SEARCH

SEARCH BY CITATION

Keywords:

  • manometry;
  • morphology;
  • ultrasound;
  • vaginal pressure measurements

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

Aims

To investigate if pelvic floor muscle (PFM) thickness and area of levator hiatus (LH) are associated with manometry measured PFM function in 109 women with pelvic organ prolapse (POP) stages I–III.

Methods

In this cross-sectional study pubovisceral muscle thickness and LH area were assessed with three-dimensional transperineal ultrasound at rest and analyzed in the axial plane. PFM function was assessed with manometry and included strength, endurance, and vaginal resting pressure. Relationships were investigated using univariate linear logistic regressions models, Pearson product-moment correlation coefficient and hierarchical multiple regression.

Results

The mean age was 49 (SD 12). There was a significant positive moderate association between muscle thickness and PFM strength (r = 0.49, P < 0.001) and endurance (r = .45, P < 0.001). A moderate negative association was found between LH area and vaginal resting pressure (r = −0.46, P < 0.001), strength (r = −0.41, P < 0.001) and endurance (r = −0.40, P < 0.001). Multivariate analyses included PFM strength, endurance, vaginal resting pressure, age, parity, BMI and socioeconomic status. Muscle thickness was best explained by PFM strength and LH area was best explained by vaginal resting pressure. However, PFM function explained only 20.0% and 26.4% of the variance in muscle thickness and LH area after controlling for age, parity, BMI, and socioeconomic status.

Conclusion

There are moderate associations between measurements using ultrasound and manometry in POP women. Thicker muscles and smaller LH were associated with higher strength and endurance. Smaller LH was additionally associated with higher vaginal resting pressure. Ultrasound and manometry measure different aspects of the PFM and cannot be used interchangeably. Neurourol. Urodynam. 33:115–120, 2014. © 2013 Wiley Periodicals, Inc.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

Dysfunction of the pelvic floor muscles (PFM) may lead to urinary and faecal incontinence, pelvic organ prolapse (POP), sexual problems and chronic pain.[1] More than 50% of parous women have pelvic floor prolapse quantification (POP-Q) stage I–IV.[2, 3] Previous research has demonstrated that women with POP have reduced PFM strength,[4-7] reduced PFM endurance,[5] reduced vaginal resting pressure,[4, 5] reduced muscle thickness of the pelvic floor[8, 9] and enlarged area of levator hiatus (LH).[10-12] Not only the stage of POP, but also the type of POP has been found to be related to the size levator hiatus.[13] In a case control study PFM strength (OR 7.5; 95% CI 1.5–36.4) and endurance (OR 11.5; 95% CI 2.0–66.9) were independently related to POP,[5] demonstrating that better PFM function gave lower odds for POP.

PFM function can be clinically measured as maximum strength, endurance and vaginal resting pressure using manometry. To date there is scant knowledge about the associations between PFM strength and endurance and PFM morphology such as thickness of levator ani and size of the LH area in women with POP. PFM training is known to increase the strength of the PFM in women with stress urinary incontinence[14, 15] and POP[16, 17] and has shown to increase muscle thickness and to reduce the resting area of LH.[18] The first aim of the present study was to investigate whether muscle thickness and size of LH (morphology) are associated with PFM strength, endurance and vaginal resting pressure (manometry assessment) in women with POP-Q stage I, II, and III. The second aim was to investigate if the manometry measurement were able to predict a significant amount of the variance in muscle thickness and levator hiatus dimensions, when controlling for the possible effect of high socioeconomic status, parity and age in POP women.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

Design

In this cross-sectional study, women with POP-Q stages I, II, and III,[19] regardless of symptoms, were enrolled by community gynaecologists working in the counties of Oslo and Akershus from 2006 to 2010. The study was approved by the Regional Medical Ethics Committee and the Norwegian social science data services. All subjects gave written informed consent to participate.

Participants were at least 1 year postpartum. Eligibility criteria were more than 1 year since last delivery. Exclusion criteria were stage 0 or 4 on POP-Q, breastfeeding, previous POP surgery, radiating back pain, pelvic cancer, neurological or psychiatric disorders. The present study was a part of a greater randomized controlled trial aiming to evaluate the effect of PFMT in women with POP.[18, 20]

Outcome Measures

Participants filled out a validated symptom-bother questionnaire[21] prior to a clinical physiotherapist examination. High socioeconomic status was assessed by questionnaire and defined as having an income of 350 000 NOK or more and a high educational level (college or university). Ability to perform a PFM contraction was assessed by visual observation and vaginal palpation.[22] PFM function (maximum strength, endurance, and vaginal resting pressure) was assessed by a physiotherapist (IHB) using a vaginal balloon catheter (balloon size 6.7 cm × 1.7 cm) connected to a high precision pressure transducer (Camtech AS, Sandvika, Oslo; Fig. 1). The manometry method has been found to be responsive and reliable.[23, 24] To ensure valid measurement, only contractions with simultaneous inward movement of the perineum were considered correct contraction.[24] The pressure transducer had conventional, current electronic sensor technology. The middle of the balloon was placed 3.5 cm proximal to the vaginal introitus.[24] Muscle strength was calculated as the mean of three maximal voluntary contractions (MVC). Vaginal resting pressure was measured as the difference between atmospheric pressure and the vaginal pressure at rest, without any voluntary PFM activity. PFM endurance was defined as a sustained maximal contraction[25] and was quantified during the first 10 sec as the area under the curve (cmH2Osec; Fig. 1).[5]

image

Figure 1. Manometry measurements included pelvic floor muscle strength measured as the mean of three maximum voluntary contractions (MVC), endurance (area under the curve for 10 sec) and vaginal resting pressure.

Download figure to PowerPoint

The POP-Q and three-dimensional (3D) transperineal ultrasound examination were performed at a university hospital by a gynecologist (MM) blinded to background data and manometry measurements. The participants emptied their bladder before examination and a bladder volume of <50 ml was confirmed on ultrasound. A GE Voluson 730 expert and E8 ultrasound system (GE Healthcare, Oslo, Norway) was used with a 3D/4D ultrasound transducer (4–8 MHz, RAB 4–8 l/obstetric) placed on the perineum. The field of view angle was set to its maximum (70° × 85°). 3D static volumes were recorded in the lithotomy position while resting. The ultrasound images were analyzed offline (4D View v 5.0 and 6.3; GE Healthcare) by one investigator (IHB) blinded to clinical and background data. The pubovisceral muscle was defined as the most medial part of the levator ani complex bordering the LH. Ultrasound images were previewed and excluded from analysis unless the complete inner border of the pubovisceral muscle was visible in the axial plane. All analyses were conducted in the plane of minimal hiatal dimensions. To find the correct axial plane both the sagittal and the axial plane were simultaneous observed while the axial plane were rotated to find the plane with minimal distance between the hyperechogenic posterior aspect of the symphysis pubis and the hyperechogenic back sling of the pubovisceral muscle.[5, 26]

LH area was defined as the area bordered by the pubovisceral muscle, symphysis pubis, and inferior pubic ramus in the axial plane (Fig. 2). Intraclass correlation coefficients (ICCs) for inter-[27] and intra-observer repeatability[28, 29] have been found to be were 0.92 and 0.56, respectively, for the 3D static volumes. The correlation between ultrasound and MRI for LH area measurement was 0.9.[30]

image

Figure 2. 3D transperineal ultrasound image of levator hiatus (LH) area and the four measurements sites of pubovisceral muscle thickness, with the mean being used in the analyses.

Download figure to PowerPoint

Pubovisceral muscle thickness was measured at rest in four different sites, with the mean used in the analyses (Fig. 2). ICCs for muscle thickness have been demonstrated to range from 0.13 to 0.70[27, 28]. Additionally, muscle thickness has been compared between ultrasound and magnetic resonance imaging (MRI), and a correlation coefficient of 0.8 for muscle thickness and 0.9 for LH area[30] were shown.

Statistical Analyses

Statistical analysis was performed using SPSS version 15. The relationships between muscle morphology and muscle strength, endurance and vaginal resting pressure were investigated using univariate linear logistic regressions models and Pearson product-moment correlation coefficient. Multiple regression is recommended when exploring predictive ability in a model when controlling for additional variables. This method was used to explore how well the variance in muscle thickness and LH area could be explained by manometry measurements (muscle strength, muscle endurance and resting pressure), after controlling for age, parity, body mass index (BMI) and socioeconomic status. The reason for choosing these control variables was that they have been found to be independently associated with POP.[5] Additionally, stage of POP was controlled for to check if the results changed due to this variable. To evaluate the effect of the different variables, we compared the standardized regression coefficients (β). Preliminary analyses were conducted to ensure no violation of the assumptions of normality, linearity, and homoscedasticity. A one way between-groups analysis of variance was conducted to explore the impact of the symptom “vaginal bulging” on muscle thickness. P-values <0.05 were considered significant. Power calculation was done for the RCT[18, 20] but no additional power calculation was done for this cross sectional study.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

From November 2005 to April 2008 145 women with POP were recruited. Thirty-six women were excluded due to exclusion criteria. The mean age of the remaining109 participants was 48.9 years (SD 11.8), median parity 2 (range 1–5) and mean BMI 25.9 kg/m2 (SD 4.5). Thirty-six of the participants (33%) were defined as having a high socioeconomic status. Nineteen women were classified to have POP stage I, 65 stage II and 24 stage III. Sixty-six women (61%) reported symptoms of SUI and 69 (63%) reported POP symptoms (vaginal bulging and/or pelvic pressure/heaviness). Ultrasound and manometry measurement are presented in Table I.

Table I. Ultrasound and Manometry Measurements of the 109 Participants
 MeanStandard deviationRange
  1. PFM, pelvic floor muscle.

Muscle thickness (mm)9.22.34.3–15.3
Levator hiatus area (cm2)23.25.312.3–38.6
PFM strength (cmH2O)30.319.24.2–93.6
PFM endurance (cmH2Osec)21115028–709
Vaginal resting pressure (cmH2O)28.610.015.9–75.2

Muscle Thickness

There was a positive moderate association between PFM thickness and PFM strength (r = 0.49, P < 0.001) and endurance (r = 0.45, P < 0.001), but not with vaginal resting pressure (r = 0.10, P = 0.143).

Due to the weak relationship between muscle thickness and resting pressure and the high correlation (multicollinearity) between PFM strength and endurance (r = 0.94, P < 0.001), only the strength measurement were entered into the hierarchical multiple regression model (Table II). Age, parity, BMI, and socioeconomic status were entered at Step1, explaining only 7.0% of the variance in muscle thickness. After entry PFM strength in Step 2, PFM strength explained an additional 20.0% of the variance in thickness after controlling for age, parity, BMI and socioeconomic status (R squared change = 0.20, F change (1,102) = 27.62, P < 0.001). The total variance explained by the model as a whole was 27.0%. Of the five variables in the model only PFM strength made an unique contribution to the prediction of muscle thickness, when the overlapping effects of all other variables was statistically removed. The standardized regression coefficient (β) was 0.48 (95% CI: 0.000–0.001, P < 0.001). Additionally controlling for stage of prolapse did not change the ability of our set of variables (manometry measures) to predict the variance in muscle thickness (R squared change = 0.20, F change (1,99) = 27.35, P < 0.001).

Table II. Hierarchical Multiple Regression
 RR squareAdjusted R squareStd. error of the estimateR square changeF changedf1df2Sig. F change
  1. a

    Predictors: (constant), high socioeconomic status, parity, BMI, age.

  2. b

    Predictors: (constant), high socioeconomic status, parity, BMI, age, muscle strength (manometry).

  3. c

    Predictors: (constant), high socioeconomic status, parity, BMI, age, muscle strength (manometry), resting pressure (manometry).

Muscle thickness, step 10.265a0.0700.0340.222820.0701.92941020.111
Muscle thickness, step 20.520b0.2700.2340.198430.20027.62011010.000
Levator hiatus, step 10.242a0.0590.0225.242640.0591.61741040.176
Levator hiatus, step 20.568c0.3220.2834.490780.26419.87021020.000

Fifty-four percent of the women did not report, or were not bothered by vaginal bulging. Twenty-one percent reported minor, 17% moderate, and 7% major bothering of vaginal bulging. Muscle thickness PFM muscle strength were not statistically significant different between women with different degrees of bothering; P = 0.210 and P = 0.184, respectively (Fig. 3).

image

Figure 3. Muscle thickness (3D ultrasound) and PFM strength (manometry) between women reporting different degrees of bothering of vaginal bulging. No statistical differences were found (P = 0.201 and P = 0.0184, respectively).

Download figure to PowerPoint

LH Area

There was a significant negative moderate association between LH area and PFM strength (r = −0.41, P < 0.001, Fig. 4), endurance (r = −0.40, P < 0.001) and resting pressure (r = −0.46, P < 0.001). For all three measurements of PFM function the values increased with a smaller LH.

image

Figure 4. A significant negative association between area of levator hiatus and pelvic floor muscle strength (maximal voluntary contraction, MVC) were found (r = 0.41, P < 0.001).

Download figure to PowerPoint

Using multiple regression age, parity, BMI, and socioeconomic status explained 5.9% of the variance in LH area (Table II). The total variance explained by the model as a whole, including PFM strength and resting pressure, was 32.2%. PFM strength and resting pressure explained an additional 26.4% of the variance in LH area when the effects of age, parity, BMI, and socioeconomic status were controlled for. Of the six variables in the model, vaginal resting pressure and PFM strength made unique contributions to the prediction of LH area, after controlling for all other variables in the model. Vaginal resting pressure contributed more (β −0.39, 95% CI: 0.03–0.01, P < 0.001) than PFM strength (β −0.25, 95% CI: 0.12–0.00, P = 0.010) in predicting the size of LH. Additionally controlling for stage of prolapse, the controlling variables at Step 1 (stage of POP, age, parity, BMI, and socioeconomic status) explained 10.2% of the variance in LH area. The total variance in LH area explained by the model as a whole, including stage of POP, was 33.6%.

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

The present study demonstrated that muscle thickness was positively associated with PFM strength and that LH size was negatively associated with higher levels of vaginal resting pressure, PFM strength and endurance in women with POP. Age, parity, BMI, and socioeconomic status could only explain 3–7% of the variance in the morphology of the pelvic floor, while the manometry measurements explained 20–26%. Besides PFM strength, endurance and vaginal resting pressure the variance may also be explained by genetic architecture, automatic function, training status and dysfunctions including muscles defects or injuries. A sensitivity analysis including stage of POP did not turn out to affect the muscle thickness by distention effect.

Assessments with transperineal ultrasound have demonstrated that women with POP have reduced muscle thickness of the pelvic floor[8, 9] and that continent women have higher increment in the urogenital diaphragm when compared with incontinent women.[31] As expected muscle thickness was associated with muscle strength. Association between muscle thickness and strength has previously been shown in women with SUI,[32] but not in women with POP. The present study confirmed this, and additionally found that muscle thickness was associated with PFM endurance, but not with vaginal resting pressure. Manometry measured strength and endurance are closely related, and they were found to have collinearity.

Our results support the finding of DeLancey et al.[4] demonstrating that vaginal resting pressure can be an important marker of “muscular closing” of the LH. A short pubovisceral muscle will naturally give a small LH area. Using manometry, we have shown that vaginal resting pressure may indirectly predict the size of the hiatus. However, the method alone is not sufficient to detect the accurate size of LH since it could explain less than 26% of the variance of LH area. Nevertheless, as ultrasound equipment is expensive and often not accessible, this measurement might be considered important women with POP. It has been shown that women with POP have enlarged area of LH.[10-12]

Strength training has shown to increase muscle thickness,[18, 32] reduce LH area[18] and elevate the bladder[18, 33] and bowel,[18] showing a potential to rebuild the morphology of the pelvic floor by improving PFM strength, endurance, and vaginal resting pressure. Narrowing of the LH and increasing muscle thickness will most likely give better support for the bladder, urethra, uterus, and bowel and may prevent pelvic floor disorders.[34] PFM training has shown to be effective in women with urinary incontinence and POP. PFM training in healthy young women may have the potential to be a primary prevention intervention for POP. However, to investigate this latter hypothesis a large RCT with a long follow-up period is needed.

The strengths of the present study are that PFM strength, endurance and vaginal resting pressure, muscle thickness and LH area were measured with methods found to have good reliability and validity.[23, 24, 27, 28, 30] A limitation of the study is the generalizability as we had a selected group of participants. However, this study was not designed to define normative data for the general female population, but to evaluate if there was any association between the manometry measurements and morphology in women with POP-Q stages I–III. The present study analyzed baseline data from a randomized controlled trial aiming to evaluate the effect of PFMT in women with POP.[18, 20] No specific power calculation was done for this study, and this is a limitation. The results however, demonstrated that the study was not underpowered. We could have included women with POP-Q stage 0 and IV to check if the associations remain the same for all stages of POP. Due to difficulties with image capturing in advanced prolapse, we chose not to include POP-Q stage IV. We did not include women with POP-Q stage 0. However, we included 19 women with POP-Q stage I and 40 women without any prolapse symptoms. It can be questioned if the association found in the present study can be generalized to the normal population. A significant portion of parous women, and especially those with POP, have partial to complete levator avulsions or injury.[35] In clinical practice, these women all present to the assessments of PFM function and most likely many of our participants may therefore also have such defects, reflecting the patient group seeking medical care for pelvic floor dysfunctions. If we had included only women without any pelvic floor disorder the results might have been stronger since a good relationship between two variables in normal subjects can be lost with pathology or abnormality. The prevalence for having at least one symptomatic pelvic floor disorder was found to be 23.7% among more than 1,900 women (≥20 years) in United States,[36] and 98% of the older female population (mean age 68 ± 6 years) have POP-Q stages I–IV.[7]

Manometry measurements of PFM function is considered an important assessment tool, and widely used assessment tool in clinical practice especially for physiotherapists and researchers treating women with pelvic floor disorders conservatively aiming to improve PFM strength and endurance. In this study, we have shown a moderate association between manometry and ultrasound measurements indicating the both modalities are useful but not interchangeable when monitoring PFM function in women with POP. It was, maybe, expected to find a better agreement between strength measurements and muscle thickness. It is of high clinical relevance that strength measurements do not explain more than 27% of PFM thickness in POP women. However, this is far more than what was explained by age, parity, BMI and socioeconomic status together (7%) and was definitively the best factor to explain these two morphological variables. From sports science there is evidence for a substantial agreement between strength and cross sectional area in athletes and healthy subjects.[37] Based on the results of the present study, one cannot assume a strong but a moderate association between muscle strength and muscle thickness in POP women.

This study highlights that transperineal 3D Ultrasound and manometry measure different aspects of the pelvic floor, and both manometry and ultrasound should be used in clinical practice. Further research may focus of finding if there is a cut off point for PFM strength, endurance and vaginal resting pressure needed to avoid pelvic floor disorders.

CONCLUSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

PFM muscle thickness was moderate positively associated with PFM strength and endurance in POP women. A significant negative moderate association between LH area and PFM strength, endurance and resting pressure were found. Thicker muscles and smaller LH were associated with higher strength and endurance, and smaller LH was associated with higher vaginal resting pressure. Only PFM strength made a unique contribution to the prediction of muscle thickness. Vaginal resting pressure contributed more than PFM strength in predicting the size of LH. Although moderate associations have been found, manometry and ultrasound measure different aspects of the pelvic floor. Both methods are important in understanding PFM muscle morphology and function, but they cannot be used interchangeably.

ACKNOWLEDGMENTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES

We thank Ingar Morten Holme, professor and biostatistician, Norwegian School of Sport Sciences, Department of Sports Medicine, Oslo, Norway for statistical assistance. Additionally, we gratefully acknowledge support for this research through the EXTRA funds from the Norwegian Foundation for Health and Rehabilitation and the Norwegian Women's Public Health Association.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONCLUSION
  8. ACKNOWLEDGMENTS
  9. REFERENCES
  • 1
    Bump RC, Norton PA. Epidemiology and natural history of pelvic floor dysfunction. Obstet Gynecol Clin North Am 1998;25:72346.
  • 2
    Swift SE. The distribution of pelvic organ support in a population of female subjects seen for routine gynecologic health care. Am J Obstet Gynecol 2000;183:27785.
  • 3
    Hagen S, Stark D, Maher C, et al. Conservative management of pelvic organ prolapse in women. Cochrane Database Syst Rev 2006;2:CD003882.
  • 4
    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;109:295302.
  • 5
    Braekken IH, Majida M, Ellstrom EM, et al. Pelvic floor function is independently associated with pelvic organ prolapse. BJOG 2009;116:170614.
  • 6
    Samuelsson EC, Victor FT, Tibblin G, et al. Signs of genital prolapse in a Swedish population of women 20 to 59 years of age and possible related factors. Am J Obstet Gynecol 1999;180:299305.
  • 7
    Nygaard I, Bradley C, Brandt D. Pelvic organ prolapse in older women: Prevalence and risk factors. Obstet Gynecol 2004;104:48997.
  • 8
    Hoyte L, Jakab M, Warfield SK, et al. Levator ani thickness variations in symptomatic and asymptomatic women using magnetic resonance-based 3-dimensional color mapping. Am J Obstet Gynecol 2004;191:85661.
  • 9
    Chen L, Hsu Y, shton-Miller JA, et al. Measurement of the pubic portion of the levator ani muscle in women with unilateral defects in 3-D models from MR images. Int J Gynaecol Obstet 2006;92:23441.
  • 10
    Hoyte L, Schierlitz L, Zou K, et al. Two- and 3-dimensional MRI comparison of levator ani structure, volume, and integrity in women with stress incontinence and prolapse. Am J Obstet Gynecol 2001;185:119.
  • 11
    DeLancey JO, Hurd WW. Size of the urogenital hiatus in the levator ani muscles in normal women and women with pelvic organ prolapse. Obstet Gynecol 1998;91:3648.
  • 12
    Athanasiou S, Chaliha C, Toozs-Hobson P, et al. Direct imaging of the pelvic floor muscles using two-dimensional ultrasound: A comparison of women with urogenital prolapse versus controls. BJOG 2007;114:8828.
  • 13
    Majida M, Braekken I, Bo K, et al. Anterior but not posterior compartment prolapse is associated with levator hiatus area: A three- and four-dimensional transperineal ultrasound study. BJOG 2011;118:32937.
  • 14
    Dumoulin C, Hay-Smith J. Pelvic floor muscle training versus no treatment, or inactive control treatments, for urinary incontinence in women. Cochrane Database Syst Rev 2010; CD005654.
  • 15
    Bo K, Talseth T, Holme I. Single blind, randomised controlled trial of pelvic floor exercises, electrical stimulation, vaginal cones, and no treatment in management of genuine stress incontinence in women. BMJ 1999;318:48793.
  • 16
    Braekken IH, Majida M, Engh ME, et al. Can pelvic floor muscle training reverse pelvic organ prolapse and reduce prolapse symptoms? An assessor-blinded, randomized, controlled trial. Am J Obstet Gynecol 2010.
  • 17
    Hagen S, Stark D, Glazener C, et al. A randomized controlled trial of pelvic floor muscle training for stages I and II pelvic organ prolapse. Int Urogynecol J Pelvic Floor Dysfunct 2009;20:4551.
  • 18
    Braekken IH, Majida M, Engh ME, et al. Morphological changes after pelvic floor muscle training measured by 3-dimensional ultrasonography: A randomized controlled trial. Obstet Gynecol 2010;115:31724.
  • 19
    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;175:107.
  • 20
    Braekken IH, Majida M, Engh ME, et al. Can pelvic floor muscle training reverse pelvic organ prolapse and reduce prolapse symptoms? An assessor-blinded, randomized, controlled trial. Am J Obstet Gynecol 2010;203:1707.
  • 21
    Mouritsen L, Larsen JP. Symptoms, bother and POPQ in women referred with pelvic organ prolapse. Int Urogynecol J Pelvic Floor Dysfunct 2003;14:1227.
  • 22
    Bo K, Sherburn M. Evaluation of female pelvic-floor muscle function and strength. Phys Ther 2005;85:26982.
  • 23
    Bo K, Kvarstein B, Hagen R, et al. Pelvic floor muscle exercise for the treatment of female stress urinary incontinence:I. Reliability of vaginal pressure measurements of pelvic floor muscle strength. Neurourol Urodyn 1990;9:4717.
  • 24
    Bo K, Kvarstein B, Hagen R, et al. Pelvic floor muscle exercise for the treatment of female stress urinary incontinence:II. Validity of vaginal pressure measurements of pelvic floor muscle strength and the necessity of supplementary methods for control of correct contraction. Neurourol Urodyn 1990;9:47987.
  • 25
    Bo K, Aschehoug A. Pelvic floor and exercise science—Strength training. In: Bo K, Berghmans B, Morkved S, Kampen MV, editors. Evidence-based physical therapy for the pelvic floor. Elsevier; 2007. 11932.
  • 26
    Dietz HP, Shek C, Clarke B. Biometry of the pubovisceral muscle and levator hiatus by three-dimensional pelvic floor ultrasound. Ultrasound Obstet Gynecol 2005;25:5805.
  • 27
    Majida M, Braekken IH, Umek W, et al. Interobserver repeatability of three- and four-dimensional transperineal ultrasound assessment of pelvic floor muscle anatomy and function. Ultrasound Obstet Gynecol 2009;33:56773.
  • 28
    Braekken IH, Majida M, Ellstrom-Engh M, et al. Test-retest and intra-observer repeatability of two-, three- and four-dimensional perineal ultrasound of pelvic floor muscle anatomy and function. Int Urogynecol J Pelvic Floor Dysfunct 2008;19:22735.
  • 29
    Braekken IH, Majida M, Engh ME, et al. Test-retest reliability of pelvic floor muscle contraction measured by 4D ultrasound. Neurourol Urodyn 2009;28:6873.
  • 30
    Majida M, Braekken IH, Bo K, et al. Validation of three-dimensional perineal ultrasound and magnetic resonance imaging measurements of the pubovisceral muscle at rest. Ultrasound Obstet Gynecol 2010;35:71522.
  • 31
    Morkved S, Salvesen KA, Bo K, et al. Pelvic floor muscle strength and thickness in continent and incontinent nulliparous pregnant women. Int Urogynecol J Pelvic Floor Dysfunct 2004;15:3849.
  • 32
    Bernstein IT. The pelvic floor muscles: Muscle thickness in healthy and urinary-incontinent women measured by perineal ultrasonography with reference to the effect of pelvic floor training. Estrogen receptor studies; biometry. Neurourol Urodyn 1997;16:23775.
  • 33
    Balmforth JR, Mantle J, Bidmead J, et al. A prospective observational trial of pelvic floor muscle training for female stress urinary incontinence. BJU Int 2006;98:8117.
  • 34
    DeLancey JO. The hidden epidemic of pelvic floor dysfunction: Achievable goals for improved prevention and treatment. Am J Obstet Gynecol 2005;192:148895.
  • 35
    Dietz HP, Simpson JM. Levator trauma is associated with pelvic organ prolapse. BJOG 2008;115:97984.
  • 36
    Nygaard I, Barber MD, Burgio KL, et al. Prevalence of symptomatic pelvic floor disorders in US women. JAMA 2008;300:13116.
  • 37
    Folland JP, Williams AG. The adaptations to strength training: Morphological and neurological contributions to increased strength. Sports Med 2007;37:14568.