Is pelvic organ support different between young nulliparous African and Caucasian women?

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1 Ultrasound Obstet Gynecol 2016; 47: Published online 2 May 2016 in Wiley Online Library (wileyonlinelibrary.com). DOI: /uog Is pelvic organ support different between young nulliparous African and Caucasian women? K. L. SHEK*, H. G. KRAUSE, V. WONG, J. GOH and H. P. DIETZ *Liverpool Clinical School, Western Sydney University, Liverpool, Australia; Nepean Clinical School, University of Sydney, Sydney, Australia; Griffith University Medical School, Nathan, Australia; Department of Gynaecology, Greenslopes Private Hospital, Greenslopes, Australia KEYWORDS: ethnicity; imaging; levator ani; levator hiatus; pelvic floor; pelvic organ prolapse; ultrasound ABSTRACT Objective There seems to be substantial variation in the prevalence of pelvic floor disorders between different ethnic groups. This may be due partially to differences in pelvic floor structure and functional anatomy. To date, data on this issue are sparse. The aim of this study was to compare hiatal dimensions, pelvic organ descent and levator biometry in young, healthy nulliparous Caucasian and African women. Methods Healthy nulliparous non-pregnant volunteers attending a local nursing school in Uganda were invited to participate in this study during two fistula camps. All volunteers underwent a simple physician-administered questionnaire and a four-dimensional translabial ultrasound examination. Offline analysis was performed to assess hiatal dimensions, pelvic organ descent, levator muscle thickness and area. To compare findings with those obtained in nulliparous non-pregnant Caucasians, we retrieved the three-dimensional/four-dimensional ultrasound volume datasets of a previously published study. Results The dataset of 76 Ugandan and 49 Caucasian women was analyzed. The two groups were not matched but they were comparable in age and body mass index. All measurements of hiatal dimensions and pelvic organ descent were significantly higher among the Ugandans (all P 0.01); however, muscle thickness and area were not significantly different between the two groups. Conclusions Substantial differences between Caucasian and Ugandan non-pregnant nulliparae were identified in this study comparing functional pelvic floor anatomy. It appears likely that these differences in functional anatomy are at least partly genetic in nature. Copyright 2015 ISUOG. Published by John Wiley & Sons Ltd. INTRODUCTION Pelvic organ prolapse (POP) is a highly prevalent condition. The lifetime risk of surgery for POP in the general female population in Western Australia was recently estimated to be 19% 1. POP can be considered a herniation of pelvic organs, i.e. bladder, uterus, small bowel and/or rectal ampulla, through the levator hiatus, the space bounded by the puborectalis component of the levator ani muscle and the os pubis. The levator hiatus is the largest potential hernia portal in the human body, the size of which has been shown to be associated with symptoms and/or signs of POP, and the latter in both asymptomatic and symptomatic populations 2,3. The etiology of POP is likely multifactorial and may be complex. Ethnicity has been proposed as a potential etiological factor. Epidemiological studies suggest that the prevalence of different forms of pelvic floor dysfunction vary among ethnic groups. Stress urinary incontinence may be more prevalent among Caucasians than African-Americans 4,5. Likewise, symptomatic POP seems to be less common among African-American compared with white women 6,7.These findings may reflect genuine differences in pelvic floor functional anatomy between populations of different ethnic backgrounds, as shown in some studies In a recent imaging study comparing South-East Asian and Caucasian pregnant nulliparous women, the former were found to have a thicker pubovisceral muscle, a smaller levator hiatus and less pelvic organ mobility 11, suggesting ethnic differences in pelvic floor functional anatomy. To date, several publications have reported findings of pelvic organ mobility and levator biometry in young nulliparous Asian and Caucasian populations ; similar data, however, are lacking for other ethnicities. The aim of this study was, first, to describe pelvic organ mobility, biometry of the levator hiatus and puborectalis muscle using translabial Correspondence to: Dr K. L. Shek, Liverpool Hospital, Locked Bag 7103, Liverpool BC NSW 1871, Australia ( shekkalai@ yahoo.com.hk) Accepted: 9 November 2015 Copyright 2015 ISUOG. Published by John Wiley & Sons Ltd. ORIGINAL PAPER

2 Pelvic floor and ethnicity 775 ultrasound in a group of young nulliparous Ugandan women and, second, to compare the findings with archived ultrasound volume data of a group of young nulliparous Caucasian women recruited for a study published previously. SUBJECTS AND METHODS Nulliparous healthy volunteers were recruited from a local nursing school in Uganda on two occasions during a fistula camp in April 2011 and July All volunteers completed a simple physician-administered questionnaire on symptoms of urinary incontinence. Four-dimensional translabial ultrasound examinations were performed with the woman in the supine position after bladder emptying, at rest, on Valsalva maneuver and on pelvic floor muscle contraction (PFMC) using a GE Voluson i ultrasound system with 8 4-MHz curved array volume transducer (GE Medical Systems, Zipf, Austria) as described previously 15. At least three ultrasound volumes on Valsalva maneuver were acquired and the volume on maximum Valsalva maneuver, i.e. the volume showing the most marked pelvic organ descent, was used for analysis of parameters on Valsalva maneuver. Hiatal dimensions, pelvic organ descent and levator muscle thickness and area were assessed offline on a desktop PC using proprietary software (4Dview v10, GE Medical Systems) as described previously 2. In brief, hiatal diameters and area were assessed in the plane of minimal hiatal dimensions as defined in the mid-sagittal plane, evident as the minimal distance between the hyperechogenic posterior aspect of the symphysis pubis and the hyperechogenic anterior border of the levator ani muscle just posterior to the anorectal muscularis. This plane is defined in the mid-sagittal orthogonal plane, which then allows representation of exactly this cross-section of the volume in the axial plane for measurement of hiatal dimensions (Figure 1). Maximum muscle thickness was determined by slowly moving the plane of minimal hiatal dimensions cranially until the plane of maximal thickness of the levator muscle was reached. In the axial view, we measured maximum diameters of the puborectalis muscle in two locations bilaterally and determined muscle area by tracing its outline at the level of maximal muscle thickness. Pelvic organ descent was measured on maximum Valsalva maneuver with reference to the posteroinferior margin of the pubic bone in the mid-sagittal plane 16. Ethics committee approval was obtained from Greenslopes Private Hospital (EC 11/09 and QIMR HREC 2015/2100). The study was approved by the administration of the School of Nursing (Kagando Hospital, Uganda) as no formal ethics committee exists at this institution. Written consent was obtained from the volunteers. To compare findings with data obtained in healthy white Caucasians, we assessed the archived three-dimensional/four-dimensional ultrasound volume datasets of a previously published study on nulliparous non-pregnant Caucasians 17. The Caucasian women had initially been recruited in a heritability study to determine whether mobility of the bladder neck is genetically influenced. They were recruited through mailouts to secondary schools in the Brisbane region in Australia. Participants had undergone translabial ultrasound imaging for the study and their ultrasound volume data were saved and archived. Volume data had been acquired using the same method as in the current study, except that imaging on PFMC was not performed, and it was evaluated in the same manner as described above by K.L.S. Statistical analysis Statistical analysis was undertaken after normality testing using Kolmogorov Smirnov testing, with Minitab version 13 (Minitab Inc., State College, PA, USA). Student s t-test was performed for continuous variables and chi-square test analysis for categorical variables. Pearson s correlation was used to evaluate the correlation between hiatal area and pelvic organ descent. A P-value of < 0.05 was considered to be statistically significant. RESULTS In total, 76 nulliparous Ugandan women were recruited. The mean age of the participants was 21.2 (range, ) years and mean body mass index was 22.6 (range, ) kg/m 2. None of the volunteers complained of symptoms of urinary incontinence. Archived ultrasound datasets of 51 nulliparous Caucasian women seen in the context of a previously published study were identified. Two were excluded from analysis because of missing volumes, leaving 49 datasets available for review. A total of seven Caucasians reported stress urinary incontinence, one of whom also reported urge urinary incontinence. No subject in either cohort had a history of pelvic floor surgery or intervention for a pelvic floor disorder. The demographic characteristics, hiatal dimensions, measures of levator muscle bulk and pelvic organ descent in the two groups are shown in Table 1. All measures of hiatal dimensions and pelvic organ descent were significantly higher among the Ugandan volunteers (all P 0.01). This was not the case for measures of muscle bulk, as muscle thickness and area were not significantly different between the two groups. There was a significant correlation between hiatal area at rest and on Valsalva maneuver and pelvic organ descent in all three compartments (all P < 0.001; Table 2). Fourteen Caucasian participants and seven African volunteers coactivated the levator ani muscle on Valsalva maneuver despite repeated attempts to teach them to avoid this during volume acquisition (chi-square test, P = 0.005). Analysis was repeated after excluding these women and the findings were nearly identical. A subanalysis of functional pelvic floor anatomy against ethnicity after exclusion of women complaining of urinary incontinence yielded almost identical results.

3 776 Shek et al. Figure 1 (a) Translabial pelvic floor ultrasound image in the mid-sagittal plane, showing descent of bladder (cystocele, C), uterus (U) and rectal ampulla (R) relative to posteroinferior margin of pubic symphysis (S). Measurements represent maximal caudad organ position on Valsalva maneuver without reference to position at rest. Measurements below inferior symphyseal margin (reference line) are negative and those above line are positive. (b) Translabial ultrasound image in the plane of minimal hiatal dimensions, showing hiatal area (dotted outline). (c) Translabial ultrasound image in the plane of maximum muscle thickness, which is usually cm cranial to the plane of minimal dimensions, showing muscle thickness (lines) in paravaginal and pararectal locations. Table 1 Demographic data and measurements of functional pelvic floor anatomy on translabial ultrasound according to ethnicity Variable Caucasian (n = 49) Ugandan (n = 76) P Age (years) 20.5 ± ± Body mass index (kg/m 2 ) 23.6 ± ± Anteroposterior hiatal diameter At rest (cm) 4.55 ± ± 0.73 < On Valsalva maneuver (cm) 4.81 ± ± 1.15 < Lateral hiatal diameter At rest (cm) 3.55 ± ± On Valsalva maneuver (cm) 3.96 ± ± Hiatal area At rest (cm 2 ) ± ± 3.27 < On Valsalva maneuver (cm 2 ) ± ± 7.72 < Maximum muscle thickness at rest (mm) 7.86 ± ± Maximum muscle area at rest (cm 2 ) 6.50± ± Bladder-neck descent (mm) 13.2 ± ± 8.7 < Bladder descent (mm) ± ± 9.1 < Uterine descent (mm) 41.5 ± ± 20.4 < Rectal descent (mm) 15 ± ± 12.5 < Data are given as mean ± SD. Bladder-neck descent is a measure of bladder-neck mobility. Bladder/uterine/rectal descent denotes position of respective organ relative to symphysis pubis; a negative value signifies position below the symphysis. DISCUSSION In this comparative study of two cohorts of young, non-pregnant nulliparae, Ugandans were found to have a significantly larger levator hiatus and greater pelvic organ descent than Caucasians. This implies greater distensibility of the levator ani muscle and greater elasticity of fascial support structures. This difference, although not unanticipated, is of unexpected magnitude. Hiatal distensibility, as determined by average hiatal area on Valsalva maneuver in Ugandans, was found to be more than 1 SD higher than in Caucasians, and differences of a similar magnitude were found for pelvic organ mobility. Muscle thickness and area, however, were similar between the groups. Studies using magnetic resonance imaging have reported a difference in pelvic anatomy between white Americans and African-Americans 18,19. A genuine difference in pelvic anatomy is likely to be responsible for the observed differences in functional anatomy in our study. Apart from genetics, however, other causes including nutrition 20 and lifestyle factors 14 may also play a role. For example, in Uganda it is common for women to walk long distances carrying heavy loads on the shoulder or head. Racial differences in the prevalence of various forms of pelvic floor dysfunction have been reported in medical literature. Our study showing greater pelvic organ descent in Ugandans than in their Caucasian counterparts appears to be in contrast to the general opinion that POP is less prevalent in the African population, as seen in epidemiological studies in Western countries 6,7.Sucha discrepancy may be explained by a change in lifestyle and diet among Africans living in Western countries. Another explanation may concern childbirth-related trauma. It

4 Pelvic floor and ethnicity 777 Table 2 Correlation between hiatal area at rest and on Valsalva maneuver and pelvic organ descent, as ascertained by translabial ultrasound in mid-sagittal plane Parameter Pearson s correlation Hiatal area at rest vs: Bladder-neck descent < Bladder descent < Uterine descent < Rectal descent < Hiatal area on Valsalva maneuver vs: Bladder-neck descent < Bladder descent < Uterine descent < Rectal descent < Correlations are negative for bladder/uterine/rectal descent as higher values for these parameters signify a higher organ position (less descent) on Valsalva maneuver. The larger the hiatal area, the lower the position of pelvic organs on Valsalva maneuver, i.e. the greater the descent. has been claimed that there is an association between pelvic floor biomechanics and labor outcomes 21,22. It is plausible that women with a more compliant or distensible pelvic floor may be less susceptible to trauma secondary to childbirth. Today there is growing evidence to suggest that trauma to the levator ani muscle is important in the pathogenesis of POP 3, Individuals or populations with a more compliant pelvic floor reflected by a more distensible hiatus and greater degree of pelvic organ mobility prior to the first delivery may be less likely to sustain levator trauma and hence less likely to develop symptomatic POP in the future. The relationship between pelvic floor biomechanical properties and childbirth-related fascial and muscular trauma is likely to be complex and deserves further study. Although data on levator morphobiometry of young nulliparous Caucasians 2 and East Asians 12 have shown a smaller hiatus and less pelvic organ mobility in the latter population, in both non-pregnant and pregnant populations 11, similar data were lacking for Africans until very recently. There is now a published study on a comparison of Black and White South African young nulliparae using identical methodology to ours 27. The results strongly support our data, in that Black South Africans showed significantly larger hiatal area and more pelvic organ descent than did White South Africans. Both studies are highly consistent with each other and have added baseline biometric measures for pelvic floor functional anatomy of nulliparous African women to the literature. Such data may also help us better understand the pathogenesis of POP. Strengths of our study include the identical methodology, for both acquisition of volume data and postprocessing analysis, in the two groups and the fact that both groups were closely matched for age and body mass index. A number of weaknesses, however, need to be acknowledged. The data presented in this study are based on ultrasound volume datasets acquired in two different P studies, in different locations and at widely differing timepoints. This may have introduced a degree of bias. However, all acquisitions were undertaken using the same ultrasound technology (Voluson systems), which has been shown to have good consistency in volume acquisition 28. All analyses of stored volume datasets were performed by K.L.S. using measurement techniques that have been shown to be highly repeatable by us and others Another potential source of bias is that offline analysis of ultrasound volume data was not blinded to ethnicity. However, the degree of differences noted between the two cohorts is unlikely to be explained completely by bias. Furthermore, as we did not collect data with regard to prolapse symptoms we are unable to determine whether Ugandans were more symptomatic than were their Caucasian counterparts. The lack of a clinical prolapse assessment is considered another weakness of this study; however, any internal examination is likely to impact on the recruitment of volunteers. In conclusion, substantial differences between unselected cohorts of Caucasian and Ugandan non-pregnant nulliparae were identified in this study comparing functional pelvic floor anatomy. Ugandans were found to have a significantly larger levator hiatus and greater pelvic organ descent than were Caucasians. This implies greater distensibility of the levator ani muscle and higher elasticity of fascial support structures. DISCLOSURE H.P.D. and K.L.S. have received unrestricted educational grants from GE Medical Systems. REFERENCES 1. Smith F, Holman D, Moorin R, Tsokos N. Lifetime risk of undergoing surgery for pelvic organ prolapse. Obstet Gynecol 2010; 116: Dietz HP, Shek KL, Clarke B. Biometry of the pubovisceral muscle and levator hiatus by three-dimensional pelvic floor ultrasound. Ultrasound Obstet Gynecol 2005; 25: Dietz HP, De Leon J, Shek KL. Ballooning of the levator hiatus. Ultrasound Obstet Gynecol 2008; 31: Bump RC. 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