Degenerative Diseases (Multiple Sclerosis, Parkinson’s Disease)

  • Petros Georgopoulos
  • Konstantinos-Vaios Mytilekas
  • Apostolos Apostolidis


Lower urinary tract symptoms (LUTS) and incontinence are highly prevalent among multiple sclerosis (MS ) patients and are strongly related to the duration, progress and severity of the neurological condition. Mixed LUTS are common, with a higher prevalence of detrusor overactivity (DO) in urodynamic investigations. Interestingly, upper urinary tract damage is infrequent in MS patients. Despite the negative effect on QoL, the majority of MS patients do not consult a urologist. Available treatments are similar as in non-neurogenic LUTS, albeit with a lower level of evidence apart from intradetrusor injections of botulinum neurotoxin A. Lifestyle interventions with or without antimuscarinics and clean intermittent catheterizations are the mainstay of management, but with significant rates of discontinuation. Invasive surgery (enterocystoplasty, urinary diversion procedures) is spared for refractory cases and those patients with upper extremity dexterity issues.

Similarly, LUTS are common in Parkinson’s disease (PD) patients, with nocturia being the most prevalent symptom and DO the most common urodynamic observation, followed by detrusor underactivity and bladder outlet obstruction. Antimuscarinics are the mainstay of medical treatment for storage LUTS in PD patients, while sparse data exist on the use of alpha-blockers. Surgical treatment of bladder outlet obstruction (BOO) is no longer a contraindication in PD patients so long as multiple system atrophy is excluded. Minimally invasive treatments, such as botulinum-A toxin bladder injections, percutaneous tibial nerve stimulation and deep brain stimulation, are considered in cases of refractory symptoms. Manipulation of the gut and urinary microbiota might play a role in the therapeutic management of both PD and associated LUTS in the future.


Multiple sclerosis Lower urinary tract Incontinence Treatment Quality of life Antimuscarinics/anticholinergics Botulinum neurotoxin Neuromodulation Catheterization Cannabinoids Parkinson’s disease Bladder Prostate Alpha-blockers Deep brain stimulation Microbiota 



Actionable Bladder Symptom and Screening Tool


Bladder outlet obstruction


Benign prostatic obstruction


Clean Intermittent Catheterization


Detrusor overactivity


Digital rectal examination


Detrusor sphincter dyssynergia


Detrusor underactivity


European Association of Urology


Expanded Disability Status Scale


International Prostate Symptom Score


Intermittent self-catheterization


Lower urinary tract symptoms


Multiple sclerosis


Multiple system atrophy


Neurogenic lower urinary tract symptoms


Non-motor symptoms


Overactive bladder


Odds ratio


Parkinson’s disease


Pelvic organ prolapse


Primary progressive multiple sclerosis


Progressive relapsing


Patient-reported outcome measures


Percutaneous tibial nerve stimulation


Post-void residual


Quality of life


Relapsing–remitting multiple sclerosis


Spinal cord injury


Sacral neuromodulation


Secondary progressive multiple sclerosis


Transurethral resection of the prostate


Urodynamic study


Urinary incontinence


United Kingdom


Urinary tract infections


Urge urinary incontinence


  1. 1.
    World Health Organization. Atlas multiple sclerosis resources in the world 2008. Geneva: WHO Press; 2008.Google Scholar
  2. 2.
    Kingwell E, Marriott JJ, Jette N, Pringsheim T, Makhani N, Morrow SA, Fisk JD, Evans C, Beland SG, Kulaga S, Dykeman J, Wolfson C, Koch MW, Marrie RA. Incidence and prevalence of multiple sclerosis in Europe: a systematic review. BMC Neurol. 2013;13:128.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Howard J, Trevick S, Younger DS. Epidemiology of multiple sclerosis. Neurol Clin. 2016;34(4):919–39.PubMedCrossRefGoogle Scholar
  4. 4.
    Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N Engl J Med. 2000;343(13):938–52. ReviewPubMedCrossRefGoogle Scholar
  5. 5.
    Lublin FD, Reingold SC, Cohen JA, Cutter GR, Sørensen PS, Thompson AJ, Wolinsky JS, Balcer LJ, Banwell B, Barkhof F, Bebo B Jr, Calabresi PA, Clanet M, Comi G, Fox RJ, Freedman MS, Goodman AD, Inglese M, Kappos L, Kieseier BC, Lincoln JA, Lubetzki C, Miller AE, Montalban X, O’Connor PW, Petkau J, Pozzilli C, Rudick RA, Sormani MP, Stüve O, Waubant E, Polman CH. Defining the clinical course of multiple sclerosis: the 2013 revisions. Neurology. 2014;83(3):278–86.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Sadiq A, Brucker BM. Management of neurogenic lower urinary tract dysfunction in multiple sclerosis patients. Curr Urol Rep. 2015;16(7):44.PubMedCrossRefGoogle Scholar
  7. 7.
    de Sèze M, Ruffion A, Denys P, Joseph PA. Perrouin-Verbe B; GENULF. The neurogenic bladder in multiple sclerosis: review of the literature and proposal of management guidelines. Mult Scler. 2007;13(7):915–28. Epub 2007 Mar 15. ReviewPubMedCrossRefGoogle Scholar
  8. 8.
    Panicker JN, Fowler CJ. Lower urinary tract dysfunction in patients with multiple sclerosis. Handb Clin Neurol. 2015;130:371–81.PubMedCrossRefGoogle Scholar
  9. 9.
    Fowler CJ, Griffiths D, de Groat WC. The neural control of micturition. Nat Rev Neurosci. 2008;9(6):453–66.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Phe V, Chartier-Kastler E, Panicker JN. Management of neurogenic bladder in patients with multiple sclerosis. Nat Rev Urol. 2016;13:275–88.PubMedCrossRefGoogle Scholar
  11. 11.
    Khalaf KM, Coyne KS, Globe DR, Armstrong EP, Malone DC, Burks J. Lower urinary tract symptom prevalence and management among patients with multiple sclerosis. Int J MS Care. 2015;17(1):14–25.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Kragt JJ, Hoogervorst EL, Uitdehaag BM, Polman CH. Relation between objective and subjective measures of bladder dysfunction in multiple sclerosis. Neurology. 2004;63(9):1716–8.PubMedCrossRefGoogle Scholar
  13. 13.
    Wyndaele JJ, Castro D, Madersbacher H. Neurogenic and faecal incontinence. In: Abrams P, editor. Incontinence. Paris: Health Publications; 2005. p. 1059–162.Google Scholar
  14. 14.
    Blaivas JG, Kaplan SA. Urologic dysfunction in patients with multiple sclerosis. Semin Neurol. 1988;8(2):159–65.PubMedCrossRefGoogle Scholar
  15. 15.
    Gallien P, Nicolas B, Robineau S, Le Bot MP, de Crouy AC, Durufle A, Edan G, Brissot R. Urological complications in multiple sclerosis: study of risk factors. Ann Readaptation Med Phys. 1998;41:155–8.CrossRefGoogle Scholar
  16. 16.
    Groen J, Pannek J, Castro Diaz D, Del Popolo G, Gross T, Hamid R, Karsenty G, Kessler TM, Schneider M, ‘t Hoen L, Blok B. Summary of European Association of Urology (EAU) Guidelines on Neuro-Urology. Eur Urol. 2016;69:324–33.PubMedCrossRefGoogle Scholar
  17. 17.
    Fowler CJ, Panicker JN, Drake M, Harris C, Harrison SC, Kirby M, Lucas M, Macleod N, Mangnall J, North A, Porter B, Reid S, Russell N, Watkiss K, Wells M. A UK consensus on the management of the bladder in multiple sclerosis. J Neurol Neurosurg Psychiatry. 2009;80:470–7.PubMedGoogle Scholar
  18. 18.
    Redelings MD, McCoy L, Sorvillo F. Multiple sclerosis mortality and patterns of comorbidity in the United States from 1990 to 2001. Neuroepidemiology. 2006;26:102–7.PubMedCrossRefGoogle Scholar
  19. 19.
    De Ridder D, van Poppel H, Demonty L, D’Hooghe B, Gonsette R, Carton H, Baert L. Bladder cancer in patients with multiple sclerosis treated with cyclophosphamide. J Urol. 1998;159(6):1881–4.PubMedCrossRefGoogle Scholar
  20. 20.
    Lawrenson R, Wyndaele JJ, Vlachonikolis I, Farmer C, Glickman S. Renal failure in patients with neurogenic lower urinary tract dysfunction. Neuroepidemiology. 2001;187:138–43.CrossRefGoogle Scholar
  21. 21.
    Ouslander JG. Management of overactive bladder. N Engl J Med. 2004;350(8):786–99. ReviewPubMedCrossRefGoogle Scholar
  22. 22.
    Clark R, Welk B. Patient reported outcome measures in neurogenic bladder. Transl Androl Urol. 2016;5(1):22–30.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Burks J, Chancellor M, Bates B, Denys P, MacDiarmid S, Nitti V, et al. Development and validation of the actionable bladder symptom screening tool for multiple sclerosis patients. Int J MS Care Winter. 2013;15(4):182–92.CrossRefGoogle Scholar
  24. 24.
    Welk B, Morrow S, Madarasz W, Baverstock R, Macnab J, Sequeira K. The validity and reliability of the neurogenic bladder symptom score. J Urol. 2014;192(2):452–7.PubMedCrossRefGoogle Scholar
  25. 25.
    Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983;33(11):1444–52.PubMedCrossRefGoogle Scholar
  26. 26.
    Kurtzke JF. On the origin of EDSS. Mult Scler Relat Disord. 2015;4(2):95–103.PubMedCrossRefGoogle Scholar
  27. 27.
    Bonniaud V, Jackowski D, Parratte B, Paulseth R, Grad S, Margetts P, Guyatt G. Quality of life in multiple sclerosis patients with urinary disorders: discriminative validation of the English version of Qualiveen. Qual Life Res. 2005;14(2):425–31.PubMedCrossRefGoogle Scholar
  28. 28.
    Blok B, Padilla-Fernández B, Pannek J, Castro-Diaz D, Del Popolo G, Groen J, Hamid R, Karsenty G, Kessler TM, Guidelines Associates: Ecclestone H, Musco S, Padilla-Fernández B, Phé V, Sartori A, ‘t Hoen L. Guidelines on neuro-urology 2018. European Association of Urology.
  29. 29.
    Campbell, MF, Wein AJ, Kavoussi LR. In: Wein AJ, Kavoussi LR, editors. Campbell-Walsh urology. Philadelphia: Elsevier/Saunders; 2012.Google Scholar
  30. 30.
    Allio BA, Peterson AC. Urodynamic and physiologic patterns associated with the common causes of neurogenic bladder in adults. Transl Androl Urol. 2016;5(1):31–8.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Litwiller SE, Frohman EM, Zimmern PE. Multiple sclerosis and the urologist. J Urol. 1999;161(3):743–57. ReviewPubMedCrossRefGoogle Scholar
  32. 32.
    Ukkonen M, Elovaara I, Dastidar P, Tammela TL. Urodynamic findings in primary progressive multiple sclerosis are associated with increased volumes of plaques and atrophy in the central nervous system. Acta Neurol Scand. 2004;109:100–5.PubMedCrossRefGoogle Scholar
  33. 33.
    Sammer U, Walter M, Knüpfer SC, Mehnert U, Bode-Lesniewska B, Kessler TM. Do we need surveillance urethro-cystoscopy in patients with neurogenic lower urinary tract dysfunction? PLoS One. 2015;10(10):e0140970.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    De Ridder D, Vermeulen C, Ketelaer P, Van Poppel H, Baert L. Pelvic floor rehabilitation in multiple sclerosis. Acta Neurol Belg. 1999;99(1):61–4.PubMedGoogle Scholar
  35. 35.
    McClurg D, Ashe RG, Marshall K, Lowe-Strong AS. Comparison of pelvic floor muscle training, electromyography biofeedback, and neuromuscular electrical stimulation for bladder dysfunction in people with multiple sclerosis: a randomized pilot study. Neurourol Urodyn. 2006;25(4):337–48.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    McClurg D, Ashe RG, Lowe-Strong AS. Neuromuscular electrical stimulation and the treatment of lower urinary tract dysfunction in multiple sclerosis—a double blind, placebo controlled, randomised clinical trial. Neurourol Urodyn. 2008;27(3):231–7.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Centonze D, Petta F, Versace V, Rossi S, Torelli F, Prosperetti C, Rossi S, Marfia GA, Bernardi G, Koch G, Miano R, Boffa L, Finazzi-Agrò E. Effects of motor cortex rTMS on lower urinary tract dysfunction in multiple sclerosis. Mult Scler. 2007;13(2):269–71.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Çetinel B, Tarcan T, Demirkesen O, Özyurt C, Şen İ, Erdoğan S, Siva A. Management of lower urinary tract dysfunction in multiple sclerosis: a systematic review and Turkish consensus report. Neurourol Urodyn. 2013;32(8):1047–57.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Amarenco G, Sutory M, Zachoval R, Agarwal M, Del Popolo G, Tretter R, Compion G, De Ridder D. Solifenacin is effective and well tolerated in patients with neurogenic detrusor overactivity: results from the double-blind, randomized, active- and placebo-controlled SONIC urodynamic study. Neurourol Urodyn. 2017;36(2):414–21.PubMedCrossRefGoogle Scholar
  40. 40.
    van Rey F, Heesakkers J. Solifenacin in multiple sclerosis patients with overactive bladder: a prospective study. Adv Urol. 2011;2011:834753.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Amend B, Hennenlotter J, Schäfer T, Horstmann M, Stenzl A, Sievert KD. Effective treatment of neurogenic detrusor dysfunction by combined high-dosed antimuscarinics without increased side-effects. Eur Urol. 2008;53(5):1021–8.PubMedCrossRefGoogle Scholar
  42. 42.
    Fader M, Glickman S, Haggar V, Barton R, Brooks R, Malone-Lee J. Intravesical atropine compared to oral oxybutynin for neurogenic detrusor overactivity: a double-blind, randomized crossover trial. J Urol. 2007;177(1):208–13. discussion 213PubMedCrossRefGoogle Scholar
  43. 43.
    Panicker JN, Fowler CJ, Kessler TM. Lower urinary tract dysfunction in the neurological patient: clinical assessment and management. Lancet Neurol. 2015;14:720–32.PubMedCrossRefGoogle Scholar
  44. 44.
    Kavia RB, De Ridder D, Constantinescu CS, Stott CG, Fowler CJ. Randomized controlled trial of Sativex to treat detrusor overactivity in multiple sclerosis. Mult Scler. 2010;16(11):1349–59.PubMedCrossRefGoogle Scholar
  45. 45.
    Freeman RM, Adekanmi O, Waterfield MR, Waterfield AE, Wright D, Zajicek J. The effect of cannabis on urge incontinence in patients with multiple sclerosis: a multicentre, randomised placebo-controlled trial (CAMS-LUTS). Int Urogynecol J Pelvic Floor Dysfunct. 2006;17(6):636–41. Epub 2006 Mar 22PubMedCrossRefGoogle Scholar
  46. 46.
    Wade DT, Makela P, Robson P, House H, Bateman C. Do cannabis-based medicinal extracts have general or specific effects on symptoms in multiple sclerosis? A double-blind, randomized, placebo-controlled study on 160 patients. Mult Scler. 2004;10(4):434–41.PubMedCrossRefGoogle Scholar
  47. 47.
    Brady CM, DasGupta R, Dalton C, Wiseman OJ, Berkley KJ, Fowler CJ. An open-label pilot study of cannabis-based extracts for bladder dysfunction in advanced multiple sclerosis. Mult Scler. 2004;10(4):425–33.PubMedCrossRefGoogle Scholar
  48. 48.
    Andersson KE. Current and future drugs for treatment of MS-associated bladder dysfunction. Ann Phys Rehabil Med. 2014;57(5):321–8.PubMedCrossRefGoogle Scholar
  49. 49.
    Koppel BS, Brust JC, Fife T, Bronstein J, Youssof S, Gronseth G, Gloss D. Systematic review: efficacy and safety of medical marijuana in selected neurologic disorders: report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology. 2014;82(17):1556–63.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Podda G, Constantinescu CS. Nabiximols in the treatment of spasticity, pain and urinary symptoms due to multiple sclerosis. Expert Opin Biol Ther. 2012;12(11):1517–31.PubMedCrossRefGoogle Scholar
  51. 51.
    Ruggieri MR Sr. Cannabinoids: potential targets for bladder dysfunction. Handb Exp Pharmacol. 2011;202:425–51.CrossRefGoogle Scholar
  52. 52.
    Tyagi P, Tyagi V, Yoshimura N, Chancellor M. Functional role of cannabinoid receptors in urinary bladder. Indian J Urol. 2010;26(1):26–35.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Bosma R, Wynia K, Havlikova E, et al. Efficacy of desmopressin in patients with multiple sclerosis suffering from bladder dysfunction: a meta-analysis. Acta Neurol Scand. 2005;112:1–5.PubMedCrossRefGoogle Scholar
  54. 54.
    Cruz F, Herschorn S, Aliotta P, Brin M, Thompson C, Lam W, Daniell G, Heesakkers J, Haag-Molkenteller C. Efficacy and safety of onabotulinumtoxinA in patients with urinary incontinence due to neurogenic detrusor overactivity: a randomised, double-blind, placebo-controlled trial. Eur Urol. 2011;60(4):742–50.PubMedCrossRefGoogle Scholar
  55. 55.
    Ginsberg D, Gousse A, Keppenne V, Sievert KD, Thompson C, Lam W, Brin MF, Jenkins B, Haag-Molkenteller C. Phase 3 efficacy and tolerability study of onabotulinumtoxinA for urinary incontinence from neurogenic detrusor overactivity. J Urol. 2012;187(6):2131–9.PubMedCrossRefGoogle Scholar
  56. 56.
    Rovner E, Dmochowski R, Chapple C, Thompson C, Lam W, Haag- Molkenteller C. OnabotulinumtoxinA improves urodynamic outcomes in patients with neurogenic detrusor overactivity. Neurourol Urodyn. 2013;32:1109–15.PubMedCrossRefGoogle Scholar
  57. 57.
    Ginsberg D, Cruz F, Herschorn S, Gousse A, Keppenne V, Aliotta P, et al. OnabotulinumtoxinA is effective in patients with urinary incontinence due to neurogenic detrusor overactivity regardless of concomitant anticholinergic use or neurologic etiology. Adv Ther. 2013;30(9):819–33.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Sussman D, Patel V, Del Popolo G, Lam W, Globe D, Pommerville P. Treatment satisfaction and improvement in health-related quality of life with onabotulinumtoxinA in patients with urinary incontinence due to neurogenic detrusor overactivity. Neurourol Urodyn. 2013;32(3):242–9.PubMedCrossRefGoogle Scholar
  59. 59.
    Mehnert U, Birzele J, Reuter K, Schurch B. The effect of botulinum toxin type a on overactive bladder symptoms in patients with multiple sclerosis: a pilot study. J Urol. 2010;184:1011–6.PubMedCrossRefGoogle Scholar
  60. 60.
    Kalsi V, Gonzales G, Popat R, Apostolidis A, Elneil S, Dasgupta P, Fowler CJ. Botulinum injections for the treatment of bladder symptoms of multiple sclerosis. Ann Neurol. 2007;62(5):452–7.PubMedCrossRefGoogle Scholar
  61. 61.
    Joussain C, Popoff M, Phé V, Even A, Falcou L, Chartier-Kastler E, Schurch B, Denys P. Long-term real life efficacy of onabotulinum toxin A for the treatment of neurogenic detrusor overactivity in a population using intermitten self-catheterization. Ann Phys Rehabil Med. 2016;59S:e105.CrossRefGoogle Scholar
  62. 62.
    Deffontaines-Rufin S, Weil M, Verollet D, Peyrat L, Amarenco G. Botulinum toxin A for the treatment of neurogenic detrusor overactivity in multiple sclerosis patients. Int Braz J Urol. 2011;37(5):642–8.PubMedCrossRefGoogle Scholar
  63. 63.
    Lekka E, Lee LK. Successful treatment with intradetrusor botulinum‑A toxin for urethral urinary leakage (catheter bypassing) in patients with endstaged multiple sclerosis and indwelling suprapubic catheters. Eur Urol. 2006;50:806–10.PubMedCrossRefGoogle Scholar
  64. 64.
    Mahfouz W, Karsenty G, Corcos J. Injection of botulinum toxin type A in the urethral sphincter to treat lower urinary tract dysfunction: review of indications, techniques and results: 2011 update. Can J Urol. 2011;18:5787–95.PubMedGoogle Scholar
  65. 65.
    Gallien P, Reymann JM, Amarenco G, Nicolas B, de Sèze M, Bellissant E. Placebo controlled, randomized, double blind study of the effects of botulinum A toxin on detrusor sphincter dyssynergia in multiple sclerosis patients. J Neurol Neurosurg Psychiatry. 2005;76:1670–6.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Kabay S, Kabay SC, Yucel M, Ozden H, Yilmaz Z, Aras O, Aras B. The clinical and urodynamic results of a 3-month percutaneous posterior tibial nerve stimulation treatment in patients with multiple sclerosis-related neurogenic bladder dysfunction. Neurourol Urodyn. 2009;28(8):964–8.PubMedCrossRefGoogle Scholar
  67. 67.
    Kabay SC, Kabay S, Yucel M, Ozden H. Acute urodynamic effects of percutaneous posterior tibial nerve stimulation on neurogenic detrusor overactivity in patients with Parkinson’s disease. Neurourol Urodyn. 2009;28(1):62–7.PubMedCrossRefGoogle Scholar
  68. 68.
    Kabay SC, Yucel M, Kabay S. Acute effect of posterior tibial nerve stimulation on neurogenic detrusor overactivity in patients with multiple sclerosis: urodynamic study. Urology. 2008;71(4):641–5.PubMedCrossRefGoogle Scholar
  69. 69.
    Gobbi C, Digesu GA, Khullar V, El Neil S, Caccia G, Zecca C. Percutaneous posterior tibial nerve stimulation as an effective treatment of refractory lower urinary tract symptoms in patients with multiple sclerosis: preliminary data from a multicentre, prospective, open label trial. Mult Scler. 2011;17(12):1514–9.PubMedCrossRefGoogle Scholar
  70. 70.
    Zecca C, Digesu GA, Robshaw P, Singh A, Elneil S, Gobbi C. Maintenance percutaneous posterior nerve stimulation for refractory lower urinary tract symptoms in patients with multiple sclerosis: an open label, multicenter, prospective study. J Urol. 2014;191(3):697–702.PubMedCrossRefGoogle Scholar
  71. 71.
    Canbaz Kabay S, Kabay S, Mestan E, Cetiner M, Ayas S, Sevim M, Ozden H, Karaman HO. Long term sustained therapeutic effects of percutaneous posterior tibial nerve stimulation treatment of neurogenic overactive bladder in multiple sclerosis patients: 12-months results. Neurourol Urodyn. 2017;36(1):104–10.PubMedCrossRefGoogle Scholar
  72. 72.
    de Sèze M, Raibaut P, Gallien P, Even-Schneider A, Denys P, Bonniaud V, Gamé X, Amarenco G. Transcutaneous posterior tibial nerve stimulation for treatment of the overactive bladder syndrome in multiple sclerosis: results of a multicenter prospective study. Neurourol Urodyn. 2011;30(3):306–11.PubMedCrossRefGoogle Scholar
  73. 73.
    Ruud Bosch JL, Groen J. Treatment of refractory urge urinary incontinence with sacral spinal nerve stimulation in multiple sclerosis patients. Lancet. 1996;348:717–9.PubMedCrossRefGoogle Scholar
  74. 74.
    Minardi D, Muzzonigro G. Sacral neuromodulation in patients with multiple sclerosis. World J Urol. 2012;30:123–8.PubMedCrossRefGoogle Scholar
  75. 75.
    Chaabane W, Guillotreau J, Castel-Lacanal E, Abu-Anz S, De Boissezon X, Malavaud B, Marque P, Sarramon JP, Rischmann P, Game X. Sacral neuromodulation for treating neurogenic bladder dysfunction: clinical and urodynamic study. Neurourol Urodyn. 2011;30(4):547–50.PubMedCrossRefGoogle Scholar
  76. 76.
    Read DJ, Matthews WB, Higson RH. The effect of spinal cord stimulation on function in patients with multiple sclerosis. Brain. 1980;103:803–33.PubMedCrossRefGoogle Scholar
  77. 77.
    Primus G. Maximal electrical stimulation in neurogenic detrusor hyperactivity: experiences in multiple sclerosis. Eur J Med. 1992;1:80–2.PubMedGoogle Scholar
  78. 78.
    Hawkes CH, Fawcett D, Cooke ED Emson PC, Paul EA, Bowcock SA. Dorsal column stimulation in multiple sclerosis: Effects on bladder, leg blood flow and peptides. Appl Neurophysiol. 1981;44:62–70.PubMedGoogle Scholar
  79. 79.
    Berg V, Bergmann S, Hovdal H, Hovdal H. The value of dorsal column stimulation in multiple sclerosis. Scand J Rehabil Med. 1982;14:183–91.PubMedGoogle Scholar
  80. 80.
    Fjorback MV, Rijkhoff N, Petersen T, Nohr M, Sinkjaer T. Event driven electrical stimulation of the dorsal penile/clitoral nerve for management of neurogenic detrusor overactivity in multiple sclerosis. Neurourol Urodyn. 2006;25(4):349–55.PubMedCrossRefGoogle Scholar
  81. 81.
    Zachoval R, Pitha J, Medova E, Heracek J, Lukes M, Zalesky M, Urban M. Augmentation cystoplasty in patients with multiple sclerosis. Urol Int. 2003;70:21–6.PubMedCrossRefGoogle Scholar
  82. 82.
    Legrand G, Rouprêt M, Comperat E, Even-Schneider A, Denys P, Chartier-Kastler E. Functional outcomes after management of end-stage neurological bladder dysfunction with ileal conduit in a multiple sclerosis population: a monocentric experience. Urology. 2011;78(4):937–41.PubMedCrossRefGoogle Scholar
  83. 83.
    Guillotreau J, Panicker JN, Castel-Lacanal E, Viala F, Roumiguié M, Malavaud B, Marque P, Clanet M, Rischmann P, Gamé X. Prospective evaluation of laparoscopic assisted cystectomy and ileal conduit in advanced multiple sclerosis. Urology. 2012;80(4):852–7.PubMedCrossRefGoogle Scholar
  84. 84.
    Vahter L, Zopp I, Kreegipuu M, Kool P, Talvik T, Gross-Paju K. Clean intermittent self-catheterization in persons with multiple sclerosis: the influence of cognitive dysfunction. Mult Scler. 2009;15(3):379–84.PubMedCrossRefGoogle Scholar
  85. 85.
    Kornhuber HH, Schutz A. Efficient treatment of neurogenic bladder disorders in multiple sclerosis with initial intermittent catheterization and ultrasound- controlled training. Eur Neurol. 1990;30:260–7.PubMedCrossRefGoogle Scholar
  86. 86.
    Castel-Lacanal E, Gamé X, De Boissezon X, Guillotreau J, Braley-Berthoumieux E, Terracol C, Gasq D, Labrunee M, Viala F, Rischmann P, Clanet M, Marque P. Impact of intermittent catheterization on the quality of life of multiple sclerosis patients. World J Urol. 2013;31(6):1445–50. Epub 2013 Jan 6CrossRefPubMedGoogle Scholar
  87. 87.
    O’Riordan JI, Doherty C, Javed M, Brophy D, Hutchinson M, Quinlan D. Do alpha-blockers have a role in lower urinary tract dysfunction in multiple sclerosis? J Urol. 1995;153(4):1114–6.PubMedCrossRefGoogle Scholar
  88. 88.
    Francomano D, Ilacqua A, Cortese A, Tartaglia G, Lenzi A, Inghilleri M, Aversa A. Effects of daily tadalafil on lower urinary tract symptoms in young men with multiple sclerosis and erectile dysfunction: a pilot study. J Endocrinol Invest. 2017;40(3):275–9.PubMedCrossRefGoogle Scholar
  89. 89.
    Hattori T, Yasuda K, Kita K, Hirayama K. Voiding dysfunction in Parkinson’s disease. Jpn J Psychiatry Neurol. 1992;46(1):181–6.PubMedGoogle Scholar
  90. 90.
    Benli E, Özer FF, Kaya Y, Özcan TŞ, Ayyıldız A. Is there a difference between Parkinson disease patients and a control group in terms of urinary symptoms and quality of life? Turk J Med Sci. 2016;46(6):1665–71.PubMedCrossRefGoogle Scholar
  91. 91.
    Araki I, Kuno S. Assessment of voiding dysfunction in Parkinson’s disease by the international prostate symptom score. J Neurol Neurosurg Psychiatry. 2000;68(4):429–33.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Lemack GE, Dewey RB Jr, Roehrborn CG, O’Suilleabhain PE, Zimmern PE. Questionnaire-based assessment of bladder dysfunction in patients with mild to moderate Parkinson’s disease. Urology. 2000;56(2):250–4.PubMedCrossRefGoogle Scholar
  93. 93.
    Campos-Sousa RN, Quagliato E, da Silva BB, et al. Urinary symptoms in Parkinson’s disease: prevalence and associated factors. Arq Neuropsiquiatr. 2003;61(2B):359–63.PubMedCrossRefGoogle Scholar
  94. 94.
    Sakakibara R, Shinotoh H, Uchiyama T, Sakuma M, Kashiwado M, Yoshiyama M, et al. Questionnaire-based assessment of pelvic organ dysfunction in Parkinson’s disease. Auton Neurosci. 2001;92(1–2):76–85.PubMedCrossRefGoogle Scholar
  95. 95.
    Yeo L, Singh R, Gundeti M, Barua JM, Masood J. Urinary tract dysfunction in Parkinson’s disease: a review. Int Urol Nephrol. 2012;44:415–24.PubMedCrossRefGoogle Scholar
  96. 96.
    Barone P, Antonini A, Colosimo C, et al. The PRIAMO study: A multicenter assessment of nonmotor symptoms and their impact on quality of life in Parkinson’s disease. Mov Disord. 2009;24:1641–9.PubMedCrossRefGoogle Scholar
  97. 97.
    Ragab MM, Mohammed ES. Idiopathic Parkinson’s disease patients at the urologic clinic. Neurourol Urodyn. 2011;30:1258–61.PubMedGoogle Scholar
  98. 98.
    Winge K, Nielsen KK. Bladder dysfunction in advanced Parkinson’s disease. Neurourol Urodyn. 2012;31:1279–83.PubMedCrossRefGoogle Scholar
  99. 99.
    Uchiyama T, Sakakibara R, Yamamoto T, et al. Urinary dysfunction in early and untreated Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2011;82:1382–6.PubMedCrossRefGoogle Scholar
  100. 100.
    Barrero R, Mir P, Cayuela A, et al. Urinary symptoms and urodynamic findings in Parkinson’s disease. Neurologia. 2007;22(2):93–8.PubMedGoogle Scholar
  101. 101.
    Zis P, Martinez-Martin P, Sauerbier A, et al. Non-motor symptoms burden in treated and untreated early Parkinson’s disease patients: argument for non-motor subtypes. Eur J Neurol. 2015;22(8):1145–50.PubMedCrossRefGoogle Scholar
  102. 102.
    Li-Mei Z, Xu-Ping Z. Investigation of urination disorder in Parkinson’s disease. Chin Med J (Engl). 2015;128(21):2906–12.CrossRefGoogle Scholar
  103. 103.
    Baig F, Lawton M, Rolinski M, et al. Delineating nonmotor symptoms in early Parkinson’s disease and first-degree relatives. Mov Disord. 2015;30(13):1759–66.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Jiang SM, Yuan YS, Tong Q, et al. The association between clinically relevant anxiety and other non-motor symptoms in Parkinson’s disease. Neurol Sci. 2015;36(11):2105–9.PubMedCrossRefGoogle Scholar
  105. 105.
    Winge K, Skau AM, Stimpel H, Nielsen KK, Werdelin L. Prevalence of bladder dysfunction in Parkinson’s disease. Neurourol Urodyn. 2006;25(2):116–22.PubMedCrossRefGoogle Scholar
  106. 106.
    Sakakibara R, Tateno F, Kishi M, Tsuyuzaki Y, Uchiyama T, Yamamoto T. Pathophysiology of bladder dysfunction in Parkinson’s disease. Neurobiol Dis. 2012;46(3):565–71.PubMedCrossRefGoogle Scholar
  107. 107.
    Ou R, Yang J, Cao B, et al. Progression of non-motor symptoms in Parkinson’s disease among different age populations: a two-year follow-up study. J Neurol Sci. 2016;360:72–7.PubMedCrossRefGoogle Scholar
  108. 108.
    Sakushima K, Yamazaki S, Fukuma S, et al. Influence of urinary urgency and other urinary disturbances on falls in Parkinson’s disease. J Neurol Sci. 2016;360:153–7.PubMedCrossRefGoogle Scholar
  109. 109.
    Krygowska-Wajs A, Weglarz W, Szczudlik ZD. Micturition disturbances in Parkinson’s disease. Clinical and urodynamic evaluation. Neurol Neurochir Pol. 2002;36(1):25–32.PubMedGoogle Scholar
  110. 110.
    Defreitas GA, Lemack GE, Zimmern PE, et al. Distinguishing neurogenic from non-neurogenic detrusor overactivity: a urodynamic assessment of lower urinary tract symptoms in patients with and without Parkinson’s disease. Urology. 2003;62(4):651–5.PubMedCrossRefGoogle Scholar
  111. 111.
    Liu Z, Uchiyama T, Sakakibara R, Yamamoto T. Underactive and overactive bladders are related to motor function and quality of life in Parkinson’s disease. Int Urol Nephrol. 2015;47(5):751–7.PubMedCrossRefGoogle Scholar
  112. 112.
    Terayama K, Sakakibara R, Ogawa A, et al. Weak detrusor contractility correlates with motor disorders in Parkinson’s disease. Mov Disord. 2012;27(14):1775–80.PubMedCrossRefGoogle Scholar
  113. 113.
    Xue P, Wang T, Zong H, Zhang Y. Urodynamic analysis and treatment of male Parkinson’s disease patients with voiding dysfunction. Chin Med J (Engl). 2014;127(5):878–81.Google Scholar
  114. 114.
    McDonald C, Winge K, Burn DJ. Lower urinary tract symptoms in Parkinson’s disease: prevalence, aetiology and management. Parkinsonism Relat Disord. 2017;35:8–16.PubMedCrossRefGoogle Scholar
  115. 115.
    Roth B, Studer UE, Fowler CJ, Kessler TM. Benign prostatic obstruction and Parkinson’s disease—should transurethral resection of the prostate be avoided? J Urol. 2009;181(5):2209–13.PubMedCrossRefGoogle Scholar
  116. 116.
    Sakakibara R, Hattori T, Uchiyama T, Yamanishi T. Videourodynamic and sphincter motor unit potential analyses in Parkinson’s disease and multiple system atrophy. J Neurol Neurosurg Psychiatry. 2001;71(5):600–6.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Sievert KD, Kunit T. Emerging techniques in ‘truly’ minimal-invasive treatment options of benign prostatic obstruction. Curr Opin Urol. 2017;27(3):287–92.PubMedCrossRefGoogle Scholar
  118. 118.
    Ogawa T, Sakakibara R, Kuno S, Ishizuka O, Kitta T, Yoshimura N. Prevalence and treatment of LUTS in patients with Parkinson disease or multiple system atrophy. Nat Rev Urol. 2017;14(2):79–89.PubMedCrossRefGoogle Scholar
  119. 119.
    Katzenschlager R, Sampaio C, Costa J, Lees A. Anticholinergics for symptomatic management of Parkinson’s disease. Cochrane Database Syst Rev. 2003;2:CD003735.Google Scholar
  120. 120.
    Zesiewicz TA, Evatt M, Vaughan CP, et al. Non-motor working group of the Parkinson Study Group (PSG) randomized, controlled pilot trial of solifenacin succinate for overactive bladder in Parkinson’s disease. Parkinsonism Relat Disord. 2015;21(5):514–20.PubMedCrossRefGoogle Scholar
  121. 121.
    Palleschi G, Pastore AL, Stocchi F, et al. Correlation between the Overactive Bladder questionnaire (OAB-q) and urodynamic data of Parkinson disease patients affected by neurogenic detrusor overactivity during antimuscarinic treatment. Clin Neuropharmacol. 2006;29(4):220–9.PubMedCrossRefGoogle Scholar
  122. 122.
    Gomes CM, Sammour ZM, Bessa Junior JD, et al. Neurological status predicts response to alpha-blockers in men with voiding dysfunction and Parkinson’s disease. Clinics (Sao Paulo). 2014;69(12):817–22.CrossRefGoogle Scholar
  123. 123.
    Anderson RU, Orenberg EK, Glowe P. OnabotulinumtoxinA office treatment for neurogenic bladder incontinence in Parkinson’s disease. Urology. 2014;83(1):22–7.PubMedCrossRefGoogle Scholar
  124. 124.
    Knüpfer SC, Schneider SA, Averhoff MM, et al. Preserved micturition after intradetrusor onabotulinumtoxinA injection for treatment of neurogenic bladder dysfunction in Parkinson’s disease. BMC Urol. 2016;16(1):55.PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Giannantoni A, Rossi A, Mearini E, et al. Botulinum toxin A for overactive bladder and detrusor muscle overactivity in patients with Parkinson’s disease and multiple system atrophy. J Urol. 2009;182(4):1453–7.PubMedCrossRefGoogle Scholar
  126. 126.
    Jiang YH, Liao CH, Tang DL, Kuo HC. Efficacy and safety of intravesical onabotulinumtoxinA injection on elderly patients with chronic central nervous system lesions and overactive bladder. PLoS One. 2014;9(8):e105989.PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Kulaksizoglu H, Parman Y. Use of botulinim toxin-A for the treatment of overactive bladder symptoms in patients with Parkinsons’s disease. Parkinsonism Relat Disord. 2010;16(8):531–4.PubMedCrossRefGoogle Scholar
  128. 128.
    Kabay S, Canbaz Kabay S, Cetiner M, et al. The clinical and urodynamic results of percutaneous posterior tibial nerve stimulation on neurogenic detrusor overactivity in patients with Parkinson’s disease. Urology. 2016;87:76–81.PubMedCrossRefGoogle Scholar
  129. 129.
    Shimizu N, Matsumoto S, Mori Y, Yoshioka N, Uemura H, Nakano N, Taneda M. Effects of deep brain stimulation on urodynamic findings in patients with Parkinson’s disease. Hinyokika Kiyo. 2007;53(9):609–12.PubMedGoogle Scholar
  130. 130.
    Seif C, Herzog J, van der Horst C, et al. Effect of subthalamic deep brain stimulation on the function of the urinary bladder. Ann Neurol. 2004;55(1):118–20.PubMedCrossRefGoogle Scholar
  131. 131.
    Finazzi-Agrò E, Peppe A, D’Amico A, et al. Effects of subthalamic nucleus stimulation on urodynamic findings in patients with Parkinson’s disease. J Urol. 2003;169(4):1388–91.PubMedCrossRefGoogle Scholar
  132. 132.
    Winge K, Nielsen KK, Stimpel H, Lokkegaard A, Jensen SR, Werdelin L. Lower urinary tract symptoms and bladder control in advanced Parkinson’s disease: effects of deep brain stimulation in the subthalamic nucleus. Mov Disord. 2007;22(2):220–5.PubMedCrossRefGoogle Scholar
  133. 133.
    Mulak A, Bonaz B. Brain-gut-microbiota axis in Parkinson’s disease. World J Gastroenterol. 2015;21(37):10609–20.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Whiteside SA, Razvi H, Dave S, Reid G, Burton JP. The microbiome of the urinary tract—a role beyond infection. Nat Rev Urol. 2015;12(2):81–90.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Petros Georgopoulos
    • 1
  • Konstantinos-Vaios Mytilekas
    • 1
  • Apostolos Apostolidis
    • 1
  1. 1.2nd Department of UrologyAristotle University of ThessalonikiThessalonikiGreece

Personalised recommendations