 In contrast, little is known about the parietal sensory cortex for bladder function in humans. Our case is unique in that his right parietal infarct led to immediate (1) bladder sensory impairment during filling and (2) an underactive detrusor (bladder weakness, without apparent prostate hyperplasia) during voiding, which were confirmed by urodynamic recording and ameliorated during the course of recovery. He also showed a
decrease in superficial and deep sensations on the left side of the body, and mild slowing of sensory evoked potentials as evoked by the left tibial nerve. Previously, a similar case was reported by Petersen et al.8 Petersen’s case 3 was an 87-year-old man who suffered from left parietal infarct. He showed prolonged first sensation at 450 mL, and had a large PVR of 150 mL, presumably due to an underactive detrusor, both findings similar to ours. The combination of bladder sensory loss and underactive detrusor has not been well documented.14 In particular, we did not know the exact mechanism of underactive detrusor in our patient. However, it is reasonable to assume that triggering/initiation of bladder contraction needs appropriate sensory input from the lower urinary tract.10 It has been documented that a dorsal rhizotomy interrupts the micturition reflex15 and lessens detrusor overactivity in patients with intractable urinary incontinence. Sensory deafferentiation within the brain might have interfered with voluntary voiding in our patient. In conclusion, we describe a case of a man who, immediately after a right parietal ischemic stroke, showed bladder sensory decrement during filling and an underactive detrusor during voiding, both of which soon ameliorated during the course of his treatment.
Conflict of Interest The authors have no conflicts of interest to declare.
References 1. de Groat WC, Griffiths D, Yoshimura N. Neural control of the lower urinary tract. Compr Physiol 2015;5:327-396. 2. Sakakibara R. Lower urinary tract dysfunction in patients with brain lesions. Handb Clin Neurol 2015;130:269-287. 3. Griffiths D. Functional imaging of structures involved in neural control of the lower urinary tract. Handb Clin Neurol 2015;130:121-133. 4. Tai C, Wang J, Jin T, et al. Brain switch for reflex micturition control detected by FMRI in rats. J Neurophysiol 2009;102:2719-2730. 5. Matsushita M, Nakasato N, Nakagawa H, et al. Primary somatosensory evoked magnetic fields elicited by sacral surface electrical stimulation. Neurosci Lett 2008;431: 77-80. 6. Kn€ upfer SC, Liechti MD, van der Lely S, et al. Sensory evoked cortical potentials of the lower urinary tract in healthy men. Neurourol Urodyn 2018;37:2614-2624. 7. Walter M, Leitner L, Michels L, et al. Reliability of supraspinal correlates to lower urinary tract stimulation in healthy participants—A fMRI study. Neuroimage 2019;191:481-492. 8. Petersen 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: 1073-1077. 9. Hirayama K, Fukutake T, Kawamura M. Thumb localizing test for detecting a lesion in the posterior columnmedial lemniscal system. J Neurol Sci 1999;167:45-49. 10. Abrams P, Cardozo L, Fall M, et al. The standardization of terminology of lower urinary tract function; report
ARTICLE IN PRESS BLADDER AUTONOMIC DYSFUNCTION AFTER A PARIETAL STROKE from the Standardization Subcommittee of the International Continence Society. Neurourol Urodynam 2002;21: 167-178. 11. Wyndaele JJ. Investigating afferent nerve activity from the lower urinary tract: highlighting some basic research techniques and clinical evaluation methods. Neurourol Urodyn 2010;29:56-62. 12. Sakakibara R, Hattori T, Yasuda K, et al. Micturitional disturbance after acute hemispheric stroke: analysis of the lesion site by CT and MRI. J Neurol Sci 1996;137: 47-56.
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13. Thomas LH, Coupe J, Cross LD, et al. Interventions for treating urinary incontinence after stroke in adults. Cochrane Database Syst Rev 2019;2:CD004462. https:// doi.org/10.1002/14651858.CD004462.pub4. 14. Tateno F, Sakakibara R, Yano M, et al. A young man with herpes simplex encephalitis: Andrew and Nathan type urodynamic abnormality. Bladder 2014;1:e4. https://doi. org/10.14440/bladder.2014.25. POL Scientific. 15. Liao JM, Cheng CL, Lee SD, et al. Impaired micturition reflex caused by acute selective dorsal or ventral root(s) rhizotomy in anesthetized rats. Neurourol Urodyn 2006;25:283-289.
Case Report
Bladder Autonomic Dysfunction after a Parietal Stroke Fuyuki Tateno, MD,* Ryuji Sakakibara, MD, PhD,* Yosuke Aiba, MD,* Osamu Takahashi, BSci,† Ayami Shimizu, BSci,† Megumi Sugiyama, BSci,† Tsuyoshi Ogata, MSc,* and Nobuo Takada, MD, PhD†
We describe a case of a 57-year-old man who, immediately after a right parietal ischemic stroke, showed urodynamically determined bladder sensory decrement during filling and an underactive detrusor during voiding, both of which were ameliorated during the course of his treatment. The lower urinary tract symptom (LUTS) occurs in stroke in up to 60% of patients, when it involves the frontal and insular cortices. In addition, LUTS does occur in parietal stroke as seen in our patient, presumably by sensory deafferentiation within the brain that is relevant to the central regulation of the micturition reflex. Key Words: Stroke—parietal lobe—deep sensation—bladder sensation—detrusor underactivity © 2019 Elsevier Inc. All rights reserved.
Introduction The brain has significant impact on the bladder. Studies have shown that the prefrontal cortex, anterior and middle cingulate cortex, supplementary motor area, insular cortex (ie, mainly anterior brain), basal ganglia, and hypothalamus are the supratentorial structures relevant to the higher control of micturition.1 3 It is also known that bladder afferent information transmits to the parietal sensory cortex in experimental animals4 and humans.5 7 However, it is not known whether a parietal lesion might cause bladder dysfunction in humans, except for a study by Petersen et al.8 We recently had a case of a man who, immediately after a parietal stroke, showed transient bladder autonomic dysfunction.
From the *Neurology, Internal Medicine, Sakura Medical Center, Toho University, Sakura, Japan; and †Clinical Physiology Unit, Sakura Medical Center, Toho University, Sakura, Japan. Received July 9, 2019; revision received December 9, 2019; accepted December 22, 2019. Address correspondence to Ryuji Sakakibara, MD, PhD, Neurology, Internal Medicine, Sakura Medical Center, Toho University, 564-1 Shimoshizu, Sakura, 285-8741, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter © 2019 Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jstrokecerebrovasdis.2019.104620
Case Report A 57-year-old man whose dyslipidemia and ulcerative colitis were being treated by his general physician suddenly developed staggering gait and numbness on the left side of his body, which brought him to our hospital on the same day he was referred. Upon his arrival, he was alert and cooperative. His motor function (manual muscle test, deep tendon reflexes) was normal, though he had felt some weakness before referral in his left-side extremities. However, superficial sensations, ie, pin prick and crude touch, were decreased to 3 out of 10 on his left-side face, arm, and leg (Fig 1). The perineal area was not examined. Deep sensations for thumb localizing test,9 2-point discrimination, and joint position were decreased in his left-side arm and leg. He had mild sensory ataxia in his left-side arm and leg, and a mild staggering gait, which was exacerbated when his eyes closed. He also had bladder dysfunction, which was not detected by the International Prostate Symptom Score of 2 out of 35 and an overactive bladder symptom score of 1 out of 15. He had begun to notice that he could store more urine than usual, so he had started to use time cueing (every 2 hours) rather than sensation for toileting. Likewise, he could hear the sound of his urine stream, but could not sense his urination otherwise. The results of his blood test showed dyslipidemia (increased neutral
Journal of Stroke and Cerebrovascular Diseases, Vol. &&, No. && (&&), 2019: 104620
1
ARTICLE IN PRESS 2
F. TATENO ET AL.
Figure 1. Brain imaging and area of decreased sensation of the patient. (A) Diffusion-weighted axial images of brain MRI. The lesion was located at the right postcentral cortex and the subcortical white matter and posterior insular cortex. (B) MR angiography. Rami of right middle cerebral artery is occluded. (C) Cerebral blood flow SPECT imaging using ECD. The area of hypoperfusion area was located diffusely throughout the right parietal cortex. (D) Area of decreased sensation of the patient. Both superficial and deep sensations were decreased in the left-side face, arm and leg. Abbreviations: ECD, 99m-Tc ethylcysteinate dimer; MRI, magnetic resonance imaging; SPECT, single-photon emission computed tomography.
lipid of 424 mg/dL, decreased low-density lipoprotein cholesterol of 52 mg/dL), and no inflammatory markers. He had no diabetes or atrial fibrillation. Brain magnetic resonance images of the patient taken on admission day showed high-signal lesions at the right postcentral cortex and the subcortical white matter and posterior insular cortex (Fig 1). MR angiography showed occlusion of rami of right middle cerebral artery. Brain single-photon emission computed tomography using 99m-Tc ethylcysteinate dimer showed areas of decreased blood flow at the right parietal cortex wider than the lesions detected in the magnetic resonance images scan. Somatosensory evoked potentials revealed no laterality by medial nerve stimulation, but a slight delay in the right-side evoked cortical P38 (right 40.7 milliseconds, left 38.9 milliseconds) by
tibial nerve stimulation. He was diagnosed with parietal stroke, and started on 10 mg/day intravenous argatrovan, an anticoagulant, and 60 mg/day intravenous edaravon, a free radical scavenger. We performed a urodynamic study with his informed consent.
Urodynamic Study Results (the Next Day after Disease Onset) The methods and definitions used for the urodynamic study and sphincter electromyography conformed to the standards proposed by the International Continence Society.10,11 He had normal motor unit potentials by sphincter electromyography. Prostate echography showed a prostate volume of 23 mL (normal <20 mL, symptomatic >30 mL).
ARTICLE IN PRESS BLADDER AUTONOMIC DYSFUNCTION AFTER A PARIETAL STROKE
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Figure 2. Urodynamic recording of the patient. Prostate echography showed a prostate volume of 23 mL (normal <20 mL, symptomatic >30 mL). A free flow could not be obtained. One hour after voluntary void in the ward, 320 mL of postvoid residual (PVR) was catheterized. During slow filling (50 mL/min), he showed delayed first sensation at 337 mL, normal desire to void at 450 mL, and maximum desire to void (bladder capacity) at 623 mL (based on the sum of voluntary-voided volume soon afterwards and final-catheterized residual volume), but no uninhibited sphincter relaxation, and we stopped infusing saline into the bladder in order to avoid overdistension bladder injury. He had no detrusor overactivity or low compliance. We then asked him to void voluntarily. However, voiding did not begin for several minutes, and he showed poor urinary flow (voided volume 88 mL). Pressure-flow analysis of this flow showed a low maximum urinary flow rate (4.5 mL/s, normal >10), low average urinary flow rate (3.1 mL/s, normal >10); no obstruction (Abrams unobstructed; Schafer 0 [normal <2]); underactive detrusor (Schafer very weak, Watts factor 10.7 watts/m2); no detrusor-sphincter dyssynergia; and a large post-void residual (PVR) volume (535 mL). Abbreviations: EMG, electromyography; Flow, urinary flow; Pabd, abdominal (rectal) pressure; Pdiff, differential detrusor pressure = Pves Pabd; Pves, vesical (bladder) pressure.
ARTICLE IN PRESS F. TATENO ET AL.
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A free flow could not be obtained. Catheterization yielded a 320-mL postvoid residual (PVR). Urethral sensation seemed preserved when catheterized. During slow filling (50 mL/min), he showed a delayed first sensation at 337 mL, normal desire to void at 450 mL, and maximum desire to void (bladder capacity) at 623 mL (based on the sum of voluntary-voided volume soon afterwards and final-catheterized residual volume), no uninhibited sphincter relaxation, and we stopped infusing saline into the bladder in order to avoid overdistension bladder injury. (Fig 2) He had no detrusor overactivity or low compliance. We then asked him to void voluntarily. However, voiding did not begin for several minutes, and he showed poor urinary flow (voided volume 88 mL). Pressure-flow analysis of this flow showed a low maximum urinary flow rate (4.5 mL/s, normal >10), low average urinary flow rate (3.1 mL/s, normal >10); no obstruction (Abrams unobstructed; Schafer 0 [normal <2]); underactive detrusor (Schafer very weak, Watts factor 10.7 watts/m2); no detrusor-sphincter dyssynergia; and a large PVR volume (535 mL). In order to ameliorate his bladder condition, we first taught him to perform clean, intermittent self-catheterization twice a day in order to avoid overdistension bladder injury. On the following 2 days, PVR spontaneously decreased to less than 100 mL and clean, intermittent selfcatheterization was stopped. After that, repeated ultrasound measurement of PVR in the ward showed a PVR less than 50 mL. Although we did not repeat urodynamics, his bladder and somatic sensation soon gradually recovered to normal before discharge at the 11th admission day.
Discussion Stroke causes bladder dysfunction in up to 60% of patients.2,12,13 Most of the lower urinary tract symptoms due to stroke are overactive bladder (urinary urgency and frequency), but in the acute phase, up to 5% of patients may show transient urinary retention.12 In addition, stroke at the brainstem or infratentorial lesions tend to show large PVRs and/or urinary retention.2 Both the right and left hemisphere are involved in bladder dysfunction. Studies have shown that the prefrontal cortex, anterior and middle cingulate cortex, supplementary motor area and insular cortex (ie, anterior half of the brain) are structures relevant to the higher control of micturition.1 3 This is also true in stroke cases, since patients with sensory aphasia (Wernicke’s aphasia, temporal lobe lesion) or those with hemianopsia (occipital lobe lesion) seldom have bladder dysfunction.2,12,13 In contrast, little is known about the parietal sensory cortex for bladder function in humans. Our case is unique in that his right parietal infarct led to immediate (1) bladder sensory impairment during filling and (2) an underactive detrusor (bladder weakness, without apparent prostate hyperplasia) during voiding, which were confirmed by urodynamic recording and ameliorated during the course of recovery. He also showed a
decrease in superficial and deep sensations on the left side of the body, and mild slowing of sensory evoked potentials as evoked by the left tibial nerve. Previously, a similar case was reported by Petersen et al.8 Petersen’s case 3 was an 87-year-old man who suffered from left parietal infarct. He showed prolonged first sensation at 450 mL, and had a large PVR of 150 mL, presumably due to an underactive detrusor, both findings similar to ours. The combination of bladder sensory loss and underactive detrusor has not been well documented.14 In particular, we did not know the exact mechanism of underactive detrusor in our patient. However, it is reasonable to assume that triggering/initiation of bladder contraction needs appropriate sensory input from the lower urinary tract.10 It has been documented that a dorsal rhizotomy interrupts the micturition reflex15 and lessens detrusor overactivity in patients with intractable urinary incontinence. Sensory deafferentiation within the brain might have interfered with voluntary voiding in our patient. In conclusion, we describe a case of a man who, immediately after a right parietal ischemic stroke, showed bladder sensory decrement during filling and an underactive detrusor during voiding, both of which soon ameliorated during the course of his treatment.
Conflict of Interest The authors have no conflicts of interest to declare.
References 1. de Groat WC, Griffiths D, Yoshimura N. Neural control of the lower urinary tract. Compr Physiol 2015;5:327-396. 2. Sakakibara R. Lower urinary tract dysfunction in patients with brain lesions. Handb Clin Neurol 2015;130:269-287. 3. Griffiths D. Functional imaging of structures involved in neural control of the lower urinary tract. Handb Clin Neurol 2015;130:121-133. 4. Tai C, Wang J, Jin T, et al. Brain switch for reflex micturition control detected by FMRI in rats. J Neurophysiol 2009;102:2719-2730. 5. Matsushita M, Nakasato N, Nakagawa H, et al. Primary somatosensory evoked magnetic fields elicited by sacral surface electrical stimulation. Neurosci Lett 2008;431: 77-80. 6. Kn€ upfer SC, Liechti MD, van der Lely S, et al. Sensory evoked cortical potentials of the lower urinary tract in healthy men. Neurourol Urodyn 2018;37:2614-2624. 7. Walter M, Leitner L, Michels L, et al. Reliability of supraspinal correlates to lower urinary tract stimulation in healthy participants—A fMRI study. Neuroimage 2019;191:481-492. 8. Petersen 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: 1073-1077. 9. Hirayama K, Fukutake T, Kawamura M. Thumb localizing test for detecting a lesion in the posterior columnmedial lemniscal system. J Neurol Sci 1999;167:45-49. 10. Abrams P, Cardozo L, Fall M, et al. The standardization of terminology of lower urinary tract function; report
ARTICLE IN PRESS BLADDER AUTONOMIC DYSFUNCTION AFTER A PARIETAL STROKE from the Standardization Subcommittee of the International Continence Society. Neurourol Urodynam 2002;21: 167-178. 11. Wyndaele JJ. Investigating afferent nerve activity from the lower urinary tract: highlighting some basic research techniques and clinical evaluation methods. Neurourol Urodyn 2010;29:56-62. 12. Sakakibara R, Hattori T, Yasuda K, et al. Micturitional disturbance after acute hemispheric stroke: analysis of the lesion site by CT and MRI. J Neurol Sci 1996;137: 47-56.
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13. Thomas LH, Coupe J, Cross LD, et al. Interventions for treating urinary incontinence after stroke in adults. Cochrane Database Syst Rev 2019;2:CD004462. https:// doi.org/10.1002/14651858.CD004462.pub4. 14. Tateno F, Sakakibara R, Yano M, et al. A young man with herpes simplex encephalitis: Andrew and Nathan type urodynamic abnormality. Bladder 2014;1:e4. https://doi. org/10.14440/bladder.2014.25. POL Scientific. 15. Liao JM, Cheng CL, Lee SD, et al. Impaired micturition reflex caused by acute selective dorsal or ventral root(s) rhizotomy in anesthetized rats. Neurourol Urodyn 2006;25:283-289.