Levator ani denervation and reinnervation 6 months after childbirth

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Levator ani denervation and reinnervation 6 months after childbirth Mary M. T. South, MD; Sandra S. Stinnett, DrPH; Donald B. Sanders, MD; Alison C. Weidner, MD OBJECTIVE: The objective of the study was to assess the prevalence of

RESULTS: Of 57 subjects, 70% had no denervation. Of the 30% with

levator ani denervation and reinnervation 6 months after the first delivery.

denervation at 6 weeks, 35% recovered by 6 months. Obstetric or maternal characteristics were not predictive of denervation or reinnervation, except subjects with persistent denervation tended toward lower body mass index (BMI) independent of mode of delivery.

STUDY DESIGN: Ninety-six primigravida women underwent quanti-

tative electromyography of the levator ani during the third trimester and twice postpartum. A 95% confidence interval for normal function was created using interference pattern analysis. Fifty-seven who completed the study are presented in this secondary data analysis. Postpartum muscle sites outside the normal range were considered abnormal. Obstetric and demographic characteristics were assessed.

CONCLUSION: Nearly one-third of women have levator ani denervation after

first delivery, but many recover by 6 months. Denervation is not clearly associated with mode of delivery, but higher maternal BMI may be protective. Key words: Delivery, levator ani, neuromuscular function, pelvic floor, quantitative electromyography

Cite this article as: South MMT, Stinnett SS, Sanders DB, et al. Levator ani denervation and reinnervation 6 months after childbirth. Am J Obstet Gynecol 2009;200:519.e1-519.e7.

I

njury to the pelvic floor at the time of childbirth and its role in the pathophysiology of pelvic floor dysfunction is a contemporary issue of interest in women’s health.1,2 The National Institute of Child Health and Development funds the Pelvic Floor Disorders Network, which was formed in 2001 to conduct research that would ultimately improve the care and quality of life for women with pelvic organ prolapse and bowel and bladder dysfunction. In March 2006, a National Institutes of Health State-ofthe-Science Conference statement was

From the Division of Urogynecology and Pelvic Reconstructive Surgery, Department of Obstetrics and Gynecology (Drs South and Weidner); the Department of Biostatistics and Bioinformatics (Dr Stinnett); and the Division of Neurology, Department of Medicine (Dr Sanders), Duke University Medical Center, Durham, NC. Received June 24, 2008; revised Dec. 1, 2008; accepted Dec. 22, 2008. Reprints not available from the authors. This study was supported in part by National Institutes of Health Grant HD38661-05 and the Charles Hammond Research Fund. 0002-9378/$36.00 © 2009 Mosby, Inc. All rights reserved. doi: 10.1016/j.ajog.2008.12.044

published on cesarean delivery on maternal request.3 This has been an area of heated debate over the past several years with the increased attention and focus on the rising US cesarean delivery rates, which includes a rise in cesarean request to approximately 4-18% of all cesarean deliveries.3 Urinary and fecal incontinence as well as pelvic organ prolapse may be associated with vaginal birth. Patient satisfaction with the birth process and quality of life postpartum are important factors to consider when determining the mode of delivery. However, support for or against cesarean delivery on maternal request for the aforementioned outcomes and others is based on weak quality data, necessitating further research.3 Multiple studies have supported an association between vaginal parity and neuromuscular abnormalities in the levator ani and external anal sphincter.1,4-8 Morphologic abnormalities in the levator ani are consistently observed in vaginally parous women as shown by magnetic resonance2 and ultrasound studies,4 and muscle loss in these women is associated with an increased risk of pelvic organ prolapse.9,10 Other recent investigations have shown a connection between levator ani

muscle denervation and prolapse using both magnetic resonance imaging and quantitative analysis of needle electromyography (QEMG).7,10 However, the prevalence and specific mechanism of permanent pelvic floor denervation injury after a single typical obstetrical delivery as well as the nature and extent of any resulting dysfunction are not clear. Others have used techniques such as surface electromyography (EMG), which is of limited precision and localization for the levator ani, a muscle directly palpated only on internal pelvic examination.11 Ideally, providers of health care to women would like to be able to predict which patient was at greatest risk of significant pelvic floor injury were she to undergo vaginal delivery. Such knowledge would possibly help us counsel patients about defined risks of different modes of delivery. We undertook this research to obtain pilot data toward an ultimate goal of defining those risk factors. We applied a fairly invasive examination technique to measure levator ani neuromuscular function in a cohort of primiparous women. We previously reported an approach to analyzing this data set.12 Our goal with this report is to simplify the statistical approach with an ultimate future goal of maximizing clinical appli-

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Urogynecology

cation of the technique. We applied this analysis method to identify the type and prevalence of levator denervation and reinnervation and the obstetrical and demographic characteristics of women with such changes.

M ATERIALS AND M ETHODS Primigravid women who presented to the Duke obstetrical clinics from 2001 to 2004 were approached to participate in this study after receipt of full institutional review board approval. We recruited singleton primigravidas less than 34 weeks’ gestational age who denied a history of pelvic surgery, prepregnancy pelvic floor symptoms, diabetes, or neuromuscular disorder. Because we wanted to study the effects of a trial of labor in as many subjects as possible, we excluded women who planned a cesarean delivery in advance of delivery (eg, a woman with maternal cardiac contraindication to labor).

EMG acquisition and analysis At 28-34 weeks’ gestation, subjects underwent baseline concentric needle EMG assessment of the levator ani muscles and analysis of the resulting digital EMG data as previously described.12,13 Briefly, the levator ani were palpated transvaginally at 2 defined points on each side intended to correspond to the puboviceralis and iliococcygeous portions of the muscle. EMG signals were recorded from these sites using a concentric needle electrode with the recording territory of the muscle at rest and with moderate and maximal activity using a Synergy 2-channel electromyograph (Oxford Instruments Medical Systems, Hawthorne, NY). This same EMG assessment was performed again at 6 weeks and 6 months postpartum. A pelvic organ prolapse quantitation (POPQ)14 and a clinical assessment of voluntary pelvic floor contraction was also performed.15 We used interference pattern analysis to analyze the EMG data. This is a widely accepted method for testing neuromuscular integrity that can used when the load against which the muscle is contracting is not measurable.16-18 For each subject, we sampled the digitally recorded signals at each muscle site during 519.e2

www.AJOG.org six 50 millisecond epochs of representative muscle activity to obtain the number of turns per second and mean turns amplitude at rest and during moderate and maximal contraction effort as previously reported.12 We pooled all QEMG data from the baseline antepartum visit in 70 subjects (those in the final analysis group) and confirmed that the data were normally distributed. We simplified the data by taking the ratio of the 2 main QEMG variables16 as follows: (number of turns per second)/(amplitude in microvolts), abbreviated here as (T/A). In these 70 subjects, the normal range of T/A (including 95% of all observations) was 0.46-1.2, inclusive of both extremes. We applied this normal range in the same group after delivery. We excluded those subjects who did not have resting and contracting T/A within the normal range in at least 3 of 4 muscle sites at the antepartum visit. At the subsequent 6 week and 6 month postpartum visits, we calculated the mean and the 95% confidence intervals for T/A for each subject at each muscle site. Each site was assessed to determine whether it was judged normal or abnormal at either postpartum visit. A site was considered to be abnormal if the entire 95% confidence interval of T/A was outside the normal range. Muscle site data that were even partially within the normal range were considered normal for that site. Furthermore, any subject with missing or uninterpretable data postpartum at any site was excluded. This ensured that to be characterized as abnormal, a subject’s levator muscle EMG was clearly abnormal compared with antepartum values. We further characterized muscle sites postpartum as having a low T/A if the 95% confidence interval of the value was less than the lower limit of normal and a high T/A if the 95% confidence interval value exceeded the upper limit of normal. If any of the 4 levator muscle sites were determined to have a low or high T/A, the subject was declared abnormal at that visit. If the levator EMG was determined to be abnormal at both the 6 week and 6 month visits, the denervation change was characterized as persistent. If

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neuromuscular function was abnormal at 6 weeks but normal at 6 months, the injury was considered recovered and consistent with reinnervation.

Obstetrical measures Each subject’s labor and delivery were managed by her obstetrician, following a protocol conforming to accepted practices of active management of labor.19 The decision of whether to use regional anesthetic was left to the subject and her physician, although once placed, epidurals were managed using a standard protocol of ropivicaine/fentanyl-loading dose and a subject-controlled analgesic pump. Routine episiotomy was not performed. Statistical analysis The frequency of levator muscle EMG abnormalities was computed for both the 6 week and 6 month visits. The odds ratios of abnormal levator EMG by race (African American vs white) adjusted for age, along with the 95% confidence intervals, were computed. For subjects at the 6 month visit, any abnormality was determined to be either reinnervated or persistent denervation and the frequency of types of denervation/reinnervation computed. Obstetrical, neonatal, or maternal characteristics for the normal, reinnervated, or persistent denervation groups were computed. We used the Wilcoxon rank sum test or Fisher’s exact test to compare groups. Because there appeared to be a trend in higher body mass index (BMI; in kilograms per square meter) for postpartum subjects with normal or recovered levators, we performed logistic regression to assess the effect of BMI on levator status by combining subjects into 3 groups with similar mode of delivery.

R ESULTS Ninety-six primigravidas were enrolled. Enrollment and analysis of the 96 are summarized in Figure 1. Eleven subjects did not meet the inclusion criterion of having resting and maximum contraction T/A values within the normal range for at least 3 of 4 muscle sites at the antepartum visit. Fifty-seven subjects com-

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FIGURE 1

Enrollment and disposition of subjects in the study

South. Levator ani denervation and reinnervation 6 months after childbirth. Am J Obstet Gynecol 2009.

pleted the final visit at 6 months postpartum and were included in the analysis. Notably, none of these 57 had missing or uninterpretable data at any site after delivery. Of these 57, 17 (30%) had QEMG evidence of levator ani abnormality at 6 weeks, and 23 (40%) met criteria for ab-

normality at 6 months postpartum. When the T/A ratio was abnormal, it was below the normal range in 88.9% of subjects at 6 weeks and 86.7% of subjects at 6 months postpartum, most consistent with a denervation injury to the neuromuscular complex.20

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Table 1 demonstrates the racial distribution of the subjects and levator denervation frequency at 6 weeks and 6 months. Although not statistically significant, African American women showed a tendency toward a lower rate of denervation at both visits. The majority of women with denervation at 6 weeks had persistent denervation at 6 months by our QEMG criteria. Neither age nor race was found to be clearly associated with denervation or reinnervation in this pilot cohort. The mode of delivery compared with denervation is shown in Table 2. We found no clear difference in denervation rates between cesarean delivery (with or without labor) when compared with vaginal delivery. We pursued this further by dividing our subjects into groups we considered relevant based on published literature21,22 and found the following denervation rates at 6 months: 2 denervated of 10 (20%) who had easy vaginal delivery with second stage of labor less than 30 minutes; 7 denervated of 15 (47%) who had second stage 30 or more minutes and neonatal head circumference less than 34.5 cm; 7 denervated of 18 (39%) who had difficult vaginal delivery with second stage 30 or more minutes and neonatal head circumference 34.5 cm or greater; 4 denervated of 8 (50%) who had cesarean in labor; and 3

TABLE 1

Demographics of subjects with levator denervation If denervated at 6 wk Maternal demographics

n

Denervation, 6 wk, n (%)

Denervation, 6 mo, n (%)

Reinnervated, n (%)

Persistent, n (%)

White

40

15 (38)

19 (48)

5 (33)

10 (67)

African American

11

2 (18)

2 (18)

1 (50)

1 (50)

................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................

Asian

4

0

1 (25)

0

0

Hispanic

1

0

1 (100)

0

0

................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................

Other

1

Overall

57

17 (30)

0

23 (40)

0

OR of denervation (adjusted)

n

OR (95% CI)

n, OR (95% CI)

0

0

................................................................................................................................................................................................................................................................................................................................................................................

6 (35)

11 (65)

................................................................................................................................................................................................................................................................................................................................................................................ .......................................................................................................................................................................................................................................................................................................................................................................

Race: African American vs white

11 vs 40

0.3 (0.04-1.8)

11 vs 40, 0.2 (0.04-1.3)

Age: ⬎ 30 y vs ⱕ 30 y

24 vs 27

1.5 (0.4-5.5)

24 vs 27, 1.2 (0.4-4.4)

................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................

CI, confidence interval; OR, odds ratio. South. Levator ani denervation and reinnervation 6 months after childbirth. Am J Obstet Gynecol 2009.

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TABLE 2

Obstetric delivery type and frequency of levator denervation If denervated at 6 wk Obstetric delivery Cesarean in labor

n

Denervation, Denervation, Reinnervated, Persistent, 6 wk, n (%) 6 mo, n (%) n (%) n (%)

8

3 (37)

4 (50)

0

3 (100)

..............................................................................................................................................................................................................................................

Elective cesarean

6

1 (17)

3 (50)

0

1 (100)

Difficult vaginal delivery

18

9 (50)

7 (39)

5 (56)

4 (44)

Longer second-stage vaginal delivery

15

3 (20)

7 (47)

0

3 (100)

Easy vaginal delivery

10

1 (10)

2 (20)

1 (100)

Overall

57 17 (30)

23 (40)

6 (35)

P value

.167

.650

.140

.............................................................................................................................................................................................................................................. a ..............................................................................................................................................................................................................................................

..............................................................................................................................................................................................................................................

0

..............................................................................................................................................................................................................................................

11 (65)

.............................................................................................................................................................................................................................................. a ..............................................................................................................................................................................................................................................

Difficult denotes deliveries with second stage at ⱖ 30 minutes and neonatal head circumference of ⱖ 34.5 cm. Longer second stage deliveries denote those with smaller infant head circumference but similar duration of labor. Easy vaginal delivery denotes those with second stage of labor ⬍ 30 minutes, regardless of head circumference a

P value based on Fisher exact test. South. Levator ani denervation and reinnervation 6 months after childbirth. Am J Obstet Gynecol 2009.

denervated of 6 (50%) who had cesarean without labor. We found no significant differences in levator denervation between these groups, but it is interesting to note that subjects with an easy vaginal delivery group had the lowest percentage of levator denervation at 6 weeks, and women with difficult deliveries that were completed vaginally had the highest. Other groups that could have been expected to have variable impact on the levator without actual delivery per vagina fell in between. Table 3 demonstrates the relationship of relevant obstetrical, neonatal, and maternal characteristics to levator status. We found no significant differences in these characteristics between subjects with normal and recovered levator ani muscles postpartum to those with persistence of denervation at 6 months. However, we were interested to note the apparent lower BMI in subjects with persistent levator denervation. We combined all 57 subjects into 3 groups with similar delivery experiences as described above: (1) vaginal deliveries that were easy with those of second stage longer than 30 minutes, (2) all cesareans, and (3) difficult vaginal deliveries. We noted a trend toward higher maternal BMI in the subjects with normal or reinnervated levators at 6 months in all 3 delivery groups as demonstrated in Figure 519.e4

2, although it approached statistical significance only in the cesarean group (P ⫽ .07).

C OMMENT Overall, 30% of primiparous women in our study suffered electromyographically detectable abnormality consistent with denervation of the levator ani at 6 weeks postpartum. The fraction of subjects with detectable abnormality at 6 months postpartum actually increased to 40%. We believe that this pattern is best explained by the EMG changes expected following neurogenic motor unit injury. Following neurogenic injury, reinnervation of denervated muscle fibers occurs via peripheral sprouting from uninjured nerve terminals. This increases the fiber density as the motor unit recovers from the injury, resulting in higher amplitude motor unit action potentials with a decrease in the number of turns per second and therefore a lower T/A ratio. In contrast, myopathic muscle fibers die or shrink after injury, and the motor unit potentials generated are from motor units that fire faster and have lower amplitude, producing a higher T/A ratio. Eighty-seven percent of the abnormal levator sites in this study had low T/A ratios at the initial postpartum visit, most consistent with a

American Journal of Obstetrics & Gynecology MAY 2009

neurogenic mechanism of injury, or denervation.20 One proposed mechanism of neurogenic injury is direct nerve compression against the bony pelvis, whereas myopathy is more likely due to direct muscle trauma (ie, tearing). Our findings in this study, particularly our observation of abnormal postpartum levator innervation in women who had undergone cesarean section, support the concept of neurogenic injury to the levator nerve as a component of pelvic floor injury in childbirth. An effect of morphologic or avulsion muscle injury on pelvic floor function has been well characterized.9,10 The extent to which denervation injury contributes to overall risk of pelvic floor symptoms attributable to childbirth is not clear, and the findings in our study need to be validated against other assessments such as magnetic resonance and condition specific questionnaires. Interestingly, African American women had a consistent trend toward a lower rate of levator denervation in our cohort, although this was not significant in our study. Several studies have noted differences in pelvic morphology seen in African American women compared with white women, which may explain the differences in levator injury rate whether by muscle avulsion or denervation.23-26 Although we did not concentrate on pelvic floor symptoms in this study, our data are consistent with the hypothesis that African Americans may suffer less significant levator neuromuscular trauma during childbirth, and this could translate into fewer or lesser symptoms of pelvic floor dysfunction later in life. Our pilot cohort study was underpowered to show a clear relationship between levator denervation and older maternal age at first delivery, and this association was confounded by the younger mean age of our African American subjects. This relationship has been of interest to other investigators, however. Dietz and Simpson27 demonstrated an impressive increase in likelihood of levator avulsion injury on transperineal ultrasound of the levator ani with increasing maternal age at first delivery, and Kearney et al2 demonstrated a similar relationship using magnetic resonance to assess levator de-

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www.AJOG.org fects. Nygaard28 reports that the protective effect of cesarean delivery on the development of urinary incontinence decreases with age and is simply not present in older women. Further studies are needed to address the risks associated with older maternal age at time of delivery and damage to the pelvic floor to help further explain these findings. Sample size was a clear limitation in our current report because it precluded definitive assessment of the role of race or age in predicting risk of levator ani denervation during the first obstetrical delivery. A post hoc power analysis demonstrated that to show a difference in race, for instance, we would have needed 47 subjects in each group. Those women in our cohort having cesarean, particularly those having cesarean in labor, had a higher frequency of levator EMG abnormality than we anticipated. Our results are supported by a study of Borello-France et al, 21 who prospectively evaluated the relationship of anal sphincter tears and urinary and fecal incontinence in primiparous women. The authors concluded that cesarean in labor was not completely protective to pelvic floor disorders because 22.9% of the women with cesarean reported urinary incontinence 6 months postpartum and 7.6% reported fecal incontinence. These findings raise the concern that elective cesarean without any labor may not be entirely protective of the levator complex. Whereas only 6 subjects in this study had a cesarean without labor, we were surprised to note that levator denervation was evident in some of these subjects. At a recent State-of-the-Science Conference sponsored by the National Institutes of Health, panelists determined that weak-quality evidence does not favor either elective cesarean delivery or planned vaginal delivery for prevention of pelvic organ prolapse, fecal incontinence, or sexual function.22 However, weak-quality evidence did support cesarean delivery over planned vaginal delivery with respect to urinary incontinence. It is possible that pregnancy itself may have a lasting negative effect on pelvic floor function, and larger prospective

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TABLE 3

Comparison of levator denervation rates by obstetric, neonatal, and maternal characteristics Variable

n ⴝ 57

Normal and reinnervated (n ⴝ 34)

Persistent (n ⴝ 23)

P valuea

Labor

.....................................................................................................................................................................................................................................

Oxytocin administration, n (%)

32

18 (56)

14 (44)

.597

.....................................................................................................................................................................................................................................

Duration epidural analgesia (min), mean (SD)

396 (235)

441 (227)

.477

.....................................................................................................................................................................................................................................

Duration of secondstage labor (min), mean (SD)

55.6 (47)

63.2 (59)

.973

..............................................................................................................................................................................................................................................

Neonatal

.....................................................................................................................................................................................................................................

Head circumference (cm), mean (SD)

34.5 (1.8)

34.4 (1.3)

.677

.....................................................................................................................................................................................................................................

Weight (g), mean (SD)

3287 (760)

3249 (683)

.464

..............................................................................................................................................................................................................................................

Maternal

.....................................................................................................................................................................................................................................

Postpartum pelvic floor contraction strength (0-9), mean (SD)

6.7 (2.1)

7.2 (2.0)

.309

.....................................................................................................................................................................................................................................

6 mo postpartum POPQ stage ⱖ 2, n (%)

13

8 (62)

5 (39)

1.000

.....................................................................................................................................................................................................................................

6 mo postpartum BMI (kg/m2), mean (SD)

26.6 (6.0)

24.4 (4.6)

.183

.....................................................................................................................................................................................................................................

6 mo postpartum BMI ⬎ 30 kg/m2, n (%)

10

7 (70)

3 (30)

.500

..............................................................................................................................................................................................................................................

BMI, body mass index; POPQ, pelvic organ prolapse quantitation; SD, standard deviation. a

For categorical variables, P value is based on the Fisher exact test. For continuous variables, P value is based on the Wilcoxon rank sum test. South. Levator ani denervation and reinnervation 6 months after childbirth. Am J Obstet Gynecol 2009.

studies addressing this issue are certainly warranted. We are intrigued by the idea that a larger maternal BMI may have a role in protection against long-term or persistent levator ani denervation. In a recent study by Baumann et al,29 evaluating the factors associated with anal sphincter laceration in more than 40,000 primiparous women, women with a BMI of 30 kg/m2 or greater had a lower risk of sphincter laceration, consistent with our findings. One possibility is that the adipose tissue in these subjects may actually act as a cushion or padding to prevent crush injury to muscle and nerves in the pelvis during childbirth. It is interesting that we found the greatest difference in BMI in subjects with and without persistent levator denervation in

those women having cesarean section, although this finding was not statistically significant. Perhaps levator denervation is a summation of that incurred by descent and pressure of the fetus in the pelvis plus actual delivery of the neonate through the pelvic outlet. Subjects undergoing cesarean have only 1 component of this total injury risk (the pressure of the fetus in the pelvis), and if maternal BMI has the greatest effect on that component of the levator injury risk, we might expect our findings. We intend to investigate this properly by assessing the distribution and volume of pelvic fat in an appropriately powered study using pelvic MRI. A recognized potential limitation of electromyography is that injured or absent muscle fibers can make it difficult or impossible to acquire an electrical signal

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FIGURE 2

Levator denervation and BMI by delivery type

Body mass index (BMI, kg/m2) of subjects by type of delivery. A trend toward higher BMI in women with persistent levator injury is noted across all delivery types. South. Levator ani denervation and reinnervation 6 months after childbirth. Am J Obstet Gynecol 2009.

for analysis, and this was particularly a risk in this single modality study, in which muscle morphology was not assessed. We anticipated this in our protocol and planned to exclude any subject with missing or uninterpretable data at either of the postpartum visits because 1 of the main goals of the study was to describe the type of neuromuscular abnormality involved. We recognized that if missing data were due to actual avulsion, excluding such subjects would lead us to underestimate the actual injury prevalence. However, none of the group of 70 subjects available for the final analysis was excluded because of missing data, so we feel this may be a lesser problem than anticipated and that our findings are likely representative of the overall study cohort. We must also consider the possibility that muscle avulsion from the bony pelvis might cause a shift in the position of the muscle so that we would unknowingly record from a different anatomic location on the levator complex post partum, and if this were to occur, we would not likely detect it as long as some muscle signal were detectable. Frequent observation of sites in which no levator activity was detected on EMG would support global loss of muscle at that site, most likely because of avulsion.30 If muscle avulsion did occur in some of our subjects, a possible explanation of our findings might be that our 519.e6

www.AJOG.org protocol fortuitously used needle sites on the levator that were not frequent areas of global muscle loss. We have reported previously an initial analysis of this same cohort using a different method of defining the normal range.12 The method reported here is simpler and facilitates statistical analysis because the EMG signal of the entire levator is pooled into a single normal range. One of our overall objectives was to simplify our analysis method to facilitate future studies testing the clinical applicability of QEMG analysis of the levator. We plan to use this method in future studies because we found overall rates of levator denervation in the cohort similar to that detected in the previous report12 with slightly better discrimination between various modes of delivery in ways that make sense clinically. This report also describes the race and age of the subjects and groups them not just by mode of delivery but by the type of delivery characteristics we believe to be relevant to risk of levator ani neuromuscular injury. We were underpowered to explore all these relationships, but our report raises interesting questions about maternal age at first delivery, maternal race, maternal BMI, and risk of levator denervation. Further investigation concerning correlation with pelvic floor symptoms and the role of pregnancy as a risk for levator denervation is also indicated. f ACKNOWLEDGMENTS We gratefully acknowledge the vital assistance of Jean Maynor, RN, and Elizabeth C. Coats, RN, without whom this study would not have been possible. We also thank Audrey A. Romero, MD, Virginia G. Branham, MD, Kristi M. Borawski, MD, Amy Murtha, MD, and Holly Muir, MB, for their assistance with protocol development and data collection.

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4. Dietz HP, Steensma AB. The prevalence of major abnormalities of the levator ani in urogynaecological patients. BJOG 2006;113: 225-30. 5. Nichols CM, Gill EJ, Nguyen T, Barber MD, Hurt WG. Anal sphincter injury in women with pelvic floor disorders. Obstet Gynecol 2004; 104:690-6. 6. Shafik A, El-Sibai O. Study of the levator ani muscle in the multipara: role of levator dysfunction in defecation disorders. J Obstet Gynaecol 2002;22:187-92. 7. Weidner AC, Barber MD, Visco AG, Bump RC, Sanders DB. Pelvic muscle electromyography of levator ani and external anal sphincter in nulliparous women and women with pelvic floor dysfunction. Am J Obstet Gynecol 2000;183: 1390-9; discussion 1399-401. 8. Pierce LM, Baumann S, Rankin MR, et al. Levator ani muscle and connective tissue changes associated with pelvic organ prolapse, parity, and aging in the squirrel monkey: a histologic study. Am J Obstet Gynecol 2007; 197:60.e1-9. 9. Dietz HP, Simpson JM. Levator trauma is associated with pelvic organ prolapse. BJOG 2008;115:979-84. 10. DeLancey JO, Morgan DM, Fenner DE, et al. Comparison of levator ani muscle defects and function in women with and without pelvic organ prolapse. Obstet Gynecol 2007;109:295-302. 11. Kiesswetter H. EMG-patterns of pelvic floor muscles with surface electrodes. Urol Int 1976;31:60-9. 12. Weidner AC, Jamison MG, Branham V, South MM, Borawski KM, Romero AA. Neuropathic injury to the levator ani occurs in 1 in 4 primiparous women. Am J Obstet Gynecol 2006;195:1851-6. 13. 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. 14. Bump RC, Mattiasson A, Bo K, et al. The standardization of terminology of female pelvic organ prolapse and pelvic floor dysfunction. Am J Obstet Gynecol 1996;175:10-7. 15. Brink CA, Sampselle CM, Wells TJ, Diokno AC, Gillis GL. A digital test for pelvic muscle strength in older women with urinary incontinence. Nurs Res 1989;38:196-9. 16. Nandedkar SD, Sanders DB, Stalberg EV. Simulation and analysis of the electromyographic interference pattern in normal muscle. Part I: turns and amplitude measurements. Muscle Nerve 1986;9:423-30. 17. Finsterer J. EMG-interference pattern analysis. J Electromyogr Kinesiol 2001;11:231-46. 18. Smyth DP. Quantitative electromyography in babies and young children with primary muscle disease and neurogenic lesions. J Neurol Sci 1982;56:199-207. 19. Hansen SL, Clark SL, Foster JC. Active pushing versus passive fetal descent in the second stage of labor: a randomized controlled trial. Obstet Gynecol 2002;99:29-34.

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www.AJOG.org 20. Fuglsang-Frederiksen A. The utility of interference pattern analysis. Muscle Nerve 2000; 23:18-36. 21. Borello-France D, Burgio KL, Richter HE, et al. Fecal and urinary incontinence in primiparous women. Obstet Gynecol 2006;108:863-72. 22. Weber AM. Elective cesarean delivery: the pelvic perspective. Clin Obstet Gynecol 2007;50:510-7. 23. Handa VL, Pannu HK, Siddique S, Gutman R, VanRooyen J, Cundiff G. Architectural differences in the bony pelvis of women with and without pelvic floor disorders. Obstet Gynecol 2003;102:1283-90.

24. Baragi RV, Delancey JO, Caspari R, Howard DH, Ashton-Miller JA. Differences in pelvic floor area between African American and European American women. Am J Obstet Gynecol 2002;187:111-5. 25. Patriquin ML, Loth SR, Steyn M. Sexually dimorphic pelvic morphology in South African whites and blacks. Homo 2003;53:255-62. 26. Hoyte L, Thomas J, Foster RT, Shott S, Jakab M, Weidner AC. Racial differences in pelvic morphology among asymptomatic nulliparous women as seen on three-dimensional magnetic resonance images. Am J Obstet Gynecol 2005;193:2035-40.

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