Transcutaneously Coupled,High-Frequency Electrical Stimulation of the Pudendal Nerve Blocks External Urethral Sphincter Contractions

Abstract

Background. Detrusor-sphincter dyssynergia is a condition in which reflexive contractions of the external urethral sphincter occur during bladder contractions, preventing the expulsion of urine. High-frequency stimulation (kHz range) has been shown to elicit a fast-acting and reversible block of action potential propagation in peripheral nerves, which may be a useful technique in the management of this condition. Objective. The aim of these experiments was to see if a newly developed stimulus delivery system, capable of transmitting current transcutaneously to remote peripheral nerves using a passive implanted conductor, was an effective way to transmit high-frequency waveforms to the pudendal nerve to block ongoing sphincter contractions. Methods. High-frequency waveforms were delivered through the skin to the pudendal nerve using a passive implanted conductor in 6 adult cats anesthetized with isoflurane. Five of the experiments were acute, terminal procedures, and the remaining cat was implanted with a permanent electrode system allowing evaluation for 6 months. Typical stimulation parameters were in the range of 1 to 10 kHz and 1 to 10 mA. Results. Complete blocking of external urethral sphincter contractions was achieved in 5 of the 6 animals. High-frequency stimulation was also tested in the chronically implanted animal without anesthesia, and the stimulation was tolerated with minimal aversive reactions. Conclusions. The transcutaneous passive implanted conductor stimulus delivery system is an effective way to stimulate the pudendal nerve at high frequency, leading to sphincter relaxation. This system may provide a simple means to implement this stimulation paradigm in people with detrusor-sphincter dyssynergia.

Keywords

Detrusor-sphincter dyssyergia Neuroprosthesis High-frequency block Bladder Spinal cord injury

References

Kaplan SA , Chancellor MB , Blaivas JG Bladder and sphincter behavior in patients with spinal cord lesions . J Urol. 1991;146:113-117.

Weld KJ , Dmochowski RR Association of level of injury and bladder behavior in patients with post-traumatic spinal cord injury. Urology. 2000;55:490-494.

Yalla SV , Blunt KJ , Fam BA , Constantinople NL , Gittes RF Detrusor-urethral sphincter dyssynergia. J Urol. 1977;118:1026-1029.

Gaunt RA , Prochazka A. Control of urinary bladder function with devices: successes and failures . Prog Brain Res. 2006;152:163-194.

Middleton JW , Lim K. , Taylor L. , Soden R. , Rutkowski S. Patterns of morbidity and rehospitalisation following spinal cord injury. Spinal Cord. 2004;42:359-367.

Bhadra N. , Bhadra N. , Kilgore K. , Gustafson KJ High frequency electrical conduction block of the pudendal nerve. J Neural Eng. 2006;3:180-187.

Tai C. , Roppolo JR , de Groat WC Block of external urethral sphincter contraction by high frequency electrical stimulation of pudendal nerve. J Urol. 2004 ;172:2069-2072.

Tai C. , Roppolo JR , de Groat WC Response of external urethral sphincter to high frequency biphasic electrical stimulation of pudendal nerve. J Urol. 2005 ;174:782-786.

Martin WD , Fletcher TF , Bradley WE Innervation of feline perineal musculature. Anat Rec . 1974;180:15-29.

10.

Kilgore KL , Bhadra N. Nerve conduction block utilising high-frequency alternating current . Med Biol Eng Comput. 2004;42:394-406.

11.

Bhadra N. , Kilgore KL High-frequency electrical conduction block of mammalian peripheral motor nerve . Muscle Nerve. 2005;32:782-790.

12.

Bhadra N. , Lahowetz EA , Foldes ST , Kilgore KL Simulation of high-frequency sinusoidal electrical block of mammalian myelinated axons. J Comput Neurosci. 2007;22:313-326.

13.

Tai C. , de Groat WC , Roppolo JR Simulation analysis of conduction block in unmyelinated axons induced by high-frequency biphasic electrical currents. IEEE Trans Biomed Eng. 2005;52:1323-1332.

14.

Tai C. , de Groat WC , Roppolo JR Simulation of nerve block by high-frequency sinusoidal electrical current based on the Hodgkin-Huxley model. IEEE Trans Neural Syst Rehabil Eng. 2005;13:415-422.

15.

Zhang X. , Roppolo JR , de Groat WC , Tai C. Simulation analysis of conduction block in myelinated axons induced by high-frequency biphasic rectangular pulses. IEEE Trans Biomed Eng. 2006;53:1433-1436.

16.

Zhang X. , Roppolo JR , de Groat WC , Tai C. Mechanism of nerve conduction block induced by high-frequency biphasic electrical currents. IEEE Trans Biomed Eng. 2006;53:2445-2454.

17.

Abdel-Gawad M. , Boyer S. , Sawan M. , Elhilali MM Reduction of bladder outlet resistance by selective stimulation of the ventral sacral root using high frequency blockade: a chronic study in spinal cord transected dogs . J Urol. 2001;166:728-733.

18.

Ishigooka M. , Hashimoto T. , Sasagawa I. , Izumiya K. , Nakada T. Modulation of the urethral pressure by high-frequency block stimulus in dogs. Eur Urol. 1994;25:334-337.

19.

Shaker HS , Tu LM , Robin S. , et al. Reduction of bladder outlet resistance by selective sacral root stimulation using high-frequency blockade in dogs: an acute study. J Urol. 1998;160:901-907.

20.

Solomonow M. , Eldred E. , Lyman J. , Foster J. Control of muscle contractile force through indirect high-frequency stimulation. Am J Phys Med. 1983; 62:71-82.

21.

Zhou B. -H, Baratta R. , Solomonow M. Manipulation of Muscle Force with Various Firing Rate and Recruitment Control Strategies. IEEE Trans Biomed Eng. 1987;34:128-139.

22.

Rubinstein JT , Tyler RS , Johnson A. , Brown CJ Electrical suppression of tinnitus with high-rate pulse trains. Otol Neurotol. 2003;24:478-485.

23.

Gan LS , Prochazka A. , Bornes TD , Denington AA , Chan KM A new means of transcutaneous coupling for neural prostheses. IEEE Trans Biomed Eng. 2007;54:509-517.

24.

Brown M. , Wickham JE The urethral pressure profile. Br J Urol. 1969;41: 211-217.

25.

Elbasiouny SM , Mushahwar VK Modulation of motoneuronal firing behavior after spinal cord injury using intraspinal microstimulation current pulses: a modeling study. J Appl Physiol. 2007;103:276-286.

26.

Williamson RP , Andrews BJ Localized electrical nerve blocking . IEEE Trans Biomed Eng. 2005;52:362-370.

27.

Brindley GS The first 500 patients with sacral anterior root stimulator implants: general description. Paraplegia . 1994;32:795-805.

28.

Miles JD , Kilgore KL , Bhadra N. , Lahowetz EA Effects of ramped amplitude waveforms on the onset response of high-frequency mammalian nerve block. J Neural Eng. 2007;4:390-398.

29.

Ungar IJ , Mortimer JT , Sweeney JD Generation of unidirectionally propagating action potentials using a monopolar electrode cuff. Ann Biomed Eng. 1986;14:437-450.

30.

Sweeney JD , Mortimer JT An asymmetric two electrode cuff for generation of unidirectionally propagated action potentials. IEEE Trans Biomed Eng. 1986;33:541-549.

31.

Duch DS , Rehberg B. , Vysotskaya TN Volatile anesthetics significantly suppress central and peripheral mammalian sodium channels. Toxicol Lett. 1998 ;100-101:255-263.

32.

Nau C. Voltage-gated ion channels. Handb Exp Pharmacol. 2008(182): 85-92.

33.

Mortimer JT Motor prostheses. In: Brooks VB , ed. The Nervous System, Vol II: Motor Control. Bethesda, MD: American Physiological Society ; 1981:155-187.

34.

Reynard JM , Vass J. , Sullivan ME , Mamas M. Sphincterotomy and the treatment of detrusor-sphincter dyssynergia: current status, future prospects. Spinal Cord. 2003 ;41:1-11.

35.

Smith CP , Nishiguchi J. , O'Leary M. , Yoshimura N. , Chancellor MB Single-institution experience in 110 patients with botulinum toxin A injection into bladder or urethra. Urology. 2005;65:37-41.

36.

Brindley GS , Polkey CE , Rushton DN , Cardozo L. Sacral anterior root stimulators for bladder control in paraplegia: the first 50 cases. J Neurol Neurosurg Psychiatry. 1986;49:1104-1114.

37.

Bhadra N. , Grunewald V. , Creasey G. , Mortimer JT Selective suppression of sphincter activation during sacral anterior nerve root stimulation. Neurourol Urodyn. 2002;21:55-64.

38.

Fang ZP , Mortimer JT Selective activation of small motor axons by quasi-trapezoidal current pulses . IEEE Trans Biomed Eng. 1991;38:168-174.

39.

Gustafson KJ , Zelkovic PF , Feng AH , Draper CE , Bodner DR , Grill WM Fascicular anatomy and surgical access of the human pudendal nerve. World J Urol . 2005 ;23:411-418.

40.

Dalmose AL , Rijkhoff NJ , Kirkeby HJ , Nohr M. , Sinkjaer T. , Djurhuus JC Conditional stimulation of the dorsal penile/clitoral nerve may increase cystometric capacity in patients with spinal cord injury. Neurourol Urodyn . 2003;22:130-137.

41.

Nakamura M. , Sakurai T. Bladder inhibition by penile electrical stimulation . Br J Urol. 1984;56:413-415.

42.

Wheeler JS Jr , Walter JS , Zaszczurynski PJ Bladder inhibition by penile nerve stimulation in spinal cord injury patients. J Urol. 1992 ;147: 100-103.

43.

Boggs JW , Wenzel BJ , Gustafson KJ , Grill WM Spinal micturition reflex mediated by afferents in the deep perineal nerve . J Neurophysiol. 2005;93: 2688-2697.

44.

Tai C. , Smerin SE , de Groat WC , Roppolo JR Pudendal-to-bladder reflex in chronic spinal-cord-injured cats. Exp Neurol. 2006;197:225-234.

45.

Gustafson KJ , Creasey GH , Grill WM A urethral afferent mediated excitatory bladder reflex exists in humans. Neurosci Lett. 2004 ; 360:9-12.

46.

Boger A. , Bhadra N. , Gustafson KJ Bladder voiding by combined high frequency electrical pudendal nerve block and sacral root stimulation. Neurourol Urodyn. 2008;27:435-439.

47.

Tai C. , Wang J. , Wang X. , Roppolo JR , de Groat WC Voiding reflex in chronic spinal cord injured cats induced by stimulating and blocking pudendal nerves. Neurourol Urodyn. 2007;26:879-886