The role of electrical stimulation in the management of lower urinary track dysfunction following spinal cord lesions
Keywords:
Urinary track dysfunction, spinal cord injuriesAbstract
Spinal cord lesions are traumatic or non-traumatic. Spinal cord injuries (SCI) may be complete or incomplete and lead to lower urinary track dysfunction (LUTD) in 95%. Multiple sclerosis is the most frequent cause of non-traumatic spinal cord lesions and leads to LUTD in more than 90% of patients 10 years after diagnosis. LUTD usually presents as neurogenic detrusor overactivity and/or detrusor-sphincter dyssynergia where oral medication is considered to be the first line of treatment and intravesical onabotulinum toxin injections the second, but there are side-effects and refractory cases. In addition, LUTD may present as detrusor underactivity where the above treatment options are not effective.
Clearly there is a need for a third line of treatment. In this review, we discuss the feasibility, safety and efficacy of electrical stimulation for the management of neurogenic LUTD, spanning from historic clinical to recent pre-clinical approaches. Neurostimulation methods are used on complete SCI patients, while neuromodulation methods are mostly used on incomplete spinal lesion patients and can be invasive or non-invasive. There is evidence that neuromodulation inhibits the development of neurogenic LUTD when applied shortly after acute spinal cord lesions. More high-quality studies are needed to prove efficacy of neuromodulation on neurogenic LUTD.
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References
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2. Steadman CJ, Grill WM. Spinal cord stimulation for the restoration of bladder function after spinal cord injury. Healthc Technol Lett. 2020;7(3). doi:10.1049/htl.2020.0026
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7. de Groat WC, Griffiths D, Yoshimura N. Neural control of the lower urinary tract. Compr Physiol. 2015;5(1). doi:10.1002/cphy.c130056
8. Panicker JN. Neurogenic Bladder: Epidemiology, Diagnosis, and Management. Semin Neurol. 2020;40(5):569-579. doi:10.1055/s-0040-1713876
9. Sivan, Manoj; Phillips, Margaret; Baguley, Ian; Nott M. Neurogenic Bladder and Bowel. In: Oxford Handbook of Rehabilitation Medicine. third. ; 2019:168-178.
10. McGee MJ, Amundsen CL, Grill WM. Electrical stimulation for the treatment of lower urinary tract dysfunction after spinal cord injury. J Spinal Cord Med. 2015;38(2). doi:10.1179/2045772314Y.0000000299
11. Martens FMJ, Sievert KD. Neurostimulation in neurogenic patients. Curr Opin Urol. 2020;30(4). doi:10.1097/MOU.0000000000000773
12. Guiho T, Azevedo-Coste C, Bauchet L, et al. Sacral Anterior Root Stimulation and Visceral Function
Outcomes in Spinal Cord Injury–A Systematic Review of the Literature Over Four Decades. World Neurosurg. 2022;157. doi:10.1016/j.wneu.2021.09.041
13. Martens FMJ, Den Hollander PP, Snoek GJ, Koldewijn EL, Van Kerrebroeck PEVA, Heesakkers JPFA. Quality of life in complete spinal cord injury patients with a Brindley bladder stimulator compared to a matched control group. Neurourol Urodyn. 2011;30(4). doi:10.1002/nau.21012
14. Katona F. Stages of vegetative afferentation in reorganization of bladder control during intravesical electrotherapy. Urol Int. 1975;30(3). doi:10.1159/000279979
15. Ebner A, Jiang C, Lindstrom S. Intravesical electrical stimulation - An experimental analysis of the mechanism of action. J Urol. 1992;148(3 I). doi:10.1016/S0022-5347(17)36778-2
16. James Walter 1, 2 IH 3, 4 BT, 5 AAC, et al. A New Electrode Design for Direct Bladder Wall Stimulation: A Pilot Minipig Study with Chronic Testing. Appl Sci. 2022;12(1149):1-10.
17. Abboud H, Hill E, Siddiqui J, Serra A, Walter B. Neuromodulation in multiple sclerosis. Mult Scler. 2017;23(13). doi:10.1177/1352458517736150
18. Herrity AN, Williams CS, Angeli CA, Harkema SJ, Hubscher CH. Lumbosacral spinal cord epidural stimulation improves voiding function after human spinal cord injury. Sci Rep. 2018;8(1). doi:10.1038/s41598-018-26602-2
19. Havton LA, Christe KL, Edgerton VR, Gad PN. Noninvasive spinal neuromodulation to map and augment lower urinary tract function in rhesus macaques. Exp Neurol. 2019;322. doi:10.1016/j.expneurol.2019.113033
20. Daia C, Bumbea AM, Dumitru Badiu C, Ciobotaru C, Onose G. Interferential electrical stimulation for improved bladder management following spinal cord injury. Biomed Reports. 2019;11(3):115122. doi:10.3892/br.2019.1227
21. Goldman HB, Lloyd JC, Noblett KL, et al. International Continence Society best practice statement for use of sacral neuromodulation. Neurourol Urodyn. 2018;37(5):1823-1848. doi:10.1002/nau.23515
22. Ammirati E, Giammò A, Manassero A, Carone R. Neuromodulation in urology, state of the art. Urol J. 2019;86(4). doi:10.1177/0391560319866075
23. Stampas A, Korupolu R, Zhu L, Smith CP, Gustafson K. Safety, Feasibility, and Efficacy of Transcutaneous Tibial Nerve Stimulation in Acute Spinal Cord Injury Neurogenic Bladder: A Randomized Control Pilot Trial. Neuromodulation Technol Neural Interface. 2019;22(6):716-722. doi:10.1111/NER.12855
24. de Wall LL, Heesakkers JPFA. Effectiveness of percutaneous tibial nerve stimulation in the treatment of overactive bladder syndrome. Res Reports Urol. 2017;9. doi:10.2147/RRU.S124981
25. Janssen DAW, Martens FMJ, de Wall LL, van Breda HMK, Heesakkers JPFA. Clinical utility of neurostimulation devices in the treatment of overactive bladder: Current perspectives. Med Devices Evid Res. 2017;10. doi:10.2147/mder.s115678
26. Girtner F, Burger M, Mayr R. Sacral neuromodulation in under- and overactive detrusor—quo vadis?: Principles and developments. Urol . 2019;58(6). doi:10.1007/s00120-019-0949-7
27. Assmann R, Douven P, Kleijnen J, et al. Stimulation Parameters for Sacral Neuromodulation on Lower Urinary Tract and Bowel Dysfunction–Related Clinical Outcome: A Systematic Review. Neuromodulation. 2020;23(8):1082-1093. doi:10.1111/ner.13255
28. Amundsen CL, Richter HE, Menefee SA, et al. Onabotulinumtoxin a vs sacral neuromodulation on refractory urgency urinary incontinence in women: A randomized clinical trial. JAMA - J Am Med Assoc. 2016;316(13). doi:10.1001/jama.2016.14617
29. Sievert, Karl-Dietrich; Amend, Bastian; Gakis G et al. Early sacral neuromodulation prevents urinary incontinence after complete spinal cord injury. Ann Neurol. Published online 2010.
30. McGuire EJ, Shi Chun Z, Horwinski ER, Lytton B. Treatment of motor and sensory detrusor instability by electrical stimulation. J Urol. 1983;129(1). doi:10.1016/S0022-5347(17)51928-X
31. Bhide AA, Tailor V, Fernando R, Khullar V, Digesu GA. Posterior tibial nerve stimulation for overactive bladder—techniques and efficacy. Int Urogynecol J. 2020;31(5). doi:10.1007/s00192-01904186-3
32. Gross T, Schneider MP, Bachmann LM, Blok BF, Groen J H, LA et al. Transcutaneous electrical nerve stimulation for treating neurogenic lower urinary tract dysfunction: a systematic review. Eur Urol. 2016;69((6)):1102-1111.
33. Chen G, Liao L, Li Y. The possible role of percutaneous tibial nerve stimulation using adhesive skin surface electrodes in patients with neurogenic detrusor overactivity secondary to spinal cord injury. Int Urol Nephrol. 2015;47(3). doi:10.1007/s11255-015-0911-6
34. De Sèze M, Raibaut P, Gallien P, et al. 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). doi:10.1002/nau.20958
35. Krhut J, Peter L, Rejchrt M, Slovak M, Skugarevska B, Zvara P. Peroneal Electric Transcutaneous
NeuroModulation (eTNM®): A Novel Method for the Treatment of the Overactive Bladder. J Healthc Eng. 2021;2021. doi:10.1155/2021/4016346
36. Finazzi-Agrò E, Rocchi C, Pachatz C, et al. Percutaneous tibial nerve stimulation produces effects on brain activity: Study on the modifications of the long latency somatosensory evoked potentials. Neurourol Urodyn. 2009;28(4). doi:10.1002/nau.20651
37. Finazzi-Agr E, Petta F, Sciobica F, Pasqualetti P, Musco S, Bove P. Percutaneous tibial nerve stimulation effects on detrusor overactivity incontinence are not due to a placebo effect: A randomized, double-blind, placebo controlled trial. J Urol. 2010;184(5). doi:10.1016/j.juro.2010.06.113
38. Peters KM, Carrico DJ, Perez-Marrero RA, et al. Randomized Trial of Percutaneous Tibial Nerve
Stimulation Versus Sham Efficacy in the Treatment of Overactive Bladder Syndrome: Results From
the SUmiT Trial. J Urol. 2010;183(4). doi:10.1016/j.juro.2009.12.036
39. Kabay S, Kabay SC, Yucel M, et al. 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). doi:10.1002/nau.20733
40. Peters KM, Feber KM, Bennett RC. Sacral versus pudendal nerve stimulation for voiding dysfunction: A prospective, single-blinded, randomized, crossover trial. Neurourol Urodyn. 2005;24(7). doi:10.1002/nau.20174
41. Li P, Liao L, Chen G, Zhang F, Tian Y. Early low-frequency stimulation of the pudendal nerve can inhibit detrusor overactivity and delay progress of bladder fibrosis in dogs with spinal cord injuries. Spinal Cord. 2013;51(9). doi:10.1038/sc.2013.60
42. Dalmose AL, Rijkhoff NJM, Kirkeby HJ, Nohr M, Sinkjaer T, Djurhuus JC. Conditional stimulatzion of the dorsal penile/clitoral nerve may increase cystometric capacity in patients with spinal cord injury. Neurourol Urodyn. 2003;22(2). doi:10.1002/nau.10031
43. 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). doi:10.1002/nau.20170
44. Schieferdecker S, Neudorfer C, El Majdoub F, Maarouf M. A Retrospective Case Series of High-Frequency Spinal Cord Stimulation (HF10-SCS) in Neurogenic Bladder Incontinence. Oper Neurosurg. 2019;17(1). doi:10.1093/ons/opy236
2. Steadman CJ, Grill WM. Spinal cord stimulation for the restoration of bladder function after spinal cord injury. Healthc Technol Lett. 2020;7(3). doi:10.1049/htl.2020.0026
3. Kirshblum, Steven; Donovan, Jayne; Nieves, Jeremiah; Gonzalez, Priscila; Cuccurullo, Sara; Luciano L. Spinal cord injuries: Bladder dysfunction. In: Physical Medicine and Rehabilitation Board Review. Fourth edi. ; 2019:566-577.
4. Birkhäuser V, Liechti MD, Anderson CE, et al. TASCI-transcutaneous tibial nerve stimulation in patients with acute spinal cord injury to prevent neurogenic detrusor overactivity: Protocol for a nationwide, randomised, sham-controlled, double-blind clinical trial. BMJ Open. 2020;10(8). doi:10.1136/bmjopen-2020-039164
5. de Sèze M, Ruffion A, Denys P, Joseph PA, Perrouin-Verbe B. The neurogenic bladder in multiple sclerosis: Review of the literature and proposal of management guidelines. Mult Scler. 2007;13(7). doi:10.1177/1352458506075651
6. de Groat WC, Yoshimura N. Plasticity in reflex pathways to the lower urinary tract following spinal cord injury. Exp Neurol. 2012;235(1):123-132. doi:10.1016/J.EXPNEUROL.2011.05.003
7. de Groat WC, Griffiths D, Yoshimura N. Neural control of the lower urinary tract. Compr Physiol. 2015;5(1). doi:10.1002/cphy.c130056
8. Panicker JN. Neurogenic Bladder: Epidemiology, Diagnosis, and Management. Semin Neurol. 2020;40(5):569-579. doi:10.1055/s-0040-1713876
9. Sivan, Manoj; Phillips, Margaret; Baguley, Ian; Nott M. Neurogenic Bladder and Bowel. In: Oxford Handbook of Rehabilitation Medicine. third. ; 2019:168-178.
10. McGee MJ, Amundsen CL, Grill WM. Electrical stimulation for the treatment of lower urinary tract dysfunction after spinal cord injury. J Spinal Cord Med. 2015;38(2). doi:10.1179/2045772314Y.0000000299
11. Martens FMJ, Sievert KD. Neurostimulation in neurogenic patients. Curr Opin Urol. 2020;30(4). doi:10.1097/MOU.0000000000000773
12. Guiho T, Azevedo-Coste C, Bauchet L, et al. Sacral Anterior Root Stimulation and Visceral Function
Outcomes in Spinal Cord Injury–A Systematic Review of the Literature Over Four Decades. World Neurosurg. 2022;157. doi:10.1016/j.wneu.2021.09.041
13. Martens FMJ, Den Hollander PP, Snoek GJ, Koldewijn EL, Van Kerrebroeck PEVA, Heesakkers JPFA. Quality of life in complete spinal cord injury patients with a Brindley bladder stimulator compared to a matched control group. Neurourol Urodyn. 2011;30(4). doi:10.1002/nau.21012
14. Katona F. Stages of vegetative afferentation in reorganization of bladder control during intravesical electrotherapy. Urol Int. 1975;30(3). doi:10.1159/000279979
15. Ebner A, Jiang C, Lindstrom S. Intravesical electrical stimulation - An experimental analysis of the mechanism of action. J Urol. 1992;148(3 I). doi:10.1016/S0022-5347(17)36778-2
16. James Walter 1, 2 IH 3, 4 BT, 5 AAC, et al. A New Electrode Design for Direct Bladder Wall Stimulation: A Pilot Minipig Study with Chronic Testing. Appl Sci. 2022;12(1149):1-10.
17. Abboud H, Hill E, Siddiqui J, Serra A, Walter B. Neuromodulation in multiple sclerosis. Mult Scler. 2017;23(13). doi:10.1177/1352458517736150
18. Herrity AN, Williams CS, Angeli CA, Harkema SJ, Hubscher CH. Lumbosacral spinal cord epidural stimulation improves voiding function after human spinal cord injury. Sci Rep. 2018;8(1). doi:10.1038/s41598-018-26602-2
19. Havton LA, Christe KL, Edgerton VR, Gad PN. Noninvasive spinal neuromodulation to map and augment lower urinary tract function in rhesus macaques. Exp Neurol. 2019;322. doi:10.1016/j.expneurol.2019.113033
20. Daia C, Bumbea AM, Dumitru Badiu C, Ciobotaru C, Onose G. Interferential electrical stimulation for improved bladder management following spinal cord injury. Biomed Reports. 2019;11(3):115122. doi:10.3892/br.2019.1227
21. Goldman HB, Lloyd JC, Noblett KL, et al. International Continence Society best practice statement for use of sacral neuromodulation. Neurourol Urodyn. 2018;37(5):1823-1848. doi:10.1002/nau.23515
22. Ammirati E, Giammò A, Manassero A, Carone R. Neuromodulation in urology, state of the art. Urol J. 2019;86(4). doi:10.1177/0391560319866075
23. Stampas A, Korupolu R, Zhu L, Smith CP, Gustafson K. Safety, Feasibility, and Efficacy of Transcutaneous Tibial Nerve Stimulation in Acute Spinal Cord Injury Neurogenic Bladder: A Randomized Control Pilot Trial. Neuromodulation Technol Neural Interface. 2019;22(6):716-722. doi:10.1111/NER.12855
24. de Wall LL, Heesakkers JPFA. Effectiveness of percutaneous tibial nerve stimulation in the treatment of overactive bladder syndrome. Res Reports Urol. 2017;9. doi:10.2147/RRU.S124981
25. Janssen DAW, Martens FMJ, de Wall LL, van Breda HMK, Heesakkers JPFA. Clinical utility of neurostimulation devices in the treatment of overactive bladder: Current perspectives. Med Devices Evid Res. 2017;10. doi:10.2147/mder.s115678
26. Girtner F, Burger M, Mayr R. Sacral neuromodulation in under- and overactive detrusor—quo vadis?: Principles and developments. Urol . 2019;58(6). doi:10.1007/s00120-019-0949-7
27. Assmann R, Douven P, Kleijnen J, et al. Stimulation Parameters for Sacral Neuromodulation on Lower Urinary Tract and Bowel Dysfunction–Related Clinical Outcome: A Systematic Review. Neuromodulation. 2020;23(8):1082-1093. doi:10.1111/ner.13255
28. Amundsen CL, Richter HE, Menefee SA, et al. Onabotulinumtoxin a vs sacral neuromodulation on refractory urgency urinary incontinence in women: A randomized clinical trial. JAMA - J Am Med Assoc. 2016;316(13). doi:10.1001/jama.2016.14617
29. Sievert, Karl-Dietrich; Amend, Bastian; Gakis G et al. Early sacral neuromodulation prevents urinary incontinence after complete spinal cord injury. Ann Neurol. Published online 2010.
30. McGuire EJ, Shi Chun Z, Horwinski ER, Lytton B. Treatment of motor and sensory detrusor instability by electrical stimulation. J Urol. 1983;129(1). doi:10.1016/S0022-5347(17)51928-X
31. Bhide AA, Tailor V, Fernando R, Khullar V, Digesu GA. Posterior tibial nerve stimulation for overactive bladder—techniques and efficacy. Int Urogynecol J. 2020;31(5). doi:10.1007/s00192-01904186-3
32. Gross T, Schneider MP, Bachmann LM, Blok BF, Groen J H, LA et al. Transcutaneous electrical nerve stimulation for treating neurogenic lower urinary tract dysfunction: a systematic review. Eur Urol. 2016;69((6)):1102-1111.
33. Chen G, Liao L, Li Y. The possible role of percutaneous tibial nerve stimulation using adhesive skin surface electrodes in patients with neurogenic detrusor overactivity secondary to spinal cord injury. Int Urol Nephrol. 2015;47(3). doi:10.1007/s11255-015-0911-6
34. De Sèze M, Raibaut P, Gallien P, et al. 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). doi:10.1002/nau.20958
35. Krhut J, Peter L, Rejchrt M, Slovak M, Skugarevska B, Zvara P. Peroneal Electric Transcutaneous
NeuroModulation (eTNM®): A Novel Method for the Treatment of the Overactive Bladder. J Healthc Eng. 2021;2021. doi:10.1155/2021/4016346
36. Finazzi-Agrò E, Rocchi C, Pachatz C, et al. Percutaneous tibial nerve stimulation produces effects on brain activity: Study on the modifications of the long latency somatosensory evoked potentials. Neurourol Urodyn. 2009;28(4). doi:10.1002/nau.20651
37. Finazzi-Agr E, Petta F, Sciobica F, Pasqualetti P, Musco S, Bove P. Percutaneous tibial nerve stimulation effects on detrusor overactivity incontinence are not due to a placebo effect: A randomized, double-blind, placebo controlled trial. J Urol. 2010;184(5). doi:10.1016/j.juro.2010.06.113
38. Peters KM, Carrico DJ, Perez-Marrero RA, et al. Randomized Trial of Percutaneous Tibial Nerve
Stimulation Versus Sham Efficacy in the Treatment of Overactive Bladder Syndrome: Results From
the SUmiT Trial. J Urol. 2010;183(4). doi:10.1016/j.juro.2009.12.036
39. Kabay S, Kabay SC, Yucel M, et al. 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). doi:10.1002/nau.20733
40. Peters KM, Feber KM, Bennett RC. Sacral versus pudendal nerve stimulation for voiding dysfunction: A prospective, single-blinded, randomized, crossover trial. Neurourol Urodyn. 2005;24(7). doi:10.1002/nau.20174
41. Li P, Liao L, Chen G, Zhang F, Tian Y. Early low-frequency stimulation of the pudendal nerve can inhibit detrusor overactivity and delay progress of bladder fibrosis in dogs with spinal cord injuries. Spinal Cord. 2013;51(9). doi:10.1038/sc.2013.60
42. Dalmose AL, Rijkhoff NJM, Kirkeby HJ, Nohr M, Sinkjaer T, Djurhuus JC. Conditional stimulatzion of the dorsal penile/clitoral nerve may increase cystometric capacity in patients with spinal cord injury. Neurourol Urodyn. 2003;22(2). doi:10.1002/nau.10031
43. 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). doi:10.1002/nau.20170
44. Schieferdecker S, Neudorfer C, El Majdoub F, Maarouf M. A Retrospective Case Series of High-Frequency Spinal Cord Stimulation (HF10-SCS) in Neurogenic Bladder Incontinence. Oper Neurosurg. 2019;17(1). doi:10.1093/ons/opy236
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2024-06-25
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