Biometry of the pubovisceral muscle and levator hiatus in nulliparous Chinese women

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1 Ultrasound Obstet Gynecol 2006; 28: Published online in Wiley InterScience ( DOI: /uog.3825 Biometry of the pubovisceral muscle and levator hiatus in nulliparous Chinese women J.-M. YANG*, S.-H. YANG and W.-C. HUANG *Division of Urogynecology, Department of Obstetrics and Gynecology, Mackay Memorial Hospital, School of Medicine and School of Health and Nutrition, Taipei Medical University, Department of Obstetrics and Gynecology, Cathay General Hospital and School of Medicine, Fu Jen Catholic University, Taipei, Taiwan KEYWORDS: body mass index; body weight; Caucasian women; Chinese women; levator hiatus; pubovisceral muscle ABSTRACT INTRODUCTION Objectives To identify using three-dimensional (3D) ultrasound the morphological features and normal biometry of the levator hiatus in nulliparous Chinese women and to explore ethnic differences between these measurements and those in nulliparous Caucasian women. Methods 3D sonographic data from 59 nulliparous Chinese women (aged years) who had no pelvic organ prolapse and no symptoms of pelvic floor dysfunction were retrieved from an image dataset and analyzed by offline post-processing. The pubovisceral muscle and levator hiatus were measured in the planes of maximal pubovisceral muscle thickness and minimum hiatal dimension, respectively. In addition, the genitohiatal and levator ani angles were measured. These values were compared with those in a published study of Caucasian women. Results In Chinese women there was no relationship between minimum anteroposterior (AP) hiatal diameter and minimum lateral hiatal diameter. Body weight was correlated with hiatal area and minimum AP hiatal diameter (r = 0.391, P = and r = 0.378, P = 0.004, respectively), whereas body mass index was correlated only with minimum AP hiatal diameter (r = 0.349, P = 0.008). There was a significant difference in average pubovisceral muscle thickness (P = 0.001) between nulliparous Chinese and Caucasian women. Conclusions Body weight, body mass index, and ethnicity are factors affecting the biometry of the levator hiatus in Chinese nulliparous women. Copyright 2006 ISUOG. Published by John Wiley & Sons, Ltd. The etiology of pelvic organ prolapse is multifactorial 1. Because genital prolapse occurs commonly in multiparous women, vaginal childbirth is assumed to be the most significant factor contributing to pelvic floor relaxation and pelvic floor dysfunction 1,2. However, ethnicity has also been suggested as a factor 1 6, with reports that Asian women are less likely to have pelvic organ prolapse than are Caucasian women 4,7,8. In a study of over 1000 women, more than 80% of Chinese women had a gynecoid pelvis, compared with 50% of Caucasian women 8. A gynecoid pelvis is considered better for vaginal delivery because of its spacious inlet, large interspinous diameter, and wide subpubic arch 9. Anecdotal evidence from cadaver dissection suggests that Chinese women have stronger pelvic support structures 7, an observation validated 40 years later by ultrasonic study of the pelvic floor 3. In the latter study, pregnant nulliparous Asian women had less pelvic organ mobility on ante- and postpartum pelvic floor sonography than did their Caucasian counterparts, although the number of Asian women in the study was small (16 versus 161 Caucasians). However, studies of pelvic floor dysfunction in various ethnic groups have yielded conflicting results 3,7, Differences in study populations and inadequate sample size in some studies may explain some of the discrepancies. Recently, two large-scale studies of urinary incontinence surveyed Chinese women from Hong Kong 10 and Taiwan 11 ;the prevalence of this functional disorder, which is frequently associated with pelvic organ prolapse 13, was similar to that reported among Caucasian women. The pelvic organs are maintained in their position by a combination of connective tissue, and smooth and striated muscle. Complex interactions between these elements are responsible for normal support. Damage to any of Correspondence to: Dr W.-C. Huang, 280, Jen-Ai Road, Section 4, Taipei, 106, Taiwan, R.O.C ( huangwc0413@hotmail.com) Accepted: 27 July 2006 Copyright 2006 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER

2 Chinese pelvic floor 711 them may contribute to pelvic organ prolapse and pelvic floor dysfunction 4,14. In nulliparous pregnant women, there is a strong relationship between morphology and function of the pelvic floor muscles 15. The advent of threedimensional (3D) ultrasound has increased our ability to evaluate the pelvic floor 16,17, improving the accuracy of length, area and volume measurements 16.Dietzet al. 17 recently used this technique to determine the biometric indices of the pubovisceral muscle and levator hiatus in 52 nulliparous Caucasian women. Following their methodology for 3D pelvic floor ultrasound, we designed this study to identify the morphological characteristics and normal biometry of the pubovisceral muscle and levator hiatus in nulliparous Chinese women. METHODS From June 2003 to April 2006, nulliparous nonpregnant women who were seen in our gynecological or urogynecological outpatient department were considered for participation in a study using 3D ultrasound to evaluate the pelvic floor in Chinese women. The study was approved by our hospital ethics committee, and oral or written consent was obtained from the subjects prior to enrollment. The women were seen for a variety of disorders, such as adnexal mass, dysfunctional uterine bleeding and infertility. Potential subjects were excluded if they met any of the following criteria: any lower urinary tract symptoms or bowel symptoms within 3 months; pelvic organ prolapse ( first-degree prolapse) on pelvic examination; a past history of pelvic surgery; any previous use of pelvic floor muscle exercises; a previous pregnancy beyond 10 weeks of gestation. All subjects underwent pelvic floor assessment, which included pelvic examination, anal digital examination and 3D ultrasound scanning. 3D ultrasound scanning of the pelvic floor and lower urinary tract was performed using a Voluson 730 (GE Medical Systems, Zipf, Austria) machine with a MHz transvaginal probe, with the patient lying supine. Sonographic volume acquisition was performed with the main transducer axis placed at the introitus in the mid-sagittal plane. All images and sonographic volumes were retrieved and stored in a desktop computer for subsequent analysis. Weight, height and body mass index (BMI) were also recorded for each subject. The sonographic data were analyzed using GE Kretz 4D View, version 5.0, software (GE Kretztechnik GmBH, Zipf, Austria) for 3D scanning. Offline postprocessing involved each retrieved sonographic record being processed first to obtain a mid-sagittal view in the multiplanar display. This view was then manipulated until an imaginary line from the puborectalis muscle behind and below the anorectal junction to the inferior border of the symphysis pubis was positioned according to the section line of the region of interest (ROI). Thus, the reconstructed image, an axial view, was in the plane of the minimum hiatal dimension (Figure 1a). Generally, the imaginary line was at approximately 130 to the axis of the anal canal. Next, the section line of the ROI in the mid-sagittal view was moved slowly upwards on the screen until the thickness of the pubovisceral muscle was maximal, the reconstructed image consequently being in the plane of maximum muscle thickness (Figure 1b). The following variables were measured in the rendered images: in the sagittal view, the genitohiatal angle; in the plane of minimum hiatal dimension, the anteroposterior (AP) and lateral diameters, and the area of the levator hiatus (Figure 2); in the plane of maximum muscle thickness, the thickness of the pubovisceral muscles in two locations near the rectum bilaterally, the pubovisceral muscle area and the levator ani angle (Figure 3). Except for the genitohiatal and levator ani angles, the definitions of the sonographic variables measured in this study were thesameasthoseofdietzet al. 17. The levator ani angle was defined as the angle of intersection between two lines passing through the main bulk of the pubovisceral muscles bilaterally in the plane of maximum muscle thickness (Figure 3). The genitohiatal angle was defined as the angle between the anorectal reflection-symphyseal line and the midline of the pubic symphysis in the sagittal view (Figure 4). The shape of the hiatus in the plane of minimum hiatal dimension was defined either as Type I, with an AP diameter/lateral diameter of 1(Figure2a), or as Type II, with an AP diameter/lateral diameter of < 1 (Figure 2b). Statistical analysis was performed using SPSS 12.0 for Windows (SPSS, Inc, Chicago, IL, USA). Descriptive statistics for measured variables were calculated. Normality was assessed with the Kolmogorov Smirnov test. A paired t-test, Student s t-test or Mann Whitney U-test was used to compare differences in paired or unpaired continuous data as appropriate. To compare ethnic differences in pelvic floor anatomy, statistical differences were calculated from the summary data (mean, SD and sample size) reported by Dietz et al. 17 using Student s t-test. Pearson s correlation coefficient (r) was used to examine for associations between normally distributed continuous variables. A P-value of < 0.05 was considered significant. RESULTS Sixty-one women met the eligibility criteria, but the datasets of two were not analyzed because the files were corrupted during data transfer, leaving data from 59 women in the analysis (Table 1). The mean height of the patients was 1.6 ± 0.1 (range, ) m and their mean weight was 51 ± 5 (range, 35 65) kg. The median gravidity was 0 (range, 0 4). Eleven women had been pregnant, but none had carried a gestation beyond 10 weeks. Reproducibility of ultrasound measurements We performed a test-retest series of 20 datasets to evaluate the inter- and intraobserver reproducibility. Each of the 20 datasets was assessed twice by two investigators (J.-M.Y. and W.-C.H.). Each examiner was

3 712 Yang et al. Figure 1 Level of the section lines (inferior border of the boxes marked ) in the sagittal view selected for the plane of minimum hiatal diameter (a) and the plane of maximum pubovisceral muscle thickness (b). The right-hand images represent the axial plane rendered volumes used for quantification of (a) hiatal dimensions and (b) muscle thickness. a, anal canal; bl, bladder; prm, puborectalis muscle; r, rectum; sp, pubic symphysis; u, urethra; v, vagina. Table 1 Intraclass correlation coefficients (ICC) for sonographic parameters of the pelvic floor (test-retest series, n = 20) Variable ICC 95% CI In the plane of maximum muscle thickness Pubovisceral muscle thickness Pubovisceral muscle area Levator ani muscle angle In the plane of minimum hiatal dimension Minimum anteroposterior hiatal diameter Minimum lateral hiatal diameter Minimum hiatal area blinded to the results of the other and to their own previous reading. Reproducibility was determined across all four measurements. Intraclass correlation coefficient values ranged from 0.41 to 0.83, with best agreement for measurements of AP and lateral hiatal diameters in the plane of the minimum hiatal dimension (0.83 and 0.79, respectively) (Table 1). Biometry and morphological characteristics in nulliparous Chinese women (n = 59) In the plane of maximum muscle thickness, the mean pubovisceral muscle thickness was 0.84 ± 0.16 (range, ) cm, mean pubovisceral muscle area was 7.39 ± 1.74 (range, ) cm 2 and mean levator ani angle was 56 ± 13 (range, 31 89). In the plane of minimum hiatal dimension, the mean minimum AP hiatal diameter was 4.29 ± 0.60 (range, ) cm, mean minimum lateral hiatal diameter was 3.92 ± 0.7 (range, ) cm and mean minimum hiatal area was ± 2.21 (range, ) cm 2. In the midsagittal plane, the mean genitohiatal angle was 142 ± 8 (range, ). There was no association between the minimum AP and lateral hiatal diameters (r = 0.141, P = 0.287). Thickness measurements of the left pubovisceral muscle were higher and ranged more widely compared with those on the right (Figure 5). The minimum AP hiatal diameter was significantly positively associated with the area of the

4 Chinese pelvic floor 713 Figure 3 Thickness, area and angle of the pubovisceral muscles. Calipers 1 4, thickness of pubovisceral muscle; 5, pubovisceral muscle area; 6, levator ani angle; r, rectum; sp, pubic symphysis; u, urethra; v, vagina. Figure 2 Hiatal dimensions and area in Type-I (a) and Type-II (b) levator hiatus. Caliper 1, anteroposterior diameter; 2, lateral diameter; 3, hiatal area; r, rectum; sp, pubic symphysis; u, urethra; v, vagina. pubovisceral muscle (r = 0.452, P < 0.001). In terms of hiatal shape, 43 (73%) of the 59 women had a Type-I levator hiatus and 16 (27%) had Type II. These two groups were not significantly different in demographic data, pubovisceral muscle thickness and area, minimum lateral hiatal diameter and genitohiatal angle. However, there were significant differences in the minimum AP hiatal diameter (4.55 ± 0.46 cm in Type I vs ± 0.35 cm in Type II, P < 0.001), levator ani angle (52 ± 11 vs. 66 ± 13, P < 0.001) and minimum Figure 4 Measurement of the genitohiatal angle in the sagittal view. a, anal canal; bl, bladder; r, rectum; sp, pubic symphysis; u, urethra; v, vagina. hiatal area (12.08 ± 2.01 cm 2 vs ± 1.57 cm 2, P < 0.001). Effect of individual constitutional factors In the 59 study subjects, age, prior early pregnancy and genitohiatal angle were not correlated with measurements of the levator hiatus and pubovisceral muscles. However, heavier weight was correlated with a larger minimum hiatal area and minimum AP hiatal diameter (r = 0.391, r 2 = 0.153, P = and r = 0.378, r 2 = 0.143, P = 0.004, respectively) and the higher the BMI, the greater the minimum AP hiatal diameter (r = 0.349, r 2 = 0.122, P = 0.008).

5 714 Yang et al. Table 2 Patient demographic data and sonographic data of the pelvic floor in two series of nulliparous women of different ethnicity Variable Present study Dietz et al. 17 P* Sample 48 Chinese women 52 Caucasian women Age (years) 26.6 ± 4.7 (19 38) 20.4 ± 1.49 (18 24) < Body mass index (kg/m 2 ) 20.1 ± 2.1 ( ) 23.5 ± 3.63 ( ) < Pubovisceral muscle thickness (cm) 0.84 ± 0.17 ( ) 0.73 ± Pubovisceral muscle area (cm 2 ) 7.43 ± 1.76 ( ) 7.59 ± Minimum AP hiatal diameter (cm) 4.35 ± 0.60 ( ) 4.52 ± Minimum lateral hiatal diameter (cm) 3.93 ± 0.47 ( ) 3.75 ± Minimum hiatal area (cm 2 ) ± 2.18 ( ) ± 2.70 ( ) Data are presented as mean ± SD (range). *Comparison between two groups from the summary of data (mean, SD and sample size) using Student s t-test. Had not been pregnant before. Dietz (pers. comm.). Range was not available. AP, anteroposterior. Pubovisceral muscle thickness (cm) R1 R2 Figure 5 Mean thickness of the pubovisceral muscle at different locations (the sites of R1, R2, L1, and L2 correspond to the locations of 1, 2, 3 and 4, respectively, in Figure 3). Open squares indicate the mean, bars show mean ± SD and whiskers show mean ± 2SD. Ethnic difference Of the 59 study subjects, 48 women who had not been pregnant before were included selectively for ethnic comparison. Based on the summary data for the two studies, we found that Chinese women had significantly higher mean pubovisceral muscle thickness than did Caucasian women (P = 0.001; Table 2). DISCUSSION We have shown that biometry of the levator hiatus in nulliparous Chinese women is affected by body weight and BMI. Also, there appear to be ethnic differences between Chinese and Caucasian women, but only in the average pubovisceral muscle thickness. We did not include any measurements in the coronal plane for two reasons. First, Dietz et al. 17 did not include a clear illustration of such measurements. Therefore, any comparison we tried to make might be invalid because of inadvertent use of different measurements. Second, the images in the coronal plane were so indistinct that our own preliminary test-retest trials yielded very poor intraclass correlation coefficients (< 0.30). Widening of the levator hiatus has been suggested as a cause of genital prolapse 18,19. Pelvic organ prolapse is L1 L2 thought to result when defective pelvic support, whether congenital or acquired, is inadequate in the face of even normal intra-abdominal pressure 4. When the levator ani muscle is damaged, most commonly as a result of obstetric injury 2, levator hiatus tends to be larger 18,19.Thelarger the hiatal area, the lower the position of the pelvic organ on Valsalva maneuver 17. The AP hiatal diameter (referred to as the genitohiatal distance in some studies 20 ) appears to vary with the genitohiatal angle (or vulvar slant), which increases in proportion to the severity of pelvic organ prolapse 20 and differs depending on the conformation of the bony pelvis 4. We did not find any association between the minimum AP hiatal diameter and the genitohiatal angle in our study subjects, none of whom had pelvic floor relaxation. Pelvic organ prolapse may also result when normal pelvic supports are subjected to chronic increases in intraabdominal pressure 4, which may result from obesity and high BMI, and which in turn stresses the pelvic floor 21 and diminishes pelvic floor muscle width and volume 22.Our study in nulliparous women supports these observations in that higher weight and BMI were correlated with larger AP hiatal dimensions. Both obesity and high BMI are also involved in urinary incontinence 6,21,22.Increased AP hiatal diameter is a sign of poor resting tone of the puborectalis muscle 20 and is associated with weak urethral closure 20,23. We did not find any significant difference in the parameters measured in the plane of minimum hiatal dimension between our nulliparous Chinese subjects and the Caucasian women studied by Dietz et al. 17 although their subjects were heavier and younger than ours. It may be that any ethnic comparisons between the two groups were unreliable, being confounded by the BMI and body weight. Interestingly, our subjects had a thicker pubovisceral muscle than did their Caucasian counterparts (0.84 ± 0.17 cm vs ± 0.16 cm, P = 0.001). This may be one of the reasons that pelvic organ mobility seems to be lower in Chinese women 3,7. In addition, the selection criteria and mean age were slightly different between the two groups. It has been reported that women with urodynamic stress incontinence and prolapse appear to have the same size of urogenital hiatus as do women with prolapse alone 19, whereas women with stress incontinence but

6 Chinese pelvic floor 715 without prolapse do not have an enlarged urogenital hiatus. Urinary continence depends on a complex control network involving several components. The anatomical component consists of the urethral support and sphincteric closure systems 24. We postulate that the similar prevalence of urinary dysfunction in Chinese and Caucasian women 3,10,11 is because of similar morphology in the center of the pelvic floor, i.e. the levator hiatus in the plane of minimum hiatal dimension. The lower incidence of pelvic organ prolapse 3,7 in Chinese women, on the other hand, may be because of differences in the bony pelvis 8, the shape of the hiatus, the thickness of the levator muscle and connective tissue elasticity and density 7. Anatomically, the levator ani muscle is composed of two portions, the lateral supportive iliococcygeus and the central sphincteric puborectalis and pubococcygeus (or pubovisceral muscles) 18,20. The central sphincteric part of the levator ani muscle is the area that is most vulnerable to damage secondary to parturition or increased intraabdominal pressure. An increase in the area of the levator hiatus is more dependent on an increase in AP rather than transverse diameter 18. It is possible that a large levator hiatus is a risk factor for failure of reconstructive pelvic surgery 25. Procedures to ameliorate incontinence may fail if the pelvic floor muscles have poor tone 26. Sonographic measurements of levator hiatal dimensions may thus be useful to identify patients with primary urodynamic stress incontinence who are at risk for pelvic organ prolapse or treatment failure, although it will require large studies to establish the normal range of these dimensions. Sonography, being non-invasive and reproducible, is a good instrument for this purpose, and new techniques are constantly being developed. For example, we were unable to measure hiatal dimensions during straining in our series because of limitations of our scanner; newer 3D scanning techniques, however, have resolved this problem 17. In conclusion, our study confirms the utility of 3D ultrasound for visualizing standardized planes, thus permitting visual reconstruction of pelvic floor anatomy. This technique diminishes operator dependence 16, opening the way for more precise measurements of the complex anatomical relationships of the female pelvis. We have shown that the biometry of the levator hiatus in nulliparous women is affected by body weight, BMI and ethnicity. ACKNOWLEDGMENTS We thank Mary Jeanne Buttrey, MD, for advice and constructive criticism of this manuscript. This study was supported by the grants from National Science Council (Research Grant No. NSC B ) and Mackay Memorial Hospital (Research Grant No. 9431). REFERENCES 1. Schaffer JI, Wai C, Boreham MK. Etiology of pelvic organ prolapse. 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