Abstract
Purpose of review
The aim of this review is to outline the clinical presentation, pathophysiology and evaluation of lower urinary tract (LUT) dysfunction in Parkinson’s disease and other parkinsonian syndromes including multiple system atrophy, dementia with Lewy bodies, progressive supranuclear palsy and corticobasal degeneration.
Recent findings
LUT dysfunction commonly occurs in neurological disorders, including patients with parkinsonian syndromes. The pattern of LUT dysfunction and its severity are variable, depending upon the site of lesion within the neural pathways. Parkinsonian syndromes are broadly divided into Parkinson’s disease (PD) and a typical parkinsonian syndromes such as multiple system atrophy (MSA), dementia with Lewy bodies (DLB), progressive supranuclear palsy (PSP) and corticobasal degeneration (CBD). Different parkinsonian syndromes have distinct clinical features (e.g. dysautonomia, early dementia, supranuclear gaze palsy, higher cortical signs), and the pattern of LUT dysfunction and its severity can differ.
Conclusions
LUT dysfunction is a common feature in patients with parkinsonian syndromes. Recognising the pattern of LUT dysfunction during the assessment of these patients can help management and possibly facilitate an earlier diagnosis.
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References
Martinez-Martin P, Schapira AH, Stocchi F, Sethi K, Odin P, MacPhee G, Brown RG, Naidu Y, Clayton L, Abe K, Tsuboi Y, MacMahon D, Barone P, Rabey M, Bonuccelli U, Forbes A, Breen K, Tluk S, Olanow CW, Thomas S, Rye D, Hand A, Williams AJ, Ondo W, Chaudhuri KR (2007) Prevalence of nonmotor symptoms in Parkinson’s disease in an international setting; study using nonmotor symptoms questionnaire in 545 patients. Mov Disord 22(11):1623–1629
Jecmenica-Lukic M, Poewe W, Tolosa E, Wenning GK (2012) Premotor signs and symptoms of multiple system atrophy. Lancet Neurol 11(4):361–368
Balash Y, Peretz C, Leibovich G, Herman T, Hausdorff JM, Giladi N (2005) Falls in outpatients with Parkinson’s disease: frequency, impact and identifying factors. J Neurol 252(11):1310–1315
Okunoye O, Kojima G, Marston L, Walters K, Schrag A (2020) Factors associated with hospitalisation among people with Parkinson’s disease - a systematic review and meta-analysis. Parkinsonism Relat Disord 71:66–72
McGrother CW, Jagger C, Clarke M, Castleden CM (1990) Handicaps associated with incontinence: implications for management. J Epidemiol Community Health 44(3):246–248
Panicker JN, Fowler CJ (2010) The bare essentials: uro-neurology. Pract Neurol 10(3):178–185
Sakakibara R, Uchiyama T, Yamanishi T, Shirai K, Hattori T (2008) Bladder and bowel dysfunction in Parkinson’s disease. J Neural Transm 115(3):443–460
Andersen JT (1985) Disturbances of bladder and urethral function in Parkinson’s disease. Int Urol Nephrol 17(1):35–41
Berger Y, Blaivas JG, DeLaRocha ER, Salinas JM (1987) Urodynamic findings in Parkinson’s disease. J Urol 138(4):836–838
Magerkurth C, Schnitzer R, Braune S (2005) Symptoms of autonomic failure in Parkinson’s disease: prevalence and impact on daily life. Clin Auton Res 15(2):76–82
Gumber A, Ramaswamy B, Ibbotson R, Ismail M, Thongchundee O, Harrop D, Allmark P, Rauf A (2017) Economic, social and financial cost of Parkinson's on individuals, carers and their families in the UK. Project Report. Centre for Health and Social Care Research, Sheffield Hallam University
Low V, Ben-Shlomo Y, Coward E, Fletcher S, Walker R, Clarke CE (2015) Measuring the burden and mortality of hospitalisation in Parkinson’s disease: a cross-sectional analysis of the English Hospital Episodes Statistics database 2009–2013. Parkinsonism Relat Disord 21(5):449–454
Xu D, Han S, Wang J, Feng J (2019) Relationship between lower urinary tract dysfunction and clinical features in Chinese Parkinson’s disease patients. Parkinsons Dis 2019:6820937
Winge K, Friberg L, Werdelin L, Nielsen KK, Stimpel H (2005) Relationship between nigrostriatal dopaminergic degeneration, urinary symptoms, and bladder control in Parkinson’s disease. Eur J Neurol 12(11):842–850
Sakakibara R, Tateno F, Kishi M, Tsuyuzaki Y, Uchiyama T, Yamamoto T (2012) Pathophysiology of bladder dysfunction in Parkinson’s disease. Neurobiol Dis 46(3):565–571
Stewart RB, Moore MT, May FE, Marks RG, Hale WE (1992) Nocturia: a risk factor for falls in the elderly. J Am Geriatr Soc 40(12):1217–1220
Temml C, Ponholzer A, Gutjahr G, Berger I, Marszalek M, Madersbacher S (2009) Nocturia is an age-independent risk factor for hip-fractures in men. Neurourol Urodyn 28(8):949–952
Nakagawa H, Niu K, Hozawa A, Ikeda Y, Kaiho Y, Ohmori-Matsuda K, Nakaya N, Kuriyama S, Ebihara S, Nagatomi R, Tsuji I, Arai Y (2010) Impact of nocturia on bone fracture and mortality in older individuals: a Japanese longitudinal cohort study. J Urol 184(4):1413–1418
Parsons JK, Mougey J, Lambert L, Wilt TJ, Fink HA, Garzotto M, Barrett-Connor E, Marshall LM (2009) Lower urinary tract symptoms increase the risk of falls in older men. BJU Int 104(1):63–68
Weiss JP (2012) Nocturia: focus on etiology and consequences. Rev Urol 14(3–4):48–55
Batla A, Simeoni S, Uchiyama T, deMin L, Baldwin J, Melbourne C, Islam S, Bhatia KP, Pakzad M, Eriksson S, Panicker JN (2021) Exploratory pilot study of exogenous sustained-release melatonin on nocturia in Parkinson’s disease. Eur J Neurol 28(6):1884–1892
Batla A, Phé V, De Min L, Panicker JN (2016) Nocturia in Parkinson’s disease: why does it occur and how to manage? Mov Disord Clin Pract 3(5):443–451. https://doi.org/10.1002/mdc3.12374
Mathias CJ, Fosbraey P, da Costa DF, Thornley A, Bannister R (1986) The effect of desmopressin on nocturnal polyuria, overnight weight loss, and morning postural hypotension in patients with autonomic failure. Br Med J (Clin Res Ed) 293(6543):353–354
Sammour ZM, Gomes CM, Barbosa ER, Lopes RI, Sallem FS, Trigo-Rocha FE, Bruschini H, Srougi M (2009) Voiding dysfunction in patients with Parkinson’s disease: impact of neurological impairment and clinical parameters. Neurourol Urodyn 28(6):510–515
Panicker JN, Fowler CJ, Kessler TM (2015) Lower urinary tract dysfunction in the neurological patient: clinical assessment and management. Lancet Neurol 14(7):720–732
Sakakibara R, Tateno F, Yamamoto T, Uchiyama T, Yamanishi T (2018) Urological dysfunction in synucleinopathies: epidemiology, pathophysiology and management. Clin Auton Res 28(1):83–101
Tateno F, Sakakibara R, Ogata T, Kishi M, Tsuyusaki Y, Takahashi O, Sugiyama M, Tateno A (2015) Lower urinary tract function in dementia with Lewy bodies (DLB). Mov Disord 30(3):411–415
Yamamoto T, Tateno F, Sakakibara R, Furukawa S, Asahina M, Uchiyama T, Hirano S, Yamanaka Y, Fuse M, Koga Y, Yanagisawa M, Kuwabara S (2016) Urinary dysfunction in progressive supranuclear palsy compared with other Parkinsonian disorders. PLoS One 11(2):e0149278
Sakakibara R, Uchiyama T, Yamanishi T, Hattori T (2004) Urinary function in patients with corticobasal degeneration; comparison with normal subjects. Neurourol Urodyn 23(2):154–158
Sakakibara R, Panicker J, Finazzi-Agro E, Iacovelli V, Bruschini H (2016) A guideline for the management of bladder dysfunction in Parkinson’s disease and other gait disorders. Neurourol Urodyn 35(5):551–563
Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Durr A, Fowler CJ, Kaufmann H, Klockgether T, Lees A, Poewe W, Quinn N, Revesz T, Robertson D, Sandroni P, Seppi K, Vidailhet M (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71(9):670–676
Sakakibara R, Hattori T, Uchiyama T, Kita K, Asahina M, Suzuki A, Yamanishi T (2000) Urinary dysfunction and orthostatic hypotension in multiple system atrophy: which is the more common and earlier manifestation? J Neurol Neurosurg Psychiatry 68(1):65–69
Kirchhof K, Apostolidis AN, Mathias CJ, Fowler CJ (2003) Erectile and urinary dysfunction may be the presenting features in patients with multiple system atrophy: a retrospective study. Int J Impot Res 15(4):293–298
Geser F, Seppi K, Stampfer-Kountchev M, Kollensperger M, Diem A, Ndayisaba JP, Ostergaard K, Dupont E, Cardozo A, Tolosa E, Abele M, Dodel R, Klockgether T, Ghorayeb I, Yekhlef F, Tison F, Daniels C, Kopper F, Deuschl G, Coelho M, Ferreira J, Rosa MM, Sampaio C, Bozi M, Schrag A, Hooker J, Kim H, Scaravilli T, Mathias CJ, Fowler C, Wood N, Quinn N, Widner H, Nilsson CF, Lindvall O, Schimke N, Eggert KM, Oertel W, del Sorbo F, Carella F, Albanese A, Pellecchia MT, Barone P, Djaldetti R, Meco G, Colosimo C, Gonzalez-Mandly A, Berciano J, Gurevich T, Giladi N, Galitzky M, Ory F, Rascol O, Kamm C, Buerk K, Maass S, Gasser T, Poewe W, Wenning GK (2005) The European multiple system atrophy-study group (EMSA-SG). J Neural Transm 112(12):1677–1686
Ito T, Sakakibara R, Yasuda K, Yamamoto T, Uchiyama T, Liu Z, Yamanishi T, Awa Y, Yamamoto K, Hattori T (2006) Incomplete emptying and urinary retention in multiple-system atrophy: when does it occur and how do we manage it? Mov Disord 21(6):816–823
Panicker JN, Simeoni S, Miki Y, Batla A, Iodice V, Holton JL, Sakakibara R, Warner TT (2019) Early presentation of urinary retention in multiple system atrophy: can the disease begin in the sacral spinal cord? J Neurol
Beck RO, Betts CD, Fowler CJ (1994) Genitourinary dysfunction in multiple system atrophy: clinical features and treatment in 62 cases. J Urol 151(5):1336–1341
Sakakibara R, Panicker J, Simeoni S, Uchiyama T, Yamamoto T, Tateno F, Kishi M, Aiba Y (2019) Bladder dysfunction as the initial presentation of multiple system atrophy: a prospective cohort study. Clin Auton Res 29(6):627–631
Yamamoto T, Asahina M, Yamanaka Y, Uchiyama T, Hirano S, Fuse M, Koga Y, Sakakibara R, Kuwabara S (2017) Postvoid residual predicts the diagnosis of multiple system atrophy in Parkinsonian syndrome. J Neurol Sci 381:230–234
Sakakibara R, Hattori T, Uchiyama T, Yamanishi T (2001) Videourodynamic and sphincter motor unit potential analyses in Parkinson’s disease and multiple system atrophy. J Neurol Neurosurg Psychiatry 71(5):600–606
Yamamoto T, Sakakibara R, Uchiyama T, Liu Z, Ito T, Awa Y, Yamamoto K, Kinou M, Yamanishi T, Hattori T (2005) When is Onuf’s nucleus involved in multiple system atrophy? A sphincter electromyography study. J Neurol Neurosurg Psychiatry 76(12):1645–1648
Mannen T, Iwata M, Toyokura Y, Nagashima K (1982) The Onuf’s nucleus and the external anal sphincter muscles in amyotrophic lateral sclerosis and Shy-Drager syndrome. Acta Neuropathol 58(4):255–260
Chalmers D, Swash M (1987) Selective vulnerability of urinary Onuf motoneurons in Shy-Drager syndrome. J Neurol 234(4):259–260
Palace J, Chandiramani VA, Fowler CJ (1997) Value of sphincter electromyography in the diagnosis of multiple system atrophy. Muscle Nerve 20(11):1396–1403
Eardley I, Quinn NP, Fowler CJ, Kirby RS, Parkhouse HF, Marsden CD, Bannister R (1989) The value of urethral sphincter electromyography in the differential diagnosis of parkinsonism. Br J Urol 64(4):360–362
Schwarz J, Kornhuber M, Bischoff C, Straube A (1997) Electromyography of the external anal sphincter in patients with Parkinson’s disease and multiple system atrophy: frequency of abnormal spontaneous activity and polyphasic motor unit potentials. Muscle Nerve 20(9):1167–1172
Valldeoriola F, Valls-Sole J, Tolosa ES, Marti MJ (1995) Striated anal sphincter denervation in patients with progressive supranuclear palsy. Mov Disord 10(5):550–555
Niu X, Cheng Y, Hu W, Fan Z, Zhang W, Shao B, Deng B (2020) Application of bulbocavernosus reflex combined with anal sphincter electromyography in the diagnosis of MSA and PD. Int J Neurosci 1–6
Cai ZY, Niu XT, Pan J, Ni PQ, Wang X, Shao B (2017) The value of the bulbocavernosus reflex and pudendal nerve somatosensory evoked potentials in distinguishing between multiple system atrophy and Parkinson’s disease at an early stage. Acta Neurol Scand 136(3):195–203
Huang HJ, Zhu XY, Wang X, Wang ZY, Zhang WL, Chen BC, Liu CF (2017) The bulbocavernosus reflex in the differential diagnosis of multiple system atrophy with predominant Parkinsonism and Parkinson’s disease. Front Neurol 8:697
Kaufmann H (1996) Consensus statement on the definition of orthostatic hypotension, pure autonomic failure and multiple system atrophy. Clin Auton Res 6(2):125–126
Kaufmann H, Norcliffe-Kaufmann L, Palma JA, Biaggioni I, Low PA, Singer W, Goldstein DS, Peltier AC, Shibao CA, Gibbons CH, Freeman R, Robertson D (2017) Natural history of pure autonomic failure: a United States prospective cohort. Ann Neurol 81(2):287–297
McKeith IG, Boeve BF, Dickson DW, Halliday G, Taylor JP, Weintraub D, Aarsland D, Galvin J, Attems J, Ballard CG, Bayston A, Beach TG, Blanc F, Bohnen N, Bonanni L, Bras J, Brundin P, Burn D, Chen-Plotkin A, Duda JE, El-Agnaf O, Feldman H, Ferman TJ, Ffytche D, Fujishiro H, Galasko D, Goldman JG, Gomperts SN, Graff-Radford NR, Honig LS, Iranzo A, Kantarci K, Kaufer D, Kukull W, Lee VMY, Leverenz JB, Lewis S, Lippa C, Lunde A, Masellis M, Masliah E, McLean P, Mollenhauer B, Montine TJ, Moreno E, Mori E, Murray M, O’Brien JT, Orimo S, Postuma RB, Ramaswamy S, Ross OA, Salmon DP, Singleton A, Taylor A, Thomas A, Tiraboschi P, Toledo JB, Trojanowski JQ, Tsuang D, Walker Z, Yamada M, Kosaka K (2017) Diagnosis and management of dementia with Lewy bodies: fourth consensus report of the DLB Consortium. Neurology 89(1):88–100
Ransmayr GN, Holliger S, Schletterer K, Heidler H, Deibl M, Poewe W, Madersbacher H, Kiss G (2008) Lower urinary tract symptoms in dementia with Lewy bodies, Parkinson disease, and Alzheimer disease. Neurology 70(4):299–303
Horimoto Y, Matsumoto M, Akatsu H, Ikari H, Kojima K, Yamamoto T, Otsuka Y, Ojika K, Ueda R, Kosaka K (2003) Autonomic dysfunctions in dementia with Lewy bodies. J Neurol 250(5):530–533
Sakakibara R, Hattori T, Tojo M, Yamanishi T, Yasuda K, Hirayama K (1993) Micturitional disturbance in progressive supranuclear palsy. J Auton Nerv Syst 45(2):101–106
Oliveira MCB, Ling H, Lees AJ, Holton JL, De Pablo-Fernandez E, Warner TT (2019) Association of autonomic symptoms with disease progression and survival in progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 90(5):555–561
Donker Kaat L, Boon AJ, Kamphorst W, Ravid R, Duivenvoorden HJ, van Swieten JC (2007) Frontal presentation in progressive supranuclear palsy. Neurology 69(8):723–729
Litvan I, Mangone CA, McKee A, Verny M, Parsa A, Jellinger K, D’Olhaberriague L, Chaudhuri KR, Pearce RK (1996) Natural history of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) and clinical predictors of survival: a clinicopathological study. J Neurol Neurosurg Psychiatry 60(6):615–620
Kim KJ, Jeong SJ, Kim JM (2018) Neurogenic bladder in progressive supranuclear palsy: a comparison with Parkinson’s disease and multiple system atrophy. Neurourol Urodyn 37(5):1724–1730
Steele JC, Richardson JC, Olszewski J (1964) Progressive supranuclear palsy. A Heterogeneous Degeneration Involving the Brain Stem, Basal Ganglia and Cerebellum with Vertical Gaze and Pseudobulbar Palsy Nuchal Dystonia and Dementia. Arch Neurol 10:333–359
Rub U, Del Tredici K, Schultz C, de Vos RA, Jansen Steur EN, Arai K, Braak H (2002) Progressive supranuclear palsy: neuronal and glial cytoskeletal pathology in the higher order processing autonomic nuclei of the lower brainstem. Neuropathol Appl Neurobiol 28(1):12–22
Albers DS, Augood SJ, Park LC, Browne SE, Martin DM, Adamson J, Hutton M, Standaert DG, Vonsattel JP, Gibson GE, Beal MF (2000) Frontal lobe dysfunction in progressive supranuclear palsy: evidence for oxidative stress and mitochondrial impairment. J Neurochem 74(2):878–881
Andrew J, Nathan PW (1964) Lesions on the anterior frontal lobes and disturbances of micturition and defaecation. Brain 87:233–262
Scaravilli T, Pramstaller PP, Salerno A, Egarter-Vigl E, Giometto B, Vitaliani R, An SF, Revesz T (2000) Neuronal loss in Onuf’s nucleus in three patients with progressive supranuclear palsy. Ann Neurol 48(1):97–101
Wenning GK, Scherfler C, Granata R, Bosch S, Verny M, Chaudhuri KR, Jellinger K, Poewe W, Litvan I (1999) Time course of symptomatic orthostatic hypotension and urinary incontinence in patients with postmortem confirmed parkinsonian syndromes: a clinicopathological study. J Neurol Neurosurg Psychiatry 67(5):620–623
Panicker JN (2020) Neurogenic bladder: epidemiology, diagnosis, and management. Semin Neurol 40(5):569–579
Pavy-Le Traon A, Cotterill N, Amarenco G, Duerr S, Kaufmann H, Lahrmann H, Tison F, Wenning GK, Goetz CG, Poewe W, Sampaio C, Schrag A, Rascol O, Martinez-Martin P, Stebbins GT (2018) Clinical rating scales for urinary symptoms in Parkinson disease: critique and recommendations. Mov Disord Clin Pract 5(5):479–491
Blok B C-DD, Del Popolo G, Groen J, Hamid R, Karsenty G, Kessler TM, Pannek J EAU Guidelines on neuro-urology. Retrieved from: https://uroweb.org/guideline/neuro-urology Access date 16/03/2021
NICE (2012) National Institute for Health and Care Excellence guideline [CG148] Urinary incontinence in neurological disease: assessment and management, 2012
Shin JH, Park KW, Heo KO, Chung SJ, Choo MS (2019) Urodynamic study for distinguishing multiple system atrophy from Parkinson disease. Neurology 93(10):e946–e953
Yamamoto T, Sakakibara R, Uchiyama T, Yamaguchi C, Nomura F, Ito T, Yanagisawa M, Yano M, Awa Y, Yamanishi T, Hattori T, Kuwabara S (2012) Receiver operating characteristic analysis of sphincter electromyography for parkinsonian syndrome. Neurourol Urodyn 31(7):1128–1134
Winge K, Jennum P, Lokkegaard A, Werdelin L (2010) Anal sphincter EMG in the diagnosis of parkinsonian syndromes. Acta Neurol Scand 121(3):198–203
Linder J, Libelius R, Nordh E, Holmberg B, Stenlund H, Forsgren L (2012) Anal sphincter electromyography in patients with newly diagnosed idiopathic parkinsonism. Acta Neurol Scand 126(4):248–255
McDonald C, Rees J, Winge K, Newton JL, Burn DJ (2020) Bladder training for urinary tract symptoms in Parkinson disease: a randomized controlled trial. Neurology 94(13):e1427–e1433
Uchiyama T, Sakakibara R, Yamamoto T, Ito T, Yamaguchi C, Awa Y, Yano M, Yanagisawa M, Kobayashi M, Higuchi Y, Ichikawa T, Yamanishi T, Hattori T, Kuwabara S (2009) Comparing bromocriptine effects with levodopa effects on bladder function in Parkinson’s disease. Mov Disord 24(16):2386–2390
Winge K, Werdelin LM, Nielsen KK, Stimpel H (2004) Effects of dopaminergic treatment on bladder function in Parkinson’s disease. Neurourol Urodyn 23(7):689–696
Brusa L, Ponzo V, Stefani A, Ceravolo R, Palermo G, Agro EF, Viselli F, Altavista MC, Iani C, Stocchi F, Stanzione P, Vitale C (2020) Extended release levodopa at bedtime as a treatment for nocturiain Parkinson’s disease: an open label study. J Neurol Sci 410:116625
Zesiewicz TA, Evatt M, Vaughan CP, Jahan I, Singer C, Ordorica R, Salemi JL, Shaw JD, Sullivan KL (2015) Randomized, controlled pilot trial of solifenacin succinate for overactive bladder in Parkinson’s disease. Parkinsonism Relat Disord 21(5):514–520
Batla A, Tayim N, Pakzad M, Panicker JN (2016) Treatment options for urogenital dysfunction in Parkinson’s disease. Curr Treat Options Neurol 18(10):45
Kabay SC, Kabay S, Yucel M, Ozden H (2009) Acute urodynamic effects of percutaneous posterior tibial nerve stimulation on neurogenic detrusor overactivity in patients with Parkinson’s disease. Neurourol Urodyn 28(1):62–67
Giannantoni A, Rossi A, Mearini E, Del Zingaro M, Porena M, Berardelli A (2009) Botulinum toxin A for overactive bladder and detrusor muscle overactivity in patients with Parkinson’s disease and multiple system atrophy. J Urol 182(4):1453–1457
Seth JH, Dowson C, Khan MS, Panicker JN, Fowler CJ, Dasgupta P, Sahai A (2013) Botulinum toxin-A for the treatment of overactive bladder: UK contributions. J Clin Urol 6(2):77–83
Funding
JNP is supported in part by funding from the United Kingdom’s Department of Health NIHR Biomedical Research Centres funding scheme. VI is supported by the National Institute for Health Research University College London Hospitals Biomedical Research Centre. CH is supporting in part by scholar grants from the SIFUD-PP (the francophone society of urodynamics), from LILIAL-GREEN GRC-01 UPMC (Group of clinical REsEarch in Neurourology), from the French Society of Physical and Rehabilitation Medicine (SOFMER) and from the endowment fund Renaître.
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Vichayanrat, E., Hentzen, C., Batla, A. et al. Lower urinary tract dysfunction in Parkinsonian syndromes. Neurol Sci 42, 4045–4054 (2021). https://doi.org/10.1007/s10072-021-05411-y
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DOI: https://doi.org/10.1007/s10072-021-05411-y