Investig Clin Urol.  2017 Dec;58(Suppl 2):S82-S89. 10.4111/icu.2017.58.S2.S82.

Pathophysiology of the underactive bladder

Affiliations
  • 1Department of Continence Medicine, The University of Tokyo Graduate School of Medicine, Tokyo, Japan. yigawa-jua@umin.ac.jp

Abstract

Underactive bladder (UAB), which has been described as a symptom complex suggestive of detrusor underactivity, is usually characterized by prolonged urination time with or without a sensation of incomplete bladder emptying, usually with hesitancy, reduced sensation on filling, and slow stream often with storage symptoms. Several causes such as aging, bladder outlet obstruction, diabetes mellitus, neurologic disorders, and nervous injury to the spinal cord, cauda equine, and peripheral pelvic nerve have been assumed to be responsible for the development of UAB. Several contributing factors have been suggested in the pathophysiology of UAB, including myogenic failure, efferent and/or afferent dysfunctions, and central nervous system dysfunction. In this review article, we have described relationships between individual contributing factors and the pathophysiology of UAB based on previous reports. However, many pathophysiological uncertainties still remain, which require more investigations using appropriate animal models.

Keyword

Aging; Denervation; Diabetic neuropathies; Ischemia; Urinary bladder diseases

MeSH Terms

Aging
Central Nervous System
Denervation
Diabetes Mellitus
Diabetic Neuropathies
Hypesthesia
Ischemia
Models, Animal
Nervous System Diseases
Rivers
Sensation
Spinal Cord
Urinary Bladder Diseases
Urinary Bladder Neck Obstruction
Urinary Bladder*
Urination

Figure

  • Fig. 1 Contributing factors and mechanisms involved in underactive bladder.


Reference

1. Chapple CR, Osman NI, Birder L, van Koeveringe GA, Oelke M, Nitti VW, et al. The underactive bladder: a new clinical concept? Eur Urol. 2015; 68:351–353. PMID: 25770481.
Article
2. Andersson KE. Bladder underactivity. Eur Urol. 2014; 65:399–401. PMID: 24268505.
Article
3. Abrams P, Cardozo L, Fall M, Griffiths D, Rosier P, Ulmsten U, et al. The standardisation of terminology of lower urinary tract function: report from the Standardisation Sub-committee of the International Continence Society. Neurourol Urodyn. 2002; 21:167–178. PMID: 11857671.
Article
4. Cucchi A, Quaglini S, Rovereto B. Proposal for a urodynamic redefinition of detrusor underactivity. J Urol. 2009; 181:225–229. PMID: 19013594.
Article
5. Fowler CJ, Griffiths D, de Groat WC. The neural control of micturition. Nat Rev Neurosci. 2008; 9:453–466. PMID: 18490916.
Article
6. de Groat WC. Integrative control of the lower urinary tract: preclinical perspective. Br J Pharmacol. 2006; 147(Suppl 2):S25–S40. PMID: 16465182.
Article
7. Miyazato M, Yoshimura N, Chancellor MB. The other bladder syndrome: underactive bladder. Rev Urol. 2013; 15:11–22. PMID: 23671401.
8. Aggarwal H, Zimmern PE. Underactive bladder: current urology reports. Curr Urol Rep. 2016; 17:17. PMID: 26874529.
9. Smith PP. Aging and the underactive detrusor: a failure of activity or activation? Neurourol Urodyn. 2010; 29:408–412. PMID: 19760756.
Article
10. Resnick NM, Yalla SV. Detrusor hyperactivity with impaired contractile function. An unrecognized but common cause of incontinence in elderly patients. JAMA. 1987; 257:3076–3081. PMID: 3586227.
Article
11. Jiang YH, Lee CL, Kuo HC. Urothelial dysfunction, suburothelial inflammation and altered sensory protein expression in men with bladder outlet obstruction and various bladder dysfunctions: correlation with urodynamics. J Urol. 2016; 196:831–837. PMID: 26930253.
Article
12. Frimodt-Moller C. Diabetic cystopathy: a review of the urodynamic and clinical features of neurogenic bladder dysfunction in diabetes mellitus. Dan Med Bull. 1978; 25:49–60. PMID: 344005.
13. Sasaki K, Yoshimura N, Chancellor MB. Implications of diabetes mellitus in urology. Urol Clin North Am. 2003; 30:1–12. PMID: 12580554.
Article
14. Kadow BT, Tyagi P, Chermansky CJ. Neurogenic causes of detrusor underactivity. Curr Bladder Dysfunct Rep. 2015; 10:325–331. PMID: 26715948.
Article
15. Chung DE, Dillon B, Kurta J, Maschino A, Cronin A, Sandhu JS. Detrusor underactivity is prevalent after radical prostatectomy: a urodynamic study including risk factors. Can Urol Assoc J. 2013; 7:E33–E37. PMID: 22277630.
Article
16. Brooks RA, Wright JD, Powell MA, Rader JS, Gao F, Mutch DG, et al. Long-term assessment of bladder and bowel dysfunction after radical hysterectomy. Gynecol Oncol. 2009; 114:75–79. PMID: 19410279.
Article
17. Gosling J. The structure of the bladder and urethra in relation to function. Urol Clin North Am. 1979; 6:31–38. PMID: 432999.
Article
18. Elbadawi A, Hailemariam S, Yalla SV, Resnick NM. Structural basis of geriatric voiding dysfunction. VII. Prospective ultrastructural/urodynamic evaluation of its natural evolution. J Urol. 1997; 157:1814–1822. PMID: 9112530.
Article
19. Resnick NM, Yalla SV, Laurino E. The pathophysiology of urinary incontinence among institutionalized elderly persons. N Engl J Med. 1989; 320:1–7. PMID: 2909873.
Article
20. Taylor JA 3rd, Kuchel GA. Detrusor underactivity: clinical features and pathogenesis of an underdiagnosed geriatric condition. J Am Geriatr Soc. 2006; 54:1920–1932. PMID: 17198500.
Article
21. Gilpin SA, Gilpin CJ, Dixon JS, Gosling JA, Kirby RS. The effect of age on the autonomic innervation of the urinary bladder. Br J Urol. 1986; 58:378–381. PMID: 3756405.
Article
22. Lepor H, Sunaryadi I, Hartanto V, Shapiro E. Quantitative morphometry of the adult human bladder. J Urol. 1992; 148(2 Pt 1):414–417. PMID: 1378909.
Article
23. Elbadawi A, Yalla SV, Resnick NM. Structural basis of geriatric voiding dysfunction. II. Aging detrusor: normal versus impaired contractility. J Urol. 1993; 150(5 Pt 2):1657–1667. PMID: 8411454.
Article
24. Mansfield KJ, Liu L, Mitchelson FJ, Moore KH, Millard RJ, Burcher E. Muscarinic receptor subtypes in human bladder detrusor and mucosa, studied by radioligand binding and quantitative competitive RT-PCR: changes in ageing. Br J Pharmacol. 2005; 144:1089–1099. PMID: 15723094.
Article
25. Ito H, Aizawa N, Fujita Y, Suzuki M, Fukuhara H, Homma Y, et al. Long-term caloric restriction in rats may prevent age related impairment of in vitro bladder function. J Urol. 2015; 193:2123–2130. PMID: 25451828.
26. Ito H, Kamei J, Aizawa N, Fujita Y, Suzuki M, Fukuhara H, et al. Preventive effects of long-term caloric restriction on aging related in vivo bladder dysfunction and molecular biological changes in the bladder and dorsal root ganglia in rats. J Urol. 2016; 196:1575–1583. PMID: 27259654.
27. Brading AF, Turner WH. The unstable bladder: towards a common mechanism. Br J Urol. 1994; 73:3–8. PMID: 8298896.
Article
28. Mills IW, Greenland JE, McMurray G, McCoy R, Ho KM, Noble JG, et al. Studies of the pathophysiology of idiopathic detrusor instability: the physiological properties of the detrusor smooth muscle and its pattern of innervation. J Urol. 2000; 163:646–651. PMID: 10647702.
Article
29. Sibley GN. The physiological response of the detrusor muscle to experimental bladder outflow obstruction in the pig. Br J Urol. 1987; 60:332–336. PMID: 3690205.
Article
30. Drake MJ, Hedlund P, Mills IW, McCoy R, McMurray G, Gardner BP, et al. Structural and functional denervation of human detrusor after spinal cord injury. Lab Invest. 2000; 80:1491–1499. PMID: 11045565.
Article
31. Drake MJ, Gardner BP, Brading AF. Innervation of the detrusor muscle bundle in neurogenic detrusor overactivity. BJU Int. 2003; 91:702–710. PMID: 12699489.
Article
32. Daneshgari F, Liu G, Birder L, Hanna-Mitchell AT, Chacko S. Diabetic bladder dysfunction: current translational knowledge. J Urol. 2009; 182(6 Suppl):S18–S26. PMID: 19846137.
Article
33. Christ GJ, Hsieh Y, Zhao W, Schenk G, Venkateswarlu K, Wang HZ, et al. Effects of streptozotocin-induced diabetes on bladder and erectile (dys)function in the same rat in vivo. BJU Int. 2006; 97:1076–1082. PMID: 16643495.
Article
34. Schroder A, Chichester P, Kogan BA, Longhurst PA, Lieb J, Das AK, et al. Effect of chronic bladder outlet obstruction on blood flow of the rabbit bladder. J Urol. 2001; 165:640–646. PMID: 11176451.
35. Levin RM, Haugaard N, O'Connor L, Buttyan R, Das A, Dixon JS, et al. Obstructive response of human bladder to BPH vs. rabbit bladder response to partial outlet obstruction: a direct comparison. Neurourol Urodyn. 2000; 19:609–629. PMID: 11002303.
Article
36. Levin RM, Schuler C, Leggett RE, Callaghan C, Maknuru S. Partial outlet obstruction in rabbits: duration versus severity. Int J Urol. 2013; 20:107–114. PMID: 23050656.
Article
37. Azadzoi KM, Chen BG, Radisavljevic ZM, Siroky MB. Molecular reactions and ultrastructural damage in the chronically ischemic bladder. J Urol. 2011; 186:2115–2122. PMID: 21944111.
Article
38. Nomiya M, Yamaguchi O, Akaihata H, Hata J, Sawada N, Kojima Y, et al. Progressive vascular damage may lead to bladder underactivity in rats. J Urol. 2014; 191:1462–1469. PMID: 24184364.
Article
39. Zhao Z, Azad R, Yang JH, Siroky MB, Azadzoi KM. Progressive changes in detrusor function and micturition patterns with chroinc bladder ischemia. Investig Clin Urol. 2016; 57:249–259.
Article
40. Malone L, Schuler C, Leggett RE, Levin RM. The effect of in vitro oxidative stress on the female rabbit bladder contractile response and antioxidant levels. ISRN Urol. 2013; 2013:639685. PMID: 23819065.
Article
41. Drake MJ, Harvey IJ, Gillespie JI. Autonomous activity in the isolated guinea pig bladder. Exp Physiol. 2003; 88:19–30. PMID: 12525852.
Article
42. Drake MJ, Harvey IJ, Gillespie JI, Van Duyl WA. Localized contractions in the normal human bladder and in urinary urgency. BJU Int. 2005; 95:1002–1005. PMID: 15839921.
Article
43. Drake MJ, Hedlund P, Harvey IJ, Pandita RK, Andersson KE, Gillespie JI. Partial outlet obstruction enhances modular autonomous activity in the isolated rat bladder. J Urol. 2003; 170:276–279. PMID: 12796704.
Article
44. Aizawa N, Homma Y, Igawa Y. Effects of mirabegron, a novel beta3-adrenoceptor agonist, on primary bladder afferent activity and bladder microcontractions in rats compared with the effects of oxybutynin. Eur Urol. 2012; 62:1165–1173. PMID: 22981677.
45. Drake MJ, Kanai A, Bijos DA, Ikeda Y, Zabbarova I, Vahabi B, et al. The potential role of unregulated autonomous bladder micromotions in urinary storage and voiding dysfunction; overactive bladder and detrusor underactivity. BJU Int. 2017; 119:22–29. PMID: 27444952.
Article
46. Lagou M, Gillespie J, Kirkwood T, Harvey I, Drake MJ. Muscarinic stimulation of the mouse isolated whole bladder: physiological responses in young and ageing mice. Auton Autacoid Pharmacol. 2006; 26:253–260. PMID: 16879490.
Article
47. de Groat WC, Yoshimura N. Afferent nerve regulation of bladder function in health and disease. Handb Exp Pharmacol. 2009; (194):91–138. PMID: 19655106.
Article
48. Morrison J. The activation of bladder wall afferent nerves. Exp Physiol. 1999; 84:131–136. PMID: 10081713.
Article
49. Iggo A. Tension receptors in the stomach and the urinary bladder. J Physiol. 1955; 128:593–607. PMID: 13243351.
Article
50. Kanai A, Andersson KE. Bladder afferent signaling: recent findings. J Urol. 2010; 183:1288–1295. PMID: 20171668.
Article
51. Ferguson DR. Urothelial function. BJU Int. 1999; 84:235–242. PMID: 10468713.
Article
52. de Groat WC. The urothelium in overactive bladder: passive bystander or active participant? Urology. 2004; 64(6 Suppl 1):7–11. PMID: 15621221.
Article
53. Birder LA, Apodaca G, De Groat WC, Kanai AJ. Adrenergic- and capsaicin-evoked nitric oxide release from urothelium and afferent nerves in urinary bladder. Am J Physiol. 1998; 275(2 Pt 2):F226–F229. PMID: 9691011.
54. Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, et al. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci. 2002; 5:856–860. PMID: 12161756.
Article
55. Birder LA, Nealen ML, Kiss S, de Groat WC, Caterina MJ, Wang E, et al. Beta-adrenoceptor agonists stimulate endothelial nitric oxide synthase in rat urinary bladder urothelial cells. J Neurosci. 2002; 22:8063–8070. PMID: 12223560.
56. Ferguson DR, Kennedy I, Burton TJ. ATP is released from rabbit urinary bladder epithelial cells by hydrostatic pressure changes: a possible sensory mechanism? J Physiol. 1997; 505(Pt 2):503–511. PMID: 9423189.
57. Yoshida M, Miyamae K, Iwashita H, Otani M, Inadome A. Management of detrusor dysfunction in the elderly: changes in acetylcholine and adenosine triphosphate release during aging. Urology. 2004; 63(3 Suppl 1):17–23.
Article
58. Smith PP, Chalmers DJ, Feinn RS. Does defective volume sensation contribute to detrusor underactivity. Neurourol Urodyn. 2015; 34:752–756. PMID: 25220925.
Article
59. Smith PP, DeAngelis A, Kuchel GA. Detrusor expulsive strength is preserved, but responsiveness to bladder filling and urinary sensitivity is diminished in the aging mouse. Am J Physiol Regul Integr Comp Physiol. 2012; 302:R577–R586. PMID: 22204955.
Article
60. Dahlin LB, Shyu BC, Danielsen N, Andersson SA. Effects of nerve compression or ischaemia on conduction properties of myelinated and non-myelinated nerve fibres. An experimental study in the rabbit common peroneal nerve. Acta Physiol Scand. 1989; 136:97–105. PMID: 2773666.
Article
61. Wang Y, Tar MT, Fu S, Melman A, Davies KP. Diabetes attenuates urothelial modulation of detrusor contractility and spontaneous activity. Int J Urol. 2014; 21:1059–1064. PMID: 24846346.
Article
62. Kirschner-Hermanns R, Daneshgari F, Vahabi B, Birder L, Oelke M, Chacko S. Does diabetes mellitus-induced bladder remodeling affect lower urinary tract function? ICI-RS 2011. Neurourol Urodyn. 2012; 31:359–364. PMID: 22415965.
Article
63. Xiao N, Wang Z, Huang Y, Daneshgari F, Liu G. Roles of polyuria and hyperglycemia in bladder dysfunction in diabetes. J Urol. 2013; 189:1130–1136. PMID: 22999997.
Article
64. Aizawa N, Wakamatsu D, Kida J, Otsuki T, Saito Y, Matsuya H, et al. Inhibitory effects of retigabine, a Kv7 channel activator, on mechanosensitive primary bladder afferent activities and nociceptive behaviors in rats. Neurourol Urodyn. 2017; 36:280–285. PMID: 26536146.
Article
65. Mohammed HA, Santer RM. Distribution and changes with age of calcitonin gene-related peptide- and substance P-immunoreactive nerves of the rat urinary bladder and lumbosacral sensory neurons. Eur J Morphol. 2002; 40:293–301. PMID: 15101445.
Article
66. Mohammed H, Hannibal J, Fahrenkrug J, Santer R. Distribution and regional variation of pituitary adenylate cyclase activating polypeptide and other neuropeptides in the rat urinary bladder and ureter: effects of age. Urol Res. 2002; 30:248–255. PMID: 12202943.
Article
67. Jiang YH, Kuo HC. Urothelial barrier deficits, suburothelial inflammation and altered sensory protein expression in detrusor underactivity. J Urol. 2017; 197:197–203. PMID: 27436428.
Article
68. de Seze 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; 13:915–928. PMID: 17881401.
69. Sakakibara R, Tateno F, Nagao T, Yamamoto T, Uchiyama T, Yamanishi T, et al. Bladder function of patients with Parkinson's disease. Int J Urol. 2014; 21:638–646. PMID: 24571321.
Article
70. Bloch F, Pichon B, Bonnet AM, Pichon J, Vidailhet M, Roze E, et al. Urodynamic analysis in multiple system atrophy: characterisation of detrusor-sphincter dyssynergia. J Neurol. 2010; 257:1986–1991. PMID: 20683607.
Article
71. Hinson JL, Boone TB. Urodynamics and multiple sclerosis. Urol Clin North Am. 1996; 23:475–481. PMID: 8701560.
Article
72. Araki I, Matsui M, Ozawa K, Takeda M, Kuno S. Relationship of bladder dysfunction to lesion site in multiple sclerosis. J Urol. 2003; 169:1384–1387. PMID: 12629367.
Article
73. Kim M, Jung JH, Park J, Son H, Jeong SJ, Oh SJ, et al. Impaired detrusor contractility is the pathognomonic urodynamic finding of multiple system atrophy compared to idiopathic Parkinson's disease. Parkinsonism Relat Disord. 2015; 21:205–210. PMID: 25534084.
Article
74. Cruz CD, Cruz F. Spinal cord injury and bladder dysfunction: new ideas about an old problem. ScientificWorldJournal. 2011; 11:214–234. PMID: 21258763.
Article
75. Sahai A, Cortes E, Seth J, Khan MS, Panicker J, Kelleher C, et al. Neurogenic detrusor overactivity in patients with spinal cord injury: evaluation and management. Curr Urol Rep. 2011; 12:404–412. PMID: 21964989.
Article
76. Panicker JN, de Seze M, Fowler CJ. Rehabilitation in practice: neurogenic lower urinary tract dysfunction and its management. Clin Rehabil. 2010; 24:579–589. PMID: 20584864.
Article
77. Sekido N, Jyoraku A, Okada H, Wakamatsu D, Matsuya H, Nishiyama H. A novel animal model of underactive bladder: analysis of lower urinary tract function in a rat lumbar canal stenosis model. Neurourol Urodyn. 2012; 31:1190–1196. PMID: 22473471.
Article
78. Daneshgari F, Leiter EH, Liu G, Reeder J. Animal models of diabetic uropathy. J Urol. 2009; 182(6 Suppl):S8–S13. PMID: 19846143.
Article
79. Aizawa N, Homma Y, Igawa Y. Characteristics of lower urinary tract dysfunction and bladder afferent nerve properties in type 2 diabetic goto-kakizaki rats. J Urol. 2013; 189:1580–1587. PMID: 23103236.
Article
80. Imamura T, Ishizuka O, Ogawa T, Yamagishi T, Yokoyama H, Minagawa T, et al. Muscarinic receptors mediate cold stress-induced detrusor overactivity in type 2 diabetes mellitus rats. Int J Urol. 2014; 21:1051–1058. PMID: 24807830.
81. Saito M, Okada S, Kazuyama E, Satoh I, Kinoshita Y, Satoh K. Pharmacological properties, functional alterations and gene expression of muscarinic receptors in young and old type 2 Goto-Kakizaki diabetic rat bladders. J Urol. 2008; 180:2701–2705. PMID: 18951563.
Article
82. Matsumoto Y, Torimoto K, Matsuyoshi H, Hirayama A, Fujimoto K, Yoshimura N, et al. Long-term effects of diabetes mellitus on voiding function in a new model of type 2 diabetes mellitus, the Spontaneously Diabetic Torii (SDT) rat. Biomed Res. 2009; 30:331–335. PMID: 20051641.
Article
83. Tatemichi S, Tsuchioka K, Yonekubo S, Maruyama K, Kobayashi M. Effects of silodosin, an alpha1a-adrenoceptor antagonist, and distigmine, an acetylcholinesterase inhibitor, and their combined effects on impaired voiding function in zucker diabetic fatty rats. Pharmacology. 2015; 95:285–292. PMID: 26023044.
84. Lowalekar SK, Cristofaro V, Radisavljevic ZM, Yalla SV, Sullivan MP. Loss of bladder smooth muscle caveolae in the aging bladder. Neurourol Urodyn. 2012; 31:586–592. PMID: 22374691.
Article
85. Oshiro T, Miyazato M, Saito S. Relationship between connexin43-derived gap junction proteins in the bladder and age-related detrusor underactivity in rats. Life Sci. 2014; 116:37–42. PMID: 25150797.
Article
86. Hotta H, Morrison JF, Sato A, Uchida S. The effects of aging on the rat bladder and its innervation. Jpn J Physiol. 1995; 45:823–836. PMID: 8713179.
Article
87. Melman A, Tar M, Boczko J, Christ G, Leung AC, Zhao W, et al. Evaluation of two techniques of partial urethral obstruction in the male rat model of bladder outlet obstruction. Urology. 2005; 66:1127–1133. PMID: 16286152.
Article
88. Hashimoto T, Nagabukuro H, Doi T. Effects of the selective acetylcholinesterase inhibitor TAK-802 on the voiding behavior and bladder mass increase in rats with partial bladder outlet obstruction. J Urol. 2005; 174:1137–1141. PMID: 16094081.
Article
89. Matsumoto S, Hanai T, Ohnishi N, Yamamoto K, Kurita T. Bladder smooth muscle cell phenotypic changes and implication of expression of contractile proteins (especially caldesmon) in rats after partial outlet obstruction. Int J Urol. 2003; 10:339–345. PMID: 12757606.
Article
90. Zeng J, Xie K, Jiang C, Mo J, Lindstrom S. Bladder mechanoreceptor changes after artificial bladder outlet obstruction in the anesthetized rat. Neurourol Urodyn. 2012; 31:178–184. PMID: 22038729.
Article
91. Matsumoto S, Hanai T, Uemura H, Levin RM. Effects of chronic treatment with vardenafil, a phosphodiesterase 5 inhibitor, on female rat bladder in a partial bladder outlet obstruction model. BJU Int. 2009; 103:987–990. PMID: 19021615.
Article
92. Somogyi GT, Yokoyama T, Szell EA, Smith CP, de Groat WC, Huard J, et al. Effect of cryoinjury on the contractile parameters of bladder strips: a model of impaired detrusor contractility. Brain Res Bull. 2002; 59:23–28. PMID: 12372544.
Article
93. Kim SJ, Lee DS, Bae WJ, Kim S, Hong SH, Lee JY, et al. Functional and molecular changes of the bladder in rats with crushing injury of nerve bundles from major pelvic ganglion to the bladder: role of RhoA/Rho kinase pathway. Int J Mol Sci. 2013; 14:17511–17524. PMID: 23985824.
Article
94. Hannan JL, Powers SA, Wang VM, Castiglione F, Hedlund P, Bivalacqua TJ. Impaired contraction and decreased detrusor innervation in a female rat model of pelvic neuropraxia. Int Urogynecol J. 2017; 28:1049–1056. PMID: 27987021.
Article
95. Kontani H, Hayashi K. Urinary bladder response to hypogastric nerve stimulation after bilateral resection of the pelvic nerve or spinal cord injury in rats. Int J Urol. 1997; 4:394–400. PMID: 9256330.
Article
96. Kwon D, Minnery B, Kim Y, Kim JH, de Miguel F, Yoshimura N, et al. Neurologic recovery and improved detrusor contractility using muscle-derived cells in rat model of unilateral pelvic nerve transection. Urology. 2005; 65:1249–1253. PMID: 15922415.
Article
97. Ishida T, Shimoda N, Sato K, Ogawa O, Nishizawa O, Kato T. Effects of ischemia on voiding function and nerve growth factor of the rat urinary bladder. Nihon Hinyokika Gakkai Zasshi. 1999; 90:564–571. PMID: 10386056.
Article
98. Ohmura M, Yokoi K, Kondo A, Miyake K, Saito M. Effects of ischemia on the function of the isolated rat detrusor muscle. Hinyokika Kiyo. 1996; 42:111–115. PMID: 8712084.
99. Saito M, Yokoi K, Ohmura M, Kondo A. Effects of ligation of the internal iliac artery on blood flow to the bladder and detrusor function in rat. Int Urol Nephrol. 1998; 30:283–292. PMID: 9696334.
Article
100. Nomiya M, Yamaguchi O, Andersson KE, Sagawa K, Aikawa K, Shishido K, et al. The effect of atherosclerosis-induced chronic bladder ischemia on bladder function in the rat. Neurourol Urodyn. 2012; 31:195–200. PMID: 21905085.
Article
Full Text Links
  • ICU
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr