Direct imaging of the pelvic floor muscles using two-dimensional ultrasound: a comparison of women with urogenital prolapse versus controls

Authors


Dr S Athanasiou, First Department of Obstetrics and Gynaecology, Alexandra Hospital, Athens, Greece. Email athanasio@otenet.gr

Abstract

Objective  To evaluate the anatomy of the levator ani muscle in women with urogenital prolapse versus matched controls without prolapse using real-time two-dimensional (2-D) ultrasound.

Design  Prospective observational study.

Setting  Tertiary referral urogynaecology unit.

Population  Forty-three women with pelvic organ prolapse (POP) and 24 women (controls) attending a gynaecology clinic without prolapse.

Methods  All participants completed a standardised symptom questionnaire.

Main outcome measures  The morphology of the vagina and paravaginal tissue was recorded at different levels. The thickness of the levator ani and the hiatal area were measured at rest. Reproducibility of the method was assessed by repeated measurements to assess intra-observer variability and inter-observer variability.

Results  This method showed good intra-observer and inter-observer reproducibility and reliability. In controls, the pubococcygeus muscle showed more regular echogenicity with no evidence of trauma, whereas in women with prolapse the muscle had mixed echogenicity. (P= 0.002). The mean thickness of the pubococcygeus did not differ between groups. The levator hiatal area was significantly larger in women with pelvic floor prolapse versus controls (17.8 cm2 versus 13.5 cm2, P < 0.001). This increase in hiatal area positively and significantly correlated with prolapse severity (P < 0.001).

Conclusions  Morphology and hiatal area can be reliably imaged using 2-D ultrasound. Prolapse was related to changes in pelvic floor morphology and increased levator hiatal area. The use of 2-D ultrasound provides an important insight into the pathophysiology of prolapse.

Introduction

Pelvic organ prolapse (POP) is a common condition affecting up to 50% of parous women and often coexists with urinary incontinence.1 Despite the high prevalence, the underlying pathophysiology has not been fully elucidated. This may explain why surgical repair of prolapse is associated with failure rates as high as 30%,2 as our insufficient understanding of the underlying structural alterations which lead to prolapse may result in inadequate correction.

The levator ani complex plays a significant role in pelvic organ support. Assessment of the integrity of pelvic organ support is difficult. The value of clinical examination alone is limited and has not been validated.3 Magnetic resonance imaging (MRI) studies have provided a detailed insight into anatomy of the levator ani complex which has been shown not to be a single muscle but to comprise two functional components varying in thickness and function. MRI studies have also showed alterations in morphology in women with stress urinary incontinence and POP.4–7 However, although MRI has provided valuable insights into pelvic floor anatomy and function, its use is limited because it is not universally available and is expensive.

Ultrasound imaging of the pelvic floor has advantages over MRI. It is safer, more economical and enables visualisation in real time. This allows assessment of levator function and dynamic changes during contraction and Valsalva. However, anatomical assessment by ultrasonography has been difficult because the complex shape of the pelvic floor muscles and their central position within the pelvis may impair adequate visualisation and definition.

This study describes the use of real-time two-dimensional (2-D) ultrasound to visualise the levator ani muscle complex. Morphometric measurements of the pelvic floor were taken in women with prolapse and compared with that of the controls with no or minimal pelvic organ descent to identify morphological changes associated with prolapse.

Methods

Women were recruited from a tertiary referral urogynaecology clinic and a general gynaecology clinic at King’s College Hospital from November 1994 to January 1996. All women completed a structured symptom questionnaire regarding urinary, bowel and prolapse symptoms.8,9 All of them underwent a vaginal examination with an empty bladder to grade the severity of prolapse using the International Continence Society (ICS) pelvic organ quantification system (POP-Q).10 Women with either no prolapse or stage I prolapse were admitted into the ‘control’ group. Women with prolapse greater than stage I were admitted into the ‘prolapse’ group. In addition, the maximum descent of the leading organ was noted.

Real-time transvaginal ultrasound was then performed with the woman at rest in the semirecumbent position after they reported their bladder felt comfortably full. Bladder volumes were therefore not standardised. The operator was unaware of the results of the clinical examination. A Kretz Combison 530 system (GE Kretztechnik, Zipf, Austria) with a 7.5-mHz probe was used. The scanning angle was 360° in a plane perpendicular to the axis of the probe. The probe was inserted into the vagina paying attention not to exert pressure on the pelvic floor muscles; in women with POP, the prolapse was reduced before insertion of the probe. Axial plane images of the pelvic floor were obtained along the vagina using the pubic symphysis as a guide at the top of the screen and adjusting the probe so symmetrical images could be obtained (Figure 1). By tilting the probe upwards or downwards, the pubococcygeus muscle ‘sling’ could be imaged in its entirety with its muscle fibres running parallel to each other. The pubococcygeus muscle thickness was measured at the level of the posterior vaginal wall. The hiatal area was measured by outlining the inferior border of the symphysis pubis anteriorly and the inner boundary of the pubococcygeus muscle using a cursor. The hiatal area was then calculated automatically by the machine’s inbuilt software. Alterations in the morphology such as presence of mixed echogenicity (i.e. loss of the smooth parallel appearance of the muscle fibres) and trauma (loss of continuity or absence of muscle) were noted on each side. The support of the anterior vaginal sulci to the lateral pelvic wall was assessed, and any loss of support was recorded. By advancing the probe more cephalad in the vagina, other parts of the pelvic floor at a higher plane were visible. Changes of the vaginal wall contours at different levels were noted. All images were obtained at rest.

Figure 1.

Ultrasonographic section at the level of mid-urethra (U) of a woman with normal support. The pubococcygeal sling (PC) is visible with hyperechogenic muscle fibres. The muscle originates from the posteriolateral aspect of the pubic symphysis (SP). The contour of the muscle is regular. The anterior vaginal sulci (V) are well supported lateral to the urethra (U). The obturator muscle (Ob) only emerges lateral to the pubococcygeus muscle (PC). LA th, levator ani thickness; R, rectum.

To ensure the reproducibility of this method, we assessed the intra-observer variability in 13 women. The inter-observer reliability was assessed by another investigator (V.K.) blinded to the initial results, who performed repeated measurements of the pubococcygeus thickness and hiatal area in nine women.

Ethical approval was obtained for this study, and all women gave informed consent.

Statistical analysis

Categorical data are expressed as percentages, and comparisons were performed with the chi-square or the Fisher’s exact test when appropriate. Continuous variables are summarised as medians and ranges and compared using nonparametric methods. In case of comparison between two groups, the Mann–Whitney test was used, whereas when more than two groups were compared, the Kruskal–Wallis test was used. For the intra- and inter-observer agreement, test–retest reliability analysis has been performed. Intraclass correlation coefficients (ICC) and 95% confidence intervals are presented.11 The correlation of the levator hiatal area and thickness with POP-Q assessment findings and the maximum descent of the leading organ was assessed using the Spearman correlation coefficient.

All statistical tests were two sided, and statistical significance has been defined at P= 0.05. All analyses were performed on SPSS 11 for Windows (SPSS Inc., Chicago, IL, USA).

Results

In total, 67 women were recruited—43 with genital prolapse (grade ≥II) and 24 (controls) without significant prolapse (grade 0 or I) were recruited. Demographic data are described in Table 1.

Table 1.  Comparison of women with and without prolapse. Demographic and ultrasound data of women with and without prolapse
 Normal, n= 24Prolapse, n= 43P
  1. NS, non significant.

  2. Data are presented as n (%) or median (range).

  3. *Women with missing values are excluded from the chi-square or Fisher’s exact test.

Age (years)47 (28–72)47 (27–70)NS
Parous women17 (81)39 (90)0.046
Parity1 (0–6)2 (0–5)NS
Mixed echogenicity
No17 (70.8)12 (30.8)0.002
Yes7 (29.2)27 (69.2) 
Trauma visible
No24 (100)25 (64.1)0.001
Yes14 (35.9) 
Trauma location
Unilateral8 (20.5)0.002
Bilateral6 (15.4) 
Paravaginal defects seen (detachment)
No23 (95.8)23 (60.5)0.002
Yes1 (4.2)15 (39.5) 
Paravaginal defect site
No23 (95.8)23 (60.5) 
Left/right1 (4.2)5 (13.2)0.003
Both sides 10 (26.3) 
Levator ani muscle thickness (mm)7.1 (3.4–8.9)6.4 (3.7–10.5)NS
Levator ani surface at rest (cm2)13.5 (10.6–18.7)17.8 (10.6–31.0)0.001

All women tolerated the ultrasound examination well. The levator hiatal area and the muscle thickness could be measured in all women. Intra- and inter-observer variability showed a very good degree of concordance (Table 2). ICC ranged from 0.62 to 0.99, generally being better for hiatal area than muscle thickness.

Table 2.  Intra-observer and inter-observer reproducibility for measurement of levator surface thickness
 ICC95% CI
  1. CI, confidence interval.

Intra-observer (n= 13)
Surface0.9920.976–0.998
Thickness0.7490.377–0.915
Inter-observer (n= 9)
Surface0.9830.932–0.996
Thickness0.6240.025–0.899

Ultrasound imaging

At the lower level of levator ani, its anterior part (the pubococcygeus muscle) was seen as a hyperechogenic structure arising from its origin on the posterior aspect of the symphysis pubis extending laterally to the pelvic viscera meeting with the contralateral fibres posterior to the anorectal junction forming a sling-like arrangement (Figure 1). At a higher scanning plane, the obturator internus muscle could be visualised as a hypoechogenic structure on the lateral pelvic sidewall. The hyperechoic line overlying the obturator internus muscle representing the obturator fascia was shown in all cases (Figure 2A). The origin of the iliococcygeus was clearly visible from the obturator fascia at a higher cephalad level. The vaginal wall at this higher level loses the ‘H’ shape appearance and becomes more flattened (Figure 2B).

Figure 2.

(A) Scanning at a higher plane. The obturator internus (Ob) muscle is visible laterally covered by the hyperechogenic fascia (obturator fascia) (Ob-f). (B) Iliococcygeus muscle (IC) originating from the obturator fascia (Ob-f). The vaginal wall (V) looses the H shape appearance and becomes more flattened. LA th, levator ani thickness; PC, pubococcygeus; R, rectum; SP, symphysis pubis; U, urethra.

In most of the controls (70.8%), the pubococcygeus muscle had regular smooth contours and muscle fibres running in parallel. In contrast, in the majority of women with prolapse (69%), the pubococcygeus muscle had mixed echogenicity (Table 1). Mixed echogenicity was not related to parity within controls or women with prolapse.

In the prolapse group, 14 women (35.9%) had evidence of muscle trauma, but the presence of trauma in parous women was not related to the number of children delivered (median parity 2.0 children in women with and without muscle trauma). Muscle trauma was not seen in controls.

The anterior vaginal sulci were visualised laterally to the proximal urethra attached to the arcus tendineous fascia pelvis. In controls, the anterior vaginal sulci were well supported, giving the vagina a characteristic ‘H shape’ (Table 1, Figure 3A). In the group with prolapse, a detachment of the anterior vaginal sulci was evident in 15 women, (P= 0.002,); this was unilateral in five and bilateral in ten women (Table 1, Figure 3B).

Figure 3.

(A) The anterior vaginal sulci (V) are visualised laterally to the proximal urethra (U) attached to the arcus tendineous fascia pelvis. They are well supported giving the vagina a characteristic ‘H shape’ appearance. (B) Paravaginal defect on the right. The left anterior vaginal sulcus (V-L) is well supported. The right anterior vaginal wall (V-R) has lost its support from the lateral pelvic sidewall. PC, pubococcygeus; R, rectum; SP, symphysis pubis.

The thickness of the pubococcygeus muscle was similar in controls and in those with prolapse (Table 1). However, the levator hiatal area was significantly larger in women with prolapse compared with that in those without prolapse (17.8 cm2 versus 13.5 cm2, P < 0.001) (Table 1).

The greater the prolapse staging the larger the levator hiatal area (P < 0.001, Figure 4), although this was not related to the thickness of the pubococcygeus muscle (P= non significant, Figure 5).

Figure 4.

Levator ani hiatal surface area at rest with respect to prolapse severity. Individual patients with median ± standard error.

Figure 5.

Levator ani muscle thickness with respect to prolapse severity. Individual patients with median ± standard error.

The correlation of the levator hiatal area and thickness with POP-Q assessment is presented in Table 3. There was a strong and significant correlation between all the POP-Q measurements (except total vaginal length) and the maximum descent of the leading organ with levator hiatal area but not with levator thickness.

Table 3.  Correlation of levator hiatal area and thickness with POP-Q assessment
 Hiatal areaThickness
ρ*Pρ*P
  • TVL, total vaginal length.

  • Aa, Ba, C, Ap, Bp, D, as defined by Bump et al.10

  • *

    Spearman correlation coefficient.

Aa0.70<0.001−0.240.059
Ba0.72<0.001−0.250.093
C0.53<0.001−0.090.472
Ap0.49<0.001−0.150.254
Bp0.51<0.001−0.050.709
TVL−0.210.0850.050.708
D0.46<0.001−0.060.674
Leading organ (maximum of Aa, Ba, C, Ap, Bp, D)0.82<0.001−0.180.165

Discussion

The position of the levator ani (within the pelvic cavity surrounded by the bony pelvis) and its complex shape make direct imaging extremely difficult. Imaging of the pelvic floor to quantify and define pelvic floor support may be a valuable technique to improve our approach to surgical repair of POP and to identify the reasons for surgical failure.

The pelvic floor consists of two muscular components, the levator ani and the coccygeus. The pubococcygeus portion of the levator ani muscle originates bilaterally from the pubic rami and extends posteriorly past the urethra and vagina to reach the anorectal junction where it joins with the contralateral fibres. This supporting muscular sling has an opening in the middle (levator ani hiatus) through which the urethra, vagina and rectum pass. Contraction of this muscle pulls the rectum, vagina and urethra towards the pubic bone and thus eliminating the levator ani hiatus through which prolapse of genital organs may occur.12 Loss of the basal tone results in widening of the hiatus and may predispose to urogenital prolapse.

A transvaginal approach was used, and this has allowed direct visualisation of the pelvic floor muscles. The resolution is theoretically better using this approach because the probe is closer to the pelvic floor structures. Intra- and inter-observer variability of this approach was shown to be very good for hiatal area and good for muscle thickness. This agrees with other ultrasound studies of levator morphology assessing hiatal area and levator thickness in women without prolapse.13,14 Although we have not collected data for variability assessment of other parameters such as muscle trauma echogenicity, levator muscle trauma assessment by ultrasound has been shown to be highly reproducible,13 and we concur with this view on the basis of excellent quality and clarity of the images obtained (Figure 3B). Regarding changes in echogenicity specifically, because of the closeness of the ultrasound probe to the pelvic muscles and the direct imaging aspects of the 2-D technique, we have been able to obtain excellent visualisation of the muscle texture (we were even able to see muscle fibres; Figures 1–3).

Although there has been criticism of the transvaginal approach with regard to possible distortion of the vaginal anatomy,15 the possibility of the distension of the levator hiatus and invasiveness, this is the only non-3D ultrasonographic method shown to date to allow excellent visualisation of the levator hiatus. Furthermore, the hiatal area and morphology of the muscle has not been actually shown to be significantly affected by the presence of the probe in the vagina per se (we used a very narrow probe) or by variable bladder volumes when scanned.

The 2-D technique we have used enabled us to measure the levator hiatal area even in women with a large degree of prolapse. With this technique, the plane of ultrasound beam is perpendicular to the axis of the probe and therefore in parallel to the plane of the levator hiatus. This results in acquiring axial images along the pelvic axis similar to those obtained by pelvic floor MRI.16,8

Women with prolapse have a significantly larger levator ani hiatal area compared with women of similar age and parity without prolapse. Furthermore, in women with prolapse, the greater the prolapse (as assessed by the maximum descent of the leading organ) the greater the hiatal area; this holds true for descent of any part of the pelvic organs. This is in agreement with previous studies.13,14,17–19 It has also been shown that in women with prolapse, the levator plate tips more vertically during straining. This is thought to be associated with an enlarged levator hiatus and increased perineal body descent.20 The increase in levator hiatal area found in our study may be related to such changes in levator angle and descent. Furthermore, we have shown that higher the degree of prolapse the greater the levator hiatal area. This relationship appears not linear but curvilinear supporting the multifactorial nature of prolapse (Figure 4). It is also apparent that there is a significant overlap in hiatal area for stages 0, I and II, whereas stages III and IV are associated with much greater hiatal area. This may have important implications in the success of various forms of treatment for prolapse and the probability of prolapse recurrence. For example, it may be that a woman with stage III or IV prolapse may in fact require a procedure that specifically addresses a large levator ani hiatal area in addition to fascial reconstruction. Furthermore, in addressing surgical failures and recurrences, it would be interesting to see how this relates to levator hiatal area and the degree of prolapse.

Levator ani muscle thickness was not significantly different between the two groups. This appears to be in contrast to previous studies which have shown that the thickness or volume of the pelvic floor muscles correlates with prolapse.8 This can be explained by the fact that different measurement methods were used and at different parts of the pelvic floor muscles. Our measurements at the level taken might not necessarily reflect the volume of the muscle or its functional status.

We attempted to subjectively assess the morphological appearance of the levator ani muscle. For this, we evaluated the muscle echogenicity and evidence of trauma. This might reflect damage from vaginal delivery or secondary damage from the gravitational effect of a large prolapse or other factors that affect muscle condition (e.g. age, lack of estrogens, neurological damage). Neither the appearance of muscle echogenicity nor evidence of trauma was related to parity, as the median parity was not different between groups. The appearance of mixed echogenicity was doubled in the prolapse group compared with that in the controls. Evidence of trauma was present exclusively in parous women who had prolapse; in other words, trauma was always associated with prolapse. In women without prolapse (i.e. controls), no evidence of trauma was detected even in the parous women. Therefore, the key factor in the development of prolapse is trauma and not parity per se. From our data, we cannot assess whether it is the first vaginal delivery associated with the degree of trauma as reported in other studies.21 Other factors may also be relevant to prolapse, such as neurological injury and estrogen deficiency. Changes in muscle structure are seen with age. The diameters of type I and II fibres decrease significantly with age and menopausal status. Splitting and fragmentation of muscle fibres are also noted in those with stress urinary incontinence, which is often coexistent with prolapse.22 Whether these degenerative changes are seen in women with prolapse and relate to changes in echogenicity is not yet defined. Other studies have shown an increase in collagen III and active metalloproteinase expressions in the vaginal tissue of women with prolapse. This has been suggested to indicate active tissue remodelling under the biomechanical stresses associated with prolapse.23A further study assessing histological changes related to these ultrasound appearances may be useful to answer this.

In women with prolapse, a higher proportion were noted to have disruption of the anterior vaginal wall sulci (paravaginal defect). This would suggest that disruption of the integrity of the anterior vaginal sulcus may be related to prolapse. This muscle disruption has been shown in previous MRI and ultrasound studies. These imaging studies comparing nulliparous versus primiparous women suggest that changes seen in levator ani morphology and disruption in integrity are likely to be secondary to vaginal-delivery-related trauma.24–26

Clinical detection of paravaginal defects and levator trauma is difficult and correlates poorly with imaging the vaginal sulcus.27–29 Visualisation of such muscle detachment with ultrasound could assist in objectively recognising defects that may be over or underestimated by clinical examination alone. Quantification may also be possible with this ultrasound technique. The significance of paravaginal defects as detected by this technique will need to be further assessed in larger studies.

We did not relate symptoms to prolapse and ultrasound findings. Previous studies have shown that symptoms have poor correlation with location and severity of prolapse.30 This study was performed to characterise the anatomical changes only. A larger study using validated symptom questionnaires would be required to relate functional changes to anatomic findings.

This study has shown that 2-D transvaginal ultrasound is a reliable and reproducible method for imaging the pelvic floor. We were able to show significant differences in both muscle morphology and structure in women with POP compared with controls.

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