| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
ORIGINAL RESEARCH |
From the *Division of Urogynecology and Reconstructive Pelvic Surgery and Department of Neurology, Oregon Health and Science University, Portland, Oregon.
Address reprint requests to: W. Thomas Gregory, MD, Assistant Professor, Obstetrics and Gynecology, Division of Urogynecology and Reconstructive Pelvic Surgery, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, L466, Portland, OR 97239; e-mail: gregoryt{at}ohsu.edu.
 |
ABSTRACT |
|---|
TOP
 ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
METHODS: Standardized examinations were prospectively performed on 2 groups: 1) healthy nulliparous women without pelvic floor disorders (n = 28) and 2) asymptomatic women who were postpartum following vaginal delivery of their first child (n = 23). The examinations included pelvic organ prolapse quantification measurements, endoanal ultrasonography, pudendal nerve terminal motor latency, sacral reflexes, and concentric needle EMG using multiple motor unit action potential analysis.
RESULTS: A mean of 11.5 (standard deviation [sd] 1.1) weeks had elapsed since first vaginal deliveries in the postpartum group. The mean fetal weight at delivery was 3,495 (sd 458) grams. There were no sphincter defects seen by ultrasonography. Compared with the nulliparous women, pudendal nerve terminal motor latency and sacral reflexes (clitoral-anal reflex, urethral-anal reflex) were not increased in the postpartum group. Each of the quantitative parameters (duration, amplitude, area, turns, and phases), measured from motor unit action potentials in the postpartum group, were larger than in the nulliparous group (P 
.004, nested analysis of variance [ANOVA]).
CONCLUSION: Quantitative EMG using multiple motor unit action potential analysis can detect the presence after vaginal childbirth of subtle nerve injury not demonstrable by pudendal nerve terminal motor latency. Even asymptomatic women show evidence of pelvic floor nerve injury after uncomplicated deliveries.
LEVEL OF EVIDENCE: II-2
Now, because of advances in neurophysiologic hardware and software,14,18,19 quantitative concentric needle EMG is a feasible test to perform clinically for the pelvic floor. A pelvic floor muscle motor unit comprises a single nerve cell, its axon, and all the skeletal muscle fibers it serves (Fig. 1). A small needle electrode located near these muscle fibers detects the summated electrical potentials and displays it as a waveform called a motor unit action potential, much as surface electrodes do during electrocardiography. With nerve injury, there are often increases in the values in certain quantifiable waveform parameters, like duration and amplitude, as well as in descriptors of the waveform's complexity, such as the number of turns and phases it has (Fig. 2). 20 The aim of this study was to use an emerging technique called multiple motor unit action potential analysis to measure these quantitative parameters in the external anal sphincter and assess whether there is evidence of nerve injury after vaginal delivery.
|
|
|
MATERIALS AND METHODS |
|---|
|
TOP
ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
= 0.05, power = 0.80). The first group comprised 28 nulliparous nonpregnant women without uroneurologic or defecatory disorders (confirmed by questionnaire) who were recruited by flyers posted at the student health center at Portland State University and at local Planned Parenthood clinics. The second group comprised 23 women postpartum from a first vaginal delivery. They were also recruited by means of posted flyers from the Oregon Health and Science University clinics and from a local community obstetric practice at their 6-week postpartum visit and scheduled for an evaluation at 12 weeks postpartum. Both groups were recruited between July 2002 and August 2003. Examinations were performed by one examiner (W.T.G.), who was not masked to subject group. Women who were again pregnant, had active colitis, were dependent on a cardiac pacemaker, or were using heparin or warfarin were excluded. Each woman was modestly compensated for her participation. Because nerve regeneration proceeds at a rate of approximately 1 mm per day,22 a 12-week postpartum evaluation was chosen because we believed reinnervation would be well underway if nerve injury occurred at the ischial spine (8–10 cm away from the anal sphincter). Each woman completed a questionnaire designed to detect episodes of difficult bowel movements (using Rome II criteria)23 or anal incontinence to either gas, liquid, or solid stool.24 We performed a pelvic examination that included a pelvic organ prolapse quantification examination,25 clinical bulbocavernosus reflexes, and a clinical measure of strength using the adaptation of the Oxford muscle grading scale for pelvic muscles26 (0 = nothing, 1 = flicker, 2 = weak squeeze, 3 = moderate squeeze and lift, 4 = good squeeze and lift, 5 = strong squeeze and lift). The pelvic organ prolapse quantification was performed in a supine position at maximal valsalva. Methods, definitions, and descriptions conform to the standards recommended by the International Continence Society. Using a 10-MHz, 360° rotating endoanal probe (B-K Medical, Copenhagen, Denmark), we performed ultrasonography of the anal sphincter to document its integrity. Each subject then underwent a battery of comprehensive pelvic floor neurophysiologic examinations.
We electrically grounded the study subject by placing a grounding pad at the inner thigh. Using the specially designed single-use St. Mark's electrode (Medtronic Corporation, Minneapolis, MN) which fits over the second digit of the gloved examining hand, we stimulated the pudendal nerve transvaginally at the ischial spine with 0.1 millisecond square waves of varying amplitudes (to supramaximal levels) until reproducible compound muscle action potentials (CMAPs) were recorded with surface electrodes placed over the external anal sphincter. The time interval between the stimulus and the onset of the CMAP for the anal sphincter is called the pudendal nerve terminal motor latency. Those CMAPs without a clearly identifiable flat baseline before the onset of the action potential were discarded because of the difficulty in determining the latency. We also recorded the perineal nerve terminal motor latency for the perineal branch of the pudendal nerve to the external urethral sphincter during the same stimulus by simultaneously recording its CMAP on another channel using a specially designed ring surface electrode fitted into the urethra over a standard Foley catheter.
We also studied 2 multisynaptic reflexes to observe electrical conduction over the entire afferent and efferent reflex arc, rather than just the efferent signal along the distal pudendal nerve. Similarly to the clinically observed bulbocavernosus reflex, we obtained the latency of the electrically induced clitoral-anal reflex by using surface-stimulating electrodes paraclitorally and recording electrodes positioned at the mucocutaneous junction of the anal mucosa as for the pudendal nerve terminal motor latency. For the urethral-anal reflex, the Foley catheter fitted with a ring electrode previously used as a recording electrode for perineal nerve terminal motor latency became the stimulating electrode. The recording surface electrodes remained positioned at the same anal location.
Short (0.1 millisecond) dual impulses (5-millesecond interstimulus interval) of increasing currents were given at the clitoris or the urethra until the subject was just able to sense it. For both the clitoral-anal and the urethral-anal reflex, the amplitude was increased to 4 times sensory threshold. At that stimulus level, an identifiable complex reflex wave was detected reproducibly and the latency measured.
We performed concentric needle EMG of the superficial and deeper portions of the external anal sphincter in a manner similar to that described by Podnar.27 We recorded approximately 20 unique motor unit action potentials from the right external anal sphincter and 20 from the left external anal sphincter (3 o'clock and 9 o'clock positions on the external anal sphincter) from each subject in the following manner. Each subject remained electrically grounded as described above. Following approximately 20 minutes of EMLA (eutectic mixture of local anesthetics cream) (AstraZeneca, Wilmington, DE) application, we located the external anal sphincter digitally and inserted a 37-mm long standard concentric EMG needle (Medtronic Inc, Minneapolis, MN) in a direction perpendicular to the muscle fibers until crisp EMG activity was detected (Fig. 1). Filter settings were 5 Hz to 10 kHz; the gain was 100–500 µV/div, and the sweep speed was 10 ms/div. We instructed the subject to relax her pelvic floor as feasible. If we noted that the level of motor unit activity was too high, we instructed her to "bear down" lightly as if she were having a bowel movement to facilitate relaxation of the external anal sphincter. Rarely, when only a single motor unit was audible, we instructed her to lightly squeeze her pelvic floor muscles and hold it, as if trying to prevent the inadvertent passage of flatus. We sampled 4–5 unique sites on each side of the external anal sphincter by advancing the needle approximately 0.5 cm in a direction perpendicular to the longitudinal direction of the muscle fiber. We also tested the ability to recruit more motor units with increasing muscle force by asking the subject to squeeze the muscles of her pelvic floor as tightly as possible or perform a cough. We digitally recorded the signal on a Sony TCD-D7 DAT recorder (Sony Corporation, Tokyo, Japan) and analyzed it using the multiple motor unit action potential software on a Medtronic Keypoint (Medtronic, Inc, Minneapolis, MN) system after the completion of the experimental protocol. The time stamp on the DAT recorder was noted with each new site to ensure that the multiple motor unit action potential analysis, performed from the DAT recording, acquired motor units from different areas in the muscle and prevented the resampling of the same motor unit.
The multiple motor unit action potential algorithm on the EMG machine automatically obtained the following parameters (Fig. 2): amplitude (positive peak to negative peak), duration (initial, main spike, and terminal portions), area (under the entire delineated waveform), area/amplitude ratio (also known as "thickness"), phases (baseline crossings plus one), and turns (shifts in waveform directions of a minimum voltage).19,20 Any motor unit action potential with an unstable baseline was discarded because this precluded accurate analysis. No further user interaction was required for determination of these quantitative parameters.
We used SPSS 11.0 (SPSS Inc, Chicago, IL) for statistical analysis. Comparisons of the means for continuous data were made with Student t tests. Many of the motor unit action potential parameters were not normally distributed. Therefore, before statistical calculations, we performed log-transformations and checked for normal distribution both visually and with the Kolmogorov-Smirnov test. Motor unit action potential parameters from each group were then compared using a nested ANOVA design to control for fixed and random effects in this study design, which retrieved multiple unique values from a given study subject in 2 different cohorts. The fixed effects were study group and muscle side, with the random effects being study subject and motor unit action potential. The nesting design placed motor unit action potential within muscle side, which was nested within study subject, which was ultimately nested within the study group. Other continuous data with fewer observations that were not normally distributed were compared using Mann-Whitney U tests. Categorical data were compared using 
2 or Fisher exact test, as indicated.
|
RESULTS |
|---|
|
TOP
ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
|
The pelvic organ prolapse quantification examinations in the postpartum women were significantly different from those in the nulliparous women. In the postpartum women, there was greater descent in all vaginal compartments (Table 2). The relative change was most striking in the anterior compartment (measurements Aa and Ba, P < .001, Mann-Whitney) and at the vaginal introitus (measurement gh, P < .001, Mann-Whitney). Additionally, the pelvic floor muscle strength was significantly lower than that in the nulliparous group (P = .001, Mann-Whitney).
|
Each of the nerve conduction evaluations demonstrated no difference between the groups (Table 3). Pudendal nerve terminal motor latencies were not reproducibly obtainable in 18% of the nulliparous subjects and 35% of the postpartum subjects. One nulliparous subject and 2 postpartum subjects requested that we not perform the sacral reflexes (the last tests performed in the study protocol). However, in the remainder of the subjects the clitoral-anal and urethral-anal reflexes were easily recorded.
|
Unlike the pudendal nerve terminal motor latency, motor unit action potential samples for quantitative EMG were obtainable from every study subject. Each of the measured values for quantitative EMG parameters obtained by the multiple motor unit action potential method was significantly larger (P < .001, nested ANOVA) in the postpartum group than in the nulliparous group (Table 3). These data are consistent with evidence of pudendal nerve injury to the anal sphincter. There were no differences in any of the values between the left and right side of the muscle in either group (nested ANOVA). Also, no statistically significant correlation was noted between the quantitative EMG parameters and fetal weight or stage 2 length (Pearson correlation) or between EMG parameters and episiotomy or degree of perineal laceration (Spearman correlation). Finally, no subject had demonstrable fibrillations or positive waves.
|
DISCUSSION |
|---|
|
TOP
ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Our findings of no change in pudendal nerve terminal motor latency in 12-week postpartum women compared with nulliparous controls concur with similar studies performed at 8 weeks postpartum by Snooks et al5,7 and several years later by Allen et al.15 Although several investigators have shown that women specifically referred for urinary and fecal incontinence have elevations in the pudendal nerve terminal motor latency,28,33 few show that vaginal delivery itself is associated with persistent prolongations of this terminal motor latency. Snooks showed that, although a large percentage of women had an increase in pudendal nerve terminal motor latency 48 hours postpartum, most had returned to normal by 8 weeks. Nonetheless, using single-fiber EMG, Snooks demonstrated that the "fiber-density" of the anal sphincter was increased compared with controls. However, when he analyzed only vaginally delivered primiparous women, there was neither an alteration in pudendal nerve terminal motor latency nor any change in fiber density, differences that were isolated to the multiparous or forceps-delivered women. In contrast to Snooks, vaginally primiparous women in our study had evidence of subtle nerve injury as measured by quantitative concentric needle EMG using multiple motor unit action potential analysis. The sensitivity of the newer technique is further underscored by the fact that the current study evaluated women after essentially uncomplicated, unassisted vaginal deliveries (one outlet vacuum), whereas 50% of the primiparous women in Snooks’ report were delivered by forceps.
In 2 other studies of nerve injury during childbirth, Smith et al34 also documented increased fiber density (single-fiber EMG) in multiparous women, whereas Allen et al15 found that quantitative concentric needle EMG in primiparous women provided evidence of pelvic nerve injury. In both these reports, needle EMG was performed on the pubococcygeus, which is innervated by direct branches of the sacral trunks.35 In contrast, both our study and Snooks et al's single-fiber EMG work5 were performed on the external anal sphincter, supplied by the pudendal nerve.
Using multiple motor unit action potential algorithms for concentric needle quantitative EMG, Podnar et al27 also investigated the role that vaginal delivery plays in pudendal nerve damage by examining the external anal sphincter. By comparing motor unit action potential parameters between a group of 18 nulliparous women (median age 39.5 years) and a group of 26 multiparous women (median age 46 years) who were a median of 22 years out from delivery, he was unable to demonstrate any difference and concluded that his study did not support the notion that injury to the innervation of the external anal sphincter occurs in uncomplicated deliveries. The differences in quantitative parameters seen in the current study and not seen in Podnar's may reflect the ongoing changes associated with evolving reinnervation that would be expected at 12 weeks postinjury. As axons in new motor units mature and regain more myelin, the temporal dispersion often seen during reinnervation (thereby affecting the motor unit action potential duration) may resolve. Serial quantitative EMG studies are necessary to define better the evolution of repair and determine whether differences seen in this study disappear. Although it is also feasible that technique differences might explain the incongruent findings, the current study was purposefully performed with the same manufacturer's EMG machine, with the same multiple motor unit action potential algorithm, and with the same protocol for performing needle EMG of the anal sphincter as used by Podnar et al.27
Whereas we demonstrated evidence of nerve injury by the quantitative EMG techniques, both nulliparous women and postpartum women had equivalent pudendal nerve terminal motor latencies of 2.2 milliseconds. Our study was designed to detect differences in the EMG parameters, and at the sample size reported, we had 80% power to demonstrate 0.2 millisecond difference in pudendal nerve terminal motor latency between the groups. Based on previous reports,36 a difference of no greater than 0.1 millisecond was to be expected. Also, in 35% of the postpartum women and 18% of nulliparous women, reproducible CMAPs could not be obtained. Occasionally, a CMAP in these individuals would appear but would not be reproducible with subsequent stimulations at the same location using the same settings. More often, however, a seemingly reproducible action potential would appear, but a stable baseline would not be present before the reproducible action potential. The short latency between the stimulus and the onset of the CMAP, combined with the typically low amplitude responses and the need for increasing voltage for stimulus, lent itself to so-called volume conduction. This tended to obscure the take-off of the true onset of the CMAP. To increase the likelihood of picking up the poorly reproducible response and to ensure that the recording electrodes were always situated in close proximity to the anal sphincter, we used separate surface electrodes at the anal sphincter and used the St. Mark's electrode transvaginally as a stimulator only. Despite these maneuvers to improve the reproducibility of the test, it is not surprising that we were unable to obtain responses in some subjects, because this is in concert with the findings of nearly 15 years of experience with this test.16 Therefore, given that 1) pudendal nerve terminal motor latency is poorly reproducible, 2) pudendal nerve terminal motor latency is prolonged only when the largest and most heavily myelinated axons are damaged, 3) sacral reflex testing is an alternate indirect measure of peripheral nerve conduction, and 4) multiple motor unit action potential analysis is now a quickly obtainable and objective measure of pelvic floor nerve injury, the pudendal nerve terminal motor latency may have little added benefit in the evaluation of pelvic floor disorders.
The presence of subtle nerve injury to the anal sphincter, as seen in this study, may serve to accelerate the normal effects of aging. In most appendicular skeletal muscle, there is a reduction of isometric strength of 1.5% per year.37 Although disuse atrophy with aging is the cause of some of the loss in strength, "sarcopenia" resulting from motor unit loss38 and muscle fiber shrinkage39 has been implicated. Groups of patients who have compromised neuromuscular systems, such as those with postpolio or Down syndrome, may show strength loss prematurely when the combined effects of the motor neuron disease and the normal effects of aging are combined. Although certainly not as dramatic, this may serve as an explanation for the fact that symptoms of fecal incontinence are not seen until many years after an initial insult from vaginal delivery (or cumulative effect with multiple deliveries). With successfully reinnervated muscle, each nerve cell innervates more muscle fibers than in muscle that has not sustained injury to its nerve supply (Fig. 1). As neurons are lost incrementally with aging, proportionally more muscle fibers are lost, because each successfully reinnervated motor unit has a greater ratio of muscle fibers per neuron. Many more muscle fibers, along with strength and function, would be lost earlier than in the uninjured patient. For the pelvic floor, this could contribute to loss in both pelvic organ support and continence.
A commonly postulated theory for the mechanism of pudendal nerve injury after vaginal delivery is that the pudendal nerve stretches with fetal descent from its fixed and tethered point at the ischial spine. Another theory is that the pressure of the fetal head against the pelvic sidewall may cause compression of the nerve. In the sphincters (urethral and anal), as well as the levator ani, injury to the small intramuscular terminal axons or the neuromuscular junction might also occur. Although needle EMG is capable of determining evidence of nerve injury, further experimental studies using an appropriate animal model32,40 will likely be required to localize and more specifically characterize the injury following child birth.
Finally, although this study shows aggregate evidence of nerve damage resulting from routine vaginal delivery, it is not large enough to define which obstetric practices or maternal or fetal characteristics lead to increased pelvic floor nerve injury. It also fails to answer whether simply carrying a pregnancy produces the same effect, because these patients all delivered vaginally and there were no patients who underwent a cesarean delivery. Furthermore, a nonblinded study has the potential for operator bias, but the multiple motor unit action potential analysis, as defined in the protocol, has the advantage of minimizing operator bias.18,41 Except when the baseline is unstable, the computer algorithm not only selects the multiple motor unit action potentials, but also calculates the motor unit action potential parameters. The test-retest and interrater reproducibility of the technique has been demonstrated,18,41 and the anal sphincter needle examination itself is standardizable.27 Therefore, quantitative EMG using multiple motor unit action potential analysis should be an essential component of neurophysiologic studies of pelvic floor disorders.
|
Footnotes |
|---|
Sources of funding: National Institutes of Health/The National Institute of Child Health and Human Development, Women's Reproductive Health Research Scholarship (NIH K12 HD-01243, PI Joanna Cain, md) and the Medical Research Foundation of Oregon.
10.1097/01.AOG.0000134527.07034.81
|
REFERENCES |
|---|
|
TOP
ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
2. Sorensen M, Tetzschner T, Rasmussen OO, Bjarnesen J, Christiansen J. Sphincter rupture in childbirth. Br J Surg 1993;80:392–4.[Medline]
3. Crawford LA, Quint EH, Pearl ML, DeLancey JO. Incontinence following rupture of the anal sphincter during delivery. Obstet Gynecol 1993;82:527–31.[Medline]
4. Donnelly V, Fynes M, Campbell D, Johnson H, O'Connell PR, O'Herlihy C. Obstetric events leading to anal sphincter damage. Obstet Gynecol 1998;92:955–61.[Abstract]
5. Snooks SJ, Setchell M, Swash M, Henry MM. Injury to innervation of pelvic floor sphincter musculature in childbirth. Lancet 1984;2:546–50.[Medline]
6. Snooks SJ, Henry MM, Swash M. Faecal incontinence due to external anal sphincter division in childbirth is associated with damage to the innervation of the pelvic floor musculature: a double pathology. Br J Obstet Gynaecol 1985;92:824–8.[Medline]
7. Snooks SJ, Swash M, Henry MM, Setchell M. Risk factors in childbirth causing damage to the pelvic floor innervation. Int J Colorectal Dis 1986;1:20–4.[Medline]
8. Snooks SJ, Swash M, Mathers SE, Henry MM. Effect of vaginal delivery on the pelvic floor: a 5-year follow-up. Br J Surg 1990;77:1358–60.[Medline]
9. Snooks SJ, Swash M, Henry MM. Abnormalities in central and peripheral nerve conduction in patients with anorectal incontinence. J R Soc Med 1985;78:294–300.[Abstract]
10. Sultan AH, Stanton SL. Occult obstetric trauma and anal incontinence. Eur J Gastroenterol Hepatol 1997;9:423–7.[Medline]
11. Hordnes K, Bergsjo P. Severe lacerations after childbirth. Acta Obstet Gynecol Scand 1993;72:413–22.[Medline]
12. Kammerer-Doak DN, Wesol AB, Rogers RG, Dominguez CE, Dorin MH. A prospective cohort study of women after primary repair of obstetric anal sphincter laceration. Am J Obstet Gynecol 1999;181:1317–22; discussion 1322–3.[Medline]
13. Abramowitz L, Sobhani I, Ganansia R, Vuagnat A, Benifla JL, Darai E, et al. Are sphincter defects the cause of anal incontinence after vaginal delivery? Results of a prospective study. Dis Colon Rectum 2000;43:590–6; discussion 596–8.[Medline]
14. Podnar S, Lukanoviè A, Vodu
ek DB. Anal sphincter electromyography after vaginal delivery: neuropathic insufficiency or normal wear and tear? Neurourol Urodyn 2000;19:249–57.[Medline]
15. Allen RE, Hosker GL, Smith AR, Warrell DW. Pelvic floor damage and childbirth: a neurophysiological study. Br J Obstet Gynaecol 1990;97:770–9.[Medline]
16. Hill J, Hosker G, Kiff ES. Pudendal nerve terminal motor latency measurements: what they do and do not tell us. Br J Surg 2002;89:1268–9.[Medline]
17. Daube J. Needle examination in clinical electromyography. AAEM Minimonograph #11. Muscle Nerve 1991;14:685–700.[Medline]
18. Stalberg E, Falck B, Sonoo M, Stalberg S, Astrom M. Multi-MUP EMG analysis–a two year experience in daily clinical work. Electroencephalogr Clin Neurophysiol 1995;97:145–54.[Medline]
19. Stalberg E, Nandedkar SD, Sanders DB, Falck B. Quantitative motor unit potential analysis. J Clin Neurophysiol 1996;13:401–22.[Medline]
20. Stalberg E, Andreassen S, Falck B, Lang H, Rosenfalck A, Trojaborg W. Quantitative analysis of individual motor unit potentials: a proposition for standardized terminology and criteria for measurement. J Clin Neurophysiol 1986;3:313–48.[Medline]
21. Weidner AC, Sanders DB, Nandedkar SD, Bump RC. Quantitative electromyographic analysis of levator ani and external anal sphincter muscles of nulliparous women. Am J Obstet Gynecol 2000;183:1249–56.[Medline]
22. Gutmann E. Histology of degeneration and regeneration. In: Licht SH, editor. Electrodiagnosis and electromyography. 3rd ed. New Haven (CT): E. Licht; 1971. p. 113–33.
23. Thompson WG, Longstreth GF, Drossman DA, Heaton KW, Irvine EJ, Muller-Lissner SA. Functional bowel disorders and functional abdominal pain. Gut 1999;45 suppl 2:II43–7.
24. Weber AM, Abrams P, Brubaker L, Cundiff G, Davis G, Dmochowski RR, et al. The standardization of terminology for researchers in female pelvic floor disorders. Int Urogynecol J Pelvic Floor Dysfunct 2001;12:178–86.[Medline]
25. Bump RC, Mattiasson A, Bo K, Brubaker LP, DeLancey JO, Klarskov P, et al. The standardization of terminology of female pelvic organ prolapse and pelvic floor dysfunction. Am J Obstet Gynecol 1996;175:10–7.[Medline]
26. Laycock J. Clinical evaluation of the pelvic floor. In: Schussler B, Laycock J, Norton P, Stanton S, editors. Pelvic floor re-education: principles and practice. New York (NH): Springer-Verlag; 1994. p. 42–8.
27. Podnar S, Rodi Z, Lukanovic A, Trsinar B, Vodusek DB. Standardization of anal sphincter EMG: technique of needle examination. Muscle Nerve 1999;22:400–3.[Medline]
28. Kiff ES, Swash M. Slowed conduction in the pudendal nerves in idiopathic (neurogenic) faecal incontinence. Br J Surg 1984;71:614–6.[Medline]
29. Parks AG, Swash M, Urich H. Sphincter denervation in anorectal incontinence and rectal prolapse. Gut 1977;18:656–65.
30. Gilpin SA, Gosling JA, Smith AR, Warrell DW. The pathogenesis of genitourinary prolapse and stress incontinence of urine: a histological and histochemical study. Br J Obstet Gynaecol 1989;96:15–23.[Medline]
31. Lin AS, Carrier S, Morgan DM, Lue TF. Effect of simulated birth trauma on the urinary continence mechanism in the rat. Urology 1998;52:143–51.[Medline]
32. Damaser MS, Broxton-King C, Ferguson C, Kim FJ, Kerns JM. Functional and neuroanatomical effects of vaginal distention and pudendal nerve crush in the female rat. J Urol 2003;170:1027–31.[Medline]
33. Laurberg S, Swash M, Snooks SJ, Henry MM. Neurologic cause of idiopathic incontinence. Arch Neurol 1988;45:1250–3.[Abstract]
34. Smith AR, Hosker GL, Warrell DW. The role of partial denervation of the pelvic floor in the aetiology of genitourinary prolapse and stress incontinence of urine: a neurophysiological study. Br J Obstet Gynaecol 1989;96:24–8.[Medline]
35. Barber MD, Bremer RE, Thor KB, Dolber PC, Kuehl TJ, Coates KW. Innervation of the female levator ani muscles. Am J Obstet Gynecol 2002;187:64–71.[Medline]
36. Sultan AH, Kamm MA, Hudson CN. Pudendal nerve damage during labour: prospective study before and after childbirth. Br J Obstet Gynaecol 1994;101:22–8.[Medline]
37. Vandervoort AA. Aging of the human neuromuscular system. Muscle Nerve 2002;25:17–25.[Medline]
38. Brown WF, Strong MJ, Snow R. Methods for estimating numbers of motor units in biceps-brachialis muscles and losses of motor units with aging. Muscle Nerve 1988;11:423–32.[Medline]
39. Essen-Gustavsson B, Borges O. Histochemical and metabolic characteristics of human skeletal muscle in relation to age. Acta Physiol Scand 1986;126:107–14.[Medline]
40. Otto LN, Slayden OD, Clark AL, Brenner RM. The rhesus macaque as an animal model for pelvic organ prolapse. Am J Obstet Gynecol 2002;186:416–21.[Medline]
41. Podnar S, Vodusek DB, Stalberg E. Comparison of quantitative techniques in anal sphincter electromyography. Muscle Nerve 2002;25:83–92.[Medline]
This article has been cited by other articles:
|
|
 |
|
  A. Spydslaug, L. I.S. Trogstad, A. Skrondal, and A. Eskild Recurrent Risk of Anal Sphincter Laceration Among Women With Vaginal Deliveries Obstet. Gynecol., February 1, 2005; 105(2): 307 - 313. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
