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Contemporary concepts in the aetiopathogenesis of detrusor underactivity

Nature Reviews Urology volume 11, pages 639–648 (2014)Cite this article

Subjects

Key Points

  • The aetiology and pathophysiology of detrusor underactivity (DUA) are poorly understood—multiple aetiological factors and pathogenic mechanisms are likely to be involved

  • Definite aetiologies include injuries or diseases of the nervous system and diabetes mellitus. Bladder outlet obstruction and normal ageing can, at present, only be considered likely causes of DUA

  • Aetiological factors probably cause DUA by interrupting processes that are essential for the generation of an efficient voiding contraction

  • Pathophysiological mechanisms can be classified as myogenic (affecting detrusor myocytes or their surrounding matrix) or neurogenic (affecting central neural control mechanisms governing the voiding reflex or afferent and/or efferent nerves)

  • To develop new effective treatments, a better understanding of the mechanism underlying the generation of a normal voiding contraction and which abnormalities cause DUA is required

Abstract

Detrusor underactivity (DUA) is a poorly understood, yet common, bladder dysfunction, referred to as underactive bladder, which is observed in both men and women undergoing urodynamic studies. Despite its prevalence, no effective therapeutic approaches exist for DUA. Exactly how the contractile function of the detrusor muscle changes with ageing is unclear. Data from physiological studies in animal and human bladders are contradictory, as are the results of the limited number of clinical studies assessing changes in urodynamic parameters with ageing. The prevalence of DUA in different patient groups suggests that multiple aetiologies are involved in DUA pathogenesis. Traditional concepts focused on either efferent innervation or myogenic dysfunction. By contrast, contemporary views emphasize the importance of the neural control mechanisms, particularly the afferent system, which can fail to potentiate detrusor contraction, leading to premature termination of the voiding reflex. In conclusion, the contemporary understanding of the aetiology and pathophysiology of DUA is limited. Further elucidation of the underlying mechanisms is needed to enable the development of new and effective treatment approaches.

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Figure 1: Major aetiologies, sites of dysfunction and pathogenic mechanisms that result in DUA.
Figure 2: Electron microscopy images of ultrastructural changes in detrusor underactivity.
Figure 3: The role of afferent function in the pathogenesis of the symptoms of DUA.

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References

  1. Abarbanel, J. & Marcus, E. L. Impaired detrusor contractility in community-dwelling elderly presenting with lower urinary tract symptoms. Urology 69, 436–440 (2007).

    PubMed  Google Scholar 

  2. Nitti, V. W., Lefkowitz, G., Ficazzola, M. & Dixon, C. M. Lower urinary tract symptoms in young men: videourodynamic findings and correlation with noninvasive measures. J. Urol. 168, 135–138 (2002).

    PubMed  Google Scholar 

  3. Resnick, N. M., Brandeis, G. H., Baumann, M. M., DuBeau, C. E. & Yalla, S. V. Misdiagnosis of urinary incontinence in nursing home women: prevalence and a proposed solution. Neurourol. Urodyn. 15, 599–613; discussion 613–618 (1996).

    CAS  PubMed  Google Scholar 

  4. Abrams, P. et al. The standardisation of terminology of lower urinary tract function: report from the Standardisation Sub-committee of the International Continence Society. Neurourol. Urodyn. 21, 167–178 (2002).

    PubMed  Google Scholar 

  5. Chancellor, M. B. & Kaufman, J. Case for pharmacotherapy development for underactive bladder. Urology 72, 966–967 (2008).

    PubMed  Google Scholar 

  6. Chapple, C. Overactive bladder and underactive bladder: a symptom syndrome or urodynamic diagnosis? Neurourol. Urodyn. 32, 305–307 (2013).

    PubMed  Google Scholar 

  7. Miyazato, M., Yoshimura, N. & Chancellor, M. B. The other bladder syndrome: underactive bladder. Rev. Urol. 15, 11–22 (2013).

    PubMed  PubMed Central  Google Scholar 

  8. Osman, N. I. et al. Detrusor underactivity and the underactive bladder: a new clinical entity? A review of current terminology, definitions, epidemiology, aetiology, and diagnosis. Eur. Urol. 65, 389–398 (2014).

    PubMed  Google Scholar 

  9. van Koeveringe, G. A., Vahabi, B., Andersson, K. E., Kirschner-Herrmans, R. & Oelke, M. Detrusor underactivity: a plea for new approaches to a common bladder dysfunction. Neurourol. Urodyn. 30, 723–728 (2011).

    CAS  PubMed  Google Scholar 

  10. Zhao, W. et al. Impaired bladder function in aging male rats. J. Urol. 184, 378–385 (2010).

    PubMed  PubMed Central  Google Scholar 

  11. Munro, D. D. & Wendt, I. R. Contractile and metabolic properties of longitudinal smooth muscle from rat urinary bladder and the effects of aging. J. Urol. 150, 529–536 (1993).

    CAS  PubMed  Google Scholar 

  12. Wilfehrt, H. M., Carson, C. C. 3rd & Marson, L. Bladder function in female rats: effects of aging and pregnancy. Physiol. Behav. 68, 195–203 (1999).

    CAS  PubMed  Google Scholar 

  13. Longhurst, P. A., Eika, B., Leggett, R. E. & Levin, R. M. Comparison of urinary bladder function in 6 and 24 month male and female rats. J. Urol. 148, 1615–1620 (1992).

    CAS  PubMed  Google Scholar 

  14. Pagala, M. K., Tetsoti, L., Nagpal, D. & Wise, G. J. Aging effects on contractility of longitudinal and circular detrusor and trigone of rat bladder. J. Urol. 166, 721–727 (2001).

    CAS  PubMed  Google Scholar 

  15. Gomez-Pinilla, P. J., Pozo, M. J. & Camello, P. J. Aging differentially modifies agonist-evoked mouse detrusor contraction and calcium signals. Age (Dordr.) 33, 81–88 (2011).

    CAS  Google Scholar 

  16. Ordway, G. A., Esbenshade, T. A., Kolta, M. G., Gerald, M. C. & Wallace, L. J. Effect of age on cholinergic muscarinic responsiveness and receptors in the rat urinary bladder. J. Urol. 136, 492–496 (1986).

    CAS  PubMed  Google Scholar 

  17. Lluel, P. et al. Functional and morphological modifications of the urinary bladder in aging female rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278, R964–R972 (2000).

    CAS  PubMed  Google Scholar 

  18. Lluel, P. et al. Increased adrenergic contractility and decreased mRNA expression of NOS III in aging rat urinary bladders. Fundam. Clin. Pharmacol. 17, 633–641 (2003).

    CAS  PubMed  Google Scholar 

  19. Yu, H. I., Wein, A. J. & Levin, R. M. Contractile responses and calcium mobilization induced by muscarinic agonists in the rat urinary bladder: effects of age. Gen. Pharmacol. 28, 623–628 (1997).

    CAS  PubMed  Google Scholar 

  20. Saito, M., Kondo, A., Gotoh, M., Kato, K. & Levin, R. M. Age-related changes in the response of the rat urinary bladder to neurotransmitters. Neurourol. Urodyn. 12, 191–200 (1993).

    CAS  PubMed  Google Scholar 

  21. Saito, M., Gotoh, M., Kato, K. & Kondo, A. Influence of aging on the rat urinary bladder function. Urol. Int. 47 (Suppl. 1), 39–42 (1991).

    PubMed  Google Scholar 

  22. Saito, M., Kondo, A., Gotoh, M. & Kato, K. Age-related changes in the rat detrusor muscle: the contractile response to inorganic ions. J. Urol. 146, 891–894 (1991).

    CAS  PubMed  Google Scholar 

  23. Chun, A. L., Wallace, L. J., Gerald, M. C., Wein, A. J. & Levin, R. M. Effects of age on urinary bladder function in the male rat. J. Urol. 141, 170–173 (1989).

    CAS  PubMed  Google Scholar 

  24. Lieu, P. K., Sa'adu, A., Orugun, E. O. & Malone-Lee, J. G. The influence of age on isometric and isotonic rat detrusor contractions. J. Gerontol. A Biol. Sci. Med. Sci. 52, M94–M96 (1997).

    CAS  PubMed  Google Scholar 

  25. Kageyama, S. et al. Effect of age on the responses of rat bladder detrusor strips to adenosine triphosphate. BJU Int. 85, 899–904 (2000).

    CAS  PubMed  Google Scholar 

  26. Lin, A. T., Yang, C. H. & Chang, L. S. Impact of aging on rat urinary bladder fatigue. J. Urol. 157, 1990–1994 (1997).

    CAS  PubMed  Google Scholar 

  27. Fry, C. H., Bayliss, M., Young, J. S. & Hussain, M. Influence of age and bladder dysfunction on the contractile properties of isolated human detrusor smooth muscle. BJU Int. 108, E91–E96 (2011).

    PubMed  Google Scholar 

  28. Yoshida, M. et al. Age-related changes in cholinergic and purinergic neurotransmission in human isolated bladder smooth muscles. Exp. Gerontol. 36, 99–109 (2001).

    CAS  PubMed  Google Scholar 

  29. Mark, S. D. et al. Detrusor contractility: Age related correlation with urinary flow rate in asymptomatic males [abstract 13]. Neurourol. Urodyn. 11, 315–317 (1992).

    Google Scholar 

  30. Lepor, H., Sunaryadi, I., Hartanto, V. & Shapiro, E. Quantitative morphometry of the adult human bladder. J. Urol. 148, 414–417 (1992).

    CAS  PubMed  Google Scholar 

  31. Holm, N. R., Horn, T. & Hald, T. Detrusor in ageing and obstruction. Scand. J. Urol. Nephrol. 29, 45–49 (1995).

    CAS  PubMed  Google Scholar 

  32. Gosling, J. A. Modification of bladder structure in response to outflow obstruction and ageing. Eur. Urol. 32 (Suppl. 1), 9–14 (1997).

    PubMed  Google Scholar 

  33. Elbadawi, A., Hailemariam, S., Yalla, S. V. & Resnick, N. M. Structural basis of geriatric voiding dysfunction. VI. Validation and update of diagnostic criteria in 71 detrusor biopsies. J. Urol. 157, 1802–1813 (1997).

    CAS  PubMed  Google Scholar 

  34. Andersson, K. E. & Arner, A. Urinary bladder contraction and relaxation: physiology and pathophysiology. Physiol. Rev. 84, 935–986 (2004).

    CAS  PubMed  Google Scholar 

  35. Lowalekar, S. K., Cristofaro, V., Radisavljevic, Z. M., Yalla, S. V. & Sullivan, M. P. Loss of bladder smooth muscle caveolae in the aging bladder. Neurourol. Urodyn. 31, 586–592 (2012).

    PubMed  Google Scholar 

  36. Cristofaro, V., Peters, C. A., Yalla, S. V. & Sullivan, M. P. Smooth muscle caveolae differentially regulate specific agonist induced bladder contractions. Neurourol. Urodyn. 26, 71–80 (2007).

    CAS  PubMed  Google Scholar 

  37. Sadegh, M. K. et al. Biomechanical properties and innervation of the female caveolin-1-deficient detrusor. Br. J. Pharmacol. 162, 1156–1170 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Lai, H. H. et al. Loss of caveolin-1 expression is associated with disruption of muscarinic cholinergic activities in the urinary bladder. Neurochem. Int. 45, 1185–1193 (2004).

    CAS  PubMed  Google Scholar 

  39. Pfisterer, M. H., Griffiths, D. J., Schaefer, W. & Resnick, N. M. The effect of age on lower urinary tract function: a study in women. J. Am. Geriatr. Soc. 54, 405–412 (2006).

    PubMed  Google Scholar 

  40. Schäfer, W. Analysis of bladder-outlet function with the linearized passive urethral resistance relation, linPURR, and a disease-specific approach for grading obstruction: from complex to simple. World J. Urol. 13, 47–58 (1995).

    PubMed  Google Scholar 

  41. Smith, A. L. et al. Urodynamic trends in the female aging population: detrusor overactivity with impaired contractility, two conditions or one? 39th Annual Meeting of the International Continence Society (San Francisco, CA) [online], (2009).

    Google Scholar 

  42. Valentini, F. A., Robain, G. & Marti, B. G. Urodynamics in women from menopause to oldest age: what motive? What diagnosis? Int. Braz. J. Urol. 37, 100–107 (2011).

    PubMed  Google Scholar 

  43. Karram, M. M., Partoll, L., Bilotta, V. & Angel, O. Factors affecting detrusor contraction strength during voiding in women. Obstet. Gynecol. 90, 723–726 (1997).

    CAS  PubMed  Google Scholar 

  44. Madersbacher, S. et al. The aging lower urinary tract: a comparative urodynamic study of men and women. Urology 51, 206–212 (1998).

    CAS  PubMed  Google Scholar 

  45. Madersbacher, S. et al. Age related urodynamic changes in patients with benign prostatic hyperplasia. J. Urol. 156, 1662–1667 (1996).

    CAS  PubMed  Google Scholar 

  46. Levin, R. M. et al. Studies on experimental bladder outlet obstruction in the cat: long-term functional effects. J. Urol. 148, 939–943 (1992).

    CAS  PubMed  Google Scholar 

  47. Saito, M., Yokoi, K., Ohmura, M. & Kondo, A. Effects of partial outflow obstruction on bladder contractility and blood flow to the detrusor: comparison between mild and severe obstruction. Urol. Int. 59, 226–230 (1997).

    CAS  PubMed  Google Scholar 

  48. Levin, R. M., Haugaard, N., Levin, S. S., Buttyan, R., Chen, M.-W., Monson, F. C., Wein, A. J. in Muscle, matrix, and bladder function (ed. Zderic, S. A.) 7–19 (Plenum Press, 1995).

    Google Scholar 

  49. Greenland, J. E. & Brading, A. F. Urinary bladder blood flow changes during the micturition cycle in a conscious pig model. J. Urol. 156, 1858–1861 (1996).

    CAS  PubMed  Google Scholar 

  50. Erdem, E., Leggett, R., Dicks, B., Kogan, B. A. & Levin, R. M. Effect of bladder ischaemia/reperfusion on superoxide dismutase activity and contraction. BJU Int. 96, 169–174 (2005).

    CAS  PubMed  Google Scholar 

  51. Zhao, Y., Levin, S. S., Wein, A. J. & Levin, R. M. Correlation of ischemia/reperfusion or partial outlet obstruction-induced spectrin proteolysis by calpain with contractile dysfunction in rabbit bladder. Urology 49, 293–300 (1997).

    CAS  PubMed  Google Scholar 

  52. Bauer, V. et al. Reactive oxygen species induced smooth muscle responses in the intestine, vessels and airways and the effect of antioxidants. Life Sci. 65, 1909–1917 (1999).

    CAS  PubMed  Google Scholar 

  53. Schröder, A. et al. Effect of chronic bladder outlet obstruction on blood flow of the rabbit bladder. J. Urol. 165, 640–646 (2001).

    PubMed  Google Scholar 

  54. Thomas, A. W., Cannon, A., Bartlett, E., Ellis-Jones, J. & Abrams, P. The natural history of lower urinary tract dysfunction in men: minimum 10-year urodynamic follow-up of untreated bladder outlet obstruction. BJU Int. 96, 1301–1306 (2005).

    PubMed  Google Scholar 

  55. George, N. J., O'Reilly, P. H., Barnard, R. J. & Blacklock, N. J. High pressure chronic retention. Br. Med. J. (Clin. Res. Ed.) 286, 1780–1783 (1983).

    CAS  Google Scholar 

  56. Djavan, B., Madersbacher, S., Klingler, C. & Marberger, M. Urodynamic assessment of patients with acute urinary retention: is treatment failure after prostatectomy predictable? J. Urol. 158, 1829–1833 (1997).

    CAS  PubMed  Google Scholar 

  57. Lifford, K. L., Curhan, G. C., Hu, F. B., Barbieri, R. L. & Grodstein, F. Type 2 diabetes mellitus and risk of developing urinary incontinence. J. Am. Geriatr. Soc. 53, 1851–1857 (2005).

    PubMed  Google Scholar 

  58. Lee, W. C. et al. Effects of diabetes on female voiding behavior. J. Urol. 172, 989–992 (2004).

    PubMed  Google Scholar 

  59. Hill, S. R., Fayyad, A. M. & Jones, G. R. Diabetes mellitus and female lower urinary tract symptoms: a review. Neurourol. Urodyn. 27, 362–367 (2008).

    PubMed  Google Scholar 

  60. Fedele, D. Therapy Insight: sexual and bladder dysfunction associated with diabetes mellitus. Nat. Clin. Pract. Urol. 2, 282–290; quiz 309 (2005).

    PubMed  Google Scholar 

  61. Sasaki, K. et al. Diabetic cystopathy correlates with a long-term decrease in nerve growth factor levels in the bladder and lumbosacral dorsal root ganglia. J. Urol. 168, 1259–1264 (2002).

    PubMed  Google Scholar 

  62. Hellweg, R., Raivich, G., Hartung, H. D., Hock, C. & Kreutzberg, G. W. Axonal transport of endogenous nerve growth factor (NGF) and NGF receptor in experimental diabetic neuropathy. Exp. Neurol. 130, 24–30 (1994).

    CAS  PubMed  Google Scholar 

  63. Longhurst, P. A. & Belis, J. A. Abnormalities of rat bladder contractility in streptozotocin-induced diabetes mellitus. J. Pharmacol. Exp. Ther. 238, 773–777 (1986).

    CAS  PubMed  Google Scholar 

  64. Waring, J. V. & Wendt, I. R. Effects of streptozotocin-induced diabetes mellitus on intracellular calcium and contraction of longitudinal smooth muscle from rat urinary bladder. J. Urol. 163, 323–330 (2000).

    CAS  PubMed  Google Scholar 

  65. Daneshgari, F., Liu, G., Birder, L., Hanna-Mitchell, A. T. & Chacko, S. Diabetic bladder dysfunction: current translational knowledge. J. Urol. 182 (Suppl. 6), S18–S26 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Burney, T. L., Senapati, M., Desai, S., Choudhary, S. T. & Badlani, G. H. Acute cerebrovascular accident and lower urinary tract dysfunction: a prospective correlation of the site of brain injury with urodynamic findings. J. Urol. 156, 1748–1750 (1996).

    CAS  PubMed  Google Scholar 

  67. Araki, I., Kitahara, M., Oida, T. & Kuno, S. Voiding dysfunction and Parkinson's disease: urodynamic abnormalities and urinary symptoms. J. Urol. 164, 1640–1643 (2000).

    CAS  PubMed  Google Scholar 

  68. Stocchi, F. et al. Urodynamic and neurophysiological evaluation in Parkinson's disease and multiple system atrophy. J. Neurol. Neurosurg. Psychiatry 62, 507–511 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Yamamoto, T. et al. Time-dependent changes and gender differences in urinary dysfunction in patients with multiple system atrophy. Neurourol. Urodyn. 33, 516–523 (2014).

    PubMed  Google Scholar 

  70. Bloch, F. et al. Urodynamic analysis in multiple system atrophy: characterisation of detrusor-sphincter dyssynergia. J. Neurol. 257, 1986–1991 (2010).

    PubMed  Google Scholar 

  71. Litwiller, S. E., Frohman, E. M. & Zimmern, P. E. Multiple sclerosis and the urologist. J. Urol. 161, 743–757 (1999).

    CAS  PubMed  Google Scholar 

  72. Plotti, F. et al. Update on urodynamic bladder dysfunctions after radical hysterectomy for cervical cancer. Crit. Rev. Oncol. Hematol. 80, 323–329 (2011).

    PubMed  Google Scholar 

  73. Zanolla, R., Campo, B., Ordesi, G. & Martino, G. Bladder urethral dysfunction after abdominoperineal resection of the rectum for ano-rectal cancer. Tumori 70, 555–559 (1984).

    CAS  PubMed  Google Scholar 

  74. Maurer, C. A. et al. Total mesorectal excision preserves male genital function compared with conventional rectal cancer surgery. Br. J. Surg. 88, 1501–1505 (2001).

    CAS  PubMed  Google Scholar 

  75. Elbadawi, A., Atta, M. A., Hanno, A. G.-E. Intrinsic neuromuscular defects in the neurogenic bladder: VIII. Effects of unilateral pelvic and pelvic plexus neurectomy on ultrastructure of the feline bladder base. Neurourol. Urodyn. 7, 77–92 (1988).

    Google Scholar 

  76. Brierly, R. D., Hindley, R. G., McLarty, E., Harding, D. M. & Thomas, P. J. A prospective controlled quantitative study of ultrastructural changes in the underactive detrusor. J. Urol. 169, 1374–1378 (2003).

    CAS  PubMed  Google Scholar 

  77. Elbadawi, A., Yalla, S. V. & Resnick, N. M. Structural basis of geriatric voiding dysfunction. II. Aging detrusor: normal versus impaired contractility. J. Urol. 150, 1657–1667 (1993).

    CAS  PubMed  Google Scholar 

  78. Elbadawi, A., Yalla, S. V. & Resnick, N. M. Structural basis of geriatric voiding dysfunction. III. Detrusor overactivity. J. Urol. 150, 1668–1680 (1993).

    CAS  PubMed  Google Scholar 

  79. Elbadawi, A., Yalla, S. V. & Resnick, N. M. Structural basis of geriatric voiding dysfunction. IV. Bladder outlet obstruction. J. Urol. 150, 1681–1695 (1993).

    CAS  PubMed  Google Scholar 

  80. Hindley, R. G., Brierly, R. D., McLarty, E., Harding, D. M. & Thomas, P. J. A qualitative ultrastructural study of the hypocontractile detrusor. J. Urol. 168, 126–131 (2002).

    CAS  PubMed  Google Scholar 

  81. Sullivan, M. P. & Yalla, S. V. Detrusor contractility and compliance characteristics in adult male patients with obstructive and nonobstructive voiding dysfunction. J. Urol. 155, 1995–2000 (1996).

    CAS  PubMed  Google Scholar 

  82. Schroder, A., Uvelius, B., Capello, S. A. & Longhurst, P. A. Regional differences in bladder enlargement and in vitro contractility after outlet obstruction in the rabbit. J. Urol. 168, 1240–1246 (2002).

    PubMed  Google Scholar 

  83. de Groat, W. C. et al. Developmental and injury induced plasticity in the micturition reflex pathway. Behav. Brain Res. 92, 127–140 (1998).

    CAS  PubMed  Google Scholar 

  84. Sugaya, K. et al. Ascending and descending brainstem neuronal activity during cystometry in decerebrate cats. Neurourol. Urodyn. 22, 343–350 (2003).

    PubMed  Google Scholar 

  85. Sugaya, K., Nishijima, S., Miyazato, M. & Ogawa, Y. Central nervous control of micturition and urine storage. J. Smooth Muscle Res. 41, 117–132 (2005).

    PubMed  Google Scholar 

  86. Blok, B. F., Willemsen, A. T. & Holstege, G. A PET study on brain control of micturition in humans. Brain 120, 111–121 (1997).

    PubMed  Google Scholar 

  87. Kim, Y. H. et al. The correlation of urodynamic findings with cranial magnetic resonance imaging findings in multiple sclerosis. J. Urol. 159, 972–976 (1998).

    CAS  PubMed  Google Scholar 

  88. Gilpin, S. A., Gilpin, C. J., Dixon, J. S., Gosling, J. A. & Kirby, R. S. The effect of age on the autonomic innervation of the urinary bladder. Br. J. Urol. 58, 378–381 (1986).

    CAS  PubMed  Google Scholar 

  89. Feber, J. L., van Asselt, E. & van Mastrigt, R. Neurophysiological modeling of voiding in rats: urethral nerve response to urethral pressure and flow. Am. J. Physiol. 274, R1473–R1481 (1998).

    CAS  PubMed  Google Scholar 

  90. Bump, R. C. The urethrodetrusor facilitative reflex in women: results of urethral perfusion studies. Am. J. Obstet. Gynecol. 182, 794–802; discussion 802–804 (2000).

    CAS  PubMed  Google Scholar 

  91. Pfisterer, M. H., Griffiths, D. J., Rosenberg, L., Schaefer, W. & Resnick, N. M. Parameters of bladder function in pre-, peri-, and postmenopausal continent women without detrusor overactivity. Neurourol. Urodyn. 26, 356–361 (2007).

    PubMed  Google Scholar 

  92. Griffiths, D., Tadic, S. D., Schaefer, W. & Resnick, N. M. Cerebral control of the bladder in normal and urge-incontinent women. Neuroimage 37, 1–7 (2007).

    PubMed  PubMed Central  Google Scholar 

  93. Smith, P. P. Aging and the underactive detrusor: a failure of activity or activation? Neurourol. Urodyn. 29, 408–412 (2010).

    PubMed  Google Scholar 

  94. Resnick, N. M. & Yalla, S. V. Detrusor hyperactivity with impaired contractile function. An unrecognized but common cause of incontinence in elderly patients. JAMA 257, 3076–3081 (1987).

    CAS  PubMed  Google Scholar 

  95. Fowler, C. J. et al. Abnormal electromyographic activity of the urethral sphincter, voiding dysfunction, and polycystic ovaries: a new syndrome? BMJ 297, 1436–1438 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Osman, N. I. & Chapple, C. R. Fowler's syndrome—a cause of unexplained urinary retention in young women? Nat. Rev. Urol. 11, 87–98 (2014).

    PubMed  Google Scholar 

  97. Panicker, J. N., DasGupta, R., Elneil, S. & Fowler, C. J. in Pelvic organ dysfunction in neurological disease: Clinical management and rehabilitation (eds Fowler, C. J., Panicker, J. N. & Emmanuel, A.) 293–306 (Cambridge University Press, 2010).

    Google Scholar 

  98. de Groat, W. C. et al. Neural control of the urethra. Scand. J. Urol. Nephrol. Suppl. 35, 35–43; discussion 106–125 (2001).

    Google Scholar 

  99. Fowler, C. J. Neurological disorders of micturition and their treatment. Brain 122, 1213–1231 (1999).

    PubMed  Google Scholar 

  100. DasGupta, R. & Fowler, C. J. The management of female voiding dysfunction: Fowler's syndrome—a contemporary update. Curr. Opin. Urol. 13, 293–299 (2003).

    PubMed  Google Scholar 

  101. Haylen, B. T. et al. An International Urogynecological Association (IUGA)/International Continence Society (ICS) joint report on the terminology for female pelvic floor dysfunction. Neurourol. Urodyn. 29, 4–20 (2010).

    PubMed  Google Scholar 

  102. Carlson, K. V., Rome, S. & Nitti, V. W. Dysfunctional voiding in women. J. Urol. 165, 143–147; discussion 147–148 (2001).

    CAS  PubMed  Google Scholar 

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  1. Department of Urology, Royal Hallamshire Hospital, Glossop Road, Sheffield, S10 2JF, South Yorkshire, UK

    Nadir I. Osman & Christopher R. Chapple

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C.R.C. is a consultant and researcher for Allergan, Astellas, Pfizer and Recordati. N.I.O. declares no competing interests.

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Osman, N., Chapple, C. Contemporary concepts in the aetiopathogenesis of detrusor underactivity. Nat Rev Urol 11, 639–648 (2014). https://doi.org/10.1038/nrurol.2014.286

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