Advertisement

Bladder dysfunction as the initial presentation of multiple system atrophy: a prospective cohort study

  • Ryuji SakakibaraEmail author
  • Jalesh Panicker
  • Sara Simeoni
  • Tomoyuki Uchiyama
  • Tatsuya Yamamoto
  • Fuyuki Tateno
  • Masahiko Kishi
  • Yosuke Aiba
Research Article

Abstract

Objectives

Multiple system atrophy (MSA) is a disease that combines autonomic (orthostatic or bladder) with motor [parkinsonian (MSA-P) or cerebellar (MSA-C)] dysfunction. While bladder dysfunction may occur earlier than motor disorders, thus far no prospective study has been available to determine how often and how early bladder autonomic dysfunction predates motor dysfunction in MSA. Therefore, we present data from detailed history-taking in patients with MSA.

Methods

This is a prospective cohort study. Detailed history-taking was performed and a questionnaire administered in 121 MSA patients (73 MSA-C, 48 MSA-P; 74 men, 47 women; age, 58 ± 8.0 years; initial recruitment period, 5 years; follow-up, 6.5 ± 4.0 years).

Results

Among the patients with MSA-C, 40 patients (55%) suffered motor dysfunction first, 22 (30%) suffered autonomic dysfunction first, and 11 (15%) initially suffered both simultaneously. Among the patients with MSA-P, 22 patients (46%) suffered motor dysfunction first, 22 (46%) suffered autonomic dysfunction first, and two (8%) initially suffered both simultaneously. Among the ‘autonomic-first’ subgroup of MSA-C patients, five suffered orthostatic dysfunction first, 13 suffered urinary dysfunction first, and four initially suffered both simultaneously. Among the ‘autonomic-first’ subgroup of MSA-P patients, six suffered orthostatic dysfunction first, nine suffered urinary dysfunction first, and seven initially suffered both simultaneously. Urinary symptoms were further preceded by erectile dysfunction in men. Overall, 18.2% of patients suffered only urinary symptoms initially, and the mean interval from the onset of urinary to the onset of motor symptoms was 2.8 years (range 1–7 years).

Conclusion

In MSA patients, 18.2% presented with bladder dysfunction as the sole initial manifestation, and the mean interval from the onset of urinary to the onset of motor symptoms was 2.8 years. It is clinically important to avoid unnecessary prostatic surgery when MSA patients see urologists before neurologists.

Keywords

Multiple system atrophy Autonomic dysfunction Urinary dysfunction Prostatic hypertrophy Nonmotor signs 

Notes

Acknowledgements

We cordially thank Prof. Niall Quinn in Queen Square, London for his valuable suggestions.

Compliance with ethical standards

Conflict of interest

We have no conflict of interest.

References

  1. 1.
    Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Dürr 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 71:670–676CrossRefGoogle Scholar
  2. 2.
    Sakakibara R, Tateno F, Yamamoto T, Uchiyama T, Yamanishi T (2018) Urological dysfunction in synucleinopathies: epidemiology, pathophysiology and management. Clin Auton Res 28:83–101CrossRefGoogle Scholar
  3. 3.
    Ogawa T, Sakakibara R, Kuno S, Ishizuka O, Kitta T, Yoshimura N (2017) Prevalence and treatment of LUTS in patients with Parkinson disease or multiple system atrophy. Nat Rev Urol 14:79–89CrossRefGoogle Scholar
  4. 4.
    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, Autonomic Disorders Consortium (2017) Natural history of pure autonomic failure: a United States prospective cohort. Ann Neurol 81:287–297Google Scholar
  5. 5.
    Sakakibara R, Hattori T, Uchiyama T, Asahina M, Yamanishi T (2000) Micturitional disturbance in pure autonomic failure. Neurology 54:499–501CrossRefGoogle Scholar
  6. 6.
    Magari T, Fukabori Y, Ogura H, Suzuki K (2013) Lower urinary tract symptoms of neurological origin in urological practice. Clin Auton Res 23:67–72CrossRefGoogle Scholar
  7. 7.
    McKay JH, Cheshire WP (2018) First symptoms in multiple system atrophy. Clin Auton Res 28:215–221.  https://doi.org/10.1007/s10286-017-0500-0 CrossRefGoogle Scholar
  8. 8.
    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 68:65–69CrossRefGoogle Scholar
  9. 9.
    Watanabe H, Saito Y, Terao S, Ando T, Kachi T, Mukai E, Aiba I, Abe Y, Tamakoshi A, Doyu M, Hirayama M, Sobue G (2002) Progression and prognosis in multiple system atrophy: an analysis of 230 Japanese patients. Brain 125:1070–1083CrossRefGoogle Scholar
  10. 10.
    Sakakibara R, Tateno F, Kishi M, Tsuyusaki Y, Terada H, Inaoka T (2014) MIBG myocardial scintigraphy in pre-motor Parkinson’s disease: a review. Parkinson Relat Disord 20:267–273CrossRefGoogle Scholar
  11. 11.
    Tateno F, Sakakibara R, Kawai T, Kishi M, Murano T (2012) Alpha-synuclein in the cerebrospinal fluid differentiates synucleinopathies (Parkinson disease, dementia with Lewy bodies, multiple system atrophy) from Alzheimer disease. Alzheimer Dis Assoc Disord 26:213–216CrossRefGoogle Scholar
  12. 12.
    Palma JA, Norcliffe-Kaufmann L, Kaufmann H (2017) Diagnosis of multiple system atrophy. Auton Neurosci 211:15–25.  https://doi.org/10.1016/j.autneu.2017.10.007 CrossRefGoogle Scholar
  13. 13.
    Sakakibara R, Panicker J, Finazzi-Agro E, Iacovelli V, Bruschini H, Parkinson’s Disease Subcommittee, The Neurourology Promotion Committee in The International Continence Society (2016) A guideline for the management of bladder dysfunction in Parkinson’s disease and other gait disorders. Neurourol Urodyn 35:551–563Google Scholar
  14. 14.
    Takahashi O, Sakakibara R, Tateno F, Kishi M, Tsuyusaki Y, Aiba Y, Yano H, Sugiyama M, Yamamoto T, Yamanishi T, Uchiyama T, Shibata C, Tomaru T (2014) Overactive bladder may precede motor disorder in Parkinson’s disease: a urodynamic study. Parkinson Relat Disord 20:1030–1032CrossRefGoogle Scholar
  15. 15.
    Tandon R, Pradhan S (2015) Autonomic predominant multiple system atrophy in the context of Parkinsonian and cerebellar variants. Clin Neurol Neurosurg 130:110–113CrossRefGoogle Scholar
  16. 16.
    Uzawa A, Sakakibara R, Tamura N, Asahina M, Yamanaka Y, Uchiyama T, Ito T, Yamamoto T, Liu Z, Hattori T (2005) Laryngeal abductor paralysis can be a solitary manifestation of multiple system atrophy. J Neurol Neurosurg Psychiatry 76:1739–1741CrossRefGoogle Scholar
  17. 17.
    Chandiramani VA, Palace J, Fowler CJ (1997) How to recognize patients with parkinsonism who should not have urological surgery. Br J Urol 80:100–104CrossRefGoogle Scholar
  18. 18.
    Köllensperger M, Geser F, Seppi K, Stampfer-Kountchev M, Sawires M, Scherfler C, Boesch S, Mueller J, Koukouni V, Quinn N, Pellecchia MT, Barone P, Schimke N, Dodel R, Oertel W, Dupont E, Østergaard K, Daniels C, Deuschl G, Gurevich T, Giladi N, Coelho M, Sampaio C, Nilsson C, Widner H, Sorbo FD, Albanese A, Cardozo A, Tolosa E, Abele M, Klockgether T, Kamm C, Gasser T, Djaldetti R, Colosimo C, Meco G, Schrag A, Poewe W, Wenning GK, European MSA Study Group (2008) Red flags for multiple system atrophy. Mov Disord 23:1093–1099Google Scholar
  19. 19.
    Yamamoto T, Asahina M, Yamanaka Y, Uchiyama T, Hirano S, Fuse M, Koga Y, Sakakibara R, Kuwabara S (2017) The utility of post-void residual volume versus sphincter electromyography to distinguish between multiple system atrophy and Parkinson’s disease. PLoS One 12(1):e0169405.  https://doi.org/10.1371/journal.pone.0169405 (eCollection 2017) CrossRefGoogle Scholar
  20. 20.
    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 76:1645–1648CrossRefGoogle Scholar
  21. 21.
    Coon EA, Cutsforth-Gregory JK, Benarroch EE (2018) Neuropathology of autonomic dysfunction in synucleinopathies. Mov Disord 33:349–358.  https://doi.org/10.1002/mds.27186 CrossRefGoogle Scholar
  22. 22.
    Sakuta M, Nakanishi T, Toyokura Y. Anal muscle electromyograms differ in amyotrophic lateral sclerosis and Shy-Drager syndrome. Neurology. 1978;28:1289–1293CrossRefGoogle Scholar
  23. 23.
    Sakakibara R, Uchiyama T, Yamanishi T, Kishi M (2009) Sphincter EMG as a diagnostic tool in autonomic disorders. Clin Auton Res 19:20–31CrossRefGoogle Scholar
  24. 24.
    Hoeritzauer I, Phé V, Panicker JN (2016) Urologic symptoms and functional neurologic disorders. Handb Clin Neurol 139:469–481CrossRefGoogle Scholar
  25. 25.
    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 30:411–415CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Neurology, Internal Medicine, Sakura Medical CenterToho UniversitySakuraJapan
  2. 2.Uro-NeurologyThe National Hospital for Neurology and Neurosurgery and UCL Institute of NeurologyLondonUK
  3. 3.Continence CenterDokkyo Medical CollegeTochigiJapan
  4. 4.NeurologyChiba UniversityChibaJapan
  5. 5.Urology, Sakura Medical CenterToho UniversitySakuraJapan

Personalised recommendations