Elsevier

Experimental Neurology

Volume 215, Issue 2, February 2009, Pages 342-348
Experimental Neurology

Electrophysiological function during voiding after simulated childbirth injuries

https://doi.org/10.1016/j.expneurol.2008.10.024Get rights and content

Abstract

During vaginal delivery dual injuries of the pudendal nerve and the external urethral sphincter (EUS), along with other injuries, are correlated with later development of stress urinary incontinence. It is not known how combinations of these injuries affect neuromuscular recovery of the micturition reflex. We investigated the EUS electromyogram (EMG) and the pudendal nerve motor branch potentials (PNMBP) during voiding 4 days, 3 weeks or 6 weeks after injury; including vaginal distension (VD), pudendal nerve crush (PNC), both PNC and VD (PNC + VD), and pudendal nerve transection (PNT); and in controls. Pudendal nerve and urethral specimens were excised and studied histologically. No bursting activity was recorded in the EUS EMG during voiding 4 days after all injuries, as well as 3 weeks after PNC + VD. Bursting activity demonstrated recovery 3 weeks after either VD or PNC and 6 weeks after PNC + VD, but the recovered intraburst frequency remained significantly decreased compared to controls. Bursting results of PNMBP were similar to the EMG, except bursting in PNMBP 4 days after VD and the recovered intraburst frequency was significantly increased compared to controls after PNC and PNC + VD. After PNT, neither the EUS nor the pudendal nerve recovered by 6 weeks after injury. Our findings indicate bursting discharge during voiding recovers more slowly after PNC + VD than after either PNC or VD alone. This was confirmed histologically in the urethra and the pudendal nerve and may explain why pudendal nerve dysfunction has been observed years after vaginal delivery.

Introduction

Vaginal childbirth can cause damage to the pudendal nerve, the levator ani, and pelvic organ fascial supports as well as the urethral and anal sphincters (Dietz and Wilson, 2005, Goldberg et al., 2005). The risk factors for injury include operative vaginal delivery, long second stage of delivery, and fetal macrosomia (Nassar et al., 2003, Hankins and Rowe, 1996). Therefore, vaginal delivery represents a potent determinant of stress urinary incontinence (SUI) (Goldberg et al. 2005). However, it is much less clear how the combination of these traumas affects the rate of recovery during the micturition reflex.

We have recently developed a dual injury model in the rat to better simulate the combination of traumas of childbirth, including injuries both to the external urinary sphincter (EUS) via vaginal distension (VD) and to its innervation, the pudendal nerve, via a bilateral pudendal nerve crush (PNC) (Jiang et al. in press). Both single injury models have been previously utilized to demonstrate, among other results, that increased duration of VD results in increased time to recovery (Pan et al. 2007); the pudendal nerve regenerates by 2 weeks later (Damaser et al. 2007); and the urethra, vagina, and bladder become ischemic after VD (Damaser et al. 2005). However, it is not clear how combinations of these injuries affect neuromuscular recovery of voiding.

In normal rats, voiding is characterized by interrupted bursting of the EUS electromyogram (EMG) (Maggi et al., 1986a, Kruse et al., 1993). The presence of the bursting EUS EMG activity is considered a hallmark for normal and effective micturition reflex recovery in rats after neurological injuries (Kruse et al. 1993). The bursting EUS EMG activity may disappear acutely after injury but shows signs of recovery at later time points (Cheng and de Groat, 2004, Chang et al., 2007, Chang and Havton, 2008).

In rats, the pudendal nerve is divided into sensory and motor nerve branches in Alcock's canal, making the rat a useful model for electrophysiological study (McKenna and Nadelhaft 1986) (McKenna and Nadelhaft 1989). We have recorded pudendal nerve motor branch potentials (PNMBP) to obtain a functional measure of pudendal efferent recovery after injury (Jiang et al. in press). The goal of this study was to determine how different simulated childbirth injuries affect the recovery of electrophysiological bursting discharge both in the EUS EMG and PNMBP during voiding, after single and combined simulated childbirth injuries, and to relate them to histological outcomes of the pudendal nerve and urethra.

Section snippets

Materials and methods

All procedures were reviewed and approved by the Institutional Animal Care and Use Committee of the Cleveland Clinic. Sixty-seven female virgin Sprague–Dawley rats (200–250 g) were randomized into five groups: uninjured control, VD, PNC, PNC + VD, and bilateral pudendal nerve transection (PNT). The recordings, including filling cystometrogram (CMG), EUS EMG, and PNMBP, were performed in the VD and PNC groups either 4 days (n = 5) or 3 weeks (n = 5) after injury. In PNC + VD and PNT groups, recordings

Electrophysiological bursting during voiding in control rats

High frequency oscillations (HFO) in bladder pressure were identified during voiding in urethane-anesthetized uninjured control rats. Both the EUS EMG and the PNMBP demonstrated bursting activity during voiding associated with HFO in bladder pressure (Fig. 1). Each wave of the HFO was associated with the bursting event in both EUS EMG and PNMBP with approximately a 50 ms time delay between the middle of the bursting event and the peak of the pressure wave. Each EUS EMG bursting event was

Discussion

Both the EUS and the pudendal nerve can be injured during vaginal delivery (Rogers and Leeman 2007) although the mechanistic pathway has not been identified. These injuries are associated with development of SUI (Goldberg et al. 2005). In this study, we used several simulated childbirth injuries to determine the effects on EUS and pudendal nerve function during filling CMG. Our recordings indicated that the bursting signal in the EUS EMG is transferred from the pudendal nerve motor branch with

Acknowledgments

This work was supported in part by NIH RO1 HD38679-08, the Cleveland Clinic, and the Rehabilitation Research and Development service of the Department of Veterans Affairs.

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